β-LGND2, an ERβ selective agonist, inhibits pathologic retinal neovascularization

Investigative Ophthalmology and Visual Science

Volumn 53, Issue 8, 2012, Pages 5066-5075

  Giddabasappa, Anand ^a   Eswaraka, Jeetendra R ^a   Barrett, Christina M ^a   Bauler, Matthew N ^a   Wu, Zhongzhi ^a   Yepuru, Muralimohan ^a   Miller, Duane D ^a   Dalton, James T ^a  

^a GTx Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; BETA LGND2; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; RADIOLIGAND; UNCLASSIFIED DRUG; VASCULOTROPIN; LIGAND;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; BINDING AFFINITY; CELL DEATH; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; HISTOLOGY; HUMAN; HUMAN CELL; MALE; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RETINA NEOVASCULARIZATION; RETINOPATHY; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MOTION; DISEASE MODEL; DRUG POTENTIATION; ENDOTHELIUM CELL;

ANGIOGENESIS INHIBITORS; ANIMALS; CELL DEATH; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ESTROGEN RECEPTOR BETA; HUMANS; LIGANDS; MICE; MICE, INBRED C57BL; RETINAL NEOVASCULARIZATION;

EID: 84867390247     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-9627     Document Type: Article

References (43)

1. Dorrell M, Uusitalo-Jarvinen HOURS, Aguilar E, Friedlander M. Ocular neovascularization: basic mechanisms and therapeutic advances. Surv Ophthalmol. 2007;52(suppl 1):S3-S19.
2. Smith LE. Through the eyes of a child: understanding retinopathy through ROP the Friedenwald lecture. Invest Ophthalmol Vis Sci. 2008;49:5177-5182.
3. Stahl A, Connor KM, Sapieha P, et al. The mouse retina as an angiogenesis model. Invest Ophthalmol Vis Sci. 2010;51: 2813-2826.
4. Volpert OV, Zaichuk T, Zhou W, et al. Inducer-stimulated Fas targets activated endothelium for destruction by anti-angiogenic thrombospondin-1 and pigment epithelium-derived factor. Nat Med. 2002;8:349-357.
5. Simo R, Carrasco E, Garcia-Ramírez M, Hernández C. Angiogenic and antiangiogenic factors in proliferative diabetic retinopathy. Curr Diabetes Rev. 2006;2:71-98.
6. Melnikova I. Wet age-related macular degeneration. Nat Rev Drug Discov. 2005;4:711-712.
7. Clark AF. Mechanism of action of the angiostatic cortisone anecortave acetate. Surv Ophthalmol. 2007;52 (suppl 1):S26-S34.
8. Akkoyun I, Yilmaz G, Oto S, Kahraman B, Haberal N, Akova YA. Impact of triamcinolone acetonide on retinal endothelial cells in a retinopathy of prematurity mouse model. Acta Ophthalmol Scand. 2007;85:791-794.
9. Sears JE. Anti-vascular endothelial growth factor and retinopathy of prematurity. Br J Ophthalmol. 2008;92:1437-1438.
10. 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: 1390-1395.
11. Lobov IB, Renard RA, Papadopoulos N, et al. Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc Natl Acad Sci U S A. 2007;104:3219-3224.
12. Barnett JM, McCollum GW, Fowler JA, et al. Pharmacologic and genetic manipulation of MMP-2 and -9 affects retinal neovascularization in rodent models of OIR. Invest Ophthalmol Vis Sci. 2007;48:907-915.
13. Smith LE, Wesolowski E, McLellan A, et al. Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci. 1994;35: 101-111.
14. Aguilar E, Dorrell MI, Friedlander D, et al. Chapter 6. Ocular models of angiogenesis. Methods Enzymol. 2008;444:115-158.
15. Miyamoto N, Mandai M, Takagi H, et al. Contrasting effect of estrogen on VEGF induction under different oxygen status and its role in murine ROP. Invest Ophthalmol Vis Sci. 2002;43: 2007-2014.
16. Wang B, Zou Y, Li H, Yan H, Pan JS, Yuan ZL. Genistein inhibited retinal neovascularization and expression of vascular endothelial growth factor and hypoxia inducible factor 1alpha in a mouse model of oxygen-induced retinopathy. J Ocul Pharmacol Ther. 2005;21:107-113.
17. Giddabasappa A, Bauler MN, Yepuru M, Chaum E, Dalton JT, Eswaraka JR. 17-β estradiol protects ARPE-19 cells from oxidative stress through estrogen receptor-β. Invest Ophthalmol Vis Sci. 2010;51:5278-5287.
18. Giddabasappa A, Bauler MN, Barrett CM, et al. GTx-822, an ER{beta}-selective agonist protects retinal pigment epithelium (ARPE-19) from oxidative stress by activating MAPK and PI3-K pathways. Invest Ophthalmol Vis Sci. 2010;51:5934-5942.
19. Yepuru M, Eswaraka J, Kearbey JD, et al. Estrogen receptor-{beta}-selective ligands alleviate high-fat diet- and ovariectomyinduced obesity in mice. J Biol Chem. 2010;285:31292-31303.
20. Ogueta SB, Schwartz SD, Yamashita CK, Farber DB. Estrogen receptor in the human eye: influence of gender and age on gene expression. Invest Ophthalmol Vis Sci. 1999;40:1906-1911.
21. Munaut C, Lambert V, Nöel A, et al. Presence of oestrogen receptor type beta in human retina. Br J Ophthalmol. 2001; 85:877-882.
22. Spyridopoulos I, Sullivan AB, Kearney M, Isner JM, Losordo DW. Estrogen-receptor-mediated inhibition of human endothelial cell apoptosis. Estradiol as a survival factor. Circulation. 1997;95:1505-1514.
23. Sundar SN, Marconett CN, Doan VB, Willoughby JA Sr, Firestone GL. Artemisinin selectively decreases functional levels of estrogen receptor-alpha and ablates estrogen-induced proliferation in human breast cancer cells. Carcinogenesis. 2008;29:2252-2258.
24. Kelly J, Ali Khan A, Yin J, Ferguson TA, Apte RS. Senescence regulates macrophage activation and angiogenic fate at sites of tissue injury in mice. J Clin Invest. 2007;117:3421-3426.
25. Davies MH, Stempel AJ, Powers MR. MCP-1 deficiency delays regression of pathologic retinal neovascularization in a model of ischemic retinopathy. Invest Ophthalmol Vis Sci. 2008;49: 4195-4202.
26. Dorrell MI, Aguilar E, Jacobson R, et al. Maintaining retinal astrocytes normalizes revascularization and prevents vascular pathology associated with oxygen-induced retinopathy. Glia. 2010;58:43-54.
27. Chen J, Smith LE. Retinopathy of prematurity. Angiogenesis. 2007;10:133-140.
28. Gu X, El-Remessy AB, Brooks SE, Al-Shabrawey M, Tsai NT, Caldwell RB. Hyperoxia induces retinal vascular endothelial cell apoptosis through formation of peroxynitrite. Am J Physiol Cell Physiol. 2003;285:C546-C554.
29. Phelps DL. Retinopathy of prematurity. N Engl J Med. 1992; 326:1078-1080.
30. Banin E, Dorrell MI, Aguilar E, et al. T2-TrpRS inhibits preretinal neovascularization and enhances physiological vascular regrowth in OIR as assessed by a new method of quantification. Invest Ophthalmol Vis Sci. 2006;47:2125-2134.
31. Spierer A, Rabinowitz R, Pri-Chen S, Rosner M. An increase in superoxide dismutase ameliorates oxygen-induced retinopathy in transgenic mice. Eye (Lond). 2005;19:86-91.
32. Connor KM, SanGiovanni JP, Lofqvist C, et al. Increased dietary intake of omega-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis. Nat Med. 2007;13:868-873.
33. Penn JS, Thum LA, Naash MI. Oxygen-induced retinopathy in the rat. Vitamins C and E as potential therapies. Invest Ophthalmol Vis Sci. 1992;33:1836-1845.
34. Borras C, Gambini J, Gomez-Cabrera MC, et al. Genistein, a soy isoflavone, up-regulates expression of antioxidant genes: involvement of estrogen receptors, ERK1/2, and NFkappaB. Faseb J. 2006;20:2136-2138.
35. Vina J, Sastre J, Pallardo FV, Gambini J, Borras C. Role of mitochondrial oxidative stress to explain the different longevity between genders: protective effect of estrogens. Free Radic Res. 2006;40:1359-1365.
36. Wang S, Wu Z, Sorenson CM, Lawler J, Sheibani N. Thrombospondin-1-deficient mice exhibit increased vascular density during retinal vascular development and are less sensitive to hyperoxia-mediated vessel obliteration. Dev Dyn. 2003;228:630-642.
37. Chen J, Connor KM, Aderman CM, Willett KL, Aspegren OP, Smith LE. Suppression of retinal neovascularization by erythropoietin siRNA in a mouse model of proliferative retinopathy. Invest Ophthalmol Vis Sci. 2009;50:1329-1335.
38. Mowat FM, Luhmann UF, Smith AJ, et al. HIF-1alpha and HIF-2alpha are differentially activated in distinct cell populations in retinal ischaemia. PLoS One. 2010;5:e11103.
39. Sears JE, Hoppe G, Ebrahem Q, Anand-Apte B. Prolyl hydroxylase inhibition during hyperoxia prevents oxygeninduced retinopathy. Proc Natl Acad Sci U S A. 2008;105: 19898-19903.
40. Mazzone M, Dettori D, Leite de Oliveira R, et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell. 2009;136:839-851.
41. Lang R, Lustig M, Francois F, Sellinger M, Plesken H. Apoptosis during macrophage-dependent ocular tissue remodelling. Development. 1994;120:3395-3403.
42. Lobov IB, Rao S, Carroll TJ, et al. WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature. Nature. 2005;437:417-421.
43. Downie LE, Pianta MJ, Vingrys AJ, Wilkinson-Berka JL, Fletcher EL. AT1 receptor inhibition prevents astrocyte degeneration and restores vascular growth in oxygen-induced retinopathy. Glia. 2008;56:1076-1090.