Non-canonical fibroblast growth factor signalling in angiogenesis

Cardiovascular Research

Volumn 78, Issue 2, 2008, Pages 223-231

  Murakami, Masahiro ^a   Elfenbein, Arye ^a   Simons, Michael ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Angiogenesis; Cadherins; FGF; Growth factors; NCAM; Signal transduction; Syndecan 4

Indexed keywords

CADHERIN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; GANGLIOSIDE; GROWTH FACTOR; NERVE CELL ADHESION MOLECULE; PROTEIN KINASE C ALPHA; SYNDECAN 4; TYROSINE KINASE RECEPTOR;

ANGIOGENESIS; BINDING AFFINITY; CELL FUNCTION; CELL MEMBRANE; CELL SURFACE; COMPLEX FORMATION; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; GENETIC VARIABILITY; HUMAN; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ENDOTHELIAL CELLS; FIBROBLAST GROWTH FACTORS; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 42349102942     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvm086     Document Type: Review

References (96)

1. Powers CJ, McLeskey SW, Wellstein A. Fibroblast growth factors, their receptors and signaling. Endocr Relat Cancer 2000;7:165-197.
2. Ornitz DM, Itoh N. Fibroblast growth factors. Genome Biol 2001;2:REVIEWS3005.
3. Antoine M, Wirz W, Tag CG, Mavituna M, Emans N, Korff Tet al. Expression pattern of fibroblast growth factors (FGFs), their receptors and antagonists in primary endothelial cells and vascular smooth muscle cells. Growth factors (Chur, Switzerland) 2005;23:87-95.
4. Karsan A, Yee E, Poirier GG, Zhou P, Craig R, Harlan JM. Fibroblast growth factor-2 inhibits endothelial cell apoptosis by Bcl-2-dependent and independent mechanisms. Am J Pathol 1997;151:1775-1784.
5. Matsumoto T, Turesson I, Book M, Gerwins P, Claesson-Welsh L. p38 MAP kinase negatively regulates endothelial cell survival, proliferation, and differentiation in FGF-2-stimulated angiogenesis. J Cell Biol 2002;156:149-160.
6. Dailey L, Ambrosetti D, Mansukhani A, Basilico C. Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev 2005;16:233-247.
7. Ortega S, Ittmann M, Tsang SH, Ehrlich M, Basilico C. Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc Natl Acad Sci USA 1998;95:5672-5677.
8. Miller DL, Ortega S, Bashayan O, Basch R, Basilico C. Compensation by fibroblast growth factor 1 (FGF1) does not account for the mild phenotypic defects observed in FGF2 null mice. Mol Cell Biol 2000;20:2260- 2268.
9. Eswarakumar VP, Lax I, Schlessinger J. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 2005;16:139- 149.
10. Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F et al. Receptor speci.city of the fibroblast growth factor family. J Biol Chem 1996;271:15292-15297.
11. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, Ornitz DM. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 2006;281:15694-15700.
12. Nourse MB, Rolle MW, Pabon LM, Murry CE. Selective control of endothelial cell proliferation with a synthetic dimerizer of FGF receptor-1. Lab Invest 2007;87:828-835.
13. Nakamura T, Mochizuki Y, Kanetake H, Kanda S. Signals via FGF receptor 2 regulate migration of endothelial cells. Biochem Biophys Res Commun 2001;289:801-806.
14. Johnson GL, Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 2002;298:1911-1912.
15. Cross MJ, Lu L, Magnusson P, Nyqvist D, Holmqvist K, Welsh M et al. The Shb adaptor protein binds to tyrosine 766 in the FGFR-1 and regulates the Ras/MEK/MAPK pathway via FRS2 phosphorylation in endothelial cells. Mol Biol Cell 2002;13:2881-2893.
16. McLaughlin AP, De Vries GW. Role of PLCgamma and Ca(2+) in VEGF- and FGF-induced choroidal endothelial cell proliferation. Am J Physiol 2001;281:C1448-C1456.
17. Partovian C, Simons M. Regulation of protein kinase B/Akt activity and Ser473 phosphorylation by protein kinase Calpha in endothelial cells. Cell signal 2004;16:951-957.
18. Lamothe B, Yamada M, Schaeper U, Birchmeier W, Lax I, Schlessinger J. The docking protein Gab1 is an essential component of an indirect mechanism for fibroblast growth factor stimulation of the phosphatidylinositol 3-kinase/Akt antiapoptotic pathway. Mol Cell Biol 2004;24:5657-5666.
19. LaVallee TM, Prudovsky IA, McMahon GA, Hu X, Maciag T. 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 1998;141:1647-1658.
20. Tsang M, Dawid IB. Promotion and attenuation of FGF signaling through the Ras-MAPK pathway. Sci STKE 2004;2004:pe17.
21. Thisse B, Thisse C. Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev Biol 2005;287:390- 402.
22. Impagnatiello MA, Weitzer S, Gannon G, Compagni A, Cotten M, Christofori G. Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. J Cell Biol 2001;152:1087-1098.
23. Lax I, Wong A, Lamothe B, Lee A, Frost A, Hawes J et al. The docking protein FRS2alpha controls a MAP kinase-mediated negative feedback mechanism for signaling by FGF receptors. Mol Cell 2002;10:709- 719.
24. Wang S, Ai X, Freeman S, Pownall M, Lu Q, Kessler D et al. QSulf1, a heparan sulfate 6-O-endosulfatase, inhibits fibroblast growth factor signaling in mesoderm induction and angiogenesis. Proc Natl Acad Sci USA 2004;101:4833-4838.
25. Lindahl U. Heparan sulfate-protein interactions - a concept for drug design? Thromb Haemost 2007;98:109-115.
26. Steinfeld R, Van Den Berghe H, David G. Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J Cell Biol 1996;133:405-416.
27. Kan M, Wang F, Xu J, Crabb J, Hou J, McKeehan W. An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science 1993;259:1918-1921.
28. Kato M, Wang H, Kainulainen V, Fitzgerald M, Ledbetter S, Ornitz D et al. Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat Med 1998;4:691-697.
29. Faham S, Hileman R, Fromm J, Linhardt R, Rees D. Heparin structure and interactions with basic fibroblast growth factor. Science 1996;271:1116-1120.
30. Ornitz DM, Leder P. Ligand specificity and heparin dependence of fibroblast growth factor receptors 1 and 3. J Biol Chem 1992;267:16305-16311.
31. Spivak-Kroizman T, Lemmon M, Dikic I, Ladbury J, Pinchasi D, Huang J et al. Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation. Cell 1994;79:1015-1024.
32. Jastrebova N, Vanwildemeersch M, Rapraeger A, Giménez-Gallego G, Lindahl U, Spillmann D. Heparan sulfate-related oligosaccharides in ternary complex formation with fibroblast growth factors 1 and 2 and their receptors. J Biol Chem 2006;281:26884-26892.
33. Zimmermann P, David G. The syndecans, tuners of transmembrane signaling. FASEB J 1999;13(suppl.):S91-S100.
34. Volk R, Schwartz J, Li J, Rosenberg R, Simons M. The role of syndecan cytoplasmic domain in basic fibroblast growth factor-dependent signal transduction. J Biol Chem 1999;274:24417-24424.
35. Horowitz A, Tkachenko E, Simons M. Fibroblast growth factor-specific modulation of cellular response by syndecan-4. J Cell Biol 2002;157:715-725.
36. Tkachenko E, Rhodes J, Simons M. Syndecans: new kids on the signaling block. Circ Res 2005;96:488-500.
37. Tkachenko E, Elfenbein A, Tirziu D, Simons M. Syndecan-4 clustering induces cell migration in a PDZ-dependent manner. Circ Res 2006;98:1398-1404.
38. Bass M, Roach K, Morgan M, Mostafavi-Pour Z, Schoen T, Muramatsu T et al. Syndecan-4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix. J Cell Biol 2007;177:527- 538.
39. Saoncella S, Calautti E, Neveu W, Goetinck P. Syndecan-4 regulates ATF-2 transcriptional activity in a Rac1-dependent manner. J Biol Chem 2004;279:47172-47176.
40. Chittenden T, Claes F, Lanahan A, Autiero M, Palac R, Tkachenko E et al. Selective regulation of arterial branching morphogenesis by synectin. Dev Cell 2006;10:783-795.
41. Keum E, Kim Y, Kim J, Kwon S, Lim Y, Han I et al. Syndecan-4 regulates localization, activity and stability of protein kinase C-alpha. Biochem J 2004;378:1007-1014.
42. Horowitz A, Murakami M, Gao Y, Simons M. Phosphatidylinositol-4,5- bisphosphate mediates the interaction of syndecan-4 with protein kinase C. Biochemistry 1999;38:15871-15877.
43. Murakami M, Horowitz A, Tang S, Ware JA, Simons M. Protein kinase C (PKC) delta regulates PKCalpha activity in a Syndecan-4-dependent manner. J Biol Chem 2002;277:20367-20371.
44. Partovian C, Zhuang Z, Moodie K, Lin M, Ouchi N, Sessa WC et al. PKCalpha activates eNOS and increases arterial blood flow in vivo. Circ Res 2005;97:482-487.
45. Sperinde GV, Nugent MA. Mechanisms of fibroblast growth factor 2 intracellular processing: a kinetic analysis of the role of heparan sulfate proteoglycans. Biochemistry 2000;39:3788-3796.
46. Tkachenko E, Lutgens E, Stan R, Simons M. Fibroblast growth factor 2 endocytosis in endothelial cells proceed via syndecan-4-dependent activation of Rac1 and a Cdc42-dependent macropinocytic pathway. J Cell Sci 2004;117:3189-3199.
47. Cizmeci-Smith G, Langan E, Youkey J, Showalter L, Carey D. Syndecan-4 is a primary-response gene induced by basic fibroblast growth factor and arterial injury in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 1997;17:172-180.
48. Song SJ, Cool SM, Nurcombe V. Regulated expression of syndecan-4 in rat calvaria osteoblasts induced by fibroblast growth factor-2. J Cell Biochem 2007;100:402-411.
49. Reiland J, Rapraeger A. Heparan sulfate proteoglycan and FGF receptor target basic FGF to different intracellular destinations. J Cell Sci 1993;105:1085-1093.
50. Stachowiak M, Fang X, Myers J, Dunham S, Berezney R, Maher P et al. Integrative nuclear FGFR1 signaling (INFS) as a part of a universal 'feed-forward-and-gate' signaling module that controls cell growth and differentiation. J Cell Biochem 2003;90:662-691.
51. Bossard C, Laurell H, Van den Berghe L, Meunier S, Zanibellato C, Prats H. Translokin is an intracellular mediator of FGF-2 trafficking. Nat Cell Biol 2003;5:433-439.
52. Lad Y, Harburger D, Calderwood D. Integrin cytoskeletal interactions. Meth Enzymol 2007;426:69-84.
53. Klein S, Bikfalvi A, Birkenmeier T, Giancotti F, Rifkin D. Integrin regulation by endogenous expression of 18-kDa fibroblast growth factor-2. J Biol Chem 1996;271:22583-22590.
54. Rusnati M, Tanghetti E, Dell'Era P, Gualandris A, Presta M. Alphavbeta3 integrin mediates the cell-adhesive capacity and biological activity of basic fibroblast growth factor (FGF-2) in cultured endothelial cells. Mol Biol Cell 1997;8:2449-2461.
55. Cai W, Chen X. Anti-angiogenic cancer therapy based on integrin alphavbeta3 antagonism. Anti-canc Agents Med Chem 2006;6:407-428.
56. Schneller M, Vuori K, Ruoslahti E. Alphavbeta3 integrin associates with activated insulin and PDGFbeta receptors and potentiates the biological activity of PDGF. EMBO J 1997;16:5600-5607.
57. Tanghetti E, Ria R, Dell'Era P, Urbinati C, Rusnati M, Ennas M et al. Biological activity of substrate-bound basic fibroblast growth factor (FGF2): recruitment of FGF receptor-1 in endothelial cell adhesion contacts. Oncogene 2002;21:3889-3897.
58. Saoncella S, Echtermeyer F, Denhez F, Nowlen J, Mosher D, Robinson S et al. Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc Natl Acad Sci USA 1999;96:2805-2810.
59. McQuade K, Beauvais D, Burbach B, Rapraeger A. Syndecan-1 regulates alphavbeta5 integrin activity in B82L fibroblasts. J Cell Sci 2006;119:2445-2456.
60. Hinsby AM, Berezin V, Bock E. Molecular mechanisms of NCAM function. Front Biosci 2004;9:2227-2244.
61. Maness PF, Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 2007;10:19-26.
62. Beggs HE, Baragona SC, Hemperly JJ, Maness PF. NCAM140 interacts with the focal adhesion kinase p125(fak) and the SRC-related tyrosine kinase p59(fyn). J Biol Chem 1997;272:8310-8319.
63. Schmid RS, Graff RD, Schaller MD, Chen S, Schachner M, Hemperly JJ et al. NCAM stimulates the Ras-MAPK pathway and CREB phosphorylation in neuronal cells. J Neurobiol 1999;38:542-558.
64. Doherty P, Williams G, Williams EJ. CAMs and axonal growth: a critical evaluation of the role of calcium and the MAPK cascade. Mol Cell Neurosci 2000;16:283-295.
65. Kiselyov VV, Soroka V, Berezin V, Bock E. Structural biology of NCAM homophilic binding and activation of FGFR. J Neurochem 2005;94:1169-1179.
66. Kiselyov VV, Skladchikova G, Hinsby AM, Jensen PH, Kulahin N, Soroka V et al. Structural basis for a direct interaction between FGFR1 and NCAM and evidence for a regulatory role of ATP. Structure 2003;11:691- 701.
67. Byeon MK, Sugi Y, Markwald RR, Hoffman S. NCAM polypeptides in heart development: association with Z discs of forms that contain the muscle-specific domain. J Cell Biol 1995;128:209-221.
68. Langley OK, Aletsee-Ufrecht MC, Grant NJ, Gratzl M. Expression of the neural cell adhesion molecule NCAM in endocrine cells. J Histochem Cytochem 1989;37:781-791.
69. Sanes JR, Schachner M, Covault J. Expression of several adhesive macromolecules (N-CAM, L1, J1, NILE, uvomorulin, laminin, fibronectin, and a heparan sulfate proteoglycan) in embryonic, adult, and denervated adult skeletal muscle. J Cell Biol 1986;102:420-431.
70. Maier CE, Watanabe M, Singer M, McQuarrie IG, Sunshine J, Rutishauser U. Expression and function of neural cell adhesion molecule during limb regeneration. Proc Natl Acad Sci USA 1986;83:8395-8399.
71. Zeromski J, Nyczak E, Dyszkiewicz W. Signi.cance of cell adhesion molecules, CD56/NCAM in particular, in human tumor growth and spreading. Folia Histochem Cytobiol 2001;39(Suppl. 2):36-37.
72. Mizutani H, Roswit W, Hemperly J, Lawley T, Compton C, Swerlick R et al. Human dermal microvascular endothelial cells express the 140-kD isoform of neural cell adhesion molecule. Biochem Biophys Res Commun 1994;203:686-693.
73. Foets BJ, van den Oord JJ, Volpes R, Missotten L. In situ immunohistochemical analysis of cell adhesion molecules on human corneal endothelial cells. Br J Ophthalmol 1992;76:205-209.
74. Bussolati B, Grange C, Bruno S, Buttiglieri S, Deregibus MC, Tei L et al. Neural-cell adhesion molecule (NCAM) expression by immature and tumor-derived endothelial cells favors cell organization into capillary-like structures. Exp Cell Res 2006;312:913-924.
75. Doukas J, Blease K, Craig D, Ma C, Chandler LA, Sosnowski BA et al. Delivery of FGF genes to wound repair cells enhances arteriogenesis and myogenesis in skeletal muscle. Mol Ther 2002;5:517-527.
76. Cavallaro U, Niedermeyer J, Fuxa M, Christofori G. N-CAM modulates tumour-cell adhesion to matrix by inducing FGF-receptor signalling. Nat Cell Biol 2001;3:650-657.
77. Gumbiner BM. Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 2005;6:622-634.
78. Wheelock MJ, Johnson KR. Cadherin-mediated cellular signaling. Curr Opin Cell Biol 2003;15:509-514.
79. Dejana E. Endothelial cell-cell junctions: happy together. Nat Rev Mol Cell Biol 2004;5:261-270.
80. Cavallaro U, Liebner S, Dejana E. Endothelial cadherins and tumor angiogenesis. Exp Cell Res 2006;312:659-667.
81. Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F et al. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 1999;98:147-157.
82. Lampugnani MG, Orsenigo F, Gagliani MC, Tacchetti C, Dejana E. Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. J Cell Biol 2006;174:593-604.
83. Luo Y, Radice GL. N-cadherin acts upstream of VE-cadherin in controlling vascular morphogenesis. J Cell Biol 2005;169:29-34.
84. Navarro P, Ruco L, Dejana E. Differential localization of VE- and N-cadherins in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization. J Cell Biol 1998;140:1475-1484.
85. Gerhardt H, Wolburg H, Redies C. N-cadherin mediates pericytic- endothelial interaction during brain angiogenesis in the chicken. Dev Dyn 2000;218:472-479.
86. Tillet E, Vittet D, Feraud O, Moore R, Kemler R, Huber P. N-cadherin deficiency impairs pericyte recruitment, and not endothelial differentiation or sprouting, in embryonic stem cell-derived angiogenesis. Exp Cell Res 2005;310:392-400.
87. Paik JH, Skoura A, Chae SS, Cowan AE, Han DK, Proia RL et al. Sphingosine 1-phosphate receptor regulation of N-cadherin mediates vascular stabilization. Genes Dev 2004;18:2392-2403.
88. Derycke LD, Bracke ME. N-cadherin in the spotlight of cell-cell adhesion, differentiation, embryogenesis, invasion and signalling. Int J Dev Biol 2004;48:463-476.
89. Suyama K, Shapiro I, Guttman M, Hazan RB. A signaling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor. Cancer Cell 2002;2:301-314.
90. Sanchez-Heras E, Howell FV, Williams G, Doherty P. The fibroblast growth factor receptor acid box is essential for interactions with N-cadherin and all of the major isoforms of neural cell adhesion molecule. J Biol Chem 2006;281:35208-35216.
91. Erez N, Zamir E, Gour BJ, Blaschuk OW, Geiger B. Induction of apoptosis in cultured endothelial cells by a cadherin antagonist peptide: involvement of fibroblast growth factor receptor-mediated signalling. Exp Cell Res 2004;294:366-378.
92. Nakashima T, Huang C, Liu D, Kameyama K, Masuya D, Kobayashi S et al. Neural-cadherin expression associated with angiogenesis in non-small-cell lung cancer patients. Br J Cancer 2003;88:1727- 1733.
93. Derycke L, Morbidelli L, Ziche M, De Wever O, Bracke M, Van Aken E. Soluble N-cadherin fragment promotes angiogenesis. Clin Exp Metastasis 2006;23:187-201.
94. Hulit J, Suyama K, Chung S, Keren R, Agiostratidou G, Shan W et al. N-cadherin signaling potentiates mammary tumor metastasis via enhanced extracellular signal-regulated kinase activation. Cancer Res 2007;67:3106-3116.
95. Miljan EA, Bremer EG. Regulation of growth factor receptors by gangliosides. Sci STKE 2002;2002:RE15.
96. Rusnati M, Urbinati C, Tanghetti E, Dell'Era P, Lortat-Jacob H, Presta M. Cell membrane GM1 ganglioside is a functional coreceptor for fibroblast growth factor 2. Proc Natl Acad Sci USA 2002;99:4367-4372.