Astrocyte hypoxic response is essential for pathological but not developmental angiogenesis of the retina

GLIA

Volumn 58, Issue 10, 2010, Pages 1177-1185

  Weidemann, Alexander ^a   Krohne, Tim U ^b   Aguilar, Edith ^b   Kurihara, Toshihide ^a,b   Takeda, Norihiko ^a   Dorrell, Michael I ^b   Simon, M Celeste ^c   Haase, Volker H ^d   Friedlander, Martin ^b   Johnson, Randall S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Astrocytes; Hypoxia inducible factor; Hypoxic response; Retinal angiogenesis; Vascular endothelial growth factor

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; VASCULOTROPIN; VON HIPPEL LINDAU PROTEIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL HYPOXIA; CONTROLLED STUDY; ENDOTHELIUM CELL; GLIA CELL; IN VIVO STUDY; MOUSE; NERVE CELL GROWTH; NONHUMAN; PRIORITY JOURNAL; RETINA; RETINA BLOOD VESSEL; RETINA NEOVASCULARIZATION; RETINOPATHY;

ANIMALS; ANOXIA; ASTROCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; DISEASE MODELS, ANIMAL; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; ISCHEMIA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; RETINA; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 77954350645     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20997     Document Type: Article

References (45)

1. 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 USA 92:10457-10461.
2. Alon T, Hemo I, Itin A, Pe'er J, Stone J, Keshet E. 1995. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med 1:1024-1028.
3. Arjamaa O, Nikinmaa M. 2006. Oxygen-dependent diseases in the retina: Role of hypoxia-inducible factors. Exp Eye Res 83:473-483.
4. Bajenaru ML, Zhu Y, Hedrick NM, Donahoe J, Parada LF, Gutmann DH. 2002. Astrocyte-specific inactivation of the neurofibromatosis 1 gene (NF1) is insufficient for astrocytoma formation. Mol Cell Biol 22:5100-5113.
5. Banin E, Dorrell MI, Aguilar E, Ritter MR, Aderman CM, Smith AC, Friedlander J, Friedlander M. 2006. T2-TrpRS inhibits preretinal neovascularization and enhances physiological vascular regrowth in OIR as assessed by a new method of quantification. Invest Ophthalmol Vis Sci 47:2125-2134.
6. Blanks JC, Johnson LV. 1986. Vascular atrophy in the retinal degenerative rd mouse. J Comp Neurol 254:543-553.
7. Boutin AT, Weidemann A, Fu Z, Mesropian L, Gradin K, Jamora C, Wiesener M, Eckardt KU, Koch CJ, Ellies LG, Haddad G, Haase VH, Simon MC, Poellinger L, Powell FL, Johnson RS. 2008. Epidermal sensing of oxygen is essential for systemic hypoxic response. Cell 133:223-234.
8. Butler JM, Guthrie SM, Koc M, Afzal A, Caballero S, Brooks HL, Mames RN, Segal MS, Grant MB, Scott EW. 2005. SDF-1 is both necessary and sufficient to promote proliferative retinopathy. J Clin Invest 115:86-93. (Pubitemid 40385508)
9. Chan-Ling T, Gock B, Stone J. 1995. The effect of oxygen on vasoformative cell division. Evidence that 'physiological hypoxia' is the stimulus for normal retinal vasculogenesis. Invest Ophthalmol Vis Sci 36:1201-1214.
10. Chen J, Connor KM, Aderman CM, Willett KL, Aspegren OP, Smith LE. 2009. Suppression of retinal neovascularization by erythropoietin siRNA in a mouse model of proliferative retinopathy. Invest Ophthalmol Vis Sci 50:1329-1335.
11. Darland DC, Massingham LJ, Smith SR, Piek E, Saint-Geniez M, D'Amore PA. 2003. Pericyte production of cell-associated VEGF is differentiation-dependent and is associated with endothelial survival. Dev Biol 264:275-288.
12. Ding K, Scortegagna M, Seaman R, Birch DG, Garcia JA. 2005. Retinal disease in mice lacking hypoxia-inducible transcription factor-2αlpha. Invest Ophthalmol Vis Sci 46:1010-1016.
13. Dioum EM, Clarke SL, Ding K, Repa JJ, Garcia JA. 2008. HIF-2α-haploinsufficient mice have blunted retinal neovascularization due to impaired expression of a proangiogenic gene battery. Invest Ophthalmol Vis Sci 49:2714-2720.
14. 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. (Pubitemid 35334359)
15. 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.
16. Dorrell MI, Friedlander M. 2006. Mechanisms of endothelial cell guidance and vascular patterning in the developing mouse retina. Prog Retin Eye Res 25:277-295.
17. Gariano RF. 2003. Cellular mechanisms in retinal vascular development. Prog Retin Eye Res 22:295-306.
18. Gariano RF, Hu D, Helms J. 2006. Expression of angiogenesis-related genes during retinal development. Gene Expr Patterns 6:187-192. (Pubitemid 43071914)
19. Gerber HP, Hillan KJ, Ryan AM, Kowalski J, Keller GA, Rangell L, Wright BD, Radtke F, Aguet M, Ferrara N. 1999. VEGF is required for growth and survival in neonatal mice. Development 126:1149-1159.
20. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C. 2003. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161:1163-1177.
21. Grimm C, Hermann DM, Bogdanova A, Hotop S, Kilic U, Wenzel A, Kilic E, Gassmann M. 2005. Neuroprotection by hypoxic preconditioning: HIF-1 and erythropoietin protect from retinal degeneration. Semin Cell Dev Biol 16:531-538.
22. Gruber M, Hu CJ, Johnson RS, Brown EJ, Keith B, Simon MC. 2007. Acute postnatal ablation of Hif-2a results in anemia. Proc Natl Acad Sci USA 104:2301-2306.
23. Haase VH, Glickman JN, Socolovsky M, Jaenisch R. 2001. Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc Natl Acad Sci USA 98:1583-1588.
24. Kaelin WG Jr., Ratcliffe PJ. 2008. Oxygen sensing by metazoans: The central role of the HIF hydroxylase pathway. Mol Cell 30:393-402.
25. Liu Y, Cox SR, Morita T, Kourembanas S. 1995. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 50 enhancer. Circ Res 77:638-643.
26. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. 1999. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399:271-275.
27. Mori K, Gehlbach P, Ando A, Dyer G, Lipinsky E, Chaudhry AG, Hackett SF, Campochiaro PA. 2002. Retina-specific expression of PDGF-B versus PDGF-A: Vascular versus nonvascular proliferative retinopathy. Invest Ophthalmol Vis Sci 43:2001-2006. (Pubitemid 34587053)
28. Otani A, Dorrell MI, Kinder K, Moreno SK, Nusinowitz S, Banin E, Heckenlively J, Friedlander M. 2004. Rescue of retinal degeneration by intravitreally injected adult bone marrow-derived lineage-negative hematopoietic stem cells. J Clin Invest 114:765-774.
29. Ozaki H, Seo MS, Ozaki K, Yamada H, Yamada E, Okamoto N, Hofmann F, Wood JM, Campochiaro PA. 2000. Blockade of vascular endothelial cell growth factor receptor signaling is sufficient to completely prevent retinal neovascularization. Am J Pathol 156:697-707.
30. Pierce EA, Avery RL, Foley ED, Aiello LP, Smith LE. 1995. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci USA 92:905-909.
31. Resnikoff S, Pascolini D, Etya'ale D, Kocur I, Pararajasegaram R, Pokharel GP, Mariotti SP. 2004. Global data on visual impairment in the year 2002. Bull World Health Organ 82:844-851.
32. Ritter MR, Banin E, Moreno SK, Aguilar E, Dorrell MI, Friedlander M. 2006. Myeloid progenitors differentiate into microglia and promote vascular repair in a model of ischemic retinopathy. J Clin Invest 116:3266-3276.
33. Ryan HE, Lo J, Johnson RS. 1998. HIF-1a is required for solid tumor formation and embryonic vascularization. EMBO J 17:3005-3015. (Pubitemid 28254373)
34. Saito Y, Uppal A, Byfield G, Budd S, Hartnett ME. 2008. Activated NAD(P)H oxidase from supplemental oxygen induces neovascularization independent of VEGF in retinopathy of prematurity model. Invest Ophthalmol Vis Sci 49:1591-1598.
35. Sandercoe TM, Geller SF, Hendrickson AE, Stone J, Provis JM. 2003. VEGF expression by ganglion cells in central retina before formation of the foveal depression in monkey retina: Evidence of developmental hypoxia. J Comp Neurol 462:42-54.
36. Smith LE, Wesolowski E, McLellan A, Kostyk SK, D'Amato R, Sullivan R, D'Amore PA. 1994. Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci 35:101-111.
37. Stalmans I, Ng YS, Rohan R, Fruttiger M, Bouche A, Yuce A, Fujisawa H, Hermans B, Shani M, Jansen S, Hicklin D, Anderson DJ, Gardiner T, Hammes HP, Moons L, Dewerchin M, Collen D, Carmeliet P. 2002. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J Clin Invest 109:327-336.
38. Stevenson L, Matesanz N, Colhoun L, Edgar K, Devine A, Gardiner TA, McDonald DM. 2010. Reduced nitrooxidative stress and neural cell death suggests a protective role for microglial cells in TNFα-/- mice in ischemic retinopathy. Invest Ophthalmol Vis Sci. [Epub ahead of print].
39. Stockmann C, Doedens A, Weidemann A, Zhang N, Takeda N, Greenberg JI, Cheresh DA, Johnson RS. 2008. Deletion of vascular endothelial growth factor in myeloid cells accelerates tumorigenesis. Nature 456:814-818.
40. Stone J, Chan-Ling T, Pe'er 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.
41. Stone J, Itin A, Alon T, Pe'er J, Gnessin H, Chan-Ling T, Keshet E. 1995. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 15(7, Pt 1):4738-4747.
42. Watanabe D, Suzuma K, Matsui S, Kurimoto M, Kiryu J, Kita M, Suzuma I, Ohashi H, Ojima T, Murakami T, Kobayashi T, Masuda S, Nagao M, Yoshimura N, Takagi H. 2005. Erythropoietin as a retinal angiogenic factor in proliferative diabetic retinopathy. N Engl J Med 353:782-792. (Pubitemid 41215487)
43. Weidemann A, Johnson RS. 2008. Biology of HIF-1α. Cell Death Differ 15:621-627.
44. Weidemann A, Kerdiles YM, Knaup KX, Rafie CA, Boutin AT, Stockmann C, Takeda N, Scadeng M, Shih AY, Haase VH, et al. 2009. The glial cell response is an essential component of hypoxia-induced erythropoiesis in mice. J Clin Invest 119:3373-3383.
45. Zhu Y, Harada T, Liu L, Lush ME, Guignard F, Harada C, Burns DK, Bajenaru ML, Gutmann DH, Parada LF. 2005. Inactivation of NF1 in CNS causes increased glial progenitor proliferation and optic glioma formation. Development 132:5577-5588.