Overexpression of KIR inhibitory ligands (HLA-I) determines that immunosurveillance of myeloma depends on diverse and strong NK cell licensing

References

• Kärre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 1986; 319:675-788; PMID:3951539; http://dx.doi.org/10.1038/319675a0
   PubMed Web of Science ®Google Scholar
• Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song YJ, Yang L, French AR, Sunwoo JB, Lemieux S, Hansen TH et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 2005; 436:709-13; PMID:16079848; http://dx.doi.org/10.1038/nature03847
   PubMed Web of Science ®Google Scholar
• Anfossi N, André P, Guia S, Falk CS, Roetynck S, Stewart CA, Breso V, Frassati C, Reviron D, Middleton D et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity 2006; 25:331-42; PMID:16901727; http://dx.doi.org/10.1016/j.immuni.2006.06.013
   PubMed Web of Science ®Google Scholar
• Thomas LM, Peterson ME, Long EO. Cutting edge: NK cell licensing modulates adhesion to target cells. J Immunol 2013; 191:3981-5; PMID:24038086; http://dx.doi.org/10.4049/jimmunol.1301159
   PubMed Web of Science ®Google Scholar
• Moretta A, Sivori S, Vitale M, Pende D, Morelli L, Augugliaro R, Bottino C, Moretta L. Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells. J Exp Med 1995; 182:875-84; PMID:7650491; http://dx.doi.org/10.1084/jem.182.3.875
   PubMed Web of Science ®Google Scholar
• Mandelboim O, Reyburn HT, Valés-Gómez M, Pazmany L, Colonna M, Borsellino G, Strominger JL. 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 hiscompatibility complex molecules. J Exp Med 1996; 184:913-22; PMID:9064351; http://dx.doi.org/10.1084/jem.184.3.913
   PubMed Web of Science ®Google Scholar
• Schönberg K, Sribar M, Enczmann J, Fischer JC, Uhrberg M. Analyses of HLA-C-specific KIR repertoires in donors with group A and B haplotypes suggest a ligand-instructed model of NK cell receptor acquisition. Blood 2011; 117:98-107; PMID:20935255; http://dx.doi.org/10.1182/blood-2010-03-273656
   PubMed 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 KIR3DL1: implications for patient and donor suitability for haploidentical stem cell transplantations. Blood 2008; 112:435-43; PMID:18385451; http://dx.doi.org/10.1182/blood-2008-01-132902
   PubMed Web of Science ®Google Scholar
• Hansasuta P, Dong T, Thananchai H, Willberg C, Aldemir H, Rowland-Jones S, Braud VM. Recognition of HLA-A3 and HLA-11 by KIR3DL2 is peptide-specific. Eur J Immunol 2004; 34:1673-9; PMID:15162437; http://dx.doi.org/10.1002/eji.200425089
   PubMed Web of Science ®Google Scholar
• Chewning JH, Gudme CN, Hsu KC, Selvakumar A, Dupont B. KIR2DS1-positive NK cells mediate alloresponse against the C2 HLA-KIR ligand group in vitro. J Immunol 2007; 179:854-68; PMID:17617576; http://dx.doi.org/10.4049/jimmunol.179.2.854
   PubMed Web of Science ®Google Scholar
• Katz G, Markel G, Mizrahi S, Arnon TI, Mandelboim O. Recognition of HLA-Cw4 and HLA-Cw6 by the NK cell killer cell Ig-like receptors NK cell receptor two domain short tail number 4. J Immunol 2001; 166:7260-7; PMID:11390475; http://dx.doi.org/10.4049/jimmunol.166.12.7260
   PubMed Web of Science ®Google Scholar
• Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, Biassoni R, Moretta L. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol 2001; 19:197-223; PMID:11244035; http://dx.doi.org/10.1146/annurev.immunol.19.1.197
   PubMed Web of Science ®Google Scholar
• Baychelier F, Sennepin A, Ermonval M, Dorgham K, Debré P, Vieillard V. Identification of a cellular ligand for the natural cytotoxicity receptor NKp44. Blood 2013; 122:2935-42; PMID:23958951; http://dx.doi.org/10.1182/blood-2013-03-489054
   PubMed Web of Science ®Google Scholar
• Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, Spies T. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999; 285:727-9; PMID:10426993; http://dx.doi.org/10.1126/science.285.5428.727
   PubMed Web of Science ®Google Scholar
• Cosman D, Mullberg J, Sutherland CL, Chin W, Armitage R, Fanslow W, Kubin M, Chalupny NJ. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 2001; 14:123-33; PMID:11239445; http://dx.doi.org/10.1016/S1074-7613(01)00095-4
   PubMed Web of Science ®Google Scholar
• Bottino C, Castriconi R, Pende D, Rivera P, Nanni M, Carnemolla B, Cantoni C, Grassi J, Marcenaro S, Reymond N et al. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J Exp Med 2003; 198:557-67; PMID:12913096; http://dx.doi.org/10.1084/jem.20030788
   PubMed Web of Science ®Google Scholar
• Díaz-Peña R, Blanco-Gelaz MA, López-Larrea C. KIR genes and their role in spondyloarthropathies. Adv Exp Med Biol 2009; 649:286-99; PMID:19731638; http://dx.doi.org/10.1007/978-1-4419-0298-6_22
   PubMed Web of Science ®Google Scholar
• Ahlenstiel G, Martin MP, Gao X, Carrington M, Rehermann B. Distinct KIR/HLA compound genotypes affect the kinetics of human antiviral natural killer cell responses. J Clin Invest 2008; 118:1017-26; PMID:18246204; http://dx.doi.org/10.1172/JCI32400
   PubMed Web of Science ®Google Scholar
• Purdy AK, Campbell KS. Natural killer cells and cancer: regulation by the killer cell Ig-likereceptors (KIR). Cancer Biol Ther 2009; 8:2211-20; PMID:19923897; http://dx.doi.org/10.4161/cbt.8.23.10455
   PubMed Web of Science ®Google Scholar
• Kröger N, Zabelina T, Berger J, Duske H, Klyuchnikov E, Binder T, Stübig T, Hilde-brandt Y, Atanackovic D, Alchalby H et al. Donor KIR haplotype B improves progression-free and overall survival after allogeneic hematopoietic stem cell transplantation for multiple myeloma. Leukemia 2011; 25:1657-61; PMID:21647155; http://dx.doi.org/10.1038/leu.2011.138
   PubMed Web of Science ®Google Scholar
• Legaz I, López-Álvarez MR, Campillo JA, Moya-Quiles MR, Bolarín JM, de la Peña J, Salgado G, Gimeno L, García-Alonso AM, Muro M, Miras M et al. KIR gene mismatching and KIR/C ligands in liver transplantation: consequences for short-term liver allograft injury. Transplantation 2013; 95:1037-44; PMID:23478359; http://dx.doi.org/10.1097/TP.0b013e318286486c
   PubMed Web of Science ®Google Scholar
• Chan CJ, Andrews DM, Smyth MJ. Receptors that interact with nectin and nectin-like proteins in the immunosurveillance and immunotherapy of cancer. Curr Opin Immunol 2012; 24:246-51; PMID:22285893; http://dx.doi.org/10.1016/j.coi.2012.01.009
   PubMed Web of Science ®Google Scholar
• Garrido F, Cabrera T, Concha A, Glew S, Ruiz-Cabello F, Stern PL. Natural history of HLA expression during tumour development. Immunol Today 1993; 14:491-9; PMID:8274189; http://dx.doi.org/10.1016/0167-5699(93)90264-L
   PubMedGoogle Scholar
• Garrido F, Cabrera T, Lopez-Nevot MA, Ruiz-Cabello F. HLA class I antigens in human tumors. Adv Cancer Res 1995; 67:155-95; PMID:8571814; http://dx.doi.org/10.1016/S0065-230X(08)60713-7
   PubMed Web of Science ®Google Scholar
• El-Sherbiny YM, Meade JL, Holmes TD, McGonagle D, Mackie SL, Morgan AW, Cook G, Feyler S, Richards SJ, Davies FE et al. The requirement for DNAM-1, NKG2D, and NKp46 in the natural killer cell-mediated killing of myeloma cells. Cancer Res 2007; 67:8444-9; PMID:17875681; http://dx.doi.org/10.1158/0008-5472.CAN-06-4230
   PubMed Web of Science ®Google Scholar
• Carbone E, Neri P, Mesuraca M, Fulciniti MT, Otsuki T, Pende D, Groh V, Spies T, Pollio G, Cosman D et al. HLAclass I, NKG2D, and natural cytotoxicity receptors regulate multiple myeloma cell recognition by natural killer cells. Blood 2005; 105:251-8; PMID:15328155; http://dx.doi.org/10.1182/blood-2004-04-1422
   PubMed Web of Science ®Google Scholar
• Bernal M, Garrido P Jiménez P, Carretero R, Almagro M, López P, Navarro P, Garrido F, Ruiz-Cabello F. Changes in activatory and inhibitory natural killer (NK) receptors may induce progression to multiple myeloma: implications for tumor evasion of T and NKcells. Hum Immunol 2009; 70:854-7; PMID:19580833; http://dx.doi.org/10.1016/j.humimm.2009.07.004
   PubMed Web of Science ®Google Scholar
• Perez-Andres M, Almeida J, Martin-Ayuso M, De Las Heras N, Moro MJ, Martin-Nuñez G, Galende J, Cuello R, Abuín I, Moreno I et al. Soluble and membrane levels of molecules involved in the interaction between clonal plasma cells and the immunological microenvironment in multiple myeloma and their association with the characteristics of the disease. Int J Cancer 2009; 124:367-75; PMID:19003959; http://dx.doi.org/10.1002/ijc.23941
   PubMed Web of Science ®Google Scholar
• Palumbo A, Attal M, Roussel M. Shifts in the therapeutic paradigm for patients newly diagnosed with multiple myeloma: maintenance therapy and overall survival. Clin Cancer Res 2011; 17:1253-63; PMID:21411441; http://dx.doi.org/10.1158/1078-0432.CCR-10-1925
   PubMed Web of Science ®Google Scholar
• Palumbo A, Anderson K. Multiple Myeloma. N Engl J Med 2011; 364:1046-60; PMID:21410373; http://dx.doi.org/10.1056/NEJMra1011442
   PubMed Web of Science ®Google Scholar
• Gabriel IH, Sergeant R, Szydlo R, Apperley JF, DeLavallade H, Alsuliman A, Khoder A, Marin D, Kanfer E, Cooper N et al. Interaction between KIR3DS1 and HLA-Bw4 predicts for progression-free survival after autologous stem cell transplantation in patients with multiple myeloma. Blood 2010; 116:2033-9; PMID:20562327; http://dx.doi.org/10.1182/blood-2010-03-273706
   PubMed Web of Science ®Google Scholar
• Rajkumar SV, Dimopoulos MA, Palumbo A, Blade J, Merlini G, Mateos MV, Kumar S, Hillengass J, Kastritis E, Richardson P et al. International Myeloma Working Group updated criteria for the diagnosis of multiple myeloma. Lancet Oncol 2014; 15:e538-48; PMID:25439696; http://dx.doi.org/10.1016/S1470-2045(14)70442-5
   PubMed Web of Science ®Google Scholar
• Perez-Persona E, Vidriales MB, Mateo G, García-Sanz R, Mateos MV, de Coca AG, Galende J, Martín-Nuñez G, Alonso JM, de Las Heras N et al. New criteria to identify risk of progression in monoclonal gammopathy of uncertain significance and smoldering multiple myeloma based on multiparameter flow cytometry analysis of bone marrow plasma cells. Blood 2007; 110:2586-92; PMID:17576818; http://dx.doi.org/10.1182/blood-2007-05-088443
   PubMed Web of Science ®Google Scholar
• Greipp PR, San Miguel J, Durie BG, Crowley JJ, Barlogie B, Bladé J, Boccadoro M, Child JA, Avet-Loiseau H, Kyle RA et al. International staging system for multiple myeloma. J Clin Oncol 2005; 23:3412-20; PMID:15809451; http://dx.doi.org/10.1200/JCO.2005.04.242
   PubMed Web of Science ®Google Scholar
• Cognet C, Farnarier C, Gauthier L, Frassati C, André P, Magérus-Chatinet A, Anfossi N, Rieux-Laucat F, Vivier E, Schleinitz N. Expression of the HLA-C2-specific activating killer-cell Ig-like receptor KIR2DS1 on NK and T cells. Clin Immunol 2010; 135:26-32; PMID:20093094; http://dx.doi.org/10.1016/j.clim.2009.12.009
   PubMed Web of Science ®Google Scholar
• Falco M, Romeo E, Marcenaro S, Martini S, Vitale M, Bottino C, Mingari MC, Moretta L, Moretta A, Pende D. 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; 185:433-41; PMID:20525888; http://dx.doi.org/10.4049/jimmunol.0903632
   PubMed Web of Science ®Google Scholar
• Parham P. MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol 2005; 5:201-14; PMID:15719024; http://dx.doi.org/10.1038/nri1570
   PubMed Web of Science ®Google Scholar
• Leung W. Infusions of allogeneic natural killer cells as cancer therapy. Clin Cancer Res 2014; 20:3390-400; PMID:24987108; http://dx.doi.org/10.1158/1078-0432.CCR-13-1766
   PubMed Web of Science ®Google Scholar
• Jiang W, Johnson C, Jayaraman J, Simecek N, Noble J, Moffatt MFC, Cookson WO, Trowsdale J, Traherne JA. Copy number variation leads to considerable diversity for B but not A haplotypes of the human KIR genes encoding NK cell receptors. Genome Res 2012; 22:1845-54; PMID:22948769; http://dx.doi.org/10.1101/gr.137976.112
   PubMed Web of Science ®Google Scholar
• Yu J, Heller G, Chewning J, Kim S, Yokoyama WM, Hsu KC. Hierarchy of the human natural killer cell response is determined by class and quantity of inhibitory receptors for self-HLA-B and HLA-C ligands. J Immunol 2007; 179:5977-89; PMID:17947671; http://dx.doi.org/10.4049/jimmunol.179.9.5977
   PubMed Web of Science ®Google Scholar
• Brodin P, Lakshmikanth T, Johansson S, Kärre K, Höglund P. The strength of inhibitory input during education quantitatively tunes the functional responsiveness of individual natural killer cells. Blood 2009; 113:2434-41; PMID:18974374; http://dx.doi.org/10.1182/blood-2008-05-156836
   PubMed Web of Science ®Google Scholar
• Carrega P, Pezzino G, Queirolo P, Bonaccorsi I, Falco M, Vita G, Pende D, Misefari A, Moretta A, Mingari MC et al. Susceptibility of human melanoma cells to autologous natural killer (NK) cell killing: HLA-related effector mechanisms and role of unlicensed NK cells. Plos One 2009; 4:e8132; PMID:19997637; http://dx.doi.org/10.1371/journal.pone.0008132
   PubMedGoogle Scholar
• Katodritou E, Terpos E, North J, Kottaridis P, Verrou E, Gastari V, Chadjiaggelidou C, Sivakumaran S, Jide-Banwo S, Tsirogianni M et al. Tumor-primed natural killer cells from patients with multiple myeloma lyse autologous, NK-resistant, bone marrow-derived malignant plasma cells. Am J Hematol 2011; 86:967-73; PMID:21919039; http://dx.doi.org/10.1002/ajh.22163
   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 et al. Coordinated expression of DNAM-1 and LFA-1 in educated NK cells. J Immunol 2015; 194:4518-27; PMID:25825444; http://dx.doi.org/10.4049/jimmunol.1401972
   PubMed Web of Science ®Google Scholar
• Ramsbottom KM, Hawkins ED, Shimoni R, McGrath M, Chan CJ, Russell SM, Smyth MJ, Oliaro J. Cutting edge: DNAX accessory molecule 1-deficient CD8+ T cells display immunological synapse defects that impair antitumor immunity. J Immunol 2014; 192:553-7; PMID:24337740; http://dx.doi.org/10.4049/jimmunol.1302197
   PubMed Web of Science ®Google Scholar
• Hou S, Ge K, Zheng X, Wei H, Sun R, Tian Z. CD226 protein is involved in immune synapse formation and triggers natural killer (NK) cell activation via its first extracellular domain. J Biol Chem 2014; 289:6969-77; PMID:24451371; http://dx.doi.org/10.1074/jbc.M113.498253
   PubMed Web of Science ®Google Scholar
• Harvey D, Pointon JJ, Sleator C, Meenagh A, Farrar C, Sun JY, Senitzer D, Middleton D, Brown MA, Wordsworth BP. Analysis of killer immunoglobulin-like receptor genes in ankylosing spondylitis. Ann Rheum Dis 2009; 68:595-8; PMID:19019897; http://dx.doi.org/10.1136/ard.2008.095927
   PubMed Web of Science ®Google Scholar
• Jones DC, Edgar RS, Ahmad T, Cummings JR, Jewell DP, Trowsdale J, Young NT. Killer Ig-like receptor (KIR) genotype and HLA ligand combinations in ulcerative colitis susceptibility. Genes Immun 2006; 7:576-82; PMID:16929347; http://dx.doi.org/10.1038/sj.gene.6364333
   PubMed Web of Science ®Google Scholar
• Witt CS, Dewing C, Sayer DC, Uhrberg M, Parham P, Christiansen FT. Population frequencies and putative haplotypes of the killer cell immunoglobulin-like receptor sequences and evidence for recombination. Transplantation 1999; 68:1784-9; PMID:10609957; http://dx.doi.org/10.1097/00007890-199912150-00024
   PubMed Web of Science ®Google Scholar
• Moretta L, Moretta A. Killer immunoglobulin-like receptors. Curr Opin Immunol 2004; 16:626-33; PMID:15342010; http://dx.doi.org/10.1016/j.coi.2004.07.010
   PubMed Web of Science ®Google Scholar
• Faure M, Long EO. KIR2DL4 (CD158d), an NK cell-activating receptor with inhibitory potential. J Immunol 2002; 168:6208-14; PMID:12055234; http://dx.doi.org/10.4049/jimmunol.168.12.6208
   PubMed Web of Science ®Google Scholar
• Uhrberg M, Valiante NM, Shum BP, Shilling HG, Lienert-Weidenbach K, Corliss B, Tyan D, Lanier LL, Parham P. Human diversity in killer cell inhibitory receptor genes. Immunity 1997; 7:753-63; PMID:9430221; http://dx.doi.org/10.1016/S1074-7613(00)80394-5
   PubMed Web of Science ®Google Scholar
• San Miguel JF, Almeida J, Mateo G, Bladé J, López-Berges C, Caballero D, Hernández J, Moro MJ, Fernández-Calvo J, Díaz-Mediavilla J et al. Immunophenotypic evaluation of the plasma cell compartment in multiple myeloma: a tool for comparing the efficacy of different treatment strategies and predicting outcome. Blood 2002; 99:1853-6; PMID:11861305; http://dx.doi.org/10.1182/blood.V99.5.1853
   PubMed Web of Science ®Google Scholar
• López-Alvarez MR, Martínez-Sánchez MV, Salgado-Cecilia MG, Campillo JA, Heine-Suñer D, Villar-Permuy F, Fuster JL, Bas A, Gil-Herrera J, Muro M et al. Association of monoclonal expansion of Epstein-Barr virus-negative CD158a+ NK cells secreting large amounts of gamma interferon with hemophagocytic lymphohistiocytosis. Clin Vaccine Immunol 2009; 16:142-5; PMID:19020108; http://dx.doi.org/10.1128/CVI.00358-08
   PubMed Web of Science ®Google Scholar