Down-regulation of the met receptor tyrosine kinase by presenilin-dependent regulated intramembrane proteolysis

Molecular Biology of the Cell

Volumn 20, Issue 9, 2009, Pages 2495-2507

  Foveau, Bénédicte ^a   Ancot, Frédéric ^a   Leroy, Catherine ^a   Petrelli, Annalisa ^b   Reiss, Karina ^c   Vingtdeux, Valérie ^d   Giordano, Silvia ^b   Fafeur, Véronique ^a   Tulasne, David ^a  

^a INSTITUT DE BIOLOGIE DE LILLE   (France)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF KIEL   (Germany)

^d JEAN PIERRE AUBERT RESEARCH CENTER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA SECRETASE; LIGAND; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY DN30; PRESENILIN; PROTEASOME INHIBITOR; PROTEIN TYROSINE KINASE; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL MEMBRANE; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME DEGRADATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; MEMBRANE TRANSPORT; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN TRANSPORT; RECEPTOR DOWN REGULATION;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANTIBODIES; CELL LINE; CELL MEMBRANE; CELL PROLIFERATION; DOGS; DOWN-REGULATION; ENZYME ACTIVATION; ENZYME INHIBITORS; HEPATOCYTE GROWTH FACTOR; HUMANS; LIGANDS; METALLOPROTEASES; MICE; PEPTIDE FRAGMENTS; PRESENILINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTO-ONCOGENE PROTEINS C-MET; RECOMBINANT PROTEINS;

EID: 65649111648     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-09-0969     Document Type: Article

References (51)

1. Birchmeier, C., Birchmeier, W., Gherardi, E., and Vande Woude, G. F. (2003). Met, metastasis, motility and more. Nat. Rev. Mol. Cell Biol. 4 , 915-925. (Pubitemid 37493640)
2. Bladt, F., Riethmacher, D., Isenmann, S., Aguzzi, A., and Birchmeier, C. (1995). Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376 , 768-771.
3. Borowiak, M., Garratt, A. N., Wustefeld, T., Strehle, M., Trautwein, C., and Birchmeier, C. (2004). Met provides essential signals for liver regeneration. Proc. Natl. Acad. Sci. USA 101 , 10608-10613. (Pubitemid 38955789)
4. Brou, C., Logeat, F., Gupta, N., Bessia, C., LeBail, O., Doedens, J. R., Cumano, A., Roux, P., Black, R. A., and Israel, A. (2000). A novel proteolytic cleavage involved in Notch signaling: the role of the disintegrin- metalloprotease TACE. Mol. Cell 5 , 207-216. (Pubitemid 30628080)
5. Comoglio, P. M., Giordano, S., and Trusolino, L. (2008). Drug development of MET inhibitors: targeting oncogene addiction and expedience. Nat. Rev. Drug Discov. 7 , 504-516.
6. Crepaldi, T., Prat, M., Giordano, S., Medico, E., and Comoglio, P. M. (1994). Generation of a truncated hepatocyte growth factor receptor in the endoplasmic reticulum. J. Biol. Chem. 269 , 1750-1755. (Pubitemid 24035370)
7. De Strooper, B. (2003). Aph-1, Pen-2, and Nicastrin with Presenilin generate an active gamma-Secretase complex. Neuron 38 , 9-12. (Pubitemid 36423348)
8. Deheuninck, J., Foveau, B., Goormachtigh, G., Leroy, C., Ji, Z., Tulasne, D., and Fafeur, V. (2008). Caspase cleavage of the MET receptor generates an HGF interfering fragment. Biochem Biophys. Res. Commun. 367 , 573-577.
9. Di Renzo, M. F., et al. (1995). Overexpression and amplification of the met/ HGF receptor gene during the progression of colorectal cancer. Clin. Cancer Res. 1 , 147-154.
10. Foveau, B., Leroy, C., Ancot, F., Deheuninck, J., Ji, Z., Fafeur, V., and Tulasne, D. (2007). Amplification of apoptosis through sequential caspase cleavage of the MET tyrosine kinase receptor. Cell Death Differ. 14 , 752-764. (Pubitemid 46444513)
11. Galardy, R. E., Grobelny, D., Foellmer, H. G., and Fernandez, L. A. (1994). Inhibition of angiogenesis by the matrix metalloprotease inhibitor N-[2R-2-(hydroxamidocarbonymethyl)-4-methylpentanoyl)]-L-tryptophan methylamide. Cancer Res. 54 , 4715-4718. (Pubitemid 24276500)
12. Galvani, A. P., Cristiani, C., Carpinelli, P., Landonio, A., and Bertolero, F. (1995). Suramin modulates cellular levels of hepatocyte growth factor receptor by inducing shedding of a soluble form. Biochem. Pharmacol. 50 , 959-966.
13. Gambarotta, G., Boccaccio, C., Giordano, S., Ando, M., Stella, M. C., and Comoglio, P. M. (1996). Ets up-regulates MET transcription. Oncogene 13 , 1911-1917. (Pubitemid 26397450)
14. Giordano, S., Di Renzo, M. F., Narsimhan, R. P., Cooper, C. S., Rosa, C., and Comoglio, P. M. (1989). Biosynthesis of the protein encoded by the c-met proto-oncogene. Oncogene 4 , 1383-1388. (Pubitemid 19273394)
15. Hammond, D. E., Carter, S., McCullough, J., Urbe, S., Vande Woude, G., and Clague, M. J. (2003). Endosomal dynamics of Met determine signaling output. Mol. Biol. Cell 14 , 1346-1354. (Pubitemid 36547405)
16. Herreman, A., Serneels, L., Annaert, W., Collen, D., Schoonjans, L., and De Strooper, B. (2000). Total inactivation of gamma-secretase activity in presenilin-deficient embryonic stem cells. Nat. Cell Biol. 2 , 461-462.
17. Huovila, A. P., Turner, A. J., Pelto-Huikko, M., Karkkainen, I., and Ortiz, R. M. (2005). Shedding light on ADAM metalloproteinases. Trends Biochem. Sci. 30 , 413-422. (Pubitemid 40942037)
18. Ivan, M., Bond, J. A., Prat, M., Comoglio, P. M., and Wynford-Thomas, D. (1997). Activated ras and ret oncogenes induce over-expression of c-met (hepatocyte growth factor receptor) in human thyroid epithelial cells. Oncogene 14 , 2417-2423. (Pubitemid 27268160)
19. Jeffers, M., Taylor, G. A., Weidner, K. M., Omura, S., and Vande-Woude, G. F. (1997). Degradation of the Met tyrosine kinase receptor by the ubiquitinproteasome pathway. Mol. Cell. Biol. 17 , 799-808. (Pubitemid 27044379)
20. Kawaida, K., Matsumoto, K., Shimazu, H., and Nakamura, T. (1994). Hepatocyte growth factor prevents acute renal failure and accelerates renal regeneration in mice. Proc. Natl. Acad. Sci. USA 91 , 4357-4361. (Pubitemid 24143432)
21. Kopitz, C., et al. (2007). Tissue inhibitor of metalloproteinases-1 promotes liver metastasis by induction of hepatocyte growth factor signaling. Cancer Res. 67 , 8615-8623. (Pubitemid 47437437)
22. Landman, N., and Kim, T. W. (2004). Got RIP? Presenilin-dependent intramembrane proteolysis in growth factor receptor signaling. Cytokine Growth Factor Rev. 15 , 337-351. (Pubitemid 39140698)
23. Longati, P., Bardelli, A., Ponzetto, C., Naldini, L., and Comoglio, P. M. (1994). Tyrosines1234-1235 are critical for activation of the tyrosine kinase encoded by the MET proto-oncogene (HGF receptor). Oncogene 9 , 49-57. (Pubitemid 2020929)
24. Maina, F., Hilton, M. C., Ponzetto, C., Davies, A. M., and Klein, R. (1997). Met receptor signaling is required for sensory nerve development and HGF promotes axonal growth and survival of sensory neurons. Genes Dev. 11 , 3341-3350. (Pubitemid 28023958)
25. Mak, H. H., Peschard, P., Lin, T., Naujokas, M. A., Zuo, D., and Park, M. (2007). Oncogenic activation of the Met receptor tyrosine kinase fusion protein, Tpr-Met, involves exclusion from the endocytic degradative pathway. Oncogene 26 , 7213-7221. (Pubitemid 350085315)
26. Migliore, C., and Giordano, S. (2008). Molecular cancer therapy: can our expectation be MET? Eur. J. Cancer 44 , 641-651.
27. Mondino, A., Giordano, S., and Comoglio, P. M. (1991). Defective posttranslational processing activates the tyrosine kinase encoded by the MET protooncogene (hepatocyte growth factor receptor). Mol. Cell. Biol. 11 , 6084-6092. (Pubitemid 21895380)
28. Mumm, J. S., Schroeter, E. H., Saxena, M. T., Griesemer, A., Tian, X., Pan, D. J., Ray, W. J., and Kopan, R. (2000). A ligand-induced extracellular cleavage regulates gamma-secretase-like proteolytic activation of Notch1. Mol. Cell 5 , 197-206. (Pubitemid 30628079)
29. Nath, D., Williamson, N. J., Jarvis, R., and Murphy, G. (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)
30. Ni, C. Y., Murphy, M. P., Golde, T. E., and Carpenter, G. (2001). gamma-Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294 , 2179-2181. (Pubitemid 33150677)
31. Park, M., Dean, M., Cooper, C. S., Schmidt, M., O'Brien, S. J., Blair, D. G., and Vande Woude, G. F. (1986). Mechanism of met oncogene activation. Cell 45 , 895-904. (Pubitemid 16083694)
32. Peschard, P., Fournier, T. M., Lamorte, L., Naujokas, M. A., Band, H., Langdon, W. Y., and Park, M. (2001). Mutation of the c-Cbl TKB domain binding site on the Met receptor tyrosine kinase converts it into a transforming protein. Mol. Cell 8 , 995-1004. (Pubitemid 34031802)
33. Peschard, P., Ishiyama, N., Lin, T., Lipkowitz, S., and Park, M. (2004). A conserved DpYR motif in the juxtamembrane domain of the Met receptor family forms an atypical c-Cbl/Cbl-b tyrosine kinase binding domain binding site required for suppression of oncogenic activation. J. Biol. Chem. 279 , 29565-29571. (Pubitemid 38915838)
34. Petrelli, A., Circosta, P., Granziero, L., Mazzone, M., Pisacane, A., Fenoglio, S., Comoglio, P. M., and Giordano, S. (2006). Ab-induced ectodomain shedding mediates hepatocyte growth factor receptor down-regulation and hampers biological activity. Proc. Natl. Acad. Sci. USA 103 , 5090-5095.
35. Petrelli, A., Gilestro, G. F., Lanzardo, S., Comoglio, P. M., Migone, N., and Giordano, S. (2002). The endophilin-CIN85-Cbl complex mediates liganddependent downregulation of c-Met. Nature 416 , 187-190. (Pubitemid 34246477)
36. Ponzetto, C., Bardelli, A., Zhen, Z., Maina, F., dalla Zonca, P., Giordano, S., Graaziani, A., Panayotou, G., and Comoglio, P. M. (1994). A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/scatter factor receptor family. Cell 77 , 261-271. (Pubitemid 24138623)
37. Ponzetto, C., Giordano, S., Peverali, F., Della Valle, G., Abate, M. L., Vaula, G., and Comoglio, P. M. (1991). c-met is amplified but not mutated in a cell line with an activated met tyrosine kinase. Oncogene 6 , 553-559. (Pubitemid 21924118)
38. Pozner-Moulis, S., Pappas, D. J., and Rimm, D. L. (2006). Met, the hepatocyte growth factor receptor, localizes to the nucleus in cells at low density. Cancer Res. 66 , 7976-7982. (Pubitemid 44299161)
39. Prat, M., Crepaldi, T., Gandino, L., Giordano, S., Longati, P., and Comoglio, P. (1991). C-terminal truncated forms of Met, the hepatocyte growth factor receptor. Mol. Cell. Biol. 11 , 5954-5962. (Pubitemid 21895364)
40. Schmidt, C., Bladt, F., Goedecke, S., Brinkmann, V., Zschiesche, W., Sharpe, M., Gherardi, E., and Birchmeier, C. (1995). Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373 , 699-702.
41. Schmidt, L., et al. (1997). Germline and somatic mutations in the tyrosine kinase domain of the MET proto-oncogene in papillary renal carcinomas. Nat. Genet. 16 , 68-73. (Pubitemid 27198158)
42. Slack, B. E., Ma, L. K., and Seah, C. C. (2001). Constitutive shedding of the amyloid precursor protein ectodomain is up-regulated by tumour necrosis factor-alpha converting enzyme. Biochem. J. 357 , 787-794. (Pubitemid 32735158)
43. Struhl, G., and Adachi, A. (2000). Requirements for presenilin-dependent cleavage of notch and other transmembrane proteins. Mol. Cell 6 , 625-636.
44. Tulasne, D., Deheuninck, J., Lourenco, F. C., Lamballe, F., Ji, Z., Leroy, C., Puchois, E., Moumen, A., Maina, F., Mehlen, P., and Fafeur, V. (2004). Proapoptotic function of the MET tyrosine kinase receptor through caspase cleavage. Mol. Cell. Biol. 24 , 10328-10339. (Pubitemid 39507870)
45. Tulasne, D., and Foveau, B. (2008). The shadow of death on the MET tyrosine kinase receptor. Cell Death Differ 15 , 427-434.
46. Tulasne, D., Paumelle, R., Weidner, K. M., Vandenbunder, B., and Fafeur, V. (1999). The multisubstrate docking site of the MET receptor is dispensable for MET-mediated RAS signaling and cell scattering. Mol. Biol. Cell 10 , 551-565. (Pubitemid 29144623)
47. Uehara, Y., Minowa, O., Mori, C., Shlota, K., Kuno, J., Noda, T., and Kitamura, N. (1995). Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373 , 702-705.
48. Wajih, N., Walter, J., and Sane, D. C. (2002). Vascular origin of a soluble truncated form of the hepatocyte growth factor receptor (c-met). Circ. Res. 90 , 46-52. (Pubitemid 34074607)
49. Weidner, K. M., Sachs, M., and Birchmeier, W. (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.
50. Yant, J., Buluwela, L., Niranjan, B., Gusterson, B., and Kamalati, T. (1998). In vivo effects of hepatocyte growth factor/scatter factor on mouse mammary gland development. Exp. Cell Res. 241 , 476-481. (Pubitemid 28366573)
51. Zhang, L., Song, L., and Parker, E. M. (1999). Calpain inhibitor I increases beta-amyloid peptide production by inhibiting the degradation of the substrate of gamma-secretase. Evidence that substrate availability limits betaamyloid peptide production. J. Biol. Chem. 274 , 8966-8972. (Pubitemid 29164699)