(Circulation. 2001;103:155.)
© 2001 American Heart Association, Inc.
Basic Science Reports |
Reduction in Myocardial Collagen Cross-Linking Parallels Left Ventricular Dilatation in Rat Models of Systolic Chamber Dysfunction
From the Laboratory of Cardiovascular Pathophysiology, Department of Physiology, University of the Witwatersrand, Johannesburg (A.J.W., O.J.T., S.S., G.R.N.), and the Departments of Anatomical Pathology and Physiology, Medical University of South Africa, Pretoria (O.J.T., E.J.L.), South Africa; and the Department of Medicine, University of Massachusetts, Worcester (T.M., E.S.C., T.E.M.).
Background—The transition from compensated left ventricular hypertrophy (LVH) to heart failure is associated with alterations in the myocardial interstitium. We hypothesized that LV dilatation is associated with modifications in collagen cross-linking.
Methods and Results—We studied 2 rat models of LV dilatation: (1) pressure-overload hypertrophy with heart failure (POH-F) induced by suprarenal abdominal aortic banding and (2) LVH induced by 7 months of isoproterenol (ISO, 0.04 mg · kg-1 · d-1) administration. In POH-F rats and in rats receiving ISO, LV dilatation and a reduced systolic chamber performance were noted. Myocardial hydroxyproline concentrations ([HPRO]) were increased in the POH-F rats, whereas in rats receiving ISO, [HPRO] was decreased. In POH-F rats, the ratio of myocardial collagen type I to type III was increased, but in rats receiving ISO, myocardial collagen I/III was unchanged. In contrast to the diverse changes in myocardial collagen concentrations and phenotypes observed in the 2 models of LV dilatation, the ratio of myocardial insoluble to soluble (relationship between cross-linked and non–cross-linked) collagen was decreased in both the POH-F and ISO groups. Moreover, administration of captopril (0.22 mmol · kg-1 · d-1), which inhibited the ISO-induced reduction in myocardial insoluble/soluble collagen but not the reduction in [HPRO], prevented the ISO-induced alterations in LV dimensions and performance.
Conclusions—Because decreases in the ratio of myocardial insoluble to soluble collagen parallel LV dilatation in rats, reductions in myocardial collagen cross-linking may be an important mechanism contributing to LV dilatation in heart disease.
Key Words: collagen • systole • diastole • mechanics • remodeling
This article has been cited by other articles:
 |
|
 |
|
  O. H.I. Majane, L. Vengethasamy, E. F. du Toit, S. Makaula, A. J. Woodiwiss, and G. R. Norton Dietary-Induced Obesity Hastens the Progression From Concentric Cardiac Hypertrophy to Pump Dysfunction in Spontaneously Hypertensive Rats Hypertension, December 1, 2009; 54(6): 1376 - 1383. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Zibadi, R. Vazquez, D. Moore, D. F. Larson, and R. R. Watson Myocardial lysyl oxidase regulation of cardiac remodeling in a murine model of diet-induced metabolic syndrome Am J Physiol Heart Circ Physiol, September 1, 2009; 297(3): H976 - H982. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Lopez, R. Querejeta, A. Gonzalez, J. Beaumont, M. Larman, and J. Diez Impact of Treatment on Myocardial Lysyl Oxidase Expression and Collagen Cross-Linking in Patients With Heart Failure Hypertension, February 1, 2009; 53(2): 236 - 242. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Vanhoutte and S. Heymans Factor XIII: the cement of the heart after myocardial infarction? Eur. Heart J., February 2, 2008; 29(4): 427 - 428. [Full Text] [PDF]
|
|
|
|
|
|
G. R. Norton, D. G. A. Veliotes, O. Osadchii, A. J. Woodiwiss, and D. P. Thomas Susceptibility to systolic dysfunction in the myocardium from chronically infarcted spontaneously hypertensive rats Am J Physiol Heart Circ Physiol, January 1, 2008; 294(1): H372 - H378. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. G. Haworth The cell and molecular biology of right ventricular dysfunction in pulmonary hypertension Eur. Heart J. Suppl., December 1, 2007; 9(suppl_H): H10 - H16. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. S. Tutor, P. Penela, and F. Mayor Jr. Anti-{beta}1-adrenergic receptor autoantibodies are potent stimulators of the ERK1/2 pathway in cardiac cells Cardiovasc Res, October 1, 2007; 76(1): 51 - 60. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. N. Tziakas, G. K. Chalikias, N. Papanas, D. A. Stakos, S. V. Chatzikyriakou, and E. Maltezos Circulating levels of collagen type I degradation marker depend on the type of atrial fibrillation Europace, August 1, 2007; 9(8): 589 - 596. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
O. E. Osadchii, G. R. Norton, R. McKechnie, D. Deftereos, and A. J. Woodiwiss Cardiac dilatation and pump dysfunction without intrinsic myocardial systolic failure following chronic beta-adrenoreceptor activation Am J Physiol Heart Circ Physiol, April 1, 2007; 292(4): H1898 - H1905. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Vanhoutte, M. W.M. Schellings, M. Gotte, M. Swinnen, V. Herias, M. K. Wild, D. Vestweber, E. Chorianopoulos, V. Cortes, A. Rigotti, et al. Increased Expression of Syndecan-1 Protects Against Cardiac Dilatation and Dysfunction After Myocardial Infarction Circulation, January 30, 2007; 115(4): 475 - 482. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Cuenca, P. Martin-Sanz, A. M. Alvarez-Barrientos, L. Bosca, and N. Goren Infiltration of Inflammatory Cells Plays an Important Role in Matrix Metalloproteinase Expression and Activation in the Heart during Sepsis Am. J. Pathol., November 1, 2006; 169(5): 1567 - 1576. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. L. Brower, J. D. Gardner, M. F. Forman, D. B. Murray, T. Voloshenyuk, S. P. Levick, and J. S. Janicki The relationship between myocardial extracellular matrix remodeling and ventricular function. Eur. J. Cardiothorac. Surg., October 1, 2006; 30(4): 604 - 610. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Rutschow, J. Li, H.-P. Schultheiss, and M. Pauschinger Myocardial proteases and matrix remodeling in inflammatory heart disease Cardiovasc Res, February 15, 2006; 69(3): 646 - 656. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. M. Alwardt, Q. Yu, H. L. Brooks, M. R. McReynolds, R. Vazquez, R. R. Watson, and D. F. Larson Comparative effects of dehydroepiandrosterone sulfate on ventricular diastolic function with young and aged female mice Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2006; 290(1): R251 - R256. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X. Liu, T. Li, S. Sun, F. Xu, and Y. Wang Role of myofibrillogenesis regulator-1 in myocardial hypertrophy Am J Physiol Heart Circ Physiol, January 1, 2006; 290(1): H279 - H285. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Q. Yu, R. R. Watson, J. J. Marchalonis, and D. F. Larson A role for T lymphocytes in mediating cardiac diastolic function Am J Physiol Heart Circ Physiol, August 1, 2005; 289(2): H643 - H651. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. J Lijnen, V. V Petrov, M. Turner, and R. H Fagard Collagen Production in Cardiac Fibroblasts During Inhibition of Aminopeptidase B Journal of Renin-Angiotensin-Aldosterone System, June 1, 2005; 6(2): 69 - 77. [Abstract] [PDF]
|
|
|
|
|
|
D. G.A. Veliotes, A. J. Woodiwiss, D. A.J. Deftereos, D. Gray, O. Osadchii, and G. R. Norton Aldosterone Receptor Blockade Prevents the Transition to Cardiac Pump Dysfunction Induced by {beta}-Adrenoreceptor Activation Hypertension, May 1, 2005; 45(5): 914 - 920. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Boerma, J. Wang, J. Wondergem, J. Joseph, X. Qiu, R. H. Kennedy, and M. Hauer-Jensen Influence of Mast Cells on Structural and Functional Manifestations of Radiation-Induced Heart Disease Cancer Res., April 15, 2005; 65(8): 3100 - 3107. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Chen, J. L. Mehta, D. Li, L. Joseph, and J. Joseph Transforming Growth Factor {beta} Receptor Endoglin Is Expressed in Cardiac Fibroblasts and Modulates Profibrogenic Actions of Angiotensin II Circ. Res., December 10, 2004; 95(12): 1167 - 1173. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Gibbs, D. G. A. Veliotes, C. Anamourlis, D. Badenhorst, O. Osadchii, G. R. Norton, and A. J. Woodiwiss Chronic {beta}-adrenoreceptor activation increases cardiac cavity size through chamber remodeling and not via modifications in myocardial material properties Am J Physiol Heart Circ Physiol, December 1, 2004; 287(6): H2762 - H2767. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Sliwa, G. R. Norton, N. Kone, G. Candy, J. Kachope, A. J. Woodiwiss, C. Libhaber, P. Sareli, and R. Essop Impact of initiating carvedilol before angiotensin-converting enzyme inhibitor therapy on cardiac function in newly diagnosed heart failure J. Am. Coll. Cardiol., November 2, 2004; 44(9): 1825 - 1830. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. H. Opie Cellular Basis for Therapeutic Choices in Heart Failure Circulation, October 26, 2004; 110(17): 2559 - 2561. [Full Text] [PDF]
|
|
|
|
|
|
O. H. Cingolani, X.-P. Yang, Y.-H. Liu, M. Villanueva, N.-E. Rhaleb, and O. A. Carretero Reduction of Cardiac Fibrosis Decreases Systolic Performance Without Affecting Diastolic Function in Hypertensive Rats Hypertension, May 1, 2004; 43(5): 1067 - 1073. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. Murtuza, K. Suzuki, G. Bou-Gharios, J. R. Beauchamp, R. T. Smolenski, T. A. Partridge, and M. H. Yacoub Transplantation of skeletal myoblasts secreting an IL-1 inhibitor modulates adverse remodeling in infarcted murine myocardium PNAS, March 23, 2004; 101(12): 4216 - 4221. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. M. Emani, A. S. Shah, M. K. Bowman, D. C. White, S. Emani, D. D. Glower, and W. J. Koch Right ventricular targeted gene transfer of a {beta}-adrenergic receptor kinase inhibitor improves ventricular performance after pulmonary artery banding J. Thorac. Cardiovasc. Surg., March 1, 2004; 127(3): 787 - 793. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Cittadini, J.o. Isgaard, M. G. Monti, C. Casaburi, A. Di Gianni, R. Serpico, G. Iaccarino, and L. Sacca Growth hormone prolongs survival in experimental postinfarction heart failure J. Am. Coll. Cardiol., June 18, 2003; 41(12): 2154 - 2163. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. L. Ennis, E. M. Escudero, G. M. Console, G. Camihort, C. G. Dumm, R. W. Seidler, M. C. Camilion de Hurtado, and H. E. Cingolani Regression of Isoproterenol-Induced Cardiac Hypertrophy by Na+/H+ Exchanger Inhibition Hypertension, June 1, 2003; 41(6): 1324 - 1329. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Badenhorst, M. Maseko, O. J Tsotetsi, A. Naidoo, R. Brooksbank, G. R Norton, and A. J Woodiwiss Cross-linking influences the impact of quantitative changes in myocardial collagen on cardiac stiffness and remodelling in hypertension in rats Cardiovasc Res, March 1, 2003; 57(3): 632 - 641. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Badenhorst, D. Veliotes, M. Maseko, O. J. Tsotetsi, R. Brooksbank, A. Naidoo, A. J. Woodiwiss, and G. R. Norton {beta}-Adrenergic Activation Initiates Chamber Dilatation in Concentric Hypertrophy Hypertension, March 1, 2003; 41(3): 499 - 504. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. W. M. Fedak, S. M. Altamentova, R. D. Weisel, N. Nili, N. Ohno, S. Verma, T.-Y. J. Lee, C. Kiani, D. A. G. Mickle, B. H. Strauss, et al. Matrix remodeling in experimental and human heart failure: a possible regulatory role for TIMP-3 Am J Physiol Heart Circ Physiol, February 1, 2003; 284(2): H626 - H634. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. F. Baicu, J. D. Stroud, V. A. Livesay, E. Hapke, J. Holder, F. G. Spinale, and M. R. Zile Changes in extracellular collagen matrix alter myocardial systolic performance Am J Physiol Heart Circ Physiol, January 1, 2003; 284(1): H122 - H132. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Li, P. Lothar Schwimmbeck, C. Tschope, S. Leschka, L. Husmann, S. Rutschow, F. Reichenbach, M. Noutsias, U. Kobalz, W. Poller, et al. Collagen degradation in a murine myocarditis model: relevance of matrix metalloproteinase in association with inflammatory induction Cardiovasc Res, November 1, 2002; 56(2): 235 - 247. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. E. Cingolani and M. C. Camilion de Hurtado Na+-H+ Exchanger Inhibition: A New Antihypertrophic Tool Circ. Res., April 19, 2002; 90(7): 751 - 753. [Full Text] [PDF]
|
|
|
|
|
|
F. G. Spinale Matrix Metalloproteinases: Regulation and Dysregulation in the Failing Heart Circ. Res., March 22, 2002; 90(5): 520 - 530. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Y. Li, T. Kadokami, P. Wang, C. F. McTiernan, and A. M. Feldman MMP inhibition modulates TNF-alpha transgenic mouse phenotype early in the development of heart failure Am J Physiol Heart Circ Physiol, March 1, 2002; 282(3): H983 - H989. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
O. J. Tsotetsi, A. J. Woodiwiss, M. Netjhardt, D. Qubu, R. Brooksbank, and G. R. Norton Attenuation of Cardiac Failure, Dilatation, Damage, and Detrimental Interstitial Remodeling Without Regression of Hypertrophy in Hypertensive Rats Hypertension, October 1, 2001; 38(4): 846 - 851. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. L. Mann and H. Taegtmeyer Dynamic Regulation of the Extracellular Matrix After Mechanical Unloading of the Failing Human Heart: Recovering the Missing Link in Left Ventricular Remodeling Circulation, September 4, 2001; 104(10): 1089 - 1091. [Full Text] [PDF]
|
|
|
|
|
|
Y. Y. Li, Y. Feng, C. F. McTiernan, W. Pei, C. S. Moravec, P. Wang, W. Rosenblum, R. L. Kormos, and A. M. Feldman Downregulation of Matrix Metalloproteinases and Reduction in Collagen Damage in the Failing Human Heart After Support With Left Ventricular Assist Devices Circulation, September 4, 2001; 104(10): 1147 - 1152. [Abstract] [Full Text] [PDF]
|
|