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Review

Novel anti-myeloma immunotherapies targeting the SLAM family of receptors

, , & , MD, Director
Article: e1308618 | Received 08 Feb 2017, Accepted 13 Mar 2017, Published online: 08 May 2017

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin 2016; 66(1):7-30; PMID:26742998; https://doi.org/10.3322/caac.21332
  • Stefanova I, Horejsí V, Ansotegui IJ, Knapp W, Stockinger H. GPI-anchored cell-surface molecules complexed to protein tyrosine kinases. Science 1991; 254(5034):1016-9; PMID:1719635; https://doi.org/10.1126/science.1719635
  • Wu N, Veillette A. SLAM family receptors in normal immunity and immune pathologies. Curr Opin Immunol 2016; 38:45-51; PMID:26682762; https://doi.org/10.1016/j.coi.2015.11.003
  • Lonial S, Vij R, Harousseau JL, Facon T, Moreau P, Mazumder A, Kaufman JL, Leleu X, Tsao LC, Westland C et al. Elotuzumab in combination with lenalidomide and low-dose dexamethasone in relapsed or refractory multiple myeloma. J Clin Oncol 2012; 30(16):1953-9; PMID:22547589; https://doi.org/10.1200/JCO.2011.37.2649
  • Cannons JL, Tangye SG, Schwartzberg PL. SLAM family receptors and SAP adaptors in immunity. Annu Rev Immunol 2011; 29:665-705; PMID:21219180; https://doi.org/10.1146/annurev-immunol-030409-101302
  • Latchman Y, McKay PF, Reiser H. Identification of the 2B4 molecule as a counter-receptor for CD48. J Immunol 1998; 161(11):5809-12; PMID:9834056
  • Brown MH, Boles K, van der Merwe PA, Kumar V, Mathew PA, Barclay AN. 2B4, the natural killer and T cell immunoglobulin superfamily surface protein, is a ligand for CD48. J Exp Med 1998; 188(11):2083-90; PMID:9841922; https://doi.org/10.1084/jem.188.11.2083
  • Dong Z, Davidson D, Pérez-Quintero LA, Kurosaki T, Swat W, Veillette A. The adaptor SAP controls NK cell activation by regulating the enzymes Vav-1 and SHIP-1 and by enhancing conjugates with target cells. Immunity 2012; 36(6):974-85; PMID:22683124; https://doi.org/10.1016/j.immuni.2012.03.023
  • Martin M, Del Valle JM, Saborit I, Engel P. Identification of Grb2 as a novel binding partner of the signaling lymphocytic activation molecule-associated protein binding receptor CD229. J Immunol 2005; 174(10):5977-86; PMID:15879090; https://doi.org/10.4049/jimmunol.174.10.5977
  • Abadia-Molina AC, Ji H, Faubion WA, Julien A, Latchman Y, Yagita H, Sharpe A, Bhan AK, Terhorst C. CD48 controls T-cell and antigen-presenting cell functions in experimental colitis. Gastroenterology 2006; 130(2):424-34; PMID:16472597; https://doi.org/10.1053/j.gastro.2005.12.009
  • Raziorrouh B, Schraut W, Gerlach T, Nowack D, Grüner NH, Ulsenheimer A, Zachoval R, Wächtler M, Spannagl M, Haas J et al. The immunoregulatory role of CD244 in chronic hepatitis B infection and its inhibitory potential on virus-specific CD8+ T-cell function. Hepatology 2010; 52(6):1934-47; PMID:21064032; https://doi.org/10.1002/hep.23936
  • Hosen N, Ichihara H, Mugitani A, Aoyama Y, Fukuda Y, Kishida S, Matsuoka Y, Nakajima H, Kawakami M, Yamagami T et al. CD48 as a novel molecular target for antibody therapy in multiple myeloma. Br J Haematol 2012; 156(2):213-24; PMID:22098460; https://doi.org/10.1111/j.1365-2141.2011.08941.x
  • Nakajima H, Cella M, Langen H, Friedlein A, Colonna M. Activating interactions in human NK cell recognition: the role of 2B4-CD48. Eur J Immunol 1999; 29(5):1676-83; PMID:10359122; https://doi.org/10.1002/(SICI)1521-4141(199905)29:05%3c1676::AID-IMMU1676%3e3.0.CO;2-Y
  • McNerney ME, Guzior D, Kumar V. 2B4 (CD244)-CD48 interactions provide a novel MHC class I-independent system for NK-cell self-tolerance in mice. Blood 2005; 106(4):1337-40; PMID:15870174; https://doi.org/10.1182/blood-2005-01-0357
  • Lee KM, Forman JP, McNerney ME, Stepp S, Kuppireddi S, Guzior D, Latchman YE, Sayegh MH, Yagita H, Park CK, Oh SB et al. Requirement of homotypic NK-cell interactions through 2B4(CD244)/CD48 in the generation of NK effector functions. Blood 2006; 107(8):3181-8; PMID:15905190; https://doi.org/10.1182/blood-2005-01-0185
  • Yang B, Wang X, Jiang J, Cheng X. Involvement of CD244 in regulating CD4+ T cell immunity in patients with active tuberculosis. PLoS One 2013; 8(4):e63261; PMID:23638187; https://doi.org/10.1371/journal.pone.0063261
  • Fauriat C, Mallet F, Olive D, Costello RT. Impaired activating receptor expression pattern in natural killer cells from patients with multiple myeloma. Leukemia 2006; 20(4):732-3; PMID:16437151; https://doi.org/10.1038/sj.leu.2404096
  • Costello RT, Boehrer A, Sanchez C, Mercier D, Baier C, Le Treut T, Sébahoun G. Differential expression of natural killer cell activating receptors in blood versus bone marrow in patients with monoclonal gammopathy. Immunology 2013; 139(3):338-41; PMID:23360454; https://doi.org/10.1111/imm.12082
  • de la Fuente MA, Tovar V, Villamor N, Zapater N, Pizcueta P, Campo E, Bosch J, Engel P. Molecular characterization and expression of a novel human leukocyte cell-surface marker homologous to mouse Ly-9. Blood 2001; 97(11):3513-20; PMID:11369645; https://doi.org/10.1182/blood.V97.11.3513
  • Graham DB, Bell MP, McCausland MM, Huntoon CJ, van Deursen J, Faubion WA, Crotty S, McKean DJ. Ly9 (CD229)-deficient mice exhibit T cell defects yet do not share several phenotypic characteristics associated with SLAM- and SAP-deficient mice. J Immunol 2006; 176(1):291-300; PMID:16365421; https://doi.org/10.4049/jimmunol.176.1.291
  • Del Valle JM, Engel P, Martin M. The cell surface expression of SAP-binding receptor CD229 is regulated via its interaction with clathrin-associated adaptor complex 2 (AP-2). J Biol Chem 2003; 278(19):17430-7; PMID:12621057; https://doi.org/10.1074/jbc.M301569200
  • Sintes J, Cuenca M, Romero X, Bastos R, Terhorst C, Angulo A, Engel P. Cutting edge: Ly9 (CD229), a SLAM family receptor, negatively regulates the development of thymic innate memory-like CD8+ T and invariant NKT cells. J Immunol 2013; 190(1):21-6; PMID:23225888; https://doi.org/10.4049/jimmunol.1202435
  • Cuenca M, Romero X, Sintes J, Terhorst C, Engel P. Targeting of Ly9 (CD229) Disrupts Marginal Zone and B1 B Cell Homeostasis and Antibody Responses. J Immunol 2016; 196(2):726-37; PMID:26667173; https://doi.org/10.4049/jimmunol.1501266
  • Yousef S, Kovacsovics-Bankowski M, Salama ME, Bhardwaj N, Steinbach M, Langemo A, Kovacsovics T, Marvin J, Binder M, Panse J et al. CD229 is expressed on the surface of plasma cells carrying an aberrant phenotype and chemotherapy-resistant precursor cells in multiple myeloma. Hum Vaccine Immunother 2015; 11(7):1606-11; PMID:26001047; https://doi.org/10.1080/21645515.2015.1046658
  • Chaidos A, Barnes CP, Cowan G, May PC, Melo V, Hatjiharissi E, Papaioannou M, Harrington H, Doolittle H, Terpos E et al. Clinical drug resistance linked to interconvertible phenotypic and functional states of tumor-propagating cells in multiple myeloma. Blood 2013; 121(2):318-28; PMID:23169779; https://doi.org/10.1182/blood-2012-06-436220
  • Yamada A,   HT, Ishibashi M, Isoda A et al. Expression and function of SLAM family molecule SLAMF3 (CD229) in myeloma. In: Proceedings of the 15th International Myeloma Workshop, 2015 ; Clinical Lymphoma, Myeloma and Leukemia; Volume 15:e242
  • Carulli G, Buda G, Azzarà A, Ciancia EM, Sammuri P, Domenichini C, Guerri V, Petrini M. CD229 expression on bone marrow plasma cells from patients with multiple myeloma and monoclonal gammopathies of uncertain significance. Acta Haematol 2016; 135(1):11-4; PMID:26303094; https://doi.org/10.1159/000380939
  • Atanackovic D, Panse J, Hildebrandt Y, Jadczak A, Kobold S, Cao Y, Templin J, Meyer S, Reinhard H, Bartels K et al. Surface molecule CD229 as a novel target for the diagnosis and treatment of multiple myeloma. Haematologica 2011; 96(10):1512-20; PMID:21606160; https://doi.org/10.3324/haematol.2010.036814
  • Valdez PA, Wang H, Seshasayee D, van Lookeren Campagne M, Gurney A, Lee WP, Grewal IS. NTB-A, a new activating receptor in T cells that regulates autoimmune disease. J Biol Chem 2004; 279(18):18662-9; PMID:14988414; https://doi.org/10.1074/jbc.M312313200
  • Stark S, Watzl C. 2B4 (CD244), NTB-A and CRACC (CS1) stimulate cytotoxicity but no proliferation in human NK cells. Int Immunol 2006; 18(2):241-7; PMID:16410313; https://doi.org/10.1093/intimm/dxh358
  • Tim Lewis DJO, Gordon KA, Sandall SL, Miyamoto J, Westendorf L, Linares G, Leiske C, Kostner H, Stone I, Anderson M et al. Abstract 1195: SGN-CD352A: A novel humanized anti-CD352 antibody-drug conjugate for the treatment of multiple myeloma. In Proceedings of AACR 107th Annual Meeting, 2016.
  • Kim JR, Mathew SO, Patel RK, Pertusi RM, Mathew PA. Altered expression of signalling lymphocyte activation molecule (SLAM) family receptors CS1 (CD319) and 2B4 (CD244) in patients with systemic lupus erythematosus. Clin Exp Immunol 2010; 160(3):348-58; PMID:20345977; https://doi.org/10.1111/j.1365-2249.2010.04116.x
  • Cruz-Munoz ME, Dong Z, Shi X, Zhang S, Veillette A. Influence of CRACC, a SLAM family receptor coupled to the adaptor EAT-2, on natural killer cell function. Nat Immunol 2009; 10(3):297-305; PMID:19151721; https://doi.org/10.1038/ni.1693
  • Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 2004; 101(16):6062-7; PMID:15075390; https://doi.org/10.1073/pnas.0400782101
  • Tai YT, Dillon M, Song W, Leiba M, Li XF, Burger P, Lee AI, Podar K, Hideshima T, Rice AG et al. Anti-CS1 humanized monoclonal antibody HuLuc63 inhibits myeloma cell adhesion and induces antibody-dependent cellular cytotoxicity in the bone marrow milieu. Blood 2008; 112(4):1329-37; PMID:17906076; https://doi.org/10.1182/blood-2007-08-107292
  • Hsi ED, Steinle R, Balasa B, Szmania S, Draksharapu A, Shum BP, Huseni M, Powers D, Nanisetti A, Zhang Y et al. CS1, a potential new therapeutic antibody target for the treatment of multiple myeloma. Clin Cancer Res 2008; 14(9):2775-84; PMID:18451245; https://doi.org/10.1158/1078-0432.CCR-07-4246
  • Collins SM, Bakan CE, Swartzel GD, Hofmeister CC, Efebera YA, Kwon H, Starling GC, Ciarlariello D, Bhaskar S, Briercheck EL et al. Elotuzumab directly enhances NK cell cytotoxicity against myeloma via CS1 ligation: evidence for augmented NK cell function complementing ADCC. Cancer Immunol Immunother 2013; 62(12):1841-9; PMID:24162108; https://doi.org/10.1007/s00262-013-1493-8
  • Zonder JA, Mohrbacher AF, Singhal S, van Rhee F, Bensinger WI, Ding H, Fry J, Afar DE, Singhal AK. A phase 1, multicenter, open-label, dose escalation study of elotuzumab in patients with advanced multiple myeloma. Blood 2012; 120(3):552-9; PMID:22184404; https://doi.org/10.1182/blood-2011-06-360552
  • van Rhee F, Szmania SM, Dillon M, van Abbema AM, Li X, Stone MK, Garg TK, Shi J, Moreno-Bost AM, Yun R et al. Combinatorial efficacy of anti-CS1 monoclonal antibody elotuzumab (HuLuc63) and bortezomib against multiple myeloma. Mol Cancer Ther 2009; 8(9):2616-24; PMID:19723891; https://doi.org/10.1158/1535-7163.MCT-09-0483
  • Jakubowiak AJ, Benson DM, Bensinger W, Siegel DS, Zimmerman TM, Mohrbacher A, Richardson PG, Afar DE, Singhal AK, Anderson KC. Phase I trial of anti-CS1 monoclonal antibody elotuzumab in combination with bortezomib in the treatment of relapsed/refractory multiple myeloma. J Clin Oncol 2012; 30(16):1960-5; PMID:22291084; https://doi.org/10.1200/JCO.2011.37.7069
  • Jakubowiak A, Offidani M, Pégourie B, De La Rubia J, Garderet L, Laribi K, Bosi A, Marasca R, Laubach J, Mohrbacher A et al. Randomized phase 2 study: elotuzumab plus bortezomib/dexamethasone vs bortezomib/dexamethasone for relapsed/refractory MM. Blood 2016; 127(23):2833-40; PMID:27091875; https://doi.org/10.1182/blood-2016-01-694604
  • Lonial S, Dimopoulos M, Palumbo A, White D, Grosicki S, Spicka I, Walter-Croneck A, Moreau P, Mateos MV, Magen H et al. Elotuzumab therapy for relapsed or refractory multiple myeloma. N Engl J Med 2015; 373(7):621-31; PMID:26035255; https://doi.org/10.1056/NEJMoa1505654
  • Mateos MV, Granell M, Oriol A, Martinez-Lopez J, Blade J, Hernandez MT, Martín J, Gironella M, Lynch M, Bleickardt E et al. Elotuzumab in combination with thalidomide and low-dose dexamethasone: a phase 2 single-arm safety study in patients with relapsed/refractory multiple myeloma. Br J Haematol 2016; 175(3):448-56; PMID:27434748; https://doi.org/10.1111/bjh.14263
  • Chu J, He S, Deng Y, Zhang J, Peng Y, Hughes T, Yi L, Kwon CH, Wang QE, Devine SM et al. Genetic modification of T cells redirected toward CS1 enhances eradication of myeloma cells. Clin Cancer Res 2014; 20(15):3989-4000; PMID:24677374; https://doi.org/10.1158/1078-0432.CCR-13-2510
  • Chu J, Deng Y, Benson DM, He S, Hughes T, Zhang J, Peng Y, Mao H, Yi L, Ghoshal K et al. CS1-specific chimeric antigen receptor (CAR)-engineered natural killer cells enhance in vitro and in vivo antitumor activity against human multiple myeloma. Leukemia 2014; 28(4):917-27; PMID:24067492; https://doi.org/10.1038/leu.2013.279
  • Sophia Danhof TG, Koch S, Schreder M, Knop S, Einsele H, Hudecek M. CAR-engineered T cells specific for the elotuzumab target SLAMF7 eliminate primary myeloma cells and confer selective fratricide of SLAMF7+ normal lymphocyte subsets. Blood 2015; 126:115.
  • Bae J, Song W, Smith R, Daley J, Tai YT, Anderson KC, Munshi NC. A novel immunogenic CS1-specific peptide inducing antigen-specific cytotoxic T lymphocytes targeting multiple myeloma. Br J Haematol 2012; 157(6):687-701; PMID:22533610; https://doi.org/10.1111/j.1365-2141.2012.09111.x
  • Wang N, Morra M, Wu C, Gullo C, Howie D, Coyle T, Engel P, Terhorst  . CD150 is a member of a family of genes that encode glycoproteins on the surface of hematopoietic cells. Immunogenetics 2001; 53(5):382-94; PMID:11486275; https://doi.org/10.1007/s002510100337
  • Schoenhals M, Frecha C, Bruyer A, Caraux A, Veyrune JL, Jourdan M, Moreaux J, Cosset FL, Verhoeyen E, Klein B. Efficient transduction of healthy and malignant plasma cells by lentiviral vectors pseudotyped with measles virus glycoproteins. Leukemia 2012; 26(7):1663-70; PMID:22318450; https://doi.org/10.1038/leu.2012.36
  • Gordiienko IM, Shlapatska LM, Kovalevska LM, Sidorenko SP. Differential expression of CD150/SLAMF1 in normal and malignant B cells on the different stages of maturation. Exp Oncol 2016; 38(2):101-7; PMID:27356578
  • Zaiss M, Hirtreiter C, Rehli M, Rehm A, Kunz-Schughart LA, Andreesen R, Hennemann B. CD84 expression on human hematopoietic progenitor cells. Exp Hematol 2003; 31(9):798-805; PMID:12962726; https://doi.org/10.1016/S0301-472X(03)00187-5
  • Sintes J, Romero X, Marin P, Terhorst C, Engel P. Differential expression of CD150 (SLAM) family receptors by human hematopoietic stem and progenitor cells. Exp Hematol 2008; 36(9):1199-204; PMID:18495325; https://doi.org/10.1016/j.exphem.2008.03.015
  • Tangye SG, van de Weerdt BC, Avery DT, Hodgkin PD. CD84 is up-regulated on a major population of human memory B cells and recruits the SH2 domain containing proteins SAP and EAT-2. Eur J Immunol 2002; 32(6):1640-9; PMID:12115647; https://doi.org/10.1002/1521-4141(200206)32:6%3c1640::AID-IMMU1640%3e3.0.CO;2-S
  • Cannons JL, Qi H, Lu KT, Dutta M, Gomez-Rodriguez J, Cheng J, Wakeland EK, Germain RN, Schwartzberg PL. Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 2010; 32(2):253-65; PMID:20153220; https://doi.org/10.1016/j.immuni.2010.01.010
  • De Salort J, Sintes J, Llinàs L, Matesanz-Isabel J, Engel P. Expression of SLAM (CD150) cell-surface receptors on human B-cell subsets: from pro-B to plasma cells. Immunol Lett 2011; 134(2):129-36; PMID:20933013; https://doi.org/10.1016/j.imlet.2010.09.021
  • Kingsbury GA, Feeney LA, Nong Y, Calandra SA, Murphy CJ, Corcoran JM, Wang Y, Prabhu Das MR, Busfield SJ et al. Cloning, expression, and function of BLAME, a novel member of the CD2 family. J Immunol 2001; 166(9):5675-80; PMID:11313408; https://doi.org/10.4049/jimmunol.166.9.5675
  • Wang G, van Driel BJ, Liao G, O'Keeffe MS, Halibozek PJ, Flipse J, Yigit B, Azcutia V, Luscinskas FW, Wang N et al. Migration of myeloid cells during inflammation is differentially regulated by the cell surface receptors Slamf1 and Slamf8. PLoS One 2015; 10(3):e0121968; PMID:25799045; https://doi.org/10.1371/journal.pone.0121968
  • Llinas L, Lázaro A, de Salort J, Matesanz-Isabel J, Sintes J, Engel P. Expression profiles of novel cell surface molecules on B-cell subsets and plasma cells as analyzed by flow cytometry. Immunol Lett 2011; 134(2):113-21; PMID:20951740; https://doi.org/10.1016/j.imlet.2010.10.009
  • Zhang W, Wan T, Li N, Yuan Z, He L, Zhu X, Yu M, Cao X. Genetic approach to insight into the immunobiology of human dendritic cells and identification of CD84-H1, a novel CD84 homologue. Clin Cancer Res 2001; 7(3 Suppl):822s-829s; PMID:11300479

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