Shedding of CD16 disassembles the NK cell immune synapse and boosts serial engagement of target cells

Journal of Cell Biology

Volumn 217, Issue 9, 2018, Pages 3267-3283

  Srpan, Katja ^a   Ambrose, Ashley ^a   Karampatzakis, Alexandros ^a   Saeed, Mezida ^a   Cartwright, Adam N R ^a   Guldevall, Karolin ^b   De Matos, Gabriela Dos Santos Cruz ^c   Önfelt, Björn ^b,d   Davis, Daniel M ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^c GLAXOSMITHKLINE   (United Kingdom)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; FCGR3B PROTEIN, HUMAN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; IMMUNOLOGICAL ANTINEOPLASTIC AGENT; KLRK1 PROTEIN, HUMAN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K; PERFORIN; RITUXIMAB;

CELL MOTION; CYTOLOGY; CYTOTOXICITY; DEGRANULATION; GENETICS; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; NATURAL KILLER CELL; NEOPLASM; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, IMMUNOLOGICAL; CELL DEGRANULATION; CELL LINE, TUMOR; CELL MOVEMENT; CYTOTOXICITY, IMMUNOLOGIC; GPI-LINKED PROTEINS; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; NEOPLASMS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; PERFORIN; RECEPTORS, IGG; RITUXIMAB;

EID: 85054612246     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201712085     Document Type: Article

References (47)

1. Bhat, R., and C. Watzl. 2007. Serial killing of tumor cells by human natural killer cells-enhancement by therapeutic antibodies. PLoS One. 2:e326. https://doi.org/10.1371/journal.pone.0000326
2. Bi, J., and Z. Tian. 2017. NK Cell Exhaustion. Front. Immunol. 8:760. https://doi.org/10.3389/fimmu.2017.00760
3. Carisey, A.F., E.M. Mace, M.B. Saeed, D.M. Davis, and J.S. Orange. 2018. Nanoscale Dynamism of Actin Enables Secretory Function in Cytolytic Cells. Curr. Biol. 28:489-502.
4. Cartwright, A.N., J. Griggs, and D.M. Davis. 2014. The immune synapse clears and excludes molecules above a size threshold. Nat. Commun. 5:5479. https://doi.org/10.1038/ncomms6479
5. Cerboni, C., M. Ardolino, A. Santoni, and A. Zingoni. 2009. Detuning CD8+ T lymphocytes by down-regulation of the activating receptor NKG2D: role of NKG2D ligands released by activated T cells. Blood. 113:2955-2964. https://doi.org/10.1182/blood -2008-06-165944
6. Cheson, B.D., and J.P. Leonard. 2008. Monoclonal antibody therapy for B-cell non-Hodgkin's lymphoma. N. Engl. J. Med. 359:613-626. https://doi.org/10.1056/NEJMra0708875
7. Choi, P.J., and T.J. Mitchison. 2013. Imaging burst kinetics and spatial coordination during serial killing by single natural killer cells. Proc. Natl. Acad. Sci. USA. 110:6488-6493. https://doi.org/10.1073/pnas.1221312110
8. Clynes, R.A., T.L. Towers, L.G. Presta, and J.V. Ravetch. 2000. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat. Med. 6:443-446. https://doi.org/10.1038/74704
9. Costello, R.T., S. Sivori, E. Marcenaro, M. Lafage-Pochitaloff, M.-J. Mozziconacci, D. Reviron, J.-A. Gastaut, D. Pende, D. Olive, and A. Moretta. 2002. Defective expression and function of natural killer cell-triggering receptors in patients with acute myeloid leukemia. Blood. 99:3661-3667. https://doi.org/10.1182/blood.V99.10.3661
10. Coudert, J.D., J. Zimmer, E. Tomasello, M. Cebecauer, M. Colonna, E. Vivier, and W. Held. 2005. Altered NKG2D function in NK cells induced by chronic exposure to NKG2D ligand-expressing tumor cells. Blood. 106:1711-1717. https://doi.org/10.1182/blood -2005-03-0918
11. Culley, F.J., M. Johnson, J.H. Evans, S. Kumar, R. Crilly, J. Casasbuenas, T. Schnyder, M. Mehrabi, M.P. Deonarain, D.S. Ushakov, et al. 2009. Natural killer cell signal integration balances synapse symmetry and migration. PLoS Biol. 7:e1000159. https://doi.org/10.1371/journal.pbio.1000159
12. Davenport, A.J., R.S. Cross, K.A. Watson, Y. Liao, W. Shi, H.M. Prince, P.A. Beavis, J.A. Trapani, M.H. Kershaw, D.S. Ritchie, et al. 2018. Chimeric antigen receptor T cells form nonclassical and potent immune synapses driving rapid cytotoxicity. Proc. Natl. Acad. Sci. USA. 115:E2068-E2076. https://doi.org/10.1073/pnas.1716266115
13. Davis, D.M., and M.L. Dustin. 2004. What is the importance of the immunological synapse? Trends Immunol. 25:323-327. https://doi.org/10.1016/j.it.2004.03.007
14. Davis, D.M., I. Chiu, M. Fassett, G.B. Cohen, O. Mandelboim, and J.L. Strominger. 1999. The human natural killer cell immune synapse. Proc. Natl. Acad. Sci. USA. 96:15062-15067. https://doi.org/10.1073/pnas.96.26.15062
15. Dustin, M.L. 2008. T-cell activation through immunological synapses and kinapses. Immunol. Rev. 221:77-89. https://doi.org/10.1111/j.1600-065X.2008.00589.x
16. Dustin, M.L., and K. Choudhuri. 2016. Signaling and Polarized Communication Across the T Cell Immunological Synapse. Annu. Rev. Cell Dev. Biol. 32:303-325. https://doi.org/10.1146/annurev-cellbio-100814-125330
17. Edwards, J.C., L. Szczepanski, J. Szechinski, A. Filipowicz-Sosnowska, P. Emery, D.R. Close, R.M. Stevens, and T. Shaw. 2004. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 350:2572-2581. https://doi.org/10.1056/NEJMoa032534
18. Fauriat, C., E.O. Long, H.-G. Ljunggren, and Y.T. Bryceson. 2010. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood. 115:2167-2176. https://doi.org/10.1182/blood -2009-08-238469
19. Goodier, M.R., C. Lusa, S. Sherratt, A. Rodriguez-Galan, R. Behrens, and E.M. Riley. 2016. Sustained Immune Complex-Mediated Reduction in CD16 Expression after Vaccination Regulates NK Cell Function. Front. Immunol. 7:384. https://doi.org/10.3389/fimmu.2016.00384
20. Groh, V., J. Wu, C. Yee, and T. Spies. 2002. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature. 419:734-738. https://doi.org/10.1038/nature01112
21. Guillerey, C., N.D. Huntington, and M.J. Smyth. 2016. Targeting natural killer cells in cancer immunotherapy. Nat. Immunol. 17:1025-1036. https://doi.org/10.1038/ni.3518
22. Guldevall, K., B. Vanherberghen, T. Frisk, J. Hurtig, A.E. Christakou, O. Manneberg, S. Lindström, H. Andersson-Svahn, M. Wiklund, and B. Önfelt. 2010. Imaging immune surveillance of individual natural killer cells confined in microwell arrays. PLoS One. 5:e15453. https://doi.org/10.1371/journal.pone.0015453
23. Gunzer, M., A. Schäfer, S. Borgmann, S. Grabbe, K.S. Zänker, E.B. Bröcker, E. Kämpgen, and P. Friedl. 2000. Antigen presentation in extracellular matrix: interactions of T cells with dendritic cells are dynamic, short lived, and sequential. Immunity. 13:323-332. https://doi.org/10.1016/S1074-7613(00)00032-7
24. Gwalani, L.A., and J.S. Orange. 2018. Single Degranulations in NK Cells Can Mediate Target Cell Killing. J. Immunol. 200:3231-3243. https://doi.org/10.4049/jimmunol.1701500
25. Halle, S., K.A. Keyser, F.R. Stahl, A. Busche, A. Marquardt, X. Zheng, M. Galla, V. Heissmeyer, K. Heller, J. Boelter, et al. 2016. In vivo killing capacity of cytotoxic T cells is limited and involves dynamic interactions and T cell cooperativity. Immunity. 44:233-245. https://doi.org/10.1016/j.immuni.2016.01.010
26. Hsu, H.-T., E.M. Mace, A.F. Carisey, D.I. Viswanath, A.E. Christakou, M. Wiklund, B. Önfelt, and J.S. Orange. 2016. NK cells converge lytic granules to promote cytotoxicity and prevent bystander killing. J. Cell Biol. 215:875-889.
27. Jenkins, M.R., J.A. Rudd-Schmidt, J.A. Lopez, K.M. Ramsbottom, S.I. Mannering, D.M. Andrews, I. Voskoboinik, and J.A. Trapani. 2015. Failed CTL/NK cell killing and cytokine hypersecretion are directly linked through prolonged synapse time. J. Exp. Med. 212:307-317. https://doi.org/10.1084/jem.20140964
28. Jing, Y., Z. Ni, J. Wu, L. Higgins, T.W. Markowski, D.S. Kaufman, and B. Walcheck. 2015. Identification of an ADAM17 cleavage region in human CD16 (FcγRIII) and the engineering of a non-cleavable version of the receptor in NK cells. PLoS One. 10:e0121788. https://doi.org/10.1371/journal.pone.0121788
29. Konjević, G., K. Mirjacić Martinović, A. Vuletić, V. Jović, V. Jurisić, N. Babović, and I. Spuzić. 2007. Low expression of CD161 and NKG2D activating NK receptor is associated with impaired NK cell cytotoxicity in metastatic melanoma patients. Clin. Exp. Metastasis. 24:1-11. https://doi.org/10.1007/s10585-006-9043-9
30. Ljunggren, H.G., and K.J. Malmberg. 2007. Prospects for the use of NK cells in immunotherapy of human cancer. Nat. Rev. Immunol. 7:329-339. https://doi.org/10.1038/nri2073
31. López-Cobo, S., C. Campos-Silva, and M. Valés-Gómez. 2016. Glycosyl-Phosphatidyl-Inositol (GPI)-Anchors and Metalloproteases: Their Roles in the Regulation of Exosome Composition and NKG2D-Mediated Immune Recognition. Front. Cell Dev. Biol. 4:97. https://doi.org/10.3389/fcell.2016.00097
32. Martz, E. 1976. Multiple target cell killing by the cytolytic T lymphocyte and the mechanism of cytotoxicity. Transplantation. 21:5-11. https://doi.org/10.1097/00007890-197601000-00002
33. Molfetta, R., L. Quatrini, B. Zitti, C. Capuano, R. Galandrini, A. Santoni, and R. Paolini. 2016. Regulation of NKG2D expression and signaling by endocytosis. Trends Immunol. 37:790-802. https://doi.org/10.1016/j.it.2016.08.015
34. Netter, P., M. Anft, and C. Watzl. 2017. Termination of the Activating NK Cell Immunological Synapse Is an Active and Regulated Process. J. Immunol. 199:2528-2535. https://doi.org/10.4049/jimmunol.1700394
35. Ogasawara, K., J.A. Hamerman, H. Hsin, S. Chikuma, H. Bour-Jordan, T. Chen, T. Pertel, C. Carnaud, J.A. Bluestone, and L.L. Lanier. 2003. Impairment of NK cell function by NKG2D modulation in NOD mice. Immunity. 18:41-51. https://doi.org/10.1016/S1074-7613(02)00505-8
36. Orange, J.S. 2008. Formation and function of the lytic NK-cell immunological synapse. Nat. Rev. Immunol. 8:713-725. https://doi.org/10.1038/nri2381
37. Peruzzi, G., L. Femnou, A. Gil-Krzewska, F. Borrego, J. Weck, K. Krzewski, and J.E. Coligan. 2013. Membrane-type 6 matrix metalloproteinase regulates the activation-induced downmodulation of CD16 in human primary NK cells. J. Immunol. 191:1883-1894. https://doi.org/10.4049/jimmunol.1300313
38. Piccinini, F., A. Kiss, and P. Horvath. 2016. CellTracker (not only) for dummies. Bioinformatics. 32:955-957. https://doi.org/10.1093/bioinformatics/btv686
39. Quatrini, L., R. Molfetta, B. Zitti, G. Peruzzi, C. Fionda, C. Capuano, R. Galandrini, M. Cippitelli, A. Santoni, and R. Paolini. 2015. Ubiquitin-dependent endocytosis of NKG2D-DAP10 receptor complexes activates signaling and functions in human NK cells. Sci. Signal. 8:ra108. https://doi.org/10.1126/scisignal.aab2724
40. Romee, R., B. Foley, T. Lenvik, Y. Wang, B. Zhang, D. Ankarlo, X. Luo, S. Cooley, M. Verneris, B. Walcheck, and J. Miller. 2013. NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease- 17 (ADAM17). Blood. 121:3599-3608. https://doi.org/10.1182/blood -2012-04-425397
41. Sims, T.N., T.J. Soos, H.S. Xenias, B. Dubin-Thaler, J.M. Hofman, J.C. Waite, T.O. Cameron, V.K. Thomas, R. Varma, C.H. Wiggins, et al. 2007. Opposing effects of PKCtheta and WASp on symmetry breaking and relocation of the immunological synapse. Cell. 129:773-785. https://doi.org/10.1016/j.cell.2007.03.037
42. Vanherberghen, B., P.E. Olofsson, E. Forslund, M. Sternberg-Simon, M.A. Khorshidi, S. Pacouret, K. Guldevall, M. Enqvist, K.-J. Malmberg, R. Mehr, and B. Önfelt. 2013. Classification of human natural killer cells based on migration behavior and cytotoxic response. Blood. 121:1326-1334. https://doi.org/10.1182/blood -2012-06-439851
43. Varadarajan, N., B. Julg, Y.J. Yamanaka, H. Chen, A.O. Ogunniyi, E. McAndrew, L.C. Porter, A. Piechocka-Trocha, B.J. Hill, D.C. Douek, et al. 2011. A high-throughput single-cell analysis of human CD8+ T cell functions reveals discordance for cytokine secretion and cytolysis. J. Clin. Invest. 121:4322-4331. https://doi.org/10.1172/JCI58653
44. Vivier, E., E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini. 2008. Functions of natural killer cells. Nat. Immunol. 9:503-510. https://doi.org/10.1038/ni1582
45. Vivier, E., D.H. Raulet, A. Moretta, M.A. Caligiuri, L. Zitvogel, L.L. Lanier, W.M. Yokoyama, and S. Ugolini. 2011. Innate or adaptive immunity? The example of natural killer cells. Science. 331:44-49. https://doi.org/10.1126/science.1198687
46. Voskoboinik, I., J.C. Whisstock, and J.A. Trapani. 2015. Perforin and granzymes: function, dysfunction and human pathology. Nat. Rev. Immunol. 15:388-400. https://doi.org/10.1038/nri3839
47. Wiemann, K., H.W. Mittrücker, U. Feger, S.A. Welte, W.M. Yokoyama, T. Spies, H.G. Rammensee, and A. Steinle. 2005. Systemic NKG2D down-regulation impairs NK and CD8 T cell responses in vivo. J. Immunol. 175:720-729. https://doi.org/10.4049/jimmunol.175.2.720