Dehydroepiandrosterone restores right ventricular structure and function in rats with severe pulmonary arterial hypertension

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 304, Issue 12, 2013, Pages

  Alzoubi, Abdallah ^a   Toba, Michie ^a   Abe, Kohtaro ^a,b   O'Neill, Kealan D ^a   Rocic, Petra ^a   Fagan, Karen A ^a,b   McMurtry, Ivan F ^a,b   Oka, Masahiko ^a,b  

^a UNIVERSITY OF SOUTH ALABAMA   (United States)

^b UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

Author keywords

Dehydroepiandrosterone; Oxidative stress; Pulmonary arterial hypertension; Rho kinase; Right ventricle; SU5416

Indexed keywords

PRASTERONE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RHO KINASE; SEMAXANIB; STAT3 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFECT; ECHOCARDIOGRAPHY; ENZYME ACTIVITY; HEART INDEX; HEART MUSCLE FIBROSIS; HEART PROTECTION; HEART RIGHT VENTRICLE; HEART RIGHT VENTRICLE FUNCTION; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PULMONARY HYPERTENSION; RAT; SYSTOLIC HYPERTENSION;

DEHYDROEPIANDROSTERONE; OXIDATIVE STRESS; PULMONARY ARTERIAL HYPERTENSION; RHO KINASE; RIGHT VENTRICLE; SU5416;

ANIMALS; ANOXIA; APOPTOSIS; BLOOD PRESSURE; DEHYDROEPIANDROSTERONE; FIBROSIS; GENE EXPRESSION; HEART VENTRICLES; HYPERTENSION, PULMONARY; INDOLES; MALE; NADP; NFATC TRANSCRIPTION FACTORS; OXIDATIVE STRESS; PULMONARY ARTERY; PYRROLES; RATS; RATS, SPRAGUE-DAWLEY; RHO-ASSOCIATED KINASES; STAT3 TRANSCRIPTION FACTOR; VENTRICULAR DYSFUNCTION;

EID: 84879186805     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00746.2012     Document Type: Article

References (54)

1. Abe K, Toba M, Alzoubi A, Ito M, Fagan KA, Cool CD, Voelkel NF, McMurtry IF, Oka M. Formation of plexiform lesions in experimental severe pulmonary arterial hypertension. Circulation 121: 2747-2754, 2010.
2. Arkles JS, Opotowsky AR, Ojeda J, Rogers F, Liu T, Prassana V, Marzec L, Palevsky HI, Ferrari VA, Forfia PR. Shape of the right ventricular Doppler envelope predicts hemodynamics and right heart function in pulmonary hypertension. Am J Respir Crit Care Med 183: 268-276, 2011.
3. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal-Ginard B, Anversa P. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114: 763-776, 2003.
4. Bhuiyan MS, Fukunaga K. Targeting sigma-1 receptor signaling by endogenous ligands for cardioprotection. Expert Opin Ther Targets 15: 145-155, 2011.
5. Bogaard HJ, Abe K, Vonk Noordegraaf A, Voelkel NF. The right ventricle under pressure: cellular and molecular mechanisms of right-heart failure in pulmonary hypertension. Chest 135: 794-804, 2009.
6. Bogaard HJ, Natarajan R, Henderson SC, Long CS, Kraskauskas D, Smithson L, Ockaili R, McCord JM, Voelkel NF. Chronic pulmonary artery pressure elevation is insufficient to explain right heart failure. Circulation 120: 1951-1960, 2009.
7. Bonnet S, de la-Roque E, Bégueret H, Marthan R, Fayon M, Dos Santos P, Savineau JP, Baulieu EE. Dehydroepiandrosterone (DHEA) prevents and reverses chronic hypoxic pulmonary hypertension. Proc Natl Acad Sci USA 100: 9488-9493, 2003.
8. Bowers R, Cool C, Murphy RC, Tuder RM, Hopken MW, Flores SC, Voelkel NF. Oxidative stress in severe pulmonary hypertension. Am J Respir Crit Care Med 169: 764-769, 2004.
9. Chan SY, Loscalzo J. Pathogenic mechanisms of pulmonary arterial hypertension. J Mol Cell Cardiol 44: 14-30, 2008.
10. Dong M, Liao JK, Fang F, Lee AP, Yan BP, Liu M, Yu CM. Increased Rho kinase activity in congestive heart failure. Eur J Heart Fail 14: 965-973, 2012.
11. Dong M, Yan BP, Liao JK, Lam YY, Yip GW, Yu CM. Rho-kinase inhibition: a novel therapeutic target for the treatment of cardiovascular diseases. Drug Discov Today 15: 622-629, 2010.
12. de La Roque ESJ, Metivier AC, Billes MA, Kraemer JP, Doutreleau S, Jougon J, Marthan R, Moore N, Fayon M, Baulieu EE, Dromer C. Dehydroepiandrosterone (DHEA) improves pulmonary hypertension in chronic obstructive pulmonary disease (COPD): a pilot study. Ann Endocrinol (Paris) 73: 20-25, 2012.
13. Faber MJ, Dalinghaus M, Lankhuizen IM, Bezstarosti K, Verhoeven AJ, Duncker DJ, Helbing WA, Lamers JM. Time dependent changes in cytoplasmic proteins of the right ventricle during prolonged pressure overload. J Mol Cell Cardiol 43: 197-209, 2007.
14. Faber MJ, Dalinghaus M, Lankhuizen IM, Steendijk P, Hop WC, Schoemaker RG, Duncker DJ, Lamers JM, Helbing WA. Right and left ventricular function after chronic pulmonary artery banding in rats assessed with biventricular pressure-volume loops. Am J Physiol Heart Circ Physiol 291: H1580-H1586, 2006.
15. Faul JL, Nishimura T, Berry GJ, Benson GV, Pearl RG, Kao PN. Triptolide attenuates pulmonary arterial hypertension and neointimal formation in rats. Am J Respir Crit Care Med 162: 2252-2258, 2000.
16. Forfia PR, Fisher MR, Mathai SC, Housten-Harris T, Hemnes AR, Borlaug BA, Chamera E, Corretti MC, Champion HC, Abraham TP, Girgis RE, Hassoun PM. Tricuspid annular displacement predicts survival in pulmonary hypertension. Am J Respir Crit Care Med 174: 1034-1041, 2006.
17. Giordano FJ. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest 115: 500-508, 2005.
18. Gomez-Arroyo JG, Farkas L, Alhussaini AA, Farkas D, Kraskauskas D, Voelkel NF, Bogaard HJ. The monocrotaline model of pulmonary hypertension in perspective. Am J Physiol Lung Cell Mol Physiol 302: L363-L369, 2012.
19. Gupte SA, Levine RJ, Gupte RS, Young ME, Lionetti V, Labinskyy V, Floyd BC, Ojaimi C, Bellomo M, Wolin MS, Recchia FA. Glucose-6-phosphate dehydrogenase-derived NADPH fuels superoxide production in the failing heart. J Mol Cell Cardiol 41: 340-349, 2006.
20. Gupte SA, Li KX, Okada T, Sato K, Oka M. Inhibitors of pentose phosphate pathway cause vasodilation: involvement of voltage-gated potassium channels. J Pharmacol Exp Ther 301: 299-305, 2002.
21. Hampl V, Bibova J, Povysilova V, Herget J. Dehydroepiandrosterone sulphate reduces chronic hypoxic pulmonary hypertension in rats. Eur Respir J 21: 862-865, 2003.
22. Handoko ML, de Man FS, Allaart CP, Paulus WJ, Westerhof N, Vonk-Noordegraaf A. Perspectives on novel therapeutic strategies for right heart failure in pulmonary arterial hypertension: lessons from the left heart. Eur Respir Rev 19: 72-82, 2010.
23. Homma N, Nagaoka T, Karoor V, Imamura M, Taraseviciene-Stewart L, Walker LA, Fagan KA, McMurtry IF, Oka M. Involvement of RhoA/Rho kinase signaling in protection against monocrotaline-induced pulmonary hypertension in pneumonectomized rats by dehydroepiandrosterone. Am J Physiol Lung Cell Mol Physiol 295: L71-L78, 2008.
24. Iwasaki Y, Asai M, Yoshida M, Nigawara T, Kambayashi M, Nakashima N. Dehydroepiandrosterone-sulfate inhibits nuclear factor-kappaBdependent transcription in hepatocytes, possibly through antioxidant effect. J Clin Endocrinol Metab 89: 3449-3454, 2004.
25. Jankov RP, Lewis P, Kantores C, Ivanovska J, Xu EZ, Van Vliet T, Lee AH, Tanswell AK, McNamara PJ. Peroxynitrite mediates rightventricular dysfunction in nitric oxide-exposed juvenile rats. Free Radic Biol Med 49: 1453-1467, 2010.
26. Kuroda J, Ago T, Matsushima S, Zhai P, Schneider MD, Sadoshima J. NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc Natl Acad Sci USA 107: 15565-15570, 2010.
27. Labrie F, Luu-The V, Labrie C, Simard J. DHEA and its transformation into androgens and estrogens in peripheral target tissues: intracrinology. Front Neuroendocrinol 22: 185-212, 2001.
28. Li JM, Gall NP, Grieve DJ, Chen M, Shah AM. Activation of NADPH oxidase during progression of cardiac hypertrophy to failure. Hypertension 40: 477-484, 2002.
29. Li Q, Xu Y, Li X, Guo Y, Liu G. Inhibition of Rho-kinase ameliorates myocardial remodeling and fibrosis in pressure overload and myocardial infarction: role of TGF-beta1-TAK1. Toxicol Lett 211: 91-97, 2012.
30. Liu D, Dillon JS. Dehydroepiandrosterone stimulates nitric oxide release in vascular endothelial cells: evidence for a cell surface receptor. Steroids 69: 279-289, 2004.
31. Liu D, Si H, Reynolds KA, Zhen W, Jia Z, Dillon JS. Dehydroepiandrosterone protects vascular endothelial cells against apoptosis through a Galphai protein-dependent activation of phosphatidylinositol 3-kinase/ Akt and regulation of antiapoptotic Bcl-2 expression. Endocrinology 148: 3068-3076, 2007.
32. Macchia A, Marchioli R, Marfisi R, Scarano M, Levantesi G, Tavazzi L, Tognoni G. A meta-analysis of trials of pulmonary hypertension: a clinical condition looking for drugs and research methodology. Am Heart J 153: 1037-1047, 2007.
33. Macchia A, Marchioli R, Tognoni G, Scarano M, Marfisi R, Tavazzi L, Rich S. Systematic review of trials using vasodilators in pulmonary arterial hypertension: why a new approach is needed. Am Heart J 159: 245-257, 2007.
34. McLaughlin VV, Presberg KW, Doyle RL, Abman SH, McCrory DC, Fortin T, Ahearn G. Prognosis of pulmonary arterial hypertension: ACCP evidence-based clinical practice guidelines. Chest 126: 78S-92S, 2004.
35. McMurtry IF, Abe K, Ota H, Fagan KA, Oka M. Rho kinase-mediated vasoconstriction in pulmonary hypertension. Adv Exp Med Biol 661: 299-308, 2010.
36. Mir SA, Chatterjee A, Mitra A, Pathak K, Mahata SK, Sarkar S. Inhibition of signal transducer and activator of transcription 3 (STAT3) attenuates interleukin-6 (IL-6)-induced collagen synthesis and resultant hypertrophy in rat heart. J Biol Chem 287: 2666-2677, 2012.
37. Oka M, Homma N, Taraseviciene-Stewart L, Morris KG, Kraskauskas D, Burns N, Voelkel NF, McMurtry IF. Rho kinase-mediated vasoconstriction is important in severe occlusive pulmonary arterial hypertension in rats. Circ Res 100: 923-929, 2007.
38. Oka M, Karoor V, Homma N, Nagaoka T, Sakao E, Golembeski SM, Limbird J, Imamura M, Gebb SA, Fagan KA, McMurtry IF. Dehydroepiandrosterone upregulates soluble guanylate cyclase and inhibits hypoxic pulmonary hypertension. Cardiovasc Res 74: 377-387, 2007.
39. Pacher P, Nagayama T, Mukhopadhyay P, Batkai S, Kass DA. Measurement of cardiac function using pressure-volume conductance catheter technique in mice and rats. Nat Protoc 3: 1422-1434, 2008.
40. Paulin R, Meloche J, Jacob MH, Bisserier M, Courboulin A, Bonnet S. Dehydroepiandrosterone inhibits the Src/STAT3 constitutive activation in pulmonary arterial hypertension. Am J Physiol Heart Circ Physiol 301: H1798-H1809, 2011.
41. Redout EM, van der Toorn A, Zuidwijk MJ, van de Kolk CW, van Echteld CJ, Musters RJ, van Hardeveld C, Paulus WJ, Simonides WS. Antioxidant treatment attenuates pulmonary arterial hypertensioninduced heart failure. Am J Physiol Heart Circ Physiol 298: H1038-H1047, 2010.
42. Rocic P, Kolz C, Reed R, Potter B, Chilian WM. Optimal reactive oxygen species concentration and p38 MAP kinase are required for coronary collateral growth. Am J Physiol Heart Circ Physiol 292: H2729-H2736, 2007.
43. Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K, Solomon SD, Louie EK, Schiller NB. Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and the Canadian Society of Echocardiography. J Am Soc Echocardiogr 23: 685-713; quiz 786-688, 2010.
44. Seshiah PN, Weber DS, Rocic P, Valppu L, Taniyama Y, Griendling KK. Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ Res 91: 406-413, 2002.
45. Simonneau G, Robbins IM, Beghetti M, Channick RN, Delcroix M, Denton CP, Elliott CG, Gaine SP, Gladwin MT, Jing ZC, Krowka MJ, Langleben D, Nakanishi N, Souza R. Updated clinical classification of pulmonary hypertension. J Am Coll Cardiol 54: S43-S54, 2009.
46. Takeshima H, Kobayashi N, Koguchi W, Ishikawa M, Sugiyama F, Ishimitsu T. Cardioprotective effect of a combination of Rho-kinase inhibitor and p38 MAPK inhibitor on cardiovascular remodeling and oxidative stress in Dahl rats. J Atheroscler Thromb 19: 326-336, 2012.
47. Taraseviciene-Stewart L, Kasahara Y, Alger L, Hirth P, McMahon G, Waltenberger J, Voelkel NF, Tuder RM. Inhibition of the VEGF receptor 2 combined with chronic hypoxia causes cell death-dependent pulmonary endothelial cell proliferation and severe pulmonary hypertension. FASEB J 15: 427-438, 2001.
48. Taraseviciene-Stewart L, Scerbavicius R, Choe KH, Cool C, Wood K, Tuder RM, Burns N, Kasper M, Voelkel NF. Simvastatin causes endothelial cell apoptosis and attenuates severe pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 291: L668-L676, 2006.
49. Tyler RC, Muramatsu M, Abman SH, Stelzner TJ, Rodman DM, Bloch KD, McMurtry IF. Variable expression of endothelial NO synthase in three forms of rat pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 276: L297-L303, 1999.
50. Urboniene D, Haber I, Fang YH, Thenappan T, Archer SL. Validation of high-resolution echocardiography and magnetic resonance imaging vs. high-fidelity catheterization in experimental pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 299: L401-L412, 2010.
51. Van Dyke K, Patel S, Vallyathan V. Lucigenin chemiluminescence assay as an adjunctive tool for assessment of various stages of inflammation: a study of quiescent inflammatory cells. J Biosci 28: 115-119, 2003.
52. Wang K, Long B, Zhou J, Li PF. miR-9 and NFATc3 regulate myocardin in cardiac hypertrophy. J Biol Chem 285: 11903-11912, 2010.
53. Webb SJ, Geoghegan TE, Prough RA, Michael Miller KK. The biological actions of dehydroepiandrosterone involves multiple receptors. Drug Metab Rev 38: 89-116, 2006.
54. Zhang J, Bian HJ, Li XX, Liu XB, Sun JP, Li N, Zhang Y, Ji XP. ERK-MAPK signaling opposes rho-kinase to reduce cardiomyocyte apoptosis in heart ischemic preconditioning. Mol Med 16: 307-315, 2010.