VEGF: An essential mediator of both angiogenesis and endochondral ossification

Journal of Dental Research

Volumn 86, Issue 10, 2007, Pages 937-950

  Dai, J ^a   Rabie, A B M ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Angiogenesis; Bone; Cartilage; Endochondral ossification; Gene therapy; Neovascularization; Recombinant protein; Vascularity; VEGF; VEGF receptor

Indexed keywords

RECOMBINANT PROTEIN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR;

ANGIOGENESIS; ANIMAL; BIOSYNTHESIS; BONE DEVELOPMENT; CARTILAGE CELL; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE THERAPY; HUMAN; OSTEOBLAST; PHYSIOLOGY; REVIEW;

ANIMALS; CHONDROCYTES; GENE EXPRESSION REGULATION; GENE THERAPY; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOBLASTS; OSTEOGENESIS; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RECOMBINANT PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 35348855682     PISSN: 00220345     EISSN: None     Source Type: Journal    
DOI: 10.1177/154405910708601006     Document Type: Review

References (171)

1. Akeno N, Czyzyk-Krzeska MF, Gross TS, Clemens TL (2001). Hypoxia induces vascular endothelial growth factor gene transcription in human osteoblast-like cells through the hypoxia-inducible factor-2alpha. Endocrinology 142:959-962.
2. Aldridge SE, Lennard TW, Williams JR, Birch MA (2005). Vascular endothelial growth factor receptors in osteoclast differentiation and function. Biochem Biophys Res Commun 335:793-798.
3. Alini M, Marriott A, Chen T, Abe S, Poole AR (1996). A novel angiogenic molecule produced at the time of chondrocyte hypertrophy during endochondral bone formation. Dev Biol 176:124-132.
4. Autiero M, Luttun A, Tjwa M, Carmeliet P (2003). Placental growth factor and its receptor, vascular endothelial growth factor receptor-1: novel targets for stimulation of ischemic tissue revascularization and inhibition of angiogenic and inflammatory disorders. J Thromb Haemost 1:1356-1370.
5. Avantaggiato V, Orlandini M, Acampora D, Oliviero S, Simeone A (1998). Embryonic expression pattern of the murine figf gene, a growth factor belonging to platelet-derived growth factor/vascular endothelial growth factor family. Mech Dev 73:221-224.
6. Baldwin ME, Catimel B, Nice EC, Roufail S, Hall NE, Stenvers KL, et al. (2001). The specificity of receptor binding by vascular endothelial growth factor-d is different in mouse and man. J Biol Chem 276:19166-19171.
7. Bassem E, El-Mofty S, Basma GM, Wong RW, Bendeus M, Rabie AB (2006). Vascular endothelial growth factor augments the healing of demineralized bone matrix grafts. Int J Surg 4:160-166.
8. Bates DO, Cui TG, Doughty JM, Winkler M, Sugiono M, Shields JD, et al. (2002). VEGF165b, an inhibitory splice variant of vascular endothelial growth factor, is down-regulated in renal cell carcinoma. Cancer Res 62:4123-4131.
9. Bhardwaj S, Roy H, Gruchala M, Viita H, Kholova I, Kokina I, et al. (2003). Angiogenic responses of vascular endothelial growth factors in periadventitial tissue. Hum Gene Ther 14:1451-1462.
10. Bluteau G, Julien M, Magne D, Mallein-Gerin F, Weiss P, Daculsi G, et al. (2007). VEGF and VEGF receptors are differentially expressed in chondrocytes. Bone 40:568-576.
11. Byrne AM, Bouchier-Hayes DJ, Harmey JH (2005). Angiogenic and cell survival functions of vascular endothelial growth factor (VEGF). J Cell Mo1 Med 9:777-794.
12. Carlevaro MF, Cermelli S, Cancedda R, Descalzi Cancedda F (2000). Vascular endothelial growth factor (VEGF) in cartilage neovascularization and chondrocyte differentiation: auto-paracrine role during endochondral bone formation. J Cell Sci 113(Pt 1):59-69.
13. Carmeliet P (2005). Angiogenesis in life, disease and medicine. Nature 438:932-936.
14. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, et al. (1996). Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380:435-439.
15. Cha HS, Bae EK, Koh JH, Chai JY, Jeon CH, Ahn KS, et al. (2007). Tumor necrosis factor-alpha induces vascular endothelial growth factor-C expression in rheumatoid synoviocytes. J Rheumatol 34:16-19.
16. Chang SC, Chuang HL, Chen YR, Chen JK, Chung HY, Lu YL, et al. (2003). Ex vivo gene therapy in autologous bone marrow stromal stem cells for tissue-engineered maxillofacial bone regeneration. Gene Ther 10:2013-2019.
17. Chen Y, Cheung KM, Kung HF, Leong JC, Lu WW, Luk KD (2002). In vivo new bone formation by direct transfer of adenoviral-mediated bone morphogenetic protein-4 gene. Biochem Biophys Res Commun 298:121-127.
18. Cohen T, Gitay-Goren H, Sharon R, Shibuya M, Halaban R, Levi BZ, et al. (1995). VEGF121, a vascular endothelial growth factor (VEGF) isoform lacking heparin binding ability, requires cell-surface heparan sulfates for efficient binding to the VEGF receptors of human melanoma cells. J Biol Chem 270:11322-11326.
19. Cramer T, Schipani E, Johnson RS, Swoboda B, Pfander D (2004). Expression of VEGF isoforms by epiphyseal chondrocytes during low-oxygen tension is HIF-1 alpha dependent. Osteoarthritis Cartilage 12:433-439.
20. Cui TG, Foster RR, Saleem M, Mathieson PW, Gillatt DA, Bates DO, et al. (2004). Differentiated human podocytes endogenously express an inhibitory isoform of vascular endothelial growth factor (VEGF 165b) mRNA and protein. Am J Physiol Renal Physiol 286:F767-F773.
21. Dass CR, Tran TMN, Choong PFM (2007). Angiogenesis inhibitors and the need for anti-angiogenic therapeutics. J Dent Res 86: 927-936.
22. Dayoub H, Dumont RJ, Li JZ, Dumont AS, Hankins GR, Kallmes DF, et al. (2003). Human mesenchymal stem cells transduced with recombinant bone morphogenetic protein-9 adenovirus promote osteogenesis in rodents. Tissue Eng 9:347-356.
23. Deckers MM, Karperien M, van der Bent C, Yamashita T, Papapoulos SE, Lowik CW (2000). Expression of vascular endothelial growth factors and their receptors during osteoblast differentiation. Endocrinology 141:1667-1674.
24. Dibbens JA, Miller DL, Damert A, Risau W, Vadas MA, Goodall GJ (1999). Hypoxic regulation of vascular endothelial growth factor mRNA stability requires the cooperation of multiple RNA elements. Mol Biol Cell 10:907-919.
25. Durkin JF, Heeley JD, Irving JT (1973). The cartilage of the mandibular condyle. Oral Sci Rev 2:29-99.
26. Eckardt H, Bundgaard KG, Christensen KS, Lind M, Hansen ES, Hvid I (2003). Effects of locally applied vascular endothelial growth factor (VEGF) and VEGF-inhibitor to the rabbit tibia during distraction osteogenesis. J Orthop Res 21:335-340.
27. Enholm B, Paavonen K, Ristimaki A, Kumar V, Gunji Y, Klefstrom J, et al. (1997). Comparison of VEGF, VEGF-B, VEGF-C and Ang-1 mRNA regulation by serum, growth factors, oncoproteins and hypoxia. Oncogene 14:2475-2483.
28. Erlebacher A, Filvaroff EH, Gitelman SE, Derynck R (1995). Toward a molecular understanding of skeletal development. Cell 80:371-378.
29. Ferrara N, Davis-Smyth T (1997). The biology of vascular endothelial growth factor. Endocr Rev 18:4-25.
30. Ferrara N, Gerber HP (2001). The role of vascular endothelial growth factor in angiogenesis. Acta Haematol 106:148-156.
31. Ferrara N, Henzel WJ (1989). Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 161:851-858.
32. Ferrara N, Gerber HP, LeCouter J (2003). The biology of VEGF and its receptors. Nat Med 9:669-676.
33. Fiedler J, Leucht F, Waltenberger J, Dehio C, Brenner RE (2005). VEGF-A and P1GF-1 stimulate chemotactic migration of human mesenchymal progenitor cells. Biochem Biophys Res Commun 334:561-568.
34. Folkman J (1995). Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1:27-31.
35. Folkman J, Shing Y (1992). Angiogenesis. J Biol Chem 267:10931-10934.
36. Fong GH, Rossant J, Gertsenstein M, Breitman ML (1995). Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376:66-70.
37. Furumatsu T, Shen ZN, Kawai A, Nishida K, Manabe H, Oohashi T, et al. (2003). Vascular endothelial growth factor principally acts as the main angiogenic factor in the early stage of human osteoblastogenesis. J Biochem (Tokyo) 133:633-639.
38. Galeano M, Deodato B, Altavilla D, Squadrito G, Seminara P, Marini H, et al. (2003). Effect of recombinant adeno-associated virus vector-mediated vascular endothelial growth factor gene transfer on wound healing after burn injury. Crit Care Med 31:1017-1025.
39. Geiger F, Bertram H, Berger I, Lorenz H, Wall O, Eckhardt C, et al. (2005). Vascular endothelial growth factor gene-activated matrix (VEGF(165)-GAM) enhances osteogenesis and angiogenesis in large segmental bone defects. J Bone Miner Res 20:2028-2035.
40. Gengrinovitch S, Greenberg SM, Cohen T, Gitay-Goren H, Rockwell P, Maione TE, et al. (1995). Platelet factor-4 inhibits the mitogenic activity of VEGF121 and VEGF165 using several concurrent mechanisms. J Biol Chem 270:15059-15065.
41. Gerber HP, Ferrara N (2003). The role of VEGF in normal and neoplastic hematopoiesis. J Mol Med 81:20-31.
42. Gerber HP, Vu TH, Ryan AM, Kowalski J, Werb Z, Ferrara N (1999). VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med 5:623-628.
43. Gille H, Kowalski J, Li B, LeCouter J, Moffat B, Zioncheck TF, et al. (2001). Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2). A reassessment using novel receptor-specific vascular endothelial growth factor mutants. J Biol Chem 276:3222-3230.
44. Gitay-Goren H, Cohen T, Tessler S, Soker S, Gengrinovitch S, Rockwell P, et al. (1996). Selective binding of VEGF121 to one of the three vascular endothelial growth factor receptors of vascular endothelial cells. J Biol Chem 271:5519-5523.
45. Gluzman-Poltorak Z, Cohen T, Herzog Y, Neufeld G (2000). Neuropilin-2 is a receptor for the vascular endothelial growth factor (VEGF) forms VEGF-145 and VEGF-165. J Biol Chem 275:18040-18045; erratum in 275:29922.
46. Gluzman-Poltorak Z, Cohen T, Shibuya M, Neufeld G (2001). Vascular endothelial growth factor receptor-1 and neuropilin-2 form complexes. J Biol Chem 276:18688-18694.
47. Gonzalez-Crussi F (1971). Vasculogenesis in the chick embryo. An ultrastructural study. Am JAnat 130:441-460.
48. Guenther HL, Fleisch H, Sorgente N (1986). Endothelial cells in culture synthesize a potent bone cell active mitogen. Endocrinology 119:193-201.
49. Haigh JJ, Gerber HP, Ferrara N, Wagner EF (2000). Conditional inactivation of VEGF-A in areas of collagen2a1 expression results in embryonic lethality in the heterozygous state. Development 127:1445-1453.
50. Harada S, Nagy JA, Sullivan KA, Thomas KA, Endo N, Rodan GA, et al. (1994). Induction of vascular endothelial growth factor expression by prostaglandin E2 and E1 in osteoblasts. J Clin Invest 93:2490-2496.
51. Harper J, Klagsbrun M (1999). Cartilage to bone - angiogenesis leads the way. Nat Med 5:617-618.
52. Harper J, Gerstenfeld LC, Klagsbrun M (2001). Neuropilin-1 expression in osteogenic cells: down-regulation during differentiation of osteoblasts into osteocytes. J Cell Biochem 81:82-92.
53. Hauser S, Weich HA (1993). A heparin-binding form of placenta growth factor (PlGF-2) is expressed in human umbilical vein endothelial cells and in placenta. Growth Factors 9:259-268.
54. Henriksen K, Karsdal M, Delaisse JM, Engsig MT (2003). RANKL and vascular endothelial growth factor (VEGF) induce osteoclast chemotaxis through an ERK1/2-dependent mechanism. J Biol Chem 278:48745-48753.
55. Herve MA, Buteau-Lozano H, Mourah S, Calvo F, Perrot-Applanat M (2005). VEGF189 stimulates endothelial cells proliferation and migration in vitro and up-regulates the expression of Flk-1/KDR mRNA. Exp Cell Res 309:24-31.
56. Hiltunen MO, Ruuskanen M, Huuskonen J, Mahonen AJ, Ahonen M, Rutanen J, et al. (2003). Adenovirus-mediated VEGF-A gene transfer induces bone formation in vivo. FASEB J 17:1147-1149.
57. Houck KA, Ferrara N, Winer J, Cachianes G, Li B, Leung DW (1991). The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol Endocrinol 5:1806-1814.
58. Houck KA, Leung DW, Rowland AM, Winer J, Ferrara N (1992). Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chem 267:26031-26037.
59. Hutchings H, Ortega N, Plouet J (2003). Extracellular matrix-bound vascular endothelial growth factor promotes endothelial cell adhesion, migration, and survival through integrin ligation. FASEB J 17:1520-1522.
60. Inoki I, Shiomi T, Hashimoto G, Enomoto H, Nakamura H, Makino K, et al. (2002). Connective tissue growth factor binds vascular endothelial growth factor (VEGF) and inhibits VEGF-induced angiogenesis. FASEB J 16:219-221.
61. Inoue N, Kondo T, Kobayashi K, Aoki M, Numaguchi Y, Shibuya M, et al. (2006). Therapeutic angiogenesis using novel vascular endothelial growth factor-E/human placental growth factor chimera genes. Arterioscler Thromb Vase Biol 27:99-105.
62. Ito H, Koefoed M, Tiyapatanaputi P, Gromov K, Goater JJ, Carmouche J, et al. (2005). Remodeling of cortical bone allografts mediated by adherent rAAV-RANKL and VEGF gene therapy. Nat Med 11:291-297.
63. Ivkovic S, Yoon BS, Popoff SN, Safadi FF, Libuda DE, Stepheson RC, et al. (2003). Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 130:2779-2791.
64. Jakobsson L, Kreuger J, Holmborn K, Lundin L, Eriksson I, Kjellen L, et al. (2006). Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev Cell 10:625-634.
65. Jiang ZL, Reay D, Kreppel F, Gambotto A, Feingold E, Kochanek S, et al. (2001). Local high-capacity adenovirus-mediated mCTLA4Ig and mCD40Ig expression prolongs recombinant gene expression in skeletal muscle. Mol Ther 3:892-900.
66. Kaku M, Kohno S, Kawata T, Fujita I, Tokimasa C, Tsutsui K, et al. (2001). Effects of vascular endothelial growth factor on osteoclast induction during tooth movement in mice. J Dent Res 80:1880-1883.
67. Kakudo N, Kusumoto K, Wang YB, Iguchi Y, Ogawa Y (2006). Immunolocalization of vascular endothelial growth factor on intramuscular ectopic osteoinduction by bone morphogenetic protein-2. Life Sci 79:1847-1855.
68. Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, et al. (2004). Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol 5:74-80.
69. Kastrup J (2003). Therapeutic angiogenesis in ischemic heart disease: gene or recombinant vascular growth factor protein therapy? Curr Gene Ther 3:197-206.
70. Kitsukawa T, Shimono A, Kawakami A, Kondoh H, Fujisawa H (1995). Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs. Development 121:4309-4318.
71. Klagsbrun M, Takashima S, Mamluk R (2002). The role of neuropilin in vascular and tumor biology, Adv Exp Med Biol 515:33-48.
72. Kleinheinz J, Stratmann U, Joos U, Wiesmann HP (2005). VEGF-activated angiogenesis during bone regeneration. J Oral Maxillofac Surg 63:1310-1316.
73. Kohno S, Kaku M, Tsutsui K, Motokawa M, Ohtani J, Tenjo K, et al. (2003). Expression of vascular endothelial growth factor and the effects on bone remodeling during experimental tooth movement. J Dent Res 82:177-182.
74. Larrivee B, Karsan A (2000). Signaling pathways induced by vascular endothelial growth factor (review). Int J Mol Med 5:447-456.
75. Leach JK, Kaigler D, Wang Z, Krebsbach PH, Mooney DJ (2006). Coating of VEGF-releasing scaffolds with bioactive glass for angiogenesis and bone regeneration. Biomaterials 27:3249-3255.
76. Lee S, Jilani SM, Nikolova GV, Carpizo D, Iruela-Arispe ML (2005). Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J Cell Biol 169:681-691.
77. Leung FY, Rabie AB, Hagg U (2004). Neovascularization and bone formation in the condyle during stepwise mandibular advancement. Eur J Orthod 26:137-141.
78. Levy AP, Levy NS, Wegner S, Goldberg MA (1995). Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J Biol Chem 270:13333-13340.
79. Li X, Aase K, Li H, von Euler G, Eriksson U (2001). Isoform-specific expression of VEGF-B in normal tissues and tumors. Growth Factors 19:49-59.
80. Lohela M, Saaristo A, Veikkola T, Alitalo K (2003). Lymphangiogenic growth factors, receptors and therapies. Thromb Haemost 90:167-184.
81. Madan A, Curtin PT (1993). A 24-base-pair sequence 3′ to the human erythropoietin gene contains a hypoxia-responsive transcriptional enhancer. Proc Natl Acad Sci USA 90:3928-3932.
82. Maes C, Carmeliet P, Moermans K, Stockmans I, Smets N, Collen D, et al. (2002). Impaired angiogenesis and endochondral bone formation in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Mech Dev 111:61-73.
83. Maes C, Stockmans I, Moermans K, Van Looveren R, Smets N, Carmeliet P, et al. (2004). Soluble VEGF isoforms are essential for establishing epiphyseal vascularization and regulating chondrocyte development and survival, J Clin Invest 113:188-199.
84. Maes C, Coenegrachts L, Stockmans I, Daci E, Luttun A, Petryk A, et al. (2006). Placental growth factor mediates mesenchymal cell development, cartilage turnover, and bone remodeling during fracture repair. J Clin Invest 116:1230-1242.
85. Maglione D, Battisti M, Tucci M (2000). Recombinant production of PIGF-1 and its activity in animal models. Farmaco 55:165-167.
86. Marconcini L, Marchio S, Morbidelli L, Cartocci E, Albini A, Ziche M, et al. (1999). c-fos-induced growth factor/vascular endothelial growth factor D induces angiogenesis in vivo and in vitro. Proc Natl Acad Sci USA 96:9671-9676.
87. Mattei MG, Borg JP, Rosnet O, Marme D, Birnbaum D (1996). Assignment of vascular endothelial growth factor (VEGF) and placenta growth factor (PLGF) genes to human chromosome 6p12-p21 and 14q24-q31 regions, respectively. Genomics 32:168-169.
88. Mayr-Wohlfart U, Waltenberger J, Hausser H, Kessler S, Gunther KP, Dehio C, et al. (2002). Vascular endothelial growth factor stimulates chemotactic migration of primary human osteoblasts. Bone 30:472-477.
89. Meyer M, Clauss M, Lepple-Wienhues A, Waltenberger J, Augustin HG, Ziche M, et al. (1999). A novel vascular endothelial growth factor encoded by Orf virus, VEGF-E, mediates angiogenesis via signalling through VEGFR-2 (KDR) but not VEGFR-1 (Flt-1) receptor tyrosine kinases. EMBO J 18:363-374.
90. Midy V, Plouet J (1994). Vasculotropin/vascular endothelial growth factor induces differentiation in cultured osteoblasts. Biochem Biophys Res Commun 199:380-386.
91. Millauer B, Wizigmann-Voos S, Schnurch H, Martinez R, Moller NP, Risau W, et al. (1993). High affinity VEGF binding and developmental expression suggest F1k-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72:835-846.
92. Min JK, Kim YM, Kim YM, Kim EC, Gho YS, Kang IJ, et al. (2003). Vascular endothelial growth factor up-regulates expression of receptor activator of NF-kappa B (RANK) in endothelial cells. Concomitant increase of angiogenic responses to RANK ligand. J Biol Chem 278:39548-39557.
93. Miyata Y, Kanda S, Ohba K, Nomata K, Hayashida Y, Eguchi J, et al. (2006). Lymphangiogenesis and angiogenesis in bladder cancer: prognostic implications and regulation by vascular endothelial growth factors-A, -C, and -D. Clin Cancer Res 12(3 Pt 1):800-806.
94. Nakagawa M, Kaneda T, Arakawa T, Morita S, Sato T, Yomada T, et al. (2000). Vascular endothelial growth factor (VEGF) directly enhances osteoclastic bone resorption and survival of mature osteoclasts. FEBS Lett 473:161-164.
95. Narazaki M, Tosato G (2006). Ligand-induced internalization selects use of common receptor neuropilin-1 by VEGF165 and semaphorin3A. Blood 107:3892-3901.
96. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z (1999). Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 13:9-22.
97. Ng YS, Rohan R, Sunday ME, Demello DE, D'Amore PA (2001). Differential expression of VEGF isoforms in mouse during development and in the adult. Dev Dyn 220:112-121.
98. Niida S, Kaku M, Amano H, Yoshida H, Kataoka H, Nishikawa S, et al. (1999). Vascular endothelial growth factor can substitute for macrophage colony-stimulating factor in the support of osteoclastic bone resorption. J Exp Med 190:293-298.
99. Niida S, Kondo T, Hiratsuka S, Hayashi S, Amizuka N, Noda T, et al. (2005). VEGF receptor 1 signaling is essential for osteoclast development and bone marrow formation in colony-stimulating factor 1-deficient mice. Proc Natl Acad Sci USA 102:14016-14021.
100. Nissen NN, Polverini PJ, Koch AE, Volin MV, Gamelli RL, DiPietro LA (1998). Vascular endothelial growth factor mediates angiogenic activity during the proliferative phase of wound healing. Am J Pathol 152:1445-1452.
101. Ogawa S, Oku A, Sawano A, Yamaguchi S, Yazaki Y, Shibuya M (1998). A novel type of vascular endothelial growth factor, VEGF-E (NZ-7 VEGF), preferentially utilizes KDR/Flk-1 receptor and carries a potent mitotic activity without heparin-binding domain. J Biol Chem 273:31273-31282.
102. Okuda N, Takeda S, Shinomiya K, Muneta T, Itoh S, Noda M, et al. (2006). ED-71, a novel vitamin D analog, promotes bone formation and angiogenesis and inhibits bone resorption after bone marrow ablation. Bone 40:281-292.
103. Olofsson B, Korpelainen E, Pepper MS, Mandriota SJ, Aase K, Kumar V, et al. (1998). Vascular endothelial growth factor B (VEGF-B) binds to VEGF receptor-1 and regulates plasminogen activator activity in endothelial cells. Proc Natl Acad Sci USA 95:11709-11714.
104. Orlandini M, Spreafico A, Bardelli M, Rocchigiani M, Salameh A, Nucciotti S, et al. (2006). Vascular endothelial growth factor-D activates VEGFR-3 expressed in osteoblasts inducing their differentiation. J Biol Chem 281:17961-17967.
105. Oyama T, Sakuta T, Matsushita K, Maruyama I, Nagaoka S, Torii M (2000). Effects of roxithromycin on tumor necrosis factor-alpha-induced vascular endothelial growth factor expression in human periodontal ligament cells in culture. J Periodontol 71:1546-1553.
106. Paavonen K, Horelli-Kuitunen N, Chilov D, Kukk E, Pennanen S, Kallioniemi OP, et al. (1996). Novel human vascular endothelial growth factor genes VEGF-B and VEGF-C localize to chromosomes 11q13 and 4q34, respectively. Circulation 93:1079-1082.
107. Park J, Ries J, Gelse K, Kloss F, von der Mark K, Wiltfang J, et al. (2003). Bone regeneration in critical size defects by cell-mediated BMP-2 gene transfer: a comparison of adenoviral vectors and liposomes. Gene Ther 10:1089-1098.
108. Park JE, Chen HH, Winer J, Houck KA, Ferrara N (1994). Placenta growth factor. Potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt-1 but not to Flk-1/KDR. J Biol Chem 269:25646-25654.
109. Peng H, Wright V, Usas A, Gearhart B, Shen HC, Cummins J, et al. (2002). Synergistic enhancement of bone formation and healing by stem cellexpressed VEGF and bone morphogenetic protein-4. J Clin Invest 110:751-759.
110. Perbal B (2004). CCN proteins: multifunctional signalling regulators. Lancet 363:62-64.
111. Petit AM, Rak J, Hung MC, Rockwell P, Goldstein N, Fendly B, et al. (1997). Neutralizing antibodies against epidermal growth factor and ErbB-2/neu receptor tyrosine kinases down-regulate vascular endothelial growth factor production by tumor cells in vitro and in vivo: angiogenic implications for signal transduction therapy of solid tumors. Am J Pathol 151:1523-1530.
112. Pfander D, Cramer T, Schipani E, Johnson RS (2003). HIF-1 alpha controls extracellular matrix synthesis by epiphyseal chondrocytes. J Cell Sci 116(Pt9):1819-1826.
113. Poltorak Z, Cohen T, Sivan R, Kandelis Y, Spira G, Vlodavsky I, et al. (1997). VEGF 145, a secreted vascular endothelial growth factor isoform that binds to extracellular matrix. J Biol Chem 272:7151-7158.
114. Polverini PJ (1995). The pathophysiology of angiogenesis. Crit Rev Oral Biol Med 6:230-247.
115. Pufe T, Harde V, Petersen W, Goldring MB, Tillmann B, Mentlein R (2004). Vascular endothelial growth factor (VEGF) induces matrix metalloproteinase expression in immortalized chondrocytes. J Pathol 202:367-374.
116. Rabie AB (1997). Vascular endothelial growth pattern during demineralized bone matrix induced osteogenesis. Connect Tissue Res 36:337-345.
117. Rabie AB, Hagg U (2002). Factors regulating mandibular condylar growth. Am J Orthod Dentofacial Orthop 122:401-409.
118. Rabie AB, Deng YM, Samman N, Hagg U (1996). The effect of demineralized bone matrix on the healing of intramembranous bone grafts in rabbit skull defects. J Dent Res 75:1045-1051.
119. Rabie AB, Leung FY, Chayanupatkul A, Hagg U (2002a). The correlation between neovascularization and bone formation in the condyle during forward mandibular positioning. Angle Orthod 72:431-438.
120. Rabie AB, Shum L, Chayanupatkul A (2002b). VEGF and bone formation in the glenoid fossa during forward mandibular positioning. Am J Orthod Dentofacial Orthop 122:202-209.
121. Rabie AB, Tang GH, Hagg U (2004). Cbfal couples chondrocytes maturation and endochondral ossification in rat mandibular condylar cartilage. Arch Oral Biol 49:109-118.
122. Rabie AB, Dai J, Xu R (2007). Recombinant AAV mediated VEGF gene therapy induces mandibular condylar growth. Gene Ther 14:972-980.
123. Risau W (1997). Mechanisms of angiogenesis. Nature 386:671-674.
124. Rissanen TT, Markkanen JE, Gruchala M, Heikura T, Puranen A, Kettunen MI, et al. (2003). VEGF-D is the strongest angiogenic and lymphangiogenic effector among VEGFs delivered into skeletal muscle via adenoviruses. Circ Res 92:1098-1106.
125. Roberts DM, Kearney JB, Johnson JH, Rosenberg MP, Kumar R, Bautch VL (2004). The vascular endothelial growth factor (VEGF) receptor Flt-1 (VEGFR-1) modulates Flk-1 (VEGFR-2) signaling during blood vessel formation. Am J Pathol 164:1531-1535.
126. Roy H, Bhardwaj S, Babu M, Jauhiainen S, Herzig KH, Bellu AR, et al. (2005). Adenovirus-mediated gene transfer of placental growth factor to perivascular tissue induces angiogenesis via upregulation of the expression of endogenous vascular endothelial growth factor-A. Hum Gene Ther 16:1422-1428.
127. Roy H, Bhardwaj S, Yla-Herttuala S (2006). Biology of vascular endothelial growth factors. FEBS Lett 580:2879-2887.
128. Selleck SB (2006). Signaling from across the way: transactivation of VEGF receptors by HSPGs. Mol Cell 22:431-432.
129. Senger DR, Van de Water L, Brown LF, Nagy JA, Yeo KT, Yeo TK, et al. (1993). Vascular permeability factor (VPF, VEGF) in tumor biology. Cancer Metastasis Rev 12:303-324.
130. Shakibaei M, Schulze-Tanzil G, Mobasheri A, Beichler T, Dressler J, Schwab W (2003). Expression of the VEGF receptor-3 in osteoarthritic chondrocytes: stimulation by interleukin-lbeta and association with beta(1)-integrins. Histochem Cell Biol 120:235-241.
131. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, et al. (1995). Failure of blood-island formation and vasculogenesis in FIk-1-deficient mice. Nature 376:62-66.
132. Shibuya M (2006). Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J Biochem Mol Biol 39:469-478.
133. Shraga-Heled N, Kessler O, Prahst C, Kroll J, Augustin H, Neufeld G (2007). Neuropilin-1 and neuropilin-2 enhance VEGF121 stimulated signal transduction by the VEGFR-2 receptor. FASEB J 21:915-926.
134. Shweiki D, Itin A, Neufeld G, Gitay-Goren H, Keshet E (1993). Patterns of expression of vascular endothelial growth factor (VEGF) and VEGF receptors in mice suggest a role in hormonally regulated angiogenesis. J Clin Invest 91:2235-2243.
135. Silins G, Grimmond S, Egerton M, Hayward N (1997). Analysis of the promoter region of the human VEGF-related factor gene. Biochem Biophys Res Commun 230:413-418.
136. Silvestre JS, Tamarat R, Ebrahimian TG, Le-Roux A, Clergue M, Emmanuel F, et al. (2003). Vascular endothelial growth factor-B promotes in vivo angiogenesis. Circ Res 93:114-123.
137. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M (1998). Neuropilin-1 is expressed by endothelial and tumor cells as an isoformspecific receptor for vascular endothelial growth factor. Cell 92:735-745.
138. Spector JA, Mehrara BJ, Luchs JS, Greenwald JA, Fagenholz PJ, Saadeh PB, et al. (2000). Expression of adenovirally delivered gene products in healing osseous tissues. Ann Plast Surg 44:522-528.
139. Street J, Bao M, deGuzman L, Bunting S, Peale FV, Ferrara N, et al. (2002). Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci USA 99:9656-9661.
140. Stringer SE (2006). The role of heparan sulphate proteoglycans in angiogenesis. Biochem Soc Trans 34(Pt 3):451-453.
141. Suto K, Yamazaki Y, Morita T, Mizuno H (2005). Crystal structures of novel vascular endothelial growth factors (VEGF) from snake venoms: insight into selective VEGF binding to kinase insert domain-containing receptor but not to fms-like tyrosine kinase-1. J Biol Chem 280:2126-2131.
142. Tamayose K, Hirai Y, Shimada T (1996). A new strategy for large-scale preparation of high-titer recombinant adeno-associated virus vectors by using packaging cell lines and sulfonated cellulose column chromatography. Hum Gene Ther 7:507-513.
143. Tammela T, Enholm B, Alitalo K, Paavonen K (2005). The biology of vascular endothelial growth factors. Cardiovasc Res 65:550-563.
144. Tang GH, Rabie AB (2005). Runx2 regulates endochondral ossification in condyle during mandibular advancement. J Dent Res 84:166-171.
145. Tarkka T, Sipola A, Jamsa T, Soini Y, Yla-Herttuala S, Tuukkanen J, et al. (2003). Adenoviral VEGF-A gene transfer induces angiogenesis and promotes bone formation in healing osseous tissues. J Gene Med 5:560-566.
146. Tessler S, Rockwell P, Hicklin D, Cohen T, Levi BZ, Witte L, et al. (1994). Heparin modulates the interaction of VEGF165 with soluble and cell associated flk-1 receptors. J Biol Chem 269:12456-12461.
147. Tischer E, Mitchell R, Hartman T, Silva M, Gospodarowicz D, Fiddes JC, et al. (1991). The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J Biol Chem 266:11947-11954.
148. Tokuda H, Hatakeyama D, Akamatsu S, Tanabe K, Yoshida M, Shibata T, et al. (2003a). Involvement of MAP kinases in TGF-beta-stimulated vascular endothelial growth factor synthesis in osteoblasts. Arch Biochem Biophys 415:117-125.
149. Tokuda H, Kato K, Oiso Y, Kozawa O (2003b). Contrasting effects of triiodothyronine on heat shock protein 27 induction and vascular endothelial growth factor synthesis stimulated by TGF-beta in osteoblasts. Mol Cell Endocrinol 201:33-38.
150. Veikkola T, Alitalo K (1999). VEGFs, receptors and angiogenesis. Semin Cancer Biol 9:211-220.
151. Vincenti V, Cassano C, Rocchi M, Persico G (1996). Assignment of the vascular endothelial growth factor gene to human chromosome 6p21.3. Circulation 93:1493-1495.
152. Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, Hanahan D, et al. (1998). MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93:411-422.
153. Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin CH (1994), Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor, J Biol Chem 269:26988-26995.
154. Wang DS, Yamazaki K, Nohtomi K, Shizume K, Ohsumi K, Shibuya M, et al. (1996), Increase of vascular endothelial growth factor mRNA expression by 1,25-dihydroxyvitamin D3 in human osteoblast-like cells. J Bone Miner Res 11:472-479.
155. Wauke K, Nagashima M, Ishiwata T, Asano G, Yoshino S (2002). Expression and localization of vascular endothelial growth factor-C in rheumatoid arthritis synovial tissue. J Rheumatol 29:34-48.
156. Wise GE, Yao S (2003). Expression of vascular endothelial growth factor in the dental follicle. Crit Rev Eukaryot Gene Expr 13(2-4):173-180.
157. Woolard J, Wang WY, Bevan HS, Qiu Y, Morbidelli L, Pritchard-Jones RO, et al. (2004). VEGF165b, an inhibitory vascular endothelial growth factor splice variant: mechanism of action, in vivo effect on angiogenesis and endogenous protein expression. Cancer Res 64:7822-7835.
158. Xiong H, Rabie AB, Hagg U (2005). Neovascularization and mandibular condylar bone remodeling in adult rats under mechanical strain. Front Biosci 10:74-82.
159. Yamada Y, Nezu J, Shimane M, Hirata Y (1997). Molecular cloning of a novel vascular endothelial growth factor, VEGF-D. Genomics 42:483-488.
160. Yatnazaki Y, Morita T (2006). Molecular and functional diversity of vascular endothelial growth factors. Mol Divers 10:515-527.
161. Yamazaki Y, Tokunaga Y, Takani K, Morita T (2005). Identification of the heparin-binding region of snake venom vascular endothelial growth factor (VEGF-F) and its blocking of VEGF-A165. Biochemistry 44:8858-8864.
162. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J (2000). Vascular-specific growth factors and blood vessel formation. Nature 407:242-248.
163. Yao S, Liu D, Pan F, Wise GE (2006). Effect of vascular endothelial growth factor on RANK gene expression in osteoclast precursors and on osteoclastogenesis. Arch Oral Biol 51:596-602.
164. Yeh LC, Lee JC (1999). Osteogenic protein-1 increases gene expression of vascular endothelial growth factor in primary cultures of fetal rat calvaria cells. Mol Cell Endocrinol 153:113-124.
165. Yuan L, Moyon D, Pardanaud L, Breant C, Karkkainen MJ, Alitalo K, et al. (2002). Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 129:4797-4806.
166. Zelzer E, Olsen BR (2005). Multiple roles of vascular endothelial growth factor (VEGF) in skeletal development, growth, and repair. Curr Top Dev Biol 65:169-187.
167. Zelzer E, Glotzer DJ, Hartmann C, Thomas D, Fukai N, Soker S, et al. (2001). Tissue specific regulation of VEGF expression during bone development requires Cbfal/Runx2. Mech Dev 106:97-106.
168. Zelzer E, McLean W, Ng YS, Fukai N, Reginato AM, Lovejoy S, et al. (2002). Skeletal defects in VEGF(120/120) mice reveal multiple roles for VEGF in skeletogenesis. Development 129:1893-1904.
169. Zelzer E, Mamluk R, Ferrara N, Johnson RS, Schipani E, Olsen BR (2004). VEGFA is necessary for chondrocyte survival during bone development. Development 131:2161-2171.
170. Zeng H, Dvorak HF, Mukhopadhyay D (2001). Vascular permeability factor (VPF)/vascular endothelial growth factor (VEGF) peceptor-1 down-modulates VPF/VEGF receptor-2-mediated endothelial cell proliferation, but not migration, through phosphatidylinositol 3-kinase-dependent pathways. J Biol Chem 276:26969-26979.
171. Zhang F, Fischer K, Lineaweaver WC (2002), DNA strand gene transfer and bone healing. J Long Term Eff Med Implants 12:113-123.