The cell and molecular biology of right ventricular dysfunction in pulmonary hypertension

European Heart Journal, Supplement

Volumn 9, Issue H, 2007, Pages

  Haworth, Sheila G ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b Great Ormond Street Hospital for Children NHS Trust ^*  (United Kingdom)

Author keywords

Pulmonary hypertension; Right ventricle; Ventricular remodelling

Indexed keywords

EID: 77949380983     PISSN: 1520765X     EISSN: None     Source Type: Journal    
DOI: 10.1093/eurheartj/sum025     Document Type: Review

References (73)

1. Conway MA, Allis J, Ouwerkerk R, Niioka T, Rajagopalan B, Radda GK. Detection of low phosphocreatine to ATP ratio in failing hypertrophied human myocardium by 31P magnetic resonance spectroscopy. Lancet 1991;338:973-976.
2. Conway MA, Bottomley PA, Ouwerkerk R, Radda GK, Rajagopalan B. Mitral regurgitation: impaired systolic function, eccentric hypertrophy, and increased severity are linked to lower phosphocreatine/ ATP ratios in humans. Circulation 1998;97:1716-1723.
3. Murray AJ, Anderson RE, Watson GC, Radda GK, Clarke K. Uncoupling proteins in human heart. Lancet 2004;364:1786-1788.
4. Miall-Allen VM, Kemp GJ, Rajagopalan B, Taylor DJ, Radda GK, Haworth SG. Magnetic resonance spectroscopy in congenital heart disease. Heart 1996;75:614-619.
5. Spindler M, Schmidt M, Geier O, Sandstede J, Hahn D, Ertl G, Beer M. Functional and metabolic recovery of the right ventricle during Bosentan therapy in idiopathic pulmonary arterial hypertension. J Cardiovasc Magn Reson 2005;7:853-854.
6. Omerovic E, Bollano E, Mobini R, Kujacic V, Madhu B, Soussi B, Fu M, Hjalmarson A, Waagstein F, Isgaard J. Growth hormone improves bioenergetics and decreases catecholamines in postinfarct rat hearts. Endocrinology 2000;141:4592-4599.
7. Omerovic E, Bollano E, Mobini R, Madhu B, Kujacic V, Soussi B, Hjalmarson A, Waagstein F. Selective beta(1)-blockade improves cardiac bioenergetics and function and decreases neuroendocrine activation in rats during early postinfarct remodeling. Biochem Biophys Res Commun 2001;281:491- 498.
8. Opie LH. Cellular basis for therapeutic choices in heart failure. Circulation 2004;110:2559-2561.
9. Beanlands RS, Nahmias C, Gordon E, Coates G, deKemp R, Firnau G, Fallen E. The effects of beta(1)-blockade on oxidative metabolism and the metabolic cost of ventricular work in patients with left ventricular dysfunction: a double-blind, placebo-controlled, positronemission tomography study. Circulation 2000;102:2070-2075.
10. Loffler R, Sauter R, Kolem H, Haase A, von Kienlin M. Localized spectroscopy from anatomically matched compartments: improved sensitivity and localization for cardiac 31P MRS in humans. J Magn Reson 1998;134:287-299.
11. Adatia I, Kemp GJ, Taylor DJ, Radda GK, Rajagopalan B, Haworth SG. Abnormalities in skeletal muscle metabolism in cyanotic patients with congenital heart disease: a 31P nuclear magnetic resonance spectroscopy study. Clin Sci (Lond) 1993;85:105-109.
12. Adamopoulos S, Kemp GJ, Thompson CH, Arnolda L, Brunotte F, Stratton JR, Radda GK, Rajagopalan B, Kremastinos DT, Coats AJ. The time course of haemodynamic, autonomic and skeletal muscle metabolic abnormalities following first extensive myocardial infarction in man. J Mol Cell Cardiol 1999;31:1913-1926.
13. Anversa P, Ricci R, Olivetti G. Quantitative structural analysis of the myocardium during physiologic growth and induced cardiac hypertrophy: a review. J Am Coll Cardiol 1986;7:1140-1149.
14. Swynghedauw B. Developmental and functional adaptation of contractile proteins in cardiac and skeletal muscles. Physiol Rev 1986;66:710-771.
15. Lompre AM, Schwartz K, d'Albis A, Lacombe G, Van Thiem N, Swynghedauw B. Myosin isoenzyme redistribution in chronic heart overload. Nature 1979;282:105-107.
16. Palmiter KA, Tyska MJ, Dupuis DE, Alpert NR, Warshaw DM. Kinetic differences at the single molecule level account for the functional diversity of rabbit cardiac myosin isoforms. J Physiol 1999;519: 669-678.
17. Sugiura S, Kobayakawa N, Fujita H, Yamashita H,Momomura S, Chaen S, Omata M, Sugi H. Comparison of unitary displacements and forces between 2 cardiac myosin isoforms by the optical trap technique: molecular basis for cardiac adaptation. Circ Res 1998;82:1029-1034.
18. Nakao K, Minobe W, Roden R, Bristow MR, Leinwand LA. Myosin heavy chain gene expression in human heart failure. J Clin Invest 1997;100:2362-2370.
19. Miyata S, Minobe W, Bristow MR, Leinwand LA. Myosin heavy chain isoform expression in the failing and nonfailing human heart. Circ Res 2000;86:386-390.
20. Marian AJ. On mice, rabbits, human heart failure. Circulation 2005;111:2276-2279.
21. Krenz M, Robbins J. Impact of beta-myosin heavy chain expression on cardiac function during stress. J Am Coll Cardiol 2004;44:2390- 2397.
22. Torbicki A, Kurzyna M, Kuca P, Fijalkowska A, Sikora J, Florczyk M, Pruszczyk P, Burakowski J, Wawrzynska L. Detectable serum cardiac troponin T as a marker of poor prognosis among patients with chronic precapillary pulmonary hypertension. Circulation 2003;108:844-848.
23. Nootens M, Kaufmann E, Rector T, Toher C, Judd D, Francis GS, Rich S. Neurohormonal activation in patients with right ventricular failure from pulmonary hypertension: relation to hemodynamic variables and endothelin levels. J Am Coll Cardiol 1995;26:1581-1585.
24. Rubens C, Ewert R, HalankM,Wensel R,Orzechowski HD, Schultheiss HP, Hoeffken G. Big endothelin-1 and endothelin-1 plasma levels are correlated with the severity of primary pulmonary hypertension. Chest 2001;120:1562-1569.
25. Zisman LS, Keller RS, Weaver B, Lin Q, Speth R, Bristow MR, Canver CC. Increased angiotensin-(1-7)-forming activity in failing human heart ventricles: evidence for upregulation of the angiotensin-converting enzyme Homologue ACE2. Circulation 2003;108:1707-1712.
26. Fu YC, Yin SC, Chi CS, Hwang B, Hsu SL. Norepinephrine induces apoptosis in neonatal rat endothelial cells via a ROS-dependent JNK activation pathway. Apoptosis 2006;11:2053-2063.
27. Gonzalez A, Lopez B, Ravassa S, Querejeta R, Larman M, Diez J, Fortuno MA. Stimulation of cardiac apoptosis in essential hypertension: potential role of angiotensin II. Hypertension 2002;39:75-80.
28. Chen X, Zhang X, Kubo H, Harris DM, Mills GD, Moyer J, Berretta R, Potts ST, Marsh JD, Houser SR. Ca2+ influx-induced sarcoplasmic reticulum Ca2+ overload causes mitochondrial-dependent apoptosis in ventricular myocytes. Circ Res 2005;97:1009-1017.
29. Schroder D, Heger J, Piper HM, Euler G. Angiotensin II stimulates apoptosis via TGF-beta1 signaling in ventricular cardiomyocytes of rat. J Mol Med 2006;84:975-983.
30. Schneiders D, Heger J, Best P, Michael PH, Taimor G. SMAD proteins are involved in apoptosis induction in ventricular cardiomyocytes. Cardiovasc Res 2005;67:87-96.
31. Regula KM, Ens K, Kirshenbaum LA. Mitochondria-assisted cell suicide: a license to kill. J Mol Cell Cardiol 2003;35:559-567.
32. Hou YP, Wu JL, Fan Q, Liu MB, Yin BL, Zhang L. Plasma concentration of Fas/Fas ligand and left ventricular function in response to metoprolol in conjunction with standard treatment. Clin Sci (Lond) 2007;112:211- 218.
33. Folino AF, Bobbo F, Schiraldi C, Tona F, Romano S, Buja G, Bellotto F. Ventricular arrhythmias and autonomic profile in patients with primary pulmonary hypertension. Lung 2003;181:321-328.
34. Rosas-Peralta M, Sandoval-Zarate J, Attie F, Pulido T, Santos E, Granados NZ, Miranda T, Escobar V. Clinical implications and prognostic significance of the study on the circadian variation of heart rate variability in patients with severe pulmonary hypertension. Gac Med Mex 2006;142:19-28.
35. Sakamaki F, Satoh T, Nagaya N, Kyotani S, Oya H, Nakanishi N, Kuribayashi S, Ishida Y. Correlation between severity of pulmonary arterial hypertension and 123I-metaiodobenzylguanidine left ventricular imaging. J Nucl Med 2000;41:1127-1133.
36. Ishikawa S, Honda M, Yamada S, Morioka S, Moriyama K. Biventricular down-regulation of beta-adrenergic receptors in right ventricular hypertrophy induced by monocrotaline. Jpn Circ J 1991;55: 1077-1085.
37. Leineweber K, Brandt K, Wludyka B, Beilfuss A, Ponicke K, Heinroth-Hoffmann I, Brodde OE. Ventricular hypertrophy plus neurohumoral activation is necessary to alter the cardiac beta-adrenoceptor system in experimental heart failure. Circ Res 2002;91:1056-1062.
38. Marks AR. A guide for the perplexed: towards an understanding of the molecular basis of heart failure. Circulation 2003;107:1456-1459.
39. Kubo H, Margulies KB, Piacentino V III, Gaughan JP, Houser SR. Patients with end-stage congestive heart failure treated with beta-adrenergic receptor antagonists have improved ventricular myocyte calcium regulatory protein abundance. Circulation 2001;104:1012-1018.
40. Pfeffer JM, Pfeffer MA, Braunwald E. Influence of chronic captopril therapy on the infarcted left ventricle of the rat. Circ Res 1985;57:84-95.
41. Zisman LS, Asano K, Dutcher DL, Ferdensi A, Robertson AD, Jenkin M, Bush EW, Bohlmeyer T, Perryman MB, Bristow MR. Differential regulation of cardiac angiotensin converting enzyme binding sites and AT1 receptor density in the failing human heart. Circulation 1998;98:1735-1741.
42. Hein S, Arnon E, Kostin S, Schonburg M, Elsasser A, Polyakova V, Bauer EP, Klovekorn WP, Schaper J. Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: structural deterioration and compensatory mechanisms. Circulation 2003;107:984-991.
43. Sakata Y, Yamamoto K, Mano T, Nishikawa N, Yoshida J, Hori M, Miwa T, Masuyama T. Activation of matrix metalloproteinases precedes left ventricular remodeling in hypertensive heart failure rats: its inhibition as a primary effect of angiotensin-converting enzyme inhibitor. Circulation 2004;109:2143-2149.
44. Busjahn A, Knoblauch H, Knoblauch M, Bohlender J, Menz M, Faulhaber HD, Becker A, Schuster H, Luft FC. Angiotensin-converting enzyme and angiotensinogen gene polymorphisms, plasma levels, cardiac dimensions. A twin study. Hypertension 1997;29:165-170.
45. Abraham WT, Raynolds MV, Gottschall B, Badesch DB, Wynne KM, Groves BM, Lowes BD, Bristow MR, Perryman MB, Voelkel NF. Importance of angiotensin-converting enzyme in pulmonary hypertension. Cardiology 1995;86(Suppl. 1):9-15.
46. Abraham WT, Raynolds MV, Badesch DB, Wynne KM, Groves BM, Roden RL, Robertson AD, Lowes BD, Zisman LS, Voelkel NF, Bristow MR, Perryman MB. Angiotensin-converting enzyme DD genotype in patients with primary pulmonary hypertension: increased frequency and association with preserved haemodynamics. J Renin Angiotensin Aldosterone Syst 2003;4:27-30.
47. Hoeper MM, Tacacs A, Stellmacher U, Lichtinghagen R. Lack of association between angiotensin converting enzyme (ACE) genotype, serum ACE activity, and haemodynamics in patients with primary pulmonary hypertension. Heart 2003;89:445-446.
48. Nagaya N, Nishikimi T, Okano Y, Uematsu M, Satoh T, Kyotani S, Kuribayashi S, Hamada S, Kakishita M, Nakanishi N, Takamiya M, Kunieda T, Matsuo H, Kangawa K. Plasma brain natriuretic peptide levels increase in proportion to the extent of right ventricular dysfunction in pulmonary hypertension. J Am Coll Cardiol 1998;31: 202-208.
49. King L, Wilkins MR. Natriuretic peptide receptors and the heart. Heart 2002;87:314-315.
50. Bruneau BG, Piazza LA, de Bold AJ. BNP gene expression is specifically modulated by stretch and ET-1 in a new model of isolated rat atria. Am J Physiol 1997;273:H2678-H2686.
51. Lourenco AP, Roncon-Albuquerque R Jr, Bras-Silva C, Faria B, Wieland J, Henriques-Coelho T, Correia-Pinto J, Leite-Moreira AF. Myocardial dysfunction and neurohumoral activation without remodeling in left ventricle of monocrotaline-induced pulmonary hypertensive rats. Am J Physiol Heart Circ Physiol 2006;291:H1587-H1594.
52. de Lemos JA, McGuire DK, Drazner MH. B-type natriuretic peptide in cardiovascular disease. Lancet 2003;362:316-322.
53. Uusimaa PA, Hassinen IE, Vuolteenaho O, Ruskoaho H. Endothelininduced atrial natriuretic peptide release from cultured neonatal cardiac myocytes: the role of extracellular calcium and protein kinase-C. Endocrinology 1992;130:2455-2464.
54. Tamura N, Ogawa Y, Chusho H, Nakamura K, Nakao K, Suda M, Kasahara M, Hashimoto R, Katsuura G, Mukoyama M, Itoh H, Saito Y, Tanaka I, Otani H, Katsuki M. Cardiac fibrosis in mice lacking brain natriuretic peptide. Proc Natl Acad Sci USA 2000;97:4239-4244.
55. Cargill RI, Lipworth BJ. Acute effects of ANP and BNP on hypoxic pulmonary vasoconstriction in humans. Br J Clin Pharmacol 1995;40:585-590.
56. Jasmin JF, Cernacek P, Dupuis J. Activation of the right ventricular endothelin (ET) system in the monocrotaline model of pulmonary hypertension: response to chronic ETA receptor blockade. Clin Sci (Lond) 2003;105:647-653.
57. Brunner F, Wolkart G, Haleen S. Defective intracellular calcium handling in monocrotaline-induced right ventricular hypertrophy: protective effect of long-term endothelin-A receptor blockade with 2-benzo[1,3]dioxol-5-yl-3-benzyl- 4-(4-methoxy-phenyl-)- 4-oxobut-2-enoate-sodium (PD 155080). J Pharmacol Exp Ther 2002;300: 442-449.
58. Stessel H, Brunner F. Effect of endothelin antagonism on contractility, intracellular calcium regulation and calcium regulatory protein expression in right ventricular hypertrophy of the rat. Basic Clin Pharmacol Toxicol 2004;94:37-45.
59. Proven A, Roderick HL, Conway SJ, Berridge MJ, Horton JK, Capper SJ, Bootman MD. Inositol 1,4,5-trisphosphate supports the arrhythmogenic action of endothelin-1 on ventricular cardiac myocytes. J Cell Sci 2006;119:3363-3375.
60. Li X, Zima AV, Sheikh F, Blatter LA, Chen J. Endothelin-1-induced arrhythmogenic Ca2+ signaling is abolished in atrial myocytes of inositol-1,4,5-trisphosphate(IP3)-receptor type 2-deficient mice. Circ Res 2005;96:1274-1281.
61. Kennedy RA, Kemp TJ, Sugden PH, Clerk A. Using U0126 to dissect the role of the extracellular signal-regulated kinase 1/2 (ERK1/2) cascade in the regulation of gene expression by endothelin-1 in cardiac myocytes. J Mol Cell Cardiol 2006;41:236-247.
62. Penna C, Rastaldo R, Mancardi D, Cappello S, Pagliaro P, Westerhof N, Losano G. Effect of endothelins on the cardiovascular system. J Cardiovasc Med (Hagerstown) 2006;7:645-652.
63. Morioka S, Honda M, Ishikawa S, Ishinaga Y, Yano S, Tanaka K, Moriyama K. Changes in contractile and non-contractile proteins, intracellular Ca2+ and ultrastructures during the development of right ventricular hypertrophy and failure in rats. Jpn Circ J 1992;56:469-474.
64. Honda M, Yamada S, Goto Y, Ishikawa S, Yoshikane H, Ishinaga Y, Kuzuo H, Morioka S, Moriyama K. Biochemical and structural remodeling of collagen in the right ventricular hypertrophy induced by monocrotaline. Jpn Circ J 1992;56:392-403.
65. Woodiwiss AJ, Tsotetsi OJ, Sprott S, Lancaster EJ, Mela T, Chung ES, Meyer TE, Norton GR. Reduction in myocardial collagen cross-linking parallels left ventricular dilatation in rat models of systolic chamber dysfunction. Circulation 2001;103:155-160.
66. Spinale FG, Coker ML, Bond BR, Zellner JL. Myocardial matrix degradation and metalloproteinase activation in the failing heart: a potential therapeutic target. Cardiovasc Res 2000;46:225-238.
67. Deschamps AM, Spinale FG. Pathways of matrix metalloproteinase induction in heart failure: bioactive molecules and transcriptional regulation. Cardiovasc Res 2006;69:666-676.
68. Ciulla MM, Paliotti R, Esposito A, Diez J, Lopez B, Dahlof B, Nicholls MG, Smith RD, Gilles L, Magrini F, Zanchetti A. Different effects of antihypertensive therapies based on losartan or atenolol on ultrasound and biochemical markers of myocardial fibrosis: results of a randomized trial. Circulation 2004;110:552-557.
69. Manso AM, Elsherif L, Kang SM, Ross RS. Integrins, membrane-type matrix metalloproteinases and ADAMs: potential implications for cardiac remodeling. Cardiovasc Res 2006;69:574-584.
70. Deschamps AM, Spinale FG. Disruptions and detours in the myocardial matrix highway and heart failure. Curr Heart Fail Rep 2005;2:10-17.
71. Deschamps AM, Spinale FG. Matrix modulation and heart failure: new concepts question old beliefs. Curr Opin Cardiol 2005;20:211-216.
72. Rensing BJ, McDougall JC, Breen JF, Vigneswaran WT, McGregor CG, Rumberger JA. Right and left ventricular remodeling after orthotopic single lung transplantation for end-stage emphysema. J Heart Lung Transplant 1997;16:926-933.
73. Kasimir MT, Seebacher G, Jaksch P, Winkler G, Schmid K, Marta GM, Simon P, Klepetko W. Reverse cardiac remodelling in patients with primary pulmonary hypertension after isolated lung transplantation. Eur J Cardiothorac Surg 2004;26:776-781.