(Circulation. 1996;93:1230-1243.)
© 1996 American Heart Association, Inc.
Articles |
Basis for Increased Microtubules in Pressure-Hypertrophied Cardiocytes
From the Cardiology Section of the Department of Medicine and the Department of Physiology, Gazes Cardiac Research Institute, Medical University of South Carolina; and the Veterans Administration Medical Center, Charleston, SC.
Background We have shown on the levels of the sarcomere and the cardiocyte that a persistent increase in microtubule density accounts to a remarkable degree for the contractile dysfunction seen in pressure-overload right ventricular hypertrophy. In the present study, we have asked whether these linked phenotypic and contractile abnormalities are an immediate and direct effect of load input into the cardiocyte or instead a concomitant of hypertrophic growth in response to pressure overloading.
Methods and Results The feline right ventricle was pressure-overloaded by pulmonary artery banding. The quantity of microtubules was estimated from immunoblots and immunofluorescent micrographs, and their mechanical effects were assessed by measuring sarcomere motion during microtubule depolymerization. The biogenesis of microtubules was estimated from Northern and Western blot analyses of tubulin mRNAs and proteins. These measurements were made in control cats and in operated cats during and after the completion of right ventricular hypertrophy; the left ventricle from each heart served as a normally loaded same-animal control. We have shown that the alterations in microtubule density and sarcomere mechanics are not an immediate consequence of pressure overloading but instead appear in parallel with the load-induced increase in cardiac mass. Of potential mechanistic importance, both these changes and increases in tubulin poly A+ mRNA and protein coexist indefinitely after a new, higher steady state of right ventricular mass is reached.
Conclusions Because we find persistent increases both in microtubules and in their biosynthetic precursors in pressure-hypertrophied myocardium, the mechanisms for this cytoskeletal abnormality must be sought through studies of the control both of microtubule stability and of tubulin synthesis.
Key Words: hypertrophy • contractility • cytoskeleton
This article has been cited by other articles:
 |
|
 |
|
  A. Bye, M. Langaas, M. A. Hoydal, O. J. Kemi, G. Heinrich, L. G. Koch, S. L. Britton, S. M. Najjar, O. Ellingsen, and U. Wisloff Aerobic capacity-dependent differences in cardiac gene expression Physiol Genomics, October 8, 2008; 33(1): 100 - 109. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. K. Mani, H. Shiraishi, S. Balasubramanian, K. Yamane, M. Chellaiah, G. Cooper, N. Banik, M. R. Zile, and D. Kuppuswamy In vivo administration of calpeptin attenuates calpain activation and cardiomyocyte loss in pressure-overloaded feline myocardium Am J Physiol Heart Circ Physiol, July 1, 2008; 295(1): H314 - H326. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Scholz, C. F. Baicu, W. J. Tuxworth, L. Xu, H. Kasiganesan, D. R. Menick, and G. Cooper IV Microtubule-dependent distribution of mRNA in adult cardiocytes Am J Physiol Heart Circ Physiol, March 1, 2008; 294(3): H1135 - H1144. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Scholz, P. McDermott, M. Garnovskaya, T. N. Gallien, S. Huettelmaier, C. DeRienzo, and G. Cooper IV Microtubule-associated protein-4 (MAP-4) inhibits microtubule-dependent distribution of mRNA in isolated neonatal cardiocytes Cardiovasc Res, August 1, 2006; 71(3): 506 - 516. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. J. Davis, J. B Pillai, M. Gupta, and M. P. Gupta Concurrent opposite effects of trichostatin A, an inhibitor of histone deacetylases, on expression of {alpha}-MHC and cardiac tubulins: implication for gain in cardiac muscle contractility Am J Physiol Heart Circ Physiol, March 1, 2005; 288(3): H1477 - H1490. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Takahashi, H. Shiraishi, Y. Ishibashi, K. L. Blade, P. J. McDermott, D. R. Menick, D. Kuppuswamy, and G. Cooper IV Phenotypic consequences of {beta}1-tubulin expression and MAP4 decoration of microtubules in adult cardiocytes Am J Physiol Heart Circ Physiol, November 1, 2003; 285(5): H2072 - H2083. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. S. Scopacasa, V. P. A. Teixeira, and K. G. Franchini Colchicine attenuates left ventricular hypertrophy but preserves cardiac function of aortic-constricted rats J Appl Physiol, April 1, 2003; 94(4): 1627 - 1633. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. R. Zile, G. R. Green, G. T. Schuyler, G. P. Aurigemma, D. C. Miller, and G. Cooper IV Cardiocyte cytoskeleton in patients with left ventricular pressure overload hypertrophy J. Am. Coll. Cardiol., March 15, 2001; 37(4): 1080 - 1084. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. C. Calaghan, J.-Y. Le Guennec, and E. White Modulation of Ca2+ Signaling by Microtubule Disruption in Rat Ventricular Myocytes and Its Dependence on the Ruptured Patch-Clamp Configuration Circ. Res., March 2, 2001; 88 (4): e32 - e37. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S Di Somma, M Marotta, G Salvatore, G Cudemo, G Cuda, F De Vivo, M P Di Benedetto, F Ciaramella, G Caputo, and O de Divitiis Changes in myocardial cytoskeletal intermediate filaments and myocyte contractile dysfunction in dilated cardiomyopathy: an in vivo study in humans Heart, December 1, 2000; 84(6): 659 - 667. [Abstract] [Full Text]
|
|
|
|
 |
|
 M. Koide, M. Hamawaki, T. Narishige, H. Sato, S. Nemoto, G. DeFreyte, M. R. Zile, G. Cooper IV, and B. A. Carabello Microtubule Depolymerization Normalizes In Vivo Myocardial Contractile Function in Dogs With Pressure-Overload Left Ventricular Hypertrophy Circulation, August 29, 2000; 102(9): 1045 - 1052. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Heling, R. Zimmermann, S. Kostin, Y. Maeno, S. Hein, B. Devaux, E. Bauer, W.-P. Klovekorn, M. Schlepper, W. Schaper, et al. Increased Expression of Cytoskeletal, Linkage, and Extracellular Proteins in Failing Human Myocardium Circ. Res., April 28, 2000; 86(8): 846 - 853. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Gomez, B. G. Kerfant, and G. Vassort Microtubule Disruption Modulates Ca2+ Signaling in Rat Cardiac Myocytes Circ. Res., January 7, 2000; 86(1): 30 - 36. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Nagatomo, B. A. Carabello, M. Hamawaki, S. Nemoto, T. Matsuo, and P. J. McDermott Translational mechanisms accelerate the rate of protein synthesis during canine pressure-overload hypertrophy Am J Physiol Heart Circ Physiol, December 1, 1999; 277(6): H2176 - H2184. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Narishige, K. L. Blade, Y. Ishibashi, T. Nagai, M. Hamawaki, D. R. Menick, D. Kuppuswamy, and G. Cooper IV Cardiac Hypertrophic and Developmental Regulation of the beta -Tubulin Multigene Family J. Biol. Chem., April 2, 1999; 274(14): 9692 - 9697. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. R. Zile, M. Koide, H. Sato, Y. Ishiguro, C. H. Conrad, J. M. Buckley, J. P. Morgan, and G. Cooper IV Role of microtubules in the contractile dysfunction of hypertrophied myocardium J. Am. Coll. Cardiol., January 1, 1999; 33(1): 250 - 260. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. C. Cicogna, K. G. Robinson, C. H. Conrad, K. Singh, R. Squire, M. P. Okoshi, and O. H. L. Bing Direct Effects of Colchicine on Myocardial Function : Studies in Hypertrophied and Failing Spontaneously Hypertensive Rats Hypertension, January 1, 1999; 33(1): 60 - 65. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. R. Zile, K. Richardson, M. K. Cowles, J. M. Buckley, M. Koide, B. A. Cowles, V. Gharpuray, and G. Cooper IV Constitutive Properties of Adult Mammalian Cardiac Muscle Cells Circulation, August 11, 1998; 98(6): 567 - 579. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. P. Bauer, S. Kuki, R. Zimmermann, and W. Schaper Upregulated and downregulated transcription of myocardial genes after pulmonary artery banding in pigs Ann. Thorac. Surg., August 1, 1998; 66(2): 527 - 531. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. T. Thompson, M. S. Rackley, and T. X. O'Brien Upregulation of the cardiac homeobox gene Nkx2-5 (CSX) in feline right ventricular pressure overload Am J Physiol Heart Circ Physiol, May 1, 1998; 274(5): H1569 - H1573. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Tagawa, M. Koide, H. Sato, M. R. Zile, B. A. Carabello, and G. Cooper IV Cytoskeletal Role in the Transition From Compensated to Decompensated Hypertrophy During Adult Canine Left Ventricular Pressure Overloading Circ. Res., April 20, 1998; 82(7): 751 - 761. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. E. D. J. ter Keurs Microtubules in Cardiac Hypertrophy : A Mechanical Role in Decompensation? Circ. Res., April 20, 1998; 82(7): 828 - 831. [Full Text] [PDF]
|
|
|
|
|
|
E. McCall, K. S. Ginsburg, R. A. Bassani, T. R. Shannon, M. Qi, A. M. Samarel, and D. M. Bers Ca flux, contractility, and excitation-contraction coupling in hypertrophic rat ventricular myocytes Am J Physiol Heart Circ Physiol, April 1, 1998; 274(4): H1348 - H1360. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Putnam, J. Cunningham, R. Dennis, J. Linderman, and D. Mooney Microtubule assembly is regulated by externally applied strain in cultured smooth muscle cells J. Cell Sci., January 11, 1998; 111(22): 3379 - 3387. [Abstract] [PDF]
|
|
|
|
 |
|
 H. Sato, T. Nagai, D. Kuppuswamy, T. Narishige, M. Koide, D. R. Menick, and G. C. IV Microtubule Stabilization in Pressure Overload Cardiac Hypertrophy J. Cell Biol., November 17, 1997; 139(4): 963 - 973. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Kuppuswamy, C. Kerr, T. Narishige, V. S. Kasi, D. R. Menick, and G. Cooper IV Association of Tyrosine-phosphorylated c-Src with the Cytoskeleton of Hypertrophying Myocardium J. Biol. Chem., February 14, 1997; 272(7): 4500 - 4508. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Tagawa, N. Wang, T. Narishige, D. E. Ingber, M. R. Zile, and G. Cooper IV Cytoskeletal Mechanics in Pressure-Overload Cardiac Hypertrophy Circ. Res., February 1, 1997; 80(2): 281 - 289. [Abstract] [Full Text]
|
|
|
|
|
|
R. A. Walsh Microtubules and Pressure-Overload Hypertrophy Circ. Res., February 1, 1997; 80(2): 295 - 296. [Full Text]
|
|