Regulation of vascular development by fibroblast growth factors

Cell and Tissue Research

Volumn 314, Issue 1, 2003, Pages 157-166

  Auguste, Patrick ^a   Javerzat, Sophie ^a   Bikfalvi, Andreas ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Angiogenesis; Fibroblast growth factors

Indexed keywords

FIBROBLAST GROWTH FACTOR;

ANGIOGENESIS; GENETIC ANALYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; ISCHEMIA; LYMPHATIC SYSTEM; MOLECULAR MECHANICS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; REVIEW; VASCULARIZATION;

ANIMALS; BLOOD VESSELS; FIBROBLAST GROWTH FACTORS; HUMANS; ISCHEMIA; LYMPHATIC SYSTEM; MODELS, BIOLOGICAL; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 0242573091     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-003-0750-0     Document Type: Review

References (98)

1. Arbeit JM, Olson DC, Hanahan D (1996) Upregulation of fibroblast growth factors and their receptors during multi-stage epidermal carcinogenesis in K14-HPV16 transgenic mice. Oncogene 13:1847-1857
2. Arese M, Chen Y, Florkiewicz RZ, Gualandris A, Shen B, Rifkin DB (1999) Nuclear activities of basic fibroblast growth factor: potentiation of low-serum growth mediated by natural or chimeric nuclear localization signals. Mol Biol Cell 10:1429-1444
3. Arman E, Haffner-Krausz R, Chen Y, Heath JK, Lonai P (1998) Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc Natl Acad Sci USA 95:5082-5087
4. Auguste P, Gursel DB, Lemiere S, Reimers D, Cuevas P, Carceller F, Di Santo JP, Bikfalvi A (2001) Inhibition of fibroblast growth factor/fibroblast growth factor receptor activity in glioma cells impedes tumor growth by both angiogenesis-dependent and -independent mechanisms. Cancer Res 61:1717-1726
5. Bikfalvi A, Klein S, Pintucci G, Quarto N, Mignatti P, Rifkin DB (1995) Differential modulation of cell phenotype by different molecular weight forms of basic fibroblast growth factor: possible intracellular signaling by the high molecular weight forms. J Cell Biol 129:233-243
6. Bikfalvi A, Klein S, Pintucci G, Rifkin DB (1997) Biological roles of fibroblast growth factor-2. Endocr Rev 18:26-45
7. Billottet C, Janji B, Thiery JP, Jouanneau J (2002) Rapid tumor development and potent vascularization are independent events in carcinoma producing FGF-1 or FGF-2. Oncogene 21:8128-8139
8. Bliznakov EG (2002) Therapeutic angiogenesis: hope or hype. Circulation 106:e220-e221
9. Bossard C, Laurell H, Van Den Berghe L, Meunier S, Zanibellato C, Prats H (2003) Translokin is an intracellular mediator of FGF-2 trafficking. Nat Cell Biol 5:433-439
10. Cao R, Brakenhielm E, Pawliuk R, Wariaro D, Post MJ, Wahlberg E, Leboulch P, Cao Y (2003) Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2. Nat Med 31:31
11. Carmeliet P (2000) Mechanisms of angiogenesis and arteriogenesis. Nat Med 6:389-395
12. Compagni A, Wilgenbus P, Impagnatiello MA, Cotten M, Christofori G (2000) Fibroblast growth factors are required for efficient tumor angiogenesis. Cancer Res 60:7163-7169
13. Cross MJ, Claesson-Welsh L (2001) FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol Sci 22:201-207
14. Deng CX, Wynshaw-Boris A, Shen MM, Daugherty C, Ornitz DM, Leder P (1994) Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev 8:3045-3057
15. Facchiano A, Russo K, Facchiano AM, De Marchis F, Facchiano F, Ribatti D, Aguzzi MS, Capogrossi MC (2003) Identification of a novel domain of fibroblast growth factor 2 controlling its angiogenic properties. J Biol Chem 278:8751-8760
16. Feraud O, Cao Y, Vittet D (2001) Embryonic stem cell-derived embryoid bodies development in collagen gels recapitulates sprouting angiogenesis. Lab Invest 81:1669-1681
17. Fernandez B, Buehler A, Wolfram S, Kostin S, Espanion G, Franz WM, Niemann H, Doevendans PA, Schaper W, Zimmermann R (2000) Transgenic myocardial overexpression of fibroblast growth factor-1 increases coronary artery density and branching. Circ Res 87:207-213
18. Flamme I, Risau W (1992) Induction of vasculogenesis and hematopoiesis in vitro. Development 116:435-439
19. +-ATPase. J Biol Chem 273:544-551
20. Fulgham DL, Widhalm SR, Martin S, Coffin JD (1999) FGF-2 dependent angiogenesis is a latent phenotype in basic fibroblast growth factor transgenic mice. Endothelium 6:185-195
21. Giavazzi R, Giuliani R, Coltrini D, Bani MR, Ferri C, Sennino B, Tosatti MP, Stoppacciaro A, Presta M (2001) Modulation of tumor angiogenesis by conditional expression of fibroblast growth factor-2 affects early but not established tumors. Cancer Res 61:309-317
22. Grines CL, Watkins MW, Helmer G, Penny W, Brinker J, Marmur JD, West A, Rade JJ, Marrott P, Hammond HK, Engler RL (2002) Angiogenic gene therapy (AGENT) trial in patients with stable angina pectoris. Circulation 105:1291-1297
23. Holash J, Maisonpierre PC, Compton D, Boland P, Alexander CR, Zagzag D, Yancopoulos GD, Wiegand SJ (1999) Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science 284:1994-1998
24. Horowitz A, Tkachenko E, Simons M (2002) Fibroblast growth factor-specific modulation of cellular response by syndecan-4. J Cell Biol 157:715-725
25. Horvath KA, Doukas J, Lu CY, Belkind N, Greene R, Pierce GF, Fullerton DA (2002) Myocardial functional recovery after fibroblast growth factor 2 gene therapy as assessed by echocardiography and magnetic resonance imaging. Ann Thorac Surg 74:481-486
26. Huss WJ, Hanrahan CF, Barrios RJ, Simons JW, Greenberg NM (2001) Angiogenesis and prostate cancer: identification of a molecular progression switch. Cancer Res 61:2736-2743
27. Huss WJ, Barrios RJ, Foster BA, Greenberg NM (2003) Differential expression of specific FGF ligand and receptor isoforms during angiogenesis associated with prostate cancer progression. Prostate 54:8-16
28. Impagnatiello MA, Weitzer S, Gannon G, Compagni A, Cotten M, Christofori G (2001) Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. J Cell Biol 152:1087-1098
29. Jarecki J, Johnson E, Krasnow MA (1999) Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF. Cell 99:211-220
30. Javerzat S, Auguste P, Bikfalvi A (2002) The role of fibroblast growth factors in vascular development. Trends Mol Med 8:483-489
31. Jouanneau J, Plouet J, Moens G, Thiery JP (1997) FGF-2 and FGF-1 expressed in rat bladder carcinoma cells have similar angiogenic potential but different tumorigenic properties in vivo. Oncogene 14:671-676
32. Kanda S, Lerner EC, Tsuda S, Shono T, Kanetake H, Smithgall TE (2000) The nonreceptor protein-tyrosine kinase c-Fes is involved in fibroblast growth factor-2-induced chemotaxis of murine brain capillary endothelial cells. J Biol Chem 275:10105-10111
33. Kandel J, Bossy-Wetzel E, Radvanyi F, Klagsbrun M, Folkman J, Hanahan D (1991) Neovascularization is associated with a switch to the export of bFGF in the multistep development of fibrosarcoma. Cell 66:1095-1104
34. Kovalenko D, Yang X, Nadeau RJ, Harkins LK, Friesel R (2003) Sef inhibits fibroblast growth factor signaling by inhibiting FGFR1 tyrosine phosphorylation and subsequent ERK activation. J Biol Chem 24:24
35. Kubo H, Cao R, Brakenhielm E, Makinen T, Cao Y, Alitalo K (2002) Blockade of vascular endothelial growth factor receptor-3 signaling inhibits fibroblast growth factor-2-induced lymphangiogenesis in mouse cornea. Proc Natl Acad Sci USA 17:17
36. Kwan CP, Venkataraman G, Shriver Z, Raman R, Liu D, Qi Y, Varticovski L, Sasisekharan R (2001) Probing fibroblast growth factor dimerization and role of heparin-like glycosaminoglycans in modulating dimerization and signaling. J Biol Chem 276:23421-23429
37. Laham RJ, Chronos NA, Pike M, Leimbach ME, Udelson JE, Pearlman JD, Pettigrew RI, Whitehouse MJ, Yoshizawa C, Simons M (2000) Intracoronary basic fibroblast growth factor (FGF-2) in patients with severe ischemic heart disease:results of a phase I open-label dose escalation study. J Am Coll Cardiol 36:2132-2139
38. Landriscina M, Bagala C, Mandinova A, Soldi R, Micucci I, Bellum S, Prudovsky I, Maciag T (2001) Copper induces the assembly of a multiprotein aggregate implicated in the release of fibroblast growth factor 1 in response to stress. J Biol Chem 276:25549-25557
39. LaVallee TM, Prudovsky IA, McMahon GA, Hu X, Maciag T (1998) Activation of the MAP kinase pathway by FGF-1 correlates with cell proliferation induction while activation of the Src pathway correlates with migration. J Cell Biol 141:1647-1658
40. Lazarous DF, Scheinowitz M, Shou M, Hodge E, Rajanayagam S, Hunsberger S, Robison WG Jr, Stiber JA, Correa R, Epstein SE, et al (1995) Effects of chronic systemic administration of basic fibroblast growth factor on collateral development in the canine heart. Circulation 91:145-153
41. Lazarous DF, Shou M, Scheinowitz M, Hodge E, Thirumurti V, Kitsiou AN, Stiber JA, Lobo AD, Hunsberger S, Guetta E, et al (1996) Comparative effects of basic fibroblast growth factor and vascular endothelial growth factor on coronary collateral development and the arterial response to injury. Circulation 94:1074-1082
42. Lazarous DF, Shou M, Stiber JA, Dadhania DM, Thirumurti V, Hodge E, Unger EF (1997) Pharmacodynamics of basic fibroblast growth factor: route of administration determines myocardial and systemic distribution. Cardiovasc Res 36:78-85
43. Lazarous DF, Unger EF, Epstein SE, Stine A, Arevalo JL, Chew EY, Quyyumi AA (2000) Basic fibroblast growth factor in patients with intermittent claudication: results of a phase I trial. J Am Coll Cardiol 36:1239-1244
44. Lederman RJ, Mendelsohn FO, Anderson RD, Saucedo JF, Tenaglia AN, Hermiller JB, Hillegass WB, Rocha-Singh K, Moon TE, Whitehouse MJ, Annex BH (2002) Therapeutic angiogenesis with recombinant fibroblast growth factor-2 for intermittent claudication (the TRAFFIC study): a randomised trial. Lancet 359:2053-2058
45. Lee SH, Schloss DJ, Jarvis L, Krasnow MA, Swain JL (2000a) Inhibition of angiogenesis by a mouse sprouty protein. J Biol Chem 26:26
46. Lee SH, Schloss DJ, Swain JL (2000b) Maintenance of vascular integrity in the embryo requires signaling through the fibroblast growth factor receptor. J Biol Chem 275:33679-33687
47. Li J, Shworak NW, Simons M (2002) Increased responsiveness of hypoxic endothelial cells to FGF2 is mediated by HIF-1alpha-dependent regulation of enzymes involved in synthesis of heparan sulfate FGF2-binding sites. J Cell Sci 115:1951-1959
48. Lin Q, Schwarz J, Bucana C, Olson EN (1997) Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276:1404-1407
49. Lin Q, Lu J, Yanagisawa H, Webb R, Lyons GE, Richardson JA, Olson EN (1998) Requirement of the MADS-box transcription factor MEF2C for vascular development. Development 125:4565-4574
50. Lu L, Holmqvist K, Cross M, Welsh M (2002) Role of the Src homology 2 domain containing protein Shb in murine brain endothelial cell proliferation and differentiation. Cell Growth Differ 13:141-148
51. Mailhos C, Modlich U, Lewis J, Harris A, Bicknell R, Ish-Horowicz D (2001) Delta4, an endothelial specific notch ligand expressed at sites of physiological and tumor angiogenesis. Differentiation 69:135-144
52. Matsumoto T, Turesson I, Book M, Gerwins P, Claesson-Welsh L (2002) p38 MAP kinase negatively regulates endothelial cell survival, proliferation, and differentiation in FGF-2-stimulated angiogenesis. J Cell Biol 156:149-160
53. Miller DL, Ortega S, Bashayan O, Basch R, Basilico C (2000) Compensation by fibroblast growth factor 1 (FGF1) does not account for the mild phenotypic defects observed in FGF2 null mice. Mol Cell Biol 20:2260-2268
54. Nakamura T, Mochizuki Y, Kanetake H, Kanda S (2001) Signals via FGF receptor 2 regulate migration of endothelial cells. Biochem Biophys Res Commun 289:801-806
55. Nguyen M, Watanabe H, Budson AE, Richie JP, Folkman J (1993) Elevated levels of the angiogenic peptide basic fibroblast growth factor in urine of bladder cancer patients. J Natl Cancer Inst 85:241-242
56. Nguyen M, Watanabe H, Budson AE, Richie JP, Hayes DF, Folkman J (1994) Elevated levels of an angiogenic peptide, basic fibroblast growth factor, in the urine of patients with a wide spectrum of cancers. J Natl Cancer Inst 86:356-361
57. Ogawa T, Takayama K, Takakura N, Kitano S, Ueno H (2002) Anti-tumor angiogenesis therapy using soluble receptors:enhanced inhibition of tumor growth when soluble fibroblast growth factor receptor-1 is used with soluble vascular endothelial growth factor receptor. Cancer Gene Ther 9:633-640
58. Ong SH, Hadari YR, Gotoh N, Guy GR, Schlessinger J, Lax I (2001) Stimulation of phosphatidylinositol 3-kinase by fibroblast growth factor receptors is mediated by coordinated recruitment of multiple docking proteins. Proc Natl Acad Sci USA 98:6074-6079
59. Ornitz DM, Itoh N (2001) Fibroblast growth factors. Genome Biol 2:3005
60. Ortega S, Ittmann M, Tsang SH, Ehrlich M, Basilico C (1998) Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc Natl Acad Sci USA 95:5672-5677
61. Pecher P, Schumacher BA (2000) Angiogenesis in ischemic human myocardium: clinical results after 3 years. Ann Thorac Surg 69:1414-1419
62. Pepper MS, Ferrara N, Orci L, Montesano R (1992) Potent synergism between vascular endothelial growth factor and basic fibroblast growth factor in the induction of angiogenesis in vitro. Biochem Biophys Res Commun 189:824-831
63. Peters K, Werner S, Liao X, Wert S, Whitsett J, Williams L (1994) Targeted expression of a dominant negative FGF receptor blocks branching morphogenesis and epithelial differentiation of the mouse lung. EMBO J 13:3296-3301
64. Pintucci G, Moscatelli D, Saponara F, Biernacki PR, Baumann FG, Bizekis C, Galloway AC, Basilico C, Mignatti P (2002) Lack of ERK activation and cell migration in FGF-2-deficient endothelial cells. FASEB J 25:25-29
65. Poole TJ, Finkelstein EB, Cox CM (2001) The role of FGF and VEGF in angioblast induction and migration during vascular development. Dev Dyn 220:1-17
66. Pourtier-Manzanedo A, Vercamer C, Van Belle E, Mattot V, Mouquet F, Vandenbunder B (2003) Expression of an Ets-1 dominant-negative mutant perturbs normal and tumor angiogenesis in a mouse ear model. Oncogene 22:1795-1806
67. Qiao J, Bush KT, Steer DL, Stuart RO, Sakurai H, Wachsman W, Nigam SK (2001) Multiple fibroblast growth factors support growth of the ureteric bud but have different effects on branching morphogenesis. Mech Dev 109:123-135
68. Rajanayagam MA, Shou M, Thirumurti V, Lazarous DF, Quyyumi AA, Goncalves L, Stiber J, Epstein SE, Unger EF (2000) Intracoronary basic fibroblast growth factor enhances myocardial collateral perfusion in dogs. J Am Coll Cardiol 35:519-526
69. Rinsch C, Quinodoz P, Pittet B, Alizadeh N, Baetens D, Montandon D, Aebischer P, Pepper MS (2001) Delivery of FGF-2 but not VEGF by encapsulated genetically engineered myoblasts improves survival and vascularization in a model of acute skin flap ischemia. Gene Ther 8:523-533
70. Rissanen TT, Markkanen JE, Arve K, Rutanen J, Kettunen MI, Vajanto I, Jauhiainen S, Cashion L, Gruchala M, Narvanen O, et al (2003) Fibroblast growth factor 4 induces vascular permeability, angiogenesis and arteriogenesis in a rabbit hindlimb ischemia model. FASEB J 17:100-102
71. Rofstad EK, Halsor EF (2000) Vascular endothelial growth factor, interleukin 8, platelet derived endothelial cell growth factor, and basic fibroblast growth factor promote angiogenesis and metastasis in human melanoma xenografts. Cancer Res 60:4932-4938
72. Rousseau B, Dubayle D, Sennlaub F, Jeanny JC, Costet P, Bikfalvi A, Javerzat S (2000) Neural and angiogenic defects in eyes of transgenic mice expressing a dominant-negative FGF receptor in the pigmented cells. Exp Eye Res 71:395-404
73. Rousseau B, Larrieu-Lahargue F, Bikfalvi A, Javerzat S (2003) Involvement of fibroblast growth factors in choroidal angiogenesis and retinal vascularization. Exp Eye Res (in press)
74. Ruel M, Laham RJ, Parker JA, Post MJ, Ware JA, Simons M, Sellke FW (2002) Longterm effects of surgical angiogenic therapy with fibroblast growth factor 2 protein. J Thorac Cardiovasc Surg 124:28-34
75. Rusnati M, Urbinati C, Tanghetti E, Dell'Era P, Lortat-Jacob H, Presta M (2002) Cell membrane GM1 ganglioside is a functional coreceptor for fibroblast growth factor 2. Proc Natl Acad Sci USA 99:4367-4372
76. Sato K, Laham RJ, Pearlman JD, Novicki D, Sellke FW, Simons M, Post MJ (2000) Efficacy of intracoronary versus intravenous FGF-2 in a pig model of chronic myocardial ischemia. Ann Thorac Surg 70:2113-2118
77. Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova AV, Yeh BK, Yayon A, Linhardt RJ, Mohammadi M (2000) Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol Cell 6:743-750
78. Seghezzi G, Patel S, Ren CJ, Gualandris A, Pintucci G, Robbins ES, Shapiro RL, Galloway AC, Rifkin DB, Mignatti P (1998) Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J Cell Biol 141:1659-1673
79. Sheikh F, Sontag DP, Fandrich RR, Kardami E, Cattini PA (2001) Overexpression of FGF-2 increases cardiac myocyte viability after injury in isolated mouse hearts. Am J Physiol Heart Circ Physiol 280:H1039-H1050
80. Simons M, Annex BH, Laham RJ, Kleiman N, Henry T, Dauerman H, Udelson JE, Gervino EV, Pike M, Whitehouse MJ, et al (2002) Pharmacological treatment of coronary artery disease with recombinant fibroblast growth factor-2:double- blind, randomized, controlled clinical trial. Circulation 105:788-793
81. Skjerpen CS, Wesche J, Olsnes S (2002) Identification of ribosome-binding protein p34 as an intracellular protein that binds acidic fibroblast growth factor. J Biol Chem 277:23864-23871
82. Stan AC, Nemati MN, Pietsch T, Walter GF, Dietz H (1995) In vivo inhibition of angiogenesis and growth of the human U-87 malignant glial tumor by treatment with an antibody against basic fibroblast growth factor. J Neurosurg 82:1044-1052
83. Sullivan CJ, Doetschman T, Hoying JB (2002) Targeted disruption of the Fgf2 gene does not affect vascular growth in the mouse ischemic hindlimb. J Appl Physiol 93:2009-2017
84. Tabata H, Silver M, Isner JM (1997) Arterial gene transfer of acidic fibroblast growth factor for therapeutic angiogenesis in vivo:critical role of secretion signal in use of naked DNA. Cardiovasc Res 35:470-479
85. Tomanek RJ, Sandra A, Zheng W, Brock T, Bjercke RJ, Holifield JS (2001) Vascular endothelial growth factor and basic fibroblast growth factor differentially modulate early postnatal coronary angiogenesis. Circ Res 88:1135-1141
86. Tsuda S, Ohtsuru A, Yamashita S, Kanetake H, Kanda S (2002) Role of c-Fyn in FGF-2-mediated tube-like structure formation by murine brain capillary endothelial cells. Biochem Biophys Res Commun 290:1354-1360
87. Udelson JE, Dilsizian V, Laham RJ, Chronos N, Vansant J, Blais M, Galt JR, Pike M, Yoshizawa C, Simons M (2000) Therapeutic angiogenesis with recombinant fibroblast growth factor-2 improves stress and rest myocardial perfusion abnormalities in patients with severe symptomatic chronic coronary artery disease. Circulation 102:1605-1610
88. Van den Berghe L, Laurell H, Huez I, Zanibellato C, Prats H, Bugler B (2000) FIF [fibroblast growth factor-2 (FGF-2)-interacting-factor], a nuclear putatively antiapoptotic factor, interacts specifically with FGF-2. Mol Endocrinol 14:1709-1724
89. Wang Y, Becker D (1997) Antisense targeting of basic fibroblast growth factor and fibroblast growth factor receptor-1 in human melanomas blocks intratumoral angiogenesis and tumor growth. Nat Med 3:887-893
90. Wu LW, Mayo LD, Dunbar JD, Kessler KM, Baerwald MR, Jaffe EA, Wang D, Warren RS, Donner DB (2000) Utilization of distinct signaling pathways by receptors for vascular endothelial cell growth factor and other mitogens in the induction of endothelial cell proliferation. J Biol Chem 275:5096-5103
91. Yamada H, Yamada E, Kwak N, Ando A, Suzuki A, Esumi N, Zack DJ, Campochiaro PA (2000) Cell injury unmasks a latent proangiogenic phenotype in mice with increased expression of FGF2 in the retina. J Cell Physiol 185:135-142
92. Yamamoto M, Sakakibara Y, Nishimura K, Komeda M, Tabata Y (2003) Improved therapeutic efficacy in cardiomyocyte transplantation for myocardial infarction with release system of basic fibroblast growth factor. Artif Organs 27:181-184
93. Yanagisawa-Miwa A, Uchida Y, Nakamura F, Tomaru T, Kido H, Kamijo T, Sugimoto T, Kaji K, Utsuyama M, Kurashima C, et al (1992) Salvage of infarcted myocardium by angiogenic action of basic fibroblast growth factor. Science 257:1401-1403
94. Yang HT, Feng Y (2000) bFGF increases collateral blood flow in aged rats with femoral artery ligation. Am J Physiol Heart Circ Physiol 278:H85-H93
95. Yang HT, Yan Z, Abraham JA, Terjung RL (2001) VEGF(121)-and bFGF-induced increase in collateral blood flow requires normal nitric oxide production. Am J Physiol Heart Circ Physiol 280:H1097-H1104
96. Zagzag D, Amirnovin R, Greco MA, Yee H, Holash J, Wiegand SJ, Zabski S, Yancopoulos GD, Grumet M (2000) Vascular apoptosis and involution in gliomas precede neovascularization:a novel concept for glioma growth and angiogenesis. Lab Invest 80:837-849
97. Zhan X, Plourde C, Hu X, Friesel R, Maciag T (1994) Association of fibroblast growth factor receptor-1 with c-Src correlates with association between c-Src and cortactin. J Biol Chem 269:20221-20224
98. Zhang Z, Coomans C, David G (2001) Membrane heparan sulfate proteoglycan supported FGF2-FGFR1 signaling:evidence in support of the "cooperative end structures" model. J Biol Chem 276:41921-41929