αvβ3-dependent cross-presentation of matrix metalloproteinase-2 by melanoma cells gives rise to a new tumor antigen

Journal of Experimental Medicine

Volumn 202, Issue 1, 2005, Pages 61-72

  Godefroy, Emmanuelle ^a   Moreau Aubry, Agnes ^a,c   Diez, Elisabeth ^a   Dreno, Brigitte ^a,b   Jotereau, Francine ^a,c   Guilloux, Yannick ^a,c  

^a INSERM   (France)

^b HÔTEL DIEU   (France)

^c UNIVERSITÉ DE NANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GELATINASE A; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TUMOR ANTIGEN; VITRONECTIN RECEPTOR; COMPLEMENTARY DNA; HLA A ANTIGEN; HLA A*0201 ANTIGEN; HLA-A*0201 ANTIGEN; PROTEASOME;

ANTIGEN SPECIFICITY; ARTICLE; CONTROLLED STUDY; CROSS PRESENTATION; DISEASE COURSE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; LEUKOCYTE; MAJOR HISTOCOMPATIBILITY COMPLEX; MELANOMA; MELANOMA CELL; MOLECULAR RECOGNITION; PRIORITY JOURNAL; T LYMPHOCYTE; ANIMAL; ANTIGEN PRESENTATION; CELL LINE; CELL STRAIN COS1; CERCOPITHECUS; COATED VESICLE; CYTOTOXIC T LYMPHOCYTE; ENZYMOLOGY; GENETICS; IMMUNOLOGY; METABOLISM; NUCLEOTIDE SEQUENCE; TUMOR CELL LINE;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; BASE SEQUENCE; CELL LINE; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; CLATHRIN-COATED VESICLES; COS CELLS; DNA, COMPLEMENTARY; EPITOPES; HLA-A ANTIGENS; HUMANS; INTEGRIN ALPHAVBETA3; MATRIX METALLOPROTEINASE 2; MELANOMA; PROTEASOME ENDOPEPTIDASE COMPLEX; T-LYMPHOCYTES, CYTOTOXIC;

EID: 22344456827     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20042138     Document Type: Article

References (50)

1. Gromme, M., and J. Neefjes. 2002. Antigen degradation or presentation by MHC class I molecules via classical and non-classical pathways. Mol. Immunol. 39:181-202.
2. Albert, M.L., J.C. Darnell, A. Bender, L.M. Francisco, N. Bhardwaj, and R.B. Darnell. 1998. Tumor-specific killer cells in paraneoplastic cerebellar degeneration. Nat. Med. 4:1321-1324.
3. Huang, A.Y., P. Golumbek, M. Ahmadzadeh, E. Jaffee, D. Pardoll, and H. Levitsky. 1994. Role of bone marrow-derived cells in presenting MHC class I-restricted tumor antigens. Science. 264:961-965.
4. Yee, C., and P. Greenberg. 2002. Modulating T-cell immunity to tumours: new strategies for monitoring T-cell responses. Nat. Rev. Cancer. 2:409-419.
5. Coulie, P.G., and P. van der Bruggen. 2003. T-cell responses of vaccinated cancer patients. Curr. Opin. Immunol. 15:131-137.
6. Yee, C., J.A. Thompson, P. Roche, D.R. Byrd, P.P. Lee, M. Piepkorn, K. Kenyon, M.M. Davis, S.R. Riddell, and P.D. Greenberg. 2000. Melanocyte destruction after antigen-specific immunotherapy of melanoma: direct evidence of T cell-mediated vitiligo. J. Exp. Med. 192:1637-1644.
7. Labarriere, N., M.C. Pandolfino, N. Gervois, A. Khammari, M.H. Tessier, B. Dreno, and F. Jotereau. 2002. Therapeutic efficacy of melanoma-reactive TIL injected in stage III melanoma patients. Cancer Immunol. Immunother. 51:532-538.
8. Dreno, B., J.M. Nguyen, A. Khammari, M.C. Pandolfino, M.H. Tessier, S. Bercegeay, A. Cassidanius, P. Lemarre, S. Billaudel, N. Labarriere, and F. Jotereau. 2002. Randomized trial of adoptive transfer of melanoma tumor-infiltrating lymphocytes as adjuvant therapy for stage III melanoma. Cancer Immunol. Immunother. 51:539-546.
9. Khasigov, P.Z., O.V. Podobed, S.A. Ktzoeva, T.M. Gatagonova, S.V. Grachev, S.S. Shishkin, and T.T. Berezov. 2001. Matrix metalloproteinases of normal human tissues. Biochemistry (Mosc.). 66:130-140.
10. Egeblad, M., and Z. Werb. 2002. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer. 2:161-174.
11. Mochizuki, N., S. Yamashita, K. Kurokawa, Y. Ohba, T. Nagai, A. Miyawaki, and M. Matsuda. 2001. Spatio-temporal images of growthfactor-induced activation of Ras and Rap1. Nature. 411:1065-1068.
12. Lopez, D., and M. Del Val. 1997. Selective involvement of proteasomes and cysteine proteases in MHC class I antigen presentation. J. Immunol. 159:5769-5772.
13. Geier, E., G. Pfeifer, M. Wilm, M. Lucchiari-Hartz, W. Baumeister, K. Eichmann, and G. Niedermann. 1999. A giant protease with potential to substitute for some functions of the proteasome. Science. 283:978-981.
14. Kessler, B.M., R. Glas, and H.L. Ploegh. 2002. MHC class I antigen processing regulated by cytosolic proteolysis-short cuts that alter peptide generation. Mol. Immunol. 39:171-179.
15. Shrimpton, C.N., G. Abbenante, R.A. Lew, and I. Smith. 2000. Development and characterization of novel potent and stable inhibitors of endopeptidase EC 3.4.24.15. Biochem. J. 345(Pt 2):351-356.
16. Yang, Z., D.K. Strickland, and P. Bornstein. 2001. Extracellular matrix metalloproteinase 2 levels are regulated by the low density lipoproteinrelated scavenger receptor and thrombospondin 2. J. Biol. Chem. 276:8403-8408.
17. Sato, H., T. Kinoshita, T. Takino, K. Nakayama, and M. Seiki. 1996. Activation of a recombinant membrane type 1-matrix metalloproteinase (MT1-MMP) by furin and its interaction with tissue inhibitor of metalloproteinases (TIMP)-2. FEBS Lett. 393:101-104.
18. Brooks, P.C., S. Stromblad, L.C. Sanders, T.L. von Schalscha, R.T. Aimes, W.G. Stetler-Stevenson, J.P. Quigley, and D.A. Cheresh. 1996. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell. 85:683-693.
19. Brooks, P.C., R.A. Clark, and D.A. Cheresh. 1994. Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science. 264:569-571.
20. Regnault, A., D. Lankar, V. Lacabanne, A. Rodriguez, C. Thery, M. Rescigno, T. Saito, S. Verbeek, C. Bonnerot, P. Ricciardi-Castagnoli, and S. Amigorena. 1999. Fcgamma receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J. Exp. Med. 189:371-380.
21. Stefanidakis, M., M. Bjorklund, E. Ihanus, C.G. Gahmberg, and E. Koivunen. 2003. Identification of a negatively charged peptide motif within the catalytic domain of progelatinases that mediates binding to leukocyte beta 2 integrins. J. Biol. Chem. 278:34674-34684.
22. Brooks, P.C., S. Silletti, T.L. von Schalscha, M. Friedlander, and D.A. Cheresh. 1998. Disruption of angiogenesis by PEX, a noncatalytic metalloproteinase fragment with integrin binding activity. Cell. 92:391-400.
23. Seftor, R.E., E.A. Seftor, and M.J. Hendrix. 1999. Molecular role(s) for integrins in human melanoma invasion. Cancer Metastasis Rev. 18:359-375.
24. Hofmann, U.B., J.R. Westphal, E.T. Waas, J.C. Becker, D.J. Ruiter, and G.N. van Muijen. 2000. Coexpression of integrin alpha(v)beta3 and matrix metalloproteinase-2 (MMP-2) coincides with MMP-2 activation: correlation with melanoma progression. J. Invest. Dermatol. 115:625-632.
25. Ye, Y., Y. Shibata, C. Yun, D. Ron, and T.A. Rapoport. 2004. A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature. 429:841-847.
26. Lilley, B.N., and H.L. Ploegh. 2004. A membrane protein required for dislocation of misfolded proteins from the ER. Nature. 429:834-840.
27. Ackerman, A.L., and P. Cresswell. 2004. Cellular mechanisms governing cross-presentation of exogenous antigens. Nat. Immunol. 5:678-684.
28. Gagnon, E., S. Duclos, C. Rondeau, E. Chevet, P.H. Cameron, O. Steele-Mortimer, J. Paiement, J.J. Bergeron, and M. Desjardins. 2002. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell. 110:119-131.
29. Desjardins, M., L.A. Huber, R.G. Parton, and G. Griffiths. 1994. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124:677-688.
30. Guermonprez, P., L. Saveanu, M. Kleijmeer, J. Davoust, P. Van Endert, and S. Amigorena. 2003. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature. 425:397-402.
31. Morgunova, E., A. Tuuttila, U. Bergmann, M. Isupov, Y. Lindqvist, G. Schneider, and K. Tryggvason. 1999. Structure of human promatrix metalloproteinase-2: activation mechanism revealed. Science. 284:1667-1670.
32. Kirkin, A.F., K. Dzhandzhugazyan, and J. Zeuthen. 1998. Melanoma-associated antigens recognized by cytotoxic T lymphocytes. APMIS. 106:665-679.
33. Wenzel, T., and W. Baumeister. 1995. Conformational constraints in protein degradation by the 20S proteasome. Nat. Struct. Biol. 2:199-204.
34. Shen, H., J.F. Miller, X. Fan, D. Kolwyck, R. Ahmed, and J.T. Harty. 1998. Compartmentalization of bacterial antigens: differential effects on priming of CD8 T cells and protective immunity. Cell. 92:535-545.
35. Brooks, P.C., A.M. Montgomery, M. Rosenfeld, R.A. Reisfeld, T. Hu, G. Klier, and D.A. Cheresh. 1994. Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell. 79:1157-1164.
36. Hofmann, U.B., A.A. Eggert, K. Blass, E.B. Brocker, and J.C. Becker. 2003. Expression of matrix metalloproteinases in the microenvironment of spontaneous and experimental melanoma metastases reflects the requirements for tumor formation. Cancer Res. 63:8221-8225.
37. Mizejewski, G.J. 1999. Role of integrins in cancer: survey of expression patterns. Proc. Soc. Exp. Biol. Med. 222:124-138.
38. Itoh, T., M. Tanioka, H. Yoshida, T. Yoshioka, H. Nishimoto, and S. Itohara. 1998. Reduced angiogenesis and tumor progression in gelatinase A-deficient mice. Cancer Res. 58:1048-1051.
39. Liotta, L.A., K. Tryggvason, S. Garbisa, I. Hart, C.M. Foltz, and S. Shafie. 1980. Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature. 284:67-68.
40. Pfeifer, A., T. Kessler, S. Silletti, D.A. Cheresh, and I.M. Verma. 2000. Suppression of angiogenesis by lentiviral delivery of PEX, a noncatalytic fragment of matrix metalloproteinase 2. Proc. Natl. Acad. Sci. USA. 97:12227-12232.
41. Coussens, L.M., B. Fingleton, and L.M. Matrisian. 2002. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science. 295:2387-2392.
42. Pluderi, M., V. Lucini, D. Caronzolo, M. Pannacci, F. Costa, G. Carrabba, C. Giussani, S. Grosso, F. Colleoni, F. Scaglione, et al. 2003. Long-term inhibition of glioma growth by systemic administration of human PEX. J. Neurosurg. Sci. 47:69-78.
43. Sheu, B.C., S.M. Hsu, H.N. Ho, H.C. Lien, S.C. Huang, and R.H. Lin. 2001. A novel role of metalloproteinase in cancer-mediated immunosuppression. Cancer Res. 61:237-242.
44. Guilloux, Y., S. Lucas, V.G. Brichard, A. Van Pel, C. Viret, E. De Plaen, F. Brasseur, B. Lethe, F. Jotereau, and T. Boon. 1996. A peptide recognized by human cytolytic T lymphocytes on HLA-A2 melanomas is encoded by an intron sequence of the N-acetylglucosaminyltransferase V gene. J. Exp. Med. 183:1173-1183.
45. Moreau-Aubry, A., S. Le Guiner, N. Labarriere, M.C. Gesnel, F. Jotereau, and R. Breathnach. 2000. A processed pseudogene codes for a new antigen recognized by a CD8(+) T cell clone on melanoma. J. Exp. Med. 191:1617-1624.
46. Viret, C., F. Davodeau, Y. Guilloux, J.D. Bignon, G. Semana, R. Breathnach, and F. Jotereau. 1993. Recognition of shared melanoma antigen by HLA-A2-restricted cytolytic T cell clones derived from human tumor-infiltrating lymphocytes. Eur. J. Immunol. 23:141-146.
47. Brichard, V., A. Van Pel, T. Wolfel, C. Wolfel, E. De Plaen, B. Lethe, P. Coulie, and T. Boon. 1993. The tyrosinase gene codes for an antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J. Exp. Med. 178:489-495.
48. Hansen, M.B., S.E. Nielsen, and K. Berg. 1989. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods. 119:203-210.
49. Labarriere, N., E. Diez, M.C. Pandolfino, C. Viret, Y. Guilloux, S. Le Guiner, J.F. Fonteneau, B. Dreno, and F. Jotereau. 1997. Optimal T cell activation by melanoma cells depends on a minimal level of antigen transcription. J. Immunol. 158:1238-1245.
50. Barille, S., R. Bataille, M.J. Rapp, J.L. Harousseau, and M. Amiot. 1999. Production of metalloproteinase-7 (matrilysin) by human myeloma cells and its potential involvement in metalloproteinase-2 activation. J. Immunol. 163:5723-5728.