Beneficial Bacteria Affect Danio rerio Development by the Modulation of Maternal Factors Involved in Autophagic, Apoptotic and Dorsalizing Processes
Background/Aims: Probiotic strains have been recognized to exert important roles in many biological systems, including immune response, growth, development and reproduction. However, to date, no studies have focused either on the relation among probiotics and maternal factors or on probiotics'...
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Published in | Cellular physiology and biochemistry Vol. 35; no. 5; pp. 1706 - 1718 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
Basel, Switzerland
Cell Physiol Biochem Press GmbH & Co KG
01.01.2015
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Subjects | |
Online Access | Get full text |
ISSN | 1015-8987 1421-9778 |
DOI | 10.1159/000373983 |
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Abstract | Background/Aims: Probiotic strains have been recognized to exert important roles in many biological systems, including immune response, growth, development and reproduction. However, to date, no studies have focused either on the relation among probiotics and maternal factors or on probiotics' ability to qualitatively and/or quantitatively modulate maternal transcripts. Methods: In this study, the effects of Lactobacillusrhamnosus administered to parental fish on the control of maternal factors involved in autophagic, apoptotic and dorsalizing processes during zebrafish embryo development were assessed through q-PCRs, WMISH and TUNEL assay. Results: The results we obtained show that probiotic induced significant changes in both maternal and zygotic mRNA levels involved in embryo development. The maternal autophagy-regulating genes herein investigated -ambra1a, ambra1b, beclin, lc3-, as well as those involved in the apoptotic process -caspase3, bcl2, bax- were modulated in disfavor and favor of the treated group, respectively. Also, the key transcripts ruling the dorsalizing process -goosecoid and chordin- were subject to a significant regulation of their gene expression. Conclusion: The results we acquired demonstrated that parentally administered Lactobacillusrhamnosus is able to modulate important physiological processes involved in zebrafish embryo development. |
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AbstractList | Background/Aims: Probiotic strains have been recognized to exert important roles in many biological systems, including immune response, growth, development and reproduction. However, to date, no studies have focused either on the relation among probiotics and maternal factors or on probiotics' ability to qualitatively and/or quantitatively modulate maternal transcripts. Methods: In this study, the effects of Lactobacillusrhamnosus administered to parental fish on the control of maternal factors involved in autophagic, apoptotic and dorsalizing processes during zebrafish embryo development were assessed through q-PCRs, WMISH and TUNEL assay. Results: The results we obtained show that probiotic induced significant changes in both maternal and zygotic mRNA levels involved in embryo development. The maternal autophagy-regulating genes herein investigated -ambra1a, ambra1b, beclin, lc3-, as well as those involved in the apoptotic process -caspase3, bcl2, bax- were modulated in disfavor and favor of the treated group, respectively. Also, the key transcripts ruling the dorsalizing process -goosecoid and chordin- were subject to a significant regulation of their gene expression. Conclusion: The results we acquired demonstrated that parentally administered Lactobacillusrhamnosus is able to modulate important physiological processes involved in zebrafish embryo development. Probiotic strains have been recognized to exert important roles in many biological systems, including immune response, growth, development and reproduction. However, to date, no studies have focused either on the relation among probiotics and maternal factors or on probiotics' ability to qualitatively and/or quantitatively modulate maternal transcripts. In this study, the effects of Lactobacillus rhamnosus administered to parental fish on the control of maternal factors involved in autophagic, apoptotic and dorsalizing processes during zebrafish embryo development were assessed through q-PCRs, WMISH and TUNEL assay. The results we obtained show that probiotic induced significant changes in both maternal and zygotic mRNA levels involved in embryo development. The maternal autophagy-regulating genes herein investigated--ambra1a, ambra1b, beclin, lc3-, as well as those involved in the apoptotic process--caspase3, bcl2, bax--were modulated in disfavor and favor of the treated group, respectively. Also, the key transcripts ruling the dorsalizing process--goosecoid and chordin--were subject to a significant regulation of their gene expression. The results we acquired demonstrated that parentally administered Lactobacillus rhamnosus is able to modulate important physiological processes involved in zebrafish embryo development. |
Author | Gioacchini, Giorgia Benato, Francesca Maradonna, Francesca Miccoli, Andrea Skobo, Tatjana Carnevali, Oliana |
Author_xml | – sequence: 1 givenname: Andrea surname: Miccoli fullname: Miccoli, Andrea – sequence: 2 givenname: Giorgia surname: Gioacchini fullname: Gioacchini, Giorgia – sequence: 3 givenname: Francesca surname: Maradonna fullname: Maradonna, Francesca – sequence: 4 givenname: Francesca surname: Benato fullname: Benato, Francesca – sequence: 5 givenname: Tatjana surname: Skobo fullname: Skobo, Tatjana – sequence: 6 givenname: Oliana surname: Carnevali fullname: Carnevali, Oliana email: o.carnevali@univpm.it |
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Keywords | Probiotics Ambra1 Bcl2 Bax Beclin1 Chordin Caspase3 Dorsalization Goosecoid Lc3 |
Language | English |
License | Open Access License: This is an Open Access article licensed under the terms of the Creative Commons Attribution-NonCommercial 3.0 Unported license (CC BY-NC) applicable to the online version of the article only. Distribution permitted for non-commercial purposes only. https://creativecommons.org/licenses/by-nc/3.0 2015 S. Karger AG, Basel. |
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References | Miller-Bertoglio VE, Fisher S, Sánchez A, Mullins MC, Halpern ME: Differential Regulation of chordin Expression Domains in Mutant Zebrafish. Dev Biol 1997;192:537-550.944168710.1006/dbio.1997.8788 Gatesoupe FJ: Bacillus sp. spores as food additive for the rotifer Brachionus plicatilis: improvement of their bacterial environment and their dietary value for larval turbot, Scophthalmus maximus L; in Kaushik SJ, Luquet P (eds): Fish Nutrition in Practice. Paris, Les Colloques, 1993, vol 61, pp 561-568. Piccolo S, Sasai Y, Lu B, De Robertis EM: Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 1996;86:589-598.875221310.1016/S0092-8674(00)80132-4 Schulte-Merker S, Hammerschmidt M, Beuchle D, Cho KW, De Robertis EM, Nusslein-Volhard C: Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos. Development 1994;120:843-852.7600961 Skobo T, Benato F, Grumati P, Meneghetti G, Cianfanelli V, Castagnaro S, Chrisam M, Di Bartolomeo S, Bonaldo P, Cecconi F, Dalla Valle L: Zebrafish ambra1a and ambra1b Knockdown Impairs Skeletal Muscle Development. PloS One DOI: 10.1371/journal.pone.0099210.2492254610.1371/journal.pone.0099210 Kratz E, Eimon PM, Mukhyala K, Stern H, Zha J, Strasser A, Hart R, and Ashkenazi A: Functional characterization of the Bcl-2 gene family in the zebrafish. Cell Death Differ 2006;13:1631-1640.1688864610.1038/sj.cdd.4402016 Gioacchini G, Maradonna F, Lombardo F, Bizzaro D, Olivotto I, Carnevali O: Increase of fecundity by probiotic administration in zebrafish (Danio rerio). Reproduction 2010;140:953-959.2083375310.1530/REP-10-0145 Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF: Stages of embryonic development of the zebrafish. Dev Dyn 1995;203:253-310.858942710.1002/aja.1002030302 Lee E, Koo Y, Ng A, Wei Y, Luby-Phelps K, Juraszek A, Xavier RJ, Cleaver O, Levine B and Amatruda JF: Autophagy is essential for cardiac morphogenesis during vertebrate development. Autophagy 2014;10:572-587.2444142310.4161/auto.27649 Meier P, Finch A, Evan G: Apoptosis in development. Nature 2000;407:796-801.1104873110.1038/35037734 Avella MA, Olivotto I, Silvi S, Place AR, Carnevali O: Effect of dietary probiotics on clownfish: a molecular approach to define how lactic acid bacteria modulate development in a marine fish. Am J Physiol Regul Integr Comp Physiol 2010;298:359-371.1992335410.1152/ajpregu.00300.2009 Rollo A, Sulpizio R, Nardi M, Silvi S, Orpianesi C, Caggiano M, Cresci A, Carnevali O: Live microbial feed supplement in aquaculture for improvement of stress tolerance. Fish Physiol Biochem 2006;32:167-177.10.1007/s10695-006-0009-2 Kane DA, Kimmel CB: The zebrafish midblastula transition. Development 1993;119:447-456.8287796 Nikoskelainen S, Ouwehand AC, Bylund G, Salminen S: Protection of rainbow trout (Oncorhuncus mykiss) from furunculosis by Lactobacillus rhamnosus. Aquaculture 2001;198:229-236.10.1016/S0044-8486(01)00593-2 Bachiller D, Klingensmith J, Kemp C, Belo JA, Anderson RM, May SR, De Robertis EM: The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature 2000;403:658-661.1068820210.1038/35001072 Stachel SE, Grunwald DJ, Myers PZ: Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish. Development 1993;117:1261-1274.8104775 Oppenheim RW: Cell death during development of the nervous system. Annu Rev Neurosci 1991;14:453-501.203157710.1146/annurev.ne.14.030191.002321 García-Arencibia M, Hochfeld WE, Toh PP, Rubinsztein DC: Autophagy, a guardian against neurodegeneration. Semin Cell Dev Biol 2010;21:691-698.2018820310.1016/j.semcdb.2010.02.008 Aubin J, Gatesoupe FJ, Labbé L, Lebrun L: Trial of probiotics to prevent the vertebral column compression syndrome in rainbow trout (Oncorhynchus mykiss Walbaum). Aquac Res 2005;36:758-767.10.1111/j.1365-2109.2005.01280.x Hogan BL: Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev 1996;10:1580-1594.868229010.1101/gad.10.13.1580 Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, Corazzari M, Fuoco C, Ucar A, Schwartz P, Gruss P, Piacentini M, Chowdhury K, Cecconi F: Ambra1 regulates autophagy and development of the nervous system. Nature 2007;447:1121-1127.1758950410.1038/nature05925 Kemphues KJ, Strome S: Fertilization and Establishment of Polarity in the Embryo; in Riddle DL, Blumenthal T, Meyer BJ, et al., (eds): C. elegans II. Cold Spring Harbor Monograph Archive, 1997.21413241 Lamari F, Castex M, Larcher T, Ledevin M, Mazurais D, Bakhrouf A, Gatesoupe FJ: Comparison of the effects of the dietary addition of two lactic acid bacteria on the development and conformation of sea bass larvae, Dicentrarchus labrax, and the influence on associated microbiota. Aquaculture 2013;376:137-145.10.1016/j.aquaculture.2012.11.016 Vendrell D, Luis BJ, De Blas I, Ruiz-Zarzuela I: Protection of rainbow trout (Oncorhynchus mykiss) from lactococcosis by probiotic bacteria. Comp Immunol Microbiol Infect Dis 2008;31:337-345.1753247010.1016/j.cimid.2007.04.002 McCabe LR, Irwin R, Schaefer L, Britton RA: Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. J Cell Physiol 2013;228:1793-1798.2338986010.1002/jcp.24340 Watabe T, Kim S, Candia A, Rothbächer U, Hashimoto C, Inoue K, Cho KW: Molecular mechanisms of Spemann's organizer formation: conserved growth factor synergy between Xenopus and mouse. Genes Dev 1995;9:3038-3050.854315010.1101/gad.9.24.3038 Sasai Y, Lu B, Steinbeisser H, Geissert D, Gont LK, De Robertis EM: Xenopus chordin: A novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 1994;79:779-790.800111710.1016/0092-8674(94)90068-X Thornberry NA, Lazebnik Y: Caspases: enemies within. Science 1998;281:1312-1316.972109110.1126/science.281.5381.1312 Balcázar JL, De Blas I, Ruiz-Zarzuela I, Vendrell D, Calvo AC, Márquez I, Gironés O, Muzquiz, JL: Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta). Br J Nutr 2007;97:522-527.1731371410.1017/S0007114507432986 Ringo E, Gatesoupe FJ: Lactic acid bacteria in fish: a review. Aquaculture 1998;160:177-203.10.1016/S0044-8486(97)00299-8 Avella MA, Place A, Du SJ, Williams E, Silvi S, Zohar Y, Carnevali O: Lactobacillus rhamnosus accelerates zebrafish backbone calcification and gonadal differentiation through effects on the GnRH and IGF systems. PLoS One DOI: 10.1371/journal.pone.0045572.2302910710.1371/journal.pone.0045572 Maradonna F, Gioacchini G, Falcinelli S, Bertotto D, Radaelli G, Olivotto I, Carnevali O: Probiotic Supplementation Promotes Calcification in Danio rerio Larvae: A Molecular Study. PloS One DOI: 10.1371/journal.pone.0083155.2435825910.1371/journal.pone.0083155 Castex M, Chim L, Pham D, Lemaire P, Wabete N, Nicolas JL, Mariojouls C: Probiotic P. acidilactici application in shrimp Litopenaeus stylirostris culture subject to vibriosis in New Caledonia. Aquaculture 2008;275:182-193.10.1016/j.aquaculture.2008.01.011 Cecconi F, Di Bartolomeo S, Nardacci R, Fuoco C, Corazzari M, Giunta L, Romagnoli A, Stoykova A, Chowdhury K, Fimia GM, Piacentini M: A novel role for autophagy in neurodevelopment. Autophagy 2007;3:506-508.1762279610.4161/auto.4616 Di Bartolomeo S, Corazzari M, Nazio F, Oliverio S, Lisi G, Antonioli M, Pagliarini V, Matteoni S, Fuoco C, Giunta L, D'Amelio M, Nardacci R, Romagnoli A, Piacentini M, Cecconi F, Fimia GM: The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J Cell Biol 2010;191:155-168.2092113910.1083/jcb.201002100 Lombardo F, Gioacchini G, Carnevali O: Probiotic-based Nutritional Effects on Killifish reproduction. Fish Aquacult 2011;J FAJ-33. Picchietti S, Mazzini M, Taddei AR, Renna R, Fausto AM, Mulero V, Carnevali O, Cresci A, Abelli L: Effects of administration of probiotic strains on GALT of larval gilthead seabream: Immunohistochemical and ultrastructural studies. Fish Shellfish Immunol 2007;22:57-67.1673045810.1016/j.fsi.2006.03.009 Verschuere L, Rombaut G, Sorgeloos P, Verstraete W: Probiotic bacteria as biological control agents in aquaculture. Microbiol Mol Biol Rev 2000;64:655-671.1110481310.1128/MMBR.64.4.655-671.2000 Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, Yuan J: Human ICE/CED3 protease nomenclature. Cell 1996;87:171.886190010.1016/S0092-8674(00)81334-3 Nishida H: Specification of embryonic axis and mosaic development in ascidians. Dev Dyn 2005;233:1177-1193.1597369210.1002/dvdy.20469 Tadros W, Lipshitz HD: Setting the stage for development: mRNA translation and stability during oocyte maturation and egg activation in Drosophila. Dev Dyn 2005;232:593-608.1570415010.1002/dvdy.20297 Gioacchini G, Giorgini E, Merrifield DL, Hardiman G, Borini A, Vaccari L, Carnevali O: Probiotics Can Induce Follicle Maturational Competence: The Danio rerio Case. Biol Reprod 2012;86:1-11.2208891910.1095/biolreprod.111.094243 Fuller R: History and development of probiotics; in Fuller R (eds): Probiotics: The Scientific Basis. London, Chapman and Hall, pp 1-8.10.1007/978-94-011-2364-8_1 Benato F, Skobo T, Gioacchini G, Moro I, Ciccosanti F, Piacentini M, Fimia GM, Carnevali O, Dalla Valle L: Ambra1 knockdown in zebrafish leads to incomplete development due to severe defects in organogenesis. Autophagy 2013;9:1-20.2334805410.4161/auto.23278 Pelegri F: Maternal factors in zebrafish development. Dev Dyn 2003;228:535-554.1457939110.1002/dvdy.10390 Merrifield DL, Dimitroglou A, Bradley G, Baker RTM, Davies SJ: Probiotic application for rainbow trout (Onchorynchus mykiss Walbum) I. Effects on growth performance, feed utilization, intestinal microbiota, and related health criteria. Aquac Nutr 2010;16:504-510.10.1111/j.1365-2095.2009.00689.x Carnevali O, De Vivo L, Sulpizio R, Gioacchini G, Olivotto I, Silvi S, Cresci A: Well-fare and growth improvement by probiotics in |
References_xml | – reference: Gioacchini G, Maradonna F, Lombardo F, Bizzaro D, Olivotto I, Carnevali O: Increase of fecundity by probiotic administration in zebrafish (Danio rerio). Reproduction 2010;140:953-959.2083375310.1530/REP-10-0145 – reference: Pelegri F: Maternal factors in zebrafish development. Dev Dyn 2003;228:535-554.1457939110.1002/dvdy.10390 – reference: García-Arencibia M, Hochfeld WE, Toh PP, Rubinsztein DC: Autophagy, a guardian against neurodegeneration. Semin Cell Dev Biol 2010;21:691-698.2018820310.1016/j.semcdb.2010.02.008 – reference: Miller-Bertoglio VE, Fisher S, Sánchez A, Mullins MC, Halpern ME: Differential Regulation of chordin Expression Domains in Mutant Zebrafish. Dev Biol 1997;192:537-550.944168710.1006/dbio.1997.8788 – reference: Gioacchini G, Giorgini E, Olivotto I, Maradonna F, Merrifield DL, Carnevali, O: The Influence of Probiotics on Zebrafish Danio Rerio Innate Immunity and Hepatic Stress. Zebrafish DOI: 10.1089/zeb.2013.0932.2456461910.1089/zeb.2013.0932 – reference: Avella MA, Place A, Du SJ, Williams E, Silvi S, Zohar Y, Carnevali O: Lactobacillus rhamnosus accelerates zebrafish backbone calcification and gonadal differentiation through effects on the GnRH and IGF systems. PLoS One DOI: 10.1371/journal.pone.0045572.2302910710.1371/journal.pone.0045572 – reference: Noh SH, Han K, Won TH, Choi YJ: Effect of antibiotics, enzyme, yeast culture and probiotics on the growth performance of Israeli carp. Korean Journal of Animal Science 1994;36:480-486. – reference: Skobo T, Benato F, Grumati P, Meneghetti G, Cianfanelli V, Castagnaro S, Chrisam M, Di Bartolomeo S, Bonaldo P, Cecconi F, Dalla Valle L: Zebrafish ambra1a and ambra1b Knockdown Impairs Skeletal Muscle Development. PloS One DOI: 10.1371/journal.pone.0099210.2492254610.1371/journal.pone.0099210 – reference: Gatesoupe, FJ: Siderophore production and probiotic effect of Vibrio sp. associated with turbot larvae, Scophthalmus maximus. Aquat Living Resour 1997;10:239-246.10.1051/alr:1997026 – reference: Nikoskelainen S, Ouwehand AC, Bylund G, Salminen S, Lilius EM: Immune enhancement in rainbow trout (Oncorhyncus mykiss) by potential probiotic bacteria (Lactobacillus rhamnosus). Fish Shellfish Immunol 2003;15:443-452.1455067010.1016/S1050-4648(03)00023-8 – reference: Tadros W, Lipshitz HD: The maternal-to-zygotic transition: a play in two acts. Development 2009;136:3033-3042.1970061510.1242/dev.033183 – reference: Nikoskelainen S, Ouwehand AC, Bylund G, Salminen S: Protection of rainbow trout (Oncorhuncus mykiss) from furunculosis by Lactobacillus rhamnosus. Aquaculture 2001;198:229-236.10.1016/S0044-8486(01)00593-2 – reference: Aubin J, Gatesoupe FJ, Labbé L, Lebrun L: Trial of probiotics to prevent the vertebral column compression syndrome in rainbow trout (Oncorhynchus mykiss Walbaum). Aquac Res 2005;36:758-767.10.1111/j.1365-2109.2005.01280.x – reference: Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, Munday NA, Raju SM, Smulson ME, Yamin TT, Yu VL, Miller DK: Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995;376:37-43.759643010.1038/376037a0 – reference: Balcázar JL, Decamp O, Vendrell D, De Blas I, Ruiz-Zarzuela I: Health and nutritional properties of probiotics in fish and shellfish. Microb Ecol 2006;18:65-70.10.1080/08910600600799497 – reference: Avella MA, Olivotto I, Silvi S, Place AR, Carnevali O: Effect of dietary probiotics on clownfish: a molecular approach to define how lactic acid bacteria modulate development in a marine fish. Am J Physiol Regul Integr Comp Physiol 2010;298:359-371.1992335410.1152/ajpregu.00300.2009 – reference: Takle H, Andersen O: Caspases and apoptosis in fish. J Fish Biol 2007;71:326-349.10.1111/j.1095-8649.2007.01665.x – reference: Jones CM, Smith JC: Inductive Signals: Revolving vertebrates. Curr Biol 1995;5:574-576.755215810.1016/S0960-9822(95)00112-6 – reference: Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, Corazzari M, Fuoco C, Ucar A, Schwartz P, Gruss P, Piacentini M, Chowdhury K, Cecconi F: Ambra1 regulates autophagy and development of the nervous system. Nature 2007;447:1121-1127.1758950410.1038/nature05925 – reference: Lee E, Koo Y, Ng A, Wei Y, Luby-Phelps K, Juraszek A, Xavier RJ, Cleaver O, Levine B and Amatruda JF: Autophagy is essential for cardiac morphogenesis during vertebrate development. Autophagy 2014;10:572-587.2444142310.4161/auto.27649 – reference: Nishida H: Specification of embryonic axis and mosaic development in ascidians. Dev Dyn 2005;233:1177-1193.1597369210.1002/dvdy.20469 – reference: Piccolo S, Sasai Y, Lu B, De Robertis EM: Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 1996;86:589-598.875221310.1016/S0092-8674(00)80132-4 – reference: Sasai Y, Lu B, Steinbeisser H, Geissert D, Gont LK, De Robertis EM: Xenopus chordin: A novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 1994;79:779-790.800111710.1016/0092-8674(94)90068-X – reference: Schulte-Merker S, Hammerschmidt M, Beuchle D, Cho KW, De Robertis EM, Nusslein-Volhard C: Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos. Development 1994;120:843-852.7600961 – reference: Gioacchini G, Giorgini E, Merrifield DL, Hardiman G, Borini A, Vaccari L, Carnevali O: Probiotics Can Induce Follicle Maturational Competence: The Danio rerio Case. Biol Reprod 2012;86:1-11.2208891910.1095/biolreprod.111.094243 – reference: Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, Yuan J: Human ICE/CED3 protease nomenclature. Cell 1996;87:171.886190010.1016/S0092-8674(00)81334-3 – reference: Tadros W, Lipshitz HD: Setting the stage for development: mRNA translation and stability during oocyte maturation and egg activation in Drosophila. Dev Dyn 2005;232:593-608.1570415010.1002/dvdy.20297 – reference: Watabe T, Kim S, Candia A, Rothbächer U, Hashimoto C, Inoue K, Cho KW: Molecular mechanisms of Spemann's organizer formation: conserved growth factor synergy between Xenopus and mouse. Genes Dev 1995;9:3038-3050.854315010.1101/gad.9.24.3038 – reference: Picchietti S, Mazzini M, Taddei AR, Renna R, Fausto AM, Mulero V, Carnevali O, Cresci A, Abelli L: Effects of administration of probiotic strains on GALT of larval gilthead seabream: Immunohistochemical and ultrastructural studies. Fish Shellfish Immunol 2007;22:57-67.1673045810.1016/j.fsi.2006.03.009 – reference: Carnevali O, De Vivo L, Sulpizio R, Gioacchini G, Olivotto I, Silvi S, Cresci A: Well-fare and growth improvement by probiotics in European sea bass juveniles (Dicentrarchus labrax, L.). Aquaculture 2006;258:430-433.10.1016/j.aquaculture.2006.04.025 – reference: Gioacchini G, Dalla Valle L, Benato F, Fimia GM, Nardacci R, Ciccosanti F, Piacentini M, Borini A, Carnevali O: Interplay between autophagy and apoptosis in the development of Danio rerio follicles and the effects of a probiotic. Reprod Fertil Dev 2013;25:1115-1125.2319528110.1071/RD12187 – reference: Cecconi F, Di Bartolomeo S, Nardacci R, Fuoco C, Corazzari M, Giunta L, Romagnoli A, Stoykova A, Chowdhury K, Fimia GM, Piacentini M: A novel role for autophagy in neurodevelopment. Autophagy 2007;3:506-508.1762279610.4161/auto.4616 – reference: Meier P, Finch A, Evan G: Apoptosis in development. Nature 2000;407:796-801.1104873110.1038/35037734 – reference: Wang J, Lenardo MJ: Role of caspases in apoptosis, development and citokyne maturation revealed by homozygous gene deficiencies. J Cell Sci 2000;113:753-757.10671365 – reference: Johnston DS, Nüsslein-Volhard C: The origin of pattern and polarity in the Drosophila embryo. Cell 1992;68:201-219.173349910.1016/0092-8674(92)90466-P – reference: Castex M, Chim L, Pham D, Lemaire P, Wabete N, Nicolas JL, Mariojouls C: Probiotic P. acidilactici application in shrimp Litopenaeus stylirostris culture subject to vibriosis in New Caledonia. Aquaculture 2008;275:182-193.10.1016/j.aquaculture.2008.01.011 – reference: Gatesoupe FJ: Bacillus sp. spores as food additive for the rotifer Brachionus plicatilis: improvement of their bacterial environment and their dietary value for larval turbot, Scophthalmus maximus L; in Kaushik SJ, Luquet P (eds): Fish Nutrition in Practice. Paris, Les Colloques, 1993, vol 61, pp 561-568. – reference: Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K, Schier AF: Zebrafish MiR-430 promotes deadenylation and clearance of maternal RNAs. Science 2006;312:75-79.1648445410.1126/science.1122689 – reference: Benato F, Skobo T, Gioacchini G, Moro I, Ciccosanti F, Piacentini M, Fimia GM, Carnevali O, Dalla Valle L: Ambra1 knockdown in zebrafish leads to incomplete development due to severe defects in organogenesis. Autophagy 2013;9:1-20.2334805410.4161/auto.23278 – reference: Thisse C, Thisse B: High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc 2008;3:59-69.1819302210.1038/nprot.2007.514 – reference: Verschuere L, Rombaut G, Sorgeloos P, Verstraete W: Probiotic bacteria as biological control agents in aquaculture. Microbiol Mol Biol Rev 2000;64:655-671.1110481310.1128/MMBR.64.4.655-671.2000 – reference: Abraham, MC, Shaham S: Death without caspases, caspases without death. Trends Cell Biol 2004;14:184-193.1506663610.1016/j.tcb.2004.03.002 – reference: Suzer C, Coban D, Kamaci HO, Saka S, Firat K, Otgucuoglu O, Kucuksari H: Lactobacillus spp. bacteria as probiotics in gilthead sea bream (Sparus aurata, L.) larvae: effects on growth performance and digestive enzyme activities. Aquaculture 2008;280:140-145.10.1016/j.aquaculture.2008.04.020 – reference: He C, Bartholomew CR, Zhou W and Klionsky DJ: Assaying autophagic activity in transgenic GFP-Lc3 and GFP-Gabarap zebrafish embryos. Autophagy 2009;5:520-526.1922146710.4161/auto.5.4.7768 – reference: Bachiller D, Klingensmith J, Kemp C, Belo JA, Anderson RM, May SR, De Robertis EM: The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature 2000;403:658-661.1068820210.1038/35001072 – reference: Kratz E, Eimon PM, Mukhyala K, Stern H, Zha J, Strasser A, Hart R, and Ashkenazi A: Functional characterization of the Bcl-2 gene family in the zebrafish. Cell Death Differ 2006;13:1631-1640.1688864610.1038/sj.cdd.4402016 – reference: Oppenheim RW: Cell death during development of the nervous system. Annu Rev Neurosci 1991;14:453-501.203157710.1146/annurev.ne.14.030191.002321 – reference: Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF: Stages of embryonic development of the zebrafish. Dev Dyn 1995;203:253-310.858942710.1002/aja.1002030302 – reference: Rollo A, Sulpizio R, Nardi M, Silvi S, Orpianesi C, Caggiano M, Cresci A, Carnevali O: Live microbial feed supplement in aquaculture for improvement of stress tolerance. Fish Physiol Biochem 2006;32:167-177.10.1007/s10695-006-0009-2 – reference: Arama E, Agapite J, Steller H: Caspase Activity and a Specific Cytochrome C Are Required for Sperm Differentiation in Drosophila. Dev Cell 2003;4:687-697.1273780410.1016/S1534-5807(03)00120-5 – reference: Ringo E, Gatesoupe FJ: Lactic acid bacteria in fish: a review. Aquaculture 1998;160:177-203.10.1016/S0044-8486(97)00299-8 – reference: Maradonna F, Gioacchini G, Falcinelli S, Bertotto D, Radaelli G, Olivotto I, Carnevali O: Probiotic Supplementation Promotes Calcification in Danio rerio Larvae: A Molecular Study. PloS One DOI: 10.1371/journal.pone.0083155.2435825910.1371/journal.pone.0083155 – reference: Lamari F, Castex M, Larcher T, Ledevin M, Mazurais D, Bakhrouf A, Gatesoupe FJ: Comparison of the effects of the dietary addition of two lactic acid bacteria on the development and conformation of sea bass larvae, Dicentrarchus labrax, and the influence on associated microbiota. Aquaculture 2013;376:137-145.10.1016/j.aquaculture.2012.11.016 – reference: Kane DA, Kimmel CB: The zebrafish midblastula transition. Development 1993;119:447-456.8287796 – reference: Lombardo F, Gioacchini G, Carnevali O: Probiotic-based Nutritional Effects on Killifish reproduction. Fish Aquacult 2011;J FAJ-33. – reference: Thornberry NA, Lazebnik Y: Caspases: enemies within. Science 1998;281:1312-1316.972109110.1126/science.281.5381.1312 – reference: Kemphues KJ, Strome S: Fertilization and Establishment of Polarity in the Embryo; in Riddle DL, Blumenthal T, Meyer BJ, et al., (eds): C. elegans II. Cold Spring Harbor Monograph Archive, 1997.21413241 – reference: Fimia GM, Di Bartolomeo S, Piacentini M, Cecconi F: Unleasing the AMBRA1-Beclin complex from dynein chains. Autophagy 2011;7:115-117.2107941510.4161/auto.7.1.14071 – reference: Hogan BL: Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev 1996;10:1580-1594.868229010.1101/gad.10.13.1580 – reference: Di Bartolomeo S, Corazzari M, Nazio F, Oliverio S, Lisi G, Antonioli M, Pagliarini V, Matteoni S, Fuoco C, Giunta L, D'Amelio M, Nardacci R, Romagnoli A, Piacentini M, Cecconi F, Fimia GM: The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J Cell Biol 2010;191:155-168.2092113910.1083/jcb.201002100 – reference: Heasman J: Patterning the Xenopus blastula. Development 1997;124:4179-4191.9334267 – reference: Vendrell D, Luis BJ, De Blas I, Ruiz-Zarzuela I: Protection of rainbow trout (Oncorhynchus mykiss) from lactococcosis by probiotic bacteria. Comp Immunol Microbiol Infect Dis 2008;31:337-345.1753247010.1016/j.cimid.2007.04.002 – reference: Balcázar JL, De Blas I, Ruiz-Zarzuela I, Vendrell D, Calvo AC, Márquez I, Gironés O, Muzquiz, JL: Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta). Br J Nutr 2007;97:522-527.1731371410.1017/S0007114507432986 – reference: Merrifield DL, Dimitroglou A, Bradley G, Baker RTM, Davies SJ: Probiotic application for rainbow trout (Onchorynchus mykiss Walbum) I. Effects on growth performance, feed utilization, intestinal microbiota, and related health criteria. Aquac Nutr 2010;16:504-510.10.1111/j.1365-2095.2009.00689.x – reference: Pérez-Sánchez T, Balcázar JL, Merrifield DL, Carnevali O, Gioacchini G, de Blas I, Ruiz-Zarzuela I: Expression of immune-related genes in rainbow trout (Oncorhynchus mykiss) induced by probiotic bacteria during Lactococcus garvieae infection. Fish Shellfish Immunol 2011;31:196-201.2162097410.1016/j.fsi.2011.05.005 – reference: Fuller R: History and development of probiotics; in Fuller R (eds): Probiotics: The Scientific Basis. London, Chapman and Hall, pp 1-8.10.1007/978-94-011-2364-8_1 – reference: McCabe LR, Irwin R, Schaefer L, Britton RA: Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. J Cell Physiol 2013;228:1793-1798.2338986010.1002/jcp.24340 – reference: Stachel SE, Grunwald DJ, Myers PZ: Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish. Development 1993;117:1261-1274.8104775 |
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SubjectTerms | Adaptor Proteins, Signal Transducing - metabolism Ambra1 Animals Apoptosis Apoptosis Regulatory Proteins - metabolism Autophagy Bax bcl-2-Associated X Protein - metabolism Bcl2 Beclin-1 Beclin1 Caspase 3 - metabolism Caspase3 Chordin Dorsalization Embryo, Nonmammalian - drug effects Embryo, Nonmammalian - metabolism Embryo, Nonmammalian - microbiology Embryonic Development - drug effects Female Gene Expression Regulation Goosecoid Lactobacillus rhamnosus - physiology Lc3 Male Microtubule-Associated Proteins - metabolism Original Paper Probiotics Probiotics - pharmacology Proto-Oncogene Proteins c-bcl-2 - metabolism RNA, Messenger - metabolism Zebrafish - growth & development Zebrafish - microbiology Zebrafish Proteins - genetics Zebrafish Proteins - metabolism |
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Title | Beneficial Bacteria Affect Danio rerio Development by the Modulation of Maternal Factors Involved in Autophagic, Apoptotic and Dorsalizing Processes |
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