88
Views
61
CrossRef citations to date
0
Altmetric
Article

Immune Cell Inhibition by SLAMF7 Is Mediated by a Mechanism Requiring Src Kinases, CD45, and SHIP-1 That Is Defective in Multiple Myeloma Cells

, , , &
Pages 41-51 | Received 31 Aug 2014, Accepted 07 Oct 2014, Published online: 20 Mar 2023

REFERENCES

  • Veillette A, Guo H. 2013. CS1, a SLAM family receptor involved in immune regulation, is a therapeutic target in multiple myeloma. Crit Rev Oncol Hematol 88:168–177. http://dx.doi.org/10.1016/j.critrevonc.2013.04.003.
  • Bouchon A, Cella M, Grierson HL, Cohen JI, Colonna M. 2001. Activation of NK cell-mediated cytotoxicity by a SAP-independent receptor of the CD2 family. J Immunol 167:5517–5521. http://dx.doi.org/10.4049/jimmunol.167.10.5517.
  • Hsi ED, Steinle R, Balasa B, Szmania S, Draksharapu A, Shum BP, Huseni M, Powers D, Nanisetti A, Zhang Y, Rice AG, van Abbema A, Wong M, Liu G, Zhan F, Dillon M, Chen S, Rhodes S, Fuh F, Tsurushita N, Kumar S, Vexler V, Shaughnessy JD, Jr, Barlogie B, van Rhee F, Hussein M, Afar DE, Williams MB. 2008. CS1, a potential new therapeutic antibody target for the treatment of multiple myeloma. Clin Cancer Res 14:2775–2784. http://dx.doi.org/10.1158/1078-0432.CCR-07-4246.
  • Tai YT, Dillon M, Song W, Leiba M, Li XF, Burger P, Lee AI, Podar K, Hideshima T, Rice AG, van Abbema A, Jesaitis L, Caras I, Law D, Weller E, Xie W, Richardson P, Munshi NC, Mathiot C, Avet-Loiseau H, Afar DE, Anderson KC. 2008. Anti-CS1 humanized monoclonal antibody HuLuc63 inhibits myeloma cell adhesion and induces antibody-dependent cellular cytotoxicity in the bone marrow milieu. Blood 112:1329–1337. http://dx.doi.org/10.1182/blood-2007-08-107292.
  • Cruz-Munoz ME, Dong Z, Shi X, Zhang S, Veillette A. 2009. Influence of CRACC, a SLAM family receptor coupled to the adaptor EAT-2, on natural killer cell function. Nat Immunol 10:297–305. http://dx.doi.org/10.1038/ni.1693.
  • Tassi I, Colonna M. 2005. The cytotoxicity receptor CRACC (CS-1) recruits EAT-2 and activates the PI3K and phospholipase Cgamma signaling pathways in human NK cells. J Immunol 175:7996–8002. http://dx.doi.org/10.4049/jimmunol.175.12.7996.
  • Perez-Quintero LA, Roncagalli R, Guo H, Latour S, Davidson D, Veillette A. 2014. EAT-2, a SAP-like adaptor, controls NK cell activation through phospholipase Cgamma, Ca++, and Erk, leading to granule polarization. J Exp Med 211:727–742. http://dx.doi.org/10.1084/jem.20132038.
  • van Rhee F, Szmania SM, Dillon M, van Abbema AM, Li X, Stone MK, Garg TK, Shi J, Moreno-Bost AM, Yun R, Balasa B, Ganguly B, Chao D, Rice AG, Zhan F, Shaughnessy JD, Jr, Barlogie B, Yaccoby S, Afar DE. 2009. Combinatorial efficacy of anti-CS1 monoclonal antibody elotuzumab (HuLuc63) and bortezomib against multiple myeloma. Mol Cancer Ther 8:2616–2624. http://dx.doi.org/10.1158/1535-7163.MCT-09-0483.
  • Zonder JA, Mohrbacher AF, Singhal S, van Rhee F, Bensinger WI, Ding H, Fry J, Afar DE, Singhal AK. 2012. A phase 1, multicenter, open-label, dose escalation study of elotuzumab in patients with advanced multiple myeloma. Blood 120:552–559. http://dx.doi.org/10.1182/blood-2011-06-360552.
  • Jakubowiak AJ, Benson DM, Bensinger W, Siegel DS, Zimmerman TM, Mohrbacher A, Richardson PG, Afar DE, Singhal AK, Anderson KC. 2012. Phase I trial of anti-CS1 monoclonal antibody elotuzumab in combination with bortezomib in the treatment of relapsed/refractory multiple myeloma. J Clin Oncol 30:1960–1965. http://dx.doi.org/10.1200/JCO.2011.37.7069.
  • Lonial S, Vij R, Harousseau JL, Facon T, Moreau P, Mazumder A, Kaufman JL, Leleu X, Tsao LC, Westland C, Singhal AK, Jagannath S. 2012. Elotuzumab in combination with lenalidomide and low-dose dexamethasone in relapsed or refractory multiple myeloma. J Clin Oncol 30:1953–1959. http://dx.doi.org/10.1200/JCO.2011.37.2649.
  • Lonial S, Kaufman J, Laubach J, Richardson P. 2013. Elotuzumab: a novel anti-CS1 monoclonal antibody for the treatment of multiple myeloma. Expert Opin Biol Ther 13:1731–1740. http://dx.doi.org/10.1517/14712598.2013.847919.
  • Collins SM, Bakan CE, Swartzel GD, Hofmeister CC, Efebera YA, Kwon H, Starling GC, Ciarlariello D, Bhaskar S, Briercheck EL, Hughes T, Yu J, Rice A, Benson DM, Jr. 2013. Elotuzumab directly enhances NK cell cytotoxicity against myeloma via CS1 ligation: evidence for augmented NK cell function complementing ADCC. Cancer Immunol Immunother 62:1841–1849. http://dx.doi.org/10.1007/s00262-013-1493-8.
  • Roncagalli R, Taylor JE, Zhang S, Shi X, Chen R, Cruz-Munoz ME, Yin L, Latour S, Veillette A. 2005. Negative regulation of natural killer cell function by EAT-2, a SAP-related adaptor. Nat Immunol 6:1002–1010. http://dx.doi.org/10.1038/ni1242.
  • Dong Z, Davidson D, Perez-Quintero LA, Kurosaki T, Swat W, Veillette A. 2012. The adaptor SAP controls NK cell activation by regulating the enzymes Vav-1 and SHIP-1 and by enhancing conjugates with target cells. Immunity 36:974–985. http://dx.doi.org/10.1016/j.immuni.2012.03.023.
  • Weber M, Treanor B, Depoil D, Shinohara H, Harwood NE, Hikida M, Kurosaki T, Batista FD. 2008. Phospholipase C-gamma2 and Vav cooperate within signaling microclusters to propagate B cell spreading in response to membrane-bound antigen. J Exp Med 205:853–868. http://dx.doi.org/10.1084/jem.20072619.
  • Dong Z, Cruz-Munoz ME, Zhong MC, Chen R, Latour S, Veillette A. 2009. Essential function for SAP family adaptors in the surveillance of hematopoietic cells by natural killer cells. Nat Immunol 10:973–980. http://dx.doi.org/10.1038/ni.1763.
  • Desai DM, Sap J, Schlessinger J, Weiss A. 1993. Ligand-mediated negative regulation of a chimeric transmembrane receptor tyrosine phosphatase. Cell 73:541–554. http://dx.doi.org/10.1016/0092-8674(93)90141-C.
  • Latour S, Fournel M, Veillette A. 1997. Regulation of T-cell antigen receptor signalling by Syk tyrosine protein kinase. Mol Cell Biol 17:4434–4441.
  • Fuchs A, Cella M, Giurisato E, Shaw AS, Colonna M. 2004. Cutting edge: CD96 (tactile) promotes NK cell-target cell adhesion by interacting with the poliovirus receptor (CD155). J Immunol 172:3994–3998. http://dx.doi.org/10.4049/jimmunol.172.7.3994.
  • Veillette A, Bookman MA, Horak EM, Bolen JB. 1988. The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck. Cell 55:301–308. http://dx.doi.org/10.1016/0092-8674(88)90053-0.
  • Lee JK, Boles KS, Mathew PA. 2004. Molecular and functional characterization of a CS1 (CRACC) splice variant expressed in human NK cells that does not contain immunoreceptor tyrosine-based switch motifs. Eur J Immunol 34:2791–2799. http://dx.doi.org/10.1002/eji.200424917.
  • Veillette A. 2010. SLAM-family receptors: immune regulators with or without SAP-family adaptors. Cold Spring Harb Perspect Biol 2:a002469. http://dx.doi.org/10.1101/cshperspect.a002469.
  • Cannons JL, Tangye SG, Schwartzberg PL. 2011. SLAM family receptors and SAP adaptors in immunity. Annu Rev Immunol 29:665–705. http://dx.doi.org/10.1146/annurev-immunol-030409-101302.
  • Veillette A, Latour S. 2003. The SLAM family of immune-cell receptors. Curr Opin Immunol 15:277–285. http://dx.doi.org/10.1016/S0952-7915(03)00041-4.
  • Sayos J, Martin M, Chen A, Simarro M, Howie D, Morra M, Engel P, Terhorst C. 2001. Cell surface receptors Ly-9 and CD84 recruit the X-linked lymphoproliferative disease gene product SAP. Blood 97:3867–3874. http://dx.doi.org/10.1182/blood.V97.12.3867.
  • Galandrini R, Tassi I, Mattia G, Lenti L, Piccoli M, Frati L, Santoni A. 2002. SH2-containing inositol phosphatase (SHIP-1) transiently translocates to raft domains and modulates CD16-mediated cytotoxicity in human NK cells. Blood 100:4581–4589. http://dx.doi.org/10.1182/blood-2002-04-1058.
  • Banh C, Miah SM, Kerr WG, Brossay L. 2012. Mouse natural killer cell development and maturation are differentially regulated by SHIP-1. Blood 120:4583–4590. http://dx.doi.org/10.1182/blood-2012-04-425009.
  • Kurosaki T. 1999. Genetic analysis of B cell antigen receptor signaling. Annu Rev Immunol 17:555–592. http://dx.doi.org/10.1146/annurev.immunol.17.1.555.
  • Lee JK, Mathew SO, Vaidya SV, Kumaresan PR, Mathew PA. 2007. CS1 (CRACC, CD319) induces proliferation and autocrine cytokine expression on human B lymphocytes. J Immunol 179:4672–4678. http://dx.doi.org/10.4049/jimmunol.179.7.4672.
  • Kim JR, Mathew SO, Patel RK, Pertusi RM, Mathew PA. 2010. Altered expression of signalling lymphocyte activation molecule (SLAM) family receptors CS1 (CD319) and 2B4 (CD244) in patients with systemic lupus erythematosus. Clin Exp Immunol 160:348–358. http://dx.doi.org/10.1111/j.1365-2249.2010.04116.x.
  • Shrivastava P, Katagiri T, Ogimoto M, Mizuno K, Yakura H. 2004. Dynamic regulation of Src-family kinases by CD45 in B cells. Blood 103:1425–1432. http://dx.doi.org/10.1182/blood-2003-03-0716.
  • Zhu JW, Brdicka T, Katsumoto TR, Lin J, Weiss A. 2008. Structurally distinct phosphatases CD45 and CD148 both regulate B cell and macrophage immunoreceptor signaling. Immunity 28:183–196. http://dx.doi.org/10.1016/j.immuni.2007.11.024.
  • Rhee I, Veillette A. 2012. Protein tyrosine phosphatases in lymphocyte activation and autoimmunity. Nat Immunol 13:439–447. http://dx.doi.org/10.1038/ni.2246.
  • Hesslein DG, Takaki R, Hermiston ML, Weiss A, Lanier LL. 2006. Dysregulation of signaling pathways in CD45-deficient NK cells leads to differentially regulated cytotoxicity and cytokine production. Proc Natl Acad Sci U S A 103:7012–7017. http://dx.doi.org/10.1073/pnas.0601851103.
  • Martin SM, Mehta IK, Yokoyama WM, Thomas ML, Lorenz RG. 2001. Development of intestinal intraepithelial lymphocytes, NK cells, and NK 11+ T cells in CD45-deficient mice. J Immunol 166:6066–6073. http://dx.doi.org/10.4049/jimmunol.166.10.6066.
  • Yamada H, Kishihara K, Kong YY, Nomoto K. 1996. Enhanced generation of NK cells with intact cytotoxic function in CD45 exon 6-deficient mice. J Immunol 157:1523–1528.
  • Lakshmikanth T, Burke S, Ali TH, Kimpfler S, Ursini F, Ruggeri L, Capanni M, Umansky V, Paschen A, Sucker A, Pende D, Groh V, Biassoni R, Hoglund P, Kato M, Shibuya K, Schadendorf D, Anichini A, Ferrone S, Velardi A, Karre K, Shibuya A, Carbone E, Colucci F. 2009. NCRs and DNAM-1 mediate NK cell recognition and lysis of human and mouse melanoma cell lines in vitro and in vivo. J Clin Invest 119:1251–1263. http://dx.doi.org/10.1172/JCI36022.
  • Gilfillan S, Chan CJ, Cella M, Haynes NM, Rapaport AS, Boles KS, Andrews DM, Smyth MJ, Colonna M. 2008. DNAM-1 promotes activation of cytotoxic lymphocytes by nonprofessional antigen-presenting cells and tumors. J Exp Med 205:2965–2973. http://dx.doi.org/10.1084/jem.20081752.
  • Iguchi-Manaka A, Kai H, Yamashita Y, Shibata K, Tahara-Hanaoka S, Honda S, Yasui T, Kikutani H, Shibuya K, Shibuya A. 2008. Accelerated tumor growth in mice deficient in DNAM-1 receptor. J Exp Med 205:2959–2964. http://dx.doi.org/10.1084/jem.20081611.
  • Kageyama R, Cannons JL, Zhao F, Yusuf I, Lao C, Locci M, Schwartzberg PL, Crotty S. 2012. The receptor Ly108 functions as a SAP adaptor-dependent on-off switch for T cell help to B cells and NKT cell development. Immunity 36:986–1002. http://dx.doi.org/10.1016/j.immuni.2012.05.016.
  • Zhao F, Cannons JL, Dutta M, Griffiths GM, Schwartzberg PL. 2012. Positive and negative signaling through SLAM receptors regulate synapse organization and thresholds of cytolysis. Immunity 36:1003–1016. http://dx.doi.org/10.1016/j.immuni.2012.05.017.
  • Kumar S, Rajkumar SV, Kimlinger T, Greipp PR, Witzig TE. 2005. CD45 expression by bone marrow plasma cells in multiple myeloma: clinical and biological correlations. Leukemia 19:1466–1470. http://dx.doi.org/10.1038/sj.leu.2403823.
  • Moreau P, Robillard N, Avet-Loiseau H, Pineau D, Morineau N, Milpied N, Harousseau JL, Bataille R. 2004. Patients with CD45 negative multiple myeloma receiving high-dose therapy have a shorter survival than those with CD45 positive multiple myeloma. Haematologica 89:547–551.
  • Pellat-Deceunynck C, Bataille R. 2004. Normal and malignant human plasma cells: proliferation, differentiation, and expansions in relation to CD45 expression. Blood Cells Mol Dis 32:293–301. http://dx.doi.org/10.1016/j.bcmd.2003.12.001.
  • Kim D, Park CY, Medeiros BC, Weissman IL. 2012. CD19−CD45low/−CD38high/CD138+ plasma cells enrich for human tumorigenic myeloma cells. Leukemia 26:2530–2537. http://dx.doi.org/10.1038/leu.2012.140.
  • Descamps G, Pellat-Deceunynck C, Szpak Y, Bataille R, Robillard N, Amiot M. 2004. The magnitude of Akt/phosphatidylinositol 3′-kinase proliferating signaling is related to CD45 expression in human myeloma cells. J Immunol 173:4953–4959. http://dx.doi.org/10.4049/jimmunol.173.8.4953.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.