Differential roles of protein kinase C and pertussis toxin-sensitive G- binding proteins in modulation of melanoma cell proliferation and motility by thrombospondin 1

Cancer Research

Volumn 58, Issue 14, 1998, Pages 3154-3162

  Guo, Neng Hua ^a   Zabrenetzky, Vivian S ^a   Chandrasekaran, Lakshmi ^a   Sipes, John M ^a   Lawler, Jack ^b   Krutzsch, Henry C ^a   Roberts, David D ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; CD36 ANTIGEN; GUANINE NUCLEOTIDE BINDING PROTEIN; PERTUSSIS TOXIN; PHOSPHATASE; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; THROMBOSPONDIN 1;

ANGIOGENESIS; ARTICLE; CANCER GROWTH; CELL MOTILITY; CELL PROLIFERATION; CHEMOTAXIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; MELANOMA CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PURIFICATION;

BLOOD PLATELETS; CELL DIVISION; CELL MOVEMENT; CHEMOTAXIS; CYCLIC AMP; ENZYME ACTIVATION; GTP-BINDING PROTEINS; HUMANS; INOSITOL PHOSPHATES; MELANOMA; PERTUSSIS TOXIN; PROTEIN KINASE C; THROMBOSPONDIN 1; TUMOR CELLS, CULTURED; VIRULENCE FACTORS, BORDETELLA;

EID: 0032527627     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Bornstein, P. Thrombospondins: structure and regulation of expression. FASEB J., 6: 3290-3299, 1992.
2. Bornstein, P. Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J. Cell Biol., 130: 503-506, 1995.
3. Roberts, D. D. Interactions of thrombospondin with sulfated glycolipids and proteoglycans of human melanoma cells. Cancer Res., 48: 6785-6793, 1988.
4. Asch, A. S., Silbiger, S., Heimer, E., and Nachman, R. L. Thrombospondin sequence motif (CSVTCG) is responsible for CD36 binding. Biochem. Biophys. Res. Commun., 182: 1208-1217, 1992.
5. Li, W. X., Howard, R. J., and Leung, L. L. Identification of SVTCG in thrombospondin as the conformation-dependent, high affinity binding site for its receptor, CD36. J. Biol. Chem., 268: 16179-16184, 1993.
6. Sipes, J. M., Guo, N., Negre, E., Vogel, T., Krutzsch, H. C., and Roberts, D. D. Inhibition of fibronectin binding and fibronectin-mediated cell adhesion to collagen by a peptide from the second type I repeat of thrombospondin. J. Cell Biol., 121: 469-477, 1993.
7. Schultz-Cherry, S., Chen, H., Mosher, D. F., Misenheimer, T. M., Krutzsch, H. C., Roberts, D. D., and Murphy-Ullrich, J. E. Regulation of transforming growth factor-β activation by discrete sequences of thrombospondin 1. J. Biol. Chem., 270: 7304-7310, 1995.
8. Guo, N. H., Krutzsch, H. C., Nègre, E., Vogel, T., Blake, D. A., and Roberts, D. D. Heparin-and sulfatide-binding peptides from the type I repeats of human thrombospondin promote melanoma cell adhesion. Proc. Natl. Acad. Sci. USA, 89: 3040-3044, 1992.
9. Hogg, P. J., Jimenez, B. M., and Chesterman, C. N. Identification of possible inhibitory reactive centers in thrombospondin 1 that may bind cathepsin G and neutrophil elastase. Biochemistry, 33: 6531-6537, 1994.
10. Lawler, J., Weinstein, R., and Hynes, R. O. Cell attachment to thrombospondin: the role of ARG-GLY-ASP, calcium, and integrin receptors. J. Cell Biol., 107: 2351-2361, 1988.
11. Gao, A. G., Lindberg, F. P., Dimitry, J. M., Brown, E. J., and Frazier, W. A. Thrombospondin modulates αvβ3 function through integrin-associated protein. J. Cell Biol., 135: 533-544, 1996.
12. Adams, J. C., and Lawler, J. Diverse mechanisms for cell attachment to platelet thrombospondin. J. Cell Sci., 104: 1061-1071, 1993.
13. Prater, C. A., Plotkin, J., Jaye, D., and Frazier, W. A. The properdin-like type I repeats of human thrombospondin contain a cell attachment site. J. Cell Biol., 112: 1031-1040, 1991.
14. Guo, N. H., Krutzsch, H. C., Nègre, E., Zabrenetzky, V. S., and Roberts, D. D. Heparin-binding peptides from the type I repeats of thrombospondin. Structural requirements for heparin binding and promotion of melanoma cell adhesion and chemotaxis. J. Biol. Chem., 267: 19349-19355, 1992.
15. Kosfeld, M. D., and Frazier, W. A. Identification of a new cell adhesion motif in two homologous peptides from the COOH-terminal cell binding domain of human thrombospondin. J. Biol. Chem., 268: 8808-8814, 1993.
16. Asch, A. S., Tepler, J., Silbiger, S., and Nachman, R. L. Cellular attachment to thrombospondin. Cooperative interactions between receptor systems. J. Biol. Chem., 266: 1740-1745, 1991.
17. Roberts, D. D., Sherwood, J. A., and Ginsburg, V. Platelet thrombospondin mediates attachment and spreading of human melanoma cells. J. Cell Biol., 104: 131-139, 1987.
18. Taraboletti, G., Roberts, D. D., and Liotta, L. A. Thrombospondin-induced tumor cell migration: haptotaxis and chemotaxis are mediated by different molecular domains. J. Cell Biol., 105: 2409-2415, 1987.
19. Zabrenetzky, V., Harris, C. C., Steeg, P. S., and Roberts, D. D. Expression of the extracellular matrix molecule thrombospondin inversely correlates with malignant progression in melanoma, lung and breast carcinoma cell lines. Int. J. Cancer, 59: 191-195, 1994.
20. Roberts, D. D. Regulation of tumor growth and metastasis by thrombospondin-1. FASEB J., 10: 1183-1191, 1996.
21. Weinstat-Saslow, D. L., Zabrenetzky, V. S., Van Houtte, K., Frazier, W. A., Roberts, D. D., and Steeg, P. S. Transfection of thrombospondin 1 complementary DNA into a human breast carcinoma cell line reduces primary tumor growth, metastatic potential, and angiogenesis. Cancer Res., 54: 6504-6511, 1994.
22. Guo, N., Krutzsch, H. C., Inman, J. K., and Roberts, D. D. Anti-proliferative and anti-tumor activities of D-reverse peptide mimetics derived from the second type-1 repeat of thrombospondin-1. J. Pept. Res., 50: 210-221, 1997.
23. Murphy-Ullrich, J. E., Gurusiddappa, S., Frazier, W. A., and Höök, M. Heparin-binding peptides from thrombospondins 1 and 2 contain focal adhesion-labilizing activity. J. Biol. Chem., 268: 26784-26789, 1993.
24. Gao, A-G., Lindberg, F. P., Finn, M. B., Blystone, S. D., Brown, E. J., and Frazier, W. A. Integrin-associated protein is a receptor for the C-terminal domain of thrombospondin. J. Biol. Chem., 271: 21-24, 1996.
25. Roberts, D. D., Cashel, J., and Guo, N. Purification of thrombospondin from human platelets. J. Tissue Cult. Methods, 16: 217-222, 1994.
26. Vogel, T., Guo, N. H., Krutzsch, H. C., Blake, D. A., Hartman, J., Mendelovitz, S., Panel, A., and Roberts, D. D. Modulation of endothelial cell proliferation, adhesion, and motility by recombinant heparin-binding domain and synthetic peptides from the type I repeats of thrombospondin. J. Cell. Biochem., 53: 74-84, 1993.
27. Legrand, C., Thibert, V., Dubernard, V., Begault, B., and Lawler, J. Molecular requirements for the interaction of thrombospondin with thrombin-activated human platelets: modulation of platelet aggregation. Blood, 79: 1995-2003, 1992.
28. Todaro, G. J., Fryling, C., and DeLarco, J. E. Transforming growth factors produced by certain human tumor cells: polypeptides that interact with epidermal growth factor receptors. Proc. Natl. Acad. Sci. USA, 77: 5258-5262, 1980.
29. Downes, C. P., Hawkins, P. T., and Irvine, R. F. Inositol 1,3,4,5-tetrakisphosphate and not phosphatidylinositol 3,4-bisphosphate is the probable precursor of inositol 1.3,4-trisphosphate in agonist-stimulated parotid gland. Biochem. J., 238: 501-506, 1986.
30. Berridge, M. J., Dawson, R. M. C., Downes, C. P., Heslop, J. P., and Irvine, R. F. Changes in the levels of inositol phosphates after agonist-dependent hydrolysis of membrane phosphoinositides. Biochem. J., 272: 473-482, 1983.
31. Barnwell, J. W., Ockenhouse, C. F., and Knowles, D. M. Monoclonal antibody OKM5 inhibits the in vitro binding of Plasmodium falciparum-infected erythrocytes to monocytes, endothelial, and C32 melanoma cells. J. Immunol., 135: 3494-3497, 1985.
32. Dawson, D. W., Pearce, S. F., Zhong, R., Silverstein, R. L., Frazier, W. A., and Bouck, N. P. CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J. Cell Biol., 138: 707-717, 1997.
33. Stracke, M. L., Guirguis, R., Liotta, L. A., and Schiffmann, E. Pertussis toxin inhibits stimulated motility independently of the anenylate cyclase pathway in human melanoma cells. Biochem. Biophys. Res. Commun., 146: 339-345, 1987.
34. Aznavoorian, S., Stracke, M. L., Parsons, J., McClanahan, J., and Liotta, L. A. Integrin αvβ3 mediates chemotactic and haptotactic motility in human melanoma cells through different signalling pathways. J. Biol. Chem., 271: 3247-3254, 1996.
35. Wessels, D., Murray, J., and Soll, D. R. Behavior of Dictyostelium amooebae is regulated primarily by the temporal dynamic of the natural cAMP wave. Cell Motil. Cytoskelet., 23: 145-156, 1992.
36. Caterina, M. J., and Devreotes, P. N. Molecular insights into eukaryotic chemotaxis. FASEB J., 5: 3078-3085, 1991.
37. Scott-Burden, T., Resink, T. J., Baur, U., Burgin, M., and Buhler, F. R. Activation of S6 kinase in cultured vascular smooth muscle cells by submitogenic levels of thrombospondin. Biochem. Biophys. Res. Commun., 150: 278-286, 1988.
38. Mc Atee, P., and Dawson, G. Rapid dephosphorylation of protein kinase C substrates by protein kinase A activators results from inhibition of diacylglycerol release. J. Biol. Chem., 264: 11193-11199, 1989.
39. Guillon, G., Gallo-Payet, N., Balestre, M-N., and Lombard, C. Cholera-toxin and corticotropin modulation of inositol phosphate accumulation induced by vasopressin and angiotensin II in rat glomerulosa cells. Biochem. J., 253: 765-775, 1988.
40. Ruoslahti, E., and Reed, J. C. Anchorage dependence, integrins, and apoptosis. Cell, 77: 477-478, 1994.
41. Juliano, R. Cooperation between soluble factors and integrin-mediated cell anchorage in the control of cell growth and differentiation. Bioessays, 18: 911-917, 1996.
42. Varner, J. A., and Cheresh, D. A. Integrins and cancer. Curr. Opin. Cell Biol., 8: 724-730, 1996.
43. Parsons, J. T. Integrin-mediated signalling: regulation by protein tyrosine kinases and small GTP-binding proteins. Curr. Opin. Cell Biol., 8: 146-152, 1996.
44. Juliano, R. L., and Haskill, S. Signal transduction from the extracellular matrix. J. Cell Biol., 120: 577-585, 1993.
45. Yamada, K. M., and Geiger, B. Molecular interactions in cell adhesion complexes. Curr. Opin. Cell Biol., 9: 76-85, 1997.
46. Guo, N., Krutzsch, H. C., Inman, J. K., and Roberts, D. D. Thrombospondin 1 and type I repeat peptides of thrombospondin 1 specifically induce apoptosis of endothelial cells. Cancer Res., 57: 1735-1742, 1997.
47. Koyama, H., Raines, E. W., Bornfeldt, K. E., Roberts, J. M., and Ross, R. Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of cdk2 inhibitors. Cell, 87: 1069-1078, 1996.
48. Aznavoorian, S., Stracke, M. L., Krutzsch, H., Schiffmann, E., and Liotta, L. Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells. J. Cell Biol., 110: 1427-1438, 1990.
49. Damsky, C., and Werb, Z. Signal transduction by integrin receptors for extracellular matrix: cooperative processing of extracellular information. Curr. Opin. Cell Biol., 4: 772-781, 1992.
50. Danilov, Y. N., and Juliano, R. L. Phorbol ester modulation of integrin-mediated cell adhesion: a postreceptor event. J. Cell Biol., 108: 1925-1933, 1989.
51. Lewis, J. M., Cheresh, D. A., and Schwanz, M. A. Protein kinase C regulates αvβ5-dependent cytoskeletal associations and focal adhesion kinase phosphorylation. J. Cell Biol., 134: 1323-1332, 1996.
52. Liu, B., Renaud, C., Nelson, K. K., Chen, Y. Q., Bazaz, R., Kowynia, J., Timar, J., Diglio, C. A., and Honn, K. V. Protein kinase C inhibitor calphostin C reduces B16 amelanotic melanoma adhesion to endothelium and lung colonization. Int. J. Cancer, 52: 147-152, 1992.
53. Lester, B. R., Weinstein, L. S., McCarthy, J. B., Sun, Z., Smith, R. S., and Furcht, L. T. The role of G-protein in matrix-mediated motility of highly and poorly invasive melanoma cells. Int. J. Cancer, 48: 113-120, 1991.
54. Yamanishi, D. T., and Meyskens, F. L., Jr. Alterations in gene expression and signal transductions in human melanocytes and melanoma cells. Crit. Rev. Oncog., 5: 429-450, 1994.
55. Taraboletti, G., Roberts, D., Liotta, L. A., and Giavazzi, R. Platelet thrombospondin modulates endothelial cell adhesion, motility, and growth: a potential angiogenesis regulatory factor. J. Cell Biol., 111: 765-772, 1990.
56. Murphy-Ullrich, J. E., Pallero, M. A., Boerth, N., Greenwood, J. A., Lincoln, T. M., and Cornwell, T. L. Cyclic GMP-dependent protein kinase is required for thrombospondin and tenascin mediated focal adhesion disassembly. J. Cell Sci., 109: 2499-2508, 1996.
57. Suchard, S. J., and Mansfield, P. J. Neutrophil thrombospondin receptors are linked to GTP-binding proteins. J. Cell. Physiol., 168: 217-227, 1996.
58. Mansfield, P. J., and Suchard, S. J. Thrombospondin promotes both chemotaxis and haptotaxis in neutrophil-like HL-60 cells. J Immunol., 150: 1959-1970, 1993.
59. Mansfield, P. J., and Suchard, S. J. Thrombospondin promotes chemotaxis and haptotaxis of human peripheral blood monocytes. J. Immunol., 153: 4219-4229, 1994.
60. Nathan, C., and Sanchez, E. Tumor necrosis factor and CD11/CD18 (β2) inlegrins act synergistically to lower cAMP in human neutrophils. J. Cell Biol., 111: 2171-2181, 1990.
61. Oh, E. S., Woods, A., and Couchman, J. R. Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J. Biol. Chem., 272: 8133-8136, 1997.
62. Lebakken, C. S., and Rapraeger, A. C. Syndecan-1 mediates cell spreading in transfected human lymphoblastoid (Raji) cells. J. Cell Biol., 132: 1209-1221, 1996.
63. Huang, M-M., Bolen, J. B., Barnwell, J. W., Shattil, S. J., and Brugge, J. S. Membrane glycoprotein IV (CD36) is physically associated with the Fyn, Lyn, and Yes proteintyrosine kinases in human platelets. Proc. Natl. Acad. Sci. USA, 88: 7844-7848, 1991.
64. Hsu, S. C., Volpert, O. V., Steck, P. A., Mikkelsen, T., Polverini, P. J., Rao, S., Chou, P., and Bouck, N. P. Inhibition of angiogenesis in human glioblastomas by chromosome 10 induction of thrombospondin-1. Cancer Res., 56: 5684-5691, 1996.
65. Tuszynski, G. P., Gasic, T. B., Rothman, V. L., Knudsen, K. A., and Gasic, G. J. Thrombospondin, a potemiator of tumor cell metastasis, Cancer Res., 47: 4130-4133, 1987.
66. Katagiri, Y., Hayashi, Y., Baba, I., Suzuki, H., Tanoue, K., and Yamazaki, H. Characterization of platelet aggregation induced by the human melanoma cell line HMV-I: roles of heparin, plasma adhesive proteins, and tumor cell membrane proteins. Cancer Res., 51: 1286-1293, 1991.