Enhanced transformation by a plasma membrane-associated met oncoprotein: Activation of a phosphoinositide 3'-kinase-dependent autocrine loop involving hyaluronic acid and CD44

Molecular and Cellular Biology

Volumn 20, Issue 10, 2000, Pages 3482-3496

  Kamikura, Darren M ^a,d   Khoury, Hanane ^b   Maroun, Christiane ^a   Naujokas, Monica A ^a   Park, Morag ^a,b,c  

^a MCGILL UNIVERSITY   (Canada)

^b ROYAL VICTORIA HOSPITAL   (Canada)

^c MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^d USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HERMES ANTIGEN; HYALURONIC ACID; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; CARCINOGENESIS; CELL CULTURE; CELL TRANSFORMATION; ENZYME ACTIVATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGENS, CD44; AUTOCRINE COMMUNICATION; CELL MEMBRANE; CELL TRANSFORMATION, NEOPLASTIC; HEPATOCYTE GROWTH FACTOR; HYALURONIC ACID; MEMBRANE PROTEINS; MICE; MICE, NUDE; MYRISTIC ACID; NUCLEAR PORE COMPLEX PROTEINS; ONCOGENE PROTEINS, FUSION; PHOSPHOPROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MET; PROTO-ONCOGENE PROTEINS PP60(C-SRC); SARCOMA, EXPERIMENTAL;

EID: 0034095213     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.10.3482-3496.2000     Document Type: Article

References (80)

1. Alessi, D. R., M. Andjelkovic, F. B. Caudwell, P. Cron, N. Maorrica, P. Cohen, and B. Hemmings. 1996. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15:6541-6551.
2. Alessi, D. R., S. R. James, C. P. Downes, A. B. Holmes, P. R. Gaffney, C. B. Reese, and P. Cohen. 1997. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase B alpha. Curr. Biol. 7:261-269.
3. Amundadottir, L. T., and P. Leder. 1998. Signal transduction pathways activated and required for mammary carcinogenesis in response to specific oncogenes. Oncogene 16:737-746.
4. Aruffo, A., I. Stamenkovic, M. Melnick, C. B. Underhill, and B. Seed. 1990. CD44 is the principal cell surface receptor for hyaluronate. Cell 61:1303-1313.
5. Backer, J. M., M. G. J. Myers, S. E. Shoelson, D. J. Chin, X. J. Sun, M. Mirapeix, P. Hu, B. Margolis, E. Y. Skolnik, J. Schlessinger, and M. F. White. 1992. Phosphatidylinositol 3′-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 11:3469-3479.
6. Benard, V., B. P. Bohl, and G. M. Bokoch. 1999. Characterization of Rac and CDC42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J. Biol. Chem. 274:13198-13204.
7. 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 376:768-771.
8. Bottaro, D. P., J. S. Rubin, D. L. Faletto, A.-L. 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.
9. Brunet, A., A. Bonni, M. J. Zigmond, M. Z. Lin, P. Juo, L. S. Hu, M. J. Anderson, K. C. Arden, J. Blenis, and M. E. Greenberg. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868.
10. Catterall, J. B., M. J. Gardner, L. M. Jones, and G. A. Turner. 1997. Binding of ovarian cancer cells to immobilized hyaluronic acid. Glycoconj. J. 14: 867-869.
11. Cerione, R. A., and Y. Zheng. 1996. The Dbl family of oncogenes. Curr. Opin. Cell Biol. 8:216-222.
12. Cloutier, J. F., L. M. Chow, and A. Veillette. 1995. Requirement of the SH3 and SH2 domains for the inhibitory function of tyrosine protein kinase p50csk in T lymphocytes. Mol. Cell. Biol. 15:5937-5944.
13. Corley-Mastick, C., M. J. Bradley, and A. R. Saltiel. 1995. Insulin stimulates the tyrosine phosphorylation of caveolin. J. Cell Biol. 129:1523-1531.
14. Cotran, R. S., V. Kumar, and S. L. Robbins. 1974. Robbins - Pathologic basis of disease, 5th ed. W. B. Saunders Company, Philadelphia, Pa.
15. Cross, D. A., D. R. Alessi, P. Cohen, M. Andjelkovich, and B. A. Hemmings. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785-789.
16. Derman, M. P., J. Y. Chen, K. C. Spokes, Z. Songyang, and L. G. Cantley. 1996. An 11 amino acid sequence from c-met initiates epithelial chemotaxis via phosphatidylinositol 3-kinase and phospholipase C. J. Biol. Chem. 271: 4251-4255.
17. Di Renzo, M. F., M. Olivero, S. Ferro, M. Prat, I. Bongarzone, A. Belfiore, A. Costantino, R. Vigneri, M. A. Pierotti, and P. M. Comoglio. 1992. Overexpression of the c-MET/HGF receptor gene in human thyroid carcinomas. Oncogene 7:2549-2553.
18. Ebens, A., K. Brose, E. D. Leonardo, M. G. J. Hanson, F. Bladt, C. Birchmeier, B. A. Barres, and M. Tessier-Lavigne. 1996. Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 17:1157-1172.
19. Fixman, E. D., T. M. Fournier, D. M. Kamikura, M. A. Naujokas, and M. Park. 1996. Pathways downstream of Shc and Grb2 are required for cell transformation by the Tpr-Met oncoprotein. J. Biol. Chem. 271:13116-13122.
20. Fixman, E. D., M. Holgado-Madruga, L. Nguyen, D. M. Kamikura, T. M. Fournier, A. J. Wong, and M. Park. 1997. Efficient cellular transformation by the Met oncoprotein requires a functional Grb2 binding site and correlates with phosphorylation of the Grb2-associated proteins Cb1 and Gab1. J. Biol. Chem. 272:20167-20172.
21. Fixman, E. D., M. A. Naujokas, G. A. Rodrigues, M. F. Moran, and M. Park. 1995. Efficient cell transformation by the Tpr-Met oncoprotein is dependent upon tyrosine 489 in the carboxy-terminus. Oncogene 10:237-249.
22. Fournier, T. M., D. Kamikura, K. Teng, and M. Park. 1996. Branching tubulogenesis, but not scatter of Madin-Darby canine kidney cells requires a functional Grb2 binding site in the Met receptor tyrosine kinase. J. Biol. Chem. 271:22211-22217.
23. Franke, T. F., S.-I. Yang, T. O. Chan, K. Datta, A. Kazlauskas, D. K. Morrison, D. R. Kaplan, and P. N. Tsichlis. 1995. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736.
24. Fruman, D. A., R. E. Meyers, and L. C. Cantley. 1998. Phosphoinositide kinases. Annu. Rev. Biochem. 67:481-507.
25. Green, S. J., G. Tarone, and C. B. Underhill. 1988. Aggregation of macrophages and fibroblasts is inhibited by a monoclonal antibody to the hyaluronan receptor. Exp. Cell Res. 178:224-232.
26. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-514.
27. Hamada, J.-I., Y. Sawamura, and E. G. Van Meir. 1998. CD44 expression and growth factors. Front. Biosci. 3:D657-D664.
28. Harder, T., and K. Simons. 1997. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 9:534-542.
29. Holgado-Madruga, M., D. R. Emlet, D. K. Moscatello, A. K. Godwin, and A. J. Wong. 1996. A Grb2-associated docking protein in EGF-and insulin-receptor signalling. Nature 379:560-564.
30. Holgado-Madruga, M., D. K. Moscatello, D. R. Emlet, R. Dieterich, and A. J. Wong. 1997. Grb2-associated binder-1 mediates phosphatidylinositol 3-kinase activation and the promotion of cell survival by nerve growth factor. Proc. Natl. Acad. Sci. USA 94:12419-12424.
31. Howard, J. 1997. Molecular motors: structural adaptations to cellular functions. Nature 389:561-567.
32. Isakoff, S. J., T. Cardozo, J. Andreev, Z. Li, K. M. Ferguson, R. Abagyan, M. A. Lemmon, A. Aronheim, and E. Y. Skolnik. 1998. Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast. EMBO J. 17:5374-5387.
33. Jeffers, M., S. Koochekpour, M. Fiscella, B. K. Sathyanarayana, and G. F. Vande Woude. 1998. Signaling requirements for oncogenic forms of the Met tyrosine kinase receptor. Oncogene 17:2691-2700.
34. Jeffers, M., L. Schmidt, N. Nakigawa, C. P. Webb, G. Weirich, T. Kishida, B. Zbar, and G. F. Vande Woude. 1997. Activating mutations for the Met tyrosine kinase receptor in human cancer. Proc. Natl. Acad. Sci. USA 94: 11445-11450.
35. Kamikura, D. M., M. A. Naujokas, and M. Park. 1996. Identification of tyrosine 489 in the carboxy terminus of the Tpr-Met oncoprotein as a major site of autophosphorylation. Biochemistry 35:1010-1017.
36. Kane, L. P., V. S. Shapiro, D. Stokoe, and A. Weiss. 1999. Induction of NF-kappaB by the Akt/PKB kinase. Curr. Biol. 9:601-604.
37. Khwaja, A., K. Lehmann, B. M. Marte, and J. Downward. 1998. Phosphoinositide 3-kinase induces scattering and tubulogenesis in epithelial cells through a novel pathway. J. Biol. Chem. 273:18793-18801.
38. Klippel, A., M.-A. Escobedo, M. S. Wachowwicz, G. Apell, T. W. Brown, M. A. Giedllin, W. M. Kavanaugh, and L. T. Williams. 1998. Activation of phosphatidylinositol 3-kinase is sufficient for cell cycle entry and promotes cellular changes characteristic of cellular transformation. Mol. Cell. Biol. 18: 5699-5711.
39. Klippel, A., C. Reinhard, W. M. Kavanaugh, G. Apell, M. A. Escobedo, and L. T. Williams. 1996. Membrane localization of phosphatidylinositol 3-kinase is sufficient to activate multiple signal-transducing kinase pathways. Mol. Cell. Biol. 16:4117-4127.
40. Lamb, R. F., R. F. Hennigan, K. Turnbull, K. D. Katsanakis, E. D. MacKenzie, G. D. Birnie, and B. W. Ozanne. 1997. AP-1-mediated invasion requires increased expression of the hyaluronan receptor CD44. Mol. Cell. Biol. 17:963-976.
41. Lemmon, M. A., K. M. Ferguson, and J. Schlessinger. 1996. PH domains: diverse sequences with a common fold recruit signaling molecules to the cell surface. Cell 85:621-624.
42. Liu, C., M. Park, and S. Tsao. 1992. Over-expression of met protooncogene but not epidermal growth factor receptor or c-erb2 in primary human colorectal carcinomas. Oncogene 7:181-185.
43. Maina, F., F. Casagranda, E. Audero, A. Simeone, P. M. Comoglio, R. Klein, and C. Ponzetto. 1996. Uncoupling of Grb2 from the Met receptor in vivo reveals complex roles in muscle development. Cell 87:531-542.
44. Maroun, C., M. Holgado-Madruga, I. Royal, M. A. Naujokas, T. M. Fournier, A. J. Wong, and M. Park. 1999. The Gab-1 PH domain is required for localization of Gab-1 at sites of cell-cell contact and epithelial morphogenesis downstream from the Met receptor tyrosine kinase. Mol. Cell. Biol. 19:1784-1799.
45. Murphy, W. M., J. B. Beckwith, and G. M. Farrow. 1994. Tumors of the kidney, bladder, and related structures, p. 98-121. In J. Rosai and L. H. Sobin (ed.), Atlas of tumor pathology, 3rd ed., vol. 11. Armed Forces Institute of Pathology, Bethesda, Md.
46. Myers, M. G. J., J. M. Backer, X. J. Sun, S. E. Shoelson, P. Hu, J. Schlessinger, M. Yoakim, B. Schaffhausen, and M. F. White. 1992. IRS-1 activates phosphatidylinositol 3′-kinase by associating with src homology 2 domains of p85. Proc. Natl. Acad. Sci. USA 89:10350-10354.
47. Nguyen, L., M. Holgado-Madruga, C. Maroun, E. D. Fixman, D. Kamikura, T. Fournier, A. Charest, M. L. Tremblay, A. J. Wong, and M. Park. 1997. Association of the multisubstrate docking protein Gab1 with the hepatocyte growth factor receptor requires a functional Grb2 binding site involving tyrosine 1356. J. Biol. Chem. 272:20811-20819.
48. Ohkawa, T., N. Ueki, T. Taguchi, Y. Shindo, M. Adachi, Y. Amuro, T. Hada, and K. Higashino. 1999. Stimulation of hyaluronan synthesis by tumor necrosis factor-alpha is mediated by the p50/p65 NF-kappa B complex in MRC-5 myofibroblasts. Biochim. Biophys. Acta 1448:416-424.
49. Park, M., M. Dean, C. S. Cooper, M. Schmidt, S. J. O'Brien, D. G. Blair, and G. Vande Woude. 1986. Mechanism of met oncogene activation. Cell 45: 895-904.
50. Pawson, T. 1995. Protein modules and signalling networks. Nature 373: 573-580.
51. Peck, D., and C. M. Isacke. 1996. CD44 phosphorylation regulates melanoma cell and fibroblast migration on, but not attachment to, a hyaluronan substratum. Curr. Biol. 6:884-890.
52. Ponzetto, C., A. Bardelli, F. Maina, P. Longati, G. Panayotou, R. Dhand, M. D. Waterfield, and P. M. Comoglio. 1993. A novel recognition motif for phosphatidylinositol 3-kinase binding mediates its association with the hepatocyte growth factor/scatter factor receptor. Mol. Cell. Biol. 13:4600-4608.
53. Ponzetto, C., A. Bardelli, Z. Zhen, F. Maina, P. dalla Zonca, S. Giordano, A. Graziani, G. Panayotou, and P. M. Comoglio. 1994. A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/scatter factor receptor family. Cell 77:261-271.
54. Rodrigues, G. A., M. A. Naujokas, and M. Park. 1991. Alternative splicing generates isoforms of the met receptor tyrosine kinase which undergo differential processing. Mol. Cell. Biol. 11:2962-2970.
55. 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.
56. Rodrigues, G. A., and M. Park. 1993. Dimerization mediated by a leucine zipper oncogenically activates the met receptor tyrosine kinase. Mol. Cell. Biol. 13:6711-6722.
57. Rodrigues, G. A., M. Park, and J. Schlessinger. 1997. Activation of the JNK pathway is essential for transformation by the Met oncogene. EMBO J. 16: 2634-2645.
58. Rong, S., M. Jeffers, J. H. Resau, I. Tsaarfaty, M. Oskarsson, and G. F. Vande Woude. 1993. Met expression and sarcoma tumorigenicity. Cancer Res. 53:5355-5360.
59. Royal, I., and M. Park. 1995. Hepatocyte growth factor induced scatter of MDCK cells requires phosphatidylinositol 3-kinase. J. Biol. Chem. 270: 27780-27787.
60. Sander, E. E., S. van Delft, J. P. ten Klooster, T. Reid, R. A. van der Kammen, F. Michiels, and J. G. Collard. 1998 Matrix-dependent Tiam1/ Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell Biol. 143: 1385-1398.
61. 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 373:699-702.
62. Schmidt, L., F.-M. Duh, F. Chen, T. Kishida, G. Glenn, P. Choyke, S. W. Scherer, Z. Zhuang, I. Lubensky, M. Dean, R. Allikmets, A. Chidambaram, U. R. Bergerheim, J. T. Feltis, C. Casadevall, A. Zamarron, M. Bernues, S. Richard, C. J. M. Lips, M. M. Walther, L.-C. Tsui, L. Geil, M. L. Orcutt, T. Stackhouse, J. Lipan, L. Slife, H. Brauch, J. Decker, G. Neihens, M. D. Hughson, H. Moch, S. Storkel, M. I. Lerman, W. M. Linehan, and B. Zber. 1997. Germline and somatic mutations in the tyrosine kinase domain of the Met proto-oncogene in papillary renal carcinomas. Nat. Genet. 16:68-73.
63. Shayesteh, L., Y. Lu, W.-L. Kuo, R. Baldocchi, T. Godfrey, C. Collins, D. Pinkel, B. Powell, G. B. Mills, and J. W. Gray. 1999. PIK3CA is implicated as an oncogene in ovarian cancer. Nat. Genet. 21:99-102.
64. 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.
65. Spicer, A., and J. A. McDonald. 1998. Characterization and molecular evolution of a vertebrate hyaluronan synthase gene family. J. Biol. Chem. 273: 1923-1932.
66. Stambolic, V., A. Suzuki, J. L. de la Pompa, G. M. Brothers, C. Mirtsos, T. Sasaki, J. Ruland, J. M. Penninger, D. P. Siderovski, and T. W. Mak. 1998. Negative regulation of PKB/Akt-dependent cell survival by the tumor supressor gene PTEN. Cell 95:29-39.
67. Sy, M. S., D. Liu, R. Schiavone, J. Ma, H. Mori, and Y. Guo. 1996. Interactions between CD44 and hyaluronic acid: their role in tumor growth and metastasis. Curr. Top. Microbiol. Immunol. 213:129-153.
68. Tang, E. D., G. Nunez, F. G. Barr, and K. L. Guan. 1999. Negative regulation of the forkhead transcription factor FKHR by Akt. J. Biol. Chem. 274: 16741-16746.
69. Taylor, S. J., and D. Shalloway. 1996. Cell cycle-dependent activation of Ras. Curr. Biol. 6:1621-1627.
70. Thomas, G., and M. N. Hall. 1997. TOR signalling and control of cell growth. Curr. Opin. Cell Biol. 9:782-787.
71. Tsao, M. S., H. Zhu, A. Giaid, J. Viallet, T. Nakamura, and M. Park. 1993. Hepatocyte growth factor/scatter factor is an autocrine factor for human normal bronchial epithelial and lung carcinoma cells. Cell Growth Differ. 4: 571-579.
72. Tsukita, S., K. Oishi, N. Sato, J. Sagara, A. Kawai, and S. Tsukita. 1994. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J. Cell Biol. 126:391-401.
73. 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 373:702-705.
74. Weidner, K. M., S. Di Cesare, M. Sachs, V. Brinkmann, J. Behrens, and W. Birchmeier. 1996. Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis. Nature 384:173-176.
75. 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.
76. Whitman, M., D. R. Kaplan, B. Schaffhausen, L. Cantley, and T. M. Roberts. 1985. Association of phosphatidylinositol kinase activity with polyoma middle-T competent for transformation. Nature 315:239-242.
77. Wu, X., K. Senechal, M. S. Neshat, Y. E. Whang, and C. L. Sawyers. 1998. The PTEN/MMAC1 tumor supressor phosphatase functions as a negative regulator of the phosphoinositide 3-kinase/Akt pathway. Proc. Natl. Acad. Sci. USA 95:15587-15591.
78. Yang, X. M., and M. Park. 1995. Expression of the hepatocyte growth factor/scatter factor receptor tyrosine kinase is localized to epithelia in the adult mouse. Lab. Investig. 73:483-491.
79. Yang, X. M., K. Vogan, P. Gros, and M. Park. 1996. Expression of the Met receptor tyrosine kinase in muscle progenitor cells in somites and limbs is absent in Splotch mice. Development 122:2163-2171.
80. Zhu, H., M. A. Naujokas, E. D. Fixman, K. Torossian, and M. Park. 1994. Tyrosine 1356 in the carboxyl-terminal tail of the HGF/SF receptor is essential for the transduction of signals for cell motility and morphogenesis. J. Biol. Chem. 269:29943-29948.