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Original Research

The inhibitory NKR-P1B receptor regulates NK cell-mediated mammary tumor immunosurveillance in mice

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Article: 2168233 | Received 20 Sep 2022, Accepted 10 Jan 2023, Published online: 22 Jan 2023

References

  • Cerwenka A, Lanier LL. Natural killer cells, viruses and cancer. Nat Rev Immunol. 2001;1(1):41–12.
  • O’Leary JG, Goodarzi M, Drayton DL, von Andrian UH. T cell- and B cell-independent adaptive immunity mediated by natural killer cells. Nat Immunol. 2006;7(5):507–516.
  • Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009;457(7229):557–561.
  • Wight A, Parsons BD, Rahim MMA, Makrigiannis AP. A Central Role for Ly49 Receptors in NK Cell Memory. J Immunol. 2020;204:2867–2875.
  • Shaw RK, Issekutz AC, Fraser R, Schmit P, Morash B, Monaco-Shawver L, et al. Bilateral adrenal EBV-associated smooth muscle tumors in a child with a natural killer cell deficiency. Blood. 2012;119(17):4009–4012.
  • Yang CM, Yang YH, Lin YT, Lu MY, Chiang BL. NATURAL KILLER CELL DEFICIENCY ASSOCIATED WITH HODGKIN’S LYMPHOMA: a CASE REPORT. J Formos Med Assoc. 2002;101:3.
  • Komiyama A, Kawai H, Yamada S, Kato M, Yanagisawa M, Miyagawa Y, et al. A Killing Defect of Natural Killer Cells With the Absence of Natural Killer Cytotoxic Factors in a Child With Hodgkin’s Disease. Blood. 1987;69(6):1686–1690.
  • Guerra N, Tan YX, Joncker NT, Choy A, Gallardo F, Xiong N, et al. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity. 2008;28(4):571–580.
  • Tu MM, Rahim MMA, Sayed C, Mahmoud AB, Makrigiannis AP. Immunosurveillance and Immunoediting of Breast Cancer via Class I MHC Receptors. Cancer Immunol Res. 2017;5:1016–1028.
  • Lanier LL. NK cell receptors. Annu Rev Immunol. 1998;16:359–393.
  • Lanier LL. NK cell recognition. Annu Rev Immunol. 2005;23:225–274.
  • Arase H, Mocarski ES, Campbell AE, Hill AB, Lanier LL. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science. 2002;296(5571):1323–1326.
  • Aguilar OA, Berry R, Rahim MMA, Reichel JJ, Popović B, Tanaka M, et al. A Viral Immunoevasin Controls Innate Immunity by Targeting the Prototypical Natural Killer Cell Receptor Family. Cell. 2017;169(1):58–71.e14.
  • Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science. 1999;285(5428):727–729.
  • Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat Immunol. 2000;1(2):119–126.
  • Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature. 2005;436(7054):1186–1190.
  • Rahim MMA, Makrigiannis AP. Ly49 receptors: evolution, genetic diversity, and impact on immunity. Immunol Rev. 2015;267(1):137–147.
  • Kärre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H–2-deficient lymphoma variants suggests alternative immune defence strategy. Nature. 1986;319(6055):675–678.
  • Kirkham CL, Carlyle JR. Complexity and Diversity of the NKR-P1:Clr (Klrb1:Clec2) Recognition Systems. Front Immunol. 2014;5:214.
  • Zhang Q, Rahim MMA, Allan DSJ, Tu MM, Belanger S, Abou-Samra E, et al. Mouse Nkrp1-Clr Gene Cluster Sequence and Expression Analyses Reveal Conservation of Tissue-Specific MHC-Independent Immunosurveillance. PLOS ONE. 2012;7(12):e50561.
  • Kung SK, Su RC, Shannon J, Miller RG. The NKR-P1B gene product is an inhibitory receptor on SJL/J NK cells. J Immunol. 1999;162(10):5876–5887.
  • Carlyle JR, Mesci A, Ljutic B, Belanger S, Tai LH, Rousselle E, et al. Molecular and genetic basis for strain-dependent NK1.1 alloreactivity of mouse NK cells. J Immunol. 2006;176(12):7511–7524.
  • Plougastel B, Dubbelde C, Yokoyama WM. Cloning of Clr, a new family of lectin-like genes localized between mouse Nkrp1a and Cd69. Immunogenetics. 2001;53(3):209–214.
  • Carlyle JR, Jamieson AM, Gasser S, Clingan CS, Arase H, Raulet DH. Missing self-recognition of Ocil/Clr-b by inhibitory NKR-P1 natural killer cell receptors. Proc Natl Acad Sci USA. 2004;101(10):3527–3532.
  • Iizuka K, Naidenko OV, Plougastel BFM, Fremont DH, Yokoyama WM. Genetically linked C-type lectin-related ligands for the NKRP1 family of natural killer cell receptors. Nat Immunol. 2003;4(8):801–807.
  • Chen P, Bélanger S, Aguilar OA, Zhang Q, St-Laurent A, Rahim MMA, et al. Analysis of the mouse 129-strain Nkrp1-Clr gene cluster reveals conservation of genomic organization and functional receptor-ligand interactions despite significant allelic polymorphism. Immunogenetics. 2011;63(10):627–640.
  • Kveberg L, Dai KZ, Inngjerdingen M, Brooks CG, Fossum S, Vaage JT. Phylogenetic and functional conservation of the NKR-P1F and NKR-P1G receptors in rat and mouse. Immunogenetics. 2011;63(7):429–436.
  • Aust JG, Gays F, Mickiewicz KM, Buchanan E, Brooks CG. The expression and function of the NKRP1 receptor family in C57BL/6 mice. J Immunol. 2009;183(1):106–116.
  • Munir M, Rahim A, Chen P, Mottashed AN, Mahmoud AB, Thomas MJ, et al. The mouse NKR-P1B:Clr-b recognition system is a negative regulator of innate immune responses. Blood. 2015;125(14):2217–2227.
  • Fine JH, Chen P, Mesci A, Allan DSJ, Gasser S, Raulet DH, et al. Chemotherapy-induced genotoxic stress promotes sensitivity to natural killer cell cytotoxicity by enabling missing-self recognition. Cancer Res. 2010;70(18):7102–7113.
  • Gordon SM, Chaix J, Rupp LJ, Wu J, Madera S, Sun JC, et al. The Transcription Factors T-bet and Eomes Control Key Checkpoints of Natural Killer Cell Maturation. Immunity. 2012;36(1):55–67.
  • Intlekofer AM, Takemoto N, Wherry EJ, Longworth SA, Northrup JT, Palanivel VR, et al. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat Immunol. 2005;6(12):1236–1244.
  • Paley MA, Gordon SM, Bikoff EK, Robertson EJ, Wherry EJ, Reiner SL. Technical Advance: fluorescent reporter reveals insights into eomesodermin biology in cytotoxic lymphocytes. J Leukoc Biol. 2013;93(2):307–315.
  • Townsend MJ, Weinmann AS, Matsuda JL, Salomon R, Farnham PJ, Biron CA, et al. T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity. 2004;20(4):477–494.
  • Wagner JA, Wong P, Schappe T, Berrien-Elliott MM, Cubitt C, Jaeger N, et al. Stage-Specific Requirement for Eomes in Mature NK Cell Homeostasis and Cytotoxicity. Cell Rep. 2020;31(9):107720.
  • Zhang J, Le Gras S, Pouxvielh K, Faure F, Fallone L, Kern N, et al. Sequential actions of EOMES and T-BET promote stepwise maturation of natural killer cells. Nat Commun. 2021;12(1):5446.
  • Gill S, Vasey AE, De Souza A, Baker J, Smith AT, Kohrt HE, et al. Rapid development of exhaustion and down-regulation of eomesodermin limit the antitumor activity of adoptively transferred murine natural killer cells. Blood. 2012;119(24):5758–5768.
  • Krneta T, Gillgrass A, Chew M, Ashkar AA. The breast tumor microenvironment alters the phenotype and function of natural killer cells. Cell Mol Immunol. 2016;13(5):628–639.
  • Beldi-Ferchiou A, Lambert M, Dogniaux S, Vély F, Vivier E, Olive D, et al. PD-1 mediates functional exhaustion of activated NK cells in patients with Kaposi sarcoma. Oncotarget. 2016;7(45):72961–72977.
  • Benson DM, Bakan CE, Mishra A, Hofmeister CC, Efebera Y, Becknell B, et al. The PD-1/PD-L1 axis modulates the natural killer cell versus multiple myeloma effect: a therapeutic target for CT-011, a novel monoclonal anti-PD-1 antibody. Blood. 2010;116(13):2286–2294.
  • da Silva IP, Gallois A, Jimenez-Baranda S, Khan S, Anderson AC, Kuchroo VK, et al. Reversal of NK-cell exhaustion in advanced melanoma by Tim-3 blockade. Cancer Immunol Res. 2014;2(5):410–422.
  • Zhang Q, Bi J, Zheng X, Chen Y, Wang H, Wu W, et al. Blockade of the checkpoint receptor TIGIT prevents NK cell exhaustion and elicits potent anti-tumor immunity. Nat Immunol. 2018;19(7):723–732.
  • Mamessier E, Sylvain A, Thibult ML, Houvenaeghel G, Jacquemier J, Castellano R, et al. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J Clin Invest. 2011;121(9):3609–3622.
  • Semeraro M, Rusakiewicz S, Minard-Colin V, Delahaye NF, Enot D, Vély F, et al. Clinical impact of the NKp30/B7-H6 axis in high-risk neuroblastoma patients. Sci Transl Med. 2015;7(283):283ra55.
  • Platonova S, Cherfils-Vicini J, Damotte D, Crozet L, Vieillard V, Validire P, et al. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res. 2011;71(16):5412–5422.
  • Hsu J, Hodgins JJ, Marathe M, Nicolai CJ, Bourgeois-Daigneault MC, Trevino TN, et al. Contribution of NK cells to immunotherapy mediated by PD-1/PD-L1 blockade. J Clin Invest. 2018;128(10):4654–4668.
  • Gao Y, Souza-Fonseca-Guimaraes F, Bald T, Ng SS, Young A, Ngiow SF, et al. Tumor immunoevasion by the conversion of effector NK cells into type 1 innate lymphoid cells. Nat Immunol. 2017;18(9):1004–1015.
  • Melero I, Bach N, Chen L. Costimulation, tolerance and ignorance of cytolytic T lymphocytes in immune responses to tumor antigens. Life Sci. 1997;60:2035–2041.
  • Mognol GP, Spreafico R, Wong V, Scott-Browne JP, Togher S, Hoffmann A, et al. Exhaustion-associated regulatory regions in CD8+ tumor-infiltrating T cells. Pnas. 2017;114(13):E2776–85.
  • Baitsch L, Baumgaertner P, Devêvre E, Raghav SK, Legat A, Barba L, et al. Exhaustion of tumor-specific CD8+ T cells in metastases from melanoma patients. J Clin Invest. 2011;121(6):2350–2360.
  • Li H, van der Leun AM, Yofe I, Lubling Y, Gelbard-Solodkin D, van Akkooi ACJ, et al. Dysfunctional CD8 T Cells Form a Proliferative, Dynamically Regulated Compartment within Human Melanoma. Cell. 2019;176(4):775–789.e18.
  • Philip M, Fairchild L, Sun L, Horste EL, Camara S, Shakiba M, et al. Chromatin states define tumour-specific T cell dysfunction and reprogramming. Nature. 2017;545(7655):452–456.
  • Thommen DS, Schreiner J, Müller P, Herzig P, Roller A, Belousov A, et al. Progression of Lung Cancer Is Associated with Increased Dysfunction of T Cells Defined by Coexpression of Multiple Inhibitory Receptors. Cancer Immunol Res. 2015;3(12):1344–1355.
  • Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol. 1992;12(3):954–961.
  • Sojka DK, Plougastel-Douglas B, Yang L, Pak-Wittel MA, Artyomov MN, Ivanova Y, et al. Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. eLife. 2014;3:e01659.
  • Chiossone L, Chaix J, Fuseri N, Roth C, Vivier E, Walzer T. Maturation of mouse NK cells is a 4-stage developmental program. Blood. 2009;113(22):5488–5496.
  • Huntington ND, Tabarias H, Fairfax K, Brady J, Hayakawa Y, Degli-Esposti MA, et al. NK Cell Maturation and Peripheral Homeostasis Is Associated with KLRG1 Up-Regulation. The Journal of Immunology. 2007;178(8):4764–4770.
  • Bélanger S, Tu MM, Rahim MMA, Mahmoud AB, Patel R, Tai LH, et al. Impaired natural killer cell self-education and “missing-self” responses in Ly49-deficient mice. Blood. 2012;120(3):592–602.
  • Philip M, Schietinger A. CD8+ T cell differentiation and dysfunction in cancer. Nat Rev Immunol. 2021;22:209–223.
  • Mamessier E, Pradel LC, Thibult ML, Drevet C, Zouine A, Jacquemier J, et al. Peripheral blood NK cells from breast cancer patients are tumor-induced composite subsets. J Immunol. 2013;190(5):2424–2436.
  • Ardolino M, Azimi CS, Iannello A, Trevino TN, Horan L, Zhang L, et al. Cytokine therapy reverses NK cell anergy in MHC-deficient tumors. J Clin Invest. 2014;124(11):4781–4794.
  • Labani-Motlagh A, Ashja-Mahdavi M, Loskog A. The Tumor Microenvironment: a Milieu Hindering and Obstructing Antitumor Immune Responses. Front Immunol. 2020;11:940.