Ischaemia-induced retinal neovascularisation and diabetic retinopathy in mice with conditional knockout of hypoxia-inducible factor-1 in retinal Müller cells

Diabetologia

Volumn 54, Issue 6, 2011, Pages 1554-1566

  Lin, M ^a,c,d   Chen, Y ^a   Jin, J ^a   Hu, Y ^a   Zhou, K K ^a   Zhu, M ^a,b   Le, Y Z ^a,b   Ge, J ^c,d,f   Johnson, R S ^e   Ma, J X ^a,b,f  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^c State Key Laboratory of Ophthalmology   (China)

^d SUN YAT SEN UNIVERSITY   (China)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f NONE   (China)

Author keywords

Angiogenesis; Diabetic retinopathy; Hypoxia; Ischaemia; M ller cells; Retina

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; INTERCELLULAR ADHESION MOLECULE 1; OXYGEN; RECOMBINASE; STREPTOZOCIN; VASCULOTROPIN; CRE RECOMBINASE; HIF1A PROTEIN, MOUSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTEGRASE; VASCULOTROPIN A;

ANGIOGRAPHY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL GENE; DIABETES MELLITUS; DIABETIC RETINOPATHY; ENZYME METABOLISM; HIF 1ALPHA GENE; HISTOPATHOLOGY; INFLAMMATION; LEUCOSTASIS; LEUKOCYTE ADHERENCE; LEUKOCYTE COUNT; MOUSE; MUELLER CELL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RETINA; RETINA ISCHEMIA; RETINA NEOVASCULARIZATION; RETINOPATHY; VISUAL DISORDER; ANIMAL; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; EXPERIMENTAL DIABETES MELLITUS; GENETICS; ISCHEMIA; LEUKOSTASIS; MALE; METABOLISM; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; RADIOGRAPHY; RETINA BLOOD VESSEL;

ANGIOGRAPHY; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; DISEASE MODELS, ANIMAL; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTEGRASES; INTERCELLULAR ADHESION MOLECULE-1; ISCHEMIA; LEUKOSTASIS; MALE; MICE; MICE, KNOCKOUT; RETINA; RETINAL NEOVASCULARIZATION; RETINAL VESSELS; STREPTOZOCIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 80052554460     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-011-2081-0     Document Type: Article

References (49)

1. Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438:932-936
2. Scott A, Fruttiger M (2010) Oxygen-induced retinopathy: a model for vascular pathology in the retina. Eye (Lond) 24:416-421
3. Ke Q, Costa M (2006) Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 70:1469-1480
4. Rey S, Semenza GL (2010) Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc Res 86:236-242
5. Loboda A, Jozkowicz A, Dulak J (2010) HIF-1 and HIF-2 transcription factors - similar but not identical. Mol Cells 29:435-442
6. 2 tension. Proc Natl Acad Sci USA 92:5510-5514
7. Maxwell PH, Wiesener MS, Chang GW et al (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399:271-275 (Pubitemid 29246458)
8. Kamura T, Sato S, Iwai K, Czyzyk-Krzeska M, Conaway RC, Conaway JW (2000) Activation of HIF1alpha ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc Natl Acad Sci USA 97:10430-10435
9. Ivan M, Kondo K, Yang H et al (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:464-468 (Pubitemid 32335941)
10. 2- regulated prolyl hydroxylation. Science 292:468-472
11. Yu F, White SB, Zhao Q, Lee FS (2001) HIF-1alpha binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc Natl Acad Sci USA 98:9630-9635 (Pubitemid 32769354)
12. Epstein AC, Gleadle JM, McNeill LA et al (2001) C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107:43-54
13. Bruick RK, McKnight SL (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294:1337-1340 (Pubitemid 33063099)
14. Semenza GL (2007) Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE 2007: cm8
15. Bai Y, Ma JX, Guo J et al (2009) Muller cell-derived VEGF is a significant contributor to retinal neovascularization. J Pathol 219:446-454
16. Ueki Y, Ash JD, Zhu M, Zheng L, Le YZ (2009) Expression of Cre recombinase in retinal Muller cells. Vis Res 49:615-621
17. Thiersch M, Lange C, Joly S et al (2009) Retinal neuroprotection by hypoxic preconditioning is independent of hypoxia-inducible factor-1 alpha expression in photoreceptors. Eur J Neurosci 29:2291-2302
18. Ozaki H, Yu AY, Della N et al (1999) Hypoxia inducible factor- 1alpha is increased in ischemic retina: temporal and spatial correlation with VEGF expression. Invest Ophthalmol Vis Sci 40:182-189 (Pubitemid 29029587)
19. Ryan HE, Poloni M, McNulty W et al (2000) Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res 60:4010-4015 (Pubitemid 30636574)
20. Das AV, Mallya KB, Zhao X et al (2006) Neural stem cell properties of Muller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev Biol 299:283-302 (Pubitemid 44550105)
21. Chen Y, Hu Y, Moiseyev G, Zhou KK, Chen D, Ma JX (2009) Photoreceptor degeneration and retinal inflammation induced by very low-density lipoprotein receptor deficiency. Microvasc Res 78:119-127
22. Martin PM, Roon P, van Ells TK, Ganapathy V, Smith SB (2004) Death of retinal neurons in streptozotocin-induced diabetic mice. Invest Ophthalmol Vis Sci 45:3330-3336 (Pubitemid 39121873)
23. Park K, Chen Y, Hu Y et al (2009) Nanoparticle-mediated expression of an angiogenic inhibitor ameliorates ischemia-induced retinal neovascularization and diabetes-induced retinal vascular leakage. Diabetes 58:1902-1913
24. Chen Y, Moiseyev G, Takahashi Y, Ma JX (2006) RPE65 gene delivery restores isomerohydrolase activity and prevents early cone loss in Rpe65-/- mice. Invest Ophthalmol Vis Sci 47: 1177-1184 (Pubitemid 46768354)
25. Zhang D, Kaufman PL, Gao G, Saunders RA, Ma JX (2001) Intravitreal injection of plasminogen kringle 5, an endogenous angiogenic inhibitor, arrests retinal neovascularization in rats. Diabetologia 44:757-765 (Pubitemid 32846031)
26. Browning J, Wylie CK, Gole G (1997) Quantification of oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci 38:1168-1174 (Pubitemid 27227046)
27. Smith LE, Wesolowski E, McLellan A et al (1994) Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci 35:101-111 (Pubitemid 24046832)
28. Cheung N, Wong TY (2008) Diabetic retinopathy and systemic vascular complications. Prog Retin Eye Res 27:161-176
29. Cheung N, Mitchell P, Wong TY (2010) Diabetic retinopathy. Lancet 376:124-136
30. DeNiro M, Al-Halafi A, Al-Mohanna FH, Alsmadi O, Al- Mohanna FA (2010) Pleiotropic effects of YC-1 selectively inhibit pathological retinal neovascularization and promote physiological revascularization in a mouse model of oxygen-induced retinopathy. Mol Pharmacol 77:348-367
31. Adams JM, Difazio LT, Rolandelli RH et al (2009) HIF-1: a key mediator in hypoxia. Acta Physiol Hung 96:19-28
32. Aiello LP, Pierce EA, Foley ED et al (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
33. Brown DM, Kaiser PK, Michels M et al (2006) Ranibizumab vs verteporfin for neovascular age-related macular degeneration. N Engl J Med 355:1432-1444 (Pubitemid 44511558)
34. Kelly BD, Hackett SF, Hirota K et al (2003) Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1. Circ Res 93:1074-1081 (Pubitemid 37485038)
35. 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
36. Amin RH, Frank RN, Kennedy A, Eliott D, Puklin JE, Abrams GW(1997) Vascular endothelial growth factor is present in glial cells of the retina and optic nerve of human subjects with nonproliferative diabetic retinopathy. Invest Ophthalmol Vis Sci 38:36-47 (Pubitemid 27051522)
37. Miyamoto K, Khosrof S, Bursell SE et al (1999) Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc Natl Acad Sci USA 96:10836-10841 (Pubitemid 29442230)
38. Connor KM, Krah NM, Dennison RJ et al (2009) Quantification of oxygen-induced retinopathy in the mouse: a model of vessel loss, vessel regrowth and pathological angiogenesis. Nat Protoc 4:1565-1573
39. Chavez JC, Almhanna K, Berti-Mattera LN (2005) Transient expression of hypoxia-inducible factor-1 alpha and target genes in peripheral nerves from diabetic rats. Neurosci Lett 374:179-182 (Pubitemid 40128291)
40. Kondo T, Kahn CR (2004) Altered insulin signaling in retinal tissue in diabetic states. J Biol Chem 279:37997-38006 (Pubitemid 39195515)
41. Wang J, Xu X, Elliott MH, Zhu M, Le YZ (2010) Muller cell-derived VEGF is essential for diabetes-induced retinal inflammation and vascular leakage. Diabetes 59:2297-2305
42. Wright WS, McElhatten RM, Messina JE, Harris NR (2010) Hypoxia and the expression of HIF-1alpha and HIF-2alpha in the retina of streptozotocin-injected mice and rats. Exp Eye Res 90:405-412
43. Zhang SX, Ma JX, Sima J et al (2005) Genetic difference in susceptibility to the blood-retina barrier breakdown in diabetes and oxygen-induced retinopathy. Am J Pathol 166:313-321 (Pubitemid 40051683)
44. Le Y-Z (2011) Conditional gene targeting: dissecting the cellular mechanisms of retinal degenerations. J Ophthalmol 2011:806783
45. Nishijima K, Ng YS, Zhong L et al (2007) Vascular endothelial growth factor-A is a survival factor for retinal neurons and a critical neuroprotectant during the adaptive response to ischemic injury. Am J Pathol 171:53-67 (Pubitemid 47339226)
46. Josko J, Mazurek M (2004) Transcription factors having impact on vascular endothelial growth factor (VEGF) gene expression in angiogenesis. Med Sci Monit 10:RA89-RA98 (Pubitemid 38525095)
47. Majmundar AJ, Wong WJ, Simon MC (2010) Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 40:294-309
48. Catrina SB, Okamoto K, Pereira T, Brismar K, Poellinger L (2004) Hyperglycemia regulates hypoxia-inducible factor-1alpha protein stability and function. Diabetes 53:3226-3232 (Pubitemid 39564499)
49. Mowat FM, Luhmann UF, Smith AJ et al (2010) HIF-1alpha and HIF-2alpha are differentially activated in distinct cell populations in retinal ischaemia. PLoS ONE 5:e11103