Heterogeneity of the angiogenic response induced in different normal adult tissues by vascular permeability factor/vascular endothelial growth factor

Laboratory Investigation

Volumn 80, Issue 1, 2000, Pages 99-115

  Pettersson, Anna ^a   Nagy, Janice A ^a   Brown, Lawrence F ^a   Sundberg, Christian ^a   Morgan, Ellen ^a   Jungles, Steven ^a   Carter, Robert ^a   Krieger, Jose E ^a,b   Manseau, Eleanor J ^a   Harvey, V Susan ^a   Eckelhoefer, Isabelle A ^a   Feng, Dian ^a   Dvorak, Ann M ^a   Mulligan, Richard C ^a   Dvorak, Harold F ^a,c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VASCULOTROPIN;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; COLLATERAL CIRCULATION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT; TISSUE BLOOD FLOW; VASCULAR ENDOTHELIUM;

EID: 17344390961     PISSN: 00236837     EISSN: None     Source Type: Journal    
DOI: 10.1038/labinvest.3780013     Document Type: Article

References (77)

1. Aird WC, Edelberg JM, Weiler-Guettler H, Simmons WW, Smith TW, and Rosenberg RD (1997). Vascular bed-specific expression of an endothelial cell gene is programmed by the tissue microenvironment. J Cell Biol 138:1117-1124.
2. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, and Isner JM (1997). Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964-967.
3. Baumgartner I, Pieczek A, Manor O, Blair R, Kearney M, Walsh K, and Isner JM (1998). Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation 97:1114-1123.
4. Bauters C, Asahara T, Zheng LP, Takeshita S, Bunting S, Ferrara N, Symes JF, and Isner JM (1994). Physiological assessment of augmented vascularity induced by VEGF in ischemic rabbit hindlimb. Am J Physiol 267:H1263-H1271.
5. Boehm T, Folkman J, Browder T, and O'Reilly MS (1997). Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance. Nature 390:404-407.
6. Brower V (1999). Genentech enlightens other angiogenesis programs. Nat Biotechnol 17:326-327.
7. Brown L, Detmar M, Claffey K, Nagy J, Feng D, Dvorak A, and Dvorak H (1997). Vascular permeability factor/vascular endothelial growth factor: a multifunctional angiogenic cytokine. In: Goldberg I and Rosen E, editors. Regulation of angiogenesis. Basel, Switzerland: Birkhauser Verlag, 233-269.
8. Brown LF, Berse B, Jackman RW, Tognazzi K, Manseau EJ, Senger DR, and Dvorak HF (1993). Expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in adenocarcinomas of the gastrointestinal tract. Cancer Res 53:4727-4735.
9. Brown LF, Tognazzi K, Dvorak HF, and Harrist TJ (1996). Strong expression of kinase insert domain-containing receptor, a vascular permeability factor/vascular endothelial growth factor receptor in AIDS-associated Kaposi's sarcoma and cutaneous angiosarcoma. Am J Pathol 148:1065-1074.
10. Brown LF, Yeo KT, Berse B, Yeo TK, Senger DR, Dvorak HF, and van de Water L (1992). Expression of vascular permeability factor (vascular endothelial growth factor) by epidermal keratinocytes during wound healing. J Exp Med 176: 1375-1379.
11. Burri PH, and Tarek MR (1990). A novel mechanism of capillary growth in the rat pulmonary microcirculation. Anat Rec 228:35-45.
12. Buschmann I and Schaper W (1999). Arteriogenesis versus angiogenesis: two mechanisms of vessel growth. News Physiol Sci 14:121-125.
13. Chang J, Most D, Bresnick S, Mehrara B, Steinbrech DS, Reinisch J, Longaker MT, and Turk AE (1999). Proliferative hemangiomas: analysis of cytokine gene expression and angiogenesis. Plast Reconstr Surg 103:1-9; discussion 10.
14. Cohen MV (1985). Coronary collaterals: Clinical and experimental observations. Mt. Kisco, NY: Futura Publishing Company.
15. Colville-Nash PR and Willoughby DA (1997). Growth factors in angiogenesis: Current interest and therapeutic potential. Mol Med Today 3:14-23.
16. Dellian M, Witwer BP, Salehi HA, Yuan F, and Jain RK (1996). Quantitation and physiological characterization of angiogenic vessels in mice: effect of basic fibroblast growth factor, vascular endothelial growth factor/vascular permeability factor, and host microenvironment. Am J Pathol 149:59-71.
17. Desjardins M and Bendayan M (1989). Heterogenous distribution of type IV collagen, entactin, heparan sulfate proteoglycan, and laminin among renal basement membranes as demonstrated by quantitative immunocytochemistry. J Histochem Cytochem 37:885-897.
18. Detmar M, Brown LF, Claffey KP, Yeo KT, Kocher O, Jackman RW, Berse B, and Dvorak HF (1994). Overexpression of vascular permeability factor/vascular endothelial growth factor and its receptors in psoriasis. J Exp Med 180:1141-1146.
19. Drake CJ and Little CD (1995). Exogenous vascular endothelial growth factor induces malformed and hyperfused vessels during embryonic neovascularization. Proc Natl Acad Sci USA 92:7657-7661.
20. Dvorak AM, Kohn S, Morgan ES, Fox P, Nagy JA, and Dvorak HF (1996). The vesiculo-vacuolar organelle (VVO): A distinct endothelial cell structure that provides a transcellular pathway for macromolecular extravasation. J Leukoc Biol 59: 100-115.
21. Dvorak HF, Brown LF, Detmar M, and Dvorak AM (1995). Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol 146:1029-1039.
22. Dvorak HF, Nagy JA, Dvorak JT, and Dvorak AM (1988). Identification and characterization of the blood vessels of solid tumors that are leaky to circulating macromolecules. Am J Pathol 133:95-109.
23. Dvorak HF, Nagy JA, Feng D, Brown LF, and Dvorak AM (1999). Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr Top Microbiol Immunol 237:97-132.
24. Feng D, Nagy J, Dvorak A, and Dvorak H (In press, 2000). Different pathways of macromolecule extravasation from hyperpermeable tumor vessels. Microvasc Res.
25. Feng D, Nagy J, Hipp J, Dvorak H, and Dvorak A (1996). Vesiculo-vacuolar organelles and the regulation of venule permeability to macromolecules by vascular permeability factor, histamine, and serotonin. J Exp Med 183:1981-1986.
26. Feng D, Nagy J, Hipp J, Pyne K, Dvorak H, and Dvorak A (1997). Reinterpretation of endothelial cell gaps induced by vasoactive mediators in guinea-pig, mouse and rat: many are transcellular pores. J Physiol (Lond) 504:747-761.
27. Folkman J (1995). Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1:27-31.
28. Folkman J (1997). Angiogenesis and angiogenesis inhibition: An overview. EXS 79:1-8.
29. Giordano FJ, Ping P, McKirnan MD, Nozaki S, DeMaria AN, Dillmann WH, Mathieu-Costello O, and Hammond HK (1996). Intracoronary gene transfer of fibroblast growth factor-5 increases blood flow and contractile function in an ischemic region of the heart. Nat Med 2:534-539.
30. Grant DS and Kleinman HK (1997). Regulation of capillary formation by laminin and other components of the extracellular matrix. EXS 79:317-333.
31. Guzman RJ, Lemarchand P, Crystal RG, Epstein SE, and Finkel T (1993). Efficient gene transfer into myocardium by direct injection of adenovirus vectors. Circ Res 73:1202-1207.
32. Hanahan D (1998). A flanking attack on cancer. Nat Med 4:13-14.
33. Hardy S, Kitamura M, Harris-Stansil T, Dai Y, and Phipps ML (1997). Construction of adenovirus vectors through Cre-Iox recombination. J Virol 71:1842-1849.
34. Henry TD (1998). Can we really grow new blood vessels? Lancet 351:1826-1827.
35. Isner JM and Asahara T (1999). Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization. J Clin Invest 103:1231-1236.
36. Isner JM, Baumgartner I, Rauh G, Schainfeld R, Blair R, Manor O, Razvi S, and Symes JF (1998). Treatment of thromboangiitis obliterans (Buerger's disease) by intramuscular gene transfer of vascular endothelial growth factor: preliminary clinical results. J Vase Surg 28:964-73; discussion 73-75.
37. Isner JM, Pieczek A, Schainfeld R, Blair R, Haley L, Asahara T, Rosenfield K, Razvi S, Walsh K, and Symes JF (1996). Clinical evidence of angiogenesis after arterial gene transfer of phVEGF165 in patient with ischaemic limb. Lancet 348: 370-374.
38. Laham RJ, Simons M, Tofukuji M, Hung D, and Sellke FW (1998). Modulation of myocardial perfusion and vascular reactivity by pericardial basic fibroblast growth factor: Insight into ischemia-induced reduction in endothelium-dependent vasodilatation. J Thorac Cardiovasc Surg 116:1022-1028.
39. Lantos P, VandenBerg S, and Kleihues P (1997). Tumors of the nervous system. In: Graham D and Lantos P, editors. Greenfield's neuropathology. London: Arnold, 583-879.
40. Li J, Brown LF, Hibberd MG, Grossman JD, Morgan JP, and Simons M (1996). VEGF, flk-1, and flt-1 expression in a rat myocardial infarction model of angiogenesis. Am J Physiol 270:1-11803-H1811.
41. Lopez JJ, Edelman ER, Stamler A, Hibberd MG, Prasad P, Caputo RP, Carrozza JP, Douglas PS, Sellke FW, and Simons M (1997). Basic fibroblast growth factor in a porcine model of chronic myocardial ischemia: A comparison of angiographic, echocardiographic and coronary flow parameters. J Pharmacol Exp Ther 282:385-390.
42. Lopez JJ, Edelman ER, Stamler A, Hibberd MG, Prasad P, Thomas KA, DiSalvo J, Caputo RP, Carrozza JP, Douglas PS, Sellke FW, and Simons M. (1998a). Angiogenic potential of perivascularly delivered aFGF in a porcine model of chronic myocardial ischemia. Am J Physiol 274:H930-H936.
43. Lopez JJ, Laham RJ, Stamler A, Pearlman JD, Bunting S, Kaplan A, Carrozza JP, Sellke FW, and Simons M. (1998b). VEGF administration in chronic myocardial ischemia in pigs. Cardiovasc Res 40:272-281.
44. Losordo DW, Vale PR, Symes JF, Dunnington CH, Esakof DD, Maysky M, Ashare AB, Lathi K, and Isner JM (1998). Gene therapy for myocardial angiogenesis: initial clinical results with direct myocardial injection of phVEGF165 as sole therapy for myocardial ischemia. Circulation 98:2800-2804.
45. Mack CA, Magovern CJ, Budenbender KT, Patel SR, Schwarz EA, Zanzonico P, Ferris B, Sanborn T, Isom P, Isom OW, Crystal RG, and Rosengart TK (1998). Salvage angiogenesis induced by adenovirus-mediated gene transfer of vascular endothelial growth factor protects against ischemic vascular occlusion. J Vase Surg 27:699-709.
46. Magovern CJ, Mack CA, Zhang J, Rosengart TK, Isom OW, and Crystal RG (1997). Regional angiogenesis induced in nonischemic tissue by an adenoviral vector expressing vascular endothelial growth factor. Hum Gene Ther 8:215-227.
47. McKee P (1996). Pathology of the skin with clinical correlations. London: Mosby International, 16.57-16.66.
48. Mulliken J and Young A (1988). Vascular birthmarks. In: Mulliken J and Young A, editors. Hemangiomas and malformations. Philadelphia: WB Saunders.
49. Nagy J, Morgan E, Herzberg K, Manseau E, Dvorak A, and Dvorak H (1995). Pathogenesis of ascites tumor growth: Angiogenesis, vascular remodeling and stroma formation in the peritoneal lining. Cancer Res 55:376-385.
50. O'Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, and Folkman J (1997). Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88:277-285.
51. Ory DS, Neugeboren BA, and Mulligan RC (1996). A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proc Natl Acad Sci USA 93:11400-11406.
52. Paku S and Paweletz N (1991). First steps of tumor-related angiogenesis. Lab Invest 65:334-346.
53. Patan S, Haenni B, and Burri PH (1993). Evidence for intussusceptive capillary growth in the chicken chorioallantoic membrane (CAM). Anat Embryol (Berl) 187:121-130.
54. Pearlman JD, Hibberd MG, Chuang ML, Harada K, Lopez JJ, Gladstone SR, Friedman M, Sellke FW, and Simons M (1995). Magnetic resonance mapping demonstrates benefits of VEGF-induced myocardial angiogenesis. Nat Med 1:1085-1089.
55. Pepper M, Tacchini-Cottier F, Sabapathy T, Montesano R, and Wagner E (1996). Endothelial cells transformed by polyoma virus middle T oncogene: A model for hemangiomas and other vascular tumors. In: Bicknell R, Lewis C, and Ferrara N, editors. Tumor angiogenesis. Oxford: Oxford University Press.
56. Pepper MS, Ferrara N, Orci L, and Montesano R (1991). Vascular endothelial growth factor (VEGF) induces plasminogen activators and plasminogen activator inhibitor-1 in microvascular endothelial cells. Biochem Biophys Res Commun 181:902-906.
57. Plate KH, Breier G, Weich HA, and Risau W (1992). Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 359:845-848.
58. Schaper W (1991). Angiogenesis in the adult heart. Basic Res Cardiol 86:51-56.
59. Schaper W and Schaper J (1993). Collateral circulation: Heart, brain, kidney, limbs. Boston: Kluwer Academic Publishers.
60. Sellke FW, Laham RJ, Edelman ER, Pearlman JD, and Simons M. (1998a). Therapeutic angiogenesis with basic fibroblast growth factor: technique and early results. Ann Thorac Surg 65:1540-1544.
61. Sellke FW, Tofukuji M, Laham RJ, Li J, Hariawala MD, Bunting S, and Simons M. (1998b). Comparison of VEGF delivery techniques on collateral-dependent microvascular reactivity. Microvasc Res 55:175-178.
62. Senger D, Van De Water L, Brown L, Nagy J, Yeo K-T, Yeo T-K, Berse B, Jackman R, Dvorak A, and Dvorak H (1993). Vascular permeability factor (VPF, VEGF) in tumor biology. Cancer Metastasis Rev 12:303-324.
63. Skalak T, Price R, and Zeller P (1998). Where do new arterioles come from? Mechanical forces and microvessel adaptation. Microcirculation 5:91-94.
64. Springer ML, Chen AS, Kraft PE, Bednarski M, and Blau HM (1998). VEGF gene delivery to muscle: potential role for vasculogenesis in adults. Mol Cell 2:549-558.
65. Strutton G (1997). Vascular tumors, ch. 38. In: Weedon D, editor. Skin pathology. Edinburgh: Churchill Livingstone, 821-854.
66. Swayne GT and Smaje LH (1989). Dynamic compliance of single perfused frog mesenteric capillaries and rat venules: A filtration coefficient correction. Int J Microcirc Clin Exp 8:43-52.
67. Swayne GT, Smaje LH, and Bergel DH (1989). Distensibility of single capillaries and venules in the rat and frog mesentery. Int J Microcirc Clin Exp 8:25-42.
68. Takahashi K, Mulliken JB, Kozakewich HP, Rogers RA, Folkman J, and Ezekowitz RA (1994). Cellular markers that distinguish the phases of hemangioma during infancy and childhood. J Clin Invest 93:2357-2364.
69. Takeshita S, Rossow ST, Kearney M, Zheng LP, Bauters C, Bunting S, Ferrara N, Symes JF, and Isner JM (1995). Time course of increased cellular proliferation in collateral arteries after administration of vascular endothelial growth factor in a rabbit model of lower limb vascular insufficiency. Am J Pathol 147:1649-1660.
70. Takeshita S, Weir L, Chen D, Zheng LP, Riessen R, Bauters C, Symes JF, Ferrara N, and Isner JM (1996). Therapeutic angiogenesis following arterial gene transfer of vascular endothelial growth factor in a rabbit model of hindlimb ischemia. Biochem Biophys Res Commun 227:628-635.
71. Unemori EN, Ferrara N, Bauer EA, and Amento EP (1992). Vascular endothelial growth factor induces interstitial collagenase expression in human endothelial cells. J Cell Physiol 153:557-562.
72. Van Belle E, Witzenbichler B, Chen D, Silver M, Chang L, Schwall R, and Isner JM (1998). Potentiated angiogenic effect of scatter factor/hepatocyte growth factor via induction of vascular endothelial growth factor: The case for paracrine amplification of angiogenesis. Circulation 97:381-390.
73. Vikkula M, Boon LM, Carraway KL III, Calvert JT, Diamonti AJ, Goumnerov B, Pasyk KA, Marchuk DA, Warman ML, Cantley LC, Mulliken JB, and Olsen BR (1996). Vascular dysmorphogenesis caused by an activating mutation in the receptor tyrosine kinase TIE2. Cell 87:1181-1190.
74. Ware JA and Simons M (1997). Angiogenesis in ischemic heart disease. Nat Med 3:158-164.
75. Warren BA (1979). The vascular morphology of tumors. In: Peterson H-I. Tumor blood circulation: Angiogenesis, vascular morphology and blood flow of experimental and human tumors. Boca Raton, FL: CRC Press, Inc., 1-47.
76. Warren RS, Yuan H, Matli MR, Gillett NA, and Ferrara N (1995). Regulation by vascular endothelial growth factor of human colon cancer tumorigenesis in a mouse model of experimental liver metastasis. J Clin Invest 95:1789-1797.
77. Witzenbichler B, Asahara T, Murohara T, Silver M, Spyridopoulos I, Magner M, Principe N, Kearney M, Hu JS, and Isner JM (1998). Vascular endothelial growth factor-C (VEGF-C/ VEGF-2) promotes angiogenesis in the setting of tissue ischemia. Am J Pathol 153:381-394.