© 1998 American Heart Association, Inc.
Original Contributions |
Time-Dependent Changes in Matrix Metalloproteinase Activity and Expression During the Progression of Congestive Heart Failure
Relation to Ventricular and Myocyte Function
From the Division of Cardiothoracic Surgery, Medical University of South Carolina, Charleston, SC.
Correspondence to Francis G. Spinale, MD, PhD, Division of Cardiothoracic Surgery, Room 418 CSB, 171 Ashley Ave, Medical University of South Carolina, Charleston, SC 29425.
Abstract—The development of
congestive heart failure (CHF) is associated with left
ventricular (LV) dilation and myocardial remodeling.
However, fundamental mechanisms that contribute to this remodeling
process with the progression of CHF remain unclear. The matrix
metalloproteinases (MMPs) have been demonstrated to play a significant
role in tissue remodeling in a number of pathological processes. The
present project tested the hypothesis that the LV dilation and
remodeling during the progression of CHF is associated with early
changes in MMP expression and zymographic activity. LV and myocyte
function, collagen content, and MMP expression and zymographic activity
were serially measured during the progression of CHF caused by
pacing-induced supraventricular tachycardia
(SVT) in pigs. After 7 days of SVT, LV end-diastolic
dimension and myocyte length both increased by 15% from control
values, and LV fractional shortening fell by 20%. At the level of the
myocyte, percent shortening fell by 16% after 7 days of SVT, with no
change in the steady-state velocity of shortening. Longer durations of
SVT caused progressive LV dilation, LV pump failure, and myocyte
contractile dysfunction. Specifically, 21 days of SVT resulted in a
>50% increase in LV dimension, a 56% fall in LV fractional
shortening, and a 33% decline in myocyte velocity of shortening. The
decline in LV and myocyte function with 21 days of SVT was accompanied
by signs and symptoms of CHF. Thus, SVT causes time-dependent changes
in LV geometry and function and the subsequent development of CHF. LV
myocardial collagen content and confluence fell by >25% after 7 days
of SVT and were accompanied by an 80% increase in LV myocardial MMP
zymographic activity against the substrate gelatin. After 14 days of
SVT, total LV myocardial collagen content was reduced by 24%, and LV
myocardial MMP zymographic activity increased by >100% from control
values. Interstitial collagenase (MMP-1),
stromelysin (MMP-3), and 72-kD gelatinase (MMP-2) were increased by
2-fold after 7 days of SVT. LV MMP zymographic activity and
abundance remained elevated with longer durations of SVT. The results
of the present study demonstrated that in this model of CHF, early
changes in LV myocardial MMP zymographic activity and protein levels
occurred with the initiation and progression of LV dilation and
dysfunction. These findings suggest that an early contributory
mechanism for the initiation of LV remodeling that occurred in this
model of developing CHF is enhanced expression and potentially
increased activity of LV myocardial MMPs.
Key Words: heart failure • metalloproteinase • myocardial remodeling
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B. Schwartzkopff, M. Fassbach, B. Pelzer, M. Brehm, and B. E. Strauer Elevated serum markers of collagen degradation in patients with mild to moderate dilated cardiomyopathy Eur J Heart Fail, August 1, 2002; 4(4): 439 - 444. [Abstract] [Full Text] [PDF]
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G. L. Brower, A. L. Chancey, S. Thanigaraj, B. B. Matsubara, and J. S. Janicki Cause and effect relationship between myocardial mast cell number and matrix metalloproteinase activity Am J Physiol Heart Circ Physiol, August 1, 2002; 283(2): H518 - H525. [Abstract] [Full Text] [PDF]
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R. Nakamura, K. Egashira, Y. Machida, S. Hayashidani, M. Takeya, H. Utsumi, H. Tsutsui, and A. Takeshita Probucol Attenuates Left Ventricular Dysfunction and Remodeling in Tachycardia-Induced Heart Failure: Roles of Oxidative Stress and Inflammation Circulation, July 16, 2002; 106(3): 362 - 367. [Abstract] [Full Text] [PDF]
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F. A. Tibayan, D. T. M. Lai, T. A. Timek, P. Dagum, D. Liang, G. T. Daughters, N. B. Ingels, and D. C. Miller Alterations in left ventricular torsion in tachycardia-induced dilated cardiomyopathy J. Thorac. Cardiovasc. Surg., July 1, 2002; 124(1): 43 - 49. [Abstract] [Full Text] [PDF]
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A. L. Chancey, G. L. Brower, and J. S. Janicki Cardiac mast cell-mediated activation of gelatinase and alteration of ventricular diastolic function Am J Physiol Heart Circ Physiol, June 1, 2002; 282(6): H2152 - H2158. [Abstract] [Full Text] [PDF]
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A. M. Romanic, S. M. Harrison, W. Bao, C. L. Burns-Kurtis, S. Pickering, J. Gu, E. Grau, J. Mao, G. M. Sathe, E. H. Ohlstein, et al. Myocardial protection from ischemia/reperfusion injury by targeted deletion of matrix metalloproteinase-9 Cardiovasc Res, June 1, 2002; 54(3): 549 - 558. [Abstract] [Full Text] [PDF]
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W. S. Bradham, G. Moe, K. A. Wendt, A. A. Scott, A. Konig, M. Romanova, G. Naik, and F. G. Spinale TNF-alpha and myocardial matrix metalloproteinases in heart failure: relationship to LV remodeling Am J Physiol Heart Circ Physiol, April 1, 2002; 282(4): H1288 - H1295. [Abstract] [Full Text] [PDF]
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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]
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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]
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W. S. Bradham, B. Bozkurt, H. Gunasinghe, D. Mann, and F. G. Spinale Tumor necrosis factor-alpha and myocardial remodeling in progression of heart failure: a current perspective Cardiovasc Res, March 1, 2002; 53(4): 822 - 830. [Abstract] [Full Text] [PDF]
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T. Walther, A. Schubert, V. Falk, C. Binner, A. Kanev, S. Bleiziffer, C. Walther, N. Doll, R. Autschbach, and F. W. Mohr Regression of Left Ventricular Hypertrophy After Surgical Therapy for Aortic Stenosis Is Associated With Changes in Extracellular Matrix Gene Expression Circulation, September 18, 2001; 104 (2009): I-54 - I-58. [Abstract] [Full Text] [PDF]
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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]
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E. E.J.M. Creemers, J. P.M. Cleutjens, J. F.M. Smits, and M. J.A.P. Daemen Matrix Metalloproteinase Inhibition After Myocardial Infarction: A New Approach to Prevent Heart Failure? Circ. Res., August 3, 2001; 89(3): 201 - 210. [Abstract] [Full Text] [PDF]
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M. L. Coker, J. R. Jolly, C. Joffs, T. Etoh, J. R. Holder, B. R. Bond, and F. G. Spinale Matrix metalloproteinase expression and activity in isolated myocytes after neurohormonal stimulation Am J Physiol Heart Circ Physiol, August 1, 2001; 281(2): H543 - H551. [Abstract] [Full Text] [PDF]
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S. M. Dolgilevich, F. M. Siri, S. A. Atlas, and C. Eng Changes in collagenase and collagen gene expression after induction of aortocaval fistula in rats Am J Physiol Heart Circ Physiol, July 1, 2001; 281(1): H207 - H214. [Abstract] [Full Text] [PDF]
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J. T. Peterson, H. Hallak, L. Johnson, H. Li, P. M. O'Brien, D. R. Sliskovic, T. M. A. Bocan, M. L. Coker, T. Etoh, and F. G. Spinale Matrix Metalloproteinase Inhibition Attenuates Left Ventricular Remodeling and Dysfunction in a Rat Model of Progressive Heart Failure Circulation, May 8, 2001; 103(18): 2303 - 2309. [Abstract] [Full Text] [PDF]
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M.H. Yacoub A novel strategy to maximize the efficacy of left ventricular assist devices as a bridge to recovery Eur. Heart J., April 1, 2001; 22(7): 534 - 540. [PDF]
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G. L. Brower and J. S. Janicki Contribution of ventricular remodeling to pathogenesis of heart failure in rats Am J Physiol Heart Circ Physiol, February 1, 2001; 280(2): H674 - H683. [Abstract] [Full Text] [PDF]
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A. J. Woodiwiss, O. J. Tsotetsi, S. Sprott, E. J. Lancaster, T. Mela, E. S. Chung, T. E. Meyer, and G. R. Norton Reduction in Myocardial Collagen Cross-Linking Parallels Left Ventricular Dilatation in Rat Models of Systolic Chamber Dysfunction Circulation, January 2, 2001; 103(1): 155 - 160. [Abstract] [Full Text] [PDF]
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F. G. Spinale, M. L. Coker, L. J. Heung, B. R. Bond, H. R. Gunasinghe, T. Etoh, A. T. Goldberg, J. L. Zellner, and A. J. Crumbley A Matrix Metalloproteinase Induction/Activation System Exists in the Human Left Ventricular Myocardium and Is Upregulated in Heart Failure Circulation, October 17, 2000; 102(16): 1944 - 1949. [Abstract] [Full Text] [PDF]
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R. B. New, A. C. Sampson, M. K. King, J. W. Hendrick, M. J. Clair, J. H. McElmurray III, J. Mandel, R. Mukherjee, Marc de Gasparo, and F. G. Spinale Effects of Combined Angiotensin II and Endothelin Receptor Blockade With Developing Heart Failure : Effects on Left Ventricular Performance Circulation, September 19, 2000; 102(12): 1447 - 1453. [Abstract] [Full Text] [PDF]
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S. Kinugawa, H. Tsutsui, S. Hayashidani, T. Ide, N. Suematsu, S. Satoh, H. Utsumi, and A. Takeshita Treatment With Dimethylthiourea Prevents Left Ventricular Remodeling and Failure After Experimental Myocardial Infarction in Mice : Role of Oxidative Stress Circ. Res., September 1, 2000; 87(5): 392 - 398. [Abstract] [Full Text] [PDF]
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L. Lu, Z. Gunja-Smith, J. F. Woessner, P. C. Ursell, T. Nissen, R. E. Galardy, Y. Xu, P. Zhu, and G. G. Schwartz Matrix metalloproteinases and collagen ultrastructure in moderate myocardial ischemia and reperfusion in vivo Am J Physiol Heart Circ Physiol, August 1, 2000; 279(2): H601 - H609. [Abstract] [Full Text] [PDF]
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B. H. Lorell and B. A. Carabello Left Ventricular Hypertrophy : Pathogenesis, Detection, and Prognosis Circulation, July 25, 2000; 102(4): 470 - 479. [Full Text] [PDF]
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F. G Spinale, M. L Coker, B. R Bond, and J. L Zellner Myocardial matrix degradation and metalloproteinase activation in the failing heart: a potential therapeutic target Cardiovasc Res, May 1, 2000; 46(2): 225 - 238. [Abstract] [Full Text] [PDF]
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I. M.C. Dixon, J. Hao, N. L. Reid, and J. C. Roth Effect of chronic AT1 receptor blockade on cardiac Smad overexpression in hereditary cardiomyopathic hamsters Cardiovasc Res, May 1, 2000; 46(2): 286 - 297. [Abstract] [Full Text] [PDF]
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J.T. Peterson, H. Li, L. Dillon, and J. W. Bryant Evolution of matrix metalloprotease and tissue inhibitor expression during heart failure progression in the infarcted rat Cardiovasc Res, May 1, 2000; 46(2): 307 - 315. [Abstract] [Full Text] [PDF]
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P.-Y. Cheung, G. Sawicki, M. Wozniak, W. Wang, M. W. Radomski, and R. Schulz Matrix Metalloproteinase-2 Contributes to Ischemia-Reperfusion Injury in the Heart Circulation, April 18, 2000; 101(15): 1833 - 1839. [Abstract] [Full Text] [PDF]
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H. Senzaki, N. Paolocci, Y. A. Gluzband, M. L. Lindsey, J. S. Janicki, M. T. Crow, and D. A. Kass {beta}-Blockade Prevents Sustained Metalloproteinase Activation and Diastolic Stiffening Induced by Angiotensin II Combined With Evolving Cardiac Dysfunction Circ. Res., April 14, 2000; 86(7): 807 - 815. [Abstract] [Full Text] [PDF]
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Y. Nagatomo, B. A. Carabello, M. L. Coker, P. J. McDermott, S. Nemoto, M. Hamawaki, and F. G. Spinale Differential effects of pressure or volume overload on myocardial MMP levels and inhibitory control Am J Physiol Heart Circ Physiol, January 1, 2000; 278(1): H151 - H161. [Abstract] [Full Text] [PDF]
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P. Rouet-Benzineb, J.-M. Buhler, P. Dreyfus, A. Delcourt, R. Dorent, J. Perennec, B. Crozatier, A. Harf, and C. Lafuma Altered balance between matrix gelatinases (MMP-2 and MMP-9) and their tissue inhibitors in human dilated cardiomyopathy: potential role of MMP-9 in myosin-heavy chain degradation Eur J Heart Fail, December 17, 1999; 1(4): 337 - 352. [Abstract] [Full Text] [PDF]
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