A disintegrin and metalloprotease (ADAM) 10 and ADAM17 are major sheddases of T cell immunoglobulin and mucin domain 3 (Tim-3)

Journal of Biological Chemistry

Volumn 288, Issue 48, 2013, Pages 34529-34544

  Möller Hackbarth, Katja ^a   Dewitz, Christin ^a   Schweigert, Olga ^a   Trad, Ahmad ^a   Garbers, Christoph ^b   Rose John, Stefan ^a   Scheller, Jürgen ^b  

^a UNIVERSITY OF KIEL   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOWN-REGULATION; ECTODOMAIN SHEDDING; IMMUNE RESPONSE; INTRACELLULAR DOMAIN; LIPOPOLYSACCHARIDES; LYSINE RESIDUES; METALLO-PROTEASE; MURINE EMBRYONIC FIBROBLASTS;

AMINO ACIDS; CELL CULTURE; CELL DEATH; IMMUNOLOGY;

BODY FLUIDS;

ADAM10 ENDOPEPTIDASE; ASPARTIC ACID; CD14 ANTIGEN; GLUTAMIC ACID; INTERLEUKIN 12; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LYSINE; MEMBRANE PROTEIN; T CELL IMMUNOGLOBULIN AND MUCIN DOMAIN 3 PROTEIN; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; EMBRYO; ENZYME SUBSTRATE; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNE RESPONSE; KIDNEY CELL; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT;

EID: 84889015170     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.488478     Document Type: Article

References (53)

1. Freeman, G. J., Casasnovas, J. M., Umetsu, D. T., and DeKruyff, R. H. (2010) TIM genes. A family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity. Immunol. Rev. 235, 172-189
2. McIntire, J. J., Umetsu, D. T., and DeKruyff, R. H. (2004) TIM-1, a novel allergy and asthma susceptibility gene. Springer Semin. Immunopathol. 25, 335-348
3. Zhu, C., Anderson, A. C., Schubart, A., Xiong, H., Imitola, J., Khoury, S. J., Zheng, X. X., Strom, T. B., and Kuchroo, V. K. (2005) The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 6, 1245-1252
4. Koguchi, K., Anderson, D. E., Yang, L., O'Connor, K. C., Kuchroo, V. K., and Hafler, D. A. (2006) Dysregulated T cell expression of TIM3 in multiple sclerosis. J. Exp. Med. 203, 1413-1418
5. Jones, R. B., Ndhlovu, L. C., Barbour, J. D., Sheth, P. M., Jha, A. R., Long, B. R., Wong, J. C., Satkunarajah, M., Schweneker, M., Chapman, J. M., Gyenes, G., Vali, B., Hyrcza, M. D., Yue, F. Y., Kovacs, C., Sassi, A., Loutfy, M., Halpenny, R., Persad, D., Spotts, G., Hecht, F. M., Chun, T. W., Mc- Cune, J. M., Kaul, R., Rini, J. M., Nixon, D. F., and Ostrowski, M. A. (2008) Tim-3 expression defines a novel population of dysfunctional T cells with highly elevated frequencies in progressive HIV-1 infection. J. Exp. Med. 205, 2763-2779
6. McMahan, R. H., Golden-Mason, L., Nishimura, M. I., McMahon, B. J., Kemper, M., Allen, T. M., Gretch, D. R., and Rosen, H. R. (2010) Tim-3 expression on PD-1+ HCV-specific human CTLs is associated with viral persistence, and its blockade restores hepatocyte-directed in vitro cytotoxicity. J. Clin. Invest. 120, 4546-4557
7. Jin, H. T., Anderson, A. C., Tan, W. G., West, E. E., Ha, S. J., Araki, K., Freeman, G. J., Kuchroo, V. K., and Ahmed, R. (2010) Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc. Natl. Acad. Sci. U.S.A. 107, 14733-14738
8. Golden-Mason, L., Palmer, B. E., Kassam, N., Townshend-Bulson, L., Livingston, S., McMahon, B. J., Castelblanco, N., Kuchroo, V., Gretch, D. R., and Rosen, H. R. (2009) Negative immune regulator Tim-3 is overexpressed on T cells in hepatitis C virus infection and its blockade rescues dysfunctional CD4+ and CD8+ T cells. J. Virol. 83, 9122-9130
9. Sakuishi, K., Apetoh, L., Sullivan, J. M., Blazar, B. R., Kuchroo, V. K., and Anderson, A. C. (2010) Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J. Exp. Med. 207, 2187-2194
10. Fourcade, J., Sun, Z., Benallaoua, M., Guillaume, P., Luescher, I. F., Sander, C., Kirkwood, J. M., Kuchroo, V., and Zarour, H. M. (2010) Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J. Exp. Med. 207, 2175-2186
11. Zhou, Q., Munger, M. E., Veenstra, R. G., Weigel, B. J., Hirashima, M., Munn, D. H., Murphy, W. J., Azuma, M., Anderson, A. C., Kuchroo, V. K., and Blazar, B. R. (2011) Coexpression of Tim-3 and PD-1 identifies a CD8+ T-cell exhaustion phenotype in mice with disseminated acute myelogenous leukemia. Blood 117, 4501-4510
12. Ngiow, S. F., von Scheidt, B., Akiba, H., Yagita, H., Teng, M. W., and Smyth, M. J. (2011) Anti-TIM3 antibody promotes T cell IFN-γ-mediated antitumor immunity and suppresses established tumors. Cancer Res. 71, 3540-3551
13. Barber, D. L., Wherry, E. J., Masopust, D., Zhu, B., Allison, J. P., Sharpe, A. H., Freeman, G. J., and Ahmed, R. (2006) Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682-687
14. Blackburn, S. D., Shin, H., Freeman, G. J., and Wherry, E. J. (2008) Selective expansion of a subset of exhausted CD8 T cells by αPD-L1 blockade. Proc. Natl. Acad. Sci. U.S.A. 105, 15016-15021
15. Sakuishi, K., Jayaraman, P., Behar, S. M., Anderson, A. C., and Kuchroo, V. K. (2011) Emerging Tim-3 functions in antimicrobial and tumor immunity. Trends Immunol. 32, 345-349
16. Anderson, A. C., Anderson, D. E., Bregoli, L., Hastings, W. D., Kassam, N., Lei, C., Chandwaskar, R., Karman, J., Su, E. W., Hirashima, M., Bruce, J. N., Kane, L. P., Kuchroo, V. K., and Hafler, D. A. (2007) Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells. Science 318, 1141-1143
17. Zhang, Y., Ma, C. J., Wang, J. M., Ji, X. J., Wu, X. Y., Moorman, J. P., and Yao, Z. Q. (2012) Tim-3 regulates pro- and anti-inflammatory cytokine expression in human CD14+ monocytes. J. Leukocyte Biol. 91, 189-196
18. Sabatos, C. A., Chakravarti, S., Cha, E., Schubart, A., Sánchez-Fueyo, A., Zheng, X. X., Coyle, A. J., Strom, T. B., Freeman, G. J., and Kuchroo, V. K. (2003) Interaction of Tim-3 and Tim-3 ligand regulates T helper type 1 responses and induction of peripheral tolerance. Nat. Immunol. 4, 1102-1110
19. Geng, H., Zhang, G. M., Li, D., Zhang, H., Yuan, Y., Zhu, H. G., Xiao, H., Han, L. F., and Feng, Z. H. (2006) Soluble form of T cell Ig mucin 3 is an inhibitory molecule in T cell-mediated immune response. J. Immunol. 176, 1411-1420
20. Edwards, D. R., Handsley, M. M., and Pennington, C. J. (2008) TheADAM metalloproteinases. Mol. Aspects Med. 29, 258-289
21. Garbers, C., Jänner, N., Chalaris, A., Moss, M. L., Floss, D. M., Meyer, D., Koch-Nolte, F., Rose-John, S., and Scheller, J. (2011) Species specificity of ADAM10 and ADAM7 in IL-6 transsignaling and novel role of ADAM10 in inducible IL-6R shedding. J. Biol. Chem. 286, 14804-14811
22. Le Gall, S. M., Bobé, P., Reiss, K., Horiuchi, K., Niu, X. D., Lundell, D., Gibb, D. R., Conrad, D., Saftig, P., and Blobel, C. P. (2009) ADAMs 10 and 17 represent differentially regulated components of a general shedding machinery for membrane proteins such as transforming growth factor α, L-selectin, and tumor necrosis factor α. Mol. Biol. Cell 20, 1785-1794
23. Scheller, J., Chalaris, A., Garbers, C., and Rose-John, S. (2011) ADAM17.A molecular switch controlling inflammatory and regenerative responses. Trends Immunol. 32, 380-387
24. Black, R. A., Rauch, C. T., Kozlosky, C. J., Peschon, J. J., Slack, J. L., Wolfson, M. F., Castner, B. J., Stocking, K. L., Reddy, P., Srinivasan, S., Nelson, N., Boiani, N., Schooley, K. A., Gerhart, M., Davis, R., Fitzner, J. N., Johnson, R. S., Paxton, R. J., March, C. J., and Cerretti, D. P. (1997) A metalloproteinase disintegrin that releases tumour-necrosis factor-α from cells. Nature 385, 729-733
25. Hartmann, D., de Strooper, B., Serneels, L., Craessaerts, K., Herreman, A., Annaert, W., Umans, L., Lübke, T., Lena Illert, A., von Figura, K., and Saftig, P. (2002) The disintegrin/metalloprotease ADAM 10 is es-sential for Notch signalling but not for α-secretase activity in fibroblasts. Hum. Mol. Genet. 11, 2615-2624
26. Reiss, K., Maretzky, T., Haas, I. G., Schulte, M., Ludwig, A., Frank, M., and Saftig, P. (2006) Regulated ADAM10-dependent ectodomain shedding of γ-protocadherin C3 modulates cell-cell adhesion. J. Biol. Chem. 281, 985-1006
27. Hundhausen, C., Misztela, D., Berkhout, T. A., Broadway, N., Saftig, P., Reiss, K., Hartmann, D., Fahrenholz, F., Postina, R., Matthews, V., Kallen, K.-J., Rose-John, S., and Ludwig, A. (2003) The disintegrin-like metalloproteinase ADAM 10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion. Blood 102, 1186-1195
28. Moss, M. L., Bomar, M., Liu, Q., Sage, H., Dempsey, P., Lenhart, P. M., Gillispie, P. A., Stoeck, A., Wildeboer, D., Bartsch, J. W., Palmisano, R., and Zhou, P. (2007) The ADAM10 prodomain is a specific inhibitor of ADAM10 proteolytic activity and inhibits cellular shedding events. J. Biol. Chem. 282, 35712-35721
29. Gonzales, P. E., Galli, J. D., and Milla, M. E. (2008) Identification of key sequence determinants for the inhibitory function of the prodomain of TACE. Biochemistry 47, 9911-9919
30. Müllberg, J., Oberthür, W., Lottspeich, F., Mehl, E., Dittrich, E., Graeve, L., Heinrich, P. C., and Rose-John, S. (1994) The soluble human IL-6 receptor. Mutational characterization of the proteolytic cleavage site. J. Immunol. 152, 4958-4968
31. Baran, P., Nitz, R., Grötzinger, J., Scheller, J., and Garbers, C. (2013) Minimal interleukin (IL-)6 receptor stalk composition for IL-6R shedding and IL-6 classic signaling. J. Biol. Chem. 288, 14756-14768
32. Caescu, C. I., Jeschke, G. R., and Turk, B. E. (2009) Active-site determinants of substrate recognition by the metalloproteinases TACE and ADAM10. Biochem. J. 424, 79-88
33. Ivetic, A., Florey, O., Deka, J., Haskard, D. O., Ager, A., and Ridley, A. J. (2004) Mutagenesis of the ezrin-radixin-moesin binding domain of Lselectin tail affects shedding, microvillar positioning, and leukocyte tethering. J. Biol. Chem. 279, 33263-33272
34. Lee, J., Su, E. W., Zhu, C., Hainline, S., Phuah, J., Moroco, J. A., Smithgall, T. E., Kuchroo, V. K., and Kane, L. P. (2011) Phosphotyrosine- dependent coupling of Tim-3 to T-cell receptor signaling pathways. Mol. Cell Biol. 31, 3963-3974
35. Ivetic, A., Deka, J., Ridley, A., and Ager, A. (2002) The cytoplasmic tail of L-selectin interacts with members of the Ezrin-Radixin-Moesin (ERM) family of proteins. Cell activation-dependent binding of Moesin but not Ezrin. J. Biol. Chem. 277, 2321-2329
36. Canobbio, I., Catricalà, S., Balduini, C., and Torti, M. (2011) Calmodulin regulates the non-amyloidogenic metabolism of amyloid precursor protein in platelets. Biochim. Biophys. Acta 1813, 500-506
37. Gifford, J. L., Ishida, H., and Vogel, H. J. (2012) Structural insights into calmodulin-regulated L-selectin ectodomain shedding. J. Biol. Chem. 287, 26513-26527
38. Ali, N., and Knaüper, V. (2007) Phorbol ester-induced shedding of the prostate cancer marker transmembrane protein with epidermal growth factor and two follistatin motifs 2 is mediated by the disintegrin and metalloproteinase-17. J. Biol. Chem. 282, 37378-37388
39. Peschon, J. J., Slack, J. L., Reddy, P., Stocking, K. L., Sunnarborg, S. W., Lee, D. C., Russell, W. E., Castner, B. J., Johnson, R. S., Fitzner, J. N., Boyce, R. W., Nelson, N., Kozlosky, C. J., Wolfson, M. F., Rauch, C. T., Cerretti, D. P., Paxton, R. J., March, C. J., and Black, R. A. (1998) An essential role for ectodomain shedding in mammalian development. Science 282, 1281-1284
40. Saftig, P., and Reiss, K. (2011) The "A Disintegrin And Metalloproteases" ADAM10 and ADAM17. Novel drug targets with therapeutic potential? Eur. J. Cell Biol. 90, 527-535
41. Moss, M. L., Sklair-Tavron, L., and Nudelman, R. (2008) Drug insight. Tumor necrosis factor-converting enzyme as a pharmaceutical target for rheumatoid arthritis. Nat. Clin. Pract. Rheumatology 4, 300-309
42. Kenny, P. (2007) TACE. A new target in epidermal growth factor receptor dependent tumors. Differentiation 75, 800-808
43. McIlwain, D. R., Lang, P. A., Maretzky, T., Hamada, K., Ohishi, K., Maney, S. K., Berger, T., Murthy, A., Duncan, G., Xu, H. C., Lang, K. S., Häussinger, D., Wakeham, A., Itie-Youten, A., Khokha, R., Ohashi, P. S., Blobel, C. P., and Mak, T. W. (2012) iRhom2 regulation of TACE controls TNF-mediated protection against Listeria and responses to LPS. Science 335, 229-232
44. Adrain, C., Zettl, M., Christova, Y., Taylor, N., and Freeman, M. (2012) Tumor necrosis factor signaling requires iRhom2 to promote trafficking and activation of TACE. Science 335, 225-228
45. Maretzky, T., McIlwain, D. R., Issuree, P. D., Li, X., Malapeira, J., Amin, S., Lang, P. A., Mak, T. W., and Blobel, C. P. (2013) iRhom2 controls the substrate selectivity of stimulated ADAM17-dependent ectodomain shedding. Proc. Natl. Acad. Sci. U.S.A. 110, 11433-11438
46. Galkina, E., Tanousis, K., Preece, G., Tolaini, M., Kioussis, D., Florey, O., Haskard, D. O., Tedder, T. F., and Ager, A. (2003) L-selectin shedding does not regulate constitutiveTcell trafficking but controls the migration pathways of antigen-activated T lymphocytes. J. Exp. Med. 198, 1323-1335
47. Venturi, G. M., Tu, L., Kadono, T., Khan, A. I., Fujimoto, Y., Oshel, P., Bock, C. B., Miller, A. S., Albrecht, R. M., Kubes, P., Steeber, D. A., and Tedder, T. F. (2003) Leukocyte migration is regulated by L-selectin endo- proteolytic release. Immunity 19, 713-724
48. Matala, E., Alexander, S. R., Kishimoto, T. K., and Walcheck, B. (2001) The cytoplasmic domain of L-selectin participates in regulating L-selectin endoproteolysis. J. Immunol. 167, 1617-1623
49. Guo, L., Takino, T., Endo, Y., Domoto, T., and Sato, H. (2012) Shedding of kidney injury molecule-1 by membrane-type 1 matrix metalloproteinase. J. Biochem. 152, 425-432
50. Lim, A. I., Chan, L. Y., Lai, K. N., Tang, S. C., Chow, C. W., Lam, M. F., and Leung, J. C. (2012) Distinct role of matrix metalloproteinase-3 in kidney injury molecule-1 shedding by kidney proximal tubular epithelial cells. Int. J. Biochem. Cell Biol. 44, 1040-1050
51. Gómez-Gaviro, M., Domínguez-Luis, M., Canchado, J., Calafat, J., Janssen, H., Lara-Pezzi, E., Fourie, A., Tugores, A., Valenzuela-Fernández, A., Mollinedo, F., Sánchez-Madrid, F., and Díaz-González, F. (2007) Expression and regulation of the metalloproteinase ADAM-8 during human neutrophil pathophysiological activation and its catalytic activity on Lselectin shedding. J. Immunol. 178, 8053-8063
52. Yoshiyama, K., Higuchi, Y., Kataoka, M., Matsuura, K., and Yamamoto, S. (1997) CD156 (human ADAM8). Expression, primary amino acid sequence, and gene location. Genomics 41, 56-62
53. Mochizuki, S., and Okada, Y. (2007) ADAMs in cancer cell proliferation and progression. Cancer Sci. 98, 621-628