Membrane-type 6 matrix metalloproteinase regulates the activation-induced downmodulation of CD16 in human primary NK cells

Journal of Immunology

Volumn 191, Issue 4, 2013, Pages 1883-1894

  Peruzzi, Giovanna ^a   Femnou, Laurette ^a   Gil Krzewska, Aleksandra ^a   Borrego, Francisco ^b   Weck, Jennifer ^a   Krzewski, Konrad ^a   Coligan, John E ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b BASQUE FOUNDATION FOR SCIENCE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; INTERLEUKIN 2; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 25; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CORRELATION ANALYSIS; EFFECTOR CELL; ENZYME INHIBITION; HUMAN; HUMAN CELL; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; T LYMPHOCYTE ACTIVATION; UPREGULATION;

ANTIBODY-DEPENDENT CELL CYTOTOXICITY; CELL COMMUNICATION; CELL COMPARTMENTATION; CELL LINE, TUMOR; CELL MEMBRANE; CELL POLARITY; CELLS, CULTURED; DIPEPTIDES; DOWN-REGULATION; ENDOCYTOSIS; GENE EXPRESSION REGULATION; GPI-LINKED PROTEINS; HUMANS; IMMUNOLOGICAL SYNAPSES; INTERLEUKIN-15; INTERLEUKIN-2; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MATRIX METALLOPROTEINASES, MEMBRANE-ASSOCIATED; PROTEIN TRANSPORT; RECEPTORS, IGG; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TETRADECANOYLPHORBOL ACETATE; TRANSCRIPTION, GENETIC;

EID: 84881411198     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300313     Document Type: Article

References (59)

1. 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.
2. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23: 225-274.
3. 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.
4. Maxfield, F. R., and T. E. McGraw. 2004. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5: 121-132.
5. Sandusky, M. M., B. Messmer, and C. Watzl. 2006. Regulation of 2B4 (CD244)- mediated NK cell activation by ligand-induced receptor modulation. Eur. J. Immunol. 36: 3268-3276.
6. Masilamani, M., G. Peruzzi, F. Borrego, and J. E. Coligan. 2009. Endocytosis and intracellular trafficking of human natural killer cell receptors. Traffic 10: 1735-1744.
7. Harrison, D., J. H. Phillips, and L. L. Lanier. 1991. Involvement of a metalloprotease in spontaneous and phorbol ester-induced release of natural killer cell-associated Fc gamma RIII (CD16-II). J. Immunol. 147: 3459-3465.
8. Grzywacz, B., N. Kataria, and M. R. Verneris. 2007. CD56(dim)CD16(+) NK cells downregulate CD16 following target cell induced activation of matrix metalloproteinases. Leukemia 21: 356-359; author reply 359.
9. Nimmerjahn, F., and J. V. Ravetch. 2008. Fcgamma receptors as regulators of immune responses. Nat. Rev. Immunol. 8: 34-47.
10. Natsume, A., R. Niwa, and M. Satoh. 2009. Improving effector functions of antibodies for cancer treatment: enhancing ADCC and CDC. Drug Des. Devel. Ther. 3: 7-16.
11. Shore, S. L., A. J. Nahmias, S. E. Starr, P. A. Wood, and D. E. McFarlin. 1974. Detection of cell-dependent cytotoxic antibody to cells infected with herpes simplex virus. Nature 251: 350-352.
12. László, A., I. Petri, and M. Ilyés. 1986. Antibody dependent cellular cytotoxicity (ADCC)-reaction and an in vitro steroid sensitivity test of peripheral lymphocytes in children with malignant haematological and autoimmune diseases. Acta Paediatr. Acad. Sci. Hung. 27: 23-29.
13. García-Foncillas, J., and E. Díaz-Rubio. 2010. Progress in metastatic colorectal cancer: growing role of cetuximab to optimize clinical outcome. Clin. Transl. Oncol. 12: 533-542.
14. Winter, M. C., and B. W. Hancock. 2009. Ten years of rituximab in NHL. Expert Opin. Drug Saf. 8: 223-235.
15. Albertini, M. R., J. A. Hank, and P. M. Sondel. 2005. Native and genetically engineered anti-disialoganglioside monoclonal antibody treatment of melanoma. Cancer Chemother. Biol. Response Modif. 22: 789-797.
16. Garnock-Jones, K. P., G. M. Keating, and L. J. Scott. 2010. Trastuzumab: a review of its use as adjuvant treatment in human epidermal growth factor receptor 2 (HER2)-positive early breast cancer. Drugs 70: 215-239.
17. Navid, F., V. M. Santana, and R. C. Barfield. 2010. Anti-GD2 antibody therapy for GD2-expressing tumors. Curr. Cancer Drug Targets 10: 200-209.
18. Liu, Q., Y. Sun, S. Rihn, A. Nolting, P. N. Tsoukas, S. Jost, K. Cohen, B. Walker, and G. Alter. 2009. Matrix metalloprotease inhibitors restore impaired NK cellmediated antibody-dependent cellular cytotoxicity in human immunodeficiency virus type 1 infection. J. Virol. 83: 8705-8712.
19. Pillet, A. H., F. Bugault, J. Thèze, L. A. Chakrabarti, and T. Rose. 2009. A programmed switch from IL-15- to IL-2-dependent activation in human NK cells. J. Immunol. 182: 6267-6277.
20. Caligiuri, M. A., C. Murray, M. J. Robertson, E. Wang, K. Cochran, C. Cameron, P. Schow, M. E. Ross, T. R. Klumpp, R. J. Soiffer, et al. 1993. Selective modulation of human natural killer cells in vivo after prolonged infusion of low dose recombinant interleukin 2. J. Clin. Invest. 91: 123-132.
21. Edsparr, K., F. M. Speetjens, A. Mulder-Stapel, R. H. Goldfarb, P. H. Basse, B. Lennernäs, P. J. Kuppen, and P. Albertsson. 2010. Effects of IL-2 on MMP expression in freshly isolated human NK cells and the IL-2-independent NK cell line YT. J. Immunother. 33: 475-481.
22. Egeblad, M., and Z. Werb. 2002. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2: 161-174.
23. Somerville, R. P., S. A. Oblander, and S. S. Apte. 2003. Matrix metalloproteinases: old dogs with new tricks. Genome Biol. 4: 216.
24. Parks, W. C., C. L. Wilson, and Y. S. López-Boado. 2004. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat. Rev. Immunol. 4: 617-629.
25. Borrego, F., A. Lopez-Beltran, J. Peña, and R. Solana. 1994. Downregulation of Fc gamma receptor IIIA alpha (CD16-II) on natural killer cells induced by anti- CD16 mAb is independent of protein tyrosine kinases and protein kinase C. Cell. Immunol. 158: 208-217.
26. Mastroianni, C. M., and G. M. Liuzzi. 2007. Matrix metalloproteinase dysregulation in HIV infection: implications for therapeutic strategies. Trends Mol. Med. 13: 449-459.
27. Nagler, A., L. L. Lanier, and J. H. Phillips. 1990. Constitutive expression of high affinity interleukin 2 receptors on human CD16-natural killer cells in vivo. J. Exp. Med. 171: 1527-1533.
28. Cacalano, N. A., and J. A. Johnston. 1999. Interleukin-2 signaling and inherited immunodeficiency. Am. J. Hum. Genet. 65: 287-293.
29. Procopio, A., A. Gismondi, R. Paolini, S. Morrone, R. Testi, M. Piccoli, L. Frati, R. B. Herberman, and A. Santoni. 1988. Proliferative effects of 12-Otetradecanoylphorbol- 13-acetate (TPA) and calcium ionophores on human large granular lymphocytes (LGL). Cell. Immunol. 113: 70-81.
30. Gibson, A. E., R. J. Noel, J. T. Herlihy, and W. F. Ward. 1989. Phenylarsine oxide inhibition of endocytosis: effects on asialofetuin internalization. Am. J. Physiol. 257: C182-C184.
31. Ferguson, S. M., and P. De Camilli. 2012. Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 13: 75-88.
32. Edsparr, K., P. H. Basse, R. H. Goldfarb, and P. Albertsson. 2011. Matrix metalloproteinases in cytotoxic lymphocytes impact on tumour infiltration and immunomodulation. Cancer Microenviron. 4: 351-360.
33. Kim, M. H., P. Albertsson, Y. Xue, R. P. Kitson, U. Nannmark, and R. H. Goldfarb. 2000. Expression of matrix metalloproteinases and their inhibitors by rat NK cells: inhibition of their expression by genistein. In Vivo 14: 557-564.
34. Carter, P., L. Presta, C. M. Gorman, J. B. Ridgway, D. Henner, W. L. Wong, A. M. Rowland, C. Kotts, M. E. Carver, and H. M. Shepard. 1992. Humanization of an anti-p185HER2 antibody for human cancer therapy. Proc. Natl. Acad. Sci. USA 89: 4285-4289.
35. Cooper, M. A., T. A. Fehniger, and M. A. Caligiuri. 2001. The biology of human natural killer-cell subsets. Trends Immunol. 22: 633-640.
36. Hatjiharissi, E., L. Xu, D. D. Santos, Z. R. Hunter, B. T. Ciccarelli, S. Verselis, M. Modica, Y. Cao, R. J. Manning, X. Leleu, et al. 2007. Increased natural killer cell expression of CD16, augmented binding and ADCC activity to rituximab among individuals expressing the FcgammaRIIIa-158 V/V and V/F polymorphism. Blood 110: 2561-2564.
37. Huenecke, S., S. Y. Zimmermann, S. Kloess, R. Esser, A. Brinkmann, L. Tramsen, M. Koenig, S. Erben, C. Seidl, T. Tonn, et al. 2010. IL-2-driven regulation of NK cell receptors with regard to the distribution of CD16+ and CD16- subpopulations and in vivo influence after haploidentical NK cell infusion. J. Immunother. 33: 200-210.
38. Miller, J. S., Y. Soignier, A. Panoskaltsis-Mortari, S. A. McNearney, G. H. Yun, S. K. Fautsch, D. McKenna, C. Le, T. E. Defor, L. J. Burns, et al. 2005. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 105: 3051-3057.
39. Passweg, J. R., U. Koehl, L. Uharek, S. Meyer-Monard, and A. Tichelli. 2006. Natural-killer-cell-based treatment in haematopoietic stem-cell transplantation. Best Pract. Res. Clin. Haematol. 19: 811-824.
40. Koehl, U., J. Sörensen, R. Esser, S. Zimmermann, H. P. Grüttner, T. Tonn, C. Seidl, E. Seifried, T. Klingebiel, and D. Schwabe. 2004. IL-2 activated NK cell immunotherapy of three children after haploidentical stem cell transplantation. Blood Cells Mol. Dis. 33: 261-266.
41. Passweg, J. R., M. Stern, U. Koehl, L. Uharek, and A. Tichelli. 2005. Use of natural killer cells in hematopoetic stem cell transplantation. Bone Marrow Transplant. 35: 637-643.
42. Park, Y. P., S. C. Choi, P. Kiesler, A. Gil-Krzewska, F. Borrego, J. Weck, K. Krzewski, and J. E. Coligan. 2011. Complex regulation of human NKG2DDAP10 cell surface expression: opposing roles of the γc cytokines and TGF-β1. Blood 118: 3019-3027.
43. Bryceson, Y. T., M. E. March, H.-G. Ljunggren, and E. O. Long. 2006. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 107: 159-166.
44. Huizinga, T. W., M. de Haas, M. Kleijer, J. H. Nuijens, D. Roos, and A. E. von dem Borne. 1990. Soluble Fc gamma receptor III in human plasma originates from release by neutrophils. J. Clin. Invest. 86: 416-423.
45. Middelhoven, P. J., J. D. Van Buul, P. L. Hordijk, and D. Roos. 2001. Different proteolytic mechanisms involved in Fc gamma RIIIb shedding from human neutrophils. Clin. Exp. Immunol. 125: 169-175.
46. de la Salle, H., J. Galon, H. Bausinger, D. Spehner, A. Bohbot, J. Cohen, J. P. Cazenave, W. H. Fridman, C. Sautès, and D. Hanau. 1997. Soluble CD16/Fc gamma RIII induces maturation of dendritic cells and production of several cytokines including IL-12. Adv. Exp. Med. Biol. 417: 345-352.
47. Galon, J., J. F. Gauchat, N. Mazières, R. Spagnoli, W. Storkus, M. Lötze, J. Y. Bonnefoy, W. H. Fridman, and C. Sautès. 1996. Soluble Fcgamma receptor type III (FcgammaRIII, CD16) triggers cell activation through interaction with complement receptors. J. Immunol. 157: 1184-1192.
48. Teillaud, C., J. Galon, M. T. Zilber, N. Mazières, R. Spagnoli, R. Kurrle, W. H. Fridman, and C. Sautès. 1993. Soluble CD16 binds peripheral blood mononuclear cells and inhibits pokeweed-mitogen-induced responses. Blood 82: 3081-3090.
49. Cecchetti, S., F. Spadaro, L. Lugini, F. Podo, and C. Ramoni. 2007. Functional role of phosphatidylcholine-specific phospholipase C in regulating CD16 membrane expression in natural killer cells. Eur. J. Immunol. 37: 2912-2922.
50. Pei, D. 1999. Leukolysin/MMP25/MT6-MMP: a novel matrix metalloproteinase specifically expressed in the leukocyte lineage. Cell Res. 9: 291-303.
51. Kang, T., J. Yi, A. Guo, X. Wang, C. M. Overall, W. Jiang, R. Elde, N. Borregaard, and D. Pei. 2001. Subcellular distribution and cytokine- and chemokine-regulated secretion of leukolysin/MT6-MMP/MMP-25 in neutrophils. J. Biol. Chem. 276: 21960-21968.
52. Schechter, I., and A. Berger. 1967. On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27: 157-162.
53. Turk, B. E., L. L. Huang, E. T. Piro, and L. C. Cantley. 2001. Determination of protease cleavage site motifs using mixture-based oriented peptide libraries. Nat. Biotechnol. 19: 661-667.
54. Starr, A. E., C. L. Bellac, A. Dufour, V. Goebeler, and C. M. Overall. 2012. Biochemical characterization and N-terminomics analysis of leukolysin, the membrane-type 6 matrix metalloprotease (MMP25): chemokine and vimentin cleavages enhance cell migration and macrophage phagocytic activities. J. Biol. Chem. 287: 13382-13395.
55. Wang, Y., J. Wu, R. Newton, N. S. Bahaie, C. Long, and B. Walcheck. 2013. ADAM17 cleaves CD16b (FcγRIIIb) in human neutrophils. Biochim. Biophys. Acta 1833: 680-685.
56. Sohail, A., Q. Sun, H. Zhao, M. M. Bernardo, J. A. Cho, and R. Fridman. 2008. MT4-(MMP17) and MT6-MMP (MMP25), a unique set of membrane-anchored matrix metalloproteinases: properties and expression in cancer. Cancer Metastasis Rev. 27: 289-302.
57. Murphy, G. 2011. Tissue inhibitors of metalloproteinases. Genome Biol. 12: 233.
58. Greene, J., M. Wang, Y. E. Liu, L. A. Raymond, C. Rosen, and Y. E. Shi. 1996. Molecular cloning and characterization of human tissue inhibitor of metalloproteinase 4. J. Biol. Chem. 271: 30375-30380.
59. Rivera, S., M. Khrestchatisky, L. Kaczmarek, G. A. Rosenberg, and D. M. Jaworski. 2010. Metzincin proteases and their inhibitors: foes or friends in nervous system physiology? J. Neurosci. 30: 15337-15357.