Effects of Losartan, HO-1 Inducers or HO-1 inhibitors on erectile signaling in diabetic rats

Journal of Sexual Medicine

Volumn 6, Issue 12, 2009, Pages 3254-3264

  Abdel Aziz, Mohamed Talaat ^a   El Asmer, Mohamed Farid ^b   Mostafa, Taymour ^a   Atta, Hazem ^a   Mahfouz, Soheir ^a   Fouad, Hanan ^a   Rashed, Laila ^a   Sabry, Dina ^a   Hassouna, Amira ^a   Abdel Aziz, Ahmed Talaat ^a   Senbel, Amira ^c   Demery, Ahmed ^d  

^a CAIRO UNIVERSITY   (Egypt)

^b AIN SHAMS UNIVERSITY   (Egypt)

^c Alexandria University Faculty of Pharmacy   (Egypt)

^d Air Force Specialized Hospital   (Egypt)

Author keywords

Diabetes; Erectile Signaling; HO 1 Inducer; HO 1 Inhibitor; Losartan

Indexed keywords

CYCLIC GMP; HEME OXYGENASE 1; LOSARTAN; MESOPORPHYRIN TIN; PROTOPORPHYRIN COBALT; ANTIHYPERTENSIVE AGENT; CARRIER PROTEIN; CYCLIC GMP-BINDING PROTEIN; GUANOSINE 3',5' PHOSPHATE BINDING PROTEIN; RNA; SIGNAL PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS CAVERNOSUM; DIABETES MELLITUS; DOWN REGULATION; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVITY; ENZYME INDUCTION; ERECTILE DYSFUNCTION; GENE EXPRESSION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; STREPTOZOCIN DIABETES; ANIMAL; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; EVALUATION; EXPERIMENTAL DIABETES MELLITUS; GENETICS; PATHOPHYSIOLOGY; PENIS ERECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TREATMENT OUTCOME;

ANIMALS; ANTIHYPERTENSIVE AGENTS; CARRIER PROTEINS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; ERECTILE DYSFUNCTION; GENE EXPRESSION; HEME OXYGENASE-1; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LOSARTAN; MALE; PENILE ERECTION; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; TREATMENT OUTCOME;

EID: 77950897784     PISSN: 17436095     EISSN: 17436109     Source Type: Journal    
DOI: 10.1111/j.1743-6109.2009.01517.x     Document Type: Article

References (67)

1. Abdel Aziz MT, El-Asmer MF, Mostafa T, Mostafa S, Atta H, Wassef MA, Fouad H, Rashed L, Sabry D, Mahfouz S. Heme oxygenase vs. Nitric oxide synthase in signaling mediating sildenafil citrate action. J Sex Med 2007, 4:1098-107.
2. Abraham NG, Rezzani R, Rodella L, Kruger A, Taller D, Li Volti G, Goodman AI, Kappas A. Overexpression of human heme oxygenase-1 attenuates endothelial cell sloughing in experimental diabetes. Am J Physiol Heart Circ Physiol 2004, 287:H2468-77.
3. Nath KA, Haggard JJ, Croatt AJ, Grande JP, Poss KD, Alam J. The indispensability of heme oxygenase-1 in protecting against acute heme protein-induced toxicity in vivo. Am J Pathol 2000, 156:1527-35.
4. Zhang F, Kaide J, Wei Y, Jiang H, Yu C, Balazy M, Abraham NG, Wang W, Nasjletti A. Carbon monoxide produced by isolated arterioles attenuates pressure-induced vasoconstriction. Am J Physiol Heart Circ Physiol 2001, 281:H350-8.
5. Otterbein LE, Bach FH, Alam J, Soares M, Tao LH, Wysk M, Davis RJ, Flavell RA, Choi AM. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000, 6:422-8.
6. McCoubrey WK, Huang TJ, Maines MD. Heme oxygenase-2 is a hemoprotein and binds heme through heme regulatory motifs that are not involved in heme catalysis. J Biol Chem 1997, 272:12568-74.
7. Kim YM, Choi BM, Kim YS, Kwon YG, Kibbe MR, Billiar TR, Tzeng E. Protective effect of p53 in vascular smooth muscle cells against nitric oxide-induced apoptosis is mediated by up-regulation of heme oxygenase-2. BMB Rep 2008, 41:164-9.
8. Abdel Aziz MT, El-Asmar MF, Mostaf T, Atta H, Wassef MA, Fouad F, Kamal N, Rashed L, Sabry D. Effect of inducible nitric oxide synthase and heme oxygenase inducers or inhibitors on molecular signaling of erectile function. J Clin Biochem Nutr 2005, 37:103-11.
9. Adaikalakoteswari A, Balasubramanyam M, Rema M, Mohan V. Differential gene expression of NADPH oxidase (p22phox) and hemoxygenase-1 in patients with Type 2 diabetes and microangiopathy. Diabet Med 2006, 23:666-74.
10. Morita T, Kourembanas S. Endothelial expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. J Clin Invest 1995, 96:2676-82.
11. Ryter SW, Alam J, Choi AMK. Heme oxygenase-1/carbon monoxide: From basic science to therapeutic applications. Physiol Rev 2006, 86:583-50.
12. Li M, Kim DH, Tsenovoy PL, Peterson SJ, Rezzani R, Rodella LF, Aronow WS, Ikehara S, Abraham NG. Treatment of obese diabetic mice with a heme oxygenase inducer reduces visceral and subcutaneous adiposity, increases adiponectin levels, and improves insulin sensitivity and glucose tolerance. Diabetes 2008, 57:1526-35.
13. Nicolai A, Li M, Kim DH, Peterson SJ, Vanella L, Positano V, Gastaldelli A, Rezzani R, Rodella LF, Drummond G, Kusmic C, L'abbate A, Kappas A, Abraham NG. Heme oxygenase-1 induction remodels adipose tissue and improves insulin sensitivity in obesity-induced diabetic rats. Hypertension 2009, 53:508-15.
14. Sambuceti G, Morbelli S, Vanella L, Kusmic C, Marini C, Massollo M, Augeri C, Corselli M, Ghersi C, Chiavarina B, Rodella LF, L'abbate A, Drummond G, Abraham NG, Frassoni F. Diabetes impairs the vascular recruitment of normal stem cells by oxidant damage; reversed by increases in pAMPK, heme oxygenase-1 and adiponectin. Stem Cells 2009, 27:399-407.
15. Abdel Aziz MT, Al-Asmar MF, Mostafa T, Atta H, Rashed L, Sabry D, Ashour S, Aziz AT. Assessment of heme oxygenase-1 (HO-1) activity in the cavernous tissues of sildenafil citrate-treated rats. Asian J Androl 2007, 9:377-81.
16. Abdel Aziz MT, Al-Asmar MF, Atta H, Shaker O, Fouad HH, Hosni H, Kamal N, Rashed L. Effect of inducers of heme oxygenase-1 on eicosanoids, cAMP and cGMP. levels in rat endothelial cells. Biochim Clinica 2002, 26:352-7.
17. Marks GS, Brien JF, Nakatsu K. What role does the heme-heme oxygenase-carbon monoxide system play in vasoregulation? Am J Physiol Regul Integr Comp Physiol 2003, 285:R522-3.
18. Ryter SW, Otterbein LE, Morse D, Choi AM. Heme oxygenase/carbon monoxide signaling pathways: Regulation and functional significance. Mol Cell Biochem 2002, 234-5:249-63.
19. Ryter SW, Morse D, Choi AM. Carbon monoxide: To boldly go where nitric oxide has gone before. Sci STKE 2004, 230:RE6.
20. Ahmad M, Turkseven S, Mingone CJ, Gupte SA, Wolin MS, Abraham NG. Heme oxygenase-1 gene expression increases vascular relaxation and decreases inducible nitric oxide synthase in diabetic rats. Cell Mol Biol 2005, 51:371-6.
21. Manrique C, Lastra G, Gardner M, Sowers JR. The Renin Angiotensin aldosterone system in hypertension: Roles of insulin resistance and oxidative stress. Med Clin North Am 2009, 93:569-82.
22. Kifor I, Williams GH, Vickers MA, Sullivan MP, Jodbert P, Dluhy RG. Tissue angiotensin II as a modulator of erectile function. I. Angiotensin peptide content, secretion and effects in the corpus cavernosum. J Urol 1997, 157:1920-5.
23. Yang R, Yang B, Wen Y, Fang F, Cui S, Lin G, Sun Z, Wang R, Dai Y. Losartan, an Angiotensin type I receptor, restores erectile function by downregulation of cavernous renin-angiotensin system in streptozocin-induced diabetic rats. J Sex Med 2009, 6:696-707.
24. Ferrario CM, Levy P. Sexual dysfunction in patients with hypertension: Implications for therapy. J Clin Hypertens (Greenwich) 2002, 4:424-32.
25. Ishizaka N, Kathy KG. Heme oxygenase-1 is regulated by angiotensin II in rat vascular smooth muscle cells. Hypertension 1997, 29:790-5.
26. Abdel Aziz MT, El-Asmar MF, Mostafa T, Atta H, Fouad HH, Roshdy NK, Rashed LA, Obaia EA, Sabry DA, Abdel Aziz AT, Drummond G, Olszanecki R. Effect of hemin and carbon monoxide releasing molecule (CORM-3) on cGMP in rat penile tissue. J Sex Med 2008, 5:336-43.
27. Abdel Aziz MT, El-Asmar MF, Haidara M, Atta HM, Roshdy NK, Rashed LA, Sabry D, Youssef MA, Abdel Aziz AT, Moustafa M. Effect of bone marrow-derived mesenchymal stem cells on cardiovascular complications in diabetic rats. Med Sci Monit 2008, 14:BR249-55.
28. Abdulla MH, Sattar MA, Khan MA, Abdullah NA, Johns EJ. Influence of sympathetic and AT-receptor blockade on angiotensin II and adrenergic agonist-induced renal vasoconstrictions in spontaneously hypertensive rats. Acta Physiol 2009, 195:397-404.
29. Bédard EL, Jiang J, Parry N, Wang H, Liu W, Garcia B, Kim P, Chakrabarti S, Buelow R, Zhong R. Peritransplant treatment with cobalt protoporphyrin attenuates chronic renal allograft rejection. Transpl Int 2005, 18:341-9.
30. Abdel Aziz MT, Mostafa T, Atta H, Mahfouz S, Wassef M, Fouad H, Kamel M, Rashed L, Sabry D, Mouhamed O. Effect of HO-1 cDNA-liposome complex transfer on erectile signalling of aged rats. Andrologia 2009, 41:176-83.
31. Abraham NG, Kushida T, McClung J, Weiss M, Quan S, Lafaro R, Darzynkiewicz Z, Wolin M. Heme oxygenase-1 attenuates glucose-mediated cell growth arrest and apoptosis in human microvessel endothelial cells. Circ Res 2003, 93:507-14.
32. Quan S, Yang L, Shnouda S, Schwartzman ML, Nasjletti A, Goodman AI, Abraham NG. Expression of human heme oxygenase-1 in the thick ascending limb attenuates angiotensin II-mediated increase in oxidative injury. Kidney Int 2004, 65:1628-39.
33. Angulo J, Cuevas P, Fernandez A, Gabancho S, Allona A, Martin-Morales A, Moncada I, Saenz de Tejada I. Activation and potentiation of NO/cGMP pathway by NG-hydroxyl-L-arginine in rabbit corpus cavernosum under normoxic and hypoxic conditions and aging. Br J Pharmacol 2003, 138:63-70.
34. Bradford MMA. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-54.
35. Jin L, Foss CE, Zhao X, Mills TM, Wang MH, McCluskey LP, Yaddanapud GS, Falck JR, Imig JD, Webb RC. Cytochrome P450 epoxygenases provide a novel mechanism for penile erection. FASEB J 2006, 20:539-41.
36. Abraham NG, Lutton JD, Levere RD. Heme metabolism and erythropoiesis in abnormal iron states. Role of aminolevulinic acid synthetase and heme oxygenase. Exp Haematol 1985, 13:833-43.
37. Giuliano F, Bernabe J, Jardin A, Rousseau JP. Antierectile role of the sympathetic nervous system in rats. J Urol 1993, 150:519-24.
38. Ushiyama M, Morita T, Kuramochi T, Yagi S, Katayama S. Erectile dysfunction in hypertensive rats results from impairment of the relaxation evoked by neurogenic carbon monoxide and nitric oxide. Hypertens Res 2004, 27:253-61.
39. Zvara P, Spiess PE, Merlin SL, Begin LR, Brock GB. Neurogenic erectile dysfunction: The course of nicotinamide adenine dinucleotide phosphate diaphorase-positive nerve fibers on the surface of the prostate. Urology 1996, 47:146-51.
40. Martinez L, Brock G, Rocha-Trigo F, Hsu G, Lue TF, Tanagho EA. Rat model for the study of penile erection: Pharmacologic and electrical-stimulation parameters. Eur Urol 1994, 25:62-70.
41. Hedlund P, Ny L, Alm P, Andersson KE. Cholinergic nerves in human corpus cavernosum and spongiosum contain nitric oxide synthase and heme oxygenase. J Urol 2000, 164:868-75.
42. Di Filippo C, Marfella R, Cuzzocrea S, Piegari E, Petronella P, Giugliano D, Rossi F, D'Amico M. Hyperglycemia in streptozotocin-induced diabetic rat increases infarct size associated with low levels of myocardial HO-1 during ischemia/reperfusion. Diabetes 2005, 54:803-10.
43. Rodella L, Lamon BD, Rezzani R, Sangras B, Goodman AI, Falck JR, Abraham NG. Carbon monoxide and biliverdin prevent endothelial cell sloughing in rats with type I diabetes. Free Radic Biol Med 2006, 40:2198-205.
44. Kruger AL, Peterson S, Turkseven S, Kaminski PM, Zhang FF, Quan S, Wolin MS, Abraham NG. D-4F induces heme oxygenase-1 and extracellular superoxide dismutase, decreases endothelial cell sloughing, and improves vascular reactivity in rat model of diabetes. Circulation 2005, 111:3126-34.
45. Alba G, El Bekay R, Chacón P, Reyes ME, Ramos E, Oliván J, Jiménez J, López JM, Martín-Nieto J, Pintado E, Sobrino F. Heme oxygenase-1 expression is down-regulated by angiotensin II and under hypertension in human neutrophils. J Leukoc Biol 2008, 84:397-405.
46. Choi AM, Tucker RW, Carlson SG, Weigand G, Holbrook NJ. Calcium mediates expression of stress-response genes in prostaglandin A2-induced growth arrest. FASEB J 1994, 8:1048-54.
47. Ishizaka N, Aizawa T, Mori I, Taguchi J, Yazaki Y, Nagai R, Ohno M. Heme oxygenase-1 is upregulated in the rat heart in response to chronic administration of angiotensin II. Am J Physiol Heart Circ Physiol 2000, 279:H672-8.
48. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 1994, 74:1141-8.
49. Ushio-Fukai M, Zafari AM, Fukui T, Ishizaka N, Griendling KK. p22-phox is a critical component of the superoxide generating NADH/NADPH oxidase system and angiotensin induced hypertrophy in cultured vascular smooth muscle cells. J Biol Chem 1996, 271:23317-21.
50. Baumgartner-Parzer SM, Wagner L, Pettermann M, Grillari J, Gessl A, Waldhausl W. High-glucose-triggered apoptosis in cultured endothelial cells. Diabetes 1995, 44:1323-7.
51. Zou MH, Shi C, Cohen RA. High glucose via peroxynitrite causes tyrosine nitration and inactivation of prostacyclin synthase that is associated with thromboxane/prostaglandin H2 receptor-mediated apoptosis and adhesion molecular expression in cultured human aortic endothelial cells. Diabetes 2002, 51:198-203.
52. Curcio F, Ceriello A. Decreased cultured endothelial cell proliferation in high glucose medium is reversed by antioxidants: New insights on the pathophysiological mechanisms of diabetic vascular complications. In Vitro Cell Dev Biol 1992, 28A:787-90.
53. Ceriello A, dello RP, Amstad P, Cerutti P. High glucose induces antioxidant enzymes in human endothelial cells in culture. Evidence linking hyperglycemia and oxidative stress. Diabetes 1996, 45:471-7.
54. Du X, Stocklauser-Färber K, Rösen P. Generation of reactive oxygen intermediates, activation of NF-κB, and induction of apoptosis in human endothelial cells by glucose: Role of nitric oxide synthase? Free Radic Biol Med 1999, 27:752-63.
55. Baynes JW. Role of oxidative stress in development of complications in diabetes. Diabetes 1991, 40:405-12.
56. Karpen CW, Cataland S, O'Dorisio TM, Panganamala RV. Production of 12-hydroxyeicosatetraenoic acid and vitamin E status in platelets from type I human diabetic subjects. Diabetes 1985, 34:526-31.
57. Flammer AJ, Hermann F, Wiesli P, Noll G, Lehmam R. Effect of losartan, compared with atenolol on endothelial function and oxidative stress in patients with type 2 diabetes and hypertension. J Hypertens 2007, 25:785-91.
58. Park K, Shin JW, Oh JK, Ryu KS, Kim SW, Paick JS. Restoration of erectile capacity in normotensive aged rats by modulation of angiotensin receptor type 1. J Androl 2005, 26:123-8.
59. Toblli JE, Stella I, Mazza ON, Ferder L, Inserra F. The effect of different antihypertensive drugs on cavernous tissue in experimental chronic renal insufficiency. J Nephrol 2006, 19:419-28.
60. Llisterri JL, Lozano Vidal JV, Aznar Vicente J, Argaya Roca M, Pol Bravo C, Sanchez Zamorano MA, Ferrario CM. Sexual dysfunction in hypertensive patients treated with losartan. Am J Med Sci 2001, 321:336-41.
61. Toblli JE, Cao G, Lombraña A, Rivero M. Functional and morphological improvement in erectile tissue of hypertensive rats by long-term combined therapy with phosphodiesterase type 5 inhibitor and losartan. J Sex Med 2007, 4:1291-303.
62. Abdel Aziz MT, Mostafa T, Atta H, Wassef MA, Fouad HH, Rashed LA, Sabry D. Putative role of carbon monoxide signaling pathway in penile erectile function. J Sex Med 2009, 6:49-60.
63. Abdel Aziz MT, Mostafa T, Atta H, Rashed L, Marzouk SA, Obaia1 EM, Sabry D, Hassouna AA, El-Shehaby AM, Abdel Aziz AT. Oral phosphodiesterase-5 inhibitors: Effect of heme oxygenase inhibition on cGMP signaling in rat cavernous tissue. Andrologia 2007, 39:66-70.
64. Lau DH, Kommu S, Mumtaz FH, Morgan RJ, Thompson CS, Mikhailidis DP. The management of phosphodiesterase-5 (PDE5) inhibitor failure. Curr Vasc Pharmacol 2006, 4:89-93.
65. Li XL, Li BY, Gao HQ, Cheng M, Xu L, Li XH, Ma YB. Effects of grape seed proanthocyanidin extracts on aortic pulse wave velocity in streptozocin induced diabetic rats. Biosci Biotechnol Biochem 2009, 73:1348-54.
66. Di Noia MA, Van Driesche S, Palmieri F, Yang LM, Quan S, Goodman AI, Abraham NG. Heme oxygenase-1 enhances renal mitochondrial transport carriers and cytochrome C oxidase activity in experimental diabetes. J Biol Chem 2006, 28:15687-93.
67. Calles-Escandon J, Cipolla M. Diabetes and endothelial dysfunction: A clinical perspective. Endocr Rev 2001, 22:36-52.