Müller Cell–Localized G-Protein–Coupled Receptor 81 (Hydroxycarboxylic Acid Receptor 1) Regulates Inner Retinal Vasculature via Norrin/Wnt Pathways

Ischemic retinopathies are characterized by a progressive microvascular degeneration followed by a postischemic aberrant neovascularization. To reinstate vascular supply and metabolic equilibrium to the ischemic tissue during ischemic retinopathies, a dysregulated production of growth factors and me...

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Published in	The American journal of pathology Vol. 189; no. 9; pp. 1878 - 1896
Main Authors	Madaan, Ankush, Chaudhari, Prabhas, Nadeau-Vallée, Mathieu, Hamel, David, Zhu, Tang, Mitchell, Grant, Samuels, Mark, Pundir, Sheetal, Dabouz, Rabah, Howe Cheng, Colin Wayne, Mohammad Nezhady, Mohammad A., Joyal, Jean-Sébastien, Rivera, José Carlos, Chemtob, Sylvain
Format	Journal Article
Language	English
Published	United States Elsevier Inc 01.09.2019
Subjects	Animals Ependymoglial Cells - metabolism Ependymoglial Cells - pathology Eye Proteins - genetics Eye Proteins - metabolism Ischemia - etiology Ischemia - metabolism Ischemia - pathology Lactic Acid - metabolism Mice Mice, Knockout Nerve Tissue Proteins - genetics Nerve Tissue Proteins - metabolism Receptors, G-Protein-Coupled - physiology Retinal Diseases - etiology Retinal Diseases - metabolism Retinal Diseases - pathology Retinal Neovascularization - etiology Retinal Neovascularization - metabolism Retinal Neovascularization - pathology Retinal Vessels - metabolism Retinal Vessels - pathology Wnt Proteins - genetics Wnt Proteins - metabolism
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ISSN	0002-9440 1525-2191 1525-2191
DOI	10.1016/j.ajpath.2019.05.016

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Abstract	Ischemic retinopathies are characterized by a progressive microvascular degeneration followed by a postischemic aberrant neovascularization. To reinstate vascular supply and metabolic equilibrium to the ischemic tissue during ischemic retinopathies, a dysregulated production of growth factors and metabolic intermediates occurs, promoting retinal angiogenesis. Glycolysis-derived lactate, highly produced during ischemic conditions, has been associated with tumor angiogenesis and wound healing. Lactate exerts its biological effects via G-protein–coupled receptor 81 (GPR81) in several tissues; however, its physiological functions and mechanisms of action in the retina remain poorly understood. Herein, we show that GPR81, localized predominantly in Müller cells, governs deep vascular complex formation during development and in ischemic retinopathy. Lactate-stimulated GPR81 Müller cells produce numerous angiogenic factors, including Wnt ligands and particularly Norrin, which contributes significantly in triggering inner retinal blood vessel formation. Conversely, GPR81-null mice retina shows reduced inner vascular network formation associated with low levels of Norrin (and Wnt ligands). Lactate accumulation during ischemic retinopathy selectively activates GPR81–extracellular signal-regulated kinase 1/2–Norrin signaling to accelerate inner retinal vascularization in wild-type animals, but not in the retina of GPR81-null mice. Altogether, we reveal that lactate via GPR81-Norrin participates in inner vascular network development and in restoration of the vasculature in response to injury. These findings suggest a new potential therapeutic target to alleviate ischemic diseases.
AbstractList	Ischemic retinopathies are characterized by a progressive microvascular degeneration followed by a postischemic aberrant neovascularization. To reinstate vascular supply and metabolic equilibrium to the ischemic tissue during ischemic retinopathies, a dysregulated production of growth factors and metabolic intermediates occurs, promoting retinal angiogenesis. Glycolysis-derived lactate, highly produced during ischemic conditions, has been associated with tumor angiogenesis and wound healing. Lactate exerts its biological effects via G-protein–coupled receptor 81 (GPR81) in several tissues; however, its physiological functions and mechanisms of action in the retina remain poorly understood. Herein, we show that GPR81, localized predominantly in Müller cells, governs deep vascular complex formation during development and in ischemic retinopathy. Lactate-stimulated GPR81 Müller cells produce numerous angiogenic factors, including Wnt ligands and particularly Norrin, which contributes significantly in triggering inner retinal blood vessel formation. Conversely, GPR81-null mice retina shows reduced inner vascular network formation associated with low levels of Norrin (and Wnt ligands). Lactate accumulation during ischemic retinopathy selectively activates GPR81–extracellular signal-regulated kinase 1/2–Norrin signaling to accelerate inner retinal vascularization in wild-type animals, but not in the retina of GPR81-null mice. Altogether, we reveal that lactate via GPR81-Norrin participates in inner vascular network development and in restoration of the vasculature in response to injury. These findings suggest a new potential therapeutic target to alleviate ischemic diseases. Ischemic retinopathies are characterized by a progressive microvascular degeneration followed by a postischemic aberrant neovascularization. To reinstate vascular supply and metabolic equilibrium to the ischemic tissue during ischemic retinopathies, a dysregulated production of growth factors and metabolic intermediates occurs, promoting retinal angiogenesis. Glycolysis-derived lactate, highly produced during ischemic conditions, has been associated with tumor angiogenesis and wound healing. Lactate exerts its biological effects via G-protein-coupled receptor 81 (GPR81) in several tissues; however, its physiological functions and mechanisms of action in the retina remain poorly understood. Herein, we show that GPR81, localized predominantly in Müller cells, governs deep vascular complex formation during development and in ischemic retinopathy. Lactate-stimulated GPR81 Müller cells produce numerous angiogenic factors, including Wnt ligands and particularly Norrin, which contributes significantly in triggering inner retinal blood vessel formation. Conversely, GPR81-null mice retina shows reduced inner vascular network formation associated with low levels of Norrin (and Wnt ligands). Lactate accumulation during ischemic retinopathy selectively activates GPR81-extracellular signal-regulated kinase 1/2-Norrin signaling to accelerate inner retinal vascularization in wild-type animals, but not in the retina of GPR81-null mice. Altogether, we reveal that lactate via GPR81-Norrin participates in inner vascular network development and in restoration of the vasculature in response to injury. These findings suggest a new potential therapeutic target to alleviate ischemic diseases.Ischemic retinopathies are characterized by a progressive microvascular degeneration followed by a postischemic aberrant neovascularization. To reinstate vascular supply and metabolic equilibrium to the ischemic tissue during ischemic retinopathies, a dysregulated production of growth factors and metabolic intermediates occurs, promoting retinal angiogenesis. Glycolysis-derived lactate, highly produced during ischemic conditions, has been associated with tumor angiogenesis and wound healing. Lactate exerts its biological effects via G-protein-coupled receptor 81 (GPR81) in several tissues; however, its physiological functions and mechanisms of action in the retina remain poorly understood. Herein, we show that GPR81, localized predominantly in Müller cells, governs deep vascular complex formation during development and in ischemic retinopathy. Lactate-stimulated GPR81 Müller cells produce numerous angiogenic factors, including Wnt ligands and particularly Norrin, which contributes significantly in triggering inner retinal blood vessel formation. Conversely, GPR81-null mice retina shows reduced inner vascular network formation associated with low levels of Norrin (and Wnt ligands). Lactate accumulation during ischemic retinopathy selectively activates GPR81-extracellular signal-regulated kinase 1/2-Norrin signaling to accelerate inner retinal vascularization in wild-type animals, but not in the retina of GPR81-null mice. Altogether, we reveal that lactate via GPR81-Norrin participates in inner vascular network development and in restoration of the vasculature in response to injury. These findings suggest a new potential therapeutic target to alleviate ischemic diseases.
Author	Chaudhari, Prabhas Dabouz, Rabah Zhu, Tang Joyal, Jean-Sébastien Mitchell, Grant Samuels, Mark Pundir, Sheetal Mohammad Nezhady, Mohammad A. Madaan, Ankush Chemtob, Sylvain Nadeau-Vallée, Mathieu Hamel, David Rivera, José Carlos Howe Cheng, Colin Wayne
Author_xml	– sequence: 1 givenname: Ankush surname: Madaan fullname: Madaan, Ankush organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada – sequence: 2 givenname: Prabhas surname: Chaudhari fullname: Chaudhari, Prabhas organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada – sequence: 3 givenname: Mathieu surname: Nadeau-Vallée fullname: Nadeau-Vallée, Mathieu organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada – sequence: 4 givenname: David surname: Hamel fullname: Hamel, David organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada – sequence: 5 givenname: Tang surname: Zhu fullname: Zhu, Tang organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada – sequence: 6 givenname: Grant surname: Mitchell fullname: Mitchell, Grant organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada – sequence: 7 givenname: Mark surname: Samuels fullname: Samuels, Mark organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada – sequence: 8 givenname: Sheetal surname: Pundir fullname: Pundir, Sheetal organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada – sequence: 9 givenname: Rabah surname: Dabouz fullname: Dabouz, Rabah organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada – sequence: 10 givenname: Colin Wayne surname: Howe Cheng fullname: Howe Cheng, Colin Wayne organization: Department of Pharmacology and Therapeutics, McGill University, Montréal, Quebec, Canada – sequence: 11 givenname: Mohammad A. surname: Mohammad Nezhady fullname: Mohammad Nezhady, Mohammad A. organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada – sequence: 12 givenname: Jean-Sébastien surname: Joyal fullname: Joyal, Jean-Sébastien organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada – sequence: 13 givenname: José Carlos surname: Rivera fullname: Rivera, José Carlos email: jc.rivera@umontreal.ca organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada – sequence: 14 givenname: Sylvain surname: Chemtob fullname: Chemtob, Sylvain email: sylvain.chemtob@umontreal.ca organization: Departments of Pediatrics, Ophthalmology and Pharmacology, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montréal, Quebec, Canada
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Cites_doi	10.1016/S0306-4522(98)00699-X 10.1002/jez.1402340202 10.1152/jappl.1987.62.5.1975 10.1523/JNEUROSCI.4756-04.2005 10.1007/s10456-009-9155-3 10.1007/s10633-009-9197-2 10.1016/j.cell.2009.07.047 10.1182/blood-2012-04-396846 10.1042/CS20060049 10.1001/archopht.1996.01100140419009 10.1371/journal.pone.0093041 10.18632/oncotarget.3565 10.1073/pnas.1217091110 10.1167/iovs.11-7185 10.1016/j.bbrc.2008.10.088 10.1038/jcbfm.2009.97 10.1161/CIRCULATIONAHA.111.040337 10.1111/apa.13586 10.1016/S0092-8674(04)00216-8 10.1523/JNEUROSCI.2841-12.2012 10.1002/sim.7263 10.1167/iovs.10-5176 10.1053/j.gastro.2014.03.014 10.1158/0008-5472.CAN-14-0319 10.1128/JVI.72.11.8463-8471.1998 10.1091/mbc.e06-04-0320 10.1111/apha.13042 10.1167/iovs.08-2297 10.1167/iovs.05-0174 10.1242/dmm.007724 10.5812/ijem.3505 10.1016/j.cell.2009.07.048 10.2337/db13-1673 10.1016/S1350-9462(00)00027-6 10.1007/s10633-005-2621-3 10.1167/iovs.07-0916 10.1167/iovs.10-6197 10.1523/JNEUROSCI.15-07-05179.1995 10.1167/iovs.08-1731 10.1056/NEJM199409223311201 10.1016/0300-9629(83)90463-2 10.1007/s11064-015-1792-x 10.1158/0008-5472.CAN-11-1457 10.1016/S1350-9462(98)00010-X 10.1038/nm.1873 10.1152/jn.1970.33.3.323 10.1002/cne.903200209 10.1016/0002-9394(66)91322-5 10.1016/j.ajog.2016.09.072 10.1186/s12974-017-0955-x 10.1007/s10456-012-9282-0 10.1111/cns.12362 10.1038/sj.onc.1204184 10.1158/0008-5472.CAN-10-2828 10.1242/dev.01117 10.1093/hmg/ddn047 10.1001/archopht.1997.01100160723009 10.1074/jbc.M806409200 10.1016/j.molmed.2010.07.003 10.1167/iovs.06-1197 10.1016/S0006-8993(01)02082-0 10.1371/journal.pone.0027385 10.2174/138161212799504902 10.1016/j.ajpath.2014.10.020 10.18632/oncotarget.12286 10.1167/iovs.10-6888 10.1111/j.1651-2227.2012.02692.x 10.1016/j.cell.2012.10.042 10.2337/diabetes.55.04.06.db05-1325 10.1523/JNEUROSCI.3210-09.2010 10.1016/S0169-328X(00)00224-2 10.1523/JNEUROSCI.15-07-04738.1995 10.1124/pr.112.007179 10.1093/cercor/bht136 10.1146/annurev.me.08.020157.002301 10.1523/JNEUROSCI.0730-10.2010 10.1073/pnas.92.3.905 10.1371/journal.pone.0033418 10.2147/EB.S94447
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References	Shin, Sorenson, Sheibani (bib62) 2014; 9 Ashton (bib7) 1957; 8 Lee, Shin, Park, Park, Park, Heo, Seo, Noh, Ryu, Suh (bib47) 2016; 7 Mendrinos, Petropoulos, Mangioris, Tsilimbaris, Papadopoulou, Geka, Pournaras (bib68) 2011; 52 Cai, Ren, Jin, Cheng, Kash, Chen, Wright, Taggart, Waters (bib39) 2008; 377 Walenta, Wetterling, Lehrke, Schwickert, Sundfor, Rofstad, Mueller-Klieser (bib77) 2000; 60 Sonveaux, Copetti, De Saedeleer, Vegran, Verrax, Kennedy, Moon, Dhup, Danhier, Frerart, Gallez, Ribeiro, Michiels, Dewhirst, Feron (bib76) 2012; 7 Luo, Xiao, Zhu, Mao, Liu, Chen, Huang, Tang, Rizzolo (bib66) 2011; 52 Pierce, Avery, Foley, Aiello, Smith (bib3) 1995; 92 Lauritzen, Morland, Puchades, Holm-Hansen, Hagelin, Lauritzen, Attramadal, Storm-Mathisen, Gjedde, Bergersen (bib41) 2014; 24 Poitry-Yamate, Poitry, Tsacopoulos (bib28) 1995; 15 Sapieha, Sirinyan, Hamel, Zaniolo, Joyal, Cho, Honore, Kermorvant-Duchemin, Varma, Tremblay, Leduc, Rihakova, Hardy, Klein, Mu, Mamer, Lachapelle, Di Polo, Beausejour, Andelfinger, Mitchell, Sennlaub, Chemtob (bib20) 2008; 14 Miller, Dowling (bib92) 1970; 33 Stahl, Connor, Sapieha, Chen, Dennison, Krah, Seaward, Willett, Aderman, Guerin, Hua, Lofqvist, Hellstrom, Smith (bib49) 2010; 51 Penn, Henry, Wall, Tolman (bib1) 1995; 36 Smith, Wesolowski, McLellan, Kostyk, D'Amato, Sullivan, D'Amore (bib48) 1994; 35 Dorfman, Dembinska, Chemtob, Lachapelle (bib13) 2008; 49 Albert, Ellington (bib30) 1985; 234 Berkowitz, Penn (bib9) 1998; 39 Cringle, Yu (bib79) 2010; 120 Li, Wang, Wang, Chen, Liu (bib73) 2014; 9 Reis, Mateus, Melo, Figueira, Cunha-Vaz, Castelo-Branco (bib63) 2014; 63 Ohlmann, Scholz, Goldwich, Chauhan, Hudl, Ohlmann, Zrenner, Berger, Cvekl, Seeliger, Tamm (bib23) 2005; 25 Krishnamoorthy, Agarwal, Prasanna, Vopat, Lambert, Sheedlo, Pang, Shade, Wordinger, Yorio, Clark, Agarwal (bib57) 2001; 86 Pierce, Foley, Smith (bib4) 1996; 114 Chen, Stahl, Krah, Seaward, Dennison, Sapieha, Hua, Hatton, Juan, Aderman, Willett, Guerin, Mammoto, Campbell, Smith (bib85) 2011; 124 Davenport, Alexander, Sharman, Pawson, Benson, Monaghan, Liew, Mpamhanga, Bonner, Neubig, Pin, Spedding, Harmar (bib40) 2013; 65 Dembinska, Rojas, Chemtob, Lachapelle (bib18) 2002; 43 Zudaire, Gambardella, Kurcz, Vermeren (bib52) 2011; 6 Hack, Taylor, Klein, Eiben, Schatschneider, Mercuri-Minich (bib15) 1994; 331 Junge, Yang, Burton, Paes, Shu, French, Costa, Rice, Ye (bib24) 2009; 139 Tsacopoulos, Poitry-Yamate, MacLeish, Poitry (bib27) 1998; 17 Schurr, Payne, Miller, Tseng, Rigor (bib37) 2001; 895 Hughson, Weisiger, Swanson (bib55) 1987; 62 Kolko, Vosborg, Henriksen, Hasan-Olive, Diget, Vohra, Gurubaran, Gjedde, Mariga, Skytt, Utheim, Storm-Mathisen, Bergersen (bib60) 2016; 41 Wang, Rattner, Zhou, Williams, Smallwood, Nathans (bib67) 2012; 151 Yu, Cringle, Yu, Su (bib81) 2007; 48 Ye, Wang, Cahill, Yu, Badea, Smallwood, Peachey, Nathans (bib25) 2009; 139 Vegran, Boidot, Michiels, Sonveaux, Feron (bib69) 2011; 71 Slevin, Kumar, Gaffney, Kumar, Krupinski (bib17) 2006; 111 Rivera, Noueihed, Madaan, Lahaie, Pan, Belik, Chemtob (bib50) 2017; 14 Dorfman, Polosa, Joly, Chemtob, Lachapelle (bib14) 2009; 50 Sapieha (bib89) 2012; 120 Fulton, Hansen, Moskowitz, Barnaby (bib11) 2005; 111 Shen, Fruttiger, Zhu, Chung, Barnett, Kirk, Lee, Coorey, Killingsworth, Sherman, Gillies (bib22) 2012; 32 Ohlmann, Seitz, Braunger, Seitz, Bosl, Tamm (bib72) 2010; 30 Madaan, Nadeau-Vallee, Rivera, Obari, Hou, Sierra, Girard, Olson, Chemtob (bib46) 2017; 216 Dwivedi, Mallawaarachchi, Alvarado (bib59) 2017; 36 Yu, Cringle (bib80) 2001; 20 Dull, Zufferey, Kelly, Mandel, Nguyen, Trono, Naldini (bib54) 1998; 72 Gade, Ellington (bib31) 1983; 76 He, Semenov, Tamai, Zeng (bib90) 2004; 131 Pierce, Luttrell, Lefkowitz (bib5) 2001; 20 Poitry-Yamate, Tsacopoulos (bib84) 1992; 320 Pournaras, Miller, Gragoudas, Husain, Munoz, Tolentino, Kuroki, Adamis (bib2) 1997; 115 Joyal, Omri, Sitaras, Rivera, Sapieha, Chemtob (bib87) 2012; 101 Liu, Wu, Zhu, Kuei, Yu, Shelton, Sutton, Li, Yun, Mirzadegan, Mazur, Kamme, Lovenberg (bib42) 2009; 284 Ashton (bib6) 1966; 62 Xin, Rodrigues, Umapathi, Kashiwabuchi, Ma, Babapoor-Farrokhran, Wang, Hu, Bhutto, Welsbie, Duh, Handa, Eberhart, Lutty, Semenza, Montaner, Sodhi (bib83) 2013; 110 Senior (bib16) 2001; 358 Stone, Itin, Alon, Pe'er, Gnessin, Chan-Ling, Keshet (bib21) 1995; 15 Sitaras, Rivera, Noueihed, Bien-Aime, Zaniolo, Omri, Hamel, Zhu, Hardy, Sapieha, Joyal, Chemtob (bib51) 2015; 185 Schafer, Luhmann, Feil, Berger (bib65) 2009; 50 Ohno, Oyama, Kaneko, Egawa, Yokoyama, Sugiura, Ohira, Yoshioka, Goto (bib74) 2018; 223 Dobson, Quinn, Abramov, Hardy, Tung, Siatkowski, Phelps (bib12) 1996; 37 Stahl, Connor, Sapieha, Willett, Krah, Dennison, Chen, Guerin, Smith (bib53) 2009; 12 Hirschi, D'Amore (bib88) 1997; 79 Draoui, Feron (bib33) 2011; 4 Kim, D'Amore, Connor (bib71) 2016; 8 Roland, Arumugam, Deng, Liu, Philip, Gomez, Burns, Ramachandran, Wang, Cruz-Monserrate, Logsdon (bib44) 2014; 74 Dhup, Dadhich, Porporato, Sonveaux (bib32) 2012; 18 Wahlin, Campochiaro, Zack, Adler (bib56) 2000; 41 Masckauchan, Agalliu, Vorontchikhina, Ahn, Parmalee, Li, Khoo, Tycko, Brown, Kitajewski (bib64) 2006; 17 Dorfman, Cuenca, Pinilla, Chemtob, Lachapelle (bib10) 2011; 52 Xu, Wang, Dabdoub, Smallwood, Williams, Woods, Kelley, Jiang, Tasman, Zhang, Nathans (bib61) 2004; 116 Hoque, Farooq, Ghani, Gorelick, Mehal (bib45) 2014; 146 Staubert, Broom, Nordstrom (bib78) 2015; 6 Berthet, Lei, Thevenet, Gruetter, Magistretti, Hirt (bib38) 2009; 29 Porporato, Payen, De Saedeleer, Preat, Thissen, Feron, Sonveaux (bib34) 2012; 15 Ye, Wang, Nathans (bib70) 2010; 16 Ghasemi, Zahediasl (bib58) 2012; 10 Xia, Liu, Cheung, Wang, Cheng, Du, Chang, Beutler, Gong (bib91) 2008; 17 Winkler, Arnold, Brassell, Puro (bib29) 2000; 41 Luhmann, Lin, Acar, Lammel, Feil, Grimm, Seeliger, Hammes, Berger (bib8) 2005; 46 Hirschhaeuser, Sattler, Mueller-Klieser (bib82) 2011; 71 Shen, Jiang, Yuan, Deng, Zheng, Zhao, Li, Wu, Gao, Hu, Zhang, Chen (bib43) 2015; 21 Dembinska, Rojas, Varma, Chemtob, Lachapelle (bib19) 2001; 42 Seitz, Hackl, Seibuchner, Tamm, Ohlmann (bib26) 2010; 30 Mason, Petersen, Lebon, Rothman, Shulman (bib36) 2006; 55 Gerhart, Leino, Drewes (bib86) 1999; 92 Brazitikos, Pournaras, Munoz, Tsacopoulos (bib35) 1993; 34 Rivera, Madaan, Zhou, Chemtob (bib75) 2016; 105 Xin (10.1016/j.ajpath.2019.05.016_bib83) 2013; 110 Dembinska (10.1016/j.ajpath.2019.05.016_bib18) 2002; 43 Madaan (10.1016/j.ajpath.2019.05.016_bib46) 2017; 216 Pierce (10.1016/j.ajpath.2019.05.016_bib4) 1996; 114 Wang (10.1016/j.ajpath.2019.05.016_bib67) 2012; 151 Mason (10.1016/j.ajpath.2019.05.016_bib36) 2006; 55 Lee (10.1016/j.ajpath.2019.05.016_bib47) 2016; 7 Luhmann (10.1016/j.ajpath.2019.05.016_bib8) 2005; 46 Luo (10.1016/j.ajpath.2019.05.016_bib66) 2011; 52 Stahl (10.1016/j.ajpath.2019.05.016_bib53) 2009; 12 Draoui (10.1016/j.ajpath.2019.05.016_bib33) 2011; 4 Ohlmann (10.1016/j.ajpath.2019.05.016_bib72) 2010; 30 Berkowitz (10.1016/j.ajpath.2019.05.016_bib9) 1998; 39 Junge (10.1016/j.ajpath.2019.05.016_bib24) 2009; 139 Dwivedi (10.1016/j.ajpath.2019.05.016_bib59) 2017; 36 Yu (10.1016/j.ajpath.2019.05.016_bib80) 2001; 20 Sapieha (10.1016/j.ajpath.2019.05.016_bib89) 2012; 120 Pournaras (10.1016/j.ajpath.2019.05.016_bib2) 1997; 115 Dhup (10.1016/j.ajpath.2019.05.016_bib32) 2012; 18 Penn (10.1016/j.ajpath.2019.05.016_bib1) 1995; 36 Berthet (10.1016/j.ajpath.2019.05.016_bib38) 2009; 29 Cringle (10.1016/j.ajpath.2019.05.016_bib79) 2010; 120 Poitry-Yamate (10.1016/j.ajpath.2019.05.016_bib84) 1992; 320 Poitry-Yamate (10.1016/j.ajpath.2019.05.016_bib28) 1995; 15 Staubert (10.1016/j.ajpath.2019.05.016_bib78) 2015; 6 Dembinska (10.1016/j.ajpath.2019.05.016_bib19) 2001; 42 Hack (10.1016/j.ajpath.2019.05.016_bib15) 1994; 331 Liu (10.1016/j.ajpath.2019.05.016_bib42) 2009; 284 Seitz (10.1016/j.ajpath.2019.05.016_bib26) 2010; 30 Wahlin (10.1016/j.ajpath.2019.05.016_bib56) 2000; 41 Schafer (10.1016/j.ajpath.2019.05.016_bib65) 2009; 50 Dull (10.1016/j.ajpath.2019.05.016_bib54) 1998; 72 Senior (10.1016/j.ajpath.2019.05.016_bib16) 2001; 358 Shen (10.1016/j.ajpath.2019.05.016_bib22) 2012; 32 Dorfman (10.1016/j.ajpath.2019.05.016_bib13) 2008; 49 Hughson (10.1016/j.ajpath.2019.05.016_bib55) 1987; 62 Hirschhaeuser (10.1016/j.ajpath.2019.05.016_bib82) 2011; 71 He (10.1016/j.ajpath.2019.05.016_bib90) 2004; 131 Xu (10.1016/j.ajpath.2019.05.016_bib61) 2004; 116 Ashton (10.1016/j.ajpath.2019.05.016_bib7) 1957; 8 Miller (10.1016/j.ajpath.2019.05.016_bib92) 1970; 33 Stahl (10.1016/j.ajpath.2019.05.016_bib49) 2010; 51 Cai (10.1016/j.ajpath.2019.05.016_bib39) 2008; 377 Rivera (10.1016/j.ajpath.2019.05.016_bib75) 2016; 105 Ohno (10.1016/j.ajpath.2019.05.016_bib74) 2018; 223 Dobson (10.1016/j.ajpath.2019.05.016_bib12) 1996; 37 Smith (10.1016/j.ajpath.2019.05.016_bib48) 1994; 35 Xia (10.1016/j.ajpath.2019.05.016_bib91) 2008; 17 Masckauchan (10.1016/j.ajpath.2019.05.016_bib64) 2006; 17 Hirschi (10.1016/j.ajpath.2019.05.016_bib88) 1997; 79 Ohlmann (10.1016/j.ajpath.2019.05.016_bib23) 2005; 25 Dorfman (10.1016/j.ajpath.2019.05.016_bib10) 2011; 52 Sitaras (10.1016/j.ajpath.2019.05.016_bib51) 2015; 185 Porporato (10.1016/j.ajpath.2019.05.016_bib34) 2012; 15 Ye (10.1016/j.ajpath.2019.05.016_bib25) 2009; 139 Tsacopoulos (10.1016/j.ajpath.2019.05.016_bib27) 1998; 17 Chen (10.1016/j.ajpath.2019.05.016_bib85) 2011; 124 Hoque (10.1016/j.ajpath.2019.05.016_bib45) 2014; 146 Brazitikos (10.1016/j.ajpath.2019.05.016_bib35) 1993; 34 Sonveaux (10.1016/j.ajpath.2019.05.016_bib76) 2012; 7 Kolko (10.1016/j.ajpath.2019.05.016_bib60) 2016; 41 Gade (10.1016/j.ajpath.2019.05.016_bib31) 1983; 76 Fulton (10.1016/j.ajpath.2019.05.016_bib11) 2005; 111 Zudaire (10.1016/j.ajpath.2019.05.016_bib52) 2011; 6 Ghasemi (10.1016/j.ajpath.2019.05.016_bib58) 2012; 10 Yu (10.1016/j.ajpath.2019.05.016_bib81) 2007; 48 Winkler (10.1016/j.ajpath.2019.05.016_bib29) 2000; 41 Rivera (10.1016/j.ajpath.2019.05.016_bib50) 2017; 14 Gerhart (10.1016/j.ajpath.2019.05.016_bib86) 1999; 92 Shin (10.1016/j.ajpath.2019.05.016_bib62) 2014; 9 Slevin (10.1016/j.ajpath.2019.05.016_bib17) 2006; 111 Kim (10.1016/j.ajpath.2019.05.016_bib71) 2016; 8 Pierce (10.1016/j.ajpath.2019.05.016_bib3) 1995; 92 Joyal (10.1016/j.ajpath.2019.05.016_bib87) 2012; 101 Shen (10.1016/j.ajpath.2019.05.016_bib43) 2015; 21 Sapieha (10.1016/j.ajpath.2019.05.016_bib20) 2008; 14 Krishnamoorthy (10.1016/j.ajpath.2019.05.016_bib57) 2001; 86 Ashton (10.1016/j.ajpath.2019.05.016_bib6) 1966; 62 Mendrinos (10.1016/j.ajpath.2019.05.016_bib68) 2011; 52 Vegran (10.1016/j.ajpath.2019.05.016_bib69) 2011; 71 Li (10.1016/j.ajpath.2019.05.016_bib73) 2014; 9 Walenta (10.1016/j.ajpath.2019.05.016_bib77) 2000; 60 Dorfman (10.1016/j.ajpath.2019.05.016_bib14) 2009; 50 Lauritzen (10.1016/j.ajpath.2019.05.016_bib41) 2014; 24 Roland (10.1016/j.ajpath.2019.05.016_bib44) 2014; 74 Schurr (10.1016/j.ajpath.2019.05.016_bib37) 2001; 895 Albert (10.1016/j.ajpath.2019.05.016_bib30) 1985; 234 Stone (10.1016/j.ajpath.2019.05.016_bib21) 1995; 15 Davenport (10.1016/j.ajpath.2019.05.016_bib40) 2013; 65 Reis (10.1016/j.ajpath.2019.05.016_bib63) 2014; 63 Pierce (10.1016/j.ajpath.2019.05.016_bib5) 2001; 20 Ye (10.1016/j.ajpath.2019.05.016_bib70) 2010; 16
References_xml	– volume: 101 start-page: 819 year: 2012 end-page: 826 ident: bib87 article-title: Neovascularization in retinopathy of prematurity: opposing actions of neuronal factors GPR91 and semaphorins 3A publication-title: Acta Paediatr – volume: 14 start-page: 1067 year: 2008 end-page: 1076 ident: bib20 article-title: The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis publication-title: Nat Med – volume: 4 start-page: 727 year: 2011 end-page: 732 ident: bib33 article-title: Lactate shuttles at a glance: from physiological paradigms to anti-cancer treatments publication-title: Dis Model Mech – volume: 10 start-page: 486 year: 2012 end-page: 489 ident: bib58 article-title: Normality tests for statistical analysis: a guide for non-statisticians publication-title: Int J Endocrinol Metab – volume: 20 start-page: 1532 year: 2001 end-page: 1539 ident: bib5 article-title: New mechanisms in heptahelical receptor signaling to mitogen activated protein kinase cascades publication-title: Oncogene – volume: 120 start-page: 99 year: 2010 end-page: 109 ident: bib79 article-title: Oxygen supply and consumption in the retina: implications for studies of retinopathy of prematurity publication-title: Doc Ophthalmol – volume: 72 start-page: 8463 year: 1998 end-page: 8471 ident: bib54 article-title: A third-generation lentivirus vector with a conditional packaging system publication-title: J Virol – volume: 151 start-page: 1332 year: 2012 end-page: 1344 ident: bib67 article-title: Norrin/Frizzled4 signaling in retinal vascular development and blood brain barrier plasticity publication-title: Cell – volume: 12 start-page: 297 year: 2009 end-page: 301 ident: bib53 article-title: Computer-aided quantification of retinal neovascularization publication-title: Angiogenesis – volume: 35 start-page: 101 year: 1994 end-page: 111 ident: bib48 article-title: Oxygen-induced retinopathy in the mouse publication-title: Invest Ophthalmol Vis Sci – volume: 79 start-page: 419 year: 1997 end-page: 428 ident: bib88 article-title: Control of angiogenesis by the pericyte: molecular mechanisms and significance publication-title: EXS – volume: 51 start-page: 2813 year: 2010 end-page: 2826 ident: bib49 article-title: The mouse retina as an angiogenesis model publication-title: Invest Ophthalmol Vis Sci – volume: 223 start-page: e13042 year: 2018 ident: bib74 article-title: Lactate increases myotube diameter via activation of MEK/ERK pathway in C2C12 cells publication-title: Acta Physiol (Oxf) – volume: 25 start-page: 1701 year: 2005 end-page: 1710 ident: bib23 article-title: Ectopic norrin induces growth of ocular capillaries and restores normal retinal angiogenesis in Norrie disease mutant mice publication-title: J Neurosci – volume: 71 start-page: 2550 year: 2011 end-page: 2560 ident: bib69 article-title: Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-kappaB/IL-8 pathway that drives tumor angiogenesis publication-title: Cancer Res – volume: 115 start-page: 1553 year: 1997 end-page: 1558 ident: bib2 article-title: Systemic hyperoxia decreases vascular endothelial growth factor gene expression in ischemic primate retina publication-title: Arch Ophthalmol – volume: 114 start-page: 1219 year: 1996 end-page: 1228 ident: bib4 article-title: Regulation of vascular endothelial growth factor by oxygen in a model of retinopathy of prematurity publication-title: Arch Ophthalmol – volume: 7 start-page: e33418 year: 2012 ident: bib76 article-title: Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis publication-title: PLoS One – volume: 110 start-page: E3425 year: 2013 end-page: E3434 ident: bib83 article-title: Hypoxic retinal Muller cells promote vascular permeability by HIF-1-dependent up-regulation of angiopoietin-like 4 publication-title: Proc Natl Acad Sci U S A – volume: 30 start-page: 183 year: 2010 end-page: 193 ident: bib72 article-title: Norrin promotes vascular regrowth after oxygen-induced retinal vessel loss and suppresses retinopathy in mice publication-title: J Neurosci – volume: 36 start-page: 2063 year: 1995 end-page: 2070 ident: bib1 article-title: The range of PaO2 variation determines the severity of oxygen-induced retinopathy in newborn rats publication-title: Invest Ophthalmol Vis Sci – volume: 41 start-page: 927 year: 2000 end-page: 936 ident: bib56 article-title: Neurotrophic factors cause activation of intracellular signaling pathways in Muller cells and other cells of the inner retina, but not photoreceptors publication-title: Invest Ophthalmol Vis Sci – volume: 63 start-page: 3926 year: 2014 end-page: 3937 ident: bib63 article-title: Neuroretinal dysfunction with intact blood-retinal barrier and absent vasculopathy in type 1 diabetes publication-title: Diabetes – volume: 55 start-page: 929 year: 2006 end-page: 934 ident: bib36 article-title: Increased brain monocarboxylic acid transport and utilization in type 1 diabetes publication-title: Diabetes – volume: 185 start-page: 581 year: 2015 end-page: 595 ident: bib51 article-title: Retinal neurons curb inflammation and enhance revascularization in ischemic retinopathies via proteinase-activated receptor-2 publication-title: Am J Pathol – volume: 52 start-page: 1693 year: 2011 end-page: 1708 ident: bib10 article-title: Immunohistochemical evidence of synaptic retraction, cytoarchitectural remodeling, and cell death in the inner retina of the rat model of oxygen-induced retinopathy (OIR) publication-title: Invest Ophthalmol Vis Sci – volume: 17 start-page: 429 year: 1998 end-page: 442 ident: bib27 article-title: Trafficking of molecules and metabolic signals in the retina publication-title: Prog Retin Eye Res – volume: 124 start-page: 1871 year: 2011 end-page: 1881 ident: bib85 article-title: Wnt signaling mediates pathological vascular growth in proliferative retinopathy publication-title: Circulation – volume: 377 start-page: 987 year: 2008 end-page: 991 ident: bib39 article-title: Role of GPR81 in lactate-mediated reduction of adipose lipolysis publication-title: Biochem Biophys Res Commun – volume: 146 start-page: 1763 year: 2014 end-page: 1774 ident: bib45 article-title: Lactate reduces liver and pancreatic injury in Toll-like receptor- and inflammasome-mediated inflammation via GPR81-mediated suppression of innate immunity publication-title: Gastroenterology – volume: 7 start-page: 70898 year: 2016 end-page: 70911 ident: bib47 article-title: G-protein-coupled receptor 81 promotes a malignant phenotype in breast cancer through angiogenic factor secretion publication-title: Oncotarget – volume: 92 start-page: 367 year: 1999 end-page: 375 ident: bib86 article-title: Distribution of monocarboxylate transporters MCT1 and MCT2 in rat retina publication-title: Neuroscience – volume: 139 start-page: 299 year: 2009 end-page: 311 ident: bib24 article-title: TSPAN12 regulates retinal vascular development by promoting Norrin- but not Wnt-induced FZD4/beta-catenin signaling publication-title: Cell – volume: 6 start-page: e27385 year: 2011 ident: bib52 article-title: A computational tool for quantitative analysis of vascular networks publication-title: PLoS One – volume: 16 start-page: 417 year: 2010 end-page: 425 ident: bib70 article-title: The Norrin/Frizzled4 signaling pathway in retinal vascular development and disease publication-title: Trends Mol Med – volume: 62 start-page: 412 year: 1966 end-page: 435 ident: bib6 article-title: Oxygen and the growth and development of retinal vessels: in vivo and in vitro studies: the XX Francis I. Proctor Lecture publication-title: Am J Ophthalmol – volume: 895 start-page: 268 year: 2001 end-page: 272 ident: bib37 article-title: Blockade of lactate transport exacerbates delayed neuronal damage in a rat model of cerebral ischemia publication-title: Brain Res – volume: 43 start-page: 2481 year: 2002 end-page: 2490 ident: bib18 article-title: Evidence for a brief period of enhanced oxygen susceptibility in the rat model of oxygen-induced retinopathy publication-title: Invest Ophthalmol Vis Sci – volume: 111 start-page: 171 year: 2006 end-page: 183 ident: bib17 article-title: Can angiogenesis be exploited to improve stroke outcome? Mechanisms and therapeutic potential publication-title: Clin Sci (Lond) – volume: 49 start-page: 458 year: 2008 end-page: 466 ident: bib13 article-title: Early manifestations of postnatal hyperoxia on the retinal structure and function of the neonatal rat publication-title: Invest Ophthalmol Vis Sci – volume: 18 start-page: 1319 year: 2012 end-page: 1330 ident: bib32 article-title: Multiple biological activities of lactic acid in cancer: influences on tumor growth, angiogenesis and metastasis publication-title: Curr Pharm Des – volume: 216 start-page: 60.e1 year: 2017 end-page: 60.e17 ident: bib46 article-title: Lactate produced during labor modulates uterine inflammation via GPR81 (HCA1) publication-title: Am J Obstet Gynecol – volume: 46 start-page: 3372 year: 2005 end-page: 3382 ident: bib8 article-title: Role of the Norrie disease pseudoglioma gene in sprouting angiogenesis during development of the retinal vasculature publication-title: Invest Ophthalmol Vis Sci – volume: 62 start-page: 1975 year: 1987 end-page: 1981 ident: bib55 article-title: Blood lactate concentration increases as a continuous function in progressive exercise publication-title: J Appl Physiol (1985) – volume: 52 start-page: 7556 year: 2011 end-page: 7564 ident: bib66 article-title: Differential expression of claudins in retinas during normal development and the angiogenesis of oxygen-induced retinopathy publication-title: Invest Ophthalmol Vis Sci – volume: 9 start-page: e93041 year: 2014 ident: bib73 article-title: Distinct pathways of ERK1/2 activation by hydroxy-carboxylic acid receptor-1 publication-title: PLoS One – volume: 17 start-page: 1605 year: 2008 end-page: 1612 ident: bib91 article-title: A model for familial exudative vitreoretinopathy caused by LPR5 mutations publication-title: Hum Mol Genet – volume: 14 start-page: 181 year: 2017 ident: bib50 article-title: Tetrahydrobiopterin (BH4) deficiency is associated with augmented inflammation and microvascular degeneration in the retina publication-title: J Neuroinflammation – volume: 71 start-page: 6921 year: 2011 end-page: 6925 ident: bib82 article-title: Lactate: a metabolic key player in cancer publication-title: Cancer Res – volume: 34 start-page: 1744 year: 1993 end-page: 1752 ident: bib35 article-title: Microinjection of L-lactate in the preretinal vitreous induces segmental vasodilation in the inner retina of miniature pigs publication-title: Invest Ophthalmol Vis Sci – volume: 331 start-page: 753 year: 1994 end-page: 759 ident: bib15 article-title: School-age outcomes in children with birth weights under 750 g publication-title: N Engl J Med – volume: 8 start-page: 441 year: 1957 end-page: 454 ident: bib7 article-title: Experimental retrolental fibroplasia publication-title: Annu Rev Med – volume: 60 start-page: 916 year: 2000 end-page: 921 ident: bib77 article-title: High lactate levels predict likelihood of metastases, tumor recurrence, and restricted patient survival in human cervical cancers publication-title: Cancer Res – volume: 21 start-page: 271 year: 2015 end-page: 279 ident: bib43 article-title: Inhibition of G protein-coupled receptor 81 (GPR81) protects against ischemic brain injury publication-title: CNS Neurosci Ther – volume: 76 start-page: 615 year: 1983 end-page: 620 ident: bib31 article-title: The anaerobic molluscan heart: adaptation to environmental anoxia: comparison with energy metabolism in vertebrate hearts publication-title: Comp Biochem Physiol A Comp Physiol – volume: 17 start-page: 5163 year: 2006 end-page: 5172 ident: bib64 article-title: Wnt5a signaling induces proliferation and survival of endothelial cells in vitro and expression of MMP-1 and Tie-2 publication-title: Mol Biol Cell – volume: 50 start-page: 2436 year: 2009 end-page: 2450 ident: bib14 article-title: Functional and structural changes resulting from strain differences in the rat model of oxygen-induced retinopathy publication-title: Invest Ophthalmol Vis Sci – volume: 139 start-page: 285 year: 2009 end-page: 298 ident: bib25 article-title: Norrin, frizzled-4, and Lrp5 signaling in endothelial cells controls a genetic program for retinal vascularization publication-title: Cell – volume: 358 start-page: 817 year: 2001 ident: bib16 article-title: Angiogenesis and functional recovery demonstrated after minor stroke publication-title: Lancet – volume: 41 start-page: 1229 year: 2016 end-page: 1236 ident: bib60 article-title: Lactate transport and receptor actions in retina: potential roles in retinal function and disease publication-title: Neurochem Res – volume: 42 start-page: 1111 year: 2001 end-page: 1118 ident: bib19 article-title: Graded contribution of retinal maturation to the development of oxygen-induced retinopathy in rats publication-title: Invest Ophthalmol Vis Sci – volume: 65 start-page: 967 year: 2013 end-page: 986 ident: bib40 article-title: International Union of Basic and Clinical Pharmacology: LXXXVIII: G protein-coupled receptor list: recommendations for new pairings with cognate ligands publication-title: Pharmacol Rev – volume: 20 start-page: 175 year: 2001 end-page: 208 ident: bib80 article-title: Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease publication-title: Prog Retin Eye Res – volume: 15 start-page: 4738 year: 1995 end-page: 4747 ident: bib21 article-title: Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia publication-title: J Neurosci – volume: 41 start-page: 3183 year: 2000 end-page: 3190 ident: bib29 article-title: Energy metabolism in human retinal Muller cells publication-title: Invest Ophthalmol Vis Sci – volume: 116 start-page: 883 year: 2004 end-page: 895 ident: bib61 article-title: Vascular development in the retina and inner ear: control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair publication-title: Cell – volume: 86 start-page: 1 year: 2001 end-page: 12 ident: bib57 article-title: Characterization of a transformed rat retinal ganglion cell line publication-title: Brain Res Mol Brain Res – volume: 234 start-page: 175 year: 1985 end-page: 183 ident: bib30 article-title: Patterns of energy metabolism in the stone crab, Menippe mercenaria, during severe hypoxia and subsequent recovery publication-title: J Exp Zool – volume: 39 start-page: 840 year: 1998 end-page: 845 ident: bib9 article-title: Abnormal panretinal response pattern to carbogen inhalation in experimental retinopathy of prematurity publication-title: Invest Ophthalmol Vis Sci – volume: 32 start-page: 15715 year: 2012 end-page: 15727 ident: bib22 article-title: Conditional Muller cell ablation causes independent neuronal and vascular pathologies in a novel transgenic model publication-title: J Neurosci – volume: 15 start-page: 5179 year: 1995 end-page: 5191 ident: bib28 article-title: Lactate released by Muller glial cells is metabolized by photoreceptors from mammalian retina publication-title: J Neurosci – volume: 74 start-page: 5301 year: 2014 end-page: 5310 ident: bib44 article-title: Cell surface lactate receptor GPR81 is crucial for cancer cell survival publication-title: Cancer Res – volume: 120 start-page: 2182 year: 2012 end-page: 2194 ident: bib89 article-title: Eyeing central neurons in vascular growth and reparative angiogenesis publication-title: Blood – volume: 131 start-page: 1663 year: 2004 end-page: 1677 ident: bib90 article-title: LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: arrows point the way publication-title: Development – volume: 92 start-page: 905 year: 1995 end-page: 909 ident: bib3 article-title: Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization publication-title: Proc Natl Acad Sci U S A – volume: 284 start-page: 2811 year: 2009 end-page: 2822 ident: bib42 article-title: Lactate inhibits lipolysis in fat cells through activation of an orphan G-protein-coupled receptor, GPR81 publication-title: J Biol Chem – volume: 52 start-page: 3215 year: 2011 end-page: 3220 ident: bib68 article-title: Vasomotor effect of intravitreal juxta-arteriolar injection of L-lactate on the retinal arterioles after acute branch retinal vein occlusion in minipigs publication-title: Invest Ophthalmol Vis Sci – volume: 6 start-page: 19706 year: 2015 end-page: 19720 ident: bib78 article-title: Hydroxycarboxylic acid receptors are essential for breast cancer cells to control their lipid/fatty acid metabolism publication-title: Oncotarget – volume: 36 start-page: 2187 year: 2017 end-page: 2205 ident: bib59 article-title: Analysis of small sample size studies using nonparametric bootstrap test with pooled resampling method publication-title: Stat Med – volume: 15 start-page: 581 year: 2012 end-page: 592 ident: bib34 article-title: Lactate stimulates angiogenesis and accelerates the healing of superficial and ischemic wounds in mice publication-title: Angiogenesis – volume: 33 start-page: 323 year: 1970 end-page: 341 ident: bib92 article-title: Intracellular responses of the Muller (glial) cells of mudpuppy retina: their relation to b-wave of the electroretinogram publication-title: J Neurophysiol – volume: 9 start-page: 362 year: 2014 end-page: 373 ident: bib62 article-title: Diabetes and retinal vascular dysfunction publication-title: J Ophthalmic Vis Res – volume: 105 start-page: 1421 year: 2016 end-page: 1433 ident: bib75 article-title: Review of the mechanisms and therapeutic avenues for retinal and choroidal vascular dysfunctions in retinopathy of prematurity publication-title: Acta Paediatr – volume: 320 start-page: 257 year: 1992 end-page: 266 ident: bib84 article-title: Glucose metabolism in freshly isolated Muller glial cells from a mammalian retina publication-title: J Comp Neurol – volume: 48 start-page: 2290 year: 2007 end-page: 2296 ident: bib81 article-title: Intraretinal oxygen distribution and consumption during retinal artery occlusion and graded hyperoxic ventilation in the rat publication-title: Invest Ophthalmol Vis Sci – volume: 111 start-page: 7 year: 2005 end-page: 13 ident: bib11 article-title: Multifocal ERG in subjects with a history of retinopathy of prematurity publication-title: Doc Ophthalmol – volume: 37 start-page: 2467 year: 1996 end-page: 2474 ident: bib12 article-title: Color vision measured with pseudoisochromatic plates at five-and-a-half years in eyes of children from the CRYO-ROP study publication-title: Invest Ophthalmol Vis Sci – volume: 29 start-page: 1780 year: 2009 end-page: 1789 ident: bib38 article-title: Neuroprotective role of lactate after cerebral ischemia publication-title: J Cereb Blood Flow Metab – volume: 24 start-page: 2784 year: 2014 end-page: 2795 ident: bib41 article-title: Lactate receptor sites link neurotransmission, neurovascular coupling, and brain energy metabolism publication-title: Cereb Cortex – volume: 50 start-page: 906 year: 2009 end-page: 916 ident: bib65 article-title: Differential gene expression in Ndph-knockout mice in retinal development publication-title: Invest Ophthalmol Vis Sci – volume: 30 start-page: 5998 year: 2010 end-page: 6010 ident: bib26 article-title: Norrin mediates neuroprotective effects on retinal ganglion cells via activation of the Wnt/beta-catenin signaling pathway and the induction of neuroprotective growth factors in Muller cells publication-title: J Neurosci – volume: 8 start-page: 67 year: 2016 end-page: 79 ident: bib71 article-title: Revisiting the mouse model of oxygen-induced retinopathy publication-title: Eye Brain – volume: 92 start-page: 367 year: 1999 ident: 10.1016/j.ajpath.2019.05.016_bib86 article-title: Distribution of monocarboxylate transporters MCT1 and MCT2 in rat retina publication-title: Neuroscience doi: 10.1016/S0306-4522(98)00699-X – volume: 234 start-page: 175 year: 1985 ident: 10.1016/j.ajpath.2019.05.016_bib30 article-title: Patterns of energy metabolism in the stone crab, Menippe mercenaria, during severe hypoxia and subsequent recovery publication-title: J Exp Zool doi: 10.1002/jez.1402340202 – volume: 62 start-page: 1975 year: 1987 ident: 10.1016/j.ajpath.2019.05.016_bib55 article-title: Blood lactate concentration increases as a continuous function in progressive exercise publication-title: J Appl Physiol (1985) doi: 10.1152/jappl.1987.62.5.1975 – volume: 9 start-page: 362 year: 2014 ident: 10.1016/j.ajpath.2019.05.016_bib62 article-title: Diabetes and retinal vascular dysfunction publication-title: J Ophthalmic Vis Res – volume: 25 start-page: 1701 year: 2005 ident: 10.1016/j.ajpath.2019.05.016_bib23 article-title: Ectopic norrin induces growth of ocular capillaries and restores normal retinal angiogenesis in Norrie disease mutant mice publication-title: J Neurosci doi: 10.1523/JNEUROSCI.4756-04.2005 – volume: 79 start-page: 419 year: 1997 ident: 10.1016/j.ajpath.2019.05.016_bib88 article-title: Control of angiogenesis by the pericyte: molecular mechanisms and significance publication-title: EXS – volume: 12 start-page: 297 year: 2009 ident: 10.1016/j.ajpath.2019.05.016_bib53 article-title: Computer-aided quantification of retinal neovascularization publication-title: Angiogenesis doi: 10.1007/s10456-009-9155-3 – volume: 120 start-page: 99 year: 2010 ident: 10.1016/j.ajpath.2019.05.016_bib79 article-title: Oxygen supply and consumption in the retina: implications for studies of retinopathy of prematurity publication-title: Doc Ophthalmol doi: 10.1007/s10633-009-9197-2 – volume: 139 start-page: 285 year: 2009 ident: 10.1016/j.ajpath.2019.05.016_bib25 article-title: Norrin, frizzled-4, and Lrp5 signaling in endothelial cells controls a genetic program for retinal vascularization publication-title: Cell doi: 10.1016/j.cell.2009.07.047 – volume: 120 start-page: 2182 year: 2012 ident: 10.1016/j.ajpath.2019.05.016_bib89 article-title: Eyeing central neurons in vascular growth and reparative angiogenesis publication-title: Blood doi: 10.1182/blood-2012-04-396846 – volume: 111 start-page: 171 year: 2006 ident: 10.1016/j.ajpath.2019.05.016_bib17 article-title: Can angiogenesis be exploited to improve stroke outcome? Mechanisms and therapeutic potential publication-title: Clin Sci (Lond) doi: 10.1042/CS20060049 – volume: 34 start-page: 1744 year: 1993 ident: 10.1016/j.ajpath.2019.05.016_bib35 article-title: Microinjection of L-lactate in the preretinal vitreous induces segmental vasodilation in the inner retina of miniature pigs publication-title: Invest Ophthalmol Vis Sci – volume: 114 start-page: 1219 year: 1996 ident: 10.1016/j.ajpath.2019.05.016_bib4 article-title: Regulation of vascular endothelial growth factor by oxygen in a model of retinopathy of prematurity publication-title: Arch Ophthalmol doi: 10.1001/archopht.1996.01100140419009 – volume: 9 start-page: e93041 year: 2014 ident: 10.1016/j.ajpath.2019.05.016_bib73 article-title: Distinct pathways of ERK1/2 activation by hydroxy-carboxylic acid receptor-1 publication-title: PLoS One doi: 10.1371/journal.pone.0093041 – volume: 6 start-page: 19706 year: 2015 ident: 10.1016/j.ajpath.2019.05.016_bib78 article-title: Hydroxycarboxylic acid receptors are essential for breast cancer cells to control their lipid/fatty acid metabolism publication-title: Oncotarget doi: 10.18632/oncotarget.3565 – volume: 110 start-page: E3425 year: 2013 ident: 10.1016/j.ajpath.2019.05.016_bib83 article-title: Hypoxic retinal Muller cells promote vascular permeability by HIF-1-dependent up-regulation of angiopoietin-like 4 publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.1217091110 – volume: 52 start-page: 7556 year: 2011 ident: 10.1016/j.ajpath.2019.05.016_bib66 article-title: Differential expression of claudins in retinas during normal development and the angiogenesis of oxygen-induced retinopathy publication-title: Invest Ophthalmol Vis Sci doi: 10.1167/iovs.11-7185 – volume: 377 start-page: 987 year: 2008 ident: 10.1016/j.ajpath.2019.05.016_bib39 article-title: Role of GPR81 in lactate-mediated reduction of adipose lipolysis publication-title: Biochem Biophys Res Commun doi: 10.1016/j.bbrc.2008.10.088 – volume: 29 start-page: 1780 year: 2009 ident: 10.1016/j.ajpath.2019.05.016_bib38 article-title: Neuroprotective role of lactate after cerebral ischemia publication-title: J Cereb Blood Flow Metab doi: 10.1038/jcbfm.2009.97 – volume: 124 start-page: 1871 year: 2011 ident: 10.1016/j.ajpath.2019.05.016_bib85 article-title: Wnt signaling mediates pathological vascular growth in proliferative retinopathy publication-title: Circulation doi: 10.1161/CIRCULATIONAHA.111.040337 – volume: 105 start-page: 1421 year: 2016 ident: 10.1016/j.ajpath.2019.05.016_bib75 article-title: Review of the mechanisms and therapeutic avenues for retinal and choroidal vascular dysfunctions in retinopathy of prematurity publication-title: Acta Paediatr doi: 10.1111/apa.13586 – volume: 116 start-page: 883 year: 2004 ident: 10.1016/j.ajpath.2019.05.016_bib61 article-title: Vascular development in the retina and inner ear: control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair publication-title: Cell doi: 10.1016/S0092-8674(04)00216-8 – volume: 32 start-page: 15715 year: 2012 ident: 10.1016/j.ajpath.2019.05.016_bib22 article-title: Conditional Muller cell ablation causes independent neuronal and vascular pathologies in a novel transgenic model publication-title: J Neurosci doi: 10.1523/JNEUROSCI.2841-12.2012 – volume: 41 start-page: 3183 year: 2000 ident: 10.1016/j.ajpath.2019.05.016_bib29 article-title: Energy metabolism in human retinal Muller cells publication-title: Invest Ophthalmol Vis Sci – volume: 36 start-page: 2187 year: 2017 ident: 10.1016/j.ajpath.2019.05.016_bib59 article-title: Analysis of small sample size studies using nonparametric bootstrap test with pooled resampling method publication-title: Stat Med doi: 10.1002/sim.7263 – volume: 51 start-page: 2813 year: 2010 ident: 10.1016/j.ajpath.2019.05.016_bib49 article-title: The mouse retina as an angiogenesis model publication-title: Invest Ophthalmol Vis Sci doi: 10.1167/iovs.10-5176 – volume: 146 start-page: 1763 year: 2014 ident: 10.1016/j.ajpath.2019.05.016_bib45 article-title: Lactate reduces liver and pancreatic injury in Toll-like receptor- and inflammasome-mediated inflammation via GPR81-mediated suppression of innate immunity publication-title: Gastroenterology doi: 10.1053/j.gastro.2014.03.014 – volume: 74 start-page: 5301 year: 2014 ident: 10.1016/j.ajpath.2019.05.016_bib44 article-title: Cell surface lactate receptor GPR81 is crucial for cancer cell survival publication-title: Cancer Res doi: 10.1158/0008-5472.CAN-14-0319 – volume: 72 start-page: 8463 year: 1998 ident: 10.1016/j.ajpath.2019.05.016_bib54 article-title: A third-generation lentivirus vector with a conditional packaging system publication-title: J Virol doi: 10.1128/JVI.72.11.8463-8471.1998 – volume: 17 start-page: 5163 year: 2006 ident: 10.1016/j.ajpath.2019.05.016_bib64 article-title: Wnt5a signaling induces proliferation and survival of endothelial cells in vitro and expression of MMP-1 and Tie-2 publication-title: Mol Biol Cell doi: 10.1091/mbc.e06-04-0320 – volume: 223 start-page: e13042 year: 2018 ident: 10.1016/j.ajpath.2019.05.016_bib74 article-title: Lactate increases myotube diameter via activation of MEK/ERK pathway in C2C12 cells publication-title: Acta Physiol (Oxf) doi: 10.1111/apha.13042 – volume: 50 start-page: 2436 year: 2009 ident: 10.1016/j.ajpath.2019.05.016_bib14 article-title: Functional and structural changes resulting from strain differences in the rat model of oxygen-induced retinopathy publication-title: Invest Ophthalmol Vis Sci doi: 10.1167/iovs.08-2297 – volume: 46 start-page: 3372 year: 2005 ident: 10.1016/j.ajpath.2019.05.016_bib8 article-title: Role of the Norrie disease pseudoglioma gene in sprouting angiogenesis during development of the retinal vasculature publication-title: Invest Ophthalmol Vis Sci doi: 10.1167/iovs.05-0174 – volume: 4 start-page: 727 year: 2011 ident: 10.1016/j.ajpath.2019.05.016_bib33 article-title: Lactate shuttles at a glance: from physiological paradigms to anti-cancer treatments publication-title: Dis Model Mech doi: 10.1242/dmm.007724 – volume: 10 start-page: 486 year: 2012 ident: 10.1016/j.ajpath.2019.05.016_bib58 article-title: Normality tests for statistical analysis: a guide for non-statisticians publication-title: Int J Endocrinol Metab doi: 10.5812/ijem.3505 – volume: 139 start-page: 299 year: 2009 ident: 10.1016/j.ajpath.2019.05.016_bib24 article-title: TSPAN12 regulates retinal vascular development by promoting Norrin- but not Wnt-induced FZD4/beta-catenin signaling publication-title: Cell doi: 10.1016/j.cell.2009.07.048 – volume: 63 start-page: 3926 year: 2014 ident: 10.1016/j.ajpath.2019.05.016_bib63 article-title: Neuroretinal dysfunction with intact blood-retinal barrier and absent vasculopathy in type 1 diabetes publication-title: Diabetes doi: 10.2337/db13-1673 – volume: 20 start-page: 175 year: 2001 ident: 10.1016/j.ajpath.2019.05.016_bib80 article-title: Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease publication-title: Prog Retin Eye Res doi: 10.1016/S1350-9462(00)00027-6 – volume: 111 start-page: 7 year: 2005 ident: 10.1016/j.ajpath.2019.05.016_bib11 article-title: Multifocal ERG in subjects with a history of retinopathy of prematurity publication-title: Doc Ophthalmol doi: 10.1007/s10633-005-2621-3 – volume: 49 start-page: 458 year: 2008 ident: 10.1016/j.ajpath.2019.05.016_bib13 article-title: Early manifestations of postnatal hyperoxia on the retinal structure and function of the neonatal rat publication-title: Invest Ophthalmol Vis Sci doi: 10.1167/iovs.07-0916 – volume: 41 start-page: 927 year: 2000 ident: 10.1016/j.ajpath.2019.05.016_bib56 article-title: Neurotrophic factors cause activation of intracellular signaling pathways in Muller cells and other cells of the inner retina, but not photoreceptors publication-title: Invest Ophthalmol Vis Sci – volume: 39 start-page: 840 year: 1998 ident: 10.1016/j.ajpath.2019.05.016_bib9 article-title: Abnormal panretinal response pattern to carbogen inhalation in experimental retinopathy of prematurity publication-title: Invest Ophthalmol Vis Sci – volume: 52 start-page: 1693 year: 2011 ident: 10.1016/j.ajpath.2019.05.016_bib10 article-title: Immunohistochemical evidence of synaptic retraction, cytoarchitectural remodeling, and cell death in the inner retina of the rat model of oxygen-induced retinopathy (OIR) publication-title: Invest Ophthalmol Vis Sci doi: 10.1167/iovs.10-6197 – volume: 15 start-page: 5179 year: 1995 ident: 10.1016/j.ajpath.2019.05.016_bib28 article-title: Lactate released by Muller glial cells is metabolized by photoreceptors from mammalian retina publication-title: J Neurosci doi: 10.1523/JNEUROSCI.15-07-05179.1995 – volume: 50 start-page: 906 year: 2009 ident: 10.1016/j.ajpath.2019.05.016_bib65 article-title: Differential gene expression in Ndph-knockout mice in retinal development publication-title: Invest Ophthalmol Vis Sci doi: 10.1167/iovs.08-1731 – volume: 35 start-page: 101 year: 1994 ident: 10.1016/j.ajpath.2019.05.016_bib48 article-title: Oxygen-induced retinopathy in the mouse publication-title: Invest Ophthalmol Vis Sci – volume: 331 start-page: 753 year: 1994 ident: 10.1016/j.ajpath.2019.05.016_bib15 article-title: School-age outcomes in children with birth weights under 750 g publication-title: N Engl J Med doi: 10.1056/NEJM199409223311201 – volume: 76 start-page: 615 year: 1983 ident: 10.1016/j.ajpath.2019.05.016_bib31 article-title: The anaerobic molluscan heart: adaptation to environmental anoxia: comparison with energy metabolism in vertebrate hearts publication-title: Comp Biochem Physiol A Comp Physiol doi: 10.1016/0300-9629(83)90463-2 – volume: 41 start-page: 1229 year: 2016 ident: 10.1016/j.ajpath.2019.05.016_bib60 article-title: Lactate transport and receptor actions in retina: potential roles in retinal function and disease publication-title: Neurochem Res doi: 10.1007/s11064-015-1792-x – volume: 71 start-page: 6921 year: 2011 ident: 10.1016/j.ajpath.2019.05.016_bib82 article-title: Lactate: a metabolic key player in cancer publication-title: Cancer Res doi: 10.1158/0008-5472.CAN-11-1457 – volume: 17 start-page: 429 year: 1998 ident: 10.1016/j.ajpath.2019.05.016_bib27 article-title: Trafficking of molecules and metabolic signals in the retina publication-title: Prog Retin Eye Res doi: 10.1016/S1350-9462(98)00010-X – volume: 14 start-page: 1067 year: 2008 ident: 10.1016/j.ajpath.2019.05.016_bib20 article-title: The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis publication-title: Nat Med doi: 10.1038/nm.1873 – volume: 33 start-page: 323 year: 1970 ident: 10.1016/j.ajpath.2019.05.016_bib92 article-title: Intracellular responses of the Muller (glial) cells of mudpuppy retina: their relation to b-wave of the electroretinogram publication-title: J Neurophysiol doi: 10.1152/jn.1970.33.3.323 – volume: 320 start-page: 257 year: 1992 ident: 10.1016/j.ajpath.2019.05.016_bib84 article-title: Glucose metabolism in freshly isolated Muller glial cells from a mammalian retina publication-title: J Comp Neurol doi: 10.1002/cne.903200209 – volume: 37 start-page: 2467 year: 1996 ident: 10.1016/j.ajpath.2019.05.016_bib12 article-title: Color vision measured with pseudoisochromatic plates at five-and-a-half years in eyes of children from the CRYO-ROP study publication-title: Invest Ophthalmol Vis Sci – volume: 62 start-page: 412 year: 1966 ident: 10.1016/j.ajpath.2019.05.016_bib6 article-title: Oxygen and the growth and development of retinal vessels: in vivo and in vitro studies: the XX Francis I. Proctor Lecture publication-title: Am J Ophthalmol doi: 10.1016/0002-9394(66)91322-5 – volume: 216 start-page: 60.e1 year: 2017 ident: 10.1016/j.ajpath.2019.05.016_bib46 article-title: Lactate produced during labor modulates uterine inflammation via GPR81 (HCA1) publication-title: Am J Obstet Gynecol doi: 10.1016/j.ajog.2016.09.072 – volume: 14 start-page: 181 year: 2017 ident: 10.1016/j.ajpath.2019.05.016_bib50 article-title: Tetrahydrobiopterin (BH4) deficiency is associated with augmented inflammation and microvascular degeneration in the retina publication-title: J Neuroinflammation doi: 10.1186/s12974-017-0955-x – volume: 15 start-page: 581 year: 2012 ident: 10.1016/j.ajpath.2019.05.016_bib34 article-title: Lactate stimulates angiogenesis and accelerates the healing of superficial and ischemic wounds in mice publication-title: Angiogenesis doi: 10.1007/s10456-012-9282-0 – volume: 21 start-page: 271 year: 2015 ident: 10.1016/j.ajpath.2019.05.016_bib43 article-title: Inhibition of G protein-coupled receptor 81 (GPR81) protects against ischemic brain injury publication-title: CNS Neurosci Ther doi: 10.1111/cns.12362 – volume: 20 start-page: 1532 year: 2001 ident: 10.1016/j.ajpath.2019.05.016_bib5 article-title: New mechanisms in heptahelical receptor signaling to mitogen activated protein kinase cascades publication-title: Oncogene doi: 10.1038/sj.onc.1204184 – volume: 71 start-page: 2550 year: 2011 ident: 10.1016/j.ajpath.2019.05.016_bib69 article-title: Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-kappaB/IL-8 pathway that drives tumor angiogenesis publication-title: Cancer Res doi: 10.1158/0008-5472.CAN-10-2828 – volume: 131 start-page: 1663 year: 2004 ident: 10.1016/j.ajpath.2019.05.016_bib90 article-title: LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: arrows point the way publication-title: Development doi: 10.1242/dev.01117 – volume: 17 start-page: 1605 year: 2008 ident: 10.1016/j.ajpath.2019.05.016_bib91 article-title: A model for familial exudative vitreoretinopathy caused by LPR5 mutations publication-title: Hum Mol Genet doi: 10.1093/hmg/ddn047 – volume: 115 start-page: 1553 year: 1997 ident: 10.1016/j.ajpath.2019.05.016_bib2 article-title: Systemic hyperoxia decreases vascular endothelial growth factor gene expression in ischemic primate retina publication-title: Arch Ophthalmol doi: 10.1001/archopht.1997.01100160723009 – volume: 284 start-page: 2811 year: 2009 ident: 10.1016/j.ajpath.2019.05.016_bib42 article-title: Lactate inhibits lipolysis in fat cells through activation of an orphan G-protein-coupled receptor, GPR81 publication-title: J Biol Chem doi: 10.1074/jbc.M806409200 – volume: 42 start-page: 1111 year: 2001 ident: 10.1016/j.ajpath.2019.05.016_bib19 article-title: Graded contribution of retinal maturation to the development of oxygen-induced retinopathy in rats publication-title: Invest Ophthalmol Vis Sci – volume: 16 start-page: 417 year: 2010 ident: 10.1016/j.ajpath.2019.05.016_bib70 article-title: The Norrin/Frizzled4 signaling pathway in retinal vascular development and disease publication-title: Trends Mol Med doi: 10.1016/j.molmed.2010.07.003 – volume: 48 start-page: 2290 year: 2007 ident: 10.1016/j.ajpath.2019.05.016_bib81 article-title: Intraretinal oxygen distribution and consumption during retinal artery occlusion and graded hyperoxic ventilation in the rat publication-title: Invest Ophthalmol Vis Sci doi: 10.1167/iovs.06-1197 – volume: 895 start-page: 268 year: 2001 ident: 10.1016/j.ajpath.2019.05.016_bib37 article-title: Blockade of lactate transport exacerbates delayed neuronal damage in a rat model of cerebral ischemia publication-title: Brain Res doi: 10.1016/S0006-8993(01)02082-0 – volume: 6 start-page: e27385 year: 2011 ident: 10.1016/j.ajpath.2019.05.016_bib52 article-title: A computational tool for quantitative analysis of vascular networks publication-title: PLoS One doi: 10.1371/journal.pone.0027385 – volume: 358 start-page: 817 year: 2001 ident: 10.1016/j.ajpath.2019.05.016_bib16 article-title: Angiogenesis and functional recovery demonstrated after minor stroke publication-title: Lancet – volume: 18 start-page: 1319 year: 2012 ident: 10.1016/j.ajpath.2019.05.016_bib32 article-title: Multiple biological activities of lactic acid in cancer: influences on tumor growth, angiogenesis and metastasis publication-title: Curr Pharm Des doi: 10.2174/138161212799504902 – volume: 185 start-page: 581 year: 2015 ident: 10.1016/j.ajpath.2019.05.016_bib51 article-title: Retinal neurons curb inflammation and enhance revascularization in ischemic retinopathies via proteinase-activated receptor-2 publication-title: Am J Pathol doi: 10.1016/j.ajpath.2014.10.020 – volume: 7 start-page: 70898 year: 2016 ident: 10.1016/j.ajpath.2019.05.016_bib47 article-title: G-protein-coupled receptor 81 promotes a malignant phenotype in breast cancer through angiogenic factor secretion publication-title: Oncotarget doi: 10.18632/oncotarget.12286 – volume: 52 start-page: 3215 year: 2011 ident: 10.1016/j.ajpath.2019.05.016_bib68 article-title: Vasomotor effect of intravitreal juxta-arteriolar injection of L-lactate on the retinal arterioles after acute branch retinal vein occlusion in minipigs publication-title: Invest Ophthalmol Vis Sci doi: 10.1167/iovs.10-6888 – volume: 101 start-page: 819 year: 2012 ident: 10.1016/j.ajpath.2019.05.016_bib87 article-title: Neovascularization in retinopathy of prematurity: opposing actions of neuronal factors GPR91 and semaphorins 3A publication-title: Acta Paediatr doi: 10.1111/j.1651-2227.2012.02692.x – volume: 151 start-page: 1332 year: 2012 ident: 10.1016/j.ajpath.2019.05.016_bib67 article-title: Norrin/Frizzled4 signaling in retinal vascular development and blood brain barrier plasticity publication-title: Cell doi: 10.1016/j.cell.2012.10.042 – volume: 55 start-page: 929 year: 2006 ident: 10.1016/j.ajpath.2019.05.016_bib36 article-title: Increased brain monocarboxylic acid transport and utilization in type 1 diabetes publication-title: Diabetes doi: 10.2337/diabetes.55.04.06.db05-1325 – volume: 36 start-page: 2063 year: 1995 ident: 10.1016/j.ajpath.2019.05.016_bib1 article-title: The range of PaO2 variation determines the severity of oxygen-induced retinopathy in newborn rats publication-title: Invest Ophthalmol Vis Sci – volume: 43 start-page: 2481 year: 2002 ident: 10.1016/j.ajpath.2019.05.016_bib18 article-title: Evidence for a brief period of enhanced oxygen susceptibility in the rat model of oxygen-induced retinopathy publication-title: Invest Ophthalmol Vis Sci – volume: 30 start-page: 183 year: 2010 ident: 10.1016/j.ajpath.2019.05.016_bib72 article-title: Norrin promotes vascular regrowth after oxygen-induced retinal vessel loss and suppresses retinopathy in mice publication-title: J Neurosci doi: 10.1523/JNEUROSCI.3210-09.2010 – volume: 86 start-page: 1 year: 2001 ident: 10.1016/j.ajpath.2019.05.016_bib57 article-title: Characterization of a transformed rat retinal ganglion cell line publication-title: Brain Res Mol Brain Res doi: 10.1016/S0169-328X(00)00224-2 – volume: 15 start-page: 4738 year: 1995 ident: 10.1016/j.ajpath.2019.05.016_bib21 article-title: Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia publication-title: J Neurosci doi: 10.1523/JNEUROSCI.15-07-04738.1995 – volume: 65 start-page: 967 year: 2013 ident: 10.1016/j.ajpath.2019.05.016_bib40 article-title: International Union of Basic and Clinical Pharmacology: LXXXVIII: G protein-coupled receptor list: recommendations for new pairings with cognate ligands publication-title: Pharmacol Rev doi: 10.1124/pr.112.007179 – volume: 24 start-page: 2784 year: 2014 ident: 10.1016/j.ajpath.2019.05.016_bib41 article-title: Lactate receptor sites link neurotransmission, neurovascular coupling, and brain energy metabolism publication-title: Cereb Cortex doi: 10.1093/cercor/bht136 – volume: 8 start-page: 441 year: 1957 ident: 10.1016/j.ajpath.2019.05.016_bib7 article-title: Experimental retrolental fibroplasia publication-title: Annu Rev Med doi: 10.1146/annurev.me.08.020157.002301 – volume: 30 start-page: 5998 year: 2010 ident: 10.1016/j.ajpath.2019.05.016_bib26 article-title: Norrin mediates neuroprotective effects on retinal ganglion cells via activation of the Wnt/beta-catenin signaling pathway and the induction of neuroprotective growth factors in Muller cells publication-title: J Neurosci doi: 10.1523/JNEUROSCI.0730-10.2010 – volume: 92 start-page: 905 year: 1995 ident: 10.1016/j.ajpath.2019.05.016_bib3 article-title: Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.92.3.905 – volume: 7 start-page: e33418 year: 2012 ident: 10.1016/j.ajpath.2019.05.016_bib76 article-title: Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis publication-title: PLoS One doi: 10.1371/journal.pone.0033418 – volume: 8 start-page: 67 year: 2016 ident: 10.1016/j.ajpath.2019.05.016_bib71 article-title: Revisiting the mouse model of oxygen-induced retinopathy publication-title: Eye Brain doi: 10.2147/EB.S94447 – volume: 60 start-page: 916 year: 2000 ident: 10.1016/j.ajpath.2019.05.016_bib77 article-title: High lactate levels predict likelihood of metastases, tumor recurrence, and restricted patient survival in human cervical cancers publication-title: Cancer Res
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Snippet	Ischemic retinopathies are characterized by a progressive microvascular degeneration followed by a postischemic aberrant neovascularization. To reinstate...
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SubjectTerms	Animals Ependymoglial Cells - metabolism Ependymoglial Cells - pathology Eye Proteins - genetics Eye Proteins - metabolism Ischemia - etiology Ischemia - metabolism Ischemia - pathology Lactic Acid - metabolism Mice Mice, Knockout Nerve Tissue Proteins - genetics Nerve Tissue Proteins - metabolism Receptors, G-Protein-Coupled - physiology Retinal Diseases - etiology Retinal Diseases - metabolism Retinal Diseases - pathology Retinal Neovascularization - etiology Retinal Neovascularization - metabolism Retinal Neovascularization - pathology Retinal Vessels - metabolism Retinal Vessels - pathology Wnt Proteins - genetics Wnt Proteins - metabolism
Title	Müller Cell–Localized G-Protein–Coupled Receptor 81 (Hydroxycarboxylic Acid Receptor 1) Regulates Inner Retinal Vasculature via Norrin/Wnt Pathways
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