Decorin is a novel antagonistic ligand of the Met receptor

Journal of Cell Biology

Volumn 185, Issue 4, 2009, Pages 743-754

  Goldoni, Silvia ^a   Humphries, Ashley ^a   Nyström, Alexander ^a   Sattar, Sampurna ^a   Owens, Rick T ^b   McQuillan, David J ^b   Ireton, Keith ^c   Iozzo, Renato V ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b LIFECELL CORPORATION   (United States)

^c UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BETA CATENIN; CBL PROTEIN; DECORIN; EPIDERMAL GROWTH FACTOR RECEPTOR; INTERNALIN B; LIGAND; PROTEIN; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; TYROSINE KINASE RECEPTOR; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CELL GROWTH; CELL MIGRATION; CONTROLLED STUDY; DRUG MECHANISM; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; RECEPTOR UPREGULATION; TUMOR GROWTH;

BETA CATENIN; BINDING, COMPETITIVE; CELL PROLIFERATION; EXTRACELLULAR MATRIX PROTEINS; HALF-LIFE; HELA CELLS; HUMANS; LIGANDS; NEOPLASM METASTASIS; NEOPLASMS; PROTEIN BINDING; PROTEOGLYCANS; PROTO-ONCOGENE PROTEINS C-CBL; PROTO-ONCOGENE PROTEINS C-MET;

BACTERIA (MICROORGANISMS);

EID: 66149095761     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200901129     Document Type: Article

References (65)

1. Aberle, H., A. Bauer, J. Stappert, A. Kispert, and R. Kemler. 1997. β-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16:3797-3804. (Pubitemid 27280995)
2. Athauda, G., A. Giubellino, J.A. Coleman, C. Horak, P.S. Steeg, M.-J. Lee, J. Trepel, J. Wimberly, J. Sun, A. Coxon, et al. 2006. c-Met ectodomain shedding rate correlates with malignant potential. Clin. Cancer Res. 12:4154-4162.
3. Basilico, C., A. Arnesano, M. Galuzzo, P.M. Comoglio, and P. Michieli. 2008. A high affinity hepatocyte growth factor-binding site in the immunoglobulin- like region of Met. J. Biol. Chem. 283:21267-21277.
4. Berthou, S., D.M. Aebersold, L.S. Schimdt, D. Stroka, C. Heigl, B. Streit, D. Stalder, G. Gruber, S. Liang, A.R. Howlett, et al. 2004. The Met kinase inhibitor SU11274 exhibits a selective inhibition pattern toward different receptor mutated variants. Oncogene. 23:5387-5393. (Pubitemid 39005814)
5. Bi, X., C. Tong, A. Dokendorff, L. Banroft, L. Gallagher, G. Guzman-Hartman, R.V. Iozzo, L.H. Augenlicht, and W. Yang. 2008. Genetic deficiency of decorin causes intestinal tumor formation through disruption of intestinal cell maturation. Carcinogenesis. 29:1435-1440.
6. Biglari, A., D. Bataille, U. Naumann, M. Weller, J. Zirger, M.G. Castro, and P.R. Lowenstein. 2004. Effects of ectopic decorin in modulating intracranial glioma progression in vivo, in a rat syngeneic model. Cancer Gene Ther. 11:721-732. (Pubitemid 39488470)
7. Birchmeier, C., W. Birchmeier, E. Gherardi, and G.F. Vande Woude. 2003. MET, metastasis, motility and more. Nat. Rev. Mol. Cell Biol. 4:915-925. (Pubitemid 37493640)
8. Brandan, E., C. Cabello-Verrugio, and C. Vial. 2008. Novel regulatory mechanisms for the proteoglycans decorin and biglycan during muscle formation and muscular dystrophy. Matrix Biol. 27:700-708.
9. Braun, L., F. Nato, B. Payrastre, J.-C. Mazié, and P. Cossart. 1999. The 213-amino-acid leucine-rich repeat region of the Listeria monocytogenes lnlB protein is sufficient for entry into mammalian cells, stimulation of Pl 3-kinase and membrane ruffling. Mol. Microbiol. 34:10-23. (Pubitemid 29460482)
10. Clevers, H. 2006. Wnt/β-catenin signaling in development and disease. Cell. 127:469-480. (Pubitemid 44647433)
11. Csordás, G., M. Santra, C.C. Reed, I. Eichstetter, D.J. McQuillan, D. Gross, M.A. Nugent, G. Hajnóczky, and R.V. Iozzo. 2000. Sustained down-regulation of the epidermal growth factor receptor by decorin. A mechanism for controlling tumor growth in vivo. J. Biol. Chem. 275:32879-32887.
12. Danilkovitch-Miagkova, A., and B. Zbar. 2002. Dysregulation of Met receptor tyrosine kinase activity in invasive tumors. J. Clin. Invest. 109:863-867. (Pubitemid 34275106)
13. Disson, O., S. Grayo, E. Huillet, G. Nikitas, F. Langa-Vives, O. Dussurget, M. Ragon, A. Le Monnier, C. Babinet, P. Cossart, and M. Lecuit. 2008. Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. Nature. 455:1114-1118.
14. Engelman, J.A., K. Zejnullahu, T. Mitsudomi, Y. Song, C. Hyland, J.O. Park, N. Lindeman, C.-M. Gale, X. Zhao, J. Christensen, et al. 2007. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science. 316:1039-1043. (Pubitemid 46799492)
15. Gao, X., M. Lorinczi, K.S. Hill, N.C. Brooks, H. Dokainish, K. Ireton, and L.A. Elferink. 2009. Met receptor tyrosine kinase degradation is altered in response to the leucine-rich repeat of the Lysteria invasion protein internalin B. J. Biol. Chem. 284:774-783.
16. Gentile, A., L. Trusolino, and P.M. Comoglio. 2008. The Met tyrosine kinase receptor in development and cancer. Cancer Metastasis Rev. 27:85-94.
17. Goldoni, S., and R.V. Iozzo. 2008. Tumor microenvironment: modulation by decorin and related molecules harboring leucine-rich tandem motifs. Int. J. Cancer. 123:2473-2479.
18. Goldoni, S., D.G. Seidler, J. Heath, M. Fassan, R. Baffa, M.L. Thakur, R.A. Owens, D.J. McQuillan, and R.V. Iozzo. 2008. An anti-metastatic role for decorin in breast cancer. Am. J. Pathol. 173:844-855.
19. Grant, D.S., C. Yenisey, R.W. Rose, M. Tootell, M. Santra, and R.V. Iozzo. 2002. Decorin suppresses tumor cell-mediated angiogenesis. Oncogene. 21:4765-4777.
20. Hammond, D.E., S. Carter, J. McCullough, S. Urbé, G. Van Woude, and M.J. Clague. 2003. Endosomal dynamics of Met determine signaling output. Mol. Biol. Cell. 14:1346-1354. (Pubitemid 36547405)
21. Herynk, M.H., R. Tsan, R. Radinsky, and G.E. Gallick. 2003. Activation of c-Met in colorectal carcinoma cells leads to constitutive association of tyrosine-phopshorylated β-catenin. Clin. Exp. Metastasis. 20:291-300. (Pubitemid 36745657)
22. Iozzo, R.V. 1998. Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67:609-652. (Pubitemid 28411140)
23. Iozzo, R.V. 2005. Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev. Mol. Cell Biol. 6:646-656. (Pubitemid 41081268)
24. Iozzo, R.V., F. Chakrani, D. Perrotti, D.J. McQuillan, T. Skorski, B. Calabretta, and I. Eichstetter. 1999a. Cooperative action of germline mutations in decorin and p53 accelerates lymphoma tumorigenesis. Proc. Natl. Acad. Sci. USA. 96:3092-3097. (Pubitemid 29148849)
25. Iozzo, R.V., D. Moscatello, D.J. McQuillan, and I. Eichstetter. 1999b. Decorin is a biological ligand for the epidermal growth factor receptor. J. Biol. Chem. 274:4489-4492. (Pubitemid 129501451)
26. Ireton, K. 2007. Entry of the bacterial Listeria monocytogenes into mammalian cells. Cell. Microbiol. 9:1365-1375. (Pubitemid 46774010)
27. Ishibe, S., J.E. Haydu, A. Togawa, A. Marlier, and L.G. Cantley. 2006. Cell confluence regulates hepatocyte growth factor-stimulated cell morphogenesis in a β-catenin-dependent manner. Mol. Cell. Biol. 26:9232-9243.
28. Jo, M., D.B. Stolz, J.E. Esplen, K. Dorko, G.K. Michalopoulos, and S.C. Strom. 2000. Cross-talk between epidermal growth factor receptor and c-Met signal pathways in transformed cells. J. Biol. Chem. 275:8806-8811. (Pubitemid 30180235)
29. Klein, P.S., and D.A. Melton. 1996. A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. USA. 93:8455-8459. (Pubitemid 26269579)
30. Knudsen, B.S., and G. Vande Woude. 2008. Showering c-MET-dependent cancers with drugs. Curr. Opin. Genet. Dev. 18:87-96.
31. Levitzki, A., and A. Gazit. 1995. Tyrosine kinase inhibition: an approach to drug development. Science. 267:1782-1788.
32. Li, N., G.-S. Xiang, H. Dokainish, K. Ireton, and L.A. Elferink. 2005. The Listeria protein internalin B mimics hepatocyte growth factor-induced receptor trafficking. Traffic. 6:459-473. (Pubitemid 40740386)
33. Li, N., M. Lorinczi, K. Ireton, and L.A. Elferink. 2007. Specific Grb2-mediated interactions regulate clathrin-dependent endocytosis of the cMet-tyrosine kinase. J. Biol. Chem. 282:16764-16775. (Pubitemid 47093241)
34. Li, X., Y. Huang, J. Jiang, and S.J. Frank. 2008a. ERK-dependent threonine phosphorylation of EGF receptor modulates receptor downregulation and signaling. Cell. Signal. 20:2145-2155.
35. Li, X., A. Pennisi, and S. Yaccoby. 2008b. Role of decorin in the antimyeloma effects of osteoblasts. Blood. 112:159-168.
36. Machner, M.P., S. Frese, W.-D. Schubert, V. Orian-Rousseau, E. Gherardi, J. Wehland, H.H. Niemann, and D.W. Heinz. 2003. Aromatic amino acids at the surface of InIB are essential for host cell invasion by Listeria monocytogenes. Mol. Microbiol. 48:1525-1536.
37. Monga, S.P., W.M. Mars, P. Pediaditakis, A. Bell, K. Mulé, W.C. Bowen, X. Wang, R. Zarnegar, and G.K. Michalopoulos. 2002. Hepatocyte growth factor induces Wnt-independent nuclear translocation of beta-catenin after MET-beta- catenin dissociation in hepatocytes. Cancer Res. 62:2064-2071. (Pubitemid 34408453)
38. Müller, T., G. Bain, X. Wang, and J. Papkoff. 2002. Regulation of epithelial cell migration and tumor formation by β-catenin signaling. Exp. Cell Res. 280:119-133. (Pubitemid 35230373)
39. Nath, D., N.J. Williamson, R. Jarvis, and G. Murphy. 2001. Shedding of c-Met is regulated by crosstalk between a G-protein coupled receptor and the EGF receptor and is mediated by a TIMP-3 sensitive metalloproteinase. J. Cell Sci. 114:1213-1220. (Pubitemid 32288534)
40. Niemann, H.H., V. Jäger, P.J.G. Butler, J. van den Heuvel, S. Schmidt, D. Ferraris, E. Gherardi, and D.W. Heinz. 2007. Structure of the human receptor tyrosine kinase Met in complex with the Listeria invasion protein lnlB. Cell. 130:235-246. (Pubitemid 47081132)
41. Niemann, H.H., M.V. Petoukhov, M. Härtlein, M. Moulin, E. Gherardi, P. Timmins, D.W. Heinz, and D.I. Svergun. 2008. X-ray and neutron small-angle scattering analysis of the complex formed by the Met receptor and the Listeria monocytogenes invasion protein InIB. J. Mol. Biol. 377:489-500.
42. Petit, A.M.V., J. Rak, M.-C. Hung, P. Rockwell, N. Goldstein, B. Fendly, and R.S. Kerbel. 1997. Neutralizing antibodies against epidermal growth factor and Erb-2/neu receptor tyrosine kinases down-regulated vascular endothelial growth factor production by tumor cells in vitro and in vivo. Angiogenic implications for signal transduction therapy of solid tumors. Am. J. Pathol. 151:1523-1530. (Pubitemid 27527914)
43. Petrelli, A., G.F. Gilestro, S. Lanzardo, P.M. Comoglio, N. Migone, and S. Giordano. 2002. The endophilin-CIN85-Cbl complex mediates ligand-dependent downregulation of c-Met. Nature. 416:187-190. (Pubitemid 34246477)
44. Petrelli, A., P. Circosta, L. Granziero, M. Mazzone, A. Pisacane, S. Fenoglio, P.M. Comoglio, and S. Giordano. 2006. Ab-induced ectodomain shedding mediates hepatocyte growth factor receptor down-regulation and hampers biological activity. Proc. Natl. Acad. Sci. USA. 103:5090-5095.
45. Ramirez, F., and D.B. Rifkin. 2003. Cell signaling events: a view from the matrix. Matrix Biol. 22:101-107. (Pubitemid 36627468)
46. Rasola, A., M. Fassetta, F. De Bacco, L. D'Alessandro, D. Gramaglia, M.G. Di Renzo, and P.M. Comoglio. 2007. A positive feedback loop between hepatocyte growth factor receptor and β-catenin sustains colorectal cancer cell invasive growth. Oncogene. 26:1078-1087. (Pubitemid 46272209)
47. Reed, C.C., J. Gauldie, and R.V. Iozzo. 2002. Suppression of tumorigenicity by adenovirus-mediated gene transfer of decorin. Oncogene. 21:3688-3695. (Pubitemid 34620532)
48. Reed, C.C., A. Waterhouse, S. Kirby, P. Kay, R.A. Owens, D.J. McQuillan, and R.V. Iozzo. 2005. Decorin prevents metastatic spreading of breast cancer. Oncogene. 24:1104-1110. (Pubitemid 40313888)
49. Reznik, T.E., Y. Sang, Y. Ma, R. Abounader, E.M. Rosen, S. Xia, and J. Laterra. 2008. Transcription-dependent epidermal growth factor receptor activation by hepatocyte growth factor. Mol. Cancer Res. 6:139-215.
50. Rodeck, U., M. Herlyn, D. Herlyn, C. Molthoff, B. Atkinson, M. Varello, Z. Steplewski, and H. Koprowski. 1987. Tumor growth modulation by a monoclonal antibody to the epidermal growth factor receptor: immunologically mediated and effector cell-independent effects. Cancer Res. 47:3692-3696. (Pubitemid 17105710)
51. Santra, M., T. Skorski, B. Calabretta, E.C. Lattime, and R.V. Iozzo. 1995. De novo decorin gene expression suppresses the malignant phenotype in human colon cancer cells. Proc. Natl. Acad. Sci. USA. 92:7016-7020.
52. Santra, M., I. Eichstetter, and R.V. Iozzo. 2000. An anti-oncogenic role for decorin: downregulation of ErbB2 leads to growth suppression and cytodifferentiation of mammary carcinoma cells. J. Biol. Chem. 275:35153-35161.
53. Schaefer, L., and R.V. Iozzo. 2008. Biological functions of the small leucinerich proteoglycans: from genetics to signal transduction. J. Biol. Chem. 283:21305-21309.
54. Schlessinger, J. 2000. Cell signaling by receptor tyrosine kinases. Cell. 103:211-225.
55. Seidler, D.G., S. Goldoni, C. Agnew, C. Cardi, M.L. Thakur, R.A. Owens, D.J. McQuillan, and R.V. Iozzo. 2006. Decorin protein core inhibits in vivo cancer growth and metabolism by hindering epidermal growth factor receptor function and triggering apoptosis via caspase-3 activation. J. Biol. Chem. 281:26408-26418. (Pubitemid 44401849)
56. Shen, Y., M. Naujokas, M. Park, and K. Ireton. 2000. lnlB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell. 103:501-510.
57. Shintani, K., A. Matsumine, K. Kusuzaki, J. Morikawa, T. Matsubara, T. Wakabayashi, K. Araki, H. Satonaka, H. Wakabayashi, T. Lino, and A. Uchida. 2008. Decorin suppresses lung metastases of murine osteosarcoma. Oncol. Rep. 19:1533-1539.
58. Sigismund, S., E. Argenzio, D. Tosoni, E. Cavallaro, S. Polo, and P.P. Di Fiore. 2008. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev. Cell. 15:209-219.
59. Stamos, J., R.A. Lazarus, X. Yao, D. Kirchhofer, and C. Wiesmann. 2004. Crystal structure of the HGF β-chain in complex with the Sema domain of the Met receptor. EMBO J. 23:2325-2335. (Pubitemid 38954840)
60. Stommel, J.M., A.C. Kimmelman, H. Ying, R. Nabioullin, A.H. Ponugoti, R. Wiedemeyer, A.H. Stegh, J.E. Bradner, K.L. Ligon, C. Brennan, et al. 2007. Coactivation of receptor tyrosine kinases affects the response of tumor cells to target therapies. Science. 318:287-290. (Pubitemid 47574858)
61. Tralhão, J.G., L. Schaefer, M. Micegova, C. Evaristo, E. Schönherr, S. Kayal, H. Veiga-Fernandes, C. Danel, R.V. Iozzo, H. Kresse, and P. Lemarchand. 2003. In vivo selective and distant killing of cancer cells using adenovirus-mediated decorin gene transfer. FASEB J. 17:464-466.
62. Trusolino, L., and P.M. Comoglio. 2002. Scatter-factor and semaphorin receptors: cell signalling for invasive growth. Nat. Rev. Cancer. 2:289-301. (Pubitemid 37328782)
63. Weigelt, B., and M.J. Bissell. 2008. Unraveling the microenvironmental influences on the normal mammary gland and breast cancer. Semin. Cancer Biol. 18:311-321.
64. Zafiropoulos, A., D. Nikitovic, P. Katonis, A. Tsatsakis, N.K. Karamanos, and G.N. Tzanakakis. 2008. Decorin-induced growth inhibition is overcome through protracted expression and activation of epidermal growth factor receptors in osteosarcoma cells. Mol. Cancer Res. 6:785-794.
65. Zhu, J.-X., S. Goldoni, G. Bix, R.A. Owens, D. McQuillan, C.C. Reed, and R.V. Iozzo. 2005. Decorin evokes protracted internalization and degradation of the EGF receptor via caveolar endocytosis. J. Biol. Chem. 280:32468-32479. (Pubitemid 41361859)