Heme Oxygenase and Ocular Disease: A Review of the Literature

REFERENCES

• Maines MD. The heme oxygenase system: past, present, and future. Antioxid Redox Signal 2004;6:797–801.
   Google Scholar
• Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 1997;37:517–554.
   PubMed Web of Science ®Google Scholar
• Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006;86:583–650.
   PubMed Web of Science ®Google Scholar
• Simon T, Anegon I, Blancou P. Heme oxygenase and carbon monoxide as an immunotherapeutic approach in transplantation and cancer. Immunotherapy 2011;3:15–18.
   PubMed Web of Science ®Google Scholar
• Kim HP, Pae HO, Back SH et al. Heme oxygenase-1 comes back to endoplasmic reticulum. Biochem Biophys Res Commun 2011;404:1–5.
   Google Scholar
• Fan W, Huang F, Zhu X et al. The heme oxygenase system and oral diseases. Oral Dis 2011;17:252–257.
   Google Scholar
• Kim YM, Pae HO, Park JE et al. Heme oxygenase in the regulation of vascular biology: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 2011;14:137–167.
   PubMed Web of Science ®Google Scholar
• Abraham NG, Lin JH, Dunn MW et al. Presence of heme oxygenase and NADPH cytochrome P-450© reductase in human corneal epithelium. Invest Ophthalmol Vis Sci 1987;28:1464–1472.
   PubMed Web of Science ®Google Scholar
• Cao L, Blute TA, Eldred WD. Localization of heme oxygenase-2 and modulation of cGMP levels by carbon monoxide and/or nitric oxide in the retina. Vis Neurosci 2000;17:319–329.
   PubMed Web of Science ®Google Scholar
• Nishimura RN, Dwyer BE, Lu SY. Localization of heme oxygenase in rat retina: effect of light adaptation. Neurosci Lett 1996;205:13–16.
   PubMedGoogle Scholar
• Ma N, Ding X, Doi M et al. Cellular and subcellular localization of heme oxygenase-2 in monkey retina. J Neurocytol 2004;33:407–415.
   Google Scholar
• Li T, Zhang H, Liang F. Existence of heme oxygenase-carbon monoxide-cyclic guanosine monophosphate pathway in human trabecular meshwork cells in vitro. J Huazhong Univ Sci Technol Med Sci 2004;24:173–177.
   Google Scholar
• Ohta K, Kikuchi T, Arai S et al. Protective role of heme oxygenase-1 against endotoxin-induced uveitis in rats. Exp Eye Res 2003;77:665–673.
   PubMed Web of Science ®Google Scholar
• Neil TK, Stoltz RA, Jiang S et al. Modulation of corneal heme oxygenase expression by oxidative stress agents. J Ocul Pharmacol Ther 1995;11:455–468.
   Google Scholar
• Laniado-Schwartzman M, Abraham NG, Conners M et al. Heme oxygenase induction with attenuation of experimentally induced corneal inflammation. Biochem Pharmacol 1997;53:1069–1075.
   PubMed Web of Science ®Google Scholar
• Padgaonkar VA, Giblin FJ, Fowler K et al. Heme oxygenase synthesis is induced in cultured lens epithelium by hyperbaric oxygen or puromycin. Exp Eye Res 1997;65:435–443.
   Google Scholar
• Rogers BS, Symons RC, Komeima K et al. Differential sensitivity of cones to iron-mediated oxidative damage. Invest Ophthalmol Vis Sci 2007;48:438–445.
   PubMed Web of Science ®Google Scholar
• Kutty G, Hayden B, Osawa Y et al. Heme oxygenase: expression in human retina and modulation by stress agents in a human retinoblastoma cell model system. Curr Eye Res 1992;11:153–160.
   PubMed Web of Science ®Google Scholar
• Ulyanova T, Szél A, Kutty RK et al. Oxidative stress induces heme oxygenase-1 immunoreactivity in Müller cells of mouse retina in organ culture. Invest Ophthalmol Vis Sci 2001;42:1370–1374.
   PubMed Web of Science ®Google Scholar
• Kutty RK, Kutty G, Wiggert B et al. Induction of heme oxygenase 1 in the retina by intense visible light: suppression by the antioxidant dimethylthiourea. Proc Natl Acad Sci USA 1995;92:1177–1181.
   PubMed Web of Science ®Google Scholar
• Roehlecke C, Schaller A, Knels L et al. The influence of sublethal blue light exposure on human RPE cells. Mol Vis 2009;15:1929–1938.
   PubMed Web of Science ®Google Scholar
• Rzymkiewicz DM, Reddan JR, Andley UP. Induction of heme oxygenase-1 modulates cis-aconitase activity in lens epithelial cells. Biochem Biophys Res Commun 2000;270:324–328.
   Google Scholar
• Black AT, Gordon MK, Heck DE et al. UVB light regulates expression of antioxidants and inflammatory mediators in human corneal epithelial cells. Biochem Pharmacol 2011;81:873–880.
   Google Scholar
• Kutty RK, Nagineni CN, Kutty G et al. Increased expression of heme oxygenase-1 in human retinal pigment epithelial cells by transforming growth factor-beta. J Cell Physiol 1994;159:371–378.
   PubMed Web of Science ®Google Scholar
• Honda S, Hjelmeland LM, Handa JT. The use of hyperoxia to induce chronic mild oxidative stress in RPE cells in vitro. Mol Vis 2001;7:63–70.
   PubMed Web of Science ®Google Scholar
• Padgaonkar VA, Leverenz VR, Dang L et al. Thioredoxin reductase may be essential for the normal growth of hyperbaric oxygen-treated human lens epithelial cells. Exp Eye Res 2004;79:847–857.
   PubMed Web of Science ®Google Scholar
• Braunstein SG, Deramaudt TG, Rosenblum DG et al. Heme oxygenase-1 gene expression as a stress index to ocular irritation. Curr Eye Res 1999;19:115–122.
   PubMed Web of Science ®Google Scholar
• Miyamura N, Ogawa T, Boylan S et al. Topographic and age-dependent expression of heme oxygenase-1 and catalase in the human retinal pigment epithelium. Invest Ophthalmol Vis Sci 2004;45:1562–1565.
   Google Scholar
• Demir MN, Demir ZA, Yalçin Tök O et al. Oxidative stress of intracameral lidocaine and levobupivacaine on ocular tissues. Br J Ophthalmol 2010;94:1083–1087.
   PubMed Web of Science ®Google Scholar
• Erdurmus M, Yagci R, Atis Ö et al. Antioxidant status and oxidative stress in primary open angle glaucoma and pseudoexfoliative glaucoma. Curr Eye Res 2011;36:713–718.
   PubMed Web of Science ®Google Scholar
• Abraham NG, Da Silva JL, Dunn MW et al. Retinal pigment epithelial cell-based gene therapy against hemoglobin toxicity. Int J Mol Med 1998;1:657–663.
   PubMed Web of Science ®Google Scholar
• Gong N, Ecke I, Mergler S et al. Gene transfer of cyto-protective molecules in corneal endothelial cells and cultured corneas: analysis of protective effects in vitro and in vivo. Biochem Biophys Res Commun 2007;357:302–307.
   Google Scholar
• Sun MH, Pang JH, Chen SL et al. Photoreceptor protection against light damage by AAV-mediated overexpression of heme oxygenase-1. Invest Ophthalmol Vis Sci 2007;48:5699–5707.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• da Silva JL, Stoltz RA, Dunn MW et al. Diminished heme oxygenase-1 mRNA expression in RPE cells from diabetic donors as quantitated by competitive RT/PCR. Curr Eye Res 1997;16:380–386.
   PubMed Web of Science ®Google Scholar
• Hanneken A, Lin FF, Johnson J et al. Flavonoids protect human retinal pigment epithelial cells from oxidative-stress-induced death. Invest Ophthalmol Vis Sci 2006;47:3164–3177.
   PubMed Web of Science ®Google Scholar
• Zheng Y, Liu Y, Ge J et al. Resveratrol protects human lens epithelial cells against H2O2-induced oxidative stress by increasing catalase, SOD-1, and HO-1 expression. Mol Vis 2010;16:1467–1474.
   PubMed Web of Science ®Google Scholar
• Johnson J, Maher P, Hanneken A. The flavonoid, eriodictyol, induces long-term protection in ARPE-19 cells through its effects on Nrf2 activation and phase 2 gene expression. Invest Ophthalmol Vis Sci 2009;50:2398–2406.
   PubMed Web of Science ®Google Scholar
• Zhu L, Liu Z, Feng Z et al. Hydroxytyrosol protects against oxidative damage by simultaneous activation of mitochondrial biogenesis and phase II detoxifying enzyme systems in retinal pigment epithelial cells. J Nutr Biochem 2010;21:1089–1098.
   PubMed Web of Science ®Google Scholar
• Wu L, Wang R. Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol Rev 2005;57:585–630.
   PubMed Web of Science ®Google Scholar
• Fan W, Huang F, Wu Z et al. Carbon monoxide: a gas that modulates nociception. J Neurosci Res 2011;89:802–807.
   Google Scholar
• Dawson TM, Snyder SH. Gases as biological messengers: nitric oxide and carbon monoxide in the brain. J Neurosci 1994;14:5147–5159.
   PubMed Web of Science ®Google Scholar
• Kajimura M, Shimoyama M, Tsuyama S et al. Visualization of gaseous monoxide reception by soluble guanylate cyclase in the rat retina. FASEB J 2003;17:506–508.
   Google Scholar
• Otterbein LE, Bach FH, Alam J et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000;6:422–428.
   PubMed Web of Science ®Google Scholar
• Lee TS, Chau LY. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med 2002;8:240–246.
   PubMed Web of Science ®Google Scholar
• Yachie A, Niida Y, Wada T et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest 1999;103:129–135.
   PubMed Web of Science ®Google Scholar
• Chin BY, Otterbein LE. Carbon monoxide is a poison. to microbes! CO as a bactericidal molecule. Curr Opin Pharmacol 2009;9:490–500.
   PubMed Web of Science ®Google Scholar
• Snyder SH, Barañano DE. Heme oxygenase: a font of multiple messengers. Neuropsychopharmacology 2001;25:294–298.
   PubMed Web of Science ®Google Scholar
• Stocker R, Yamamoto Y, McDonagh AF et al. Bilirubin is an antioxidant of possible physiological importance. Science 1987;235:1043–1046.
   PubMed Web of Science ®Google Scholar
• Abraham NG, Kappas A. Heme oxygenase and the cardiovascular-renal system. Free Radic Biol Med 2005;39:1–25.
   PubMed Web of Science ®Google Scholar
• Fondevila C, Shen XD, Tsuchiyashi S et al. Biliverdin therapy protects rat livers from ischemia and reperfusion injury. Hepatology 2004;40:1333–1341.
   PubMedGoogle Scholar
• Clark JE, Foresti R, Sarathchandra P et al. Heme oxygenase-1-derived bilirubin ameliorates postischemic myocardial dysfunction. Am J Physiol Heart Circ Physiol 2000;278:H643–H651.
   PubMed Web of Science ®Google Scholar
• Nakao A, Otterbein LE, Overhaus M et al. Biliverdin protects the functional integrity of a transplanted syngeneic small bowel. Gastroenterology 2004;127:595–606.
   PubMed Web of Science ®Google Scholar
• Bellner L, Vitto M, Patil KA et al. Exacerbated corneal inflammation and neovascularization in the HO-2 null mice is ameliorated by biliverdin. Exp Eye Res 2008;87:268–278.
   Google Scholar
• Willis D, Moore AR, Frederick R et al. Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat Med 1996;2:87–90.
   PubMed Web of Science ®Google Scholar
• Hadziahmetovic M, Song Y, Ponnuru P et al. Age-dependent retinal iron accumulation and degeneration in hepcidin knockout mice. Invest Ophthalmol Vis Sci 2011;52:109–118.
   PubMed Web of Science ®Google Scholar
• Picard E, Ranchon-Cole I, Jonet L et al. Light-induced retinal degeneration correlates with changes in iron metabolism gene expression, ferritin level, and aging. Invest Ophthalmol Vis Sci 2011;52:1261–1274.
   Google Scholar
• Balla G, Jacob HS, Balla J et al. Ferritin: a cytoprotective antioxidant strategem of endothelium. J Biol Chem 1992;267:18148–18153.
   PubMed Web of Science ®Google Scholar
• Orino K, Lehman L, Tsuji Y et al. Ferritin and the response to oxidative stress. Biochem J 2001;357:241–247.
   PubMed Web of Science ®Google Scholar
• Cermak J, Balla J, Jacob HS et al. Tumor cell heme uptake induces ferritin synthesis resulting in altered oxidant sensitivity: possible role in chemotherapy efficacy. Cancer Res 1993;53:5308–5313.
   PubMed Web of Science ®Google Scholar
• Hunt RC, Hunt DM, Gaur N et al. Hemopexin in the human retina: protection of the retina against heme-mediated toxicity. J Cell Physiol 1996;168:71–80.
   Google Scholar
• Otterbein LE, Soares MP, Yamashita K et al. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 2003;24:449–455.
   PubMed Web of Science ®Google Scholar
• Patil K, Bellner L, Cullaro G, Gotlinger KH et al. Heme oxygenase-1 induction attenuates corneal inflammation and accelerates wound healing after epithelial injury. Invest Ophthalmol Vis Sci 2008;49:3379–3386.
   PubMed Web of Science ®Google Scholar
• Rossi S, D’Amico M, Capuano A, Romano M et al. Hyperglycemia in streptozotocin-induced diabetes leads to persistent inflammation and tissue damage following uveitis due to reduced levels of ciliary body heme oxygenase-1. Mediators Inflamm 2006;2006:60285.
   Google Scholar
• Biteman B, Hassan IR, Walker E et al. Interdependence of lipoxin A4 and heme-oxygenase in counter-regulating inflammation during corneal wound healing. FASEB J 2007;21:2257–2266.
   Google Scholar
• Bellner L, Patil KA, Castellano K et al. Targeted suppression of HO-2 gene expression impairs the innate anti-inflammatory and repair responses of the cornea to injury. Mol Vis 2011;17:1144–1152.
   Google Scholar
• Halilovic A, Patil KA, Bellner L et al. Knockdown of heme oxygenase-2 impairs corneal epithelial cell wound healing. J Cell Physiol 2011;226:1732–1740.
   PubMed Web of Science ®Google Scholar
• Gronert K. Resolution, the grail for healthy ocular inflammation. Exp Eye Res 2010;91:478–485.
   PubMed Web of Science ®Google Scholar
• Sun MH, Pang JH, Chen SL et al. Retinal protection from acute glaucoma-induced ischemia-reperfusion injury through pharmacologic induction of heme oxygenase-1. Invest Ophthalmol Vis Sci 2010;51:4798–4808.
   PubMed Web of Science ®Google Scholar
• Organisciak DT, Darrow RM, Barsalou L et al. Light history and age-related changes in retinal light damage. Invest Ophthalmol Vis Sci 1998;39:1107–1116.
   PubMed Web of Science ®Google Scholar
• Frank RN, Amin RH, Puklin JE. Antioxidant enzymes in the macular retinal pigment epithelium of eyes with neovascular age-related macular degeneration. Am J Ophthalmol 1999;127:694–709.
   PubMed Web of Science ®Google Scholar
• Udono-Fujimori R, Takahashi K, Takeda K et al. Expression of heme oxygenase-1 is repressed by interferon-gamma and induced by hypoxia in human retinal pigment epithelial cells. Eur J Biochem 2004;271:3076–3084.
   PubMedGoogle Scholar
• Chen W, Hunt DM, Lu H et al. Expression of antioxidant protective proteins in the rat retina during prenatal and postnatal development. Invest Ophthalmol Vis Sci 1999;40:744–751.
   Google Scholar
• Sacca GB, Sáenz DA, Jaliffa CO et al. Photic regulation of heme oxygenase activity in the golden hamster retina: involvement of dopamine. J Neurochem 2003;85:534–542.
   PubMed Web of Science ®Google Scholar
• Privitera MG, Potenza M, Bucolo C et al. Hemin, an inducer of heme oxygenase-1, lowers intraocular pressure in rabbits. J Ocul Pharmacol Ther 2007;23:232–239.
   Google Scholar
• Stagni E, Privitera MG, Bucolo C et al. A water-soluble carbon monoxide-releasing molecule (CORM-3) lowers intraocular pressure in rabbits. Br J Ophthalmol 2009;93:254–257.
   Google Scholar
• Bucolo C, Drago F. Carbon monoxide and the eye: implications for glaucoma therapy. Pharmacol Ther 2011;130:191–201.
   PubMed Web of Science ®Google Scholar
• Bergers G, Song S. The role of pericytes in blood-vessel formation and maintenance. Neuro-oncology 2005;7:452–464.
   PubMed Web of Science ®Google Scholar
• Geraldes P, Yagi K, Ohshiro Y et al. Selective regulation of heme oxygenase-1 expression and function by insulin through IRS1/phosphoinositide 3-kinase/Akt-2 pathway. J Biol Chem 2008;283:34327–34336.
   PubMed Web of Science ®Google Scholar
• Hammes HP, Bartmann A, Engel L et al. Antioxidant treatment of experimental diabetic retinopathy in rats with nicanartine. Diabetologia 1997;40:629–634.
   PubMed Web of Science ®Google Scholar
• Arden GB, Sivaprasad S. Hypoxia and oxidative stress in the causation of diabetic retinopathy. Curr Diabetes Rev 2011;7:291–304.
   PubMedGoogle Scholar
• Grochot-Przeczek A, Dulak J, Jozkowicz A. Heme oxygenase-1 in neovascularisation: a diabetic perspective. Thromb Haemost 2010;104:424–431.
   PubMed Web of Science ®Google Scholar
• Yong PH, Zong H, Medina RJ et al. Evidence supporting a role for N-(3-formyl-3,4-dehydropiperidino)lysine accumulation in Müller glia dysfunction and death in diabetic retinopathy. Mol Vis 2010;16:2524–2538.
   PubMed Web of Science ®Google Scholar
• Szabo ME, Gallyas E, Bak I et al. Heme oxygenase-1-related carbon monoxide and flavonoids in ischemic/reperfused rat retina. Invest Ophthalmol Vis Sci 2004;45:3727–3732.
   PubMedGoogle Scholar
• Peng PH, Chao HM, Juan SH et al. Pharmacological preconditioning by low dose cobalt protoporphyrin induces heme oxygenase-1 overexpression and alleviates retinal ischemia-reperfusion injury in rats. Curr Eye Res 2011;36:238–246.
   PubMed Web of Science ®Google Scholar
• Peng PH, Ko ML, Chen CF et al. Haem oxygenase-1 gene transfer protects retinal ganglion cells from ischaemia/reperfusion injury. Clin Sci 2008;115:335–342.
   PubMed Web of Science ®Google Scholar
• Bucolo C, Drago F. Focus on molecules: heme oxygenase-1. Exp Eye Res 2009;89:822–823.
   PubMed Web of Science ®Google Scholar
• Noda M, Fujita K, Lee CH et al. The Principle and the Potential Approach to ROS-Dependent Cytotoxicity by Non-Pharmaceutical Therapies: optimal use of Medical Gases with Antioxidant Properties. Curr Pharm Des 2011.
   Google Scholar
• Abraham NG, da Silva JL, Lavrovsky Y et al. Adenovirus-mediated heme oxygenase-1 gene transfer into rabbit ocular tissues. Invest Ophthalmol Vis Sci 1995;36:2202–2210.
   PubMed Web of Science ®Google Scholar
• Liu MM, Tuo J, Chan CC. Gene therapy for ocular diseases. Br J Ophthalmol 2011;95:604–612.
   Google Scholar