Biochemistry (Moscow)

, Volume 67, Issue 1, pp 47–55 | Cite as

The Blood Platelet as a Model for Regulating Blood Coagulation on Cell Surfaces and Its Consequences

  • F. A. Ofosu
Article

Abstract

Platelets actively participate in regulating thrombin production following physical or chemical injury to blood vessels. Injury to blood vessels initiates activation of the large numbers of platelets that appear in the subendothelium where they become exposed to tissue factor and to molecules adhesive for platelets and normally found in the extracellular matrix. The complex of plasma factor VIIa with extravascular tissue factor both initiates and localizes thrombin production on platelets and on extravascular cells. Thrombin production at these sites in turn enhances platelet activation and the subsequent hemostatic plug formation to minimize bleeding. Thrombin production and platelet activation also initiate the process of wound healing requiring thrombin-dependent cell activation and platelet-dependent formation of new blood vessels (angiogenesis). Activated platelets release from their storage granules several proteins and other factors that regulate local thrombin formation and the responses of blood vessel cells to injury to assure hemostasis and effective wound healing. Failure to localize and adequately regulate thrombin production and/or platelet activation can have pathological consequences, including the development and propagation of atherosclerosis and enhancement of tumor development. The primary basis for the pathological consequences of the failure to adequately regulate thrombin production is that the multi-functional thrombin activates several types of cells to initiate their mitogenesis. Mitogenesis precedes many of the undesirable consequences of poorly regulated thrombin production and platelet activation. In addition, activated platelets release a variety of products which influence the functions of several cell types to the extent that inadequate regulation of platelet activation (by excessive thrombin production) could contribute to the pathogenesis of acute and chronic arterial thrombosis and to tumor development. Activated platelets participate in tumor development by releasing several factors that positively (and negatively) regulate blood vessel formation.

platelets thrombin blood coagulation hemostasis arterial thrombosis angiogenesis 

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REFERENCES

  1. 1.
    Davie, E. W., Fujikawa, K., and Kisiel, W. (1991) Biochemistry, 30, 10363-10369.Google Scholar
  2. 2.
    Mann, K. G. (1999) Thromb. Haemost., 82, 165-174.Google Scholar
  3. 3.
    Wilcox, J. R., Smith, K. M., and Schwartz, S. M. (1989) Proc. Natl. Acad. Sci. USA, 86, 2839-2843.Google Scholar
  4. 4.
    Rapaport, S. I., and Rao, V. M. (1992) Atheroscler. Thromb., 12, 1111-1121.Google Scholar
  5. 5.
    Mann, K. G., Nesheim, M., Church, W., Haley, P., and Krishnaswamy, S. (1990) Blood, 76, 1-16.Google Scholar
  6. 6.
    Rawala-Sheikh, R., Ahmad, S. S., and Walsh, P. N. (1990) Biochemistry, 29, 2606-2611.Google Scholar
  7. 7.
    Kane, W. H., Lindout, M. J., Jackson, C. M., and Majerns, P. W. (1980) J. Biol. Chem., 255, 1170-1174.Google Scholar
  8. 8.
    Tracy, P. B., Eide, L. L., and Mann, K. G. (1985) J. Biol. Chem., 260, 2119-2124.Google Scholar
  9. 9.
    Brinkman, H.-J. M., Mertens, K., Holthuis, J., Zwart-Huinik, L. A., Grijin, K., and van Mourik, J. A. (1994) Br. J. Haematol., 87, 332-342.Google Scholar
  10. 10.
    Fingerle, J., Johnson, R., Clowes, A. W., Majesky, M. W., and Reidy, M. A. (1989) Proc. Natl. Acad. Sci. USA, 86, 8412-8416.Google Scholar
  11. 11.
    Kalafatis, M., Egan, J. O., van' t Veer, C., Cawthern, K. M., and Mann, K. G. (1997) Crit. Rev. Eukaryot. Gene Expr., 7, 241-280.Google Scholar
  12. 12.
    Davey, M. G., and Luscher, E. F. (1967) Nature, 216, 857-858.Google Scholar
  13. 13.
    Shuman, M. A., and Levine, S. P. (1978) J. Clin. Invest., 61, 1102-1106.Google Scholar
  14. 14.
    Ofosu, F. A., Sie, P., Modi, J., Fernandez, F., Buchanan, M. R., and Blajchman, M. A. (1987) Biochem. J., 243, 579-588.Google Scholar
  15. 15.
    Yang, X., Blajchman, M. A., Cravens, S., Smith, L. M., Anvari, N., and Ofosu, F. A. (1990) Biochem. J., 272, 399-406.Google Scholar
  16. 16.
    Strukova, S. M. (2001) Biochemistry (Moscow), 66, 8-18.Google Scholar
  17. 17.
    Morris, R., Winjard, P., Blake, D., and Morris, C. (1994) Ann. Rheum. Dis., 53, 72-79.Google Scholar
  18. 18.
    Browder, T., Folkman, J., and Pirie-Shepherd, S. (2000) J. Biol. Chem., 275, 1521-1524.Google Scholar
  19. 19.
    Ross, R. (1993) Nature (London), 362, 801-809.Google Scholar
  20. 20.
    Marcus, A. J. (1994) Sem. Hematol., 31, 267-269.Google Scholar
  21. 21.
    Altieri, D. C. (1995) J. Leukoc. Biol., 58, 120-127.Google Scholar
  22. 22.
    Tordai, A. J. W., Fenton II, J. W., Anderson, T., and Gelfand, E. W. (1993) J. Immunol., 150, 4876-4886.Google Scholar
  23. 23.
    Molloy, C. J., Pawlowski, J. E., Taylor, D. S., Turner, C. E., Weber, H., Peluso, M., and Seiler, S. M. (1996) J. Clin. Invest., 97, 1173-1183.Google Scholar
  24. 24.
    Grandaliano, G., Valente, A. J., and Abbound, H. E. (1994) J. Exp. Med., 179, 1773-1741.Google Scholar
  25. 25.
    Sower, L. E., Froelich, C. J., Carney, D. H., Fenton II, J. W., and Kimpel, G. R. (1995) J. Immunol., 155, 895-901.Google Scholar
  26. 26.
    Henrikson, K. P., Salazar, S. L., Fenton II, J. W., and Pentecost, B. T. (1999) Br. J. Cancer, 79, 401-406.Google Scholar
  27. 27.
    Grand, R., Turnell, A., and Graham, P. (1996) Biochem. J., 313, 353-358.Google Scholar
  28. 28.
    Glusa, E., Paintz, M., and Bretschneider, E. (1996) Semin. Thromb. Hemost., 22, 261-266.Google Scholar
  29. 29.
    Carney, D. H., Redin, W., and McCroskey, L. (1992) Semin. Thromb. Hemost., 18, 91-103.Google Scholar
  30. 30.
    Crino, G. C., Cicala, M., Bucci, L., Sorrentino, J. M., Maraganore, J. M., and Stone, S. R. (1996) J. Exp. Med., 183, 821-827.Google Scholar
  31. 31.
    Bouchard, B. A., Shatos, M. A., and Tracy, P. B. (1997) Arterioscler. Thromb. Vasc. Biol., 17, 1-9.Google Scholar
  32. 32.
    Plescia, J., and Altieri, D. C. (1996) Biochem. J., 319, 873-879.Google Scholar
  33. 33.
    Sorensen, B. B., Freskgard, P. O., Nielsen, L. S., Rao, L. V. M., Ezban, M., and Petersen, L. C. (1999) J. Biol. Chem., 274, 21349-21354.Google Scholar
  34. 34.
    Ruf, W., and Mueller, B. (1999) Thromb. Haemost., 82, 183-192.Google Scholar
  35. 35.
    Cirino, G., Cicala, C., Bucci, M., Sorrentino, L., Ambrosin, G., DeDominicis, G., and Altieri, D. C. (1997) J. Clin. Invest., 79, 2446-2451.Google Scholar
  36. 36.
    Gasic, G. P., Arenas, C. P., Gasic, T. B., and Gasic, G. J. (1992) Proc. Natl. Acad. Sci. USA, 89, 2317-2320.Google Scholar
  37. 37.
    Nicholson, A. C., Nachman, R. L., Altieri, D. C., Summers, B. D., Ruf, W., Edgington, T. S., and Hajjar, D. P. (1996) J. Biol. Chem., 271, 28407-28413.Google Scholar
  38. 38.
    Berndt, M. C., Gregory, C., Dowden, G., and Castaldi, P. A. (1986) Ann. N. Y. Acad. Sci., 485, 374-386.Google Scholar
  39. 49.
    Fuster, V., Steele, P. M., and Cheseboro, J. H. (1985) J. Am. Coll. Cardiol., 5, 175B-184B.Google Scholar
  40. 40.
    Harrison, E., and Cramer, E. M. (1993) Blood Rev., 7, 52-62.Google Scholar
  41. 41.
    Monkovic, D. D., and Tracy, P. B. (1990) J. Biol. Chem., 265, 17132-17140.Google Scholar
  42. 42.
    Alberin, L., Safa, O., Clementson, K. J., Esmon, C. T., and Dale, G. L. (1999) Blood, 38, 4268-4374.Google Scholar
  43. 43.
    Fukami, M. H., Holmsen, H., Kowalsky, M. A., and Niewaroski, S. (2001) in Hemostasis and Thrombosis: Basic Principles and Practice (Colman, R. W., et al., eds.) Lippincott Williams and Wilkens, Philadelphia, USA, pp. 561-573.Google Scholar
  44. 44.
    Ahmad, S. S., and Walsh, P. N. (1994) Trends Cardiovasc. Med., 4, 271-278.Google Scholar
  45. 45.
    Scandura, J. M., and Walsh, P. N. (1996) Biochemistry, 35, 8903-8913.Google Scholar
  46. 46.
    Badellino, K. O., and Walsh, P. N. (2000) Biochemistry, 39, 4769-4777.Google Scholar
  47. 47.
    Bar-Shavit, R., Benezra, M., Eldor, A., Hy-Am, E., Fenton II, J. W., Wilner, G. D., and Vlodavsky, I. (1990) Cell Regul., I, 453-463.Google Scholar
  48. 48.
    Hattori, R., Hamilton, K. K., Fugate, R. D., McEver, R. P., and Sims, P. J. (1989) J. Biol. Chem., 264, 7768-7771.Google Scholar
  49. 59.
    Ofosu, F. A. (1996) in Recent Advances in Blood Coagulation (Poller, L., and Ludlam, C. A., eds.) Churchill Livingstone, Edinburgh, pp. 33-48.Google Scholar
  50. 50.
    Taubman, M. B., Fallon, J., Schecter, A., Giesen, P., Mendlowitz, M., Fyte, B., Marmur, J., and Nemerson, Y. (1997) Thromb. Haemost., 78, 200-204.Google Scholar
  51. 51.
    Osterud, B. (1997) Thromb. Haemost., 78, 755-758.Google Scholar
  52. 52.
    Libby, P., Egan, D., and Skarlatos, S. (1998) Circulation, 96, 4095-4103.Google Scholar
  53. 53.
    Kurantsin-Mills, J., Ofosu, F. A., Safa, T. K., Siegel, R. S., and Lessin, L. S. (1992) Br. J. Haematol., 81, 539-544.Google Scholar
  54. 54.
    Kurantsin-Mills, J., Ibe, B. O., Natta, C. L., Raj, J. U., Siegel, R. S., and Lessin, L. S. (1994) Br. J. Haematol., 87, 580-585.Google Scholar
  55. 55.
    Ibe, B. O., Kurantsin-Mills, J., Raj, J. U., and Lessin, L. A. (1995) Eur. J. Clin. Invest., 24, 57-64.Google Scholar
  56. 56.
    Ibe, B. O., Kurantsin-Mills, J., and Raj, J. U. (1997) Am. J. Physiol., 272, L597-602.Google Scholar
  57. 57.
    Key, N. S., Slungaard, A., Dandelet, L., Nelson, S. C., Moertel, C., Styles, L. A., Kuypers, F. A., and Bach, R. R. (1998) Blood, 98, 4216-4263.Google Scholar
  58. 58.
    Banner, D., D'Arcey, A., Chene, C., Winkler, F., Guha, A., Koningsberg, W., Nemerson, Y., and Kirchhofer, D. (1996) Nature, 380, 41-46.Google Scholar
  59. 59.
    Prydz, H., Camerer, E., Rottingen, J. A., Wisler, M. T., and Gjernes, E. (1999) Thromb. Haemost., 82, 165-174.Google Scholar
  60. 60.
    Clemetson, K. J. (1999) Curr. Biol., 9, R110-R112.Google Scholar
  61. 62.
    Ip, J. H., Fuster, V., Israel, D., Badimon, L., Badimon, J., and Cheseboro, J. H. (1991) J. Am. Coll. Cardiol., 17, 77B-88B.Google Scholar
  62. 62.
    Koedam, J. A., Haner, R. J., Beeser-Visser, N. H., Bouma, B. N., and Sizma, J. J. (1990) Eur. J. Biochem., 189, 229-234.Google Scholar
  63. 63.
    Novotny, W. F. (1994) Sem. Thromb. Hemost., 20, 101-108.Google Scholar
  64. 64.
    Broze, G. J., Girard, T. J., and Novotny, W. F. (1990) Biochemistry, 29, 7539-7546.Google Scholar
  65. 65.
    Huang, Z. F., Wun, T. C., and Broze, G. J. (1993) J. Biol. Chem., 268, 26950-26955.Google Scholar
  66. 66.
    Lindhout, T., Franssen, J., and Willems, G. (1995) Thromb. Haemost., 74, 910-915.Google Scholar
  67. 67.
    Jesty, J., Wun, T. C., and Lorenz, A. (1994) Biochemistry, 33, 12686-12694.Google Scholar
  68. 68.
    Gouin-Thibault, I., Dewar, L., Craven, S., Kulczycky, M., Wun, T.-Z., and Ofosu, F. A. (1996) Br. J. Haematol., 95, 738-746.Google Scholar
  69. 69.
    Sandset, P. M., Abilgaard, U., and Larsen, M. L. (1988) Thromb. Res., 50, 803-813.Google Scholar
  70. 70.
    Novotny, W. F., Brown, S. G., Miletich, J. P., Rader, D. J., and Broze, G. J., Jr. (1991) Blood, 78, 387-393.Google Scholar
  71. 71.
    Lupu, C., Lupu, F., Dennehy, U., Kakkar, V. V., and Scully, M. F. (1995) Arteriorscler. Thromb. Vasc. Biol., 15, 2055-2062.Google Scholar
  72. 72.
    McGee, M. P., and Chou, T. (2001) J. Biol. Chem., 276, 7827-7835.Google Scholar
  73. 73.
    Rogers, G. M., and Shuman, M. A. (1983) Proc. Natl. Acad. Sci. USA, 82, 2523-2527.Google Scholar
  74. 74.
    Stern, D. M., Nawroth, P. P., Kisiel, W., Handley, D., Drillings, M., and Bartos, J. (1984) J. Clin. Invest., 74, 1910-1921.Google Scholar
  75. 75.
    McGee, M. P., and Rothberger, H. (1986) J. Exp. Med., 164, 1902-1914.Google Scholar
  76. 76.
    Sugo, T., Nakamikawa, C., Tanabe, S., and Matsuda, M. (1995) J. Biochem., 117, 244-250.Google Scholar
  77. 77.
    Ofosu, F. A., Dewar, L., Craven, S., and Xianjun, Y. (1999) Thromb. Haemost. (Suppl.), August, 713.Google Scholar
  78. 78.
    Broze, G. J. (1997) in Recent Advances in Blood Coagulation (Poller, L., and Ludlam, C. A., eds.) Vol. 7, Churchill Livingstone, Edinburgh, pp. 1-17.Google Scholar
  79. 79.
    Galiani, D., and Broze, G. J. (1991) Science, 253, 909-912.Google Scholar
  80. 80.
    Scandura, J. M., and Walsh, P. M. (1996) Biochemistry, 35, 8903-8913.Google Scholar
  81. 81.
    Walsh, P. N. (1999) Thromb. Haemost., 82, 234-242.Google Scholar
  82. 82.
    Gronke, R. S., Knauer, D. J., Veeraraghavan, S., and Baker, J. B. (1989) Blood, 73, 472-478.Google Scholar
  83. 83.
    Knauer, D. J., Majumdar, D., Fong, P. C., and Knauer, M. F. (2000) J. Biol. Chem., 275, 37340-37346.Google Scholar
  84. 84.
    Cunningham, D. D., and Donovan, F. M. (1997) Adv. Exp. Med. Biol., 425, 67-75.Google Scholar
  85. 85.
    Zoller, B., and Dahlback, B. (1997) in Recent Advances in Blood Coagulation (Poller, L., and Ludlam, C. L., eds.) Vol. 7, Churchill Livingston, Edinburgh, pp. 49-67.Google Scholar
  86. 86.
    Camire, K. M., Kalafatis, M., Simioni, P., Girolami, A., and Tracy, P. B. (1998) Blood, 91, 2818-2829.Google Scholar
  87. 87.
    Briede, J. J., Tans, G., Willems, G. M., Hemker, H. C., and Lindhout, T. (1002) J. Biol. Chem., 276, 7164-7168.Google Scholar
  88. 88.
    George, J. N. (2000) Lancet, 355, 1531-1539.Google Scholar
  89. 89.
    Levy-Toledano, S. (1999) Haemostasis, 29, 4-15.Google Scholar
  90. 90.
    Ross, R. (1999) New Engl. J. Med., 340, 115-126.Google Scholar
  91. 91.
    Kawai, Y., and Montegomery, R. R. (1987) Ann. N. Y. Acad. Sci., 509, 60-70.Google Scholar
  92. 92.
    Sixma, J. J., Nievelstein, P. F. E. M., Zwaginga, J. J., and Groot, P. G. (1987) Ann. N. Y. Acad. Sci., 516, 39-54.Google Scholar
  93. 93.
    Kawai, Y., Handa, M., Nagai, H., Kamata, T., Anbo, H., Kawano, K., Araki, Y., Yamamoto, M., Ikeda, Y., and Watanabe, K. (1989) Acta Haematol. Jap., 52, 1312-1321.Google Scholar
  94. 94.
    Vu, T. K. H., Hung, D. T., Wheaton, V. I., and Couglin, S. R. (1991) Cell, 64, 1057-1068.Google Scholar
  95. 95.
    Couglin, S. R., Vu, T. K. H., Hung, D. T., and Wheaton, V. I. (1991) J. Clin. Invest., 89, 351-355.Google Scholar
  96. 96.
    Brass, L. F., Vassallo, R. R., Jr., Belemonte, E., Ahuja, M., Cichowski, K., and Hoxie, J. A. (1992) J. Biol. Chem., 267, 13795-13798.Google Scholar
  97. 97.
    Liu, L., Freedman, J., Hornstein, A., Fenton II, J. W., Song, Y., and Ofosu, F. A. (1997) J. Biol. Chem., 272, 1997-2004.Google Scholar
  98. 98.
    Leung, L., and Nachman, R. (1986) Annu. Rev. Med., 37, 179-186.Google Scholar
  99. 99.
    Hawiger, J., Brass, L. F., and Salzman, E. W. (1994) in Hemostasis and Thrombosis: Basic Principles and Clinical Practice (Colman, R. W., Hirsh, J., Marder, V. J., and Salzman, E. W., eds.) 3rd ed., JB Lippincott Company, Philadelphia.Google Scholar
  100. 100.
    Brass, L. F., Manning, D. R., Cichowski, K., and Abrams, C. S. (1997) Thromb. Haemost., 78, 581-589.Google Scholar
  101. 101.
    Shattil, S. J. (1997) Thromb. Haemost., 78, 318-325.Google Scholar
  102. 102.
    Martinson, E. A., Scheibe, S., Marx-Grunitz, A., and Presek, P. (1998) Thromb. Haemost., 80, 976-981.Google Scholar
  103. 103.
    Musial, J., Undas, A., Undas, R., Brozek, J., and Szczeklik, A. (2001) Thromb. Haemost., 85, 221-225.Google Scholar
  104. 104.
    Ross, R., Bowen-Pope, D. F., and Raines, E. W. (1985) Ann. N. Y. Acad. Sci., 454, 254-260.Google Scholar
  105. 105.
    Rosenberg, R. D., Reilly, C., and Fritze, L. (1985) Ann. N. Y. Acad. Sci., 454, 270-278.Google Scholar
  106. 106.
    Hirsh, J., Dalen, J. E., Fuster, V., Patrano, C., and Roth, G. (1995) Chest, 108, 7S-257S.Google Scholar
  107. 107.
    Hirsh, J. (1987) New Engl. J. Med., 316, 1543-1544.Google Scholar
  108. 108.
    Schini-Kerth, V. B., Bassus, S., Fisslthaler, B., Kirchmaier, C. M., and Busse, R. (1997) Circulation, 96, 3888-3896.Google Scholar
  109. 109.
    Fingetle, J., Johnson, R., Clowes, A. W., Majesky, M. W., and Reidy, M. A. (1999) Proc. Natl. Acad. Sci. USA, 86, 8412-8416.Google Scholar
  110. 110.
    Sumiyoshi, A., Asada, Y., Maratsuka, K., Hayashi, T., Kisanuki, A., Tsuneyoshi, A., and Sato, Y. (1995) Ann. N. Y. Acad. Sci., 748, 74-84.Google Scholar
  111. 111.
    Grotendorst, G. R., Chang, T., Seppae, H. E. J., Kleinman, H. K., and Martin, G. R. (1982) J. Cell. Physiol., 113, 261-266.Google Scholar
  112. 112.
    Williams, L. T., Antoniades, H. N., and Goetzl, E. J. (1983) J. Clin. Invest., 72, 1759-1763.Google Scholar
  113. 113.
    Dore, M. (1998) Am. Heart J., 135, 5146-5151.Google Scholar
  114. 114.
    Buttrum, S. M., Hatton, R., and Nash, G. B. (1993) Blood, 82, 1165-1174.Google Scholar
  115. 115.
    Hamburger, S. A., and McEver, R. P. (1990) Blood, 76, 550-554.Google Scholar
  116. 116.
    Larson, E., Cell, A., Gilbert, G. E., Furie, B. C., Erban, J. K., Bonfati, R., Wagner, D. D., and Furie, B. (1989) Cell, 59, 305-312.Google Scholar
  117. 117.
    Siverstein, R. I., Asch, A. S., and Nachman, R. L. (1989) J. Clin. Invest., 84, 546-561.Google Scholar
  118. 118.
    Silverstein, R. I., and Nachman, R. L. (1987) J. Clin. Invest., 79, 867-875.Google Scholar
  119. 119.
    Lahar, J., Schwartz, M. A., and Hynes, R. O. (1982) Cell, 31, 253-262.Google Scholar
  120. 120.
    Aiken, M. L., Ginsburg, M. A., and Plow, E. F. (1986) J. Clin. Invest., 78, 1713-1716.Google Scholar
  121. 121.
    Parker, C. J., Stone, O. L., White, V. F., and Bershaw, N. J. (1986) Br. J. Haematol., 71, 245-252.Google Scholar
  122. 122.
    Hope, W., Martin, T. J., Chesterman, C. N., and Morgan, F. J. (1979) Nature, 282, 210-212.Google Scholar
  123. 123.
    Senior, R. M., Griffin, G. L., Haung, J. S., Walz, D. A., and Deuel, T. F. (1983) J. Cell Biol., 96, 382-385.Google Scholar
  124. 124.
    Ross, R., and Vogel, A. (1978) Cell, 14, 203-210.Google Scholar
  125. 125.
    Ben-Ezra, J., Sheibani, K., Hwabg, D. L., and Lev-Ran, A. (1990) Am. J. Pathol., 137, 755-759.Google Scholar
  126. 126.
    Hwang, D. L., Lev-Ran, A., Yen, C. F., and Sniecinski, I. (1992) Regul. Pept., 37, 95-100.Google Scholar
  127. 127.
    Nakamura, T., Teremato, H., and Ichihara, A. (1986) Proc. Natl. Acad. Sci. USA, 83, 6489-6493.Google Scholar
  128. 128.
    Bar, R. S., Boes, M., Booth, B. A., Dake, B. L., Henley, S., and Hart, M. N. (1989) Endocrinology, 124, 1841-1848.Google Scholar
  129. 129.
    Wartiovaara, U., Salven, P., Mikkola, H., Lassila, R., Kaukonen, J., Joukov, V., Orpana, A., Ristimaki, A., Heikinheimo, M., Joensuu, H., Aitalo, K., and Palotie, A. (1998) Thromb. Haemost., 80, 171-175.Google Scholar
  130. 130.
    Karey, K. P., and Sirbasku, D. A. (1989) Blood, 74, 1093-1100.Google Scholar
  131. 131.
    Mohle, R., Green, D., Moore, M. A. S., Nachman, R. L., and Rafii, S. (1997) Proc. Natl. Acad. Sci. USA, 94, 663-669.Google Scholar
  132. 132.
    Rosen, E. M., Lamuzus, K., Laterra, J., Polverini, P. J., Rubin, J. S., and Goldberg, I. D. (1997) in Plasminogen-Related Growth Factors (Gheradi, E., ed.) John Wiley and Sons, Chichester, UK, pp. 215-226.Google Scholar
  133. 133.
    Taylor, S., and Folkman, J. (1982) Nature, 257, 307-312.Google Scholar
  134. 134.
    Maione, T. E., Gray, G. S., Petro, J., Hunt, A. J., Donner, A. L., Bauer, S. I., Carson, H., and Sharpe, R. J. (1990) Science, 247, 77-79.Google Scholar
  135. 135.
    Maione, T. E., Gray, G. S., Hunt, A. J., and Sharpe, R. J. (1991) Cancer Res., 51, 2077-2083.Google Scholar
  136. 136.
    Good, D. J., Polverini, P. J., Rastinejad, F., Bean, M. M. L., Lemona, R. S., Frazier, W. A., and Boyck, N. P. (1990) Proc. Natl. Acad. Sci. USA, 87, 6624-6628.Google Scholar
  137. 137.
    Roberts, A. B., and Sporn, M. B. (1989) Annu. Rev. Resp. Dis., 140, 1126-1128.Google Scholar

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© MAIK “Nauka/Interperiodica” 2002

Authors and Affiliations

  • F. A. Ofosu
    • 1
  1. 1.Department of Pathology and Molecular MedicineMcMaster UniversityHamiltonCanada

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