© 1995 American Heart Association, Inc.
Articles |
Contraction-Induced Cell Wounding and Release of Fibroblast Growth Factor in Heart
From the Departments of Anatomy and Cellular Biology (M.S.F.C., K.M., P.L.M.) and Pharmacology and Toxicology (R.W.C., H.C.), The Medical College of Georgia, Augusta.
Correspondence to Dr Paul L. McNeil, Department of Anatomy and Cellular Biology, The Medical College of Georgia, Augusta, GA 30912-2000.
Abstract The heart hypertrophies in response to certain forms of increased mechanical load, but it is not understood how, at the molecular level, the mechanical stimulus of increased load is transduced into a cell growth response. One possibility is that mechanical stress provokes the release of myocyte-derived autocrine growth factors. Two such candidate growth factors, acidic and basic fibroblast growth factor (aFGF and bFGF, respectively), are released via mechanically induced disruptions of the cell plasma membrane. In the present study, we demonstrate that transient, survivable disruption (wounding) of the cardiac myocyte plasma membrane is a constitutive event in vivo. Frozen sections of normal rat heart were immunostained to reveal the distribution of the wound event marker, serum albumin. Quantitative image analysis of these sections indicated that an average of 25% of the myocytes contained cytosolic serum albumin; ie, this proportion had suffered a plasma membrane wound. Wounding frequency increased approximately threefold after ß-adrenergic stimulation of heart rate and force of contraction. Heparin-Sepharose chromatography, enzyme-linked immunosorbent assay, growth assay coupled with antibody neutralization, and two-dimensional SDS-PAGE followed by immunoblotting were used to demonstrate that both aFGF and bFGF were released from an ex vivo beating rat heart. Importantly, ß-adrenergic stimulation of heart rate and force of contraction increased FGF release. Cell wounding is a fundamental but previously unrecognized aspect of the biology of the cardiac myocyte. We propose that contraction-induced cardiac myocyte wounding releases aFGF and bFGF, which then may act as autocrine growth-promoting stimuli.
Key Words: fibroblast growth factor • myocardium • cell injury • plasma membrane • heart hypertrophy
This article has been cited by other articles:
 |
|
 |
|
  C. Etard, U. Roostalu, and U. Strahle Shuttling of the chaperones Unc45b and Hsp90a between the A band and the Z line of the myofibril J. Cell Biol., March 24, 2008; 180(6): 1163 - 1175. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. C. Squires, S. M. Muehlbauer, and J. Brojatsch Proteasomes Control Caspase-1 Activation in Anthrax Lethal Toxin-mediated Cell Killing J. Biol. Chem., November 23, 2007; 282(47): 34260 - 34267. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Amano, K. Miyake, J.L. Borke, and P.L. McNeil Breaking Biological Barriers with a Toothbrush J. Dent. Res., August 1, 2007; 86(8): 769 - 774. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. E. Ingber Cellular mechanotransduction: putting all the pieces together again FASEB J, May 1, 2006; 20(7): 811 - 827. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 O. Farkas, J. Lifshitz, and J. T. Povlishock Mechanoporation induced by diffuse traumatic brain injury: an irreversible or reversible response to injury? J. Neurosci., March 22, 2006; 26(12): 3130 - 3140. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Zolkiewska Ecto-ADP-ribose Transferases: Cell-Surface Response to Local Tissue Injury Physiology, December 1, 2005; 20(6): 374 - 381. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. McNeil and P. L. McNeil Yolk granule tethering: a role in cell resealing and identification of several protein components J. Cell Sci., October 15, 2005; 118(20): 4701 - 4708. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. F. Vatner FGF Induces Hypertrophy and Angiogenesis in Hibernating Myocardium Circ. Res., April 15, 2005; 96(7): 705 - 707. [Full Text] [PDF]
|
|
|
|
 |
|
 P. Camelliti, T. K. Borg, and P. Kohl Structural and functional characterisation of cardiac fibroblasts Cardiovasc Res, January 1, 2005; 65(1): 40 - 51. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Palmen, M. J.A.P. Daemen, L. J. De Windt, J. Willems, W. R.M. Dassen, S. Heeneman, R. Zimmermann, M. Van Bilsen, and P. A. Doevendans Fibroblast growth factor-1 improves cardiac functional recovery and enhances cell survival after ischemia and reperfusion: A fibroblast growth factor receptor, protein kinase c, and tyrosine kinase-dependent mechanism J. Am. Coll. Cardiol., September 1, 2004; 44(5): 1113 - 1123. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Kardami, Z.-S. Jiang, S. K Jimenez, C. J Hirst, F. Sheikh, P. Zahradka, and P. A Cattini Fibroblast growth factor 2 isoforms and cardiac hypertrophy Cardiovasc Res, August 15, 2004; 63(3): 458 - 466. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. K Jimenez, F. Sheikh, Y. Jin, K. A Detillieux, J. Dhaliwal, E. Kardami, and P. A Cattini Transcriptional regulation of FGF-2 gene expression in cardiac myocytes Cardiovasc Res, June 1, 2004; 62(3): 548 - 557. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. H. Singleton and J. T. Povlishock Identification and Characterization of Heterogeneous Neuronal Injury and Death in Regions of Diffuse Brain Injury: Evidence for Multiple Independent Injury Phenotypes J. Neurosci., April 7, 2004; 24(14): 3543 - 3553. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. L. House, C. Bolte, M. Zhou, T. Doetschman, R. Klevitsky, G. Newman, and J. E. J. Schultz Cardiac-Specific Overexpression of Fibroblast Growth Factor-2 Protects Against Myocardial Dysfunction and Infarction in a Murine Model of Low-Flow Ischemia Circulation, December 23, 2003; 108(25): 3140 - 3148. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. Hocher, R. Ziebig, C. Altermann, R. Krause, G. Asmus, C.-M. Richter, T. Slowinski, P. Sinha, and H.-H. Neumayer Different Impact of Biomarkers as Mortality Predictors among Diabetic and Nondiabetic Patients Undergoing Hemodialysis J. Am. Soc. Nephrol., September 1, 2003; 14(9): 2329 - 2337. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. A. Detillieux, F. Sheikh, E. Kardami, and P. A. Cattini Biological activities of fibroblast growth factor-2 in the adult myocardium Cardiovasc Res, January 1, 2003; 57(1): 8 - 19. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. T. A. Meij, F. Sheikh, S. K. Jimenez, P. W. Nickerson, E. Kardami, and P. A. Cattini Exacerbation of myocardial injury in transgenic mice overexpressing FGF-2 is T cell dependent Am J Physiol Heart Circ Physiol, February 1, 2002; 282(2): H547 - H555. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. L. McNeil Repairing a torn cell surface: make way, lysosomes to the rescue J. Cell Sci., January 3, 2002; 115(5): 873 - 879. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M.F. Orellana, A.K. Smith, J.L. Waller, E. DeLeon Jr., and J.L. Borke Plasma Membrane Disruption in Orthodontic Tooth Movement in Rats J. Dent. Res., January 1, 2002; 81(1): 43 - 47. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. W. Stroetz, N. E. Vlahakis, B. J. Walters, M. A. Schroeder, and R. D. Hubmayr Validation of a new live cell strain system: characterization of plasma membrane stress failure J Appl Physiol, June 1, 2001; 90(6): 2361 - 2370. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Sheikh, D. P. Sontag, R. R. Fandrich, E. Kardami, and P. A. Cattini Overexpression of FGF-2 increases cardiac myocyte viability after injury in isolated mouse hearts Am J Physiol Heart Circ Physiol, March 1, 2001; 280(3): H1039 - H1050. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Miyake, P. L. McNeil, K. Suzuki, R. Tsunoda, and N. Sugai An actin barrier to resealing J. Cell Sci., January 10, 2001; 114(19): 3487 - 3494. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Jin, F. Sheikh, K. A. Detillieux, and P. A. Cattini Role for Early Growth Response-1 Protein in alpha 1-Adrenergic Stimulation of Fibroblast Growth Factor-2 Promoter Activity in Cardiac Myocytes Mol. Pharmacol., May 1, 2000; 57(5): 984 - 990. [Abstract] [Full Text]
|
|
|
|
 |
|
 M. E. Hartnett, C. M. Garcia, and P. A. D’Amore Release of bFGF, an Endothelial Cell Survival Factor, by Osmotic Shock Invest. Ophthalmol. Vis. Sci., November 1, 1999; 40(12): 2945 - 2951. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. P. Grembowicz, D. Sprague, and P. L. McNeil Temporary Disruption of the Plasma Membrane Is Required for c-fos Expression in Response to Mechanical Stress Mol. Biol. Cell, April 1, 1999; 10(4): 1247 - 1257. [Abstract] [Full Text]
|
|
|
|
|
|
K. A. Detillieux, J. T. A. Meij, E. Kardami, and P. A. Cattini alpha 1-Adrenergic stimulation of FGF-2 promoter in cardiac myocytes and in adult transgenic mouse hearts Am J Physiol Heart Circ Physiol, March 1, 1999; 276(3): H826 - H833. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. Straub, F. Duclos, D. P. Venzke, J. C. Lee, S. Cutshall, C. J. Leveille, and K. P. Campbell Molecular Pathogenesis of Muscle Degeneration in the {delta}-Sarcoglycan-Deficient Hamster Am. J. Pathol., November 1, 1998; 153(5): 1623 - 1630. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Grima, C. C. S. Wong, L.-j. Zhu, S.-d. Zong, and C. Y. Cheng Testin Secreted by Sertoli Cells Is Associated with the Cell Surface, and Its Expression Correlates with the Disruption of Sertoli-Germ Cell Junctions but Not the Inter-Sertoli Tight Junction J. Biol. Chem., August 14, 1998; 273(33): 21040 - 21053. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. S. F. Clarke, M. M. Bamman, and D. L. Feeback Bed rest decreases mechanically induced myofiber wounding and consequent wound-mediated FGF release J Appl Physiol, August 1, 1998; 85(2): 593 - 600. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Ortega, M. Ittmann, S. H. Tsang, M. Ehrlich, and C. Basilico Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2 PNAS, May 12, 1998; 95(10): 5672 - 5677. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Rosenfeldt, D. J. Lee, and F. Grinnell Increased c-fos mRNA Expression By Human Fibroblasts Contracting Stressed Collagen Matrices Mol. Cell. Biol., May 1, 1998; 18(5): 2659 - 2667. [Abstract] [Full Text]
|
|
|
|
|
|
S. Corda, A. Mebazaa, M.-P. Gandolfini, C. Fitting, F. Marotte, J. Peynet, D. Charlemagne, J.-M. Cavaillon, D. Payen, L. Rappaport, et al. Trophic Effect of Human Pericardial Fluid on Adult Cardiac Myocytes : Differential Role of Fibroblast Growth Factor-2 and Factors Related to Ventricular Hypertrophy Circ. Res., November 19, 1997; 81(5): 679 - 687. [Abstract] [Full Text]
|
|
|
|
 |
|
 T. A. Fischer, P. L. McNeil, R. Khakee, P. Finn, R. A. Kelly, M. A. Pfeffer, and J. M. Pfeffer Cardiac Myocyte Membrane Wounding in the Abruptly Pressure-Overloaded Rat Heart Under High Wall Stress Hypertension, November 1, 1997; 30(5): 1041 - 1046. [Abstract] [Full Text]
|
|
|
|
|
|
V. Straub, J. A. Rafael, J. S. Chamberlain, and K. P. Campbell Animal Models for Muscular Dystrophy Show Different Patterns of Sarcolemmal Disruption J. Cell Biol., October 20, 1997; 139(2): 375 - 385. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. L. McNeil and R. A. Steinhardt Loss, Restoration, and Maintenance of Plasma Membrane Integrity J. Cell Biol., April 7, 1997; 137(1): 1 - 4. [Full Text] [PDF]
|
|
|
|
|
|
J.-W. Gu, D. Santiago, Y. Olowe, and J. Weinberger Basic Fibroblast Growth Factor as a Biochemical Marker of Exercise-Induced Ischemia Circulation, March 4, 1997; 95(5): 1165 - 1168. [Abstract] [Full Text]
|
|
|
|
 |
|
 N. M. Ananyeva, A. V. Tjurmin, J. A. Berliner, G. M. Chisolm, G. Liau, J. A. Winkles, and C. C. Haudenschild Oxidized LDL Mediates the Release of Fibroblast Growth Factor-1 Arterioscler. Thromb. Vasc. Biol., March 1, 1997; 17(3): 445 - 453. [Abstract] [Full Text]
|
|
|
|
|
|
G. C. Cheng, W. H. Briggs, D. S. Gerson, P. Libby, A. J. Grodzinsky, M. L. Gray, and R. T. Lee Mechanical Strain Tightly Controls Fibroblast Growth Factor-2 Release From Cultured Human Vascular Smooth Muscle Cells Circ. Res., January 1, 1997; 80(1): 28 - 36. [Abstract] [Full Text]
|
|
|
|
|
|
B. W. Doble, Y. Chen, D. G. Bosc, D. W. Litchfield, and E. Kardami Fibroblast Growth Factor-2 Decreases Metabolic Coupling and Stimulates Phosphorylation as Well as Masking of Connexin43 Epitopes in Cardiac Myocytes Circ. Res., October 1, 1996; 79(4): 647 - 658. [Abstract] [Full Text]
|
|
|
|
|
|
R. Dono, J. Faulhaber, A. Galli, A. Zuniga, T. Volk, G. Texido, R. Zeller, and H. Ehmke FGF2 Signaling Is Required for the Development of Neuronal Circuits Regulating Blood Pressure Circ. Res., January 11, 2002; 90 (1): e5 - e10. [Abstract] [Full Text] [PDF]
|
|