Two independent signaling pathways mediate the antiapoptotic action of macrophage-stimulating protein on epithelial cells

Molecular and Cellular Biology

Volumn 20, Issue 6, 2000, Pages 2218-2227

  Danilkovitch, Alla ^a   Donley, Shannon ^a   Skeel, Alison ^a   Leonard, Edward J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR; INTEGRIN; MACROPHAGE ACTIVATING FACTOR; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ADHESION; CELL SURVIVAL; ENZYME ACTIVATION; EPITHELIUM CELL; EXTRACELLULAR MATRIX; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS; CELL LINE; DOGS; EPITHELIAL CELLS; GROWTH SUBSTANCES; HEPATOCYTE GROWTH FACTOR; MAP KINASE SIGNALING SYSTEM; PROTEIN PRECURSORS; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0033995556     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.6.2218-2227.2000     Document Type: Article

References (89)

1. Alessi, D. R., and P. Cohen. 1998. Mechanism of activation and function of protein kinase B. Curr. Opin. Genet. Dev. 8:55-62.
2. Alessi, D. R., A. Cuenda, P. Cohen, D. T. Dudley, and A. R. Saltiel. 1995. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 270:27489-27494.
3. Aplin, A. E., and R. L Juliano. 1999. Integrin and cytoskeletal regulation of growth factor signaling to the MAP kinase pathway. J. Cell Sci. 112:695-706.
4. Assoian, R. K., and X. Zhu. 1997. Cell anchorage and the cytoskeleton as partners in growth factor dependent cell cycle progression. Curr. Opin. Cell Biol. 9:93-98.
5. Berra, E., M. T. Diaz-Meco, and J. Moscat. 1998. The activation of p38 and apoptosis by the inhibition of Erk is antagonized by the phosphoinositide 3-kinase/Akt pathway. J. Biol. Chem. 273:10792-10797. (Erratum, 273:16630.)
6. Blume-Jensen, P., R. Janknecht, and T. Hunter. 1998. The kit receptor promotes cell survival via activation of PI 3-kinase and subsequent Akt-mediated phosphorylation of Bad on Ser136. Curr. Biol. 8:779-782.
7. Boudreau, N., C. J. Sympson, Z. Werb, and M. J. Bissell. 1995. Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 267:891-893.
8. Bozzo, C., G. Bellomo, L. Silengo, G. Tarone, and F. Altruda. 1997. Soluble integrin ligands and growth factors independently rescue neuroblastoma cells from apoptosis under nonadherent conditions. Exp. Cell Res. 237:326-337.
9. Clark, E. A., and J. S. Brugge. 1995. Integrins and signal transduction pathways: the road taken. Science 268:233-239.
10. Cooper, J. A., F. S. Esch, S. S. Taylor, and T. Hunter. 1984. Phosphorylation sites in enolase and lactate dehydrogenase utilized by tyrosine protein kinases in vivo and in vitro. J. Biol. Chem. 259:7835-7841.
11. Coucouvanis, E., and G. R. Martin. 1995. Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 83:279-287.
12. Cowley, S., H. Paterson, P. Kemp, and C. J. Marshall. 1994. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77:841-852.
13. Danilkovitch, A., and E. J. Leonard. 1999. Kinases involved in MSP/RON signaling. J. Leukoc. Biol. 65:345-348.
14. Danilkovitch, A., A. Skeel, and E. J. Leonard. 1999. Macrophage stimulating protein-induced epithelial cell adhesion is mediated by a PI3-K dependent but FAK independent mechanism. Exp. Cell Res. 248:575-582.
15. Darmon, A. J., D. W. Nicholson, and R. C. Bleackley. 1995. Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature 377:446-448.
16. Datta, K., T. F. Franke, T. O. Chan, A. Makris, S. I. Yang, D. R. Kaplan, D. K. Morrison, E. A. Golemis, and P. N. Tsichlis. 1995. AH/PH domain-mediated interaction between Akt molecules and its potential role in Akt regulation. Mol. Cell. Biol. 15:2304-2310.
17. Day, M. L., R. G. Foster, K. C. Day, X. Zhao, P. Humphrey, P. Swanson, A. A. Postigo, S. H. Zhang, and D. C. Dean. 1997. Cell anchorage regulates apoptosis through the retinoblastoma tumor suppressor/E2F pathway. J. Biol. Chem. 272:8125-8128.
18. Degen, S. J., L. A. Stuart, S. Han, and C. S. Jamison. 1991. Characterization of the mouse cDNA and gene coding for a hepatocyte growth factor-like protein: expression during development. Biochemistry 30:9781-9791.
19. Downward, J. 1998. Mechanisms and consequences of activation of protein kinase B/Akt. Curr. Opin. Cell Biol. 10:262-267.
20. Dudek, H., S. R. Datta, T. F. Franke, M. J. Birnbaum, R. Yao, G. M. Cooper, R. A. Segal, D. R. Kaplan, and M. E. Greenberg. 1997. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275: 661-665.
21. Eves, E. M., W. Xiong, A. Bellacosa, S. G. Kennedy, P. N. Tsichlis, M. R. Rosner, and N. Hay, 1998. Akt, a target of phosphatidylinositol 3-kinase, inhibits apoptosis in a differentiating neuronal cell line. Mol. Cell. Biol. 18:2143-2152.
22. Fan, S., J. A. Wang, R. Q. Yuan, S. Rockwell, J. Andres, A. Zlatapolskiy, I. D. Goldberg, and E. M. Rosen. 1998. Scatter factor protects epithelial and carcinoma cells against apoptosis induced by DNA-damaging agents. Oncogene 17:131-141.
23. Fernandes-Alnemri, T., G. Litwack, and E. S. Alnemri. 1994. CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1 beta-converting enzyme. J. Biol. Chem. 269:30761-30764.
24. Folkman, J., and A. Moscona. 1978. Role of cell shape in growth control. Nature 273:345-349.
25. Franke, T. F., D. R. Kaplan, and L. C. Cantley. 1997. PI3K: downstream AKTion blocks apoptosis. Cell 88:435-437.
26. Freedman, V. H., and S. I. Shin. 1974. Cellular tumorigenicity in nude mice: correlation with cell growth in semi-solid medium. Cell 3:355-359.
27. Frisch, S. M., and H. Francis. 1994. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124:619-626.
28. Frisch, S. M., and E. Ruoslahti. 1997. Integrins and anoikis. Curr. Opin. Cell Biol. 9:701-706.
29. Frisch, S. M., K. Vuori, E. Ruoslahti, and P. Y. Chan-Hui. 1996. Control of adhesion-dependent cell survival by focal adhesion kinase. J. Cell Biol. 134: 793-799.
30. Gardner, A. M., and G. L. Johnson. 1996. Fibroblast growth factor-2 suppression of tumor necrosis factor alpha-mediated apoptosis requires Ras and the activation of mitogen-activated protein kinase. J. Biol. Chem. 271:14560-14566.
31. Gaudino, G., A. Follenzi, L. Naldini, C. Collesi, M. Santoro, K. A. Gallo, P. J. Godowski, and P. M. Comoglio. 1994. Ron is a heterodimeric tyrosine kinase receptor activated by the HGF homologue MSP. EMBO J. 13:3524-3532.
32. Giancotti, F. G. 1997. Integrin signaling: specificity and control of cell survival and cell cycle progression. Curr. Opin. Cell Biol. 9:691-700.
33. Guillonneau, X., M. Bryckaert, C. Launay-Longo, Y. Courtois, and F. Mascarelli. 1998. Endogenous FGF1-induced activation and synthesis of extracellular signal-regulated kinase 2 reduce cell apoptosis in retinal-pigmented epithelial cells. J. Biol. Chem. 273:22367-22373.
34. Hall, P. A., P. J. Coates, B. Ansari, and D. Hopwood. 1994. Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J. Cell Sci. 107:3569-3577.
35. Hockenbery, D. 1995. Defining apoptosis. Am. J. Pathol. 144:16-19.
36. Hungerford, J. E., M. T. Compton, M. L. Matter, B. G. Hoffstrom, and C. A. Otey. 1996. Inhibition of pp125FAK in cultured fibroblasts results in apoptosis. J. Cell Biol. 135:1383-1390.
37. Hynes, R. O. 1992. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69:11-25.
38. Iwama, A., K. Okano, T. Sudo, Y. Matsuda, and T. Suda. 1994. Molecular cloning of a novel receptor tyrosine kinase gene, STX, derived from enriched hematopoietic stem cells. Blood 83:3160-3169.
39. Izzard, R. A., S. P. Jackson, and G. C. Smith. 1999. Competitive and noncompetitive inhibition of the DNA-dependent protein kinase. Cancer Res. 59:2581-2586.
40. Joseph-Silverstein, J., and R. L. Silverstein. 1998. Cell adhesion molecules: an overview. Cancer Investig. 16:176-182.
41. Juliano, R. 1996. Cooperation between soluble factors and integrin-mediated cell anchorage in the control of cell growth and differentiation. Bioessays 18:911-917.
42. Kauffmann-Zeh, A., P. Rodriguez-Viciana, E. Ulrich, C. Gilbert, P. Coffer, J. Downward, and G. Evan. 1997. Suppression of c-Myc-induced apoptosis by Ras signalling through PI(3)K and PKB. Nature 385:544-548.
43. Kennedy, S. G., A. J. Wagner, S. D. Conzen, J. Jordan, A. Bellacosa, P. N. Tsichlis, and N. Hay. 1997. The PI 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes Dev. 11:701-713.
44. Khwaja, A., and J. Downward. 1997. Lack of correlation between activation of Jun-NH2-terminal kinase and induction of apoptosis after detachment of epithelial cells. J. Cell Biol. 139:1017-1023.
45. Khwaja, A., P. Rodriguez-Viciana, S. Wennstrom, P. H. Warne, and J. Downward. 1997. Matrix adhesion and Ras transformation both activate a phosphoinositide 3-OH kinase and protein kinase B/Akt cellular survival pathway. EMBO J. 16:2783-2793.
46. Kulik, G., and M. J. Weber. 1998. Akt-dependent and -independent survival signaling pathways utilized by insulin-like growth factor I. Mol. Cell. Biol. 18:6711-6718.
47. Kumar, C. C. 1998. Signaling by integrin receptors. Oncogene 17:1365-1373.
48. Le Gall, M., D. Grall, J. C. Chambard, J. Pouyssegur, and E. Van Obberghen-Schilling. 1998. An anchorage-dependent signal distinct from p42/44 MAP kinase activation is required for cell cycle progression. Oncogene 17:1271-1277.
49. Leonard, E. J., and A. Skeel. 1976. A serum protein that stimulates macrophage movement, chemotaxis and spreading. Exp. Cell Res. 102:434-438.
50. Leonard, E. J., and A. H. Skeel. 1978. Isolation of macrophage stimulating protein (MSP) from human serum. Exp. Cell Res. 114:117-126.
51. Majno, G., and I. Joris. 1995. Apoptosis, oncosis, and necrosis. An overview of cell death. Am. J. Pathol. 146:3-15.
52. McGill, G., A. Shimamura, R. C. Bates, R. E. Savage, and D. E. Fisher. 1997. Loss of matrix adhesion triggers rapid transformation-selective apoptosis in fibroblasts. J. Cell Biol. 138:901-911.
53. Meredith, J. E. J., B. Fazeli, and M. A. Schwartz. 1993. The extracellular matrix as a cell survival factor. Mol. Biol. Cell 4:953-961.
54. Meredith, J. E. J., and M. A. Schwartz. 1997. Integrins, adhesion and apoptosis. Trends Cell Biol. 7:146-150.
55. Moro, L., M. Venturino, C. Bozzo, L. Silengo, F. Altruda, L. Beguinot, G. Tarone, and P. Defilippi. 1998. Integrins induce activation of EGF receptor: role in MAP kinase induction and adhesion-dependent cell survival. EMBO J. 17:6622-6632.
56. Navarro, P., A. M. Valverde, M. Benito, and M. Lorenzo. 1998. Insulin/IGF-I rescues immortalized brown adipocytes from apoptosis down-regulating Bcl-xS expression, in a PI 3-kinase- and map kinase-dependent manner. Exp. Cell Res. 243:213-221.
57. Nunez, G., and L. del Peso. 1998. Linking extracellular survival signals and the apoptotic machinery. Curr. Opin. Neurobiol. 8:613-618.
58. Otey, C. A. 1996. pp125FAK in the focal adhesion. Int. Rev. Cytol. 167:161-183.
59. Parrizas, M., A. R. Saltiel, and D. LeRoith. 1997. Insulin-like growth factor 1 inhibits apoptosis using the phosphatidylinositol 3′-kinase and mitogen-activated protein kinase pathways. J. Biol. Chem. 272:154-161.
60. Philpott, K. L., M. J. McCarthy, A. Klippel, and L. L. Rubin. 1997. Activated phosphatidylinositol 3-kinase and Akt kinase promote survival of superior cervical neurons. J. Cell Biol. 139:809-815.
61. Plopper, G. E., H. P. McNamee, L. E. Dike, K. Bojanowski, and D. E. Ingber. 1995. Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex. Mol. Biol. Cell 6:1349-1365.
62. Polakowska, R. R., M. Piacentini, R. Bartlett, L. A. Goldsmith, and A. R. Haake. 1994. Apoptosis in human skin development: morphogenesis, periderm, and stem cells. Dev. Dyn. 199:176-188.
63. Fowis, G., R. Bonjouklian, M. M. Berggren, A. Gallegos, R. Abraham, C. Ashendel, L. Zalkow, W. F. Matter, J. Dodge, and G. Grindey. 1994. Wortmannin, a potent and selective inhibitor of phosphatidylinositol-3-kinase. Cancer Res. 54:2419-2423.
64. Ronsin, C., F. Muscatelli, M. G. Mattel, and R. Breathnach. 1993. A novel putative receptor protein tyrosine kinase of the met family. Oncogene 8:1195-1202.
65. Rosenzweig, K. E., M. B. Youmell, S. T. Palayoor, and B. D. Price. 1997. Radiosensitization of human tumor cells by the phosphatidylinositol3-kinase inhibitors wortmannin and LY294002 correlates with inhibition of DNA-dependent protein kinase and prolonged G2-M delay. Clin. Cancer Res. 3:1149-1156.
66. Ruoslahti, E., and J. C. Reed. 1994. Anchorage dependence, integrins, and apoptosis. Cell 77:477-478.
67. Sanchez-Margalet, V., I. D. Goldfine, C. J. Vlahos, and C. K. Sung. 1994. Role of phosphatidylinositol-3-kinase in insulin receptor signaling: studies with inhibitor, LY294002. Biochem. Biophys. Res. Commun. 204:446-452.
68. Schaller, M. D., C. A. Otey, J. D. Hildebrand, and J. T. Parsons. 1995. Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains. J. Cell Biol. 130:1181-1187.
69. Scheid, M. P., and V. Duronio. 1998. Dissociation of cytokine-induced phosphorylation of Bad and activation of PKB/akt: involvement of MEK up-stream of Bad phosphorylation. Proc. Natl. Acad. Sci. USA 95:7439-7444.
70. Schlaepfer, D. D., and T. Hunter. 1997. Focal adhesion kinase overexpression enhances ras-dependent integrin signaling to ERK2/mitogen-activated protein kinase through interactions with and activation of c-Src. J. Biol. Chem. 272:13189-13195.
71. Schwartz, M. A. 1997. Integrins, oncogenes, and anchorage independence. J. Cell Biol. 139:575-578.
72. Seger, R., and E. G. Krebs. 1995. The MAPK signaling cascade. FASEB J. 9:726-735.
73. Songyang, Z., D. Baltimore, L. C. Cantley, D. R. Kaplan, and T. F. Franke. 1997. Interleukin 3-dependent survival by the Akt protein kinase. Proc. Natl. Acad. Sci. USA 94:11345-11350.
74. Stoker, M., C. O'Neill, S. Berryman, and V. Waxman. 1968. Anchorage and growth regulation in normal and virus-transformed cells. Int. J. Cancer 3:683-693.
75. Ui, M., T. Okada, K. Hazeki, and O. Hazeki. 1995. Wortmannin as a unique probe for an intracellular signalling protein, phosphoinositide 3-kinase. Trends Biochem. Sci. 20:303-307.
76. Ulrich, E., A. Duwel, A. Kauffmann-Zeh, C. Gilbert, D. Lyon, B. Rudkin, G. Evan, and D. Martin-Zanca. 1998. Specific TrkA survival signals interfere with different apoptotic pathways. Oncogene 16:825-832.
77. Valentinis, B., K. Reiss, and R. Baserga. 1998. Insulin-like growth factor-I-mediated survival from anoikis: role of cell aggregation and focal adhesion kinase. J. Cell. Physiol. 176:648-657.
78. Vlahos, C. J., W. F. Matter, K. Y. Hui, and R. F. Brown. 1994. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269:5241-5248.
79. Wang, M.-H., A. Iwama, A. A. Dlugosz, Y. Sun, A. Skeel, S. H. Yuspa, T. Suda, and E. J. Leonard. 1996. Macrophage stimulating protein induces proliferation and migration of murine keratinocytes. Exp. Cell Res. 226:39-46.
80. Wang, M.-H., A. Iwama, A. Skeel, T. Suda, and E. J. Leonard. 1995. The murine stk gene product, a transmembrane protein tyrosine kinase, is a receptor for macrophage stimulating protein. Proc. Natl. Acad. Sci. USA 92:3933-3937.
81. Wang, M.-H., F. A. Montero-Julian, I. Dauny, and E. J. Leonard. 1996. Requirement of phosphatidylinositol-3 kinase for epithelial cell migration activated by human macrophage stimulating protein. Oncogene 13:2167-2175.
82. Wang, M.-H., C. Ronsin, M.-C. Gesnel, L. Coupey, A. Skeel, E. J. Leonard, and R. Breathnach. 1994. Identification of the ron gene product as the receptor for the human macrophage stimulating protein. Science 266:117-119.
83. Wary, K. K., F. Mainiero, S. J. Isakoff, E. E. Marcantonio, and F. G. Giancotti. 1996. The adaptor protein She couples a class of integrins to the control of cell cycle progression. Cell 87:733-743.
84. Werner, H., and D. Le Roith. 1997. The insulin-like growth factor-I receptor signaling pathways are important for tumorigenesis and inhibition of apoptosis. Crit. Rev. Oncog. 8:71-92.
85. Xia, Z., M. Dickens, J. Raingeaud, R. J. Davis, and M. E. Greenberg. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331.
86. Xu, L. H., L. V. Owens, G. C. Sturge, X. Yang, E. T. Liu, R. J. Craven, and W. G. Cance. 1996. Attenuation of the expression of the focal adhesion kinase induces apoptosis in tumor cells. Cell Growth Differ. 7:413-418.
87. Yao, R., and G. M. Cooper. 1995. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267: 2003-2006.
88. Yoshimura, T., N. Yuhki, M.-H. Wang, A. Skeel, and E. J. Leonard. 1993. Cloning, sequencing and expression of human macrophage stimulating protein (MSP) confirms MSP as a kringle protein, and locates the gene on chromosome 3. J. Biol. Chem. 268:15461-15468.
89. Yuspa, S. H., P. Hawley-Nelson, B. Koehler, and J. R. Stanley. 1980. A survey of transformation markers in differentiating epidermal cell lines in culture. Cancer Res. 40:4694-4703.