Heme oxygenase in the retina in diabetes

Current Eye Research

Volumn 27, Issue 5, 2003, Pages 301-308

  Cukiernik, Mark ^a   Mukherjee, Suranjana ^a   Downey, Donal ^a   Chakabarti, Subrata ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Blood flow; Diabetes; Heme oxygenase; mRNA; Retina

Indexed keywords

ENDOTHELIN 1; GLUCOSE; GLYCOSYLATED HEMOGLOBIN; HEME OXYGENASE; HEME OXYGENASE 1; HEME OXYGENASE 2; HEME OXYGENASE INHIBITOR; MESSENGER RNA; MOLSIDOMINE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE; PROTOPORPHYRIN TIN; STREPTOZOCIN; UNCLASSIFIED DRUG;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; COLOR ULTRASOUND FLOWMETRY; CONTROLLED STUDY; DIABETES MELLITUS; DRUG EFFECT; ENZYME LOCALIZATION; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZATION; RAT; RETINA; RETINA BLOOD VESSEL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; STREPTOZOCIN DIABETES; TISSUE DISTRIBUTION; UPREGULATION;

ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; ENDOTHELIN-1; ENZYME INHIBITORS; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HEMOGLOBIN A, GLYCOSYLATED; MALE; METALLOPORPHYRINS; MOLSIDOMINE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PROTOPORPHYRINS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; UP-REGULATION;

EID: 0344413040     PISSN: 02713683     EISSN: None     Source Type: Journal    
DOI: 10.1076/ceyr.27.5.301.17227     Document Type: Article

References (56)

1. Zimmet P, Alberti KG, Shaw J. Global and societal implications of the diabetes epidemic. Nature. 2001;414:782-787.
2. Songer TJ. The economic costs of NIDDM. Diabetes Metab Rev. 1992;8:389-404.
3. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001;414:813-820.
4. DCCT Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med. 1993;329:977-986.
5. Candido R, Allen TJ. Haemodynamics in microvascular complications in type 1 diabetes. Diabetes Metab Res Rev. 2002;18:286-304.
6. Chen S, Evans T, Deng D, Cukiernik M, Chakrabarti S. Hyperhexosemia induced functional and structural changes in the kidneys: Role of endothelins. Nephron. 2002; 90:86-94.
7. Deng D, Evans T, Mukherjee K, Downey D, Chakrabarti S. Diabetes-induced vascular dysfunction in the retina: Role of endothelins. Diabetologia. 1999;42:1228-1234.
8. Giugliano D, Ceriello A, Paolisso G. Oxidative stress and diabetic vascular complications. Diabetes Care. 1996;19: 257-267.
9. Chakrabarti S, Cukiernik M, Hileeto D, Evans T, Chen S. Role of vasoactive factors in the pathogenesis of early changes in diabetic retinopathy. Diabetes Metab Res Rev. 2000;16:393-407.
10. Maines MD. The heme oxygenase system: A regulator of second messenger gases. Annu Rev Pharmacol Toxicol. 1997;37:517-554.
11. Cosso L, Maineri EP, Traverse N, Rosatto N, Pronzato MA, Cottalasso D, Marinari UM, Odetti P. Induction of heme oxygenase 1 in liver of spontaneously diabetic rats. Free Radic Res. 2001;34:189-191.
12. Nishimura RN, Dwyer BE, Lu SY. Localization of heme oxygenase in rat retina: Effect of light adaptation. Neurosci Lett. 1996;205:13-16.
13. Furchgott RF, Jothianandan D. Endothelium-dependent and -independent vasodilation involving cyclic GMP: Relaxation induced by nitric oxide, carbon monoxide and light. Blood Vessels. 1991;28:52-61.
14. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science. 1987;235:1043-1046.
15. Lin F, Girotti AW. Hemin-enhanced resistance of human leukemia cells to oxidative killing: Antisense determination of ferritin involvement. Arch Biochem Biophys. 1998; 352:51-58.
16. Durante W, Christodoulides N, Cheng K, Peyton KJ, Sunahara RK, Schafer AI. cAMP induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle. Am J Physiol. 1997;273:H317-H323.
17. Foresti R, Motterlini R. The heme oxygenase pathway and its interaction with nitric oxide in the control of cellular homeostasis. Free Radic Res. 1999;31:459-475.
18. Chen S, Apostolova MD, Cherian MG, Chakrabarti S. Interaction of endothelin-1 with vasoactive factors in mediating glucose-induced increased permeability in endothelial cells. Lab Invest. 2000;80:1311-1321.
19. Tulis DA, Durante W, Peyton KJ, Evans AJ, Schafer AI. Heme oxygenase-1 attenuates vascular remodeling following balloon injury in rat carotid arteries. Atherosclerosis. 2001;155:113-122.
20. Benigni A, Zoja C, Noris M, Corna D, Benedetti G, Bruzzi I, Todeschini M, Remuzzi G. Renoprotection by nitric oxide donor and lisinopril in the remnant kidney model. Am J Kidney Dis. 1999;33:746-753.
21. Evans T, Xi DD, Mukherjee K, Downey D, Chakrabarti S. Endothelins, their receptors, and retinal vascular dysfunction in galactose-fed rats. Diabetes Res Clin Pract. 2000;48:75-85.
22. Hileeto D, Cukiernik M, Mukherjee S, Evans T, Barbin Y, Downey D, Karmazyn M, Chakrabarti S. Contributions of endothelin-1 and sodium hydrogen exchanger-1 in the diabetic myocardium. Diabetes Metab Res Rev. 2002;18:386-394.
23. Csonka C, Varga E, Kovacs P, Ferdinandy P, Blasig IE, Szilvassy Z, Tosaki A. Heme oxygenase and cardiac function in ischemic/reperfused rat hearts. Free Radic Biol Med. 1999;27:119-126.
24. McCoubrey WK, Jr., Ewing JF, Maines MD. Human heme oxygenase-2: Characterization and expression of a full-length cDNA and evidence suggesting that the two HO-2 transcripts may differ by choice of poly-adenylation signal. Arch Biochem Biophys. 1992;295:13-20.
25. Yan SD, Schmidt AM, Anderson GM, Zhang J, Brett J, Zou YS, Pinsky D, Stern D. Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem. 1994;269:9889-9897.
26. Kappas A, Maines MD. Tin: A potent inducer of heme oxygenase in kidney. Science. 1976;192:60-62.
27. Stocker R. Induction of haem oxygenase as a defence against oxidative stress. Free Radic Res Commun. 1990; 9:101-112.
28. Paredi P, Biernacki W, Invernizzi G, Kharitonov SA, Barnes PJ. Exhaled carbon monoxide levels elevated in diabetes and correlated with glucose concentration in blood: A new test for monitoring the disease? Chest. 1999;116: 1007-1011.
29. 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.
30. Weiss G, Werner-Felmayer G, Werner ER, Grunewald K, Wachter H, Hentze MW. Iron regulates nitric oxide synthase activity by controlling nuclear transcription. J Exp Med. 1994;180:969-976.
31. Foresti R, Motterlini R. The heme oxygenase pathway and its interaction with nitric oxide in the control of cellular homeostasis. Free Radic Res. 1999;31:459-475.
32. Ramos KS, Lin H, McGrath JJ. Modulation of cyclic guanosine monophosphate levels in cultured aortic smooth muscle cells by carbon monoxide. Biochem Pharmacol. 1989;38:1368-1370.
33. Turcanu V, Dhouib M, Poindron P. Nitric oxide synthase inhibition by haem oxygenase decreases macrophage nitricoxide-dependent cytotoxicity: A negative feedback mechanism for the regulation of nitric oxide production. Res Immunol. 1998;149:741-744.
34. White KA, Marietta MA. Nitric oxide synthase is a cytochrome P-450 type hemoprotein. Biochemistry. 1992;31:6627-6631.
35. Utz J, Ullrich V Carbon monoxide relaxes ileal smooth muscle through activation of guanylate cyclase. Biochem Pharmacol. 1991;41:1195-1201.
36. Hartsfield CL, Alam J, Cook JL, Choi AM. Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide. Am J Physiol. 1997; 273:L980-L988.
37. McCoubrey WK, Jr., Cooklis MA, Maines MD. The structure, organization and differential expression of the rat gene encoding biliverdin reductase. Gene. 1995;160:235-240.
38. McCoubrey WK, Jr., Eke B, Maines MD. Multiple transcripts encoding heme oxygenase-2 in rat testis: Developmental and cell-specific regulation of transcripts and protein. Biol Reprod. 1995;53:1330-1338.
39. Rotenberg MO, Maines MD. Characterization of a cDNA-encoding rabbit brain heme oxygenase-2 and identification of a conserved domain among mammalian heme oxygenase isozymes: Possible heme-binding site? Arch Biochem Biophys. 1991;290:336-344.
40. Gosling RG. Doppler ultrasound assessment of occlusive arterial disease. Practitioner. 1978;220:599-609.
41. Senn BC, Kaiser HJ, Schotzau A, Flammer J. Reproducibility of color Doppler imaging in orbital vessels. Ger J Ophthalmol. 1996;5:386-391.
42. Rojanapongpun P, Morrison B, Drance SM. Reproducibility of transcranial Doppler ultrasound examinations of the ophthalmic artery flow velocity. Br J Ophthalmol. 1993;77:22-24.
43. Tranquart F, Berges O, Koskas P, Arsene S, Rossazza C, Pisella PJ, Pourcelot L. Color doppler imaging of orbital vessels: Personal experience and literature review. J Clin Ultrasound. 2003;31:258-273.
44. Dimitrova G, Kato S, Yamashita H, Tamaki Y, Nagahara M, Fukushima H, Kitano S. Relation between retrobulbar circulation and progression of diabetic retinopathy. Br J Ophthalmol. 2003;87:622-625.
45. Rassam SM, Patel V, Kohner EM. The effect of experimental hypertension on retinal vascular autoregulation in humans: A mechanism for the progression of diabetic retinopathy. Exp Physiol. 1995;80:53-68.
46. Kohner EM, Patel V, Rassam SM. Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy. Diabetes. 1995;44:603-607.
47. Maines MD. Zinc protoporphyrin is a selective inhibitor of heme oxygenase activity in the neonatal rat. Biochim Biophys Acta. 1981;673:339-350.
48. Chakder S, Rathi S, Ma XL, Rattan S. Heme oxygenase inhibitor zinc protoporphyrin IX causes an activation of nitric oxide synthase in the rabbit internal anal sphincter. J Pharmacol Exp Ther. 1996;277:1376-1382.
49. Kutty RK, Maines MD. Hepatic heme metabolism: Possible role of biliverdin in the regulation of heme oxygenase activity. Biochem Biophys Res Commun. 1984;122:40-46.
50. Ow DW, Sundaresan V, Rothstein DM, Brown SE, Ausubel FM. Promoters regulated by the glnG (ntrC) and nifA gene products share a heptameric consensus sequence in the -15 region. Proc Natl Acad Sci USA. 1983;80:2524-2528.
51. Dore S, Takahashi M, Ferris CD, Zakhary R, Hester LD, Guastella D, Snyder SH. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci USA. 1999;96:2445-2450.
52. Stocker R, Glazer AN, Ames BN. Antioxidant activity of albumin-bound bilirubin. Proc Natl Acad Sci USA. 1987;84:5918-5922.
53. Hammes HP, Bartmann A, Engel L, Wulfroth P. Antioxidant treatment of experimental diabetic retinopathy in rats with nicanartine. Diabetologia. 1997;40:629-634.
54. Chen K, Gunter K, Maines MD. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J Neurochem. 2000;75:304-313.
55. da Silva JL, Stoltz RA, Dunn MW, Abraham NG, Shibahara S. 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.
56. Hayashi K, Haneda M, Koya D, Maeda S, Isshiki K, Kikkawa R. Enhancement of glomerular heme oxygenase-1 expression in diabetic rats. Diabetes Res Clin Pract. 2001;52:85-96.