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Angiogenesis: possibilities for therapeutic interventions

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Abstract

Vascular proliferation normally occurd only during embryonic development, the female reproductive cycle and wound healing. Various pathological conditions such as diabetic retinopathy are characterized by persistent, uncontrolled angiogenesis. At the other hand, impaired development of new blood vessels has been found to be related with myocardial infarction. A series of anti‐angiogenic drugs are currently included in experimental cancer treatment, whereas the failure of ulcers to heal may be limited by increased angiogenesis upon administration of growth factors. In the present review control mechanisms of the vasculature are summarized and therapeutic approaches discussed.

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References

  1. Dameron KM, Volpert OV, Tainsky MA, Bouck N. Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science 1994; 265: 1582–4.

    Google Scholar 

  2. Pepper MS, Ferrara N, Orci L, Montesano R. Potent synergism between vascular endothelial growth factor and basic fibroblast growth factor in the induction of angiogenesis in vitro. Biochem Biophys Res Commun 1992; 189: 824–31.

    Google Scholar 

  3. Barger AC, Beeuwkes R, III, Lainey LL, Silverman KJ. Hypothesis: vasa vasorum and neovascularization of human coronary arteries. A possible role in the pathophysiology of atherosclerosis. N Engl J Med 1984; 310: 175–7.

    Google Scholar 

  4. O'Brien ER, Garvin MR, Dev R. Angiogenesis in human coronary atherosclerotic plaques. Am J Pathol 1994; 145: 883–94.

    Google Scholar 

  5. Stavri GT, Hong Y, Zachary IC. Hypoxia and platelet-derived growth factor-BB synergistically upregulate the expression of vascular endothelial growth factor in vascular smooth muscle cells. FEBS Lett 1995; 358: 311–5.

    Google Scholar 

  6. Miller JW, Adamis AP, Shima DT, D'Amore PA, Moulton RS, O'Reilly MS, Folkman J, Dvorak HF, Brown LF, Berse B, et al. Vascular endothelial growth factor/vascular permeability factor is temporally and spatially correlated with ocular angiogenesis in a primate model. Am J Pathol 1994; 145: 574–84.

    Google Scholar 

  7. Aiello LP, Avery RL, Arrigg PG, Keyt BA, Jampel HD, Shah ST, Pasquale LR, Thieme H, Iwamoto MA, Park JE, et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med 1994; 331: 1480–7.

    Google Scholar 

  8. Dvorak HF, Brown LF, Detmar M, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability and angiogenesis. Am J Pathol 1995; 146: 1029–39.

    Google Scholar 

  9. Schweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxiainitiated angiogenesis. Nature 1992; 359: 843–5.

    Google Scholar 

  10. Peacock DJ, Banquerigo ML, Brahn E. Angiogenesis inhibition suppress collagen arthritis. J Exp Med 1992; 175: 1135–8.

    Google Scholar 

  11. Nicholoff BJ, Mitra RS, Varani J, Dixit VM, Polverini PJ. Aberrant production of interleukin-8 and thrombospondin-1 by psoriatic keratinocytes mediates angiogenesis. Am J Pathol 1994; 144: 820–8.

    Google Scholar 

  12. Takahashi K, Mulliken JB, Kozahewich HP, Rogers RA, Kolkman J, Ezehowitz RA. Cellular markers that distinguish the phases of hemangioma during infancy and childhood. J Clin Invest 1994; 93(6): 2357–64.

    Google Scholar 

  13. Hull MA, Cullen DJE, Hawkey CJ. Basic fibroblast growth factor in gastric ulceration: mucosal levels and therapeutic potential. Gastroenterology 1994; 106: Suppl A97. Abstract.

  14. Folkman J, Szabo S, Stovroff M, Mc Neil P, Li W, Shing Y. Duodenal ulcer: discovery of a new mechanism and development of angiogenic therapy which accelerates healing. Ann Surg 1991; 214: 414–27.

    Google Scholar 

  15. Folkman J. Angiogenesis in female reproductive organs. In: Alexander NH, d'Arrangues C, eds. Steroid hormones and uterine bleeding. Washington, DC: AAAS Press 1992; 143–58.

    Google Scholar 

  16. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971; 285: 1182–6.

    Google Scholar 

  17. Folkman J. Angiogenesis in cancer, vascular, rheumatoid, and other disease. Nat Med 1995; 1: 27–31.

    Google Scholar 

  18. Folkman J. Tumor angiogenesis. In: Holland JF, Frei E III, Bast RC Jr, Kufe DW, Morton DL, Weichselbaum RR, eds. Cancer Medicine. 3rd ed Vol 1. Philadelphia: Lea & Febiger, 1993: 153–70.

    Google Scholar 

  19. Folkman J. Clinical applications of research on angiogenesis. N Engl J Med 1995; 333: 1757–63.

    Google Scholar 

  20. Pepper MS, Ferrara N, Orci L, Montesano R. Potent synergism between vascular endothelial growth factor and basic fibroblast growth factor in the induction of angiogenesis in vitro. Biochem Biophys Res Commun 1992; 189: 824–31.

    Google Scholar 

  21. Holmgren L, O'Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med 1995; 1: 149–153.

    Google Scholar 

  22. Holzman D. New view of metastasis is spreading. J Natl Cancer Inst 1996; 88: 1336–8.

    Google Scholar 

  23. Zhang H-T, Craft P, Scott PAE, Ziche M, Weich HA, Harris AL, Bicknell R. Enhancement of tumor growth and vascular density by transfection of vascular endothelial growth factor by MCF-7 human breast carcinoma cells. J Natl Cancer Inst 1995; 87

  24. Dickinson AJ, Fox SB, Persad RA, Hollyer J, Sibley GNA, Harris AL. Quantification of angiogenesis as an independent predictor of prognosis in invasive bladder carcinomas. Br J Urol 1994; 74: 762–6.

    Google Scholar 

  25. Yoshino S, Kato M, Okada K. Prognostic significance of microvessel count in low stage renal cell carcinoma. Int J Urol 1995; 2: 156–60.

    Google Scholar 

  26. Gasparini G, Fox SB, Verderio P, Bonoldi E, Bevilacqua P, Borachi P, Dante S, Marubini E, Harris AL. Determination of angiogenesis adds information to Estrogen receptor status in predicitng the efficacy of adjuvant tamoxifen in nodepositive breast cancer patients. Clin Cancer Res 1996; 2: 1191–8.

    Google Scholar 

  27. Takahashi Y, Kitadai Y, Bucana CD, Cleary KR, Ellis LM. Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res 1995; 55: 3664–8.

    Google Scholar 

  28. Jensen HM, Chen I, De Vault MR, Lewis AE. Angiogenesis induced by “normal” human breast tissue: a probable marker for pre cancer. Science 1982; 218: 293–4.

    Google Scholar 

  29. Takahashi Y, Cleary KR, Mai M, Kitadai Y, Bucana CD, Ellis LM. Significance of vessel count and vascular endothelial growth factor and its receptor (KDR) in intestinal-type gastric cancer. Clin Cancer Res 1996; 2: 1679–84.

    Google Scholar 

  30. McCulloch P, Choy A, Martin L. Association between tumour angiogenesis and tumour cell shedding into effluent venous blood during breast cancer surgery. Lancet 1995; 346: 1334–5.

    Google Scholar 

  31. Fontanini G, Vignati S, Bigini D, Lucchi M, Mussi A, Basolo F, Angeletti CA, Bevilacqua G. Neoangiogenesis: a putative marker of malignancy in non-small-cell lung cancer (NSCLC) development. Int J Cancer 1996; 67: 615–9.

    Google Scholar 

  32. Fontanini G, Vignati S, Bigini D, Lucchi M, Mussi A, Angeletti CA, Bevilacqua G. Microvessel count predicts metastatic disease and overall survival in non-small-cell lung carcinomas. J Pathol 1995; 177: 57–63.

    Google Scholar 

  33. Mattern J, Kallinowski F, Herfarth C, Volm M. Association of resistance-related protein expression with poor vascularization and low levels of oxygen in human rectal cancer. Int J Cancer 1996; 67: 20–3.

    Google Scholar 

  34. Lindmark G, Gerdin B, Sundberg C, Pahlman L, Bergstrom,Glimelius B. Prognostic significance of the microvascular count in colorectal cancer. J Clin Oncol 1996; 14: 461–6 & (reply) J Clin Oncol 1996; 14: 2402-3.

    Google Scholar 

  35. Pape H, Geismar D, Schmitt G. Capillar density in preirradiated breast cancer. Reg Cancer Treat 1994; 7: 118–20.

    Google Scholar 

  36. Astrow AB. Rethinking cancer. Lancet 1994; 343: 494–5.

    Google Scholar 

  37. Shipper H, Goh CR, Wang TL. Rethinking cancer; should we control rather than kill. Parts 1 & 2. Can J Oncol 1993; 3: 207–16 & 220-4.

    Google Scholar 

  38. Fan TPD, Jaggar R, Bichnell R. Controlling the vasculature: angiogenesis, anti-angiogenesis and vascular targeting of gene therapy. Trends Pharmacol Sci 1995; 16: 57–66.

    Google Scholar 

  39. White CW, Sonsheimer HM, Crouck EC, Wilson H, Fan LL. Treatment of pulmonary hemangiomatosis with recombinant interferon alfa-za. N Engl J Med 1989; 320: 1197–200.

    Google Scholar 

  40. Ezekowitz RAB, Mulliken JB, Folkman J. Interferon alfa-2a therapy for life-threatening hemangiomas of infancy. N Engl J Med 1992; 326: 1456–63; N Engl J Med 1994; 330: 300; & N Engl J Med 1995; 333: 595-6.

    Google Scholar 

  41. Singh RK, Gutman M, Bucana CD, Sanchez R, Llansa N, Fidler IJ. Interferons and down-regulate the expression of basic fibroblast growth factor in human carcinomas. Proc Natl Acad Sci USA 1995; 92: 4562–6.

    Google Scholar 

  42. Ingber D, Fujita T, Kishimoto S, Sudo K, Kanamaru T, Brem H, Folkman J. Synthetic analogues of fumagillin that inhibit angiogenesis and suppress tumour growth. Nature 1990; 348: 555–7.

    Google Scholar 

  43. Abe J, Zhou W, Takuwa N, Taguchi J, Kurukawa K, Kumada M, Takuwa Y. A fumagillin derivative angiogenesis inhibitor, AGM-1470, inhibits activation of cyclin-dependent kinases and phosphorylation of retinoblastomagene product but not protein tyrosyl phosphorylation or proto-oncogene expression in vascular endothelial cells. Cancer Res 1994; 54: 3407–12.

    Google Scholar 

  44. Peacock DJ, Banquerigo ML, Brahn E. Angiogenesis inhibtion suppresses collagen arthritis. J Exp Med 1992; 175: 1135–8.

    Google Scholar 

  45. Brem H and Folkman J. Analysis of Experimental Antiangiogenic therapy. J Ped Surg 1993; 28: 445–51.

    Google Scholar 

  46. Yazaki T, Takamiyn Y, Costello PC, Mineta T, Menon AG, Rabkin SD, Martuza RL. Inhibtion of angiogenesis and growth of human non-malignant and malignant meningiomas by TNP-470. J Neurooncol 1995; 23(1): 23–9.

    Google Scholar 

  47. Hu DE, Fan TP. Suppression of VEGF-induced angiogenesis by the protein kinase inhibitor, Lavendustin A. Br J Pharmacol 1995; 114(2): 262–8.

    Google Scholar 

  48. Takano S, Gately S, Neville ME, Herblin WF, Gross JL, Engelhard H, Perricone M, Eidsvoog K, Brem S. Suramin, an anticancer and angiosuppressive agent, inhibits endothelial cell binding of basic fibroblast growth factor, migration, proliferation, and induction of urokinase-type plasminogen activator. Cancer Res 1994; 54(10): 2654–60.

    Google Scholar 

  49. Presenti E, Sola F, Mongelli N, Grandi M, Spreafico F. Suramin prevents neovascularization and tumour growth through blocking of basic fibroblast growth factor activity. Br J Cancer 1992; 66(2): 367–72.

    Google Scholar 

  50. Pepper MS, Vasalli JD, Wilks JW, Schweigerer L, Orei L, Montesano R. Modulation of bovine microvascular endothelial cell proteolytic properties by inhibitors of angiogenesis. J Cell Biochem 1994; 55(4): 419–34.

    Google Scholar 

  51. Gagliardi A, Hadd H, Collins DC. Inhibition of angiogenesis by suramin. Cancer Res 1992; 52(18): 5073–5.

    Google Scholar 

  52. Larsen AK. Suramin: an anticancer drug with unique biological effects. Cancer Chemother Pharmacol 1993; 32: 96–8.

    Google Scholar 

  53. Stein CA. Suramin: a novel antineoplastic agent with multiple potential mechanisms of action. Cancer Res 1993; 53: 2239–48.

    Google Scholar 

  54. Van Oosterom AT, de Smedt EA, Denis LC, de Bruijn EA, Mahler C. Surmain for prostatic cancer: a phase I/II study in advanced extensively pretreated disease. Eur J Cancer 1990: 26: 422.

    Google Scholar 

  55. de Bruijn EA, Pattyn G, Denis L, Mahler C, van Oosterom AT, de Smedt E. Therapeutic drug monitoring of suramin and protein binding. J Liq Chromatogr 1991; 14(20): 3719–33.

    Google Scholar 

  56. Braddock PS, Hu D.-E, Fan T-PD, Stratford IJ, Harris AL, Bicknell RA. A structure-activity analysis of antagonism of the growth factor and angiogenic activity of basic fibroblast growth factor by suramin and related polyanions. Br J Cancer 1994; 69: 890–898.

    Google Scholar 

  57. Ny T, Sawdey M, Lawrence D, Millan JL, Loskutoff DJ. Cloning and sequence of a cDNA coding for the human beta-migrating endothelial-cell-type plasminogen activator inhibitor. Proc Natl Acad Sci USA 1986; 83: 6776–80.

    Google Scholar 

  58. Liotta LA, Steeg PS, Stetler-Stevenson WG. Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 1991; 64: 327–36.

    Google Scholar 

  59. Eisenstein R, Kuettner KE, Neopolitan C, Soble LW, Sorgente N. The resistance of certain tissues to invasion III. Cartilage extracts inhibit the growth of fibroblasts and endothelial cells in culture. Am J Pathol 1975; 81: 337–48.

    Google Scholar 

  60. Brem H, Folkman J. Inhibition of tumor angiogenesismediated by cartilage. J Exp Med 1975; 141: 427–39.

    Google Scholar 

  61. Langer R, Conn H, Vacanti J, Haudenschild JC, Folkman J. Control of tumourgrowth in animals by infusion of an angiogenic inhibitor. Proc Natl Acad Sci USA 1980; 77: 4331–5.

    Google Scholar 

  62. Moses MA, Sudhalter J, Langer R. Identification of an inhibitor of neovascularisation from cartilage. Science 1990; 248: 1408–1410.

    Google Scholar 

  63. Moses MA, Sudhalter J, Langer R. Isolation and characterization of an inhibitor of neovescularization from scapular chondrocytes. J Cell Biol 1992; 119: 475–82.

    Google Scholar 

  64. Bagavandoss P, Kaytes P, Vogeli G, Wells PA and Willis JW. Recombinant truncated thrombospondin-1 monomer modulates endothelial cell plasminogen activator inhibitor 1 accumulation and proliferation in vitro. Biochem Biophys Res Commun 1990; 170: 867–72.

    Google Scholar 

  65. Blei F, Wilson L, Mignatti P, Rifkin D. Mechanism of action of angiostatic steroids: suppression of plasminogen activator activity via stimulation of plasminogen activator inhibitor synthesis. J Cell Physiol 1993; 155: 568–78.

    Google Scholar 

  66. Davies B, Brown PD, East N, Crimmin MJ, Balkwill FR. A synthetic matrix metalloproteinase inhibitor decreases tumor burden and prolongs survival of mice bearing human ovarian carcinoma xenografts. Cancer Res 1993; 53: 2087–91.

    Google Scholar 

  67. Taylor S, Folkman J. Protamine is an inhibitor of angiogenesis. Nature 1982; 297: 307–12.

    Google Scholar 

  68. Maione TE, Gray GS, Petro J, Hunt AJ, Donner AL, Bauer SI, Carson HF, Sharper KJ. Inhibition of angiogenesis by recombinant human platelet factor-4 and related peptides. Science 1990; 247: 77–9.

    Google Scholar 

  69. Maione TE, Gray GS, Hunt AJ, Sharpe RJ. Inhibition of tumor growth in mice by an analogue of platelet factor-4 that lacks affinity for heparin and retains potent angiostatic activity. Cancer Res 1991; 51: 2077–83.

    Google Scholar 

  70. Crum R, Szabo S, Folkman J. A new class of steroids inhibits angiogenesis in the presence of heparin ar a heparin fragment. Science 1985; 230: 1375–78.

    Google Scholar 

  71. Ingber DE, Madri J, Folkman J. A possible mechanism of inhibition of angiogenesis by angiostatic steroids: induction of capillary basement membrane dissolution. Endocrinology 1986; 119: 1768–75.

    Google Scholar 

  72. Folkman J, Ingber DE. Angiostatic steroids. Method of discovery and mechanisms of action. Ann Surg 1987; 206: 374–83.

    Google Scholar 

  73. Folkman J, Klagsbrun M, Sasse J, Wadzinski M, Ingber D, Vlodavsky I. A heparin-binding angiogenic factor-basic fibroblast growth factor-is stored within basement membrane Am J Pathol 1988; 130: 393–400.

    Google Scholar 

  74. Sohn K-H, Lee H-Y, Chung H-Y, Young H-S, Yi S-Y, Kim K-W. Anti-angiogenic activity of triterpene acids. Cancer Letters 1995; 94: 213–8.

    Google Scholar 

  75. Otsuka T, Takase S, Terano H, Okuhara M. New angiogenesis inhibitors, WF-16775 A and A2. J Antibiotics 1992; 45(12): 1970–3.

    Google Scholar 

  76. Kretzschmar L, Metze D, Vering KH, Bonsmann G. Papillomatosis confluens et reticularis. Erfolgreiche therpaie mit minocyclin. Hautartz 1996; 47: 209–13.

    Google Scholar 

  77. Yamashita T, Sahai M, Kaway Y, Aino M, Takahashi K. A new activity of herbimycin A: inhibition of angiogenesis. J Antibiot 1989; 42: 1015–7.

    Google Scholar 

  78. Soldi R, Somavio F, Aglietta M, Primo L, Defilippi P, Marchisio PC, Bussolino F. Platelet-activating factor (PAF) induces the early tyrosine phosphorylation of focal adhesion kinase (p125FAK) in human endothelial cells. Oncogene 1996; 13: 515–25.

    Google Scholar 

  79. Millauer B, Wizigmann-Voos S, Schnürch H, Martinez R, Miller NPH, Risau W, Ullrich A. High affinity VEGF binding and developmental expression suggests Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 1993; 72: 835–46.

    Google Scholar 

  80. Schweigerer L, Christeleit K, Fleischmann G, Adlerceutz H, Wahala K, Hase T, Schwab M, Ludwig R, Fotsis T. Identification in human urine of a natural growth inhibitor of cells derived from solid paediatric tumors. Eur J Clin Invest 1992; 22: 260–4.

    Google Scholar 

  81. Aldercreutz H, Hongo H, Higashi A, Fotsis Y, Hamalainen E, Okada H. Urinary excretion of lignans and isoflavoid phytoestrogens in Japanese men and women consuming a traditionel Japanese diet. Am J Clin Nutr 1991; 54: 1093–100.

    Google Scholar 

  82. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton N, McClain J, Aldrich TH, Papadopoulos N, Daly TJ, Davis S, Sato TN, Yancopoulos GD. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Sience 1997; 277: 55–60.

    Google Scholar 

  83. Prehn RT. The inhibition of tumor growth by tumor mass. Cancer Res 1991; 51: 2–4.

    Google Scholar 

  84. O'Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, Lane WS, Cao Y, Sage EH, Folkman J. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis Lung carcinoma. Cell 1994; 79: 315–28.

    Google Scholar 

  85. Lerch OG, Rickli EE, Legier W, Gillessen D. Localization of individual lysine-binding regions in human plasminogen and investigation of the complex-forming properties. Eur J Biochem 1980; 107: 7–13.

    Google Scholar 

  86. Grant DS, Kleinman HK, Goldberg ID, Bhagara MM, Nickoloff BJ, Kinsella JL, Polverini P, Rosen EM. Scatter facror induces blood vessel formation in vivo. Proc Natl Acad Sci USA 1993; 90: 1937–41.

    Google Scholar 

  87. Tsarfaty I, Resau JH, Rulang S, Keydar I, Faletto DL, Vande Woude GF. The net proto-oncogene receptor and lumen formation. Science 1992; 257: 1258–61.

    Google Scholar 

  88. Fotsis T, Zhang Y, Pepper MS, Aldercreutz H, Montesano R, Nauroth PP, Schweigerer L. The endogenous oestrogen metabolite 2-methoxyoestradiol inhibits angiogenesis and suppresses tumour growth. Nature 1994; 368: 237–239.

    Google Scholar 

  89. O'Shea KS, Dixit V. Unique distribution of extracellular matrix component thrombospondin in the developing mouse embryo. J Cell Biol 1988; 107: 2737–48.

    Google Scholar 

  90. Rastinejad F, Polverini PJ, Bouck NP. Regulation of the activity of a new inhibitor of angiogenesis by a cancer suppressor gene. Cell 1989; 56: 345–55.

    Google Scholar 

  91. Good DJ, Polverini RJ, Rastinejad F, Le Beau MN, Leuras RS, Frazer WA, Bouck NP. A tumor suppressor dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc Natl Acad Sci USA 1990; 87: 6624–8.

    Google Scholar 

  92. Tolsma SS, Volpert OV, Good DJ, Frazer WA, Polverini PJ, Bouck N. Peptids from two separate domains of the matrix molecule TSP-1 have antiangiogenic activity. J Cell Biol 1993; 122: 497–511.

    Google Scholar 

  93. Nicosia RF, Tuszunski GP. Matrix bound thrombospondin promotes angiogenesis in vitro. J Cell Biol 1994; 124: 184–93.

    Google Scholar 

  94. Roberts DD. Regulation of tumour growth and metastasis by thrombospondin-1. FASEB J 1996; 10: 1183–91.

    Google Scholar 

  95. Harning R, Koo GC, Szalay J. Regulation of the metastasis of murine ocular melanoma by natural killer cells. Invest Ophthalmol Vis Sci 1989; 30(9): 1909–15.

    Google Scholar 

  96. Ingber D, Folkman J. Inhibition of angiogenesis through modulation of collagen metabolism. Lab Invest 1988; 59: 44–51.

    Google Scholar 

  97. Norrby K. L-Proline, LACA, inhibits mast cell induced angiogenesis. Int J Microcirc Clin Exp 1993; 12: 119–29.

    Google Scholar 

  98. Klohs WD, Steinkampf RW, Wicha MS, Marlin AE, Tunas JB, Leopold WR. Collagen production inhibitors evaluated as antitumour-agents. JNCI/J Natl Cancer Inst 1985; 75: 353–59.

    Google Scholar 

  99. Lewko WM, Liotta LA, Wicha MS, Vanderhaar BK, Kidwell WR. Sensitivity of N-nitrosomethylurea-induced rat mammary tumour to cis-hydroxyproline, an inhibitor of collagen production. Cancer Res 1981; 41: 2855–62.

    Google Scholar 

  100. Wicha MS, Liotta LA, Lewko LA, Kidwell WR. Blocking basement membrane collagen deposition inhibits the growth of 7,12-dimethylbenzanthracene-induced rat mammary tumours. Cancer Lett 1981; 12: 9–12.

    Google Scholar 

  101. Tay EML, Ryhanen L, Kitto J. Proline analogues inhibit human skin fibroblasts growth and collagen production in culture. Invest Dermatol 1983; 80: 261–67.

    Google Scholar 

  102. Bastaki M, Missirlis E, Klouras N, Karakiulakis G, Maragoudalis E. Suppression of angiogenesis by the antitumor agent titanocene dichloride. Eur J Pharmacol 1994; 251: 263–69.

    Google Scholar 

  103. Majewski S, Kamisinski MJ, Szwito A, Kuminska G, Melejczk J. Inhibition of tumor induced angiogenesis by systemically administered protamine sulfates. Int J Cancer 1984; 33: 831–33.

    Google Scholar 

  104. Neufeld G, Gospodarowicz D. Protamine sulfate inhibits mitogenic activities of the extracellular matrix and fibroblast growth factor, but potentiates that of epidermal growth factor. J Cell Physiol 1987; 132: 287–94.

    Google Scholar 

  105. Cockerill GW, Bert AG, Ryan GR, Gamble JR, Vadas MA, Cockerill PN. Regulation of granulocyte-macrophage colony-stimulating factor and E-selection expression in endothelial cells by cyclosporin A and the T-cell transcription factor NFAT. Blood 1995; 86(7): 2689–98.

    Google Scholar 

  106. Norrby K. Cyclosporin is angiostatic. Experienta 1992; 48: 1135–38.

    Google Scholar 

  107. Feinberg RN, Beebe DC. Hyaluronate in vasculogenesis. Science 1983; 220: 1177–79.

    Google Scholar 

  108. Belsky E, Toole BP. Hyaluronate and hyaluronidase in the developing chick embryo kidney. Cell Differ 1983; 12: 61–6.

    Google Scholar 

  109. Montesano R, Kumar S, Orci L, Pepper MS. Synergisti effect of hyaluronan oligosaccharides and vascular endothelial growth factor on angiogenesis in vitro. Lab Invest 1996; 75: 249–62.

    Google Scholar 

  110. Lowe JB, Stoolman LM, Nair RP, Larssen RD, Berherd TC, Marks RM. ELAM-1-dependant cell adhesion to vascular endothelium determined by a transfected human fucosyl transferase cDNA. Cell (Cambridge, Mass) 1990; 63: 475–84.

    Google Scholar 

  111. Phillips ML, Nudelman E, Gaeta FCA, Perez M, Singhal AK, Nakomori S.-I, Paulson JC. ELAM—1 mediates cell adhesion by recognition of a carbohydrate ligand, sialyl-Lex. Science 1990; 250: 1130–32.

    Google Scholar 

  112. Walz G, Aruffo A, Kolanus W, Bevilacqua M, Seed B. Recognition by ELAM-1 of the sialyl-Lex determinant on myeloid and tumor cells. Science 1990; 250: 1132–35.

    Google Scholar 

  113. Nguyen M, Folkman J, Bischoff J. 1-Deoxymannojirimycin inhibits capillary tube formation in vitro. J Biol Chem 1992; 267: 26157–65.

    Google Scholar 

  114. Jayson GC, Gallagher JT. Heparin oligosaccharides: inhibitors of the biological activity of bFGF on CaCo-2 cells. Brit J Cancer 1997; 75: 9–16.

    Google Scholar 

  115. Inoue K, Korenga H, Tanaka NG, Sakamoto N, Kadoya S. The sulfated polysaccharide-peptidoglycon complex potently inhibits embryonic angiogenesis and tumour growth in the presence of cortisone acetate. Carbohydr Res 1988; 181: 135–42.

    Google Scholar 

  116. Tanaku NG, Sakamoto N, Korenaga H, Inoue K, Ogamura H, Osada Y. The combination of bacterial polysaccharide and tamoxifen inhibits angiogenesis and tumour growth. Int J Radiat Biol 1191; 60: 79–83.

    Google Scholar 

  117. Colburn P, Buonassis V. Estrogen binding sites in endothelial cell cultures. Science 1978; 201: 817–9.

    Google Scholar 

  118. Venkov CD, Rankin AB, Vaughan DE. Identification of authetic estrogen receptor in cultured endothelial cells: a potential mechanism for steroid hormone regulation of endothelial function. Circulation 1996; 94: 727–33.

    Google Scholar 

  119. Iafrati MD, Karas RH, Aronovitz M, Kim S, Sullivan TR, Lulahn DB, O'Donnell TF, Korach KS, Mendelsohn ME. Estrogen inhibits the vascular injury response in estrogen receptor-deficient mice. Nature med 1997; 3(5): 545–8.

    Google Scholar 

  120. Voest EE, Kenyon BM, O'Reilly MS, Truit G, D'Amato RJ, Folkman J. Inhibition of angiogenesis in vivo by IL-12. J Nat Cancer Inst 1995; 87(8): 581–6.

    Google Scholar 

  121. Sgadari C, Angiolillo AL, Tosato G. Inhibition of angiogenesis by IL-12 is mediated by the interferon-inducible protein 10. Blood 1996; 87(9): 3877–82.

    Google Scholar 

  122. Angiolillo AL, Sgadari C, Tosato G. A role for the interferoninducible protein 10 in inhibition of angiogenesis by IL-12. Ann NY Acad Sci 1996; 795:158–67.

    Google Scholar 

  123. Sakkoula E, Pipili-Synetos E, Mragoudakis ME. Involvement of nitric oxide in the inhibition of angiogenesis by interleukin-2. Br J Pharmacol 1997; 122: 793–795.

    Google Scholar 

  124. Millauer B, Shanver LK, Plate KH, Risau W, Ulrich A. Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1 mutant. Nature 1994; 367: 576–9.

    Google Scholar 

  125. Olson KA, French TC, Vallee BL, Fett JW. A monoclonal antibody to human angiogenin suppresses tumor growth in athymic mice. Cancer Res 1994; 54: 4576–9.

    Google Scholar 

  126. Huang X, Molema G, King S, Watkins L, Edgington TS, Thorpe PE. Tumor infarction in mice by antibody-directed targeting of tissue factor to tumor vasculature. Science 1997; 275: 547–50.

    Google Scholar 

  127. Kawakami-Kimura N, Narita T, Ohmori K, Yoneda T, Matsumoto K, Nakamura T, Kannagi R. Involvement of hepatocyte growth factor in increased integrin expression on HepG 2 cells triggered by adhesion to endothelial cells. Brit J Cancer 1997; 75: 47–53.

    Google Scholar 

  128. Horwitz AF. Integrins and health. Sci Amer 1997; May: 46–53.

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Authors and Affiliations

  1. Laboratory of Experimental Oncology (LEO), Herestraat 49, B-3000, Leuven, Belgium

    W. Wynendaele, A.T. van Oosterom, A. Pawinski & E.A. de Bruijn

  2. Laboratory of Human Toxicology (NIDDR), Department of Pharmaceutics, University of Utrecht, Sorbonnelaan 16, PO Box80082, 3508 TB, Utrecht, The Netherlands

    E.A. de Bruijn & R.A. Maesi

Authors
  1. W. Wynendaele
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  2. A.T. van Oosterom
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  3. A. Pawinski
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  4. E.A. de Bruijn
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  5. R.A. Maesi
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Wynendaele, W., van Oosterom, A., Pawinski, A. et al. Angiogenesis: possibilities for therapeutic interventions. Pharm World Sci 20, 225–235 (1998). https://doi.org/10.1023/A:1008600603059

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  • DOI: https://doi.org/10.1023/A:1008600603059

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