Expression of pro- and anti-angiogenic factors during the formation of the periocular vasculature and development of the avian cornea

Developmental Dynamics

Volumn 242, Issue 6, 2013, Pages 738-751

  Kwiatkowski, Sam ^a   Munjaal, Ravi P ^a   Lee, Teresa ^a   Lwigale, Peter Y ^a  

^a RICE UNIVERSITY   (United States)

Author keywords

Angioblast; Anti angiogenic; Ocular development; Periocular vasculature; Pro angiogenic; Vasculogenesis

Indexed keywords

BIOLOGICAL FACTOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; NETRIN; NETRIN 1; NETRIN 4; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN NPN2; PROTEIN UNC5B; SEMAPHORIN; SEMAPHORIN 3E; SEMAPHORIN 3G; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; BIRD; CELL INVASION; CORNEA; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIAL PROGENITOR CELL; EYE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUAIL;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BACTERIAL PROTEINS; CORNEA; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; LUMINESCENT PROTEINS; NEOVASCULARIZATION, PHYSIOLOGIC; QUAIL; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84878150521     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23956     Document Type: Article

References (99)

1. Acevedo LM, Barillas S, Weis SM, Göthert JR, Cheresh DA. 2008. Semaphorin 3A suppresses VEGF-mediated angiogenesis yet acts as a vascular permeability factor. Blood 111:2674-2680.
2. Adams RH, Alitalo K. 2007. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8:464-478.
3. Adams RH, Eichmann A. 2010. Axon guidance molecules in vascular patterning. Cold Spring Harb Perspect Biol 2:1-18.
4. Adler R, Belecky-Adams TL. 2002. The role of bone morphogenetic proteins in the differentiation of the ventral optic cup. Development 129:3161-3171.
5. Aiello LP, Pierce EA, Foley ED, Takagi H, Chen H, Riddle L, Ferrara N, King GL, Smith LE. 1995. Suppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc Natl Acad Sci U S A 92:10457-10461.
6. Ambati BK, Nozaki M, Singh N, Takeda A, Jani PD, Suthar T, Albuquerque RJ, Richter E, Sakurai E, Newcomb MT, Kleinman ME, Caldwell RB, Lin Q, Ogura Y, Orecchia A, Samuelson DA, Agnew DW, St Leger J, Green WR, Mahasreshti PJ, Curiel DT, Kwan D, Marsh H, Ikeda S, Leiper LJ, Collinson JM, Bogdanovich S, Khurana TS, Shibuya M, Baldwin ME, Ferrara N, Gerber HP, De Falco S, Witta J, Baffi JZ, Raisler BJ, Ambati J. 2006. Corneal avascularity is due to soluble VEGF receptor-1. Nature 443:993-997.
7. Ambati BK, Patterson E, Jani P, Jenkins C, Higgins E, Singh N, Suthar T, Vira N, Smith K, Caldwell R. 2007. Soluble vascular endothelial growth factor receptor-1 contributes to the corneal antiangiogenic barrier. Br J Ophthalmol 91:505-508.
8. Andrae J, Gallini R, Betsholtz C. 2008. Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 22:1276-1312.
9. Argraves WS, Larue AC, Fleming PA, Drake CJ. 2002. VEGF signaling is required for the assembly but not the maintenance of embryonic blood vessels. Dev Dyn 225:298-304.
10. Armulik A, Abramsson A, Betsholtz C. 2005. Endothelial/pericyte interactions. Circ Res 97:512-523.
11. Auerbach R, Lewis R, Shinners B, Kubai L, Akhtar N. 2003. Angiogenesis assays: a critical overview. Clin Chem 49:32-40.
12. Bagri A, Tessier-Lavigne M, Watts RJ. 2009. Neuropilins in tumor biology. Clin Cancer Res 15:1860-1864.
13. Bates D, Taylor GI, Minichiello J, Farlie P, Cichowitz A, Watson N, Klagsbrun M, Mamluk R, Newgreen DF. 2003. Neurovascular congruence results from a shared patterning mechanism that utilizes Semaphorin3A and Neuropilin-1. Dev Biol 255:77-98.
14. Benny O, Nakai K, Yoshimura T, Bazinet L, Akula JD, Nakao S, Hafezi-Moghadam A, Panigrahy D, Pakneshan P, D'Amato RJ. 2010. Broad spectrum antiangiogenic treatment for ocular neovascular diseases. PLoS ONE 5:e12515.
15. Bjarnegård M, Enge M, Norlin J, Gustafsdottir S, Fredriksson S, Abramsson A, Takemoto M, Gustafsson E, Fässler R, Betsholtz C. 2004. Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 131:1847-1857.
16. Blaber SI, Culajay JF, Khurana A, Blaber M. 1999. Reversible thermal denaturation of human FGF-1 induced by low concentrations of guanidine hydrochloride. Biophys J 77:470-477.
17. Bouvrée K, Larrivée B, Lv X, Yuan L, DeLafarge B, Freitas C, Mathivet T, Bréant C, Tessier-Lavigne M, Bikfalvi A, Eichmann A, Pardanaud L. 2008. Netrin-1 inhibits sprouting angiogenesis in developing avian embryos. Dev Biol 318:172-183.
18. Callander DC, Lamont RE, Childs SJ, McFarlane S. 2007. Expression of multiple class three semaphorins in the retina and along the path of zebrafish retinal axons. Dev Dyn 236:2918-2924.
19. Cao R, Lim S, Ji H, Zhang Y, Yang Y, Honek J, Hedlund EM, Cao Y. 2011. Mouse corneal lymphangiogenesis model. Nat Protoc 6:817-826.
20. Carmeliet P. 2003. Angiogenesis in health and disease. Nat Med 9:653-660.
21. Carmeliet P, Tessier-Lavigne M. 2005. Common mechanisms of nerve and blood vessel wiring. Nature 436:193-200.
22. Chan B, Yuan HT, Ananth Karumanchi S, Sukhatme VP. 2008. Receptor tyrosine kinase Tie-1 overexpression in endothelial cells upregulates adhesion molecules. Biochem Biophys Res Commun 371:475-479.
23. Chen P, Yin H, Wang Y, Mi J, He W, Xie L, Wang Y. 2010. Multi-gene targeted antiangiogenic therapies for experimental corneal neovascularization. Mol Vis 16:310-319.
24. Chilton JK, Guthrie S. 2003. Cranial expression of class 3 secreted semaphorins and their neuropilin receptors. Dev Dyn 228:726-733.
25. Creuzet S, Couly G, Le Douarin NM. 2005. Patterning the neural crest derivatives during development of the vertebrate head: insights from avian studies. J Anat 207:447-459.
26. Crivellato E. 2011. The role of angiogenic growth factors in organogenesis. Int J Dev Biol 55:365-375.
27. Eichmann A, Yuan L, Moyon D, Lenoble F, Pardanaud L, Breant C. 2005. Vascular development: from precursor cells to branched arterial and venous networks. Int J Dev Biol 49:259-267.
28. Ellenberg D, Azar DT, Hallak JA, Tobaigy F, Han KY, Jain S, Zhou Z, Chang JH. 2010. Novel aspects of corneal angiogenic and lymphangiogenic privilege. Prog Retin Eye Res 29:208-248.
29. Etchevers HC, Vincent C, Douarin NML, Couly GF. 2001. The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 128:1059-1068.
30. Ferguson JE, Kelley RW, Patterson C. 2005. Mechanisms of endothelial differentiation in embryonic vasculogenesis. Arterioscler Thromb Vasc Biol 25:2246-2254.
31. 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.
32. Friesel R, Maciag T. 1995. Molecular mechanisms of angiogenesis: fibroblast growth factor signal transduction. FASEB J 9:919-925.
33. Gaengel K, Genové G, Armulik A, Betsholtz C. 2009. Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol 29:630-638.
34. Gammill LS, Gonzales C, Bronner-Fraser M. 2006. Neuropilin 2/Semaphorin 3F signaling is essential for cranial neural crest migration and trigeminal ganglion condensation. Dev Neurobiol 67:47-56.
35. Gitler AD, Lu MM, Epstein JA. 2004. PlexinD1 and semaphorin signaling are required in endothelial cells for cardiovascular development. Dev Cell 7:107-116.
36. Gu C. 2005. Semaphorin 3E and Plexin-D1 control vascular pattern independently of neuropilins. Science 307:265-268.
37. Gu C, Rodriguez ER, Reimert DV, Shu T, Fritzsch B, Richards LJ, Kolodkin AL, Ginty DD. 2003. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev Cell 5:45-57.
38. Guttmann-Raviv N, Shraga-Heled N, Varshavsky A, Gulmaraes-Sternberg C, Kessler O, Neufeld G. 2007. Semaphorin-3A and Semaphorin-3F work together to repel endothelial cells and to inhibit their survival by induction of apoptosis. J Biol Chem 282:26294-26305.
39. Han X, Zhang MC. 2010. Potential anti-angiogenic role of Slit2 in corneal neovascularization. Exp Eye Res 90:742-749.
40. Harada T, Harada C, Parada LF. 2007. Molecular regulation of visual system development: more than meets the eye. Genes Dev 21:367-378.
41. Hay ED. 1980. Development of the vertebrate cornea. Int Rev Cytol 63:263-322.
42. Hellberg C, Ostman A, Heldin CH. 2010. PDGF and vessel maturation. Recent Results Cancer Res 180:103-114.
43. Hellström M, Kalén M, Lindahl P, Abramsson A, Betsholtz C. 1999. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126:3047-3055.
44. Hiruma T. 1996. Formation of the ocular arteries in the chick embryo: observations of corrosion casts by scanning electron microscopy. Anat Embryol (Berl) 193:585-592.
45. Hiruma T, Hirakow R. 1995. Formation of the pharyngeal arch arteries in the chick embryo. Observations of corrosion casts by scanning electron microscopy. Anat Embryol 191:415-423.
46. Hughes AFW. 1934. On the development of the blood vessels in the head of the chick. Philos Trans R Soc B 224:75-130.
47. Iljin K, Petrova TV, Veikkola T, Kumar V, Poutanen M, Alitalo K. 2002. A fluorescent Tie1 reporter allows monitoring of vascular development and endothelial cell isolation from transgenic mouse embryos. FASEB J 16:1764-1774.
48. Itoh N, Ornitz DM. 2004. Evolution of the FGF and FGFR gene families. Trends Genet 20:563-569.
49. Javerzat S, Auguste P, Bikfalvi A. 2002. The role of fibroblast growth factors in vascular development. Trends Mol Med 8:483-489.
50. Jiang Y, Liu M, Gershon MD. 2003. Netrins and DCC in the guidance of migrating neural crest-derived cells in the developing bowel and pancreas. Dev Biol 258:364-384.
51. Kawasaki T, Kitsukawa T, Bekku Y, Matsuda Y, Sanbo M, Yagi T, Fujisawa H. 1999. A requirement for Neuropilin-1 in embryonic vessel formation. Development 126:4895-4902.
52. Kenyon BM, Voest EE, Chen CC, Flynn E, Folkman J, D'Amato RJ. 1996. A model of angiogenesis in the mouse cornea. Invest Ophthalmol Vis Sci 37:1625-1632.
53. 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.
54. Kok A, Lovicu FJ, Chamberlain CG, McAvoy JW. 2002. Influence of platelet-derived growth factor on lens epithelial cell proliferation and differentiation. Growth Factors 20:27-34.
55. Kubilus JK, Linsenmayer TF. 2010. Developmental guidance of embryonic corneal innervation: roles of Semaphorin3A and Slit2. Dev Biol 344:172-184.
56. Kutschera S, Weber H, Weick A, De Smet F, Genove G, Takemoto M, Prahst C, Riedel M, Mikelis C, Baulande S, Champseix C, Kummerer P, Conseiller E, Multon MC, Heroult M, Bicknell R, Carmeliet P, Betsholtz C, Augustin HG. 2011. Differential endothelial transcriptomics identifies Semaphorin 3G as a vascular class 3 semaphorin. Arterioscler Thromb Vasc Biol 31:151-159.
57. Larrivée B, Freitas C, Trombe M, Lv X, Delafarge B, Yuan L, Bouvrée K, Bréant C, Del Toro R, Bréchot N, Germain S, Bono F, Dol F, Claes F, Fischer C, Autiero M, Thomas JL, Carmeliet P, Tessier-Lavigne M, Eichmann A. 2007. Activation of the Unc5B receptor by Netrin-1 inhibits sprouting angiogenesis. Genes Dev 21:2433-2447.
58. Latker CH, Kuwabara T. 1981. Regression of the tunica vasculosa lentis in the postnatal rat. Invest Ophthalmol Vis Sci 21:689-699.
59. Lejmi E, Leconte L, Pédron-Mazoyer S, Ropert S, Raoul W, Lavalette S, Bouras I, Feron JG, Maitre-Boube M, Assayag F, Feumi C, Alemany M, Jie TX, Merkulova T, Poupon MF, Ruchoux MM, Tobelem G, Sennlaub F, Plouët J. 2008. Netrin-4 inhibits angiogenesis via binding to Neogenin and recruitment of Unc5B. Proc Natl Acad Sci U S A 105:12491-12496.
60. Lindahl P, Johansson BR, Levéen P, Betsholtz C. 1997. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277:242-245.
61. Lu X, Le Noble F, Yuan L, Jiang Q, De Lafarge B, Sugiyama D, Bréant C, Claes F, De Smet F, Thomas JL, Autiero M, Carmeliet P, Tessier-Lavigne M, Eichmann A. 2004. The netrin receptor Unc5B mediates guidance events controlling morphogenesis of the vascular system. Nature 432:179-186.
62. Lwigale PY, Bronner-Fraser M. 2009. Semaphorin3A/Neuropilin-1 signaling acts as a molecular switch regulating neural crest migration during cornea development. Dev Biol 336:257-265.
63. Lwigale PY, Cressy PA, Bronner-Fraser M. 2005. Corneal keratocytes retain neural crest progenitor cell properties. Dev Biol 288:284-293.
64. Matsushima M, Ogata N, Takada Y, Tobe T, Yamada H, Takahashi K, Uyama M. 1996. FGF receptor 1 expression in experimental choroidal neovascularization. Jpn J Ophthalmol 40:329-338.
65. McAvoy JW, Chamberlain CG., de Iongh RU, Richardson NA, Lovicu FJ. 1991. The role of fibroblast growth factor in eye lens development. Ann N Y Acad Sci 638:256-274.
66. McCabe KL, Shiau CE, Bronner-Fraser M. 2007. Identification of candidate secreted factors involved in trigeminal placode induction. Dev Dyn 236:2925-2935.
67. Miao HQ, Soker S, Feiner L, Alonso JL, Raper JA, Klagsbrun M. 1999. Neuropilin-1 mediates Collapsin-1/Semaphorin III inhibition of endothelial cell motility: functional competition of Collapsin-1 and vascular endothelial growth factor-165. J Cell Biol 146:233-241.
68. 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.
69. Morcillo J, Martínez-Morales JR, Trousse F, Fermin Y, Sowden JC, Bovolenta P. 2006. Proper patterning of the optic fissure requires the sequential activity of Bmp7 and Shh. Development 133:3179-3190.
70. Moura RS, Coutinho-Borges JP, Pacheco AP, daMota PO, Correia-Pinto J. 2011. FGF signaling pathway in the developing chick lung: expression and inhibition studies. PLoS One 6:e17660.
71. Murakami M, Nguyen LT, Zhang ZW, Moodie KL, Carmeliet P, Stan RV, Simons M. 2008. The FGF system has a key role in regulating vascular integrity. J Clin Invest 118:3355-3366.
72. 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.
73. Pan Q, Chathery Y, Wu Y, Rathore N, Tong RK, Peale F, Bagri A, Tessier-Lavigne M, Koch AW, Watts RJ. 2007. Neuropilin-1 binds to VEGF121 and regulates endothelial cell migration and sprouting. J Biol Chem 282:24049-24056.
74. Pellegrini L. 2001. Role of heparan sulfate in fibroblast growth factor signalling: a structural view. Curr Opin Struct Biol 11:629-634.
75. 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.
76. Presta M, Dell'Era P, Mitola S, Moroni E, Ronca R, Rusnati M. 2005. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev 16:159-178.
77. Rajasekharan S, Kennedy TE. 2009. The netrin protein family. Genome Biol 10:239-239.
78. Reneker LW, Overbeek PA. 1996. Lens-specific expression of PDGF-A alters lens growth and development. Dev Biol 180:554-565.
79. Risau W, Flamme I. 1995. Vasculogenesis. Annu Rev Cell Dev Biol 11:73-91.
80. Rolny C, Nilsson I, Magnusson P, Armulik A, Jakobsson L, Wentzel P, Lindblom P, Norlin J, Betsholtz C, Heuchel R, Welsh M, Claesson-Welsh L. 2006. Platelet-derived growth factor receptor-beta promotes early endothelial cell differentiation. Blood 108:1877-1886.
81. 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.
82. Ruhrberg C, Gerhardt H, Golding M, Watson R, Ioannidou S, Fujisawa H, Betsholtz C, Shima DT. 2002. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev 16:2684-2698.
83. Saint-Geniez M, D'Amore PA. 2004. Development and pathology of the hyaloid, choroidal and retinal vasculature. Int J Dev Biol 48:1045-1058.
84. Sakurai A, Gavard J, Annas-Linhares Y, Basile JR, Amornphimoltham P, Palmby TR, Yagi H, Zhang F, Randazzo PA, Li X, Weigert R, Gutkind JS. 2010. Semaphorin 3E initiates antiangiogenic signaling through Plexin D1 by regulating Arf6 and R-Ras. Mol Cell Biol 30:3086-3098.
85. Sato Y, Poynter G, Huss D, Filla MB, Czirok A, Rongish BJ, Little CD, Fraser SE, Lansford R. 2010. Dynamic analysis of vascular morphogenesis using transgenic quail embryos. PLoS ONE 5:e12674.
86. Schmidt A, Brixius K, Bloch W. 2007. Endothelial precursor cell migration during vasculogenesis. Circ Res 101:125-136.
87. Serini G, Valdembri D, Zanivan S, Morterra G, Burkhardt C, Caccavari F, Zammataro L, Primo L, Tamagnone L, Logan M, Tessier-Lavigne M, Taniguchi M, Püschel AW, Bussolino F. 2003. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 424:391-397.
88. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376:62-66.
89. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M. 1998. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92:735-745.
90. Steffensky M, Steinbach K, Schwarz U, Schlosshauer B. 2006. Differential impact of semaphorin 3E and 3A on CNS axons. Int J Dev Neurosci 24:65-72.
91. Suárez Y, Sessa WC. 2009. MicroRNAs as novel regulators of angiogenesis. Circ Res 104:442-454.
92. Tam SJ, Watts RJ. 2010. Connecting vascular and nervous system development: angiogenesis and the blood-brain barrier. Annu Rev Neurosci 33:379-408.
93. 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.
94. Torres-Vázquez J, Gitler AD, Fraser SD, Berk JD, Van N Pham, Fishman MC, Childs S, Epstein JA, Weinstein BM. 2004. Semaphorin-Plexin signaling guides patterning of the developing vasculature. Dev Cell 7:117-123.
95. Weiss O, Kaufman R, Michaeli N, Inbal A. 2012. Abnormal vasculature interferes with optic fissure closure in lmo2 mutant zebrafish embryos. Dev Biol 369:191-198.
96. Xu S. 2009. MicroRNA expression in the eyes and their significance in relation to functions. Prog Retin Eye Res 28:87-116.
97. Yamada E, Tobe T, Yamada H, Okamoto N, Zack DJ, Werb Z, Soloway PD, Campochiaro PA. 2001. TIMP-1 promotes VEGF-induced neovascularization in the retina. Histol Histopathol 16:87-97.
98. Zhang J, Cao R, Zhang Y, Jia T, Cao Y, Wahlberg E. 2009. Differential roles of PDGFR-alpha and PDGFR-beta in angiogenesis and vessel stability. FASEB J 23:153-163.
99. Zhou M, Sutliff RL, Paul RJ, Lorenz JN, Hoying JB, Haudenschild CC, Yin M, Coffin JD, Kong L, Kranias EG, Luo W, Boivin GP, Duffy JJ, Pawlowski SA, Doetschman T. 1998. Fibroblast growth factor 2 control of vascular tone. Nat Med 4:201-207.