Thin filament protein dynamics in fully differentiated adult cardiac myocytes: Toward a model of sarcomere maintenance

Journal of Cell Biology

Volumn 145, Issue 7, 1999, Pages 1483-1495

  Michele, Daniel E ^a   Albayya, Paris P ^a   Metzger, Joseph M ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Cardiomyocyte; Muscle proteins; Muscle structure; Tropomyosin; Troponin

Indexed keywords

MUSCLE PROTEIN; TROPOMYOSIN; TROPONIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DYNAMICS; GENE TRANSFER; HEART MUSCLE CELL; MODEL; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN METABOLISM; PROTEIN SYNTHESIS; RAT; SARCOMERE; THIN FILAMENT;

ADENOVIRIDAE; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; EPITOPES; FEMALE; GENE TRANSFER TECHNIQUES; HALF-LIFE; HUMANS; MICROFILAMENTS; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; MUSCLE PROTEINS; MYOCARDIAL CONTRACTION; MYOCARDIUM; POLYMERS; PROTEIN ISOFORMS; RATS; RECOMBINANT FUSION PROTEINS; SARCOMERES; TROPOMYOSIN; TROPONIN I;

ANIMALIA;

EID: 0033612534     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.7.1483     Document Type: Article

References (43)

1. Auerbach, D., B. Rothen-Ruthishauser, S. Bantle, M. Leu, E. Ehler, D. Helfman, and J.-C. Perriard. 1997. Molecular mechanisms of myofibril assembly in heart. Cell Struct. Fund. 22:139-146.
2. Blanchard, E.M., K. Iizuka, M. Christe, D.A. Conner, A. Geisterfer-Lowrance, F.J. Schoen, D.W. Maughn, C.E. Seidman, and J.G. Seidman. 1997. Targeted ablation of the murine alpha-tropomyosin gene. Circ. Res. 81:1005-1010.
3. Dabiri, G.A., K.K. Turnacioglu, J.M. Sanger, and J.W. Sanger. 1997. Myofibrillogenesis visualized in living embryonic cardiomyocytes. Proc. Natl. Acad. Sci. USA. 94:9493-9498.
4. Dome, J.S., B. Mittal, M.B. Pochapin, J.M. Sanger, and J.W. Sanger. 1988. Incorporation of fluorescently labeled actin and tropomyosin into muscle cells. Cell Differ. 23:37-52.
5. Dlugosz, A.A., P.B. Antin, V.T. Nachmias, and H. Holzer. 1984. The relationship between stress-fiber-like structures and nascent myofibrils in cultured cardiac myocytes. J. Cell Biol. 99:2268-2278.
6. Endo, M., Y. Nonomura, T. Masaki, I. Ohtsuki, and S. Ebashi. 1966. Localization of native tropomyosin in relation to striation patterns. J. Biochem. 60: 605-608.
7. Eppenberger, M.E., I. Hauser, T. Bächi, M.C. Schaub, U.T. Brunner, C.A. Dechesne, and H.M. Eppenberger. 1988. Immunocytochemical analysis of the regeneration of myofibrils in long-term cultures of adult cardiac myocytes of the rat. Dev. Biol. 130:1-15.
8. Helfman, D.M., C. Berthier, J. Grossman, M. Leu, E. Ehler, E. Perriard, and J.-C. Perriard. 1999. Nonmuscle tropomyosin-4 requires co-expression with other low molecular weight isoforms for binding to the thin filaments in cardiac myocytes. J. Cell. Sci. 112:371-380.
9. Hibberd, M.G., and B.R. Jewell. 1982. Calcium-and length-dependent force production in rat ventricular muscle. J. Physiol. Lond. 329:527-540.
10. Hitchcock-DeGregori, S.E. 1994. Structural requirements of tropomyosin for binding to filamentous actin. In Actin: Biophysics, Biochemistry and Cell Biology. J.E. Estes, and P.J. Higgins, editors. Plenum Press, NY. 85-96.
11. Imanaka-Yoshida, K., J.M. Sanger, and J.W. Sanger. 1993. Contractile protein dynamics of myofibrils in paired adult rat cardiomyocytes. Cell Motil. Cytoskelet. 26:301-312.
12. Jacobson, S.L. 1977. Culture of spontaneously contracting myocardial cells from adult rats. Cell Struct. Funct. 2:1-9.
13. James, J., and J. Robbins. 1997. Molecular remodeling of contractile function. Am. J. Physiol. 273:H2105-H2118.
14. Kreuz, A.J., A. Simcox, and D. Maughan. 1996. Alterations in flight muscle ultrastructure and function in Drosophila tropomyosin mutants. J. Cell Biol. 135:673-687.
15. Lemanski, L.F., M.S. Mooseker, L.D. Peachey, and M.R. Iyengar. 1976. Studies of muscle proteins in embryonic myocardial cells of cardiac lethal mutant Mexican axolotls by use of heavy meromyosin binding and sodium dodecyl sulfate polyacrylamide gel electrophoresis. J. Cell Biol. 68:375-388.
16. Liu, H., and A. Bretscher. 1989. Disruption of a single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton. Cell. 57:233-242.
17. LoRusso, S.M., K. Imanaka-Yoshida, H. Shuman, J.M. Sanger, and J.W. Sanger. 1992. Incorporation of fluorescently labeled contractile proteins into freshly isolated living adult cardiac myocytes. Cell Motil. Cytoskelet. 21:111-122.
18. LoRusso, S.M., D. Rhee, J.M. Sanger, and J.W. Sanger. 1997. Premyofibrils in spreading adult cardiomyocytes in tissue culture: Evidence for reexpression of the embryonic program for myofibrillogenesis in adult cells. Cell Motil. Cytoskelet. 37:183-198.
19. Martin, A.F. 1981. Turnover of cardiac troponin subunits. J. Biol. Chem. 236: 964-968.
20. MacLeod, A.R., and C. Gooding. 1988. Human hTmα gene: expression in muscle and nonmuscle tissue. Mol. Cell. Biol. 8:433-440.
21. Messerli, J.M., M.E. Eppenberger-Eberhardt, B.M. Rutishauser, P. Schwarb, P. von Arx, S.K. Koch-Schneidemann, H.M. Eppenberger, and J.C. Perriard. 1993. Remodelling of the cardiomyocyte architecture visualized by three-dimensional confocal microscopy. Histochemistry. 100:193-202.
22. Metzger, J.M., M.S. Parmacek, E. Barr, K. Pasyk, W.-I. Lin, K.L. Cochrane, L.J. Field, and J.M. Leiden. 1993. Skeletal troponin C reduces contractile sensitivity to acidosis in adult cardiac myocytes from transgenic mice. Proc. Natl. Acad. Sci. USA. 90:9036-9040.
23. Molloy, J., A. Kreuz, R. Miller, T. Tansey, and D. Maughan. 1992. Effects of tropomyosin deficiency in flight muscle of Drosophila melanogaster. In Mechanism of Myofilament Sliding in Muscle. H. Sugi, and G. Pollack, editors. Plenum Press, New York. 165-172.
24. Morkin, E. 1970. Postnatal muscle fiber assembly: localization of newly synthesized myofibrillar proteins. Science. 167:1499-1501.
25. Moses, R.L., and W.C. Claycomb. 1982a. Culture of terminally and differentiated adult cardiac cells in culture. Am. J. Anat. 164:113-131.
26. Moses, R.L., and W.C. Claycomb. 1982b. Disorganization and reestablishment of cardiac cell ultrastructure in adult rat ventricular muscle cells. J. Ultrastruct. Res. 81:358-374.
27. 2+ regulation of mechanical properties of striated muscle: mechanistic studies using extraction and replacement of regulatory proteins. Circ. Res. 70:865-884.
28. Murphy, A.M., L. Jones II, H.F. Sims, and A.W. Strauss. 1991. Molecular cloning of rat cardiac troponin I and analysis of troponin I isoform expression in developing rat heart. Biochemistry. 30:707-712.
29. Muthuchamy, M., I.L. Grupp, G. Grupp, B.A. O'Toole, A.B. Kier, G.P. Boivin, J. Neumann, and D.F. Wieczorek. 1995. Molecular and physiological effects of overexpressing striated muscle β-tropomyosin in the murine adult heart. J. Biol. Chem. 270:30593-30603.
30. Puszkin, S., E. Puszkin, J. Maimon, C. Roualt, W. Schook, C. Ores, S. Kochwa, and R. Rosenfield. 1977. α-Actinin and tropomyosin interactions with a hybrid complex of erythrocyte actin and muscle myosin. J. Biol. Chem. 252: 5529-5537.
31. Rethinasamy, P., M. Muthuchamy, T. Hewett, G. Boivin, B.M. Wolska, C. Evans, R.J. Solaro, and D.F. Wieczorek. 1998. Molecular and physiological effects of α-tropomyosin ablation in the mouse. Circ. Res. 82:116-123.
32. Rhee, D., J.M. Sanger, and J.W. Sanger. 1994. The premyofibril: evidence for its role in myofibrillogenesis. Cell. Motil. Cytoskelet. 28:1-24.
33. 2+ activated tension in adenovirus infected adult cardiac myocytes. J. Mol. Cell. Biochem. 181:143-155.
34. Sanger, J.W., B. Mittal, and J.M. Sanger. 1984. Analysis of myofibrillar structure and assembly using fluorescently labeled contractile proteins. J. Cell Biol. 98:825-833.
35. Sanger, J.M., B. Mittal, M. Pochapin, and J.W. Sanger. 1986. Observations of microfilament bundles in living cells microinjected with fluorescently labelled contractile proteins. J. Cell Sci. Suppl. 5:17-44.
36. Schiaffino, S., and C. Reggiani. 1996. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol. Rev. 76:371-423.
37. Soldati, T., and J.-C. Perriard. 1991. Intracompartmental sorting of essential myosin light chains: molecular dissection and in vivo monitoring by epitope tagging. Cell. 66:277-289.
38. Tobacman, L.S. 1996. Thin filament-mediated regulation of cardiac contraction. Annu. Rev. Physiol. 58:447-481.
39. Trombitás, K., P.H.W W. Baatesen, J.J.-C. Lin, L.F. Lemanski, and G.H. Pollack. 1990. Immunoelectron microscopic observations of tropomyosin localization in striated muscle. J. Musc. Res. Cell Motil. 11:445-452.
40. von Arx, P., S. Bantle, T. Soldati, and J.C. Perriard. 1995. Dominant negative effect of cytoplasmic actin isoproteins on cardiomyocyte cytoarchitecture and function. J. Cell Biol. 131:1759-1773.
41. Wang, S.-M. M.L. Greaser, E. Schultz, J.C. Bulinski, J.J.-C. Lin, and J.L. Lessard. 1988. Studies on cardiac myofibrillogenesis with antibodies to titin, actin, tropomyosin and myosin. J. Cell Biol. 107:1075-1083.
42. Westfall, M.V., E.M. Rust, and J.M. Metzger. 1997. Slow skeletal troponin I gene transfer, expression and myofilament incorporation enhances adult cardiac myocyte function. 1997. Proc. Natl. Acad. Sci. USA. 94:5444-5449.
43. Westfall, M.V., E.M. Rust, F. Albayya, and J.M. Metzger. 1998. Adenovirus-mediated myofilament gene transfer into adult cardiac myocytes. Methods Cell. Biol. 52:307-322.