Expression of LLT1 and its receptor CD161 in lung cancer is associated with better clinical outcome

References

• Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: From immunosurveillance to tumor escape. Nat Immunol. 2002;3:991–8. doi:10.1038/ni1102-991. PMID:12407406.
   PubMed Web of Science ®Google Scholar
• Fridman WH, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: Impact on clinical outcome. Nat Rev Cancer. 2012;12:298–306. doi:10.1038/nrc3245. PMID:22419253.
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell. 2011;144:646–74. doi:10.1016/j.cell.2011.02.013. PMID:21376230.
   PubMed Web of Science ®Google Scholar
• Bindea G, Mlecnik B, Tosolini M, Kirilovsky A, Waldner M, Obenauf AC, Angell H, Fredriksen T, Lafontaine L, Berger A, et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity. 2013;39:782–95. doi:10.1016/j.immuni.2013.10.003. PMID:24138885.
   PubMed Web of Science ®Google Scholar
• Dieu-Nosjean M-C, Giraldo NA, Kaplon H, Germain C, Fridman WH, Sautès-Fridman C. Tertiary lymphoid structures, drivers of the anti-tumor responses in human cancers. Immunol Rev. 2016;271:260–75. doi:10.1111/imr.12405. PMID:27088920.
   PubMed Web of Science ®Google Scholar
• Chen L, Flies DB. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat Rev Immunol. 2013;13:227–42. doi:10.1038/nri3405. PMID:23470321.
   PubMed Web of Science ®Google Scholar
• Sharma P, Allison JP. Immune checkpoint targeting in cancer therapy: Toward combination strategies with curative potential. Cell. 2015;161:205–14. doi:10.1016/j.cell.2015.03.030. PMID:25860605.
   PubMed Web of Science ®Google Scholar
• Dempke WCM, Fenchel K, Uciechowski P, Dale SP. Second- and third-generation drugs for immuno-oncology treatment-The more the better? Eur J Cancer Oxf Engl 1990. 2017;74:55–72.
   PubMed Web of Science ®Google Scholar
• Fridman WH, Zitvogel L, Sautès-Fridman C, Kroemer G. The immune contexture in cancer prognosis and treatment. Nat Rev Clin Oncol. 2017;14(12):717–734. doi:10.1038/nrclinonc.2017.101. PMID:28741618.
   PubMed Web of Science ®Google Scholar
• Aldemir H, Prod'homme V, Dumaurier M-J, Retiere C, Poupon G, Cazareth J, Bihl F, Braud VM. Cutting edge: Lectin-like transcript 1 is a ligand for the CD161 receptor. J Immunol Baltim Md 1950. 2005;175:7791–5.
   Google Scholar
• Rosen DB, Bettadapura J, Alsharifi M, Mathew PA, Warren HS, Lanier LL. Cutting edge: Lectin-like transcript-1 is a ligand for the inhibitory human NKR-P1A receptor. J Immunol Baltim Md 1950. 2005;175:7796–9.
   Google Scholar
• Fergusson JR, Fleming VM, Klenerman P. CD161-expressing human T cells. Front Immunol. 2011;2:36. doi:10.3389/fimmu.2011.00036. PMID:22566826.
   PubMed Web of Science ®Google Scholar
• Germain C, Meier A, Jensen T, Knapnougel P, Poupon G, Lazzari A, Neisig A, Håkansson K, Dong T, Wagtmann N, et al. Induction of lectin-like transcript 1 (LLT1) protein cell surface expression by pathogens and interferon-γ contributes to modulate immune responses. J Biol Chem. 2011;286:37964–75. doi:10.1074/jbc.M111.285312. PMID:21930700.
   PubMed Web of Science ®Google Scholar
• Germain C, Bihl F, Zahn S, Poupon G, Dumaurier M-J, Rampanarivo HH, Padkjær SB, Spee P, Braud VM. Characterization of alternatively spliced transcript variants of CLEC2D gene. J Biol Chem. 2010;285:36207–15. doi:10.1074/jbc.M110.179622. PMID:20843815.
   PubMed Web of Science ®Google Scholar
• Germain C, Guillaudeux T, Galsgaard ED, Hervouet C, Tekaya N, Gallouet A-S, Fassy J, Bihl F, Poupon G, Lazzari A, et al. Lectin-like transcript 1 is a marker of germinal center-derived B-cell non-Hodgkin's lymphomas dampening natural killer cell functions. Oncoimmunology. 2015;4:e1026503. doi:10.1080/2162402X.2015.1026503. PMID:26405582.
   PubMed Web of Science ®Google Scholar
• Dieu-Nosjean M-C, Antoine M, Danel C, Heudes D, Wislez M, Poulot V, Rabbe N, Laurans L, Tartour E, de Chaisemartin L, et al. Long-term survival for patients with non–small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol. 2008;26:4410–7. doi:10.1200/JCO.2007.15.0284. PMID:18802153.
   PubMed Web of Science ®Google Scholar
• Germain C, Gnjatic S, Tamzalit F, Knockaert S, Remark R, Goc J, Lepelley A, Becht E, Katsahian S, Bizouard G, et al. Presence of B cells in tertiary lymphoid structures is associated with a protective immunity in patients with lung cancer. Am J Respir Crit Care Med. 2014;189:832–44. doi:10.1164/rccm.201309-1611OC. PMID:24484236.
   PubMed Web of Science ®Google Scholar
• Germain C, Gnjatic S, Dieu-Nosjean M-C. Tertiary lymphoid structure-associated B cells are key players in anti-tumor immunity. Front Immunol. 2015;6:67. doi:10.3389/fimmu.2015.00067. PMID:25755654.
   PubMed Web of Science ®Google Scholar
• Goc J, Germain C, Vo-Bourgais TKD, Lupo A, Klein C, Knockaert S, de Chaisemartin L, Ouakrim H, Becht E, Alifano M, et al. Dendritic cells in tumor-associated tertiary lymphoid structures signal a Th1 cytotoxic immune contexture and license the positive prognostic value of infiltrating CD8+ T cells. Cancer Res. 2014;74:705–15. doi:10.1158/0008-5472.CAN-13-1342. PMID:24366885.
   PubMed Web of Science ®Google Scholar
• Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, Nair VS, Xu Y, Khuong A, Hoang CD, et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med. 2015;21:938–45. doi:10.1038/nm.3909. PMID:26193342.
   PubMed Web of Science ®Google Scholar
• Bohnhorst JØ, Bjørgan MB, Thoen JE, Natvig JB, Thompson KM. Bm1-Bm5 classification of peripheral blood B cells reveals circulating germinal center founder cells in healthy individuals and disturbance in the B cell subpopulations in patients with primary Sjögren's syndrome. J Immunol Baltim Md 1950. 2001;167:3610–8.
   Google Scholar
• Llibre A, López-Macías C, Marafioti T, Mehta H, Partridge A, Kanzig C, Rivellese F, Galson JD, Walker LJ, Milne P, et al. LLT1 and CD161 Expression in Human Germinal Centers Promotes B Cell Activation and CXCR4 Downregulation. J Immunol Baltim Md 1950. 2016;196:2085–94.
   Google Scholar
• Martin E, Treiner E, Duban L, Guerri L, Laude H, Toly C, Premel V, Devys A, Moura IC, Tilloy F, et al. Stepwise development of MAIT cells in mouse and human. PLoS Biol. 2009;7:e54. doi:10.1371/journal.pbio.1000054. PMID:19278296.
   PubMed Web of Science ®Google Scholar
• Zhang HH, Song K, Rabin RL, Hill BJ, Perfetto SP, Roederer M, Douek DC, Siegel RM, Farber JM. CCR2 identifies a stable population of human effector memory CD4+ T cells equipped for rapid recall response. J Immunol Baltim Md 1950. 2010;185:6646–63.
   Google Scholar
• Schrum S, Probst P, Fleischer B, Zipfel PF. Synthesis of the CC-chemokines MIP-1alpha, MIP-1beta, and RANTES is associated with a type 1 immune response. J Immunol Baltim Md 1950. 1996;157:3598–604.
   Google Scholar
• Salmond RJ, Emery J, Okkenhaug K, Zamoyska R. MAPK, phosphatidylinositol 3-kinase, and mammalian target of rapamycin pathways converge at the level of ribosomal protein S6 phosphorylation to control metabolic signaling in CD8T cells. J Immunol Baltim Md 1950. 2009;183:7388–97.
   Google Scholar
• Wang PL, O'Farrell S, Clayberger C, Krensky AM. Identification and molecular cloning of tactile. A novel human T cell activation antigen that is a member of the Ig gene superfamily. J Immunol Baltim Md 1950. 1992;148:2600–8.
   Google Scholar
• Fuchs A, Cella M, Giurisato E, Shaw AS, Colonna M. Cutting edge: CD96 (tactile) promotes NK cell-target cell adhesion by interacting with the poliovirus receptor (CD155). J Immunol Baltim Md 1950. 2004;172:3994–8.
   Google Scholar
• Springer TA. Adhesion receptors of the immune system. Nature. 1990;346:425–34. doi:10.1038/346425a0. PMID:1974032.
   PubMed Web of Science ®Google Scholar
• Hogg N, Landis RC. Adhesion molecules in cell interactions. Curr Opin Immunol. 1993;5:383–90. doi:10.1016/0952-7915(93)90057-Y. PMID:7688516.
   PubMed Web of Science ®Google Scholar
• Mayne M, Moffatt T, Kong H, McLaren PJ, Fowke KR, Becker KG, Namaka M, Schenck A, Bardoni B, Bernstein CN, et al. CYFIP2 is highly abundant in CD4+ cells from multiple sclerosis patients and is involved in T cell adhesion. Eur J Immunol. 2004;34:1217–27. doi:10.1002/eji.200324726. PMID:15048733.
   PubMed Web of Science ®Google Scholar
• Witherden DA, Boismenu R, Havran WL. CD81 and CD28 costimulate T cells through distinct pathways. J Immunol Baltim Md 1950. 2000;165:1902–9.
   Google Scholar
• Wiley SR, Goodwin RG, Smith CA. Reverse signaling via CD30 ligand. J Immunol Baltim Md 1950. 1996;157:3635–9.
   Google Scholar
• Alonso-Ramirez R, Loisel S, Buors C, Pers J-O, Montero E, Youinou P, Renaudineau Y. Rationale for targeting CD6 as a treatment for autoimmune diseases. Arthritis. 2010;2010:130646. doi:10.1155/2010/130646. PMID:22076177.
   PubMedGoogle Scholar
• Gulen MF, Kang Z, Bulek K, Youzhong W, Kim TW, Chen Y, Altuntas CZ, Bak-Jenson K, McGeachy MJ, Do JS, et al. The receptor SIGIRR suppresses Th17 cell proliferation via inhibition of the interleukin-1 receptor pathway and mTOR kinase activation. Immunity 2010;32:54–66. doi:10.1016/j.immuni.2009.12.003. PMID:20060329.
   PubMed Web of Science ®Google Scholar
• Garlanda C, Dinarello CA, Mantovani A. The interleukin-1 family: Back to the future. Immunity. 2013;39:1003–18. doi:10.1016/j.immuni.2013.11.010. PMID:24332029.
   PubMed Web of Science ®Google Scholar
• Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman W-H, Pagès F, Trajanoski Z, Galon J. ClueGO: A Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinforma Oxf Engl. 2009;25:1091–3. doi:10.1093/bioinformatics/btp101.
   PubMed Web of Science ®Google Scholar
• Srenathan U, Steel K, Taams LS. IL-17+ CD8+ T cells: Differentiation, phenotype and role in inflammatory disease. Immunol Lett. 2016;178:20–6. doi:10.1016/j.imlet.2016.05.001. PMID:27173097.
   PubMed Web of Science ®Google Scholar
• Croft M. Co-stimulatory members of the TNFR family: Keys to effective T-cell immunity? Nat Rev Immunol. 2003;3:609–20. doi:10.1038/nri1148. PMID:12974476.
   PubMed Web of Science ®Google Scholar
• Becht E, Giraldo NA, Lacroix L, Buttard B, Elarouci N, Petitprez F, Selves J, Laurent-Puig P, Sautès-Fridman C, Fridman WH, et al. Estimating the population abundance of tissue-infiltrating immune and stromal cell populations using gene expression. Genome Biol. 2016;17:218. doi:10.1186/s13059-016-1070-5. PMID:27765066.
   PubMed Web of Science ®Google Scholar
• Platonova S, Cherfils-Vicini J, Damotte D, Crozet L, Vieillard V, Validire P, André P, Dieu-Nosjean M-C, Alifano M, Régnard J-F, et al. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res. 2011;71:5412–22. doi:10.1158/0008-5472.CAN-10-4179. PMID:21708957.
   PubMed Web of Science ®Google Scholar
• Mark NM, Kargl J, Busch SE, Yang GHY, Metz HE, Zhang H, Hubbard JJ, Pipavath SNJ, Madtes DK, Houghton AM. COPD alters immune cell composition and immune checkpoint inhibitor efficacy in NSCLC. Am J Respir Crit Care Med. 2017. doi:10.1164/rccm.201704-0795OC. PMID:28934595.
   PubMed Web of Science ®Google Scholar
• Iliopoulou EG, Karamouzis MV, Missitzis I, Ardavanis A, Sotiriadou NN, Baxevanis CN, Rigatos G, Papamichail M, Perez SA. Increased frequency of CD4+ cells expressing CD161 in cancer patients. Clin Cancer Res Off J Am Assoc Cancer Res. 2006;12:6901–9. doi:10.1158/1078-0432.CCR-06-0977.
   PubMed Web of Science ®Google Scholar
• Pozo D, Valés-Gómez M, Mavaddat N, Williamson SC, Chisholm SE, Reyburn H. CD161 (human NKR-P1A) signaling in NK cells involves the activation of acid sphingomyelinase. J Immunol Baltim Md 1950. 2006;176:2397–406.
   Google Scholar
• Bai A, Robson S. Beyond ecto-nucleotidase: CD39 defines human Th17 cells with CD161. Purinergic Signal. 2015;11:317–9. doi:10.1007/s11302-015-9457-4. PMID:26059452.
   PubMed Web of Science ®Google Scholar
• Takahashi T, Dejbakhsh-Jones S, Strober S. Expression of CD161 (NKR-P1A) defines subsets of human CD4 and CD8T cells with different functional activities. J Immunol Baltim Md 1950. 2006;176:211–6.
   Google Scholar
• Welters MJP, Ma W, Santegoets SJ, Goedemans R, Ehsan I, Jordanova KS, van Ham VJ, van Unen V, Koning F, van Egmond SI, et al. Intratumoral HPV16-specific T-cells constitute a type 1 oriented tumor microenvironment to improve survival in HPV16-driven oropharyngeal cancer. Clin Cancer Res. 2017. doi:10.1158/1078-0432.CCR-17-2140. PMID:29018052.
   PubMed Web of Science ®Google Scholar
• Gasper DJ, Tejera MM, Suresh M. CD4T-cell memory generation and maintenance. Crit Rev Immunol. 2014;34:121–46. doi:10.1615/CritRevImmunol.2014010373. PMID:24940912.
   PubMed Web of Science ®Google Scholar
• Poggi A, Costa P, Zocchi MR, Moretta L. Phenotypic and functional analysis of CD4+ NKRP1A+ human T lymphocytes. Direct evidence that the NKRP1A molecule is involved in transendothelial migration. Eur J Immunol. 1997;27:2345–50. doi:10.1002/eji.1830270932. PMID:9341779.
   PubMed Web of Science ®Google Scholar
• Maggi L, Santarlasci V, Capone M, Rossi MC, Querci V, Mazzoni A, Cimaz R, De Palma R, Liotta F, Maggi E, et al. Distinctive features of classic and nonclassic (Th17 derived) human Th1 cells. Eur J Immunol. 2012;42:3180–8. doi:10.1002/eji.201242648. PMID:22965818.
   PubMed Web of Science ®Google Scholar
• Cosmi L, De Palma R, Santarlasci V, Maggi L, Capone M, Frosali F, Rodolico G, Querci V, Abbate G, Angeli R, et al. Human interleukin 17-producing cells originate from a CD161+CD4+ T cell precursor. J Exp Med. 2008;205:1903–16. doi:10.1084/jem.20080397. PMID:18663128.
   PubMed Web of Science ®Google Scholar
• Fergusson JR, Smith KE, Fleming VM, Rajoriya N, Newell EW, Simmons R, Marchi E, Björkander S, Kang Y-H, Swadling L, et al. CD161 defines a transcriptional and functional phenotype across distinct human T cell lineages. Cell Rep. 2014;9:1075–88. doi:10.1016/j.celrep.2014.09.045. PMID:25437561.
   PubMed Web of Science ®Google Scholar
• Pesenacker AM, Bending D, Ursu S, Wu Q, Nistala K, Wedderburn LR. CD161 defines the subset of FoxP3+ T cells capable of producing proinflammatory cytokines. Blood. 2013;121:2647–58. doi:10.1182/blood-2012-08-443473. PMID:23355538.
   PubMed Web of Science ®Google Scholar
• Afzali B, Mitchell PJ, Edozie FC, Povoleri GAM, Dowson SE, Demandt L, Walter G, Canavan JB, Scotta C, Menon B, et al. CD161 expression characterizes a subpopulation of human regulatory T cells that produces IL-17 in a STAT3-dependent manner. Eur J Immunol. 2013;43:2043–54. doi:10.1002/eji.201243296. PMID:23677517.
   PubMed Web of Science ®Google Scholar
• Sakuishi K, Apetoh L, Sullivan JM, Blazar BR, Kuchroo VK, Anderson AC. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J Exp Med. 2010;207:2187–94. doi:10.1084/jem.20100643. PMID:20819927.
   PubMed Web of Science ®Google Scholar
• Aspeslagh S, Postel-Vinay S, Rusakiewicz S, Soria J-C, Zitvogel L, Marabelle A. Rationale for anti-OX40 cancer immunotherapy. Eur J Cancer Oxf Engl 1990. 2016;52:50–66.
   PubMed Web of Science ®Google Scholar
• Weixler B, Cremonesi E, Sorge R, Muraro MG, Delko T, Nebiker CA, Däster S, Governa V, Amicarella F, Soysal SD, et al. OX40 expression enhances the prognostic significance of CD8 positive lymphocyte infiltration in colorectal cancer. Oncotarget. 2015;6:37588–99. doi:10.18632/oncotarget.5940. PMID:26439988.
   PubMed Web of Science ®Google Scholar
• Dawicki W, Bertram EM, Sharpe AH, Watts TH. 4-1BB and OX40 act independently to facilitate robust CD8 and CD4 recall responses. J Immunol Baltim Md 1950. 2004;173:5944–51.
   Google Scholar
• Kennedy MK, Willis CR, Armitage RJ. Deciphering CD30 ligand biology and its role in humoral immunity. Immunology. 2006;118:143–52. doi:10.1111/j.1365-2567.2006.02354.x. PMID:16771849.
   PubMed Web of Science ®Google Scholar
• Morimoto S, Kanno Y, Tanaka Y, Tokano Y, Hashimoto H, Jacquot S, Morimoto C, Schlossman SF, Yagita H, Okumura K, et al. CD134L engagement enhances human B cell Ig production: CD154/CD40, CD70/CD27, and CD134/CD134L interactions coordinately regulate T cell-dependent B cell responses. J Immunol Baltim Md 1950. 2000;164:4097–104.
   Google Scholar
• Cerutti A, Schaffer A, Goodwin RG, Shah S, Zan H, Ely S, Casali P. Engagement of CD153 (CD30 ligand) by CD30+ T cells inhibits class switch DNA recombination and antibody production in human IgD+ IgM+ B cells. J Immunol Baltim Md 1950. 2000;165:786–94.
   Google Scholar
• Weinstein JS, Lezon-Geyda K, Maksimova Y, Craft S, Zhang Y, Su M, Schulz VP, Craft J, Gallagher PG. Global transcriptome analysis and enhancer landscape of human primary T follicular helper and T effector lymphocytes. Blood. 2014;124:3719–29. doi:10.1182/blood-2014-06-582700. PMID:25331115.
   PubMed Web of Science ®Google Scholar
• Kim M-Y, Gaspal FMC, Wiggett HE, McConnell FM, Gulbranson-Judge A, Raykundalia C, Walker LSK, Goodall MD, Lane PJL. CD4(+)CD3(-) accessory cells costimulate primed CD4T cells through OX40 and CD30 at sites where T cells collaborate with B cells. Immunity 2003;18:643–54. doi:10.1016/S1074-7613(03)00110-9. PMID:12753741.
   PubMed Web of Science ®Google Scholar
• Jiang SH, Shen N, Vinuesa CG. Posttranscriptional T cell gene regulation to limit Tfh cells and autoimmunity. Curr Opin Immunol. 2015;37:21–7. doi:10.1016/j.coi.2015.09.003. PMID:26432764.
   PubMed Web of Science ®Google Scholar
• McCall MN, Bolstad BM, Irizarry RA. Frozen robust multiarray analysis (fRMA). Biostat Oxf Engl. 2010;11:242–53. doi:10.1093/biostatistics/kxp059.
   PubMed Web of Science ®Google Scholar
• Detterbeck FC, Boffa DJ, Tanoue LT. THe new lung cancer staging system. CHEST J. 2009;136:260–71. doi:10.1378/chest.08-0978.
   PubMed Web of Science ®Google Scholar
• Brambilla E, Travis WD, Colby TV, Corrin B, Shimosato Y. The new World Health Organization classification of lung tumours. Eur Respir J. 2001;18:1059–68. doi:10.1183/09031936.01.00275301. PMID:11829087.
   PubMed Web of Science ®Google Scholar