NSAIDs inhibit neovascularization of choroid through HO-1-dependent pathway

Laboratory Investigation

Volumn 91, Issue 9, 2011, Pages 1277-1290

  Yoshinaga, Narimasa ^a   Arimura, Noboru ^a   Otsuka, Hiroki ^a   Kawahara, Ko Ichi ^a,b   Hashiguchi, Teruto ^a   Maruyama, Ikuro ^a   Sakamoto, Taiji ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

^b OSAKA INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

age related macular degeneration; anti VEGF; choroidal atrophy; oxidative stress; photodynamic therapy; steroid

Indexed keywords

BROMFENAC; HEME OXYGENASE 1; HYDROGEN PEROXIDE; INDOMETACIN; NONSTEROID ANTIINFLAMMATORY AGENT; STANNSOPORFIN; TRANSCRIPTION FACTOR NRF2; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; AQUEOUS HUMOR; ARTICLE; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MALE; NONHUMAN; OXIDATIVE STRESS; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SUBRETINAL NEOVASCULARIZATION; WESTERN BLOTTING;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; APOPTOSIS; BENZOPHENONES; BLOTTING, WESTERN; BROMOBENZENES; CELL LINE; CELLS, CULTURED; CHOROIDAL NEOVASCULARIZATION; FLUORESCENT ANTIBODY TECHNIQUE; HEME OXYGENASE-1; IMMUNOHISTOCHEMISTRY; RATS; RETINAL PIGMENT EPITHELIUM; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 80052287276     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2011.101     Document Type: Article

References (51)

1. Bressler NM, Bressler SB, Fine SL. Age-related macular degeneration. Surv Ophthalmol 1988;32:375-413.
2. Soubrane G. Choroidal neovascularization in pathologic myopia: recent developments in diagnosis and treatment. Surv Ophthalmol 2008;53:121-138. (Pubitemid 351381556)
3. Cohen SY, Laroche A, Leguen Y, et al. Etiology of choroidal neovascularization in young patients. Ophthalmology 1996;103: 1241-1244. (Pubitemid 26282507)
4. TAP study group. Photodynamic therapy of subfoveal choroidal neovascularization in age-related macular degeneration with verteporfin: one-year results of 2 randomized clinical trials-TAP report. Treatment of age-related macular degeneration with photodynamic therapy (TAP) Study Group. Arch Ophthalmol 1999;117:1329-1345.
5. Rosenfeld PJ, Brown DM, Heier JS, et al. Ranibizumab for neovascular age-related macular degeneration. N Engl J Med 2006;355:1419-1431. (Pubitemid 44511557)
6. 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. (Pubitemid 47339226)
7. Robinson GS, Ju M, Shih SC, et al. Nonvascular role for VEGF: VEGFR-1, 2 activity is critical for neural retinal development. FASEB J 2001;15:1215-1217.
8. Murakami Y, Ikeda Y, Yonemitsu Y, et al. Inhibition of choroidal neovascularization via brief subretinal exposure to a newly developed lentiviral vector pseudotyped with Sendai viral envelope proteins. Hum Gene Ther 2010;21:199-209.
9. Saint-Geniez M, Kurihara T, Sekiyama E, et al. An essential role for RPEderived soluble VEGF in the maintenance of the choriocapillaris. Proc Natl Acad Sci USA 2009;106:18751-18756.
10. 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;118:523-530.
11. Sakamoto T, Soriano D, Nassaralla J, et al. Effect of intravitreal administration of indomethacin on experimental subretinal neovascularization in the subhuman primate. Arch Ophthalmol 1995; 113:222-226.
12. Takahashi H, Yanagi Y, Tamaki Y, et al. COX-2-selective inhibitor, etodolac, suppresses choroidal neovascularization in a mice model. Biochem Biophys Res Commun 2004;325:461-466. (Pubitemid 39458017)
13. Takahashi K, Saishin Y, Saishin Y, et al. Topical nepafenac inhibits ocular neovascularization. Invest Ophthalmol Vis Sci 2003;44:409-415. (Pubitemid 36134303)
14. Yanni SE, Clark ML, Yang R, et al. The effects of nepafenac and amfenac on retinal angiogenesis. Brain Res Bull 2010;81:310-319.
15. Kim SJ, Toma HS. Inhibition of choroidal neovascularization by intravitreal ketorolac. Arch of Ophthalmol 2010;128:596-600.
16. Kim SJ, Toma HS, Barnett JM, Penn JS. Ketorolac inhibits choroidal neovascularization by suppression of retinal VEGF. Exp Eye Res 2010;91:537-543.
17. Wilson HL, Schwartz DM, Bhatt HR, et al. Statin and aspirin therapy are associated with decreased rates of choroidal neovascularization among patients with age-related macular degeneration. Am J Ophthalmol 2004;137:615-624. (Pubitemid 38446673)
18. Rezaei KA, Toma H, Cai J, et al. Reduced choroidal neovascular membrane formation in cyclooxygenase-2 null mice. Invest Ophthalmol Vis Sci 2010;52:701-707.
19. Tegeder I, Pfeilschifter J, Geisslinger G. Cyclooxygenase-independent actions of cyclooxygenase inhibitors. FASEB J 2001;15:2057-2072. (Pubitemid 32927924)
20. Ponka P. Cell biology of heme. Am J Med Sci 1999;318:241-256. (Pubitemid 30349676)
21. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 1997;37:517-554. (Pubitemid 27238886)
22. Brouard S, Otterbein LE, Anrather J, et al. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J Exp Med 2000;192:1015-1026.
23. Alcaraz MJ, Habib A, Créminon C, et al. Heme oxygenase-1 induction by nitric oxide in RAW 264.7 macrophages is upregulated by a cyclooxygenase-2 inhibitor. Biochim Biophys Acta 2001;1526:13-16. (Pubitemid 32245766)
24. Hou CC, Hung SL, Kao SH, et al. Celecoxib induces heme-oxygenase expression in glomerular mesangial cells. Ann NY Acad Sci 2005; 1042:235-245.
25. Nascimento-Silva V, Arruda MA, Barja-Fidalgo C, et al. Novel lipid mediator aspirin-triggered lipoxin A4 induces heme oxygenase-1 in endothelial cells. Am J Physiol Cell Physiol 2005;289:C557-C563. (Pubitemid 41192664)
26. Grosser N, Abate A, Oberle S, et al. Heme oxygenase-1 induction may explain the antioxidant profile of aspirin. Biochem Biophys Res Commun 2003;308:956-960. (Pubitemid 36976552)
27. Cantoni L, Valaperta R, Ponsoda X, et al. Induction of hepatic heme oxygenase-1 by diclofenac in rodents: role of oxidative stress and cytochrome P-450 activity. J Hepatol 2003;38:776-783. (Pubitemid 36613344)
28. Arimura N, Ki-i Y, Hashiguchi T, et al. Intraocular expression and release of high-mobility group box 1 protein in retinal detachment. Lab Invest 2009;89:278-289.
29. Otsuka H, Arimura N, Sonoda S, et al. Stromal cell-derived factor-1 is essential for photoreceptor cell protection in retinal detachment. Am J Pathol 2010;177:2268-2277.
30. Fujimoto T, Sonoda KH. Choroidal neovascularization enhanced by Chlamydia pneumoniae via Toll-like receptor 2 in the retinal pigment epithelium. Invest Ophthalmol Vis Sci 2010;51:4694-4702.
31. Honda M, Sakamoto T, Ishibashi T, et al. Experimental subretinal neovascularization is inhibited by adenovirus-mediated soluble VEGF/flt-1 receptor gene transfection: a role of VEGF and possible treatment for SRN in age-related macular degeneration. Gene Ther 2000;7:978-985. (Pubitemid 30386663)
32. Aburaya M, Tanaka K-I, Hoshino T, et al. Heme oxygenase-1 protects gastric mucosal cells against non-steroidal anti-inflammatory drugs. J Biol Chem 2006;281:33422-33432. (Pubitemid 46036723)
33. Jones MK, Wang H, Peskar BM, et al. Inhibition of angiogenesis by nonsteroidal anti-inflammatory drugs: insight into mechanisms and implications for cancer growth and ulcer healing. Nat Med 1999;5: 1418-1423.
34. Jones MK, Szabó IL, Kawanaka H, et al. von Hippel Lindau tumor suppressor and HIF-1alpha: new targets of NSAIDs inhibition of hypoxia-induced angiogenesis. FASEB J 2002;16:264-266.
35. Ferrara N. Vascular endothelial growth factor and the regulation of angiogenesis. Recent Prog Horm Res 2000;55:15-35.
36. Tsutsumi C, Sonoda KH, Egashira K, et al. The critical role of ocularinfiltrating macrophages in the development of choroidal neovascularization. J Leukoc Biol 2003;74:25-32. (Pubitemid 38040433)
37. Ghosh S, May MJ, Kopp EB. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 1998;16:225-260. (Pubitemid 28183365)
38. Jaiswal AK. Nrf2 signaling in coordinated activation of activation of antioxidant gene expression. Free Radic Biol Med 2004;36: 1199-1207. (Pubitemid 38526313)
39. Kaspar JW, Niture SK, Jaiswal AK. Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 2009;47:1304-1309.
40. Healy ZR, Lee NH, Gao X, et al. Divergent responses of chondrocytes and endothelial cells to shear stress: cross-talk among COX-2, the phase 2 response, and apoptosis. Proc Natl Acad Sci USA 2005;102: 14010-14015. (Pubitemid 41377694)
41. Bussolati B, Ahmed A, Pemberton H, et al. Bifunctional role for VEGFinduced heme oxygenase-1 in vivo: induction of angiogenesis and inhibition of leukocytic infiltration. Blood 2004;103:761-766. (Pubitemid 38129530)
42. Dulak J, Loboda A, Zagó rska A, Jó zkowicz A. Complex role of heme oxygenase-1 in angiogenesis. Antioxid Redox Signal 2004;6: 858-866. (Pubitemid 39237939)
43. Bussolati B, Mason JC. Dual role of VEGF-induced heme-oxygenase-1 in angiogenesis. Antioxid Redox Signal 2006;8:1153-1163. (Pubitemid 44192315)
44. Mandal MN, Patlolla JM, Zheng L, et al. Curcumin protects retinal cells from light-and oxidant stress-induced cell death. Free Radic Biol Med 2009;46:672-679.
45. Shyong MP, Lee FL, Hen WH, et al. Viral delivery of heme oxygenase-1 attenuates photoreceptor apoptosis in an experimental model of retinal detachment. Vision Res 2008;48:2394-2402.
46. Sun MH, Su Pang JH, Chen SL, et al. Retinal protection from acute glaucoma-induced ischemia-reperfusion injury through pharmacological induction of heme oxygenase-1 by cobalt protoporphyrin. Invest Ophthalmol Vis Sci 2010;51:4798-4808.
47. Qin S, McLaughlin AP, De Vries GW. Protection of RPE cells from oxidative injury by 15-deoxy-delta12,14-prostaglandin J2 by augmenting GSH and activating MAPK. Invest Ophthalmol Vis Sci 2006;47: 5098-5105. (Pubitemid 46586417)
48. Gamache DA, Graff G, Brady MT, et al. Nepafenac, a unique nonsteroidal prodrug with potential utility in the treatment of traumainduced ocular inflammation. I: assessment of anti-inflammatory efficacy. Inflammation 2000;24:357-370. (Pubitemid 30367882)
49. Isaka M, Inada K, Tsutsumi S, et al. Ocular tissue distribution in rabbit after instillation of bromfenac sodium ophthalmic solution. Drug Metabol Pharmacokinet 1999;14:32-41.
50. Kida T, Ogawa T, McNamara TR, et al. Evaluations of the human COX-1 and COX-2 inhibition for amfenac, bromfenac, ciclofenac, and ketorolac. Annu Meet Guide Abstr Am Coll Clin Pharm 2007; (Suppl):274.
51. Abdollahi A, Folkman J. Evading tumor evasion: current concepts and perspectives of anti-angiogenic cancer therapy. Drug Resist Updat 2010;13:16-28.