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Journal of Biomedicine and Biotechnology
Volume 2010, Article ID 858606, 8 pages
http://dx.doi.org/10.1155/2010/858606
Review Article

Assembly and Dynamics of Myofibrils

Joseph W. Sanger, Jushuo Wang, Yingli Fan, Jennifer White, and Jean M. Sanger

Department of Cell and Developmental Biology, SUNY Upstate Medical University, Syracuse, NY 13210, USA

Received 31 December 2009; Accepted 15 March 2010

Academic Editor: Aikaterini Kontrogianni-Konstantopoulos

Copyright © 2010 Joseph W. Sanger et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. M. Chapman, C. F. A. Pantin, and E. A. Robson, “Muscle in coelenterates,” Revue Canadienne de Biologie, vol. 21, pp. 267–278, 1962. View at Google Scholar
  2. J. del Castillo, M. Anderson, and D. S. Smith, “Proventriculus of a marine annelid: muscle preparation with the longest recorded sarcomere,” Proceedings of the National Academy of Sciences of the United States of America, vol. 69, no. 7, pp. 1669–1672, 1972. View at Google Scholar · View at Scopus
  3. H. E. Huxley, “Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle,” Journal of Molecular Biology, vol. 7, pp. 281–308, 1963. View at Google Scholar
  4. T. F. Robertson and S. Winegrad, “Variation of thin filament length in heart muscle,” Nature, vol. 267, pp. 74–75, 1977. View at Google Scholar
  5. A. Du, J. M. Sanger, K. K. Linask, and J. W. Sanger, “Myofibrillogenesis in the first cardiomyocytes formed from isolated quail precardiac mesoderm,” Developmental Biology, vol. 257, no. 2, pp. 382–394, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. J. W. Sanger, J. M. Sanger, and C. Franzini-Armstrong, “Assembly of the skeletal muscle cell,” in Myology, A. G. Engel and C. Franzini-Armstrong, Eds., pp. 45–65, McGraw-Hill, New York, NY, USA, 3rd edition, 2004. View at Google Scholar
  7. J. W. Sanger, S. Kang, C. C. Siebrands et al., “How to build a myofibril,” Journal of Muscle Research and Cell Motility, vol. 26, no. 6–8, pp. 343–354, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. A. L. Stout, J. Wang, J. M. Sanger, and J. W. Sanger, “Tracking changes in Z-band organization during myofibrillogenesis with FRET imaging,” Cell Motility and the Cytoskeleton, vol. 65, no. 5, pp. 353–367, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Morimoto, “Sarcomeric proteins and inherited cardiomyocytes,” Cardiovascular Research, vol. 77, pp. 659–666, 2008. View at Google Scholar
  10. D. W. Piston and G.-J. Kremers, “Fluorescent protein FRET: the good, the bad and the ugly,” Trends in Biochemical Sciences, vol. 32, no. 9, pp. 407–414, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. K. A. Clark, A. S. McElhinny, M. C. Beckerle, and C. C. Gregorio, “Striated muscle cytoarchitecture: an intricate web of form and function,” Annual Review of Cell and Developmental Biology, vol. 18, pp. 637–706, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. J. M. Sanger and J. W. Sanger, “The dynamic Z bands of striated muscle cells,” Science Signaling, vol. 1, no. 32, article pe37, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Y. Boateng and P. H. Goldspink, “Assembly and maintenance of the sarcomere night and day,” Cardiovascular Research, vol. 77, no. 4, pp. 667–675, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. B. A. Danowski, K. Imanaka-Yoshida, J. M. Sanger, and J. W. Sanger, “Costameres are sites of force transmission to the substratum in adult rat cardiomyocytes,” Journal of Cell Biology, vol. 118, no. 6, pp. 1411–1420, 1992. View at Google Scholar · View at Scopus
  15. J. M. Ervasti, “Costameres: the Achilles' heel of Herculean muscle,” Journal of Biological Chemistry, vol. 278, no. 16, pp. 13591–13594, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. D. Frank, C. Kuhn, H. A. Katus, and N. Frey, “The sarcomeric Z-disc: a nodal point in signaling and disease,” Journal of Molecular Medicine, vol. 84, pp. 446–468, 2006. View at Google Scholar
  17. S. Lange, E. Ehler, and M. Gautel, “From A to Z and back? Multicompartment proteins in the sarcomere,” Trends in Cell Biology, vol. 16, no. 1, pp. 11–18, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. A. G. Engel and B. Q. Banker, “Ultrastructural changes in diseased muscle,” in Myology, A. G. Engel and C. Franzini-Armstrong, Eds., pp. 749–887, McGraw-Hill, New York, NY, USA, 3rd edition, 2004. View at Google Scholar
  19. M. Heidenhain, “Uber die Entstehung der quergestreiften Muskelsubstanz bei der Forelle,” Archiv Mikroskopische Anatomie EntivMech, vol. 83, pp. 427–522, 1913. View at Google Scholar
  20. J. Auber, “La myofibrillogenese du muscle stile. I. lnsectes,” Journal of Microscopy, vol. 8, pp. 197–232, 1969. View at Google Scholar
  21. J. Aronson, “Sarcomere size in developing muscles of a tarsonemid mite,” The Journal of Biophysical and Biochemical Cytology, vol. 11, pp. 147–156, 1961. View at Google Scholar · View at Scopus
  22. E. Lazarides and K. Weber, “Actin antibody: the specific visualization of actin filaments in nonmuscle cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 71, pp. 2268–2271, 1974. View at Google Scholar
  23. J. W. Sanger, “Changing patterns of actin localization during cell division,” Proceedings of the National Academy of Sciences of the United States of America, vol. 72, no. 5, pp. 1913–1916, 1975. View at Google Scholar · View at Scopus
  24. E. Lazarides and K. Burridge, “Alpha-actinin: immunofluorescent localization of a muscle structural protein in non-muscle cells,” Cell, vol. 6, pp. 289–299, 1975. View at Google Scholar
  25. K. Weber and U. Groeschel-Stewart, “Antibody to myosin: the specific visualization of myosin containing filaments in nonmuscle cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 71, no. 11, pp. 4561–4564, 1974. View at Google Scholar · View at Scopus
  26. J. W. Sanger, J. M. Sanger, and B. M. Jockusch, “Differences in the stress fibers between fibrblasts and epithelial cells,” Journal of Cell Biology, vol. 96, no. 4, pp. 961–969, 1983. View at Google Scholar · View at Scopus
  27. B. Mittal, J. M. Sanger, and J. W. Sanger, “Visualization of myosin in living cells,” Journal of Cell Biology, vol. 105, no. 4, pp. 1753–1760, 1987. View at Google Scholar · View at Scopus
  28. B. Mittal, J. M. Sanger, and J. W. Sanger, “Binding and distribution of fluorescently labeled filamin in permeabilized and living cells,” Cell Motility and the Cytoskeleton, vol. 8, no. 4, pp. 345–359, 1987. View at Google Scholar · View at Scopus
  29. R. R. Kulikowski and F. J. Manasek, “Myosin localization in cultured embryonic cardiac myocytes,” in Motility in Cell Function, F. A. Pepe, J. W. Sanger, and V. T. Nachmias, Eds., pp. 433–435, Academic Press, New York, NY, USA, 1979. View at Google Scholar
  30. J. R. Fallon and V. T. Nachmias, “Localization of cytoplasmic and skeletal myosins in developing muscle cells by double-label immunofluorescence,” Journal of Cell Biology, vol. 87, no. 1, pp. 237–247, 1980. View at Google Scholar · View at Scopus
  31. A. A. Dlugosz, P. B. Antin, V. T. Nachmias, and H. Holtzer, “The relationship between stress fiber-like structures and nascent myofibrils in cultured cardiac myocytes,” Journal of Cell Biology, vol. 99, no. 6, pp. 2268–2278, 1984. View at Google Scholar · View at Scopus
  32. A. Leal, S. Endele, C. Stengel et al., “A novel myosin heavy chain gene in human chromosome 19q13.3,” Gene, vol. 312, no. 1-2, pp. 165–171, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. E. Golomb, X. Ma, S. S. Jana et al., “Identification and characterization of nonmuscle myosin II-C, a new member of the myosin II family,” Journal of Biological Chemistry, vol. 279, no. 4, pp. 2800–2808, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. W. Lu, S. H. Seeholzer, M. Han et al., “Cellular nonmuscle myosins NMHC-IIA and NMHC-IIB and vertebrate heart looping,” Developmental Dynamics, vol. 237, no. 12, pp. 3577–3590, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. J. W. Sanger, B. Mittal, and J. M. Sanger, “Formation of myofibrils in spreading chick cardiac myocytes,” Cell Motility, vol. 4, no. 6, pp. 405–416, 1984. View at Google Scholar
  36. J. W. Sanger, B. Mittal, and J. M. Sanger, “Analysis of myofibrillar structure and assembly using fluorescently labeled contractile proteins,” Journal of Cell Biology, vol. 98, no. 3, pp. 825–833, 1984. View at Google Scholar · View at Scopus
  37. J. M. Sanger, B. Mittal, M. B. Pochapin, and J. W. Sanger, “Myofibrillogenesis in living cells microinjected with fluorescently labeled alpha-actinin,” Journal of Cell Biology, vol. 102, no. 6, pp. 2053–2066, 1986. View at Google Scholar · View at Scopus
  38. G. A. Dabiri, K. K. Turnacioglu, J. M. Sanger, and J. W. Sanger, “Myofibrillogenesis visualized in living embryonic cardiomyocytes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 17, pp. 9493–9498, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Rhee, J. M. Sanger, and J. W. Sanger, “The premyofibril: evidence for its role in myofibrillogenesis,” Cell Motility and the Cytoskeleton, vol. 28, no. 1, pp. 1–24, 1994. View at Google Scholar · View at Scopus
  40. A. Du, J. M. Sanger, and J. W. Sanger, “Cardiac myofibrillogenesis inside intact embryonic hearts,” Developmental Biology, vol. 318, no. 2, pp. 236–246, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. A. H. Conrad, W. A. Clark, and G. W. Conrad, “Subcellular compartmentalization of myosin isoforms in embryonic chick heart ventricle myocytes during cytokinesis,” Cell Motility and the Cytoskeleton, vol. 19, no. 3, pp. 189–206, 1991. View at Google Scholar · View at Scopus
  42. A. H. Conrad, T. Jaffredo, and G. W. Conrad, “Differential localization of cytoplasmic myosin II isoforms a and B in avian interphase and dividing embryonic and immortalized cardiomyocytes and other cell types in vitro,” Cell Motility and the Cytoskeleton, vol. 31, no. 2, pp. 93–112, 1995. View at Publisher · View at Google Scholar · View at Scopus
  43. M.-H. Lu, C. DiLullo, T. Schultheiss et al., “The vinculin/sarcomeric-a-actinin/a-actin nexus in cultured cardiac myocytes,” Journal of Cell Biology, vol. 117, no. 5, pp. 1007–1022, 1992. View at Publisher · View at Google Scholar · View at Scopus
  44. H. Holtzer, T. Hijikata, Z. X. Lin et al., “Independent assembly of 1.6?µm long bipolar MHC filaments and I-Z-I bodies,” Cell Structure and Function, vol. 22, no. 1, pp. 83–93, 1997. View at Google Scholar · View at Scopus
  45. S. M. Wang, M. L. Greaser, E. Schultz, J. C. Bulinski, J. J. Lin, and J. L. Lessard, “Studies on cardiac myofibrillogenesis with antibodies to titin, actin, tropomyosin, and myosin,” The Journal of Cell Biology, vol. 107, pp. 1075–1083, 1988. View at Google Scholar
  46. J. Wang, N. Shaner, B. Mittal et al., “Dynamics of Z-band based proteins in developing skeletal muscle cells,” Cell Motility and the Cytoskeleton, vol. 61, no. 1, pp. 34–48, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. J. M. Sanger, B. Mittal, A. Wegner, B. M. Jockusch, and J. W. Sanger, “Differential response of stress fibers and myofibrils to gelsolin,” European Journal of Cell Biology, vol. 43, no. 3, pp. 421–428, 1987. View at Google Scholar
  48. J. M. Sanger, G. Dabiri, B. Mittal, M. A. Kowalski, J. G. Haddad, and J. W. Sanger, “Disruption of microfilament organization in living non-muscle cells by microinjection of vitamin-D binding protein or DNaseI,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, pp. 5474–5478, 1990. View at Google Scholar
  49. J. Wang, J. M. Sanger, and J. W. Sanger, “Differential effects of Latrunculin-A on myofibrils in cultures of skeletal muscle cells: insights into mechanisms of myofibrillogenesis,” Cell Motility and the Cytoskeleton, vol. 62, no. 1, pp. 35–47, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. J. M. Sanger and J. W. Sanger, “Banding and polarity of actin filaments in interphase and cleaving cells,” Journal of Cell Biology, vol. 86, no. 2, pp. 568–575, 1980. View at Google Scholar · View at Scopus
  51. S. M. LoRusso, D. Rhee, J. M. Sanger, and J. W. Sanger, “Premyofibrils in spreading adult cardiomyocytes in tissue culture: evidence for reexpression of the embryonic program for myofibrillogenesis in adult cells,” Cell Motility and the Cytoskeleton, vol. 37, no. 3, pp. 183–198, 1997. View at Publisher · View at Google Scholar · View at Scopus
  52. J. M. Sanger, J. S. Dome, and J. W. Sanger, “Unusual cleavage furrows in vertebrate tissue culture cells: insights into the mechanisms of cytokinesis,” Cell Motility and the Cytoskeleton, vol. 39, no. 2, pp. 95–106, 1998. View at Publisher · View at Google Scholar · View at Scopus
  53. J. M. Sanger and J. W. Sanger, “Assembly of cytoskeletal proteins into cleavage furrows of tissue culture cells,” Microscopy Research and Technique, vol. 49, no. 2, pp. 190–201, 2000. View at Publisher · View at Google Scholar · View at Scopus
  54. J. W. Sanger and J. M. Sanger, “Green fluorescent proteins improve myofibril research,” Biophotonics International, vol. 8, no. 3, pp. 44–46, 2001. View at Google Scholar
  55. M. L. Golson, J. M. Sanger, and J. W. Sanger, “Inhibitors arrest myofibrillogenesis in skeletal muscle cells at early stages of assembly,” Cell Motility and the Cytoskeleton, vol. 59, no. 1, pp. 1–16, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. J. W. Sanger, J. Wang, B. Holloway, A. Du, and J. M. Sanger, “Myofibrillogenesis in skeletal muscle cells in zebrafish,” Cell Motility and the Cytoskeleton, vol. 66, no. 8, pp. 556–566, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. K. K. Turnacioglu, B. Mittal, G. A. Dabiri, J. M. Sanger, and J. W. Sanger, “Zeugmatin is part of the Z-band targeting region of titin,” Cell Structure and Function, vol. 22, no. 1, pp. 73–82, 1997. View at Google Scholar · View at Scopus
  58. K. K. Turnacioglu, B. Mittal, G. A. Dabiri, J. M. Sanger, and J. W. Sanger, “An N-terminal fragment of titin coupled to green fluorescent protein localizes to the Z-bands in living muscle cells: overexpression leads to myofibril disassembly,” Molecular Biology of the Cell, vol. 8, no. 4, pp. 705–717, 1997. View at Google Scholar · View at Scopus
  59. E. Ehler, B. M. Rothen, S. P. Hämmerle, M. Komiyama, and J.-C. Perriard, “Myofibrillogenesis in the developing chicken heart: assembly of Z-disk, M-line and the thick filaments,” Journal of Cell Science, vol. 112, no. 10, pp. 1529–1539, 1999. View at Google Scholar · View at Scopus
  60. P. F. M. Van der Ven, J. W. Bartsch, M. Gautel, H. Jockusch, and D. O. Fürst, “A functional knock-out of titin results in defective myofibril assembly,” Journal of Cell Science, vol. 113, no. 8, pp. 1405–1414, 2000. View at Google Scholar · View at Scopus
  61. M. Gotthardt, R. E. Hammer, N. Hübner et al., “Conditional expression of mutant M-line titins results in cardiomyopathy with altered sarcomere structure,” Journal of Biological Chemistry, vol. 278, no. 8, pp. 6059–6065, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Kontrogianni-Konstantopoulos, D. H. Catino, J. C. Strong, and R. J. Bloch, “De novo myofibrillogenesis in C2C12 cells: evidence for the independent assembly of M bands and Z disks,” American Journal of Physiology, vol. 290, no. 2, pp. C626–C637, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Lange, K. Ouyang, G. Meyer et al., “Obscurin determines the architecture of the longitudinal sarcoplasmic reticulum,” Journal of Cell Science, vol. 122, no. 15, pp. 2640–2650, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. A. N. Tullio, D. Accili, V. J. Ferrans et al., “Nonmuscle myosin II-B is required for normal development of the mouse heart,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 23, pp. 12407–12412, 1997. View at Publisher · View at Google Scholar · View at Scopus
  65. K. Takeda, Z.-X. Yu, S. Qian, T. K. Chin, R. S. Adelstein, and V. J. Ferrans, “Nonmuscle myosin II localizes to the Z-lines and intercalated discs of cardiac muscle and to the Z-lines of skeletal muscle,” Cell Motility and the Cytoskeleton, vol. 46, no. 1, pp. 59–68, 2000. View at Google Scholar · View at Scopus
  66. D. E. Rudy, T. A. Yatskievych, P. B. Antin, and C. C. Gregorio, “Assembly of thick, thin, and titin filaments in chick precardiac explants,” Developmental Dynamics, vol. 221, no. 1, pp. 61–71, 2001. View at Publisher · View at Google Scholar · View at Scopus
  67. N. M. McKenna, J. B. Meigs, and Y.-L. Wang, “Exchangeability of alpha-actinin in living cardiac fibroblasts and muscle cells,” Journal of Cell Biology, vol. 101, no. 6, pp. 2223–2232, 1985. View at Google Scholar · View at Scopus
  68. J. Wang, J. M. Sanger, S. Kang et al., “Ectopic expression and dynamics of TPM1a and TPM1? in myofibrils of avian myotubes,” Cell Motility and the Cytoskeleton, vol. 64, no. 10, pp. 767–776, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Wang, H. Thurston, E. Essandoh et al., “Tropomyosin expression and dynamics in developing avian embryonic muscles,” Cell Motility and the Cytoskeleton, vol. 65, no. 5, pp. 379–392, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Vink, M. Simonetta, P. Transidico et al., “In vitro FRAP identifies the minimal requirements for Mad2 kinetochore dynamics,” Current Biology, vol. 16, no. 8, pp. 755–766, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. L. Stryer, “Fluorescence energy transfer as a spectroscopic ruler,” Annual Review of Biochemistry, vol. 47, pp. 819–846, 1978. View at Google Scholar · View at Scopus
  72. K. R. Chi, “Microscopy: ever-increasing resolution,” Nature, vol. 462, no. 7273, pp. 675–678, 2009. View at Publisher · View at Google Scholar · View at Scopus