Development of astrocytes in the vertebrate eye

Developmental Dynamics

Volumn 243, Issue 12, 2014, Pages 1501-1510

  Tao, Chenqi ^a,b   Zhang, Xin ^b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Astrocyte; Bmp; Fgf; GFAP; HIF; Lif; Optic disc; Optic stalk; Pax2; Pdgf; RA; Shh; VEGF

Indexed keywords

ASTROCYTE; CELL EXPANSION; CELL PROLIFERATION; EYE DEVELOPMENT; HUMAN; MORPHOGENESIS; NERVE CELL DIFFERENTIATION; NEURORETINA; NONHUMAN; OPTIC DISK; OPTIC NERVE; PRIORITY JOURNAL; RETINA; REVIEW; VERTEBRATE; ANGIOGENESIS; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; EMBRYOLOGY; METABOLISM; PHYSIOLOGY;

VERTEBRATA;

ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; RETINA;

EID: 84924120827     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24190     Document Type: Review

References (159)

1. Adler R, Belecky-Adams TL. 2002. The role of bone morphogenetic proteins in the differentiation of the ventral optic cup. Development 129:3161-3171.
2. Allaman I, Belanger M, Magistretti PJ. 2011. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 34:76-87.
3. Armstrong RC, Harvath L, Dubois-Dalcq ME. 1990. Type 1 astrocytes and oligodendrocyte-type 2 astrocyte glial progenitors migrate toward distinct molecules. J Neurosci Res 27:400-407.
4. Bassett EA, Williams T, Zacharias AL, Gage PJ, Fuhrmann S, West-Mays JA. 2010. AP-2alpha knockout mice exhibit optic cup patterning defects and failure of optic stalk morphogenesis. Hum Mol Genet 19:1791-1804.
5. Bernardinelli Y, Muller D, Nikonenko I. 2014. Astrocyte-synapse structural plasticity. Neural Plast 2014:232105.
6. Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, Rozovsky I, Stahl N, Yancopoulos GD, Greenberg ME. 1997. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 278:477-483.
7. Burne JF, Staple JK, Raff MC. 1996. Glial cells are increased proportionally in transgenic optic nerves with increased numbers of axons. J Neurosci 16:2064-2073.
8. Butt AM, Ransom BR. 1989. Visualization of oligodendrocytes and astrocytes in the intact rat optic nerve by intracellular injection of lucifer yellow and horseradish peroxidase. Glia 2:470-475.
9. Cai Z, Feng GS, Zhang X. 2010. Temporal requirement of the protein tyrosine phosphatase Shp2 in establishing the neuronal fate in early retinal development. J Neurosci 30:4110-4119.
10. Cai Z, Grobe K, Zhang X. 2014. The role of heparan sulfate proteoglycans in optic disc and stalk morphogenesis. Dev Dyn [Epub ahead of print].
11. Cai ZG, Tao CQ, Li HG, Ladher R, Gotoh N, Feng GS, Wang F, Zhang X. 2013. Deficient FGF signaling causes optic nerve dysgenesis and ocular coloboma. Development 140:2711-2723.
12. Carbe C, Garg A, Cai Z, Li H, Powers A, Zhang X. 2013. An allelic series at the paired box gene 6 (Pax6) locus reveals the functional specificity of Pax genes. J Biol Chem 288:12130-12141.
13. Cardozo MJ, Sanchez-Arrones L, Sandonis A, Sanchez-Camacho C, Gestri G, Wilson SW, Guerrero I, Bovolenta P. 2014. Cdon acts as a Hedgehog decoy receptor during proximal-distal patterning of the optic vesicle. Nat Commun 5:4272.
14. Chan-Ling T, Chu Y, Baxter L, Weible M, Hughes S. 2009. In vivo characterization of Astrocyte Precursor Cells (APCs) and astrocytes in developing rat retinae: differentiation, proliferation, and apoptosis. Glia 57:39-53.
15. Chan-Ling T, Stone J. 1992. Degeneration of astrocytes in feline retinopathy of prematurity causes failure of the blood-retinal barrier. Invest Ophthalmol Vis Sci 33:2148-2159.
16. Chanling TL. 1994. Glial, neuronal and vascular interactions in the mammalian retina. Prog Retin Eye Res 13:357-389.
17. Chen SY, Li H, Gaudenz K, Paulson A, Guo FL, Trimble R, Peak A, Seidel C, Deng CX, Furuta Y, Xie T. 2013. Defective FGF signaling causes coloboma formation and disrupts retinal neurogenesis. Cell Res 23:254-273.
18. Chiang C, Ying LTT, Lee E, Young KE, Corden JL, Westphal H, Beachy PA. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383:407-413.
19. Chow RL, Lang RA. 2001. Early eye development in vertebrates. Annu Rev Cell Dev Biol 17:255-296.
20. Chu Y, Hughes S, Chan-Ling T. 2001. Differentiation and migration of astrocyte precursor cells and astrocytes in human fetal retina: relevance to optic nerve coloboma. FASEB J 15:2013-2015.
21. Culican SM, Baumrind NL, Yamamoto M, Pearlman AL. 1990. Cortical Radial Glia - Identification in Tissue-Culture and Evidence for Their Transformation to Astrocytes. J Neurosci 10:684-692.
22. Dakubo GD, Beug ST, Mazerolle CJ, Thurig S, Wang YP, Wallace VA. 2008. Control of glial precursor cell development in the mouse optic nerve by sonic hedgehog from retinal ganglion cells. Brain Res 1228:27-42.
23. Dakubo GD, Wallace VA. 2004. Hedgehogs and retinal ganglion cells: organizers of the mammalian retina. Neuroreport 15:479-482.
24. Dakubo GD, Wang YP, Mazerolle C, Campsall K, McMahon AP, Wallace VA. 2003. Retinal ganglion cell-derived sonic hedgehog signaling is required for optic disc and stalk neuroepithelial cell development. Development 130:2967-2980.
25. De Keyser J, Mostert JP, Koch MW. 2008. Dysfunctional astrocytes as key players in the pathogenesis of central nervous system disorders. J Neurol Sci 267:3-16.
26. Dickman ED, Thaller C, Smith SM. 1997. Temporally-regulated retinoic acid depletion produces specific neural crest, ocular and nervous system defects. Development 124:3111-3121.
27. Dimou L, Simon C, Kirchhoff F, Takebayashi H, Gotz M. 2008. Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J Neurosci 28:10434-10442.
28. Dorrell MI, Aguilar E, Friedlander M. 2002. Retinal vascular development is mediated by endothelial filopodia, a preexisting astrocytic template and specific R-cadherin adhesion. Invest Ophthalmol Vis Sci 43:3500-3510.
29. Dorrell MI, Aguilar E, Jacobson R, Trauger SA, Friedlander J, Siuzdak G, Friedlander M. 2010. Maintaining retinal astrocytes normalizes revascularization and prevents vascular pathology associated with oxygen-induced retinopathy. Glia 58:43-54.
30. Duan LJ, Takeda K, Fong GH. 2014. Hypoxia inducible factor-2 alpha regulates the development of retinal astrocytic network by maintaining adequate supply of astrocyte progenitors. Plos One 9:e84736.
31. Dutton GN. 2004. Congenital disorders of the optic nerve: excavations and hypoplasia. Eye (Lond) 18:1038-1048.
32. Edwards MM, Mammadova-Bach E, Alpy F, Klein A, Hicks WL, Roux M, Simon-Assmann P, Smith RS, Orend G, Wu J, Peachey NS, Naggert JK, Lefebvre O, Nishina PM. 2010. Mutations in Lama1 disrupt retinal vascular development and inner limiting membrane formation. J Biol Chem 285:7697-7711.
33. Edwards MM, McLeod DS, Li RZ, Grebe R, Bhutto I, Mu XQ, Lutty GA. 2012. The deletion of Math5 disrupts retinal blood vessel and glial development in mice. Exp Eye Res 96:147-156.
34. Ells AL, Gole GA, Hildebrand PL, Ingram A, Wilson CM, Williams RG. 2013. Posterior to the ridge laser treatment for severe stage 3 retinopathy of prematurity. Eye 27:525-530.
35. Evans AL, Gage PJ. 2005. Expression of the homeobox gene Pitx2 in neural crest is required for optic stalk and ocular anterior segment development. Hum Mol Genet 14:3347-3359.
36. Fancy SPJ, Zhao C, Franklin RJM. 2004. Increased expression of Nkx2.2 and Olig2 identifies reactive oligodendrocyte progenitor cells responding to demyelination in the adult CNS. Mol Cell Neurosci 27:247-254.
37. Ffrench-Constant C, Miller RH, Burne JF, Raff MC. 1988. Evidence that migratory oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells are kept out of the rat retina by a barrier at the eye-end of the optic nerve. J Neurocytol 17:13-25.
38. Ffrenchconstant C, Raff MC. 1986. The oligodendrocyte-type-2 astrocyte cell lineage is specialized for myelination. Nature 323:335-338.
39. Fields RD, Stevens-Graham B. 2002. New insights into neuron-glia communication. Science 298:556-562.
40. Friedlander M. 2007. Fibrosis and diseases of the eye. J Clin Invest 117:576-586.
41. Fruttiger M, Calver AR, Kruger WH, Mudhar HS, Michalovich D, Takakura N, Nishikawa SI, Richardson WD. 1996. PDGF mediates a neuron-astrocyte interaction in the developing retina. Neuron 17:1117-1131.
42. Fuhrmann S. 2010. Eye morphogenesis and patterning of the optic vesicle. Curr Top Dev Biol 93:61-84.
43. Fulton BP, Burne JF, Raff MC. 1991. Glial cells in the rat optic nerve. The search for the type-2 astrocyte. Ann N Y Acad Sci 633:27-34.
44. Gage PJ, Qian M, Wu D, Rosenberg KI. 2008. The canonical Wnt signaling antagonist DKK2 is an essential effector of PITX2 function during normal eye development. Dev Biol 317:310-324.
45. Galli R, Pagano SF, Gritti A, Vescovi AL. 2000. Regulation of neuronal differentiation in human CNS stem cell progeny by leukemia inhibitory factor. Dev Neurosci 22:86-95.
46. Gardner TW, Lieth E, Khin SA, Barber AJ, Bonsall DJ, Lesher T, Rice K, Brennan WA. 1997. Astrocytes increase barrier properties and ZO-1 expression in retinal vascular endothelial cells. Invest Ophthalmol Vis Sci 38:2423-2427.
47. Gariano RF. 2003. Cellular mechanisms in retinal vascular development. P Retin Eye Res 22:295-306.
48. Gariano RF. 2010. Special features of human retinal angiogenesis. Eye (Lond) 24:401-407.
49. Gnanaguru G, Bachay G, Biswas S, Pinzon-Duarte G, Hunter DD, Brunken WJ. 2013. Laminins containing the beta 2 and gamma 3 chains regulate astrocyte migration and angiogenesis in the retina. Development 140:2050-2060.
50. Herrera J, Yang H, Zhang SC, Proschel C, Tresco P, Duncan ID, Luskin M, Mayer-Proschel M. 2001. Embryonic-derived glial-restricted precursor cells (GRP cells) can differentiate into astrocytes and oligodendrocytes in vivo. Exp Neurol 171:11-21.
51. Heyer J, Escalante-Alcalde D, Lia M, Boettinger E, Edelmann W, Stewart CL, Kucherlapati R. 1999. Postgastrulation Smad2-deficient embryos show defects in embryo turning and anterior morphogenesis. Proc Natl Acad Sci U S A 96:12595-12600.
52. Hirota S, Liu Q, Lee HS, Hossain MG, Lacy-Hulbert A, McCarty JH. 2011. The astrocyte-expressed integrin alphavbeta8 governs blood vessel sprouting in the developing retina. Development 138:5157-5166.
53. Hollander H, Makarov F, Dreher Z, van Driel D, Chan-Ling TL, Stone J. 1991. Structure of the macroglia of the retina: sharing and division of labour between astrocytes and Muller cells. J Comp Neurol 313:587-603.
54. Horsford DJ, Nguyen MT, Sellar GC, Kothary R, Arnheiter H, McInnes RR. 2005. Chx10 repression of Mitf is required for the maintenance of mammalian neuroretinal identity. Development 132:177-187.
55. Huh S, Hatini V, Marcus RC, Li SC, Lai E. 1999. Dorsal-ventral patterning defects in the eye of BF-1-deficient mice associated with a restricted loss of shh expression. Dev Biol 211:53-63.
56. Huxlin KR, Sefton AJ, Furby JH. 1992. The Origin and Development of Retinal Astrocytes in the Mouse. J Neurocytol 21:530-544.
57. Jean D, Ewan K, Gruss P. 1998. Molecular regulators involved in vertebrate eye development. Mech Dev 76:3-18.
58. Kaur C, Sivakumar V, Yong Z, Lu J, Foulds WS, Ling EA. 2007. Blood-retinal barrier disruption and ultrastructural changes in the hypoxic retina in adult rats: the beneficial effect of melatonin administration. J Pathol 212:429-439.
59. Kang SH, Fukaya M, Yang JK, Rothstein JD, Bergles DE. 2010. NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 68:668-681.
60. Kettenmann H, Ransom BR. 2005. Neuroglia. New York: Oxford University Press. xix, 601 p.
61. Kim JH, Yu YS, Kim KW, Kim JH. 2010. Impaired retinal vascular development in anencephalic human fetus. Histochem Cell Biol 134:277-284.
62. Kleihues P, Sobin LH. 2000. World Health Organization classification of tumors. Cancer 88:2887.
63. Koblar SA, Turnley AM, Classon BJ, Reid KL, Ware CB, Cheema SS, Murphy M, Bartlett PF. 1998. Neural precursor differentiation into astrocytes requires signaling through the leukemia inhibitory factor receptor. Proc Natl Acad Sci U S A 95:3178-3181.
64. Kubota Y, Hirashima M, Kishi K, Stewart CL, Suda T. 2008. Leukemia inhibitory factor regulates microvessel density by modulating oxygen-dependent VEGF expression in mice. J Clin Invest 118:2393-2403.
65. Kumar S, Duester G. 2010. Retinoic acid signaling in perioptic mesenchyme represses Wnt signaling via induction of Pitx2 and Dkk2. Dev Biol 340:67-74.
66. Kuwabara T. 1975. Development of the optic nerve of the rat. Invest Ophthalmol 14:732-745.
67. Lavialle M, Aumann G, Anlauf E, Prols F, Arpin M, Derouiche A. 2011. Structural plasticity of perisynaptic astrocyte processes involves ezrin and metabotropic glutamate receptors. Proc Natl Acad Sci U S A 108:12915-12919.
68. Ligon KL, Fancy SPJ, Franklin RJM, Rowitch DH. 2006. Olig gene function in CNS development and disease. Glia 54:1-10.
69. Ling TL, Mitrofanis J, Stone J. 1989. Origin of retinal astrocytes in the rat - evidence of migration from the optic-nerve. J Comp Neurol 286:345-352.
70. Ling TL, Stone J. 1988. The development of astrocytes in the cat retina: evidence of migration from the optic nerve. Brain Res Dev Brain Res 44:73-85.
71. Liu Y, Han SSW, Wu YY, Tuohy TMF, Xue HP, Cai JL, Back SA, Sherman LS, Fischer I, Rao MS. 2004. CD44 expression identifies astrocyte-restricted precursor cells. Dev Biol 276:31-46.
72. Lowe LA, Yamada S, Kuehn MR. 2001. Genetic dissection of nodal function in patterning the mouse embryo. Development 128:1831-1843.
73. Ly A, Yee P, Vessey KA, Phipps JA, Jobling AI, Fletcher EL. 2011. Early inner retinal astrocyte dysfunction during diabetes and development of hypoxia, retinal stress, and neuronal functional loss. Invest Ophthalmol Vis Sci 52:9316-9326.
74. Macdonald R, Barth KA, Xu QL, Holder N, Mikkola I, Wilson SW. 1995. Midline signaling is required for pax gene-regulation and patterning of the eyes. Development 121:3267-3278.
75. Markiewicz I, Lukomska B. 2006. The role of astrocytes in the physiology and pathology of the central nervous system. Acta Neurobiol Exp (Wars) 66:343-358.
76. Martinez-Morales JR, Wittbrodt J. 2009. Shaping the vertebrate eye. Curr Opin Genet Dev 19:511-517.
77. Matt N, Ghyselinck NB, Pellerin I, Dupe V. 2008. Impairing retinoic acid signalling in the neural crest cells is sufficient to alter entire eye morphogenesis. Dev Biol 320:140-148.
78. Mercier S, David V, Ratie L, Gicquel I, Odent S, Dupe V. 2013. NODAL and SHH dose-dependent double inhibition promotes an HPE-like phenotype in chick embryos. Dis Models Mech 6:537-543.
79. Meyer DB. 1977. Book review of 'Handbook of Sensory Physiology Volume V (2) Auditory System' by W. D. Keidel and W. D. Neff, Psycholl Med 7:545-545, doi:10.1017/S0033291700004566.
80. Mi H, Barres BA. 1999. Purification and characterization of astrocyte precursor cells in the developing rat optic nerve. J Neurosci 19:1049-1061.
81. Mi HY, Haeberle H, Barres BA. 2001. Induction of astrocyte differentiation by endothelial cells. J Neurosci 21:1538-1547.
82. Miller RH, David S, Patel R, Abney ER, Raff MC. 1985. A quantitative immunohistochemical study of macroglial cell-development in the rat optic-nerve - in vivo evidence for 2 distinct astrocyte lineages. Dev Biol 111:35-41.
83. Miller RH, Ffrenchconstant C, Raff MC. 1989. The macroglial cells of the rat optic-nerve. Ann Rev Neurosci 12:517-534.
84. Mitchell P, Wang JJ, Wong TY, Smith W, Klein R, Leeder SR. 2005. Retinal microvascular signs and risk of stroke and stroke mortality. Neurology 65:1005-1009.
85. Miyawaki T, Uemura A, Dezawa M, Yu RT, Ide C, Nishikawa S, Honda Y, Tanabe Y, Tanabe T. 2004. Tlx, an orphan nuclear receptor, regulates cell numbers and astrocyte development in the developing retina. J Neurosci 24:8124-8134.
86. Molofsky AV, Krencik R, Ullian EM, Tsai HH, Deneen B, Richardson WD, Barres BA, Rowitch DH. 2012. Astrocytes and disease: a neurodevelopmental perspective. Genes Dev 26:891-907.
87. Morcillo J, Martinez-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.
88. Mudhar HS, Pollock RA, Wang C, Stiles CD, Richardson WD. 1993. PDGF and its receptors in the developing rodent retina and optic nerve. Development 118:539-552.
89. Mui SH, Kim JW, Lemke G, Bertuzzi S. 2005. Vax genes ventralize the embryonic eye. Genes Dev 19:1249-1259.
90. Muller F, Albert S, Blader P, Fischer N, Hallonet M, Strahle U. 2000. Direct action of the Nodal-related signal Cyclops in induction of sonic hedgehog in the ventral midline of the CNS. Development 127:3889-3897.
91. Nakagaito Y, Yoshida T, Satoh M, Takeuchi M. 1995. Effects of leukemia inhibitory factor on the differentiation of astrocyte progenitor cells from embryonic mouse cerebral hemispheres. Brain Res Dev Brain Res 87:220-223.
92. Nakamura-Ishizu A, Kurihara T, Okuno Y, Ozawa Y, Kishi K, Goda N, Tsubota K, Okano H, Suda T, Kubota Y. 2012. The formation of an angiogenic astrocyte template is regulated by the neuroretina in a HIF-1-dependent manner. Deve Biol 363:106-114.
93. Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, Miyazono K, Taga T. 1999. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 284:479-482.
94. Nakatsuji Y, Miller RH. 2001. Density dependent modulation of cell cycle protein expression in astrocytes. J Neurosci Res 66:487-496.
95. Nasrallah I, Golden JA. 2001. Brain, eye, and face defects as a result of ectopic localization of Sonic Hedgehog protein in the developing rostral neural tube. Teratology 64:107-113.
96. Nguyen M, Arnheiter H. 2000. Signaling and transcriptional regulation in early mammalian eye development: a link between FGF and MITF. Development 127:3581-3591.
97. Nomura M, Li E. 1998. Smad2 role in mesoderm formation, left-right patterning and craniofacial development. Nature 393:786-790.
98. Orentas DM, Miller RH. 1996. A novel form of migration of glial precursors. Glia 16:27-39.
99. Otteson DC, Shelden E, Jones JM, Kameoka J, Hitchcock PF. 1998. Pax2 expression and retinal morphogenesis in the normal and Krd mouse. Dev Biol 193:209-224.
100. Patton N, Aslam T, MacGillivray T, Pattie A, Deary IJ, Dhillon B. 2005. Retinal vascular image analysis as a potential screening tool for cerebrovascular disease: a rationale based on homology between cerebral and retinal microvasculatures. J Anat 206:319-348.
101. Pringle NP, Guthrie S, Lumsden A, Richardson WD. 1998. Dorsal spinal cord neuroepithelium generates astrocytes but not oligodendrocytes. Neuron 20:883-893.
102. Pringle NP, Mudhar HS, Collarini EJ, Richardson WD. 1992. Pdgf Receptors in the rat CNS - during late neurogenesis, Pdgf alpha-receptor expression appears to be restricted to glial-cells of the oligodendrocyte lineage. Development 115:535-551.
103. Purrello VS, Cormaci G, Denaro L, Reale S, Costa A, Lalicata C, Sabbatini M, Marchetti B, Avola R. 2002. Effect of growth factors on nuclear and mitochondrial ADP-ribosylation processes during astroglial cell development and aging in culture. Mech Ageing Dev 123:511-520.
104. Raff MC, Abney ER, Cohen J, Lindsay R, Noble M. 1983. Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides, and growth characteristics. J Neurosci 3:1289-1300.
105. Raff MC, Abney ER, Miller RH. 1984. Two glial cell lineages diverge prenatally in rat optic nerve. Dev Biol 106:53-60.
106. Ramón y Cajal S. 1893. La rétinue des vertébrés. La Cellule 9:17-257.
107. Rao MS, Noble M, Mayer-Proschel M. 1998. A tripotential glial precursor cell is present in the developing spinal cord. Proc Natl Acad Sci U S A 95:3996-4001.
108. Redwine JM, Armstrong RC. 1998. In vivo proliferation of oligodendrocyte progenitors expressing PDGFalphaR during early remyelination. J Neurobiol 37:413-428.
109. Reichenbach A, Wohlrab F. 1986. Morphometric parameters of Muller (Glial) cells dependent on their topographic localization in the nonmyelinated part of the rabbit retina - a consideration of functional-aspects of radial glia. J Neurocytol 15:451-459.
110. Reneker LW, Overbeek PA. 1996. Lens-specific expression of PDGF-A in transgenic mice results in retinal astrocytic hamartomas. Invest Ophthalmol Vis Sci 37:2455-2466.
111. Richards LJ, Kilpatrick TJ, Dutton R, Tan SS, Gearing DP, Bartlett PF, Murphy M. 1996. Leukaemia inhibitory factor or related factors promote the differentiation of neuronal and astrocytic precursors within the developing murine spinal cord. Eur J Neurosci 8:291-299.
112. Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A, Kessaris N, Richardson WD. 2008. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 11:1392-1401.
113. Rompani SB, Cepko CL. 2010. A common progenitor for retinal astrocytes and oligodendrocytes. J Neurosci 30:4970-4980.
114. 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.
115. Rungger-Brandle E, Dosso AA, Leuenberger PM. 2000. Glial reactivity, an early feature of diabetic retinopathy. Invest Ophthalmol Vis Sci 41:1971-1980.
116. Ruzhynsky VA, Furimsky M, Park DS, Wallace VA, Slack RS. 2009. E2F4 is required for early eye patterning. Dev Neurosci 31:238-246.
117. Sanek NA, Taylor AA, Nyholm MK, Grinblat Y. 2009. Zebrafish zic2a patterns the forebrain through modulation of Hedgehog-activated gene expression. Development 136:3791-3800.
118. Sapieha P, Sirinyan M, Hamel D, Zaniolol K, Joyal JS, Cho JH, Honore JC, Kermorvant-Duchemin E, Varma DR, Tremblay S, Leduc M, Rihakova L, Hardy P, Klein WH, Mu XQ, Mamer O, Lachapelle P, Di Polo A, Beausiour C, Andelfinger G, Mitchell G, Sennlaub F, Chemtob S. 2008. The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis. Nat Med 14:1067-1076.
119. Schmechel DE, Rakic P. 1979. Arrested proliferation of radial glial cells during mid-gestation in Rhesus-monkey. Nature 277:303-305.
120. Schnitzer J. 1987. Retinal astrocytes - their restriction to vascularized parts of the mammalian retina. Neurosci Lett 78:29-34.
121. Schwarz M, Cecconi F, Bernier G, Andrejewski N, Kammandel B, Wagner M, Gruss P. 2000. Spatial specification of mammalian eye territories by reciprocal transcriptional repression of Pax2 and Pax6. Development 127:4325-4334.
122. Scott A, Fruttiger M. 2010. Oxygen-induced retinopathy: a model for vascular pathology in the retina. Eye 24:416-421.
123. Sehgal R, Sheibani N, Rhodes SJ, Adams TLB. 2009. BMP7 and SHH regulate Pax2 in mouse retinal astrocytes by relieving TLX repression. Deve Biol 332:429-443.
124. Skoff RP. 1990. Gliogenesis in rat optic nerve: astrocytes are generated in a single wave before oligodendrocytes. Dev Biol 139:149-168.
125. Small RK, Riddle P, Noble M. 1987. Evidence for migration of oligodendrocyte type-2 astrocyte progenitor cells into the developing rat optic-nerve. Nature 328:155-157.
126. Smith LEH. 2004. Pathogenesis of retinopathy of prematurity. Growth Horm IGF Res 14:S140-S144.
127. Somjen GG. 1988. Nervenkitt: notes on the history of the concept of neuroglia. Glia 1:2-9.
128. Steinmetz RL, Brooks HL. 2002. Diode laser photocoagulation to the ridge and avascular retina in threshold retinopathy of prematurity. Retina 22:48-52.
129. Stenzel D, Lundkvist A, Sauvaget D, Busse M, Graupera M, van der Flier A, Wijelath ES, Murray J, Sobel M, Costell M, Takahashi S, Fassler R, Yamaguchi Y, Gutmann DH, Hynes RO, Gerhardt H. 2011. Integrin-dependent and -independent functions of astrocytic fibronectin in retinal angiogenesis. Development 138:4451-4463.
130. Stone J, ChanLing T, Peer J, Itin A, Gnessin H, Keshet E. 1996. Roles of vascular endothelial growth factor and astrocyte degeneration in the genesis of retinopathy of prematurity. Invest Ophthalmol Vis Sci 37:290-299.
131. Stone J, Dreher Z. 1987. Relationship between astrocytes, ganglion-cells and vasculature of the retina. J Comp Neurol 255:35-49.
132. Stone J, Itin A, Alon T, Peer J, Gnessin H, Chanling T, Keshet E. 1995. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth-factor (Vegf) expression by neuroglia. J Neurosci 15:4738-4747.
133. Take-uchi M, Clarke JDW, Wilson SW. 2003. Hedgehog signalling maintains the optic stalk-retinal interface through the regulation of Vax gene activity. Development 130:955-968.
134. Tang K, Xie X, Park JI, Jamrich M, Tsai S, Tsai MJ. 2010. COUP-TFs regulate eye development by controlling factors essential for optic vesicle morphogenesis. Development 137:725-734.
135. Tasman W, Patz A, McNamara JA, Kaiser RS, Trese MT, Smith BT. 2006. Retinopathy of prematurity: the life of a lifetime disease. Am J Ophthalmol 141:167-174.
136. Torres M, Gomez-Pardo E, Gruss P. 1996. Pax2 contributes to inner ear patterning and optic nerve trajectory. Development 122:3381-3391.
137. Tout S, Chan-Ling T, Hollander H, Stone J. 1993. The role of Muller cells in the formation of the blood-retinal barrier. Neuroscience 55:291-301.
138. Tsai HH, Miller RH. 2002. Glial cell migration directed by axon guidance cues. Trends Neurosci 25:173-175.
139. Uemura A, Kusuhara S, Wiegand SJ, Yu RT, Nishikawa S. 2006. Tlx acts as a proangiogenic switch by regulating extracellular assembly of fibronectin matrices in retinal astrocytes. J Clin Invest 116:369-377.
140. Ulshafer RJ, Clavert A. 1979. Cell death and optic fiber penetration in the optic stalk of the chick. J Morphol 162:67-76.
141. Varlet I, Collignon J, Robertson EJ. 1997. nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation. Development 124:1033-1044.
142. Volterra A, Meldolesi J. 2005. Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6:626-640.
143. Wallace VA, Raff MC. 1999. A role for Sonic hedgehog in axon-to-astrocyte signalling in the rodent optic nerve. Development 126:2901-2909.
144. Wang Y, Dakubo GD, Thurig S, Mazerolle CJ, Wallace VA. 2005a. Retinal ganglion cell-derived sonic hedgehog locally controls proliferation and the timing of RGC development in the embryonic mouse retina. Development 132:5103-5113.
145. Wang Y, Rattner A, Zhou Y, Williams J, Smallwood PM, Nathans J. 2012. Norrin/Frizzled4 signaling in retinal vascular development and blood brain barrier plasticity. Cell 151:1332-1344.
146. Wang YP, Dakubo GD, Thurig S, Mazerolle CJ, Wallace VA. 2005b. Retinal ganglion cell-derived sonic hedgehog locally controls proliferation and the timing of RGC development in the embryonic mouse retina. Development 132:5103-5113.
147. Watanabe T, Raff MC. 1988. Retinal astrocytes are immigrants from the optic-nerve. Nature 332:834-837.
148. Weidemann A, Krohne TU, Aguilar E, Kurihara T, Takeda N, Dorrell MI, Simon MC, Haase VH, Friedlander M, Johnson RS. 2010. Astrocyte hypoxic response is essential for pathological but not developmental angiogenesis of the retina. Glia 58:1177-1185.
149. Xie J, Aszterbaum M, Zhang X, Bonifas JM, Zachary C, Epstein E, McCormick F. 2001. A role of PDGFRalpha in basal cell carcinoma proliferation. Proc Natl Acad Sci U S A 98:9255-9259.
150. Yang XH. 2004. Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis. Semin Cell Dev Biol 15:91-103.
151. Yoshida T, Satoh M, Nakagaito Y, Kuno H, Takeuchi M. 1993. Cytokines affecting survival and differentiation of an astrocyte progenitor cell line. Brain Res Dev Brain Res 76:147-150.
152. Zhang R, Huang H, Cao P, Wang Z, Chen Y, Pan Y. 2013. Sma- and Mad-related protein 7 (Smad7) is required for embryonic eye development in the mouse. J Biol Chem 288:10275-10285.
153. Zhang W, Mulieri PJ, Gaio U, Bae GU, Krauss RS, Kang JS. 2009. Ocular abnormalities in mice lacking the immunoglobulin superfamily member Cdo. FEBS J 276:5998-6010.
154. Zhang Y, Stone J. 1997. Role of astrocytes in the control of developing retinal vessels. Invest Ophthalmol Vis Sci 38:1653-1666.
155. Zhao L, Zevallos SE, Rizzoti K, Jeong Y, Lovell-Badge R, Epstein DJ. 2012. Disruption of SoxB1-dependent sonic hedgehog expression in the hypothalamus causes septo-optic dysplasia. Dev Cell 22:585-596.
156. Zhu X, Hill RA, Dietrich D, Komitova M, Suzuki R, Nishiyama A. 2011. Age-dependent fate and lineage restriction of single NG2 cells. Development 138:745-753.
157. Zhu X, Hill RA, Nishiyama A. 2008a. NG2 cells generate oligodendrocytes and gray matter astrocytes in the spinal cord. Neuron Glia Biol 4:19-26.
158. Zhu XQ, Bergles DE, Nishiyama A. 2008b. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135:145-157.
159. Zuercher J, Fritzsche M, Feil S, Mohn L, Berger W. 2012. Norrin stimulates cell proliferation in the superficial retinal vascular plexus and is pivotal for the recruitment of mural cells. Hum Mol Genet 21:2619-2630.