Association of retinal vascular endothelial growth factor with avascular retina in a rat model of retinopathy of prematurity

Archives of Ophthalmology

Volumn 128, Issue 8, 2010, Pages 1014-1021

  Budd, Steven J ^a   Thompson, Hilary ^b   Hartnett, M Elizabeth ^a,c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAP BINDING PROTEIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

AMBIENT AIR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE OVEREXPRESSION; NEWBORN; NONHUMAN; OXYGEN TENSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA NEOVASCULARIZATION; RETROLENTAL FIBROPLASIA;

ALTERNATIVE SPLICING; ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; INFANT, NEWBORN; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; RETINAL NEOVASCULARIZATION; RETINAL VESSELS; RETINOPATHY OF PREMATURITY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 77955463898     PISSN: 00039950     EISSN: 15383601     Source Type: Journal    
DOI: 10.1001/archophthalmol.2010.158     Document Type: Article

References (55)

1. Terry TL. Extreme prematurity and fibroblastic overgrowth of persistent vascular sheath behind each crystalline lens: (1) preliminary report. Am J Ophthalmol. 1942;25:203-204.
2. Ashton N, Ward B, Serpell G. Effect of oxygen on developing retinal vessels with particular reference to the problem of retrolental fibroplasia. Br J Ophthalmol. 1954;38(7):397-432.
3. Patz A, Eastham A, Higginbotham DH, Kleh T. Oxygen studies in retrolental fibroplasia, II: the production of the microscopic changes of retrolental fibroplasia in experimental animals. Am J Ophthalmol. 1953;36(11):1511-1522.
4. Michaelson IC. The mode of development of the vascular system of the retina: with some observations on its significance for certain retinal diseases. Trans Ophthalmol Soc U K. 1948;68:137-180.
5. Smith LEH, Wesolowski E, McLellan A, et al. Oxygen induced retinopathy in the mouse. Invest Ophthalmol Vis Sci. 1994;35(1):101-111.
6. Stiller R, von Mering R, König V, Huch A, Huch R. How well does reflectance pulse oximetry reflect intrapartum fetal acidosis? Am J Obstet Gynecol. 2002; 186(6):1351-1357. (Pubitemid 34665083)
7. Smith LE. Through the eyes of a child: understanding retinopathy through ROP: the Friedenwald lecture. Invest Ophthalmol Vis Sci. 2008;49(12):5177-5182. doi: 10.1167/iovs.08-2584.
8. Hellström A, Engstrom E, Hard A-L, et al. Postnatal serum insulin-like growth factor I deficiency is associated with retinopathy of prematurity and other complications of premature birth. Pediatrics. 2003;112(5):1016-1020.
9. Hellström A, Hard AL, Engstrom E, et al. Early weight gain predicts retinopathy in preterm infants: new, simple, efficient approach to screening. Pediatrics. 2009; 123(4):e638-e645 doi:10.1542/peds.2008-2697.
10. Penn JS, Henry MM, Wall PT, Tolman BL. The range of PaO2 variation determines the severity of oxygen induced retinopathy in newborn rats. Invest Ophthalmol Vis Sci. 1995;36(10):2063-2070.
11. Cunningham S, Fleck BW, Elton RA, McIntosh N. Transcutaneous oxygen levels in retinopathy of prematurity. Lancet. 1995;346(8988):1464-1465.
12. Pierce EA, Foley ED, Smith LE. Regulation of vascular endothelial growth factor by oxygen in a model of retinopathy of prematurity. Arch Ophthalmol. 1996; 114(10):1219-1228.
13. Gao G, Li Y, Zhang D, Gee S, Crosson C, Ma J. Unbalanced expression of VEGF and PEDF in ischemia-induced retinal neovascularization. FEBS Lett. 2001; 489(2-3):270-276. (Pubitemid 32126422)
14. Carmeliet P, Ferreira V, Breier G, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 1996;380(6573):435-439.
15. Chan-Ling T, Gock B, Stone J. The effect of oxygen on vasoformative cell division: evidence that "physiological hypoxia" is the stimulus for normal retinal vasculogenesis. Invest Ophthalmol Vis Sci. 1995;36(7):1201-1214.
16. Stone J, Itin A, Alon T, et al. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci. 1995;15(7, pt 1):4738-4747.
17. Sonmez K, Drenser KA, Capone A Jr, Trese MT. Vitreous levels of stromal cell-derived factor 1 and vascular endothelial growth factor in patients with retinopathy of prematurity. Ophthalmology. 2008;115(6):1065-1070, e1.
18. Alon T, Hemo I, Itin A, Pe'er J, Stone J, Keshet E. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med. 1995;1(10):1024-1028.
19. Lofqvist C, Chen J, Connor KM, et al. IGFBP3 suppresses retinopathy through suppression of oxygen-induced vessel loss and promotion of vascular regrowth. Proc Natl Acad Sci U S A. 2007;104(25):10589-10594.
20. Hellström A, Perruzzi C, Ju M, et al. Low IGF-1 suppresses VEGF-survival signalling in retinal endothelial cells: direct correlation with clinical retinopathy of prematurity. Proc Natl Acad Sci U S A. 2001;98(10):5804-5808.
21. Chang KH, Chan-Ling T, McFarland EL, et al. IGF binding protein-3 regulates hematopoietic stem cell and endothelial precursor cell function during vascular development. Proc Natl Acad Sci U S A. 2007;104(25):10595-10600.
22. Penn JS, Henry MM, Tolman BL. Exposure to alternating hypoxia and hyperoxia causes severe proliferative retinopathy in the newborn rat. Pediatr Res. 1994; 36(6):724-731.
23. Hartnett ME, Martiniuk DJ, Saito Y, Geisen P, Peterson LJ, McColm JR. Triamcinolone reduces neovascularization, capillary density and IGF-1 receptor phosphorylation in a model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci. 2006;47(11):4975-4982. (Pubitemid 46586402)
24. Liu K, Akula JD, Falk C, Hansen RM, Fulton AB. The retinal vasculature and function of the neural retina in a rat model of retinopathy of prematurity. Invest Ophthalmol Vis Sci. 2006;47(6):2639-2647.
25. Penn JS, Tolman BL, Henry MM. Oxygen-induced retinopathy in the rat: relationship of retinal nonperfusion to subsequent neovascularization. Invest Ophthalmol Vis Sci. 1994;35(9):3429-3435.
26. Chan-Ling T. Glial, vascular and neuronal cytogenesis in whole-mounted cat retina. Microsc Res Tech. 1997;36(1):1-16.
27. Budd S, Byfield G, Martiniuk D, Geisen P, Hartnett ME. Reduction in endothelial tip cell filopodia corresponds to reduced intravitreous but not intraretinal vascularization in a model of ROP. Exp Eye Res. 2009;89(5):718-727.
28. Geisen P, Peterson LJ, Martiniuk D, Uppal A, Saito Y, Hartnett ME. Neutralizing antibody to VEGF reduces intravitreous neovascularization and may not interfere with ongoing intraretinal vascularization in a rat model of retinopathy of prematurity. Mol Vis. 2008;14:345-357.
29. Werdich XQ, Penn JS. Specific involvement of SRC family kinase activation in the pathogenesis of retinal neovascularization. Invest Ophthalmol Vis Sci. 2006; 47(11):5047-5056.
30. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem. 1951;193(1):265-275.
31. Vandesompele J, De Preter K, Pattyn F, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3(7):RESEARCH0034. doi:10.1186/gb-2002-3-7 -research0034.
32. Edwards D, Berry JJ. The efficiency of simulation-based multiple comparisons. Biometrics. 1987;43(4):913-928.
33. McColm JR, Geisen P, Hartnett ME. VEGF isoforms and their expression after a single episode of hypoxia or repeated fluctuations between hyperoxia and hypoxia: relevance to clinical ROP. Mol Vis. 2004;10:512-520. (Pubitemid 41358245)
34. Ferrara N, Gerber HP, Lecouter J. The biology of VEGF and its receptors. Nat Med. 2003;9(6):669-676.
35. Hartnett ME, Martiniuk DJ, Byfield GE, Geisen P, Zeng G, Bautch VL. Neutralizing VEGF decreases tortuosity and alters endothelial cell division orientation in arterioles and veins in rat model of ROP: relevance to plus disease. Invest Ophthalmol Vis Sci. 2008;49(7):3107-3114.
36. Mintz-Hittner HA, Kuffel RR Jr. Intravitreal injection of bevacizumab (Avastin) for treatment of stage 3 retinopathy of prematurity in zone I or posterior zone II. Retina. 2008;28(6):831-838.
37. Robinson GS, Aiello LP. Angiogenic factors in diabetic ocular disease: mechanisms of today, therapies for tomorrow. Int Ophthalmol Clin. 1998;38(2):89-102.
38. Adamis AP, Miller JW, Bernal MT, et al. Increased vascular endothelial growth factor levels in the vitreous of eyes with proliferative diabetic retinopathy. Am J Ophthalmol. 1994;118(4):445-450.
39. Aiello LP, Avery RL, Arrigg PG, et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 1994;331(22):1480-1487.
40. Young TL, Anthony DC, Pierce E, Foley E, Smith LE. Histopathology and vascular endothelial growth factor in untreated and diode laser-treated retinopathy of prematurity. J AAPOS. 1997;1(2):105-110.
41. Hellström M, Phng LK, Hofmann JJ, et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature. 2007;445(7129):776-780.
42. Bentley K, Gerhardt H, Bates PA. Agent-based simulation of notch-mediated tip cell selection in angiogenic sprout initialisation. J Theor Biol. 2008;250(1):25-36. (Pubitemid 350160711)
43. Smith LE, Kopchick JJ, Chen W, et al. Essential role of growth hormone in ischemiainduced retinal neovascularization. Science. 1997;276(5319):1706-1709.
44. Morita M, Ohneda O, Yamashita T, et al. HLF/HIF-2α is a key factor in retinopathy of prematurity in association with erythropoietin. EMBO J. 2003;22(5):1134-1146.
45. Smith LE, Shen W, Perruzzi C, et al. Regulation of vascular endothelial growth factor-dependent retinal neovascularization by insulin-like growth factor-1 receptor. Nat Med. 1999;5(12):1390-1395.
46. Wu Z, Wang S, Sorenson CM, Sheibani N. Attenuation of retinal vascular development and neovascularization in transgenic mice over-expressing thrombospondin- 1 in the lens. Dev Dyn. 2006;235(7):1908-1920.
47. Dawson DW, Volpert OV, Gillis P, et al. Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science. 1999;285(5425):245-248. (Pubitemid 29329995)
48. Huang Q, Wang S, Sorenson CM, Sheibani N. PEDF-deficient mice exhibit an enhanced rate of retinal vascular expansion and are more sensitive to hyperoxiamediated vessel obliteration. Exp Eye Res. 2008;87(3):226-241.
49. Dorrell MI, Aguilar E, Jacobson R, et al. Maintaining retinal astrocytes normalizes revascularization and prevents vascular pathology associated with oxygeninduced retinopathy. Glia. 2010;58(1):43-54.
50. Shibuya M. Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J Biochem Mol Biol. 2006;39(5):469-478.
51. Oosthuyse B, Moons L, Storkebaum E, et al. Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat Genet. 2001;28(2):131-138.
52. Laudenbach V, Fontaine RH, Medja F, et al. Neonatal hypoxic preconditioning involves vascular endothelial growth factor. Neurobiol Dis. 2007;26(1):243-252.
53. Nishijima K, Ng YS, Zhong L, et al. 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. 2007;171(1):53-67.
54. Voelkel NF, Vandivier RW, Tuder RM. Vascular endothelial growth factor in the lung. Am J Physiol Lung Cell Mol Physiol. 2006;290(2):L209-L221.
55. Early Treatment for Retinopathy of Prematurity Cooperative Group. Revised indications for the treatment of retinopathy of prematurity: results of the Early Treatment for Retinopathy of Prematurity Randomized Trial. Arch Ophthalmol. 2003; 121(12):1684-1694.