Role of transiently altered sarcolemmal membrane permeability and basic fibroblast growth factor release in the hypertrophic response of adult rat ventricular myocytes to increased mechanical activity in vitro

Journal of Clinical Investigation

Volumn 97, Issue 2, 1996, Pages 281-291

  Kaye, David ^a   Pimental, David ^a   Prasad, Sanjay ^a   Mäki, Tiina ^a   Berger, Hans Jörg ^a   McNeil, Paul L ^b   Smith, Thomas W ^a   Kelly, Ralph A ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

2,3 butanedione monoxime; Angiogenesis; Fluorescence activated cell sorting

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; CELL PROTEIN; FIBROBLAST GROWTH FACTOR 2; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; NEUTRALIZING ANTIBODY; PHENYLALANINE; RECOMBINANT BASIC FIBROBLAST GROWTH FACTOR;

ADAPTATION; ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL STRAIN 3T3; CONTROLLED STUDY; CYTOSOL; ELECTROSTIMULATION; HEART MUSCLE FIBER MEMBRANE; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE PACING; HEART VENTRICLE WALL; HEART WORK; MALE; MECHANICAL STRESS; MEMBRANE DAMAGE; MITOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CARDIOMEGALY; CELL MEMBRANE PERMEABILITY; CELL SIZE; CELLS, CULTURED; ELECTRIC STIMULATION; FIBROBLAST GROWTH FACTOR 2; MALE; MUSCLE PROTEINS; MYOCARDIUM; RATS; RATS, SPRAGUE-DAWLEY; SARCOLEMMA; STRESS, MECHANICAL;

EID: 0030071564     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI118414     Document Type: Article

References (70)

1. Cooper IV, G., R. L Kent, and D. L. Mann. 1989. Load induction of cardiac hypertrophy. J Mol. Cell. Cardiol 21:11-30.
2. Chien, K. R., K. U. Knowlton, H. Zhu, and S. Chien. 1991. Regulation of cardiac gene expression during myocardial growth and hypertrophy: molecular studies of an adaptive physiologic response FASEB J. 5.3037-3046.
3. Parker, T. G., and M. D. Schneider. 1991. Growth factors, proto-oncogenes, and plasticity of the cardiac phenotype Annu. Rev. Physiol. 53:179-200.
4. 1-adrenergic receptor interaction. Circ Res. 56:884-894.
5. 1-adrenergic receptor-stimulated hypertrophy of cultured rat heart myocytes. J. Clin. Invest. 85:1206-1214
6. Clark, W. A., S. J. Rudnick, J. J. LaPres, L. C. Andersen, and M. C. LaPointe 1993. Regulation of hypertrophy and atrophy in cultured adult heait cells. Circ Res. 73:1163-1176.
7. Knowlton, K. U., E. Baracchini, R. S. Ross, A. N Harris, S. A. Henderson, S. M Evans, C C Glembotski, and K R. Chien. 1991. Co-regulation of the atrial natriuretic factor and cardiac myosin light chain-2 genes during α-adrenergic stimulation of neonatal rat ventricular cells. Identification of cis sequences within an embryonic and a constitutive contractile protein gene which mediate inducible expression J. Biol. Chem, 266:7759-7768.
8. 1-adrenergic stimulation J. Biol. Chem. 269.13490-13496.
9. Clark, W. A., S J Rudnick, L. C. Anderson, and J. J. LaPres 1994 Myosin heavy chain synthesis is independently regulated in hypertrophy and atrophy of isolated adult cardiac myocytes. J. Biol. Chem., 269.25562-25569.
10. Bogoyevitch, M. A., P E. Glennon, M. B. Andersson, A. Clerk, A. Lazou, C. J Marshall, P J Parker, and P. H. Sugden. 1994. Endothelin-1 and fibroblast growth factors stimulate the mitogen-activated protein kinase signaling cascade in cardiac myocytes. The potential role of the cascade in the integration of two signaling pathways leading to myocyte hypertrophy. J. Biol Chem. 269 1110-1119.
11. 2+-dependent signaling. Circ Res. 76:1-15
12. Sachs, F 1989 Ion channels as mechanical transducers. In Cell Shape. Determinants, Regulation and Regulatory Role. W. D. Stein and F Bronner, editors Academic Press, New York. 63-92.
13. Schwartz, M. A. 1993 Spreading of human endothelial cells on fibronectin or vitronectin triggers elevation of intracellular free calcium. J. Cell Biol 120:1003-1010.
14. Juliano, R. L., and S. Haskill. 1993. Signal transduction from the extracellular matrix. J Cell Biol 120:577-585.
15. Fujimoto, T., S. Nakade, A. Miyawaki, K. Mikoshiba, and K. Ogawa. 1992. Localization of inositol 1,4,5-triphosphate receptor-like protein in plasmalemmal caveolae, J. Cell Biol. 119:1507-1513.
16. Davies, P. F., and S. C. Tripathi. 1993. Mechanical stress mechanism. An endothelial paradigm. Circ Res. 72:239-245.
17. Ingber, D. 1991. Integrins as mechanochemical transducers. Curr Opin. Cell Biol. 3:841-848.
18. Casscells, W., E. Speir, J. Sasse, K Klagsbrun, P Allen, M. Lee, M Chiba, L. Haggroth, B. Calvo, J. Folkman, and S. E. Epstein 1990. Isolation and characterization of heparin-binding growth factors from human myocardium J Clin Invest. 85:433-441
19. Kardami, E., and R Fandrich. 1989. Basic fibroblast growth factor in atria and ventricles of the vertebrate heart. J. Cell Biol 109.1865-1875.
20. Sasaki, H., H. Hoshi, Y M. Hong, T Suzuki, T. Kato, H. Sasaki, M. Saito, H Youki, K. Karube, S. Konno, M. Onodera, T. Saito, and S. Aoyagi. 1989. Purification of acidic fibroblast growth factor from bovine heart and its localization in the cardiac myocytes. J. Biol. Chem 264:17606-17612
21. Weiner, H L., and J. L. Swain 1989. Acidic fibroblast growth factor is expressed by cardiac myocytes in culture and the protein is localized to the extracellular matrix. Proc. Natl. Acad. Sci. USA. 86:2683-2687.
22. Speir, E., V Tanner, A M. Gonzalez, J. Farris, A. Baird, and W. Casscells. 1992. Acidic and basic fibroblast growth factors in adult rat heart myocytes. Localization, regulation in culture, and effects on DNA synthesis. Circ. Res. 71:251-259
23. Engelmann, G L., C A. Dionne, and M. C. Jaye. 1993. Acidic fibroblast growth factor and heart development Role in myocyte proliferation and capillary angiogenesis Circ Res 72:7-19.
24. Mima, T., H. Ueno, D. A. Fischman, L T. Williams, and T. Mikawa 1995. Fibroblast growth factor receptor is required for in vivo cardiac myocyte proliferation at early embryonic stages of heart development. Proc. Natl. Acad. Sci. USA. 92.467-471.
25. Parker, T. G., K.-L Chow, R J Schwartz, and M. D. Schneider. 1992. Positive and negative control of the skeletal α-actin promoter in cardiac muscle A proximal serum response element is sufficient for induction by basic fibroblast growth factor (FGF) but not for inhibition by acidic FGF J Biol. Chem 267:3343-3350
26. Jin, Y., K. B. S. Pasumarthi, M E. Bock, A. Lytras, E. Kaidami, and P. A. Cattini. 1994. Cloning and expression of fibroblast growth factor receptor-1 isoforms in the mouse heart evidence for isoform switching during heart development. J. Mol Cell. Cardiol 26:1449-1459.
27. Mason, I. J. 1994. The ins and outs of fibroblast growth factors. Cell 78: 547-552.
28. McNeil, P. L , L Muthukrishnan, E. Warder, and P A D'Amore 1989. Growth factors are released by mechanically wounded endothelial cells. J Cell Biol. 109.811-822.
29. McNeil, P. L., and R. Khakee. 1992. Disruptions of muscle fiber plasma membranes: role in exercise-induced damage. Am. J Pathol. 140:1097-1109.
30. McNeil, P. L. 1993. Cellular and molecular adaptations to injurious mechanical force. Trends Cell Biol. 3:302-307.
31. Berger, H -J., S. K. Prasad, A. J. Davidoff, D Pimentai, Ø Ellingsen, J. D Marsh, T. W. Smith, and R. A. Kelly. 1994. Continual electric field stimulation preserves contractile function of adult ventricular myocytes in primary culture. Am. J. Physiol. 266:H341-H349.
32. Ellingsen, Ø., A. J. Davidoff, S. K. Prasad, H.-J. Berger, J. P. Springhorn, J. D Marsh, R. A. Kelly, and T. W. Smith. 1993. Adult rat ventricular myocytes cultured in defined medium: phenotype and electromechanical function. Am. J. Physiol 265:H747-H754.
33. Chomczynski, P., and N. Sacchi. 1987 Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
34. McNeil, P. L 1989. Incorporation of macromolecules into living cells. Methods Cell Biol 29:153-173.
35. Claycomb, W. C., and M. C. Palazzo. 1980. Culture of the terminally differentiated adult cardiac muscle cell. A light and scanning electron microscope study. Dev. Biol. 80:466-482.
36. Claycomb, W. C. 1988. Atnal natriuretic factor mRNA is developmentally regulated in heart ventricles and actively expressed in cultured ventricular cardiac muscle cells of rat and human. Biochem. J. 255:617-620.
37. Kato, S., C. T. Ivester, M. R. Zile, and P. J. McDermott. 1995. Growth effects of electrically stimulated contraction on adult feline cardiocytes in primary culture. Am. J. Physiol 268:H2495-H2504.
38. Eid, H., D. M. Larson, J. P. Springhorn, M. A. Attawia, R. C. Nayak, T W. Smith, and R. A. Kelly. 1992. Role of epicardial mesothelial cells in the modification of phenotype and function of adult rat ventricular myocytes in long-term coculture. Circ. Res. 71 40-50.
39. Bugaisky, K. B., and R. Zak. 1989 Differentiation of adult rat cardiac myocytes in cell culture Circ. Res. 64:493-500.
40. Sadoshima, J.-I., and S. Izumo 1993. Molecular characterization of angiotensin II-induced hypertrophy of cardiac myocytes and hyperplasia of cardiac fibroblasts. Critical role of the AT1 receptor subtype. Circ. Res. 73:413-423
41. Sadoshima, J.-I., Y. Xu, H.S. Slayter, and S. Izumo. 1993. Autocnne release of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Cell 75:977-984.
42. Ito, H., Y. Hirata, S. Adachi, M Tanaka, M. Tsujino, A. Koike, A. Nogami, F. Marumo, and M. Hiroe. 1993. Endothelin-1 is an autocrine/paracrine factor in the mechanism of angiotensin II-induced hypertrophy in cultured rat cardiomyocytes. J Clin. Invest 92:398-403.
43. Shubeita, H. E., P. M. McDonough, A. N. Harris, K. U Knowlton, C. C. Glembotski, J. H. Brown, and K.R. Chien. 1990. Endothelin induction of mositol phospholipid hydrolysis, sarcomere assembly, and cardiac gene expression in ventricular myocytes. A paracrine mechanism for myocardial cell hypertrophy. J Biol. Chem. 265:20555-20562
44. Donohue, T. J., L. D. Dworkin, M. N. Lango, K. Fliegner, R. P. Lango, J. A. Benstein, W. R. Slater, and V. M. Catanese 1994. Induction of myocardial insulin-like growth factor-I gene expression in left ventricular hypertrophy Circulation. 89:799-809.
45. Mann, D L., R. L. Kent, and G. Cooper IV 1989 Load regulation of the properties of adult feline cardiocytes: growth induction by cellular deformation. Circ. Res. 64:1079-1090.
46. Sadoshima, J., L Jahn, T. Takahashi, T. J. Kulik, and S Izumo. 1992 Molecular characterization of the stretch-induced adaptation of cultured cardiac cells: an in vitro model of load-induced hypertrophy. J. Biol Chem 267: 10551-10560.
47. Sadoshima, J , and S. Izumo 1993. Mechanical stretch rapidly activates multiple signal transduction pathways in cardiac myocytes. potential involvement of an autocrine/paracrine mechanism. EMBO (Eur. Mol Biol. Organ.) J. 12:1681-1692
48. Bishop, J. E , J J. Mitchell, P. M. Absher, L Baldor, H A. Geller, J. Woodcock-Mitchell, M. J. Hamblin, P. Vacek, and R. B. Low. 1993. Cyclic mechanical deformation stimulates human lung fibroblast proliferation and autocrine growth factor activity. Am. J. Respir. Cell Mol. Biol. 9:126-133.
49. Antonio, J., and W. J Gonyea. 1993. Progressive stretch overload of skeletal muscle results in hypertrophy before hyperplasia. J. Appl Physiol. 74. 1893-1898.
50. Wilson, E., Q Mai, K. Sudhir, R. H. Weiss, and H. E Ives. 1993. Mechanical strain induces growth of vascular smooth muscle cells via autocrine action of PDGF. J. Cell Biol 123:741-747.
51. Ivester, C. T., R. L. Kent, H. Tagawa, H. Tsutsui, T. Imamura, G. Cooper IV, and P. J. McDermott. 1993. Electrically stimulated contraction accelerates protein synthesis rates in adult feline cardiocytes. Am. J. Physiol. 265: H666-H674.
52. Kubisch, C., B. Wollnik, A. Maass, R. Meyer, H. Vetter, and L Neyses. 1993. Immediate-early gene induction by repetitive mechanical but not electrical activity in adult rat cardiomyocytes. FEBS Lett. 335:37-40.
53. Sadoshima, J.-I., T. Takahashi, L. Jahn, and S. Izumo. 1992 Roles of mechano-sensitive ion channels, cytoskeleton, and contractile activity in stretch-induced immediate-early gene expression and hypertrophy of cardiac myocytes. Proc. Natl. Acad. Sci USA. 89:9905-9909.
54. Morino, N., T. Mimura, K. Hamasaki, K. Tobe, K. Ueki, K. Kikuchi, K. Takehara, T. Kadowaki, Y. Yazaki, and Y. Nojima. 1995. Matrix/integrin interaction activates the mitogen-activated protein kinase, p44erk-1 and p42erk-2. J. Biol Chem. 270:269-273.
55. Yamazaki, T., K. Tobe, E. Hoh, K. Maemura, T. Kaida, I. Komuro, H. Tamemoto, T Kadowaki, R. Nagai, and Y. Yazaki. 1993. Mechanical loading activates mitogen-activated protein kinase and S6 peptide kinase in cultured rat cardiac myocytes. J. Biol. Chem. 266:12069-12076.
56. Parlow, M. H , D. L. Bolender, N. P Kokan-Moore, and J. Lough. 1991. Localization of bFGF-like proteins as puctuate inclusions in the preseptation myocardium of the chicken embryo. Dev. Biol. 146:139-147.
57. Spirito, P , Y.-M Fu, Z -X. Zu, S. E Epstein, and W. Casscells. 1991. Immunohistochemical localization of basic and acidic fibroblast growth factors in the developing rat heart. Circulation. 84:322-332.
58. Sugi, Y., J. Sasse, and J. Lough. 1993. Inhibition of precardiac mesoderm cell proliferation by antisense oligodeoxynucleotide complementary to fibroblast growth factor-2 (FGF-2). Dev. Biol. 157:28-37.
59. Padua, R R., and E. Kardami. 1993. Increased basic fibroblast growth factor (bFGF) accumulation and distinct patterns of localization in isoproterenol-induced cardiomyocyte injury Growth Factors. 8:291-306.
60. Clarke, M S F., R W. Caldwell, H. Chiao, K. Miyake, and P. L. McNeil. 1995. Contraction-induced cell wounding and release of fibroblast growth factor in heart. Circ. Res. 76:927-934.
61. Yamazaki, T., I. Komuro, S. Kudoh, Y. Zou, I. Shiojima, T. Mizuno, H. Takano, Y. Hiroi, K. Ueki, K Tobe, et al 1995. Angiotensin II partly mediates mechanical stress-induced cardiac hypertrophy. Circ. Res. 77:258-265.
62. Fishel, R. S., V. Thourani, S. J. Eisenberg, S. Y Shai, M. A. Corson, E. G. Nabel, K. E. Bernstein, and B. C. Berk. 1995. Fibroblast growth factor stimulates angiotensm converting enzyme expression in vascular smooth muscle cells Possible mediator of the response to vascular injury. J Clin. Invest. 95: 377-387.
63. Perrella, M. A., T Maki, S Prasad, D. Pimentai, K. Singh, N. Takahashi, M. Yoshizumi, A. Alali, S. Higashiyama, R. A. Kelly, et al. 1994 Regulation of heparin-binding epidermal growth factor-like growth factor (HB-EGF) mRNA levels by hypertrophic stimuli in neonatal and adult rat cardiac myocytes. J Biol Chem. 269 27045-27050.
64. 2+], and cross-bridge kinetics. J. Physiol. 476:487-500.
65. Miyamoto, M , K.-I. Naruo, C. Seko, S. Matsumoto, T. Kondo, and T. Kurokawa. 1993. Molecular cloning of a novel cytokine cDNA encoding the ninth member of the fibroblast growth factor family, which has a unique secretion property. Mol. Cell. Biol. 13:4251-4259.
66. Vagner, S., M.-C. Gensac, A. Maret, F. Bayard, F. Amalric, H. Prats, and A -C. Prats. 1995. Alternative translation of human fibroblast fibroblast growth factor 2 mRNA occurs by internal entry of ribosomes. Mol. Cell. Biol. 15:35-44
67. Wiedlocha, A , P O Falnes, I. H. Madshus, K. Sandvig, and S Olsnes. 1994. Dual mode of signal transduction by externally added acidic fibroblast growth factor. Cell. 76:1039-1051.
68. Clarke, M. S. F., R. Khakee, and P. L. McNeil. 1993. Loss of cytoplasmic basic fibroblast growth factor from physiologically wounded myofibers of normal and dystrophic muscle. J Cell Sci 106:121-133
69. Benzaquen, L R., A. Nicholson-Weller, and J. A. Halperin. 1994. Terminal complement proteins C5b-9 release basic fibroblast growth factor and platelet derived growth factor from endothelial cells. J. Exp. Med. 179:985-992.
70. Steinhardt, R. A., G. Hi, and J. M Alderton. 1994. Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release. Science (Wash. DC). 263:390-393.