SLAMF7 selectively favors degranulation to promote cytotoxicity in human NK cells.


Journal

European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201

Informations de publication

Date de publication:
01 2022
Historique:
revised: 01 09 2021
received: 28 05 2021
accepted: 20 10 2021
pubmed: 26 10 2021
medline: 10 2 2022
entrez: 25 10 2021
Statut: ppublish

Résumé

NK cells play an important role in immunity by recognizing and eliminating cells undergoing infection or malignant transformation. This role is dependent on the ability of NK cells to lyse targets cells in a perforin-dependent mechanism and by secreting inflammatory cytokines. Both effector functions are controlled by several cell surface receptors. The Signaling Lymphocyte Activation Molecule (SLAM) family of receptors plays an essential role in regulating NK cell activation. Several studies have demonstrated that SLAMF7 regulates NK cell activation. However, the molecular and cellular mechanisms by which SLAMF7 influences NK effector functions are unknown. Here, we present evidence that physiological ligation of SLAMF7 in human NK cells enhances the lysis of target cells expressing SLAMF7. This effect was dependent on the ability of SLAMF7 to promote NK cell degranulation rather than cytotoxic granule polarization or cell adhesion. Moreover, SLAMF7-dependent NK cell degranulation was predominantly dependent on PLC-γ when compared to PI3K. These data provide novel information on the cellular mechanism by which SLAMF7 regulates human NK cell activation. Finally, this study supports a model for NK cell activation where activated receptors contribute by regulating specific discrete cellular events rather than multiple cellular processes.

Identifiants

pubmed: 34693521
doi: 10.1002/eji.202149406
doi:

Substances chimiques

SLAMF7 protein, human 0
Signaling Lymphocytic Activation Molecule Family 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

62-74

Subventions

Organisme : CIHR
Pays : Canada

Informations de copyright

© 2021 Wiley-VCH GmbH.

Références

Quatrini, L., Chiesa, M. D., Sivori, S., Mingari, M. C., Pende, D. and Moretta, L., Human NK cells, their receptors and function. Eur. J. Immunol. 2021.
Bryceson, Y. T., March, M. E., Ljunggren, H. G. and Long, E. O., Activation, coactivation, and costimulation of resting human natural killer cells. Immunol. Rev. 2006. 214: 73-91.
Bryceson, Y. T., March, M. E., Ljunggren, H. G. and Long, E. O., Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood. 2006. 107: 159-166.
Bryceson, Y. T., March, M. E., Barber, D. F., Ljunggren, H. G. and Long, E. O., Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J. Exp. Med. 2005. 202: 1001-1012.
Barber, D. F. and Long, E. O., Coexpression of CD58 or CD48 with intercellular adhesion molecule 1 on target cells enhances adhesion of resting NK cells. J. Immunol. 2003, 170: 294-299.
Kupfer, A., Dennert, G. and Singer, S. J., Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets. Proc Natl. Acad. Sci. USA. 1983. 80: 7224-7228.
Orange, J. S., Harris, K. E., Andzelm, M. M., Valter, M. M., Geha, R. S. and Strominger, J. L., The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc. Natl. Acad. Sci. USA. 2003. 100: 14151-14156.
Wulfing, C., Purtic, B., Klem, J. and Schatzle, J. D., Stepwise cytoskeletal polarization as a series of checkpoints in innate but not adaptive cytolytic killing. Proc. Natl. Acad. Sci. USA. 2003. 100: 7767-7772.
de Saint Basile, G., Menasche, G. and Fischer, A., Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules. Nat. Rev. Immunol. 2010. 10: 568-579.
Chen, X., Allan, D. S. J., Krzewski, K., Ge, B., Kopcow, H. and Strominger, J. L., CD28-stimulated ERK2 phosphorylation is required for polarization of the microtubule organizing center and granules in YTS NK cells. Proc. Natl. Acad. Sci. USA. 2006. 103: 10346-10351.
Veillette, A. and Latour, S., The SLAM family of immune-cell receptors. Curr. Opin. Immunol. 2003. 15: 277-285.
Veillette, A., Immune regulation by SLAM family receptors and SAP-related adaptors. Nat. Rev. Immunol. 2006. 6: 56-66.
Veillette, A., SLAM-family receptors: immune regulators with or without SAP-family adaptors. Cold Spring Harb. Perspect. Biol. 2010. 2: a002469.
Ostrakhovitch, E. A. and Li, S. S., The role of SLAM family receptors in immune cell signaling. Biochem. Cell. Biol. 2006. 84: 832-843.
Howie, D., Simarro, M., Sayos, J., Guirado, M., Sancho, J. and Terhorst, C., Molecular dissection of the signaling and costimulatory functions of CD150 (SLAM): CD150/SAP binding and CD150-mediated costimulation. Blood 2002. 99: 957-965.
Tangye, S. G., Lazetic, S., Woollatt, E., Sutherland, G. R., Lanier, L. L. and Phillips, J. H., Cutting edge: human 2B4, an activating NK cell receptor, recruits the protein tyrosine phosphatase SHP-2 and the adaptor signaling protein SAP. J. Immunol. 1999. 162: 6981-6985.
Latour, S., Gish, G., Helgason, C. D., Humphries, R. K., Pawson, T. and Veillette, A., Regulation of SLAM-mediated signal transduction by SAP, the X-linked lymphoproliferative gene product. Nat. Immunol. 2001. 2: 681-690.
Latour, S., Roncagalli, R., Chen, R., Bakinowski, M., Shi, X., Schwartzberg, P. L. et al., Binding of SAP SH2 domain to FynT SH3 domain reveals a novel mechanism of receptor signalling in immune regulation. Nat. Cell Biol. 2003. 5: 149-154.
Meinke, S. and Watzl, C., NK cell cytotoxicity mediated by 2B4 and NTB-A is dependent on SAP acting downstream of receptor phosphorylation. Front. Immunol. 2013. 4: 3.
Bloch-Queyrat, C., Fondaneche, M. C., Chen, R., Yin, L., Relouzat, F., Veillette, A. et al., Regulation of natural cytotoxicity by the adaptor SAP and the Src-related kinase Fyn. J. Exp. Med. 2005. 202: 181-192.
Dong, Z., Cruz-Munoz, M. E., Zhong, M. C., Chen, R., Latour, S. and Veillette, A., Essential function for SAP family adaptors in the surveillance of hematopoietic cells by natural killer cells. Nat. Immunol. 2009. 10: 973-980.
Cruz-Munoz, M. E., Dong, Z., Shi, X., Zhang, S. and Veillette, A., Influence of CRACC, a SLAM family receptor coupled to the adaptor EAT-2, on natural killer cell function. Nat. Immunol. 2009. 10: 297-305.
Dong, Z., Davidson, D., Perez-Quintero, L. A., Kurosaki, T., Swat, W. and 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: 974-985.
Claus, M., Meinke, S., Bhat, R. and Watzl, C., Regulation of NK cell activity by 2B4, NTB-A and CRACC. Front. Biosci. 2008. 13: 956-965.
Stark, S. and Watzl, C., 2B4 (CD244), NTB-A and CRACC (CS1) stimulate cytotoxicity but no proliferation in human NK cells. Int. Immunol. 2006. 18: 241-247.
Perez-Quintero, L. A., Roncagalli, R., Guo, H., Latour, S., Davidson, D. and Veillette, A., EAT-2, a SAP-like adaptor, controls NK cell activation through phospholipase Cgamma, Ca++, and Erk, leading to granule polarization. J. Exp. Med. 2014. 211: 727-742.
Bouchon, A., Cella, M., Grierson, H. L., Cohen, J. I. and Colonna, M., Activation of NK cell-mediated cytotoxicity by a SAP-independent receptor of the CD2 family. J. Immunol. 2001. 167: 5517-5521.
Tassi, I. and Colonna, M., The cytotoxicity receptor CRACC (CS-1) recruits EAT-2 and activates the PI3K and phospholipase Cgamma signaling pathways in human NK cells. J. Immunol. 2005. 175 7996-8002.
Johnson, D. R., Locus-specific constitutive and cytokine-induced HLA class I gene expression. J. Immunol. 2003. 170: 1894-1902.
Long, E. O., Negative signaling by inhibitory receptors: the NK cell paradigm. Immunol. Rev. 2008. 224: 70-84.
Bryceson, Y. T. and Long, E. O., Line of attack: NK cell specificity and integration of signals. Curr. Opin. Immunol. 2008. 20: 344-352.
Barber, D. F., Faure, M. and Long, E. O., LFA-1 contributes an early signal for NK cell cytotoxicity. J. Immunol. 2004. 173: 3653-3659.
Long, E. O., Kim, H. S., Liu, D., Peterson, M. E. and Rajagopalan, S., Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu. Rev. Immunol. 2013. 31: 227-258.
Bryceson, Y. T., Pende, D., Maul-Pavicic, A., Gilmour, K. C., Ufheil, H., Vraetz, T. et al., A prospective evaluation of degranulation assays in the rapid diagnosis of familial hemophagocytic syndromes. Blood 2012. 119: 2754-2763.
Lanier, L. L., NK cell recognition. Annu. Rev. Immunol. 2005. 23: 225-274.
Bryceson, Y. T., Ljunggren, H. G. and Long, E. O., Minimal requirement for induction of natural cytotoxicity and intersection of activation signals by inhibitory receptors. Blood 2009. 114: 2657-2666.
Cannons, J. L. and Tangye, S. G., Schwartzberg PL. SLAM family receptors and SAP adaptors in immunity. Annu. Rev. Immunol. 2011. 29: 665-705.
Ma, C. S., Nichols, K. E. and Tangye, S. G., Regulation of cellular and humoral immune responses by the SLAM and SAP families of molecules. Annu. Rev. Immunol. 2007. 25: 337-379.
Veillette, A., NK cell regulation by SLAM family receptors and SAP-related adapters. Immunol. Rev. 2006. 214: 22-34.
Veillette, A., Cruz-Munoz, M. E. and Zhong, M. C., SLAM family receptors and SAP-related adaptors: matters arising. Trends Immunol. 2006. 27: 228-234.
Veillette, A., SLAM Family Receptors Regulate Immunity with and without SAP-related Adaptors. J. Exp. Med. 2004. 199: 1175-1178.
Guo, H., Cranert, S. A., Lu, Y., Zhong, M. C., Zhang, S., Chen, J. et al., Deletion of Slam locus in mice reveals inhibitory role of SLAM family in NK cell responses regulated by cytokines and LFA-1. J. Exp. Med. 2016. 213: 2187-2207.
Zhao, F., Cannons, J. L., Dutta, M., Griffiths, G. M. and Schwartzberg, P. L., Positive and negative signaling through SLAM receptors regulate synapse organization and thresholds of cytolysis. Immunity 2012. 36: 1003-1016.
Cannons, J. L., Qi, H., Lu, K. T., Dutta, M., Gomez-Rodriguez, J., Cheng, J. et al., Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 2010. 32: 253-265.
Caraux, A., Kim, N., Bell, S. E., Zompi, S., Ranson, T., Lesjean-Pottier, S. et al., Phospholipase C-gamma2 is essential for NK cell cytotoxicity and innate immunity to malignant and virally infected cells. Blood 2006. 107: 994-1002.
Jiang, K., Zhong, B., Gilvary, D. L., Corliss, B. C., Hong-Geller, E., Wei, S. et al., Pivotal role of phosphoinositide-3 kinase in regulation of cytotoxicity in natural killer cells. Nat. Immunol. 2000. 1: 419-425.
Jiang, K., Zhong, B., Gilvary, D. L., Corliss, B. C., Vivier, E., Hong-Geller, E. et al., Syk regulation of phosphoinositide 3-kinase-dependent NK cell function. J. Immunol. 2002. 168: 3155-3164.
Carlin, L. M., Evans, R., Milewicz, H., Fernandes, L., Matthews, D. R., Perani, M. et al., A targeted siRNA screen identifies regulators of Cdc42 activity at the natural killer cell immunological synapse. Sci. Signal 2011. 4: ra81.
Kim, N., Saudemont, A., Webb, L., Camps, M., Ruckle, T., Hirsch, E. et al., The p110delta catalytic isoform of PI3K is a key player in NK-cell development and cytokine secretion. Blood 2007. 110: 3202-3208.
Zebedin, E., Simma, O., Schuster, C., Putz, E. M., Fajmann, S., Warsch, W. et al., Leukemic challenge unmasks a requirement for PI3Kdelta in NK cell-mediated tumor surveillance. Blood 2008. 112: 4655-4664.
Yea, S. S., So, L., Mallya, S., Lee, J., Rajasekaran, K., Malarkannan, S. et al., Effects of novel isoform-selective phosphoinositide 3-kinase inhibitors on natural killer cell function. PLoS One 2014, 9: e99486.
Guo, H., Samarakoon, A., Vanhaesebroeck, B. and Malarkannan, S., The p110 delta of PI3K plays a critical role in NK cell terminal maturation and cytokine/chemokine generation. J. Exp. Med. 2008. 205: 2419-2435.
Mace, E. M., Phosphoinositide-3-Kinase Signaling in Human Natural Killer Cells: New Insights from Primary Immunodeficiency. Front. Immunol. 2018. 9: 445.
Hsi, E. D., Steinle, R., Balasa, B., Szmania, S., Draksharapu, A., Shum, B. P. et al., CS1, a potential new therapeutic antibody target for the treatment of multiple myeloma. Clin. Cancer Res. 2008. 14: 2775-2784.
von Wenserski, L., Schultheiss, C., Bolz, S., Schliffke, S., Simnica, D., Willscher, E. et al., SLAMF receptors negatively regulate B cell receptor signaling in chronic lymphocytic leukemia via recruitment of prohibitin-2. Leukemia 2021. 35: 1073-1086.
Elmaagacli, A. H., Salwender, H., Jehn, C., Dahmash, F., Singh, A., Wilson, O. et al., Strong expression of SLAMF7 in natural killer/T-cell lymphoma and large granular lymphocyte leukemia - a prominent biomarker and potential target for anti-SLAMF7 antibody therapy. Leuk. Lymphoma 2019. 60: 3335-3338.
Cossarizza, A., Chang, H. D., Radbruch, A., Acs, A., Adam, D., Adam-Klages, S. et al., Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition). Eur. J. Immunol. 2019. 49: 1457-1973.

Auteurs

Arturo Gutierrez-Guerrero (A)

Facultad de Medicina, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, México.
Instituto de Investigación en Ciencias Básicas y Aplicadas, Mexico City, México.

Ismael Mancilla-Herrera (I)

Instituto Nacional de Perinatología, Mexico City, México.

Jose L Maravillas-Montero (JL)

Red de Apoyo a la Investigación, Universidad Nacional Autónoma de México, Mexico City, México.
Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, México.

Ivan Martinez-Duncker (I)

Centro de Investigación en Dinámica celular, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, México.

Andre Veillette (A)

Institute de Recherches Cliniques de Montréal (IRCM), Montréal, Québec, Canada.

Mario E Cruz-Munoz (ME)

Facultad de Medicina, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, México.

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