Degradation of the Met tyrosine kinase receptor by the ubiquitin- proteasome pathway

Molecular and Cellular Biology

Volumn 17, Issue 2, 1997, Pages 799-808

  Jeffers, Michael ^a   Taylor, Gregory A ^a   Weidner, K Michael ^b   Omura, Satoshi ^c   Vande Woude, George F ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c KITASATO INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; GROWTH FACTOR RECEPTOR; PROTEASOME; PROTEIN TYROSINE KINASE; SCATTER FACTOR; UBIQUITIN;

ANIMAL CELL; ARTICLE; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; RECEPTOR AFFINITY; SIGNAL TRANSDUCTION;

EID: 0031045984     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.2.799     Document Type: Article

References (68)

1. Bladt, F., D. Riethmacher, S. Isenmann, A. Aguzzi, and C. Birchmeier. 1995. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature (London) 375:768-771.
2. Bottaro, D. P., J. S. Rubin, D. L. Faletto, A. M. Chan, T. E. Kmiecik, G. F. Vande Woude, and S. A. Aaronson. 1991. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 251:802-804.
3. Brinkmann, V., H. Foroutan, M. Sachs, K. M. Weidner, and W. Birchmeier. 1995. Hepatocyte growth factor/scatter factor induces a variety of tissue-specific morphogenic programs in epithelial cells. J. Cell Biol. 131:1573-1586.
4. Brizzi, M. F., J. M. Blechman, G. Cavalloni, D. Givol, Y. Yarden, and L. Pegoraro. 1994. Protein kinase C-dependent release of a functional whole extracellular domain of the mast cell growth factor (MGF) receptor by MGF-dependent human myeloid cells. Oncogene 9:1583-1589.
5. Bussolino, F., M. F. Di Renzo, M. Ziche, E. Bocchietto, M. Olivero, L. Naldini, G. Guadino, L. Tamagnone, A. Coffer, and P. M. Comoglio. 1992. Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. J. Cell Biol. 119:629-641.
6. Carlberg, K., P. Tapley, C. Haystead, and L. Rohrschneider. 1991. The role of kinase activity and the kinase insert region in ligand-induced internalization and degradation of the c-fms protein. EMBO J. 10:877-883.
7. Ciechanover, A. 1994. The ubiquitin-proteasome proteolytic pathway. Cell 79:13-21.
8. Crepaldi, T., M. Prat, S. Giordano, E. Medico, and P. M. Comoglio. 1994. Generation of a truncated hepatocyte growth factor receptor in the endoplasmic reticulum. J. Biol. Chem. 269:1750-1755.
9. Deshaies, R. J. 1995. Make it or break it: the role of ubiquitin-dependent proteolysis in cellular regulation. Trends Cell Biol. 5:428-434.
10. Downing, J. R., M. F. Roussel, and C. J. Sherr. 1989. Ligand and protein kinase C downmodulate the colony-stimulating factor 1 receptor by independent mechanisms. Mol. Cell. Biol. 9:2890-2896.
11. Escobedo, J. A., P. J. Barr, and L. T. Williams. 1988. Role of tyrosine kinase and membrane-spanning domains in signal transduction by the platelet-derived growth factor receptor. Mol. Cell. Biol. 8:5126-5131.
12. Faletto, D. L., D. R. Kaplan, D. O. Halverson, E. R. Rosen, and G. F. Vande Woude. 1993. Signal transduction in c-met mediated motogenesis, p. 107-130. In I. D. Goldberg and E. M. Rosen (ed.), Hepatocyte growth factor-scatter factor (HGF-SF) and the c-Met receptor. Birkhäuser Verlag, Basel, Switzerland.
13. Faletto, D. L., I. Tsarfaty, T. E. Kmiecik, M. Gonzatti, T. Suzuki, and G. F. Vande Woude. 1992. Evidence for non-covalent clusters of the c-met protooncogene product. Oncogene 7:1149-1157.
14. Fenteany, G., R. F. Standaert, W. S. Lane, S. Choi, E. J. Corey, and S. L. Schreiber. 1995. Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268:726-731.
15. Galcheva-Gargova, Z., S. J. Theroux, and R. J. Davis. 1995. The epidermal growth factor receptor is covalently linked to ubiquitin. Oncogene 11:2649-2655.
16. Gherardi, E., M. Sharpe, K. Lane, A. Sirulnik, and M. Stoker. 1993. Hepatocyte growth factor/scatter factor (HGF/SF), the c-met receptor and the behaviour of epithelial cells. Symp. Soc. Exp. Biol. 47:163-181.
17. Giordano, S., M. F. Di Renzo, R. P. Narsimhan, C. S. Cooper, C. Rosa, and P. M. Comoglio. 1989. Biosynthesis of the protein encoded by the c-met protooncogene. Oncogene 4:1383-1388.
18. Grant, D. S., H. K. Kleinman, I. D. Goldberg, M. M. Bhargava, B. J. Nickloff, J. L. Kinsella, P. Polverini, and E. M. Rosen. 1993. Scatter factor induces blood vessel formation in vivo. Proc. Natl. Acad. Sci. USA 90:1937-1941.
19. Higashio, K., and N. Shima. 1993. Tumor cytotoxic activity of HGF-SF, p. 351-368. In I. D. Goldberg and E. M. Rosen (ed.), Hepatocyte growth factor-scatter factor (HGF-SF) and the c-Met receptor. Birkhäuser-Verlag, Basel, Switzerland.
20. Honegger, A. M., T. J. Dull, S. Felder, E. Van Obberghen, F. Bellot, D. Szapary, A. Schmidt, A. Ullrich, and J. Schlessinger. 1987. Point mutation at the ATP binding site of EGF receptor abolishes protein-tyrosine kinase activity and alters cellular routing. Cell 51:199-209.
21. Jeffers, M., S. Rong, M. Anver, and G. F. Vande Woude. 1996. Autocrine hepatocyte growth factor/scatter factor signaling induces transformation and the invasive/metastatic phenotype in C127 cells. Oncogene 13:853-861.
22. Jeffers, M., S. Rong, and G. F. Vande Woude. 1996. Hepatocyte growth factor/scatter factor-Met signalling in tumorigenicity and invasion/metastasis. J. Mol. Med. 74:505-513.
23. Lin, Y. J., and G. M. Clinton. 1991. A soluble protein related to the HER-2 proto-oncogene product is released from human breast carcinoma cells. Oncogene 6:639-643.
24. Lowy, D. R., E. Rands, and E. M. Scolnick. 1978. Helper-independent transformation by unintegrated Harvey sarcoma virus DNA. J. Virol. 26:291-298.
25. Matsumoto, K., and T. Nakamura. 1992. Hepatocyte growth factor: molecular structure, roles in liver regeneration, and other biological functions. Crit. Rev. Oncog. 3:27-54.
26. Matsumoto, K., and T. Nakamura. 1993. Roles of HGF as a pleiotropic factor in organ regeneration, p. 225-250. In I. D. Goldberg and E. M. Rosen (ed.), Hepatocyte growth factor-scatter factor (HGF-SF) and the met receptor. Birkhäuser-Verlag, Basel, Switzerland.
27. Misumi, Y., Y. Misumi, K. Miki, A. Takatsuki, G. Tamura, and Y. Ikehara. 1986. Novel blockade by Brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes. J. Biol. Chem. 261:11398-11403.
28. Miyazawa, K., K. Toyama, A. Gotoh, P. C. Hendrie, C. Mantel, and H. E. Broxmeyer. 1994. Ligand-dependent polyubiquitination of c-kit gene product: a possible mechanism of receptor down modulation in M07e cells. Blood 83:137-145.
29. Montesano, R., K. Matsumoto, T. Nakamura, and L. Orci. 1991. Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 67:901-908.
30. Mori, S., L. Claesson-Welsh, Y. Okuyama, and Y. Saito. 1995. Ligand-induced polyubiquitination of receptor tyrosine kinases. Biochem. Biophys. Res. Commun. 213:32-39.
31. Mori, S., C.-H. Heldin, and L. Claesson-Welsh. 1992. Ligand-induced polyubiquitination of the platelet-derived growth factor β-receptor. J. Biol. Chem. 267:6429-6434.
32. Mori, S., C.-H. Heldin, and L. Claesson-Welsh. 1993. Ligand-induced ubiquitination of the platelet-derived growth factor β-receptor plays a negative regulatory role in its mitogenic signaling. J. Biol. Chem. 268:577-583.
33. Mori, S., K. Tanaka, S. Omura, and Y. Saito. 1995. Degradation process of ligand-stimulated platelet-derived growth factor β-receptor involves ubiquitin-proteasome proteolytic pathway. J. Biol. Chem. 270:29447-29452.
34. Naldini, L., K. M. Weidner, E. Vigna, G. Gaudino, A. Bardelli, C. Ponzetto, R. P. Narsimhan, G. Hartmann, R. Zarnegar, G. K. Michalopoulos, W. Birchmeier, and P. M. Comoglio. 1991. Scatter factor and hepatocyte growth factor are indistinguishable ligands for the MET receptor. EMBO J. 10:2867-2878.
35. Nusrat, A., C. A. Parkos, A. E. Bacarra, P. J. Godowski, C. Delp-Archer, E. M. Rosen, and J. L. Madara. 1994. Hepatocyte growth factor/scatter factor effects on epithelia. Regulation of intercellular junctions in transformed and nontransformed cell lines, basolateral polarization of c-met receptor in transformed and natural intestinal epithelia, and induction of rapid wound repair in a transformed model epithelium. J. Clin Invest. 93:2056-2065.
36. O'Bryan, J. P., Y.-W. Fridell, R. Koski, B. Varnum, and E. T. Liu. 1995. The transforming receptor tyrosine kinase, Axl, is post-translationally regulated by proteolytic cleavage. J. Biol. Chem. 270:551-557.
37. Omura, S., T. Fujimoto, K. Otoguro, K. Matsuzaki, R. Moriguchi, H. Tanaka, and Y. Sasaki. 1991. Lactacystin, a novel microbial metabolite, induces neuritogenesis of neuroblastoma cells. J. Antibiot. (Tokyo) 44:113-116.
38. Omura, S., K. Matsuzaki, T. Fujimoto, K. Kosuge, T. Furuya, S. Fujita, and A. Nakagawa. 1991. Structure of lactacystin, a new microbial metabolite which induces differentiation of neuroblastoma cells. J. Antibiot. (Tokyo) 44:117-118.
39. Prat, M., T. Crepaldi, L. Gandino, S. Giordano, P. Longati, and P. Comoglio. 1991. C-terminal truncated forms of Met, the hepatocyte growth factor receptor. Mol. Cell. Biol. 11:5954-5962.
40. Pupa, S. M., S. Menard, D. Morelli, B. Pozzi, G. De Palo, and M. I. Colnaghi. 1993. The extracellular domain of the c-erbB-2 oncoprotein is released from tumor cells by proteolytic cleavage. Oncogene 8:2917-2923.
41. Rodrigues, G. A., and M. Park. 1994. Autophosphorylation modulates the kinase activity and oncogenic potential of the Met receptor tyrosine kinase. Oncogene 9:2019-2027.
42. Rong, S., M. Bodescot, D. Blair, J. Dunn, T. Nakamura, K. Mizuno, M. Park, A. Chan, S. Aaronson, and G. F. Vande Woude. 1992. Tumorigenicity of the met proto-oncogene and the gene for hepatocyte growth factor. Mol. Cell. Biol. 12:5152-5158.
43. Rose-John, S., and P. C. Heinrich. 1994. Soluble receptors for cytokines and growth factors: generation and biological function. J. 300:281-290.
44. Rubin, J. S., D. P. Bottaro, and S. A. Aaronson. 1993. Hepatocyte growth factor/scatter factor and its receptor, the c-met proto-oncogene product. Biochim. Biophys. Acta 1155:357-371.
45. Rusciano, D., P. Lorenzoni, and M. M. Burger. 1995. Expression of constitutively activated hepatocyte growth factor/scatter factor receptor (c-met) in B16 melanoma cells selected for enhanced liver colonization. Oncogene 11:1979-1987.
46. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.
47. Santos, O. F. P., E. J. G. Barros, X.-M. Yang, K. Matsumoto, T. Nakamura, M. Park, and S. K. Nigam. 1994. Involvement of hepatocyte growth factor in kidney development. Dev. Biol. 163:525-529.
48. Schmidt, C., F. Bladt, S. Goedecke, V. Brinkmann, W. Zschiesche, M. Sharpe, E. Gherardi, and C. Birchmeier. 1995. Scatter factor/hepatocyte growth factor is essential for liver development. Nature (London) 373:699-702.
49. Sonnenberg, E., D. Meyer, K. M. Weidner, and C. Birchmeier. 1993. Scatter factor/hepatocyte growth factor and its receptor, the c-met tyrosine kinase, can mediate a signal exchange between mesenchyme and epithelia during mouse development. J. Cell Biol. 123:223-235.
50. Soriano, J. V., M. S. Pepper, T. Nakamura, L. Orci, and R. Montesano. 1995. Hepatocyte growth factor stimulates extensive development of branching duct-like structures by cloned mammary gland epithelial cells. J. Cell Sci. 108:413-430.
51. Sorki, A., B. Westermark, C.-H. Heldin, and L. Claesson-Welsh. 1991. Effect of receptor kinase inactivation on the rate of internalization and degradation of PDGF and the PDGF β-receptor. J. Cell Biol. 112:469-478.
52. Southern, P. J., and P. Berg. 1982. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter. J. Mol. Appl. Genet. 1:327-341.
53. Stoker, M., E. Gherardi, M. Ferryman, and J. Gray. 1987. Scatter factor is a fibroblast-derived modulator of epithelial cell mobility. Nature (London) 327:239-242.
54. Streit, A., C. D. Stern, C. Thery, G. W. Ireland, S. Aparicio, M. J. Sharpe, and E. Gherardi. 1995. A role for HGF/SF in neural induction and its expression in Hensen's node during gastrulation. Development 121:813-824.
55. Trowbridge, I. S., J. F. Collawn, and C. R. Hopkins. 1993. Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol. 9:129-161.
56. Tsarfaty, I., J. H. Resau, S. Rulong, I. Keydar, D. L. Faletto, and G. F. Vande Woude. 1992. The met proto-oncogene receptor and lumen formation. Science 257:1258-1261.
57. Tsarfaty, I., S. Rong, J. H. Resau, S. Rulong, P. Pinto da Silva, and G. F. Vande Woude. 1994. Met mediated signaling in mesenchymal to epithelial cell conversion. Science 263:98-101.
58. Uehara, Y., O. Minowa, C. Mori, K. Shiota, J. Kuno, T. Noda, and N. Kitamura. 1995. Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature (London) 373:702-705.
59. Ullrich, A., and J. Schlessinger. 1990. Signal transduction by receptors with tyrosine kinase activity. Cell 61:203-212.
60. Weidner, K. M., M. Sachs, and W. Birchmeier. 1993. The Met receptor tyrosine kinase transduces motility, proliferation, and morphogenic signals of scatter factor/hepatocyte growth factor in epithelial cells. J. Cell Biol. 121:145-154.
61. Weidner, K. M., M. Sachs, D. Riethmacher, and W. Birchmeier. 1995. Mutation of juxtamembrane tyrosine residue 1001 suppresses loss-of-function mutations of the met receptor in epithelial cells. Proc. Natl. Acad. Sci. USA 92:2597-2601.
62. Wells, A., J. B. Welsh, C. S. Lazar, H. S. Wiley, G. N. Gill, and M. G. Rosenfeld. 1990. Ligand-induced transformation by a noninternalizing epidermal growth factor receptor. Science 247:962-964.
63. Woolf, A. S., M. Kolatsi-Joannou, P. Hardman, E. Anermarcher, C. Moorby, L. G. Fine, P. S. Jat, M. D. Noble, and E. Gherardi. 1995. Roles of hepatocyte growth factor/scatter factor and the met receptor in the early development the metanephros. J. Cell Biol. 128:171-184.
64. Cdc28-mediated control of Cln3 cyclin degradation. Mol. Cell. Biol. 15:731-741.
65. Yang, Y., E. Spitzer, D. Meyer, M. Sachs, C. Niemann, G. Hartmann, K. M. Weidner, C. Birchmeier, and W. Birchmeier. 1995. Sequential requirement of hepatocyte growth factor and neuregulin in the morphogenesis and differentiation of the mammary gland. J. Cell Biol. 131:1-12.
66. Yee, N. S., C.-W. M. Hsiau, H. Serve, K. Vosseller, and P. Besmer. 1994. Mechanism of down-regulation of c-kit receptor. J. Biol. Chem. 269:31991-31998.
67. Yee, N. S., H. Langen, and P. Besmer. 1993. Mechanism of kit ligand, phorbol ester, and calcium-induced down-regulation of c-kit receptors in mast cells. J. Biol. Chem. 268:14189-14201.
68. Zhen, Z., S. Giordano, P. Longati, E. Medico, M. Campiglio, and P. M. Comoglio. 1994. Structural and functional domains critical for constitutive activation of the HGF-receptor (Met). Oncogene 9:1691-1697.