Radiobiology of Blood Vessels

Part of the Prostaglandins, Leukotrienes, and Cancer book series (PLAC, volume 5)


Why should the cancer specialist be interested in the radiobiology of blood vessels? This chapter will attempt to answer this question, review the current state of knowledge of vascular radiation biology and suggest directions for future investigations. Radiation effects on normal tissues are divided into two categories based on time of appearance. Acute effects occur during a course of fractionated radiation therapy or shortly thereafter. Late effects occur more than two months after completion of radiation and may appear many years later. Acute radiation damage to normal tissues can be understood in terms of cell proliferation kinetics (1). It results from an imbalance between cell killing and tissue regeneration. The latter may occur by recruitment of quiescent “stem” cells into the cell cycle; shortening of the cycle time of proliferating cells; or repopulation of the tissue with cells from outside of the irradiated field. The timing and severity of the acute effects depend upon : (1) transit time for maturing cells within the tissue compartment; (2) dose fraction size; and (3) protraction (the total time in which the radiation is delivered).


Radiat Oncol Biol Phys Radiation Injury Aortic Smooth Muscle Cell Endothelial Cell Culture Sublethal Damage 
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  1. 1.
    Bloomer WD, Hellman S. Medical Intelligence. Current Concepts. Normal tissue responses to radiation therapy. N Engl J Med 293:80–83, 1975.PubMedCrossRefGoogle Scholar
  2. 2.
    Fletcher GH. “Textbook of Radiotherapy”, 3rd Edition (Lea and Febiger, Philadelphia), 1980, pp 181–184.Google Scholar
  3. 3.
    Withers HR, Peters LJ, Kogelnik HD. The pathobiology of late effects of irradiation. In: Radiation Biology in Cancer Research, (RE Meyn, HR Withers, eds, Raven Press, New York), 1980, pp 439–448.Google Scholar
  4. 4.
    Withers HR, Mason KA, Thames HD. Late radiation response of kidney assayed by tubule-cell survival. Brit J Radiol 59:587–595, 1986.PubMedCrossRefGoogle Scholar
  5. 5.
    Michalowski A. The pathogenesis of late side-effects of radiotherapy. Clin Radiol 37:203–207, 1986.PubMedCrossRefGoogle Scholar
  6. 6.
    Van der Kogel AJ. Mechanisms of late radiation injury in the spinal cord. In: Radiation Biology in Cancer Research, (RE Meyn, HR Withers, eds, Raven Press, New York), 1980, pp 461–470.Google Scholar
  7. 7.
    Fowler JF. Dose response curves for organ function or cell survival. Radiol 56:497–500, 1983.Google Scholar
  8. 8.
    Wheldon TE, Michalowski AS, Kirk J. The effect of irradiation on function in self-renewing normal tissues with differing proliferative organization. Brit J Radiol 55:759–766, 1982.PubMedCrossRefGoogle Scholar
  9. 9.
    Hopewell JW. The importance of vascular damage in the development of late radiation effects in normal tissues. In: “Radiation Biology in Cancer Research,” (RE Meyn, HR Withers, eds, Raven Press, New York), 1980, pp 449–459.Google Scholar
  10. 10.
    Casarett GW. “Radiation Histopathology,” Volume I, CRC (CRC Press, Florida, Boca Raton), 1980, pp 39–50.Google Scholar
  11. 11.
    Sams A. Histological changes in the larger blood vessels of the hind limb of the mouse after X-irradiation. Int J Radiat Biol 9:165–74, 1964.CrossRefGoogle Scholar
  12. 12.
    Solesvik OV, Rofstad EK, Brustad T. Vascular changes in a human malignant melanoma xenograft following single-dose irradiation. Radiat Res 98:115–128, 1984.PubMedCrossRefGoogle Scholar
  13. 13.
    Denekamp J. Vascular endothelium as the vulnerable element in tumors. Acta Radiol (Oncol) 23:217–225, 1984.CrossRefGoogle Scholar
  14. 14.
    Peters LJ, Mason KA, Withers HR. Effect of lung irradiation on metastases: radiobiological studies and clinical correlations, In: Radiation Biology in Cancer Research (RE Meyn, MR Withers, eds, Raven Press, New York), 1980, pp 461–470.Google Scholar
  15. 15.
    Heisel MA, Laug WE, Stowe SM, Jones PA. Effects of X-irradiation on artificial blood vessel wall degradation by invasive tumor cells. Cancer Res 44:2441–2445, 1984.PubMedGoogle Scholar
  16. 16.
    Heisel MA, Laug WE, Jones PA. Inhibition by bovine endothelial cells of degradation by HT 1080 fibrosarcoma, cells of extracellular matrix proteins. J Natl Cancer Inst 71:1183–1187, 1983.PubMedGoogle Scholar
  17. 17.
    Law MP. Radiation-induced vascular injury and its relation to late effects in normal tisues. Adv Radiat Biol 9:37–73, 1981.Google Scholar
  18. 18.
    Eassa EH, Casarett GW. Effect of epsilon-amino-n-caproic acid on radiation-induced increase in capillary permeability. Radiology 106:679–688, 1973.PubMedGoogle Scholar
  19. 19.
    Hahn GL, Menconi MJ, Polger P. The effect of gamma radiation on prostacyclin production in cultured pulmonary artery endothelium, In: Prostaglandins and Cancer (TJ Powles, RS Bockman, KV Honn, P Ramwell, eds, Alan R Liss, New York), pp 381–384, 1981.Google Scholar
  20. 20.
    Wharton JT, Delclos L, Gallager S, Smith JP. Radiation hepatitis induced by abdominal irradiation with the cobalt 60 moving strip technique. Am J Roentgenol 117:73–80, 1973.Google Scholar
  21. 21.
    Ingold JA, Reed GB, Kaplan HS, Bagshaw MA. Radiation hepatitis. Am J Roentgenol 93:200–208, 1965.Google Scholar
  22. 22.
    Hebard DW, Jackson KL, Christensen GM. Radiat Res 81:441–454, 1980. The chronological development of late radiation injury in the liver of the rat.PubMedCrossRefGoogle Scholar
  23. 23.
    Hopewell JW, Wright EA. The nature of latent cerebral irradiation damage and its modification by hypertension. Brit J Radiol 43:161–167, 1970.PubMedCrossRefGoogle Scholar
  24. 24.
    Ackerman LV. The pathology of radiation effect of normal and neoplastic tissue. Am J Roentgenol Radium Ther Nucl Med 114:447–459, 1972.PubMedGoogle Scholar
  25. 25.
    Rubin P, Keys H, Paulter C. Changing concepts in the tolerance of radioresistant and radiosensitive normal tissues and organs; In: Biological Bases and Clinical Implications of Tumor Radioresistant (GH Fletcher et al eds, Mason, New York), 1980, pp 175–195.Google Scholar
  26. 26.
    Moss WT, Brand WN, Battifora H. The heart and blood vessels, In: “Radiation Oncology, Rationale, Technique, Results” (CV Mosby Co, St. Louis), 1973, pp 248–256.Google Scholar
  27. 27.
    Asscher AW, Wilson C, Anson SG. Sensitization of blood vessels to hypertensive damage by X-irradiation. Lancet 1:580–583, 1961.PubMedCrossRefGoogle Scholar
  28. 28.
    El-Naggar AM, El-Baz LM, Carsten AL, Chanana AD, Cronkite EP. Radiation-induced damage to blood vessels: a study of dose-effect relationship with time after X-irradiation. Int J Radiat Biol 34:359–366, 1978.CrossRefGoogle Scholar
  29. 29.
    Lindsay S, Entenman C, Ellis EE, Geraci CL. Aortic arteriosclerosis in the dog after localized aortic irradiation with electrons. Circ Res 10:61–67, 1962.PubMedGoogle Scholar
  30. 30.
    Lindsay S, Kohn HI, Dakin RL, Jew J. Aortic arteriosclerosis in the dog after localized aortic x-irradiation. Circ Res 10:51–60, 1962.PubMedGoogle Scholar
  31. 31.
    Silverberg GD, Britt RH, Goffinet DR. Radiation-induced carotid artery disease. Cancer 41:130–137, 1978.PubMedCrossRefGoogle Scholar
  32. 32.
    McReynolds RA, Gold GL, Roberts WC. Coronary heart disease after mediastinal irradiation for Hodgkin’s disease. Am J Med 60:39–45, 1976.PubMedCrossRefGoogle Scholar
  33. 33.
    Dollinger MR, Lavine DM, Foye LV. Myocardial infarction due to post-irradiation fibrosis of the coronary arteries. JAMA 195:316–319, 1966.PubMedCrossRefGoogle Scholar
  34. 34.
    Cohn KE, Stewart JR, Fajardo LF. Hancock EW. Heart disease following radiation. Medicine 46:281–298, 1967.PubMedCrossRefGoogle Scholar
  35. 35.
    Amromin GD, Gildenhorn HL, Solomon RD, Nadkarni BB, Jacobs ML. The synergism of x-irradiation and cholesterol-fat feeding on the development of coronary artery lesions. J Atheroscler Res 4:325–334, 1964.PubMedCrossRefGoogle Scholar
  36. 36.
    Artom C, Lofland HB, Clarkson TB. Ionizing radiation, atherosclerosis, and lipid metabolism in pigeons. Radiat Res 26:165–177, 1965.PubMedCrossRefGoogle Scholar
  37. 37.
    Fajardo LF and Lee A. Rupture of major vessels after radiation. Cancer 36:904–913, 1975.PubMedCrossRefGoogle Scholar
  38. 38.
    Colquhoun J. Hypoplasia of the abdominal aorta following therapeutic irradiation in infancy. Radiology 86:454–456, 1966.PubMedGoogle Scholar
  39. 39.
    Fonkalsrud EW, Sanchez M, Zerubavel R, Mahoney A. Serial changes in arterial structure following radiation therapy. Surg Gynecol Obstet 145:395–400, 1977.PubMedGoogle Scholar
  40. 40.
    Ross R. The pathogenesis of atherosclerosis. N Engl J Med 314:488–500, 1986.PubMedCrossRefGoogle Scholar
  41. 41.
    Goldberg ID, Botnick LE, Stemerman MB, Hannon EC. In vivo aortic smooth muscle cell kinetics: response to irradiation in the rat. Cell Tissue Kin 15:675, 1982.Google Scholar
  42. 42.
    Goldberg ID, Stemerman MB, Schnipper LE, Ransil BJ, Crooks GW, Fuhro RL. Vascular smooth muscle cell kinetics: a new assay for studying patterns of cellular proliferation in vivo. Science 205:920–922, 1979.PubMedCrossRefGoogle Scholar
  43. 43.
    Rosen EM, Goldberg ID, Myrick KV and Levenson SE. Radiation survival properties of cultured vascular smooth muscle cells. Radiat Res 100:182–191, 1984.PubMedCrossRefGoogle Scholar
  44. 44.
    Rosen EM, Goldberg ID, Myrick KV, Levenson SE. Radiation survival of vascular smooth muscle cells as a function of age. Int J Radiat Biol 48:71–79, 1985.CrossRefGoogle Scholar
  45. 45.
    Rosen EM, Goldberg ID, Myrick KV, Halpin PA, Levenson SE. Survival and repair of potentially lethal radiation damage in confluent vascular smooth muscle cell cultures. Radiother Oncol 5:159–163, 1986.PubMedCrossRefGoogle Scholar
  46. 46.
    Martin DF, Fischer JJ. Radiation sensitivity of cultured rabbit aortic endothelial cells. Int J Radiat Oncol Biol Phys 10:1903–1906, 1984.PubMedCrossRefGoogle Scholar
  47. 47.
    Kwock L, Chaney EL, Guilford WB, Clark RL, Zaramba J. Effect of ionizing radiation on the pulmonary vasculature and isolated pulmonary artery endothelium. Int J Radiat Oncol Biol Phys 9 (suppl 1):166–167, 1983 (Abstr).Google Scholar
  48. 48.
    Nias AHW. The clinical significance of cell survival curves, In: “The Biological and Clinical Basis of Radiosensitivity” (M Friedman, ed, Charles C. Thomas, Springfield, IL), pp 156–169, 1974.Google Scholar
  49. 49.
    Kwock L, Doublas WH, Lin PS, Baur WE, Fanburg BL. Endothelial cell damage after gamma-irradiation in vitro: Impaired uptake of alpha-aminoisobutyric acid. Am Rev Respir Dis 125:95–99, 1982.PubMedGoogle Scholar
  50. 50.
    Rhee JG, Lee I, Song CW. The clonogenic response of bovine aortic endothelial cells in culture to radiation. Radiat Res 106:182–189, 1986.PubMedCrossRefGoogle Scholar
  51. 51.
    Little JB. Repair of sublethal and potentially lethal radiation damage in plateau phase cultures of human cells. Nature 224:804–806, 1969.PubMedCrossRefGoogle Scholar
  52. 52.
    DeGowin RL, Lewis LJ, Mason RE, Borke MK, Hoak JC. Radiation-induced inhibition of human endothelial cells replicating in culture. Radiat Res 68:244–250, 1976.PubMedCrossRefGoogle Scholar
  53. 53.
    Griem ML, Fischer-Dzoga K, Dimitrievich GS. Radiosensitivity of vascular tissue. II. Differential radiosensitivity of endothelial and smooth muscle cells. Int. J Radiat Oncol Biol Phys 9 (Suppl 1):167, 1983 (abstr).Google Scholar
  54. 54.
    Withers HR. The dose-survival relationship for irradiation of epithelial cells of mouse skin. Br J Radiol 40:187–194, 1967.PubMedCrossRefGoogle Scholar
  55. 55.
    Withers HR, Elkind M. Microcolony survival assay for cells of mouse intestinal mucosa exposed to radiation. Int J Radiat Biol 17:261–267, 1970.CrossRefGoogle Scholar
  56. 56.
    Thompson LH, Suit HD. Proliferation kinetics of x-irradiated mouse L cells studied with time lapse photography-II. Int J Radiat Biol 15:347–362, 1969.CrossRefGoogle Scholar
  57. 57.
    Johnson LK, Longenecker JP, Fajardo LF. Differential radiation response of cultured endothelial cells and smooth myocytes. Anal Quant Cytol 4:188–198, 1982.PubMedGoogle Scholar
  58. 58.
    DeGowin RL, Lewis LJ, Hoak JC, Mueller AL, Gibson DP. Radiosensitivity of human endothelial cells in culture. J Lab Clin Med 84:42–48, 1974.Google Scholar
  59. 59.
    Rubin DB, Drab EA, Ward WF, Bauer KD. Cell cycle changes and cytotoxicity and irradiated cultures of bovine aortic endothelial cells. Radiat Res 108:206–214, 1986.PubMedCrossRefGoogle Scholar
  60. 60.
    Fischer JJ. Proliferation of rat aortic endothelial cells following x-irradiation. Radiat Res 92:405–410, 1982.PubMedCrossRefGoogle Scholar
  61. 61.
    Schwartz SM. Dynamic maintenance of the endothelium, In: “The Endothelial Cell - A Pluripotent Control Cell of the Vessel Wall,” (DGS Thilo-Korner, RI Freshney, eds, S Karger, Basel), 1983, pp 113–125.Google Scholar
  62. 62.
    Sholley MM, Gimbrone MA, Cotiran RS. Cellular migration and replication in endothelial regeneration: a study using irradiated endothelial cultures. Lab Invest 36:18–25, 1977.PubMedGoogle Scholar
  63. 63.
    Hirsch EZ, Chisolm GM, White HM. Reendothelialization and maintenance of endothelial integrity in longitudinal denuded tracks in the thoracic aorta of rats. Atherosclerosis 46:287–307, 1983.PubMedCrossRefGoogle Scholar
  64. 64.
    Burkel WE, Vinter DW, Ford JW, Kahn RH, Graham LM, Stanley JC. Sequential studies of healing in endothelial seeded vascular protheses: Histologic and ultrastructure characteristics of graft incorporation. J Surg Res 30:305–324, 1981.PubMedCrossRefGoogle Scholar
  65. 65.
    Hladovec J, Rossman P. Circulating endothelial cells isolated together with platelets and the experimental modification of their counts in rats. Thrombosis Res 3:665–674, 1973.CrossRefGoogle Scholar
  66. 66.
    Bouvier CA, Gaynor E, Cintron JR, Bernhardt B, Spaet TH. Circulating endothelium as an indication of vascular injury. Thrombos Diathes Haemorrh Supple 40:163–168, 1970.Google Scholar
  67. 67.
    Fischer JJ, Unpublished data.Google Scholar
  68. 68.
    Narayan K, Cliff WJ. Morphology of irradiated microvasculature: A combined in vivo and electron microscopic study. Am J Pathol 106:47–62, 1982.PubMedGoogle Scholar
  69. 69.
    Rosen EM, Mueller SN, Noveral JP, Levine EM. Proliferative characteristics of clonal endothelial cell strains. J Cell Physiol 107:123–137, 1981.PubMedCrossRefGoogle Scholar
  70. 70.
    Repin VS, Dolgov VV, Zaikina OE, Novikov ID, Antonov AS, Nikolaeva MA, Smirnov VN. Heterogeneity of endothelium in human aorta. A quantitative analysis by scanning electron microscopy. Atherosclerosis 50:35–52, 1984.PubMedCrossRefGoogle Scholar
  71. 71.
    Thilo-Korner DGS, Freshney RI, eds, “The Endothelial Cell -A Pluripotent Control Cell of the Vessel Wall,” S. Karger, Basel, 1983.Google Scholar
  72. 72.
    Chamley-Campbell J, Campbell GR, Ross R. The smooth muscle cell in culture. Physiol Rev 59:1–61, 1979.PubMedGoogle Scholar
  73. 73.
    Ross R, Klebanoff SJ. The smooth muscle cell. I. In Vivo synthesis of connective tissue proteins. J Cell Biol 50: 159–171, 1971.PubMedCrossRefGoogle Scholar
  74. 74.
    Rubin DB, Drab EA, Ward WF, Smith LJ, Fowell SM. Enzymatic responses to radiation in cultured vascular endothelial and smooth muscle cells. Radiat Res 99:420–432, 1984.PubMedCrossRefGoogle Scholar
  75. 75.
    Eldor A, Vlodavsky I, Hyam E, Atzmon R, Fuks Z. The effect of radiation on prostacyclin (PGI) production by cultured endothelial cells. Prostaglandins 25:263–279, 1983.PubMedCrossRefGoogle Scholar
  76. 76.
    Hahn GL, Menconi MJ, Cahill M, Polgar P. The influence of gamma radiation on arachidonic acid release and prostacyclin synthesis. Prostaglandins 25:783–791, 1983.PubMedCrossRefGoogle Scholar
  77. 77.
    Rubin DB, Drab EA, Ts’ao CH, Gardner D, Ward WF. Prostacyclin (PGI) synthesis in irradiated endothelial cells cultued from bovine aorta. J Appl Physiol 58:592–597, 1985.PubMedGoogle Scholar
  78. 78.
    Ts’ao C, Ward WF. Acute radiation effects on the content and release of plasminogen activator activity in cultured aortic endothelial cells. Radiat Res 101:394–401, 1985.PubMedCrossRefGoogle Scholar
  79. 79.
    Sporn LA, Rubin P, Marder VJ, Wagner DD. Irradiation induced release of von Willebrand protein from endothelial cells in culture. Blood 64:567–570, 1984.PubMedGoogle Scholar
  80. 80.
    Friedman M, Ryan US, Davenport WC, Chaney EL, Strickland DL Kwock L. Reversible alterations in cultured pulmonary artery endothelial cell monolayer morphology and albumin permeability induced by ionizing radiation. J Cell Physiol 129:237–249, 1986.PubMedCrossRefGoogle Scholar
  81. 81.
    Friedman M, Saunders DS, Madden MC, Chaney EL, Kwock L. The effects of ionizing radiation on the pulmonary endothelial cell uptake of alpha-aminoisobutyric acid and synthesis of prostacyclin. Radiat Res 106:171–181, 1986.PubMedCrossRefGoogle Scholar
  82. 82.
    Dorer FE, Kahn JR, Lentz KE, Levine M, Skeggs LT. Hydrolysis of bradykinin by angiotensin-converting enzyme. Circ Res 34:824–827, 1974.PubMedGoogle Scholar
  83. 83.
    Sinzinger H, Firbas W, Cromwell M. Radiation induced alterations in rabbit aortic prostacyclin formation. Prostaglandins 24:323–329, 1982.PubMedCrossRefGoogle Scholar
  84. 84.
    Sinzinger H, Cromwell M, Firbas W. Long-lasting depression of rabbit aortic prostacyclin formation by single-dose irradiation. Radiat Res 97:533–536, 1984.PubMedCrossRefGoogle Scholar
  85. 85.
    Allen JB, Sagerman RH, Stuart MJ. Irradiation decreases vascular prostacyclin formation with no concomitant effect on platelet thromboxane production. Lancet 2:1193–1196, 1981.PubMedCrossRefGoogle Scholar
  86. 86.
    Baluda VP, Sushkevich GN, Parshkov EM, Lukoyanova TI. Influence of gamma-rays Co-60 and fast neutrons on intravascular platelet aggregation and prostacyclin-like activity of the vascular wall. ZKb Med 62:243, 1982.Google Scholar
  87. 87.
    Sakariassen KS, Bolhuis PA, Sixma JJ. Human blood platelet adhesion to artery subendothelium is mediated by factor VIII - von Willebrand factor bound to the subendothelium. Nature 279:636–638, 1979.PubMedCrossRefGoogle Scholar
  88. 88.
    Guidotti GG, Borghetti AF, Gazzola GC. The regulation of amino acid transport in animal cells. Biochim Biophys ActaGoogle Scholar
  89. 89.
    Lee S-L, Douglas WHJ, Lin P-S, Fanburg BL. Ultrastructural changes of bovine pulmonary artery endothelial cells irradiated in vitro with a 137-Cs source. Tissue Cell 15:193–204, 1983.PubMedCrossRefGoogle Scholar
  90. 90.
    Koteies GJ. Radiation effects on cell membrane. Radiat Environ Biophys 21:1, 1982.CrossRefGoogle Scholar
  91. 91.
    Ts’ao CH, Ward WF, Port CD. Radiation injury in rat lung. I. Prostacyclin (PGI) production, arterial perfusion, and ultrastructure. Rad Res 96:284–293, 1983.CrossRefGoogle Scholar
  92. 92.
    Ward WF, Solliday NH, Molteni A, Port CD. Radiation injury in rat lung. II. Angiotensin-converting enzyme activity. Radiat Res 96:294–300, 1983.PubMedCrossRefGoogle Scholar
  93. 93.
    Ts’ao CH, Ward WF, Port CD. Radiation injury in rat lung III. Plasminogen activator and fibrinolytic inhibitor activities. Radiat Res 96:301–308, 1983.PubMedCrossRefGoogle Scholar
  94. 94.
    Ward WF, Molteni A, Ts’ao CH, Solliday NH. Radiation injury in rat lung. IV. Modification by D-Penicillamine. Radiat Res 98:397–406, 1984.PubMedCrossRefGoogle Scholar
  95. 95.
    Ward WF, Molteni A, Solliday NH, Jones GE. The relationship between endothelial dysfunction and collagen accumulation in irradiated rat lung. Int J Radiat Oncol Biol Phys 11:1985–1990, 1985.PubMedCrossRefGoogle Scholar
  96. 96.
    Down JD, Nicholas D, Steel GG. Lung damage after hemithoracic irradiation: Dependence on mouse strain. Radiother Oncol 6:43–50, 1986.PubMedCrossRefGoogle Scholar
  97. 97.
    Martin BM. Unpublished data, 1986.Google Scholar
  98. 98.
    Reinhold HS, Buisman GH. Radiosensitivity of capillary endothelium. Brit J Radiol 46:54–57, 1973.PubMedCrossRefGoogle Scholar
  99. 99.
    Reinhold HS, Buisman GH. Repair of radiation damaqe to capillary endothelium. Brit J Radiol 48:727–731, 1975.PubMedCrossRefGoogle Scholar
  100. 100.
    Reinhold HS. Radiation and the microcirculation. In: “Frontiers of Radiation Therapy and oncology,” Vol 6 (JM Vaeth, ed, Karger, Basel), 1972, pp 21–43.Google Scholar
  101. 101.
    Gillette EL, Maurer GD, Severin GA. Endothelial repair of radiation damage following beta irradiation. Radiology 116:175–177, 1975.PubMedGoogle Scholar
  102. 102.
    Fike JR, Gillette EL. Co gamma and negative pi meson irradiation of microvasculature. Int J Radiat Oncol Biol Phys 4:825–828, 1978.PubMedGoogle Scholar
  103. 103.
    Fike JR, Gillette EL, Clow DJ. Repair of sublethal radiation damage by capillaries. Int J Radiat Oncol Biol Phys 5:339–342, 1979.PubMedCrossRefGoogle Scholar
  104. 104.
    Van den Brenk HAS. Macro-colony assay for measurement of reparative angiogenesis after x-irradiation. Int J Radiat Biol 21:607–611, 1972.CrossRefGoogle Scholar
  105. 105.
    Van den Brenk HAS, Sharpington C, Orton C, Stone M. Effects of x-radiation on growth and function of the repair blasteoma (granulation tissue). II. Measurements of angiogenesis in the Selye pouch in the rat. Int J Radiat Biol 25:277–289, 1974.CrossRefGoogle Scholar
  106. 106.
    Hopewell JW, Patterson TJS. The effects of previous x-irradiation on the revascularization of free skin grafts in the pig. Proc Brit Microcirc Soc, Northampton, 1971.Google Scholar
  107. 107.
    Sholley MM, Ferguson GP, Seibel HR, Montour JL, Wilson JD. Mechanisms of neovascularization: Vascular ’sprouting can occur without proliferation of endothelial cells. Lab Invest 51:624–634, 1984.PubMedGoogle Scholar
  108. 108.
    Yamaura H, Yamada K, Matsuzawa T. Radiation effect on the proliferating capillaries in rat transparent chambers. Int J Radiat Biol 30:179–187, 1976.CrossRefGoogle Scholar
  109. 109.
    Hirst DG, Denekamp J, Travis EL. The response of mesenteric vessels to irradiation. Radiat Res 77:259–275, 1979.PubMedCrossRefGoogle Scholar
  110. 110.
    Hirst DG, Denekamp J, Hobson B. Proliferation studies of the endothelial and smooth muscle cells of the mouse mesentery after irradiation. Cell Tissue Kinet 13:91–104, 1980.PubMedGoogle Scholar
  111. 111.
    Fajardo LF, Stewart JR. Capillary injury preceding radiation induced myocardial fibrosis. Radiology 101:429–433, 1971.PubMedGoogle Scholar
  112. 112.
    Stewart FA, Denekamp J, Hirst DG. Proliferation kinetics of the mouse bladder after irradiation. Cell Tissue Kinet 13:75–89, 1980.PubMedGoogle Scholar
  113. 113.
    Hobson B, Denekamp J. Endothelial proliferation in tumors and normal tissues. Continuous labelling studies, Brit J Cancer 49:405–413, 1984.PubMedCrossRefGoogle Scholar
  114. 114.
    Halle JS, Rosenman JG, Varia MA, Fowler WC, Walton LA, Currie JL. 1000 cGy single dose palliation for advanced carcinoma of the cervix or endometrium. Int J Radiat Oncol Biol Phys 12:1947–1950, 1985.Google Scholar
  115. 115.
    Thomlinson RH, Gray LH. Histological structure of some human lung cancers and possible implications for radiotherapy. Brit J Cancer 9:539–549, 1955.PubMedCrossRefGoogle Scholar
  116. 116.
    Evans HTS, Naylor PFD. The effect of oxygen breathing and radiotherapy upon the tissue oxygen tension of some human tumors. Brit J Radiol 36:418, 1963.CrossRefGoogle Scholar
  117. 117.
    Denekamp J, Hirst DG, Stewart FA, Terry NHA. Is tumor radiosensitization by misonidazale a general phenomenon? Br J Cancer 41:1–9, 1980.PubMedCrossRefGoogle Scholar
  118. 118.
    Bush RS. The significance of anemia in clinical radiation therapy (Editorial). Int J Radiat Oncol Biol Phys 12:2047–2050, 1986.PubMedCrossRefGoogle Scholar
  119. 119.
    Hirst DG. Anemia: A problem or an opportunity in radiotherapy? Int J Radiat Oncol Biol Phys 12:2009–2017, 1986.PubMedCrossRefGoogle Scholar
  120. 120.
    Siracka E, Siracky J, Pappova N, Revesz L: Vascularization and radiocurability in cancer of the uterine cervix. A retrospective study. Neoplasma 29:183–188, 1982.PubMedGoogle Scholar
  121. 121.
    Kolstad P. Intercapillary distance, oxygen tension, and local recurrence in cervix cancer. Scand J Clin Lab Invest 22 Suppl 106:145, 1968.Google Scholar
  122. 122.
    Brown MJ. Sensitizers and protectors in radiotherapy, Cancer 55:2222–2228, 1985.PubMedCrossRefGoogle Scholar
  123. 123.
    Teicher BA, Rose CM. Perfluorochemical emulsions can increase tumor radiosensitivity. Science 223:934–936, 1984.PubMedCrossRefGoogle Scholar
  124. 124.
    Fischer JJ, Rockwell S, Martin DF: Perfluorochemicals and hyperbaric oxygen in radiation therapy. Int J Radiat Oncol Biol Phys 12:95–102, 1986.PubMedGoogle Scholar
  125. 125.
    Schwartz SM. Molecular biology of the vascular wall. Proceedings of a meeting. Arteriosclerosis 4:647–656, 1984.Google Scholar
  126. 126.
    Stiles CD. The molecular biology of platelet-derived growth factor. Cell 33:653–655, 1983.PubMedCrossRefGoogle Scholar
  127. 127.
    Carpenter G, Cohen S. Epidermal growth factor. Ann Rev Biochem 48:193–216, 1979.PubMedCrossRefGoogle Scholar
  128. 128.
    Maciag T, Hoover GA, Weinstein R. High and low molecular weight forms of endothelial cell growth factor. J Biol Chem 257:5333–5336, 1982.PubMedGoogle Scholar
  129. 129.
    Schwartz SM, Gajdusek CM. Growth factors and the vessel wall. Prog Hemost Thromb 6:85–112, 1982.PubMedGoogle Scholar
  130. 130.
    Doolittle RF, Hunkapiller MW, Hood LE et al. Simian sarcoma virus oncogene, v-sis, is derived from the gene (or genes) encoding a platelet-derived growth factor. Science 221:275–277, 1983.PubMedCrossRefGoogle Scholar
  131. 131.
    Stoschek CM, King LE. Functional and structural characteristics of EGF and its receptor and their relationship to transforming proteins. J Cell Biochem 31:135–152, 1986.CrossRefGoogle Scholar
  132. 132.
    Collins T, Ginsburg D, Boss JM, Orkin SH, Pober JS. Cultured human endothelial cells express platelet-derived growth factor B chain: cDNA cloning and structural analysis. Nature 316:748–750, 1985.PubMedCrossRefGoogle Scholar
  133. 133.
    Grotendorst GR, Seppa H, Kleinman HK, Martin GR. Attachment of smooth muscle cells to collagen and their migration toward platelet derived growth factor. Proc Natl Acad Sci USA 78:3669–3672, 1981.PubMedCrossRefGoogle Scholar
  134. 134.
    Folkman J. How is blood vessel growth regulated in normal and neoplastic tissue? G.H.A. Clowes Memorial Award Lecture. Cancer Res 46:467–473, 1986.PubMedGoogle Scholar
  135. 135.
    Folkman J. Tumor angiogenesis. Adv Cancer Res 43:175–203, 1985.PubMedCrossRefGoogle Scholar
  136. 136.
    Shing Y, Folkman J, Haudenschild C, Lund D, Crum R, Klagsbrun M. Angiogenesis is stimulated by a tumor-derived endothelial cell growth factor. J Cell Biochem 29:275–287, 1985.PubMedCrossRefGoogle Scholar
  137. 137.
    Kurachi K, Davie EW, Strydom DJ, Riordan JF, Vallee BL. Sequence of cDNA and gene for angiogenin, a human angiogenesis factor. Biochemistry 24:5494–5499, 1985.PubMedCrossRefGoogle Scholar
  138. 138.
    Palmer KA, Scheraga HA, Riordan JF, Vallee BL. A preliminary three-dimensional structure of angiogenin. Proc Natl Acad Sci USA 83:1965–1969, 1986.PubMedCrossRefGoogle Scholar
  139. 139.
    Shapiro R, Riordan JF, Vallee BL. Characteristic ribonucleolytic activity of human angiogenin. Biochemistry 25:3527–3532, 1986.PubMedCrossRefGoogle Scholar
  140. 140.
    Castellot JJ, Karnovsky MJ, Rosenberg RD. Endothelium, heparin, and regulation of vascular smooth muscle cell growth, In: “The Biology of Endothelial Cells” (EA Jaffe, ed, Martinus Nijhoff, Boston), 1984, pp 118–128.Google Scholar
  141. 141.
    Thornton SC, Mueller SN, Levine EN. Human endothelial cells: use of heparin in cloning and long-term serial cultivation. Science 222:623–625, 1983.PubMedCrossRefGoogle Scholar
  142. 142.
    Heimark RL, Schwartz SM. The role of membrane-membrane interactions in the regulation of endothelial cell growth. J Cell Biol 100:1934–1940, 1985.PubMedCrossRefGoogle Scholar

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© Kluwer Academic Publishers, Boston 1988

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