Beta-lapachone inhibits pathological retinal neovascularization in oxygen-induced retinopathy via regulation of HIF-1α

Journal of Cellular and Molecular Medicine

Volumn 18, Issue 5, 2014, Pages 875-884

  Park, Sung Wook ^a,b   Kim, Jin Hyoung ^a   Kim, Ko Eun ^a   Jeong, Moon Hee ^c   Park, Hyunsung ^d   Park, Bongju ^d   Suh, Young Ger ^b   Park, Woo Jin ^c   Kim, Jeong Hun ^a,b  

^a Seoul National University Hospital   (South Korea)

^b Seoul National University   (South Korea)

^c Gwangju Institute of Science and Technology (GIST)   (South Korea)

^d University of Seoul   (South Korea)

Author keywords

Hypoxia induced factor 1 ; Oxygen induced retinopathy; Retinal neovascularization; Retinopathy of prematurity; Vascular endothelial growth factor; lapachone

Indexed keywords

BETA-LAPACHONE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NAPHTHOQUINONE; OXYGEN; VASCULOTROPIN A;

ANIMAL; APOPTOSIS; ASTROCYTE; C57BL MOUSE; CELL HYPOXIA; DRUG EFFECTS; ENDOTHELIUM CELL; GENETIC TRANSCRIPTION; GENETICS; HUMAN; INTRAOCULAR DRUG ADMINISTRATION; METABOLISM; PATHOLOGY; PROTEIN DEGRADATION; RETINA; RETINAL NEOVASCULARIZATION;

ANIMALS; APOPTOSIS; ASTROCYTES; CELL HYPOXIA; ENDOTHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INJECTIONS, INTRAOCULAR; MICE, INBRED C57BL; NAPHTHOQUINONES; OXYGEN; PROTEOLYSIS; RETINA; RETINAL NEOVASCULARIZATION; TRANSCRIPTION, GENETIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84900543413     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12235     Document Type: Article

References (42)

1. Carmeliet P. Angiogenesis in life, disease and medicine. Nature. 2005; 438: 932-6.
2. Sapieha P, Joyal JS, Rivera JC, et al. Retinopathy of prematurity: understanding ischemic retinal vasculopathies at an extreme of life. J Clin Invest. 2010; 120: 3022-32.
3. Weidemann A, Krohne TU, Aguilar E, et al. Astrocyte hypoxic response is essential for pathological but not developmental angiogenesis of the retina. Glia. 2010; 58: 1177-85.
4. Reynolds JD. Bevacizumab for retinopathy of prematurity. N Engl J Med. 2011; 364: 677-8.
5. Mintz-Hittner HA, Kennedy KA, Chuang AZ. Efficacy of intravitreal bevacizumab for stage 3+ retinopathy of prematurity. N Engl J Med. 2011; 364: 603-15.
6. Kurihara T, Westenskow PD, Bravo S, et al. Targeted deletion of Vegfa in adult mice induces vision loss. J Clin Invest. 2012; 122: 4213-7.
7. Kim J, Ahn JH, Kim JH, et al. Fenofibrate regulates retinal endothelial cell survival through the AMPK signal transduction pathway. Exp Eye Res. 2007; 84: 886-93.
8. Kim JH, Kim KH, Kim JH, et al. Homoisoflavanone inhibits retinal neovascularization through cell cycle arrest with decrease of cdc2 expression. Biochem Biophys Res Commun. 2007; 362: 848-52.
9. Kim JH, Kim JH, Yu YS, et al. Deguelin inhibits retinal neovascularization by down-regulation of HIF-1alpha in oxygen-induced retinopathy. J Cell Mol Med. 2008; 12: 2407-15.
10. Kim JH, Kim JH, Oh M, et al. N-hydroxy-7-(2-naphthylthio) heptanomide inhibits retinal and choroidal angiogenesis. Mol Pharm. 2009; 6: 513-9.
11. Kim JH, Kim JH, Lee YM, et al. Decursin inhibits retinal neovascularization via suppression of VEGFR-2 activation. Mol Vis. 2009; 15: 1868-75.
12. Park SW, Cho CS, Jun HO, et al. Anti-angiogenic effect of luteolin on retinal neovascularization via blockade of reactive oxygen species production. Invest Ophthalmol Vis Sci. 2012; 53: 7718-26.
13. Lee JS, Park AH, Lee SH, et al. Beta-lapachone, a modulator of NAD metabolism, prevents health declines in aged mice. PLoS ONE. 2012; 7: e47122.
14. Smith LE, Wesolowski E, McLellan A, et al. Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci. 1994; 35: 101-11.
15. Ngamwongsatit P, Banada PP, Panbangred W, et al. WST-1-based cell cytotoxicity assay as a substitute for MTT-based assay for rapid detection of toxigenic Bacillus species using CHO cell line. J Microbiol Methods. 2008; 73: 211-5.
16. Kim JH, Kim C, Kim JH, et al. Absence of intravitreal bevacizumab-induced neuronal toxicity in the retina. Neurotoxicology. 2008; 29: 1131-5.
17. Kung HN, Chien CL, Chau GY, et al. Involvement of NO/cGMP signaling in the apoptotic and anti-angiogenic effects of beta-lapachone on endothelial cells in vitro. J Cell Physiol. 2007; 211: 522-32.
18. Dorrell MI, Aguilar E, Friedlander M. Retinal vascular development is mediated by endothelial filopodia, a preexisting astrocytic template and specific R-cadherin adhesion. Invest Ophthalmol Vis Sci. 2002; 43: 3500-10.
19. Ozaki H, Yu AY, Della N, et al. Hypoxia inducible factor-1alpha is increased in ischemic retina: temporal and spatial correlation with VEGF expression. Invest Ophthalmol Vis Sci. 1999; 40: 182-9.
20. Rosenfeld PJ, Moshfeghi AA, Puliafito CA. Optical coherence tomography findings after an intravitreal injection of bevacizumab (avastin) for neovascular age-related macular degeneration. Ophthalmic Surg Lasers Imaging. 2005; 36: 331-5.
21. Rosenfeld PJ, Brown DM, Heier JS, et al. Ranibizumab for neovascular age-related macular degeneration. N Engl J Med. 2006; 355: 1419-31.
22. Brown DM, Kaiser PK, Michels M, et al. Ranibizumab versus verteporfin for neovascular age-related macular degeneration. N Engl J Med. 2006; 355: 1432-44.
23. Group CR, Martin DF, Maguire MG, et al. Ranibizumab and bevacizumab for neovascular age-related macular degeneration. N Engl J Med. 2011; 364: 1897-908.
24. 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: 53-67.
25. Saint-Geniez M, Maharaj AS, Walshe TE, et al. Endogenous VEGF is required for visual function: evidence for a survival role on muller cells and photoreceptors. PLoS ONE. 2008; 3: e3554.
26. Rosenfeld PJ, Shapiro H, Tuomi L, et al. Characteristics of patients losing vision after 2 years of monthly dosing in the phase III ranibizumab clinical trials. Ophthalmology. 2011; 118: 523-30.
27. Eremina V, Jefferson JA, Kowalewska J, et al. VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med. 2008; 358: 1129-36.
28. Lin M, Hu Y, Chen Y, et al. Impacts of hypoxia-inducible factor-1 knockout in the retinal pigment epithelium on choroidal neovascularization. Invest Ophthalmol Vis Sci. 2012; 53: 6197-206.
29. 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.
30. Schmidt D, Textor B, Pein OT, et al. Critical role for NF-kappaB-induced JunB in VEGF regulation and tumor angiogenesis. EMBO J. 2007; 26: 710-9.
31. Arany Z, Foo SY, Ma Y, et al. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature. 2008; 451: 1008-12.
32. 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: 1390-5.
33. Kim JH, Park SW, Yu YS, et al. Hypoxia-induced insulin-like growth factor II contributes to retinal vascularization in ocular development. Biochimie. 2012; 94: 734-40.
34. Yoshida T, Zhang H, Iwase T, et al. Digoxin inhibits retinal ischemia-induced HIF-1alpha expression and ocular neovascularization. FASEB J. 2010; 24: 1759-67.
35. Shin BH, Lim Y, Oh HJ, et al. Pharmacological activation of Sirt1 ameliorates polyglutamine-induced toxicity through the regulation of autophagy. PLoS ONE. 2013; 8: e64953.
36. Taylor CT. Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem J. 2008; 409: 19-26.
37. Guzy RD, Hoyos B, Robin E, et al. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 2005; 1: 401-8.
38. Griguer CE, Oliva CR, Kelley EE, et al. Xanthine oxidase-dependent regulation of hypoxia-inducible factor in cancer cells. Cancer Res. 2006; 66: 2257-63.
39. Semenza GL. Hypoxia-inducible factor 1 and the molecular physiology of oxygen homeostasis. J Lab Clin Med. 1998; 131: 207-14.
40. Ivan M, Kondo K, Yang H, et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science. 2001; 292: 464-8.
41. 2-regulated prolyl hydroxylation. Science. 2001; 292: 468-72.
42. Masson N, Willam C, Maxwell PH, et al. Independent function of two destruction domains in hypoxia-inducible factor-alpha chains activated by prolyl hydroxylation. EMBO J. 2001; 20: 5197-206.