CD8+ T lymphocytes are sensitive to NKG2A/HLA-E licensing interaction: role in the survival of cancer patients

References

• Martínez-Sánchez MV, Periago A, Legaz L, Gimeno L, Mrowiec A, Montes-Barqueros NR et al. Overexpression of KIR inhibitory ligands (HLA-I) determines that immunosurveillance of myeloma depends on diverse and strong NK cell licensing. Oncoimmunology. 2015 Oct 29;5(4):e1093721. doi:10.1080/2162402X.2015.1093721.
   Web of Science ®Google Scholar
• Martínez-Sánchez MV, Fuster JL, Campillo JA, Galera AM, Bermúdez-Cortés M, Llinares ME et al. Expression of NK cell receptor ligands on leukemic cells is associated with the outcome of childhood acute leukemia. Cancers. 2021;13:2294. doi:10.3390/cancers13102294.
   Web of Science ®Google Scholar
• Guillamón CF, Martínez-Sánchez M V, Gimeno L, Mrowiec A, Martínez-García J, Server-Pastor G et al. NK cell education in tumor immune surveillance: DNAM-1/KIR receptor ratios as predictive biomarkers for solid tumor outcome. Cancer Immunology Research. 2018; Dec;6(12):1537-1547. http://can. doi:10.1158/2326-6066.CIR-18-0022.
   PubMed Web of Science ®Google Scholar
• Guillamón CF, Martínez-Sánchez M V, Gimeno L, Campillo JA, Server-Pastor G, Martínez-García J et al. Activating KIRs on educated NK cells support downregulation of CD226 and inefficient tumor immunosurveillance. Cancer Immunology Research. 2019;7:1307–12. doi: 10.1158/2326-6066.CIR-18-0847.
   PubMed Web of Science ®Google Scholar
• Guillamón CF, Gimeno L, Server G, Martıinez-Sanchez MV, Escudero JF, Lopez-Cubillana P, et al. Immunological risk stratification of bladder cancer based on peripheral blood natural killer cell biomarkers. European Urology Oncology. 2019;4:246-255. doi: 10.1016/j.euo.2019.04.009.
   PubMed Web of Science ®Google Scholar
• Narni-Mancinelli E, Vivier E, Kerdiles YM. The ‘T-cell-ness’ of NK cells: unexpected similarities between NK cells and T cells. Int Immunol. 2011;23:427–431. doi:10.1093/intimm/dxr035.
   PubMed Web of Science ®Google Scholar
• Parham P. Taking license with natural killer cell maturation and repertoire development. Immunol Rev. 2006;214(1):155–160. doi:10.1111/j.1600-065X.2006.00462.x.
   PubMed Web of Science ®Google Scholar
• Rosenberg J, Huang J. CD8+ T cells and NK cells: parallel and complementary soldiers of immunotherapy. Curr Opin Chem Eng. 2018;19:9–20. doi:10.1016/j.coche.2017.11.006.
   PubMed Web of Science ®Google Scholar
• Kurd N, Robey EA. T-cell selection in the thymus: a spatial and temporal perspective. Immunol Rev. 2016;271(1):114–126. doi:10.1111/imr.12398.
   PubMed Web of Science ®Google Scholar
• Anfossi N, André P, Guia S, Falk CS, Roetynck S, Stewart CA et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity. 2006;25(2):331–342. doi:10.1016/j.immuni.2006.06.013.
   Web of Science ®Google Scholar
• Béziat V, Descours B, Parizot C, Debré P, Vieillard V. NK cell terminal differentiation: correlated stepwise decrease of NKG2A and acquisition of KIRs. PLoS ONE. 2010;5:1–12. doi:10.1371/journal.pone.0011966.
   Web of Science ®Google Scholar
• Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song YJ, Yang L et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature. 2005;436(7051):709–713. doi:10.1038/nature03847.
   Web of Science ®Google Scholar
• Kärre K. Natural killer cell recognition of missing self. Nat Immunol. 2008;9(5):477–480. doi:10.1038/ni0508-477.
   PubMed Web of Science ®Google Scholar
• Parham P. MHC class I molecules and KIRS in human history, health and survival. Nat Rev Immunol. 2005;5(3):201–214. doi:10.1038/nri1570.
   PubMed Web of Science ®Google Scholar
• Pende D, Falco M, Vitale M, Cantoni C, Vitale C, Munari E et al. Killer Ig-like receptors (KIRs): their role in NK cell modulation and developments leading to their clinical exploitation. Front Immunol. 2019;May 28;10:1179. doi:10.3389/fimmu.2019.01179.
   PubMed Web of Science ®Google Scholar
• Hilton HG, Parham P. Missing or altered self: human NK cell receptors that recognize HLA-C. Immunogenetics. 2017;69(8–9):567–579. doi:10.1007/s00251-017-1001-y.
   PubMed Web of Science ®Google Scholar
• Johansson MH, Höglund E, Nakamura MC, Ryan JC, Höglund P. Alpha1/alpha2 domains of H-2D(d), but not H-2L(d), induce ‘missing self’ reactivity in vivo–no effect of H-2L(d) on protection against NK cells expressing the inhibitory receptor Ly49G2. Eur J Immunol. 1998;28:4198–4206. doi:10.1002/(SICI)1521-4141(199812)28:12<4198::AID-IMMU4198>3.0.CO;2-9.
   PubMed Web of Science ®Google Scholar
• Enqvist M, Ask EH, Forslund E, Carlsten M, Abrahamsen G, Béziat V, Andersson S, Schaffer M, Spurkland A, Bryceson Y, Önfelt B, Malmberg KJ. J Immunol. 2015 May 1;194(9):4518–27. doi:10.4049/jimmunol.1401972. Epub 2015 Mar 30. PMID:25825444
   Google Scholar
• Schafer JR, Salzillo TC, Chakravarti N, Kararoudi MN, Trikha P, Foltz JA, et al. Education-dependent activation of glycolysis promotes the cytolytic potency of licensed human natural killer cells. J Allergy Clin Immunol. 2019;143(1):346–358. e6. doi:10.1016/j.jaci.2018.06.047.
   Web of Science ®Google Scholar
• Guillamón CF, Martínez-Sánchez MV, Gimeno L, Mrowiec A, Martínez-García J, Server-Pastor G et al. NK cell education in tumor immune surveillance: DNAM-1/KIR receptor ratios as predictive biomarkers for solid tumor outcome. Cancer Immunology Research. 2018;Dec;6(12):1537–1547. doi:10.1159/2326-6066.CIR-18-0022.
   PubMed Web of Science ®Google Scholar
• Goodridge JP, Jacobs B, Saetersmoen ML, Clement D, Hammer Q, Clancy T et al. Remodeling of secretory lysosomes during education tunes functional potential in NK cells. Nat Commun. 2019;Jan 31;10(1):514. doi:10.1038/s41467-019-08384-x.
   PubMed Web of Science ®Google Scholar
• Khaznadar Z, Boissel N, Agaugué S, Henry G, Cheok M, Vignon M et al. Defective NK cells in acute myeloid leukemia patients at diagnosis are associated with blast transcriptional signatures of immune evasion. The Journal of Immunology. 2015;195(6):2580–2590. doi:10.4049/jimmunol.1500262.
   Web of Science ®Google Scholar
• Carlsten M, Björkström NK, Norell H, Bryceson Y, Van Hall T, Baumann BC et al. DNAX accessory molecule-1 mediated recognition of freshly isolated ovarian carcinoma by resting natural killer cells. Cancer Res. 2007;67(3):1317–1325. doi:10.1158/0008-5472.CAN-06-2264.
   Web of Science ®Google Scholar
• Labani-Motlagh A, Israelsson P, Ottander U, Lundin E, Nagaev I, Nagaeva O et al. Differential expression of ligands for NKG2D and DNAM-1 receptors by epithelial ovarian cancer-derived exosomes and its influence on NK cell cytotoxicity. Tumor Biology. 2016;37(4):5455–5466. doi:10.1007/s13277-015-4313-2.
   Google Scholar
• Peng Y, Xi C, Zhu Y, Yin L, Wei J, Zhang J-J et al. Altered expression of CD226 and CD96 on natural killer cells in patients with pancreatic cancer. Oncotarget. 2016;7(41):66586–66594. doi:10.18632/oncotarget.11953.
   Google Scholar
• Guillerey C, De Andrade LF, Vuckovic S, Miles K, Ngiow SF, Yong MCR et al. Immunosurveillance and therapy of multiple myeloma are CD226 dependent. J Clin Invest. 2015;125(5):2077–2089. doi:10.1172/JCI77181.
   Web of Science ®Google Scholar
• Mandelboim O, Reyburn HT, Valés-Gómez M, Pazmany L, Colonna M, Borsellino G et al. Protection from lysis by natural killer cells of group 1 and 2 specificity is mediated by residue 80 in human histocompatibility leukocyte antigen C alleles and also occurs with empty major histocompatibility complex molecules. J Exp Med. 1996;184(3):913–922. doi:10.1084/jem.184.3.913.
   Web of Science ®Google Scholar
• Foley BA, De Santis D, Van Beelen E, Lathbury LJ, Christiansen FT, Witt CS. The reactivity of Bw4+ HLA-B and HLA-A alleles with kir3dll: implications for patient and donor suitability for haploidentical stem cell transplantations. Blood. 2008;112:435–443. doi:10.1182/blood-2008-01-132902.
   PubMed Web of Science ®Google Scholar
• Hansasuta P, Dong T, Thananchai H, Weekes M, Willberg C, Aldemir H et al. Recognition of HLA-A3 and HLA-A11 by KIR3DL2 is peptide-specific. Eur J Immunol. 2004;34(6):1673–1679. doi:10.1002/eji.200425089.
   Web of Science ®Google Scholar
• Horowitz A, Djaoud Z, Nemat-Gorgani N, Blokhuis J, Hilton HG, Béziat V et al. Class I HLA haplotypes form two schools that educate NK cells in different ways. Science Immunology. 2016;1(3):eaag1672. doi:10.1126/sciimmunol.aag1672.
   Web of Science ®Google Scholar
• Braud VM, Allan DS, O’Callaghan CA, Söderström K, D’Andrea A, Ogg GS et al. HL-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature. 1998;391(6669):795–799. doi:10.1038/35869.
   Web of Science ®Google Scholar
• López-Botet M, Llano M, Navarro F, Bellón T. NK cell recognition of non-classical HLA class I molecules. Semin Immunol. 2000; 12(2): 109–119. doi: 10.1006/smim.2000.0213.
   Google Scholar
• Lee N, Goodlett DR, Ishitani A, Marquardt H, Geraghty DE. HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. Journal of Immunology (Baltimore, Md : 1950). 1998;160:4951–4960.
   PubMed Web of Science ®Google Scholar
• McCutcheon JA, Gumperz J, Smith KD, Lutz CT, Parham P. Low HLA-C expression at cell surfaces correlates with increased turnover of heavy chain mRNA. J Exp Med. 1995;181:2085–2095. doi:10.1084/jem.181.6.2085.
   PubMed Web of Science ®Google Scholar
• Kiepiela P, Leslie AJ, Honeyborne I, Ramduth D, Thobakgale C, Chetty S et al. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature. 2004;432(7018):769–775. doi:10.1038/nature03113.
   Web of Science ®Google Scholar
• Lee N, Llano M, Carretero M, Ishitani A, Navarro F, López-Botet M et al. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc Natl Acad Sci U S A; 1998; 95, 5199–5204. doi: 10.1073/pnas.95.9.5199.
   Google Scholar
• Parham P, Guethlein LA. Genetics of natural killer cells in human health, disease, and survival. Annu Rev Immunol. 2018;36(1):519–548. doi:10.1146/annurev-immunol-042617-053149.
   PubMed Web of Science ®Google Scholar
• Merino AM, Song W, He D, Mulenga J, Allen S, Hunter E et al. HLA-B signal peptide polymorphism influences the rate of HIV-1 acquisition but not viral load. J Infect Dis. 2012;205(12):1797–1805. doi:10.1093/infdis/jis275.
   Web of Science ®Google Scholar
• Merino AM, Sabbaj S, Easlick J, Goepfert P, Kaslow RA, Tang J. Dimorphic HLA-B signal peptides differentially influence HLA-E- and natural killer cell-mediated cytolysis of HIV-1-infected target cells. Clin Exp Immunol. 2013;174(3):414–423. doi:10.1111/cei.12187.
   Web of Science ®Google Scholar
• Hallner A, Bernson E, Hussein BA, Ewald Sander F, Brune M, Aurelius J et al. The HLA-B −21 dimorphism impacts on NK cell education and clinical outcome of immunotherapy in acute myeloid leukemia. Blood. 2019;133(13):1479–1488. doi:10.1182/blood-2018-09-874990.
   Web of Science ®Google Scholar
• Yunis EJ, Romero V, Diaz-Giffero F, Zuñiga J, Koka P. Natural killer cell receptor NKG2A/HLA-E interaction dependent differential thymopoiesis of hematopoietic progenitor cells influences the outcome of HIV infection. J Stem Cells. 2007;2:237–248.
   PubMedGoogle Scholar
• Falco M, Romeo E, Marcenaro S, Martini S, Vitale M, Bottino C et al. Combined genotypic and phenotypic killer cell Ig-like receptor analyses reveal KIR2DL3 alleles displaying unexpected monoclonal antibody reactivity: identification of the amino acid residues critical for staining. J Immunol. 2010;185(1):433–441. doi:10.4049/jimmunol.0903632.
   Google Scholar
• Li Y, Kurlander RJ. Comparison of anti-CD3 and anti-CD28-coated beads with soluble anti-CD3 for expanding human T cells: differing impact on CD8 T cell phenotype and responsiveness to restimulation. J Transl Med. 2010;8(1):104. doi:10.1186/1479-5876-8-104.
   PubMed Web of Science ®Google Scholar
• Abel AM, Yang C, Thakar MS, Malarkannan S. Natural killer cells: development, maturation, and clinical utilization. Front Immunol. 2018;9:1869.
   PubMed Web of Science ®Google Scholar
• Schuster IS, Coudert JD, Andoniou CE, Degli-Esposti MA. ‘Natural Regulators’: NK cells as modulators of T cell immunity. Front Immunol. 2016;7:235. doi:10.3389/fimmu.2016.00235.
   PubMed Web of Science ®Google Scholar
• Rajasekaran K, Riese MJ, Rao S, Wang L, Thakar MS, Sentman CL et al. Signaling in effector lymphocytes: insights toward safer immunotherapy. Front Immunol. 2016;7:176. doi:10.3389/fimmu.2016.00176.
   PubMed Web of Science ®Google Scholar
• Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009;457(7229):557–561. doi:10.1038/nature07665.
   PubMed Web of Science ®Google Scholar
• Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL et al. Innate or adaptive immunity? The example of natural killer cells. Science (New York, N Y). 2011;331(6013):44–49. doi:10.1126/science.1198687.
   Web of Science ®Google Scholar
• Sun JC, Beilke JN, Lanier LL. Immune memory redefined: characterizing the longevity of natural killer cells. Immunol Rev. 2010;236(1):83–94. doi:10.1111/j.1600-065X.2010.00900.x.
   PubMed Web of Science ®Google Scholar
• Yawata M, Yawata N, Draghi M, Little A-M, Partheniou F, Parham P. Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function. J Exp Med. 2006;203(3):633–645. doi:10.1084/jem.20051884.
   Web of Science ®Google Scholar
• Liang R, Zhu X, Lan T, Ding D, Zheng Z, Chen T et al. TIGIT promotes CD8+T cells exhaustion and predicts poor prognosis of colorectal cancer. Cancer Immunology, Immunotherapy. 2021;70(10):2781-2793. doi:10.1007/s00262-021-02886-8.
   Web of Science ®Google Scholar
• Liu Z, Zhou Q, Wang Z, Zhang H, Zeng H, Huang Q et al. Intratumoral TIGIT+CD8+T-cell infiltration determines poor prognosis and immune evasion in patients with muscle-invasive bladder cancer. Journal for ImmunoTherapy of Cancer. 2020;8(2):978. doi:10.1136/jitc-2020-000978.
   Web of Science ®Google Scholar
• Wagner AK, Kadri N, Snäll J, Brodin P, Gilfillan S, Colonna M et al. Expression of CD226 is associated to but not required for NK cell education. Nat Commun. 2017;8:15627. doi:10.1038/ncomms15627.
   Web of Science ®Google Scholar
• Guillamón CF, Martínez-Sánchez MV, Gimeno L, Mrowiec A, Martínez-García J, Server-Pastor G et al. NK cell education in tumor immune surveillance: DNAM-1/KIR receptor ratios as predictive biomarkers for solid tumor outcome. Cancer Immunology Research. 2018;6(12):1537–1547. doi:10.1160/2326-6066.CIR-18-0022.
   Web of Science ®Google Scholar
• Sanchez-Correa B, Valhondo I, Hassouneh F, Lopez-Sejas N, Pera A, Bergua JM et al. DNAM-1 and the TIGIT/PVRIG/TACTILE axis: novel immune checkpoints for natural killer cell-based cancer immunotherapy. Cancers. 2019;11(6):877. doi:10.3390/cancers11060877.
   Web of Science ®Google Scholar
• Gilfillan S, Chan CJ, Cella M, Haynes NM, Rapaport AS, Boles KS et al. DNAM-1 promotes activation of cytotoxic lymphocytes by nonprofessional antigen-presenting cells and tumors. J Exp Med. 2008;205(13):2965–2973. doi:10.1084/jem.20081752.
   Web of Science ®Google Scholar
• Weulersse M, Asrir A, Pichler AC, Lemaitre L, Braun M, Carrié N et al. Eomes-dependent loss of the co-activating receptor CD226 restrains CD8+ T cell anti-tumor functions and limits the efficacy of cancer immunotherapy. Immunity. 2020;53(4):824–839. e10. doi:10.1016/j.immuni.2020.09.006.
   Web of Science ®Google Scholar
• Chauvin JM, Zarour HM. TIGIT in cancer immunotherapy. J. Immunother. Cancer. 2020;8(2):e000957. doi:10.1136/jitc-2020-000957.
   Google Scholar
• 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. doi:10.1038/s41590-018-0132-0.
   Web of Science ®Google Scholar
• Held W, Mariuzza RA. Cis interactions of immunoreceptors with MHC and non-MHC ligands. Nat Rev Immunol. 2008;8:269–278. doi:10.1038/nri2278.
   PubMed Web of Science ®Google Scholar
• Hoare HL, Sullivan LC, Pietra G, Clements CS, Lee EJ, Ely LK et al. . Structural basis for a major histocompatibility complex class Ib-restricted T cell response. Nat Immunol. 2006;7:256–264. doi:10.1038/ni1312
   Google Scholar
• Jensen PE, Sullivan BA, Reed-Loisel LM, Weber DA. Qa-1, a nonclassical class I histocompatibility molecule with roles in innate and adaptive immunity. Immunol Res. 2004;29(1–3):81–92. doi:10.1385/IR:29:1-3:081.
   PubMed Web of Science ®Google Scholar
• Mueller DL. Mechanisms maintaining peripheral tolerance. Nat Immunol. 2010;11(1):21–27. doi:10.1038/ni.1817.
   PubMed Web of Science ®Google Scholar