A distinct innate lymphoid cell population regulates tumor-associated T cells
A previously uncharacterized population of innate lymphoid cells (ILCs) in the tumor microenvironment limits T cell expansion and cytokine production, and associates with early recurrence in patients with cancer. Depletion of this regulatory immunosuppressive cell population overcomes this effect, s...
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| Published in | Nature medicine Vol. 23; no. 3; pp. 368 - 375 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.03.2017
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1078-8956 1546-170X 1546-170X |
| DOI | 10.1038/nm.4278 |
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| Abstract | A previously uncharacterized population of innate lymphoid cells (ILCs) in the tumor microenvironment limits T cell expansion and cytokine production, and associates with early recurrence in patients with cancer. Depletion of this regulatory immunosuppressive cell population overcomes this effect, suggesting important implications for cancer immunotherapy.
Antitumor T cells are subject to multiple mechanisms of negative regulation
1
,
2
,
3
. Recent findings that innate lymphoid cells (ILCs) regulate adaptive T cell responses
4
,
5
,
6
led us to examine the regulatory potential of ILCs in the context of cancer. We identified a unique ILC population that inhibits tumor-infiltrating lymphocytes (TILs) from high-grade serous tumors, defined their suppressive capacity
in vitro
, and performed a comprehensive analysis of their phenotype. Notably, the presence of this CD56
+
CD3
−
population in TIL cultures was associated with reduced T cell numbers, and further functional studies demonstrated that this population suppressed TIL expansion and altered TIL cytokine production. Transcriptome analysis and phenotypic characterization determined that regulatory CD56
+
CD3
−
cells exhibit low cytotoxic activity, produce IL-22, and have an expression profile that overlaps with those of natural killer (NK) cells and other ILCs. NKp46 was highly expressed by these cells, and addition of anti-NKp46 antibodies to TIL cultures abrogated the ability of these regulatory ILCs to suppress T cell expansion. Notably, the presence of these regulatory ILCs in TIL cultures corresponded with a striking reduction in the time to disease recurrence. These studies demonstrate that a previously uncharacterized ILC population regulates the activity and expansion of tumor-associated T cells. |
|---|---|
| AbstractList | Antitumor T cells are subject to multiple mechanisms of negative regulation. Recent findings that innate lymphoid cells (ILCs) regulate adaptive T cell responses led us to examine the regulatory potential of ILCs in the context of cancer. We identified a unique ILC population that inhibits tumor-infiltrating lymphocytes (TILs) from high-grade serous tumors, defined their suppressive capacity in vitro, and performed a comprehensive analysis of their phenotype. Notably, the presence of this CD56+CD3- population in TIL cultures was associated with reduced T cell numbers, and further functional studies demonstrated that this population suppressed TIL expansion and altered TIL cytokine production. Transcriptome analysis and phenotypic characterization determined that regulatory CD56+CD3- cells exhibit low cytotoxic activity, produce IL-22, and have an expression profile that overlaps with those of natural killer (NK) cells and other ILCs. NKp46 was highly expressed by these cells, and addition of anti-NKp46 antibodies to TIL cultures abrogated the ability of these regulatory ILCs to suppress T cell expansion. Notably, the presence of these regulatory ILCs in TIL cultures corresponded with a striking reduction in the time to disease recurrence. These studies demonstrate that a previously uncharacterized ILC population regulates the activity and expansion of tumor-associated T cells.Antitumor T cells are subject to multiple mechanisms of negative regulation. Recent findings that innate lymphoid cells (ILCs) regulate adaptive T cell responses led us to examine the regulatory potential of ILCs in the context of cancer. We identified a unique ILC population that inhibits tumor-infiltrating lymphocytes (TILs) from high-grade serous tumors, defined their suppressive capacity in vitro, and performed a comprehensive analysis of their phenotype. Notably, the presence of this CD56+CD3- population in TIL cultures was associated with reduced T cell numbers, and further functional studies demonstrated that this population suppressed TIL expansion and altered TIL cytokine production. Transcriptome analysis and phenotypic characterization determined that regulatory CD56+CD3- cells exhibit low cytotoxic activity, produce IL-22, and have an expression profile that overlaps with those of natural killer (NK) cells and other ILCs. NKp46 was highly expressed by these cells, and addition of anti-NKp46 antibodies to TIL cultures abrogated the ability of these regulatory ILCs to suppress T cell expansion. Notably, the presence of these regulatory ILCs in TIL cultures corresponded with a striking reduction in the time to disease recurrence. These studies demonstrate that a previously uncharacterized ILC population regulates the activity and expansion of tumor-associated T cells. Antitumor T cells are subject to multiple mechanisms of negative regulation1–3. Recent findings that innate lymphoid cells (ILCs) regulate adaptive T cell responses4–6 led us to examine the regulatory potential of ILCs in the context of cancer. We identified a unique ILC population that inhibits tumor-infiltrating lymphocytes (TILs) from high-grade serous tumors, defined their suppressive capacity in vitro, and performed a comprehensive analysis of their phenotype. Notably, the presence of this CD56+CD3− population in TIL cultures was associated with reduced T cell numbers, and further functional studies demonstrated that this population suppressed TIL expansion and altered TIL cytokine production. Transcriptome analysis and phenotypic characterization determined that regulatory CD56+CD3− cells exhibit low cytotoxic activity, produce IL-22, and have an expression profile that overlaps with those of natural killer (NK) cells and other ILCs. NKp46 was highly expressed by these cells, and addition of anti-NKp46 antibodies to TIL cultures abrogated the ability of these regulatory ILCs to suppress T cell expansion. Notably, the presence of these regulatory ILCs in TIL cultures corresponded with a striking reduction in the time to disease recurrence. These studies demonstrate that a previously uncharacterized ILC population regulates the activity and expansion of tumor-associated T cells. Antitumor T cells are subject to multiple mechanisms of negative regulation. Recent findings that innate lymphoid cells (ILCs) regulate adaptive T cell responses led us to examine the regulatory potential of ILCs in the context of cancer. We identified a unique ILC population that inhibits tumor-infiltrating lymphocytes (TILs) from high-grade serous tumors, defined their suppressive capacity in vitro, and performed a comprehensive analysis of their phenotype. Notably, the presence of this CD56 super(+)CD3 super(-) population in TIL cultures was associated with reduced T cell numbers, and further functional studies demonstrated that this population suppressed TIL expansion and altered TIL cytokine production. Transcriptome analysis and phenotypic characterization determined that regulatory CD56 super(+)CD3 super(-) cells exhibit low cytotoxic activity, produce IL-22, and have an expression profile that overlaps with those of natural killer (NK) cells and other ILCs. NKp46 was highly expressed by these cells, and addition of anti-NKp46 antibodies to TIL cultures abrogated the ability of these regulatory ILCs to suppress T cell expansion. Notably, the presence of these regulatory ILCs in TIL cultures corresponded with a striking reduction in the time to disease recurrence. These studies demonstrate that a previously uncharacterized ILC population regulates the activity and expansion of tumor-associated T cells. A previously uncharacterized population of innate lymphoid cells (ILCs) in the tumor microenvironment limits T cell expansion and cytokine production, and associates with early recurrence in patients with cancer. Depletion of this regulatory immunosuppressive cell population overcomes this effect, suggesting important implications for cancer immunotherapy. Antitumor T cells are subject to multiple mechanisms of negative regulation 1 , 2 , 3 . Recent findings that innate lymphoid cells (ILCs) regulate adaptive T cell responses 4 , 5 , 6 led us to examine the regulatory potential of ILCs in the context of cancer. We identified a unique ILC population that inhibits tumor-infiltrating lymphocytes (TILs) from high-grade serous tumors, defined their suppressive capacity in vitro , and performed a comprehensive analysis of their phenotype. Notably, the presence of this CD56 + CD3 − population in TIL cultures was associated with reduced T cell numbers, and further functional studies demonstrated that this population suppressed TIL expansion and altered TIL cytokine production. Transcriptome analysis and phenotypic characterization determined that regulatory CD56 + CD3 − cells exhibit low cytotoxic activity, produce IL-22, and have an expression profile that overlaps with those of natural killer (NK) cells and other ILCs. NKp46 was highly expressed by these cells, and addition of anti-NKp46 antibodies to TIL cultures abrogated the ability of these regulatory ILCs to suppress T cell expansion. Notably, the presence of these regulatory ILCs in TIL cultures corresponded with a striking reduction in the time to disease recurrence. These studies demonstrate that a previously uncharacterized ILC population regulates the activity and expansion of tumor-associated T cells. Antitumor T cells are subject to multiple mechanisms of negative regulation. Recent findings that innate lymphoid cells (ILCs) regulate adaptive T cell responses led us to examine the regulatory potential of ILCs in the context of cancer. We identified a unique ILC population that inhibits tumor-infiltrating lymphocytes (TILs) from high-grade serous tumors, defined their suppressive capacity in vitro, and performed a comprehensive analysis of their phenotype. Notably, the presence of this CD56+ CD3- population in TIL cultures was associated with reduced T cell numbers, and further functional studies demonstrated that this population suppressed TIL expansion and altered TIL cytokine production. Transcriptome analysis and phenotypic characterization determined that regulatory CD56+ CD3- cells exhibit low cytotoxic activity, produce IL-22, and have an expression profile that overlaps with those of natural killer (NK) cells and other ILCs. NKp46 was highly expressed by these cells, and addition of anti-NKp46 antibodies to TIL cultures abrogated the ability of these regulatory ILCs to suppress T cell expansion. Notably, the presence of these regulatory ILCs in TIL cultures corresponded with a striking reduction in the time to disease recurrence. These studies demonstrate that a previously uncharacterized ILC population regulates the activity and expansion of tumor-associated T cells. Antitumor T cells are subject to multiple mechanisms of negative regulation. Recent findings that innate lymphoid cells (ILCs) regulate adaptive T cell responses led us to examine the regulatory potential of ILCs in the context of cancer. We identified a unique ILC population that inhibits tumor-infiltrating lymphocytes (TILs) from high-grade serous tumors, defined their suppressive capacity in vitro, and performed a comprehensive analysis of their phenotype. Notably, the presence of this CD56 CD3 population in TIL cultures was associated with reduced T cell numbers, and further functional studies demonstrated that this population suppressed TIL expansion and altered TIL cytokine production. Transcriptome analysis and phenotypic characterization determined that regulatory CD56 CD3 cells exhibit low cytotoxic activity, produce IL-22, and have an expression profile that overlaps with those of natural killer (NK) cells and other ILCs. NKp46 was highly expressed by these cells, and addition of anti-NKp46 antibodies to TIL cultures abrogated the ability of these regulatory ILCs to suppress T cell expansion. Notably, the presence of these regulatory ILCs in TIL cultures corresponded with a striking reduction in the time to disease recurrence. These studies demonstrate that a previously uncharacterized ILC population regulates the activity and expansion of tumor-associated T cells. |
| Audience | Academic |
| Author | Pugh, Trevor J Bernardini, Marcus Q Berman, Hal K Yang, S Y Cindy Yen, Pei Hua Yam, Jennifer Y Lopez-Verges, Sandra Nie, Jessica Lang, Philipp A Johnson, Dylan J Pniak, Michael Sowamber, Ramlogan Martin, Bernard Clarke, Blaise A Nguyen, Linh T Milea, Anca Katz, Sarah Rachel Lanier, Lewis L Crome, Sarah Q Shaw, Patricia A Ohashi, Pamela S |
| AuthorAffiliation | 4 Departments of Medical Biophysics and Immunology, University of Toronto, Toronto, Ontario, Canada 5 Division of Gynecologic Oncology, University Health Network, Toronto, Ontario, Canada 3 Gorgas Memorial Institute of Health Studies, Panama City, Panama 6 Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada 2 Department of Microbiology and Immunology and the Parker Institute for Cancer Immunotherapy, University of California San Francisco, San Francisco, California, USA 7 Department of Molecular Medicine II, Medical Faculty, Heinrich Heine University, Düsseldorf, Germany 1 Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario, Canada |
| AuthorAffiliation_xml | – name: 1 Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario, Canada – name: 3 Gorgas Memorial Institute of Health Studies, Panama City, Panama – name: 5 Division of Gynecologic Oncology, University Health Network, Toronto, Ontario, Canada – name: 7 Department of Molecular Medicine II, Medical Faculty, Heinrich Heine University, Düsseldorf, Germany – name: 6 Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada – name: 2 Department of Microbiology and Immunology and the Parker Institute for Cancer Immunotherapy, University of California San Francisco, San Francisco, California, USA – name: 4 Departments of Medical Biophysics and Immunology, University of Toronto, Toronto, Ontario, Canada |
| Author_xml | – sequence: 1 givenname: Sarah Q surname: Crome fullname: Crome, Sarah Q organization: Princess Margaret Cancer Centre, University Health Network – sequence: 2 givenname: Linh T surname: Nguyen fullname: Nguyen, Linh T organization: Princess Margaret Cancer Centre, University Health Network – sequence: 3 givenname: Sandra surname: Lopez-Verges fullname: Lopez-Verges, Sandra organization: Department of Microbiology and Immunology and the Parker Institute for Cancer Immunotherapy, University of California San Francisco, Gorgas Memorial Institute of Health Studies – sequence: 4 givenname: S Y Cindy surname: Yang fullname: Yang, S Y Cindy organization: Princess Margaret Cancer Centre, University Health Network, Departments of Medical Biophysics and Immunology, University of Toronto – sequence: 5 givenname: Bernard surname: Martin fullname: Martin, Bernard organization: Princess Margaret Cancer Centre, University Health Network – sequence: 6 givenname: Jennifer Y surname: Yam fullname: Yam, Jennifer Y organization: Princess Margaret Cancer Centre, University Health Network – sequence: 7 givenname: Dylan J surname: Johnson fullname: Johnson, Dylan J organization: Princess Margaret Cancer Centre, University Health Network, Departments of Medical Biophysics and Immunology, University of Toronto – sequence: 8 givenname: Jessica surname: Nie fullname: Nie, Jessica organization: Princess Margaret Cancer Centre, University Health Network – sequence: 9 givenname: Michael surname: Pniak fullname: Pniak, Michael organization: Princess Margaret Cancer Centre, University Health Network – sequence: 10 givenname: Pei Hua surname: Yen fullname: Yen, Pei Hua organization: Princess Margaret Cancer Centre, University Health Network – sequence: 11 givenname: Anca surname: Milea fullname: Milea, Anca organization: Princess Margaret Cancer Centre, University Health Network – sequence: 12 givenname: Ramlogan surname: Sowamber fullname: Sowamber, Ramlogan organization: Princess Margaret Cancer Centre, University Health Network – sequence: 13 givenname: Sarah Rachel surname: Katz fullname: Katz, Sarah Rachel organization: Division of Gynecologic Oncology, University Health Network – sequence: 14 givenname: Marcus Q surname: Bernardini fullname: Bernardini, Marcus Q organization: Division of Gynecologic Oncology, University Health Network – sequence: 15 givenname: Blaise A surname: Clarke fullname: Clarke, Blaise A organization: Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 16 givenname: Patricia A surname: Shaw fullname: Shaw, Patricia A organization: Princess Margaret Cancer Centre, University Health Network, Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 17 givenname: Philipp A surname: Lang fullname: Lang, Philipp A organization: Princess Margaret Cancer Centre, University Health Network, Department of Molecular Medicine II, Medical Faculty, Heinrich Heine University – sequence: 18 givenname: Hal K surname: Berman fullname: Berman, Hal K organization: Princess Margaret Cancer Centre, University Health Network, Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 19 givenname: Trevor J orcidid: 0000-0002-8073-5888 surname: Pugh fullname: Pugh, Trevor J organization: Departments of Medical Biophysics and Immunology, University of Toronto – sequence: 20 givenname: Lewis L orcidid: 0000-0003-1308-3952 surname: Lanier fullname: Lanier, Lewis L organization: Department of Microbiology and Immunology and the Parker Institute for Cancer Immunotherapy, University of California San Francisco – sequence: 21 givenname: Pamela S surname: Ohashi fullname: Ohashi, Pamela S email: pohashi@uhnresearch.ca organization: Princess Margaret Cancer Centre, University Health Network, Departments of Medical Biophysics and Immunology, University of Toronto |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28165478$$D View this record in MEDLINE/PubMed |
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| Cites_doi | 10.1084/jem.20080718 10.1002/1521-4141(2001010)31:10<3048::AID-IMMU3048>3.0.CO;2-1 10.1038/nri3365 10.1073/pnas.1118834109 10.1084/jem.20010934 10.1038/nature14189 10.1172/JCI41264 10.1053/j.gastro.2011.06.069 10.4049/jimmunol.181.9.6394 10.1038/nrclinonc.2015.209 10.1084/jem.20121172 10.1038/ni.2534 10.1016/j.it.2015.07.004 10.4049/jimmunol.0902598 10.1016/j.it.2013.03.002 10.1038/ni.3482 10.1371/journal.pone.0013940 10.1002/eji.200323986 10.1186/ar1453 10.1084/jem.177.1.155 10.1038/nm1296 10.1371/journal.pone.0003377 10.1186/1471-2105-12-323 10.1038/nri3726 10.1084/jem.20082387 10.1038/ni909 10.1016/j.cell.2016.04.014 10.1038/nature12240 10.4049/jimmunol.1004122 10.4049/jimmunol.178.4.2141 10.1038/ni904 10.4049/jimmunol.180.3.1729 10.1182/blood-2013-11-536888 10.1038/nature10624 10.1126/science.1079490 10.1126/science.1215621 10.1002/1521-4141(200106)31:6<1656::AID-IMMU1656>3.0.CO;2-V 10.1093/bioinformatics/bts635 10.1093/bioinformatics/bts196 10.1158/1078-0432.CCR-08-0196 10.1016/j.immuni.2016.04.023 10.1016/j.immuni.2016.05.002 10.1128/JVI.00717-08 10.1186/s13059-014-0550-8 |
| ContentType | Journal Article |
| Copyright | Springer Nature America, Inc. 2017 COPYRIGHT 2017 Nature Publishing Group Copyright Nature Publishing Group Mar 2017 |
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| DOI | 10.1038/nm.4278 |
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| References | Love, Huber, Anders (CR45) 2014; 15 Peppa (CR22) 2013; 210 Smyth, Ngiow, Ribas, Teng (CR1) 2016; 13 Simhadri (CR33) 2008; 3 Beilke, Kuhl, Van Kaer, Gill (CR13) 2005; 11 Chiesa (CR39) 2003; 33 Waggoner, Cornberg, Selin, Welsh (CR19) 2011; 481 Tothill (CR34) 2008; 14 Gasteiger, Rudensky (CR5) 2014; 14 Rydyznski, Waggoner (CR37) 2015; 36 Dobin (CR42) 2013; 29 Schildberg, Klein, Freeman, Sharpe (CR3) 2016; 44 Hepworth (CR25) 2013; 498 Roy (CR32) 2008; 180 Soderquest (CR18) 2011; 186 Takeda, Dennert (CR9) 1993; 177 Lang (CR20) 2012; 109 Khattri, Cox, Yasayko, Ramsdell (CR30) 2003; 4 Piccioli, Sbrana, Melandri, Valiante (CR40) 2002; 195 Artis, Spits (CR6) 2015; 517 Fontenot, Gavin, Rudensky (CR29) 2003; 4 Su (CR15) 2001; 31 Nguyen (CR26) 2010; 5 Callahan, Postow, Wolchok (CR2) 2016; 44 Spits (CR7) 2013; 13 Noone (CR16) 2008; 82 Zhou, Wei, Tian (CR11) 2007; 178 Bernink (CR31) 2013; 14 Tai (CR12) 2008; 205 Rivas (CR14) 2010; 184 Che, Huston (CR38) 1994; 13 DeLuca (CR43) 2012; 28 Spits, Bernink, Lanier (CR8) 2016; 17 Ahlenstiel (CR23) 2011; 141 Koues (CR27) 2016; 165 Hori, Nomura, Sakaguchi (CR28) 2003; 299 Narni-Mancinelli (CR21) 2012; 335 Fodil-Cornu (CR36) 2008; 181 Lee, Kim, Fodil-Cornu, Vidal, Biron (CR35) 2009; 206 Crome, Lang, Lang, Ohashi (CR4) 2013; 34 Waggoner, Taniguchi, Mathew, Kumar, Welsh (CR17) 2010; 120 Li, Dewey (CR44) 2011; 12 Villanueva (CR10) 2005; 7 Munneke (CR24) 2014; 124 Spaggiari (CR41) 2001; 31 MK Callahan (BFnm4278_CR2) 2016; 44 MJ Smyth (BFnm4278_CR1) 2016; 13 S Roy (BFnm4278_CR32) 2008; 180 LT Nguyen (BFnm4278_CR26) 2010; 5 D Piccioli (BFnm4278_CR40) 2002; 195 H Spits (BFnm4278_CR7) 2013; 13 SQ Crome (BFnm4278_CR4) 2013; 34 D Artis (BFnm4278_CR6) 2015; 517 LH Tai (BFnm4278_CR12) 2008; 205 G Gasteiger (BFnm4278_CR5) 2014; 14 SN Waggoner (BFnm4278_CR19) 2011; 481 MR Hepworth (BFnm4278_CR25) 2013; 498 MI Love (BFnm4278_CR45) 2014; 15 H Spits (BFnm4278_CR8) 2016; 17 SN Waggoner (BFnm4278_CR17) 2010; 120 R Khattri (BFnm4278_CR30) 2003; 4 S Che (BFnm4278_CR38) 1994; 13 K Takeda (BFnm4278_CR9) 1993; 177 CE Rydyznski (BFnm4278_CR37) 2015; 36 S Hori (BFnm4278_CR28) 2003; 299 G Ahlenstiel (BFnm4278_CR23) 2011; 141 CM Noone (BFnm4278_CR16) 2008; 82 E Narni-Mancinelli (BFnm4278_CR21) 2012; 335 JN Beilke (BFnm4278_CR13) 2005; 11 A Dobin (BFnm4278_CR42) 2013; 29 MN Rivas (BFnm4278_CR14) 2010; 184 OI Koues (BFnm4278_CR27) 2016; 165 JM Munneke (BFnm4278_CR24) 2014; 124 PA Lang (BFnm4278_CR20) 2012; 109 HC Su (BFnm4278_CR15) 2001; 31 RW Tothill (BFnm4278_CR34) 2008; 14 D Peppa (BFnm4278_CR22) 2013; 210 MD Chiesa (BFnm4278_CR39) 2003; 33 B Li (BFnm4278_CR44) 2011; 12 JH Bernink (BFnm4278_CR31) 2013; 14 N Fodil-Cornu (BFnm4278_CR36) 2008; 181 J Villanueva (BFnm4278_CR10) 2005; 7 SH Lee (BFnm4278_CR35) 2009; 206 GM Spaggiari (BFnm4278_CR41) 2001; 31 DS DeLuca (BFnm4278_CR43) 2012; 28 R Zhou (BFnm4278_CR11) 2007; 178 FA Schildberg (BFnm4278_CR3) 2016; 44 JD Fontenot (BFnm4278_CR29) 2003; 4 VR Simhadri (BFnm4278_CR33) 2008; 3 K Soderquest (BFnm4278_CR18) 2011; 186 |
| References_xml | – volume: 205 start-page: 3187 year: 2008 end-page: 3199 ident: CR12 article-title: Positive regulation of plasmacytoid dendritic cell function via Ly49Q recognition of class I MHC publication-title: J. Exp. Med. doi: 10.1084/jem.20080718 – volume: 31 start-page: 3048 year: 2001 end-page: 3055 ident: CR15 article-title: NK cell functions restrain T cell responses during viral infections publication-title: Eur. J. Immunol. doi: 10.1002/1521-4141(2001010)31:10<3048::AID-IMMU3048>3.0.CO;2-1 – volume: 13 start-page: 145 year: 2013 end-page: 149 ident: CR7 article-title: Innate lymphoid cells—a proposal for uniform nomenclature publication-title: Nat. Rev. Immunol. doi: 10.1038/nri3365 – volume: 109 start-page: 1210 year: 2012 end-page: 1215 ident: CR20 article-title: Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8 T-cell immunity publication-title: Proc. Natl. Acad. Sci. USA doi: 10.1073/pnas.1118834109 – volume: 195 start-page: 335 year: 2002 end-page: 341 ident: CR40 article-title: Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells publication-title: J. Exp. Med. doi: 10.1084/jem.20010934 – volume: 517 start-page: 293 year: 2015 end-page: 301 ident: CR6 article-title: The biology of innate lymphoid cells publication-title: Nature doi: 10.1038/nature14189 – volume: 120 start-page: 1925 year: 2010 end-page: 1938 ident: CR17 article-title: Absence of mouse 2B4 promotes NK cell–mediated killing of activated CD8 T cells, leading to prolonged viral persistence and altered pathogenesis publication-title: J. Clin. Invest. doi: 10.1172/JCI41264 – volume: 141 start-page: 1231 year: 2011 end-page: 1239.e2 ident: CR23 article-title: Early changes in natural killer cell function indicate virologic response to interferon therapy for hepatitis C publication-title: Gastroenterology doi: 10.1053/j.gastro.2011.06.069 – volume: 181 start-page: 6394 year: 2008 end-page: 6405 ident: CR36 article-title: Ly49h-deficient C57BL/6 mice: a new mouse cytomegalovirus-susceptible model remains resistant to unrelated pathogens controlled by the NK gene complex publication-title: J. Immunol. doi: 10.4049/jimmunol.181.9.6394 – volume: 13 start-page: 143 year: 2016 end-page: 158 ident: CR1 article-title: Combination cancer immunotherapies tailored to the tumour microenvironment publication-title: Nat. Rev. Clin. Oncol. doi: 10.1038/nrclinonc.2015.209 – volume: 210 start-page: 99 year: 2013 end-page: 114 ident: CR22 article-title: Up-regulation of a death receptor renders antiviral T cells susceptible to NK cell–mediated deletion publication-title: J. Exp. Med. doi: 10.1084/jem.20121172 – volume: 14 start-page: 221 year: 2013 end-page: 229 ident: CR31 article-title: Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues publication-title: Nat. Immunol. doi: 10.1038/ni.2534 – volume: 36 start-page: 536 year: 2015 end-page: 546 ident: CR37 article-title: Boosting vaccine efficacy the natural (killer) way publication-title: Trends Immunol. doi: 10.1016/j.it.2015.07.004 – volume: 184 start-page: 6790 year: 2010 end-page: 6798 ident: CR14 article-title: NK cell regulation of CD4 T cell–mediated graft-versus-host disease publication-title: J. Immunol. doi: 10.4049/jimmunol.0902598 – volume: 34 start-page: 342 year: 2013 end-page: 349 ident: CR4 article-title: Natural killer cells regulate diverse T cell responses publication-title: Trends Immunol. doi: 10.1016/j.it.2013.03.002 – volume: 17 start-page: 758 year: 2016 end-page: 764 ident: CR8 article-title: NK cells and type 1 innate lymphoid cells: partners in host defense publication-title: Nat. Immunol. doi: 10.1038/ni.3482 – volume: 5 start-page: e13940 year: 2010 ident: CR26 article-title: Expansion and characterization of human melanoma tumor-infiltrating lymphocytes (TILs) publication-title: PLoS One doi: 10.1371/journal.pone.0013940 – volume: 33 start-page: 1657 year: 2003 end-page: 1666 ident: CR39 article-title: The natural killer cell–mediated killing of autologous dendritic cells is confined to a cell subset expressing CD94/NKG2A, but lacking inhibitory killer Ig-like receptors publication-title: Eur. J. Immunol. doi: 10.1002/eji.200323986 – volume: 7 start-page: R30 year: 2005 end-page: R37 ident: CR10 article-title: Natural killer cell dysfunction is a distinguishing feature of systemic onset juvenile rheumatoid arthritis and macrophage activation syndrome publication-title: Arthritis Res. Ther. doi: 10.1186/ar1453 – volume: 177 start-page: 155 year: 1993 end-page: 164 ident: CR9 article-title: The development of autoimmunity in C57BL/6 lpr mice correlates with the disappearance of natural killer type 1–positive cells: evidence for their suppressive action on bone marrow stem cell proliferation, B cell immunoglobulin secretion, and autoimmune symptoms publication-title: J. Exp. Med. doi: 10.1084/jem.177.1.155 – volume: 11 start-page: 1059 year: 2005 end-page: 1065 ident: CR13 article-title: NK cells promote islet allograft tolerance via a perforin-dependent mechanism publication-title: Nat. Med. doi: 10.1038/nm1296 – volume: 3 start-page: e3377 year: 2008 ident: CR33 article-title: Dendritic cells release HLA-B-associated transcript-3 positive exosomes to regulate natural killer function publication-title: PLoS One doi: 10.1371/journal.pone.0003377 – volume: 12 start-page: 323 year: 2011 ident: CR44 article-title: RSEM: accurate transcript quantification from RNA–Seq data with or without a reference genome publication-title: BMC Bioinformatics doi: 10.1186/1471-2105-12-323 – volume: 14 start-page: 631 year: 2014 end-page: 639 ident: CR5 article-title: Interactions between innate and adaptive lymphocytes publication-title: Nat. Rev. Immunol. doi: 10.1038/nri3726 – volume: 206 start-page: 2235 year: 2009 end-page: 2251 ident: CR35 article-title: Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection publication-title: J. Exp. Med. doi: 10.1084/jem.20082387 – volume: 4 start-page: 337 year: 2003 end-page: 342 ident: CR30 article-title: An essential role for Scurfin in CD4 CD25 T regulatory cells publication-title: Nat. Immunol. doi: 10.1038/ni909 – volume: 165 start-page: 1134 year: 2016 end-page: 1146 ident: CR27 article-title: Distinct gene regulatory pathways for human innate versus adaptive lymphoid cells publication-title: Cell doi: 10.1016/j.cell.2016.04.014 – volume: 498 start-page: 113 year: 2013 end-page: 117 ident: CR25 article-title: Innate lymphoid cells regulate CD4 T-cell responses to intestinal commensal bacteria publication-title: Nature doi: 10.1038/nature12240 – volume: 186 start-page: 3304 year: 2011 end-page: 3308 ident: CR18 article-title: Cutting edge: CD8 T cell priming in the absence of NK cells leads to enhanced memory responses publication-title: J. Immunol. doi: 10.4049/jimmunol.1004122 – volume: 178 start-page: 2141 year: 2007 end-page: 2147 ident: CR11 article-title: NK3-like NK cells are involved in protective effect of polyinosinic–polycytidylic acid on type 1 diabetes in nonobese diabetic mice publication-title: J. Immunol. doi: 10.4049/jimmunol.178.4.2141 – volume: 4 start-page: 330 year: 2003 end-page: 336 ident: CR29 article-title: Foxp3 programs the development and function of CD4 CD25 regulatory T cells publication-title: Nat. Immunol. doi: 10.1038/ni904 – volume: 180 start-page: 1729 year: 2008 end-page: 1736 ident: CR32 article-title: NK cells lyse T regulatory cells that expand in response to an intracellular pathogen publication-title: J. Immunol. doi: 10.4049/jimmunol.180.3.1729 – volume: 124 start-page: 812 year: 2014 end-page: 821 ident: CR24 article-title: Activated innate lymphoid cells are associated with a reduced susceptibility to graft-versus-host disease publication-title: Blood doi: 10.1182/blood-2013-11-536888 – volume: 13 start-page: 258 year: 1994 end-page: 269 ident: CR38 article-title: Natural killer cell suppression of IgM production publication-title: Nat. Immun. – volume: 481 start-page: 394 year: 2011 end-page: 398 ident: CR19 article-title: Natural killer cells act as rheostats modulating antiviral T cells publication-title: Nature doi: 10.1038/nature10624 – volume: 299 start-page: 1057 year: 2003 end-page: 1061 ident: CR28 article-title: Control of regulatory T cell development by the transcription factor Foxp3 publication-title: Science doi: 10.1126/science.1079490 – volume: 335 start-page: 344 year: 2012 end-page: 348 ident: CR21 article-title: Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses publication-title: Science doi: 10.1126/science.1215621 – volume: 31 start-page: 1656 year: 2001 end-page: 1665 ident: CR41 article-title: NK cell–mediated lysis of autologous antigen-presenting cells is triggered by the engagement of the phosphatidylinositol 3-kinase upon ligation of the natural cytotoxicity receptors NKp30 and NKp46 publication-title: Eur. J. Immunol. doi: 10.1002/1521-4141(200106)31:6<1656::AID-IMMU1656>3.0.CO;2-V – volume: 29 start-page: 15 year: 2013 end-page: 21 ident: CR42 article-title: STAR: ultrafast universal RNA–seq aligner publication-title: Bioinformatics doi: 10.1093/bioinformatics/bts635 – volume: 28 start-page: 1530 year: 2012 end-page: 1532 ident: CR43 article-title: RNA-SeQC: RNA–seq metrics for quality control and process optimization publication-title: Bioinformatics doi: 10.1093/bioinformatics/bts196 – volume: 14 start-page: 5198 year: 2008 end-page: 5208 ident: CR34 article-title: Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome publication-title: Clin. Cancer Res. doi: 10.1158/1078-0432.CCR-08-0196 – volume: 44 start-page: 1069 year: 2016 end-page: 1078 ident: CR2 article-title: Targeting T cell co-receptors for cancer therapy publication-title: Immunity doi: 10.1016/j.immuni.2016.04.023 – volume: 44 start-page: 955 year: 2016 end-page: 972 ident: CR3 article-title: Coinhibitory pathways in the B7–CD28 ligand–receptor family publication-title: Immunity doi: 10.1016/j.immuni.2016.05.002 – volume: 82 start-page: 9299 year: 2008 end-page: 9302 ident: CR16 article-title: Natural killer cells regulate T-cell proliferation during human parainfluenza virus type 3 infection publication-title: J. Virol. doi: 10.1128/JVI.00717-08 – volume: 15 start-page: 550 year: 2014 ident: CR45 article-title: Moderated estimation of fold change and dispersion for RNA–seq data with DESeq2 publication-title: Genome Biol. – volume: 14 start-page: 5198 year: 2008 ident: BFnm4278_CR34 publication-title: Clin. Cancer Res. doi: 10.1158/1078-0432.CCR-08-0196 – volume: 109 start-page: 1210 year: 2012 ident: BFnm4278_CR20 publication-title: Proc. Natl. Acad. Sci. USA doi: 10.1073/pnas.1118834109 – volume: 36 start-page: 536 year: 2015 ident: BFnm4278_CR37 publication-title: Trends Immunol. doi: 10.1016/j.it.2015.07.004 – volume: 186 start-page: 3304 year: 2011 ident: BFnm4278_CR18 publication-title: J. Immunol. doi: 10.4049/jimmunol.1004122 – volume: 13 start-page: 258 year: 1994 ident: BFnm4278_CR38 publication-title: Nat. Immun. – volume: 299 start-page: 1057 year: 2003 ident: BFnm4278_CR28 publication-title: Science doi: 10.1126/science.1079490 – volume: 82 start-page: 9299 year: 2008 ident: BFnm4278_CR16 publication-title: J. Virol. doi: 10.1128/JVI.00717-08 – volume: 206 start-page: 2235 year: 2009 ident: BFnm4278_CR35 publication-title: J. Exp. Med. doi: 10.1084/jem.20082387 – volume: 4 start-page: 330 year: 2003 ident: BFnm4278_CR29 publication-title: Nat. Immunol. doi: 10.1038/ni904 – volume: 3 start-page: e3377 year: 2008 ident: BFnm4278_CR33 publication-title: PLoS One doi: 10.1371/journal.pone.0003377 – volume: 17 start-page: 758 year: 2016 ident: BFnm4278_CR8 publication-title: Nat. Immunol. doi: 10.1038/ni.3482 – volume: 11 start-page: 1059 year: 2005 ident: BFnm4278_CR13 publication-title: Nat. Med. doi: 10.1038/nm1296 – volume: 34 start-page: 342 year: 2013 ident: BFnm4278_CR4 publication-title: Trends Immunol. doi: 10.1016/j.it.2013.03.002 – volume: 178 start-page: 2141 year: 2007 ident: BFnm4278_CR11 publication-title: J. Immunol. doi: 10.4049/jimmunol.178.4.2141 – volume: 15 start-page: 550 year: 2014 ident: BFnm4278_CR45 publication-title: Genome Biol. doi: 10.1186/s13059-014-0550-8 – volume: 165 start-page: 1134 year: 2016 ident: BFnm4278_CR27 publication-title: Cell doi: 10.1016/j.cell.2016.04.014 – volume: 195 start-page: 335 year: 2002 ident: BFnm4278_CR40 publication-title: J. Exp. Med. doi: 10.1084/jem.20010934 – volume: 498 start-page: 113 year: 2013 ident: BFnm4278_CR25 publication-title: Nature doi: 10.1038/nature12240 – volume: 13 start-page: 145 year: 2013 ident: BFnm4278_CR7 publication-title: Nat. Rev. Immunol. doi: 10.1038/nri3365 – volume: 205 start-page: 3187 year: 2008 ident: BFnm4278_CR12 publication-title: J. Exp. Med. doi: 10.1084/jem.20080718 – volume: 44 start-page: 1069 year: 2016 ident: BFnm4278_CR2 publication-title: Immunity doi: 10.1016/j.immuni.2016.04.023 – volume: 31 start-page: 3048 year: 2001 ident: BFnm4278_CR15 publication-title: Eur. J. Immunol. doi: 10.1002/1521-4141(2001010)31:10<3048::AID-IMMU3048>3.0.CO;2-1 – volume: 13 start-page: 143 year: 2016 ident: BFnm4278_CR1 publication-title: Nat. Rev. Clin. Oncol. doi: 10.1038/nrclinonc.2015.209 – volume: 7 start-page: R30 year: 2005 ident: BFnm4278_CR10 publication-title: Arthritis Res. Ther. doi: 10.1186/ar1453 – volume: 180 start-page: 1729 year: 2008 ident: BFnm4278_CR32 publication-title: J. Immunol. doi: 10.4049/jimmunol.180.3.1729 – volume: 29 start-page: 15 year: 2013 ident: BFnm4278_CR42 publication-title: Bioinformatics doi: 10.1093/bioinformatics/bts635 – volume: 28 start-page: 1530 year: 2012 ident: BFnm4278_CR43 publication-title: Bioinformatics doi: 10.1093/bioinformatics/bts196 – volume: 14 start-page: 631 year: 2014 ident: BFnm4278_CR5 publication-title: Nat. Rev. Immunol. doi: 10.1038/nri3726 – volume: 124 start-page: 812 year: 2014 ident: BFnm4278_CR24 publication-title: Blood doi: 10.1182/blood-2013-11-536888 – volume: 31 start-page: 1656 year: 2001 ident: BFnm4278_CR41 publication-title: Eur. J. Immunol. doi: 10.1002/1521-4141(200106)31:6<1656::AID-IMMU1656>3.0.CO;2-V – volume: 335 start-page: 344 year: 2012 ident: BFnm4278_CR21 publication-title: Science doi: 10.1126/science.1215621 – volume: 4 start-page: 337 year: 2003 ident: BFnm4278_CR30 publication-title: Nat. Immunol. doi: 10.1038/ni909 – volume: 120 start-page: 1925 year: 2010 ident: BFnm4278_CR17 publication-title: J. Clin. Invest. doi: 10.1172/JCI41264 – volume: 44 start-page: 955 year: 2016 ident: BFnm4278_CR3 publication-title: Immunity doi: 10.1016/j.immuni.2016.05.002 – volume: 14 start-page: 221 year: 2013 ident: BFnm4278_CR31 publication-title: Nat. Immunol. doi: 10.1038/ni.2534 – volume: 181 start-page: 6394 year: 2008 ident: BFnm4278_CR36 publication-title: J. Immunol. doi: 10.4049/jimmunol.181.9.6394 – volume: 177 start-page: 155 year: 1993 ident: BFnm4278_CR9 publication-title: J. Exp. Med. doi: 10.1084/jem.177.1.155 – volume: 481 start-page: 394 year: 2011 ident: BFnm4278_CR19 publication-title: Nature doi: 10.1038/nature10624 – volume: 141 start-page: 1231 year: 2011 ident: BFnm4278_CR23 publication-title: Gastroenterology doi: 10.1053/j.gastro.2011.06.069 – volume: 210 start-page: 99 year: 2013 ident: BFnm4278_CR22 publication-title: J. Exp. Med. doi: 10.1084/jem.20121172 – volume: 12 start-page: 323 year: 2011 ident: BFnm4278_CR44 publication-title: BMC Bioinformatics doi: 10.1186/1471-2105-12-323 – volume: 5 start-page: e13940 year: 2010 ident: BFnm4278_CR26 publication-title: PLoS One doi: 10.1371/journal.pone.0013940 – volume: 184 start-page: 6790 year: 2010 ident: BFnm4278_CR14 publication-title: J. Immunol. doi: 10.4049/jimmunol.0902598 – volume: 517 start-page: 293 year: 2015 ident: BFnm4278_CR6 publication-title: Nature doi: 10.1038/nature14189 – volume: 33 start-page: 1657 year: 2003 ident: BFnm4278_CR39 publication-title: Eur. J. Immunol. doi: 10.1002/eji.200323986 |
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| Snippet | A previously uncharacterized population of innate lymphoid cells (ILCs) in the tumor microenvironment limits T cell expansion and cytokine production, and... Antitumor T cells are subject to multiple mechanisms of negative regulation. Recent findings that innate lymphoid cells (ILCs) regulate adaptive T cell... Antitumor T cells are subject to multiple mechanisms of negative regulation1–3. Recent findings that innate lymphoid cells (ILCs) regulate adaptive T cell... |
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| Title | A distinct innate lymphoid cell population regulates tumor-associated T cells |
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