Journal of Cardiac Failure
Volume 15, Issue 7 , Pages 616-628 , September 2009

Upregulating the Heme Oxygenase System Suppresses Left Ventricular Hypertrophy in Adult Spontaneously Hypertensive Rats for 3 Months

  • Joseph Fomusi Ndisang, PhD

      Affiliations

    • Corresponding Author InformationCorrespondence to: Dr. Joseph Fomusi Ndisang, Department of Physiology, College of Medicine, University of Saskatchewan, 107 Wiggins Road, Saskatoon, SK, Canada S7N 5E5. Tel: (306) 966-6533; Fax: (306) 966-6532.
    • ,
  • Ashok Jadhav, DVM, PhD

Received 13 August 2008 ,Revised 9 February 2009 ,Accepted 19 February 2009.

References 

  1. Iglarz M, Touyz RM, Viel EC, Amiri F, Schiffrin EL. Involvement of oxidative stress in the profibrotic action of aldosterone. Interaction wtih the renin-angiotension system. Am J Hypertens. 2004;17:597–603
  2. Li X, Meng Y, Wu P, Zhang Z, Yang X. Angiotensin II and Aldosterone stimulating NF-kappaB and AP-1 activation in hepatic fibrosis of rat. Regul Pept. 2007;138:15–25
  3. Plo I, Lautier D, Levade T, Sekouri H, Jaffrezou JP, Laurent G, et al. Phosphatidylcholine-specific phospholipase C and phospholipase D are respectively implicated in mitogen-activated protein kinase and nuclear factor kappaB activation in tumour-necrosis-factor-alpha-treated immature acute-myeloid-leukaemia cells. Biochem J. 2000;351(Pt 2):459–467
  4. Makita N, Yasuda H. Alterations of phosphoinositide-specific phospholipase C and protein kinase C in the myocardium of spontaneously hypertensive rats. Basic Res Cardiol. 1990;85:435–443
  5. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol. 2006;7:589–600
  6. Christ M, Meyer C, Sippel K, Wehling M. Rapid aldosterone signaling in vascular smooth muscle cells: involvement of phospholipase C, diacylglycerol and protein kinase C alpha. Biochem Biophys Res Commun. 1995;213:123–129
  7. Fiebeler A, Schmidt F, Muller DN, Park JK, Dechend R, Bieringer M, et al. Mineralocorticoid receptor affects AP-1 and nuclear factor-kappab activation in angiotensin II-induced cardiac injury. Hypertension. 2001;37:787–793
  8. Abraham NG, Kappas A. Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev. 2008;60:79–127
  9. 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;156:1527–1535
  10. Hintze KJ, Theil EC. DNA and mRNA elements with complementary responses to hemin, antioxidant inducers, and iron control ferritin-L expression. Proc Natl Acad Sci U S A. 2005;102:15048–15052
  11. Lavrovsky Y, Schwartzman ML, Levere RD, Kappas A, Abraham NG. Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc Natl Acad Sci USA. 1994;91:5987–5991
  12. Lavrovsky Y, Song CS, Chatterjee B, Roy AK. Age-dependent increase of heme oxygenase-1 gene expression in the liver mediated by NFkappaB. Mech Ageing Dev. 2000;114:49–60
  13. Sasaki T, Takahashi T, Maeshima K, Shimizu H, Toda Y, Morimatsu H, et al. Heme arginate pretreatment attenuates pulmonary NF-kappaB and AP-1 activation induced by hemorrhagic shock via heme oxygenase-1 induction. Med Chem. 2006;2:271–274
  14. Jadhav A, Torlakovic E, Ndisang JF. Interaction Among Heme Oxygenase, Nuclear Factor-{kappa}B, and Transcription Activating Factors in Cardiac Hypertrophy in Hypertension. Hypertension. 2008;52:910–917
  15. Turkseven S, Kruger A, Mingone CJ, Kaminski P, Inaba M, Rodella LF, et al. Antioxidant mechanism of heme oxygenase-1 involves an increase in superoxide dismutase and catalase in experimental diabetes. Am J Physiol Heart Circ Physiol. 2005;289:H701–H707
  16. Vreman HJ, Ekstrand BC, Stevenson DK. Selection of metalloporphyrin heme oxygenase inhibitors based on potency and photoreactivity. Pediatr Res. 1993;33:195–200
  17. Ndisang JF, Lane N, Jadhav A. Crosstalk between the heme oxygenase system, aldosterone, and phospholipase C in hypertension. J Hypertens. 2008;26:1188–1199
  18. Ndisang JF, Zhao W, Wang R. Selective regulation of blood pressure by heme oxygenase-1 in hypertension. Hypertension. 2002;40:315–321
  19. Rikitake Y, Oyama N, Wang CY, Noma K, Satoh M, Kim HH, et al. Decreased perivascular fibrosis but not cardiac hypertrophy in ROCK1+/- haploinsufficient mice. Circulation. 2005;112:2959–2965
  20. Ndisang JF, Wu L, Zhao W, Wang R. Induction of heme oxygenase-1 and stimulation of cGMP production by hemin in aortic tissues from hypertensive rats. Blood. 2003;101:3893–3900
  21. Delanty N, Reilly MP, Pratico D, Lawson JA, McCarthy JF, Wood AE, et al. 8-epi PGF2 alpha generation during coronary reperfusion. A potential quantitative marker of oxidant stress in vivo. Circulation. 1997;95:2492–2499
  22. Pardo Mindan FJ, Panizo A. Alterations in the extracellular matrix of the myocardium in essential hypertension. Eur Heart J. 1993;14(Suppl J):12–14
  23. Levick S, Loch D, Rolfe B, Reid RC, Fairlie DP, Taylor SM, et al. Antifibrotic activity of an inhibitor of group IIA secretory phospholipase A2 in young spontaneously hypertensive rats. J Immunol. 2006;176:7000–7007
  24. Belik J, Jankov RP, Pan J, Tanswell AK. Peroxynitrite inhibits relaxation and induces pulmonary artery muscle contraction in the newborn rat. Free Radic Biol Med. 2004;37:1384–1392
  25. Silvestre JS, Robert V, Heymes C, Aupetit-Faisant B, Mouas C, Moalic JM, et al. Myocardial production of aldosterone and corticosterone in the rat. Physiological regulation. J Biol Chem. 1998;273:4883–4891
  26. Lee KY, Ito K, Hayashi R, Jazrawi EP, Barnes PJ, Adcock IM. NF-kappaB and activator protein 1 response elements and the role of histone modifications in IL-1beta-induced TGF-beta1 gene transcription. J Immunol. 2006;176:603–615
  27. Xia C, Bao Z, Yue C, Sanborn BM, Liu M. Phosphorylation and regulation of G-protein-activated phospholipase C-beta 3 by cGMP-dependent protein kinases. J Biol Chem. 2001;276:19770–19777
  28. Sun Y, Zhang J, Lu L, Chen SS, Quinn MT, Weber KT. Aldosterone-induced inflammation in the rat heart: role of oxidative stress. Am J Pathol. 2002;161:1773–1781
  29. Arima S, Kohagura K, Xu HL, Sugawara A, Abe T, Satoh F, et al. Nongenomic vascular action of aldosterone in the glomerular microcirculation. J Am Soc Nephrol. 2003;14:2255–2263
  30. Ndisang JF, Wang R, Vannacci A, Marzocca C, Fantappie O, Mazzanti R, et al. Haeme oxygenase-1 and cardiac anaphylaxis. Br J Pharmacol. 2001;134:1689–1696
  31. He Z, Hu Y, Feng L, Lu Y, Bao D, Xi Y, et al. Association between HMOX-1 genotype and cardiac function during exercise. Appl Physiol Nutr Metab. 2008;33:450–460
  32. Segers VF, Lemmens K, Hendrickx J, Sys SU, De Keulenaer GW. Inhibition of heme oxygenase-1 impairs cardiac muscle sensitivity to beta-adrenergic stimulation. Basic Res Cardiol. 2005;100:224–230
  33. Kiemer AK, Vollmar AM, Bilzer M, Gerwig T, Gerbes AL. Atrial natriuretic peptide reduces expression of TNF-alpha mRNA during reperfusion of the rat liver upon decreased activation of NF-kappaB and AP-1. J Hepatol. 2000;33:236–246
  34. Rosendorff C. The renin-angiotensin system and vascular hypertrophy. J Am Coll Cardiol. 1996;28:803–812
  35. Botros FT, Schwartzman ML, Stier CT, Goodman AI, Abraham NG. Increase in heme oxygenase-1 levels ameliorates renovascular hypertension. Kidney Int. 2005;68:2745–2755
  36. Zhao D, Vellaichamy E, Somanna NK, Pandey KN. Guanylyl cyclase/natriuretic peptide receptor-A gene disruption causes increased adrenal angiotensin II and aldosterone levels. Am J Physiol Renal Physiol. 2007;293:F121–F127
  37. Oda S, Sano T, Morishita Y, Matsuda Y. Pharmacological profile of HS-142-1, a novel nonpeptide atrial natriuretic peptide (ANP) antagonist of microbial origin. II. Restoration by HS-142-1 of ANP-induced inhibition of aldosterone production in adrenal glomerulosa cells. J Pharmacol Exp Ther. 1992;263:241–245
  38. Pascoe L, Curnow KM, Slutsker L, Connell JM, Speiser PW, New MI, et al. Glucocorticoid-suppressible hyperaldosteronism results from hybrid genes created by unequal crossovers between CYP11B1 and CYP11B2. Proc Natl Acad Sci USA. 1992;89:8327–8331
  39. Alam J, Cai J, Smith A. Isolation and characterization of the mouse heme oxygenase-1 gene. Distal 5' sequences are required for induction by heme or heavy metals. J Biol Chem. 1994;269:1001–1009
  40. Apak R, Guclu K, Ozyurek M, Karademir SE, Altun M. Total antioxidant capacity assay of human serum using copper(II)-neocuproine as chromogenic oxidant: the CUPRAC method. Free Radic Res. 2005;39:949–961
  41. Fenning A, Harrison G, Rose'meyer R, Hoey A, Brown L. l-Arginine attenuates cardiovascular impairment in DOCA-salt hypertensive rats. Am J Physiol Heart Circ Physiol. 2005;289:H1408–H1416
  42. Gutsmann-Conrad A, Pahlavani MA, Heydari AR, Richardson A. Expression of heat shock protein 70 decreases with age in hepatocytes and splenocytes from female rats. Mech Ageing Dev. 1999;107:255–270
  43. Wang R, Shamloul R, Wang X, Meng Q, Wu L. Sustained normalization of high blood pressure in spontaneously hypertensive rats by implanted hemin pump. Hypertension. 2006;48:685–692
  44. Hu CM, Chen YH, Chiang MT, Chau LY. Heme oxygenase-1 inhibits angiotensin II-induced cardiac hypertrophy in vitro and in vivo. Circulation. 2004;110:309–316
  45. Tongers J, Fiedler B, Konig D, Kempf T, Klein G, Heineke J, et al. Heme oxygenase-1 inhibition of MAP kinases, calcineurin/NFAT signaling, and hypertrophy in cardiac myocytes. Cardiovasc Res. 2004;63:545–552
  46. Yoshida T, Maulik N, Ho YS, Alam J, Das DK. H(mox-1) constitutes an adaptive response to effect antioxidant cardioprotection: A study with transgenic mice heterozygous for targeted disruption of the Heme oxygenase-1 gene. Circulation. 2001;103:1695–1701
  47. Liu X, Pachori AS, Ward CA, Davis JP, Gnecchi M, Kong D, et al. Heme oxygenase-1 (HO-1) inhibits postmyocardial infarct remodeling and restores ventricular function. Faseb J. 2006;20:207–216
  48. Mark A, Hock T, Kapturczak MH, Agarwal A, Hill-Kapturczak N. Induction of heme oxygenase-1 modulates the profibrotic effects of transforming growth factor-beta in human renal tubular epithelial cells. Cell Mol Biol (Noisy-le-grand). 2005;51:357–362
  49. Keyse SM, Tyrrell RM. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA. 1989;86:99–103

 Supported by the Heart & Stroke Foundation of Saskatchewan, Canada, and the Canadian Institutes of Health Research/University of Saskatchewan College of Medicine Bridge funding.

PII: S1071-9164(09)00060-8

doi: 10.1016/j.cardfail.2009.02.003

Journal of Cardiac Failure
Volume 15, Issue 7 , Pages 616-628 , September 2009

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