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. 1968 Sep 1;38(3):538–555. doi: 10.1083/jcb.38.3.538

MITOSIS AND INTERMEDIATE-SIZED FILAMENTS IN DEVELOPING SKELETAL MUSCLE

H Ishikawa 1, R Bischoff 1, H Holtzer 1
PMCID: PMC2108373  PMID: 5664223

Abstract

A new class of filaments intermediate in diameter between actin and myosin filaments has been demonstrated in skeletal muscle cells cultured from chick embryos. These filaments, which account for the majority of free filaments, average 100 A in diameter. They may run for more than 2 µ in a single section and can be distinguished in size and appearance from the thick and thin filaments assembled into myofibrils. The 100-A filaments are seen scattered throughout the sarcoplasm at all stages of development and show no obvious association with the myofibrils. The 100-A filaments are particularly conspicuous in myotubes fragmented by the mitotic inhibitors, colchicine and Colcemid. In addition, filaments similar in size and appearance to those found in myotubes are present in fibroblasts, chondrocytes, and proliferating mononucleated myoblasts. The 100-A filaments are present in cells arrested in metaphase by mitotic inhibitors. Definitive thick (about 150 A) or thin (about 60 A) myofilaments are not found in skeletal myogenic cells arrested in metaphase. Myogenic cells arrested in metaphase do not bind fluorescein-labeled antibody directed against myosin or actin. For these reasons, it is concluded that not all "thin" filaments in myogenic cells are uniquely associated with myogenesis.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ALLEN E. R., PEPE F. A. ULTRASTRUCTURE OF DEVELOPING MUSCLE CELLS IN THE CHICK EMBRYO. Am J Anat. 1965 Jan;116:115–147. doi: 10.1002/aja.1001160107. [DOI] [PubMed] [Google Scholar]
  2. Abbott J., Holtzer H. The loss of phenotypic traits by differentiated cells, V. The effect of 5-bromodeoxyuridine on cloned chondrocytes. Proc Natl Acad Sci U S A. 1968 Apr;59(4):1144–1151. doi: 10.1073/pnas.59.4.1144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Biberfeld P., Ericsson J. L., Perlmann P., Raftell M. Increased occurrence of cytoplasmic filaments in in vitro propagated rat liver epithelial cells. Exp Cell Res. 1965 Aug;39(1):301–305. doi: 10.1016/0014-4827(65)90034-0. [DOI] [PubMed] [Google Scholar]
  4. Bischoff R., Holtzer H. The effect of mitotic inhibitors in myogenesis in vitro. J Cell Biol. 1968 Jan;36(1):111–127. [PMC free article] [PubMed] [Google Scholar]
  5. Brinkley B. R., Stubblefield E., Hsu T. C. The effects of colcemid inhibition and reversal on the fine structure of the mitotic apparatus of Chinese hamster cells in vitro. J Ultrastruct Res. 1967 Jul;19(1):1–18. doi: 10.1016/s0022-5320(67)80057-1. [DOI] [PubMed] [Google Scholar]
  6. Buckley I. K., Porter K. R. Cytoplasmic fibrils in living cultured cells. A light and electron microscope study. Protoplasma. 1967;64(4):349–380. doi: 10.1007/BF01666538. [DOI] [PubMed] [Google Scholar]
  7. DE PETRIS S., KARLSBAD G., PERNIS B. Filamentous structures in the cytoplasm of normal mononuclear phagocytes. J Ultrastruct Res. 1962 Aug;7:39–55. doi: 10.1016/s0022-5320(62)80025-2. [DOI] [PubMed] [Google Scholar]
  8. Ezerman E. B., Ishikawa H. Differentiation of the sarcoplasmic reticulum and T system in developing chick skeletal muscle in vitro. J Cell Biol. 1967 Nov 1;35(2):405–420. doi: 10.1083/jcb.35.2.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Firket H. Ultrastructural aspects of myofibrils formation in cultured skeletal muscle. Z Zellforsch Mikrosk Anat. 1967;78(3):313–327. doi: 10.1007/BF00325316. [DOI] [PubMed] [Google Scholar]
  10. Fischman D. A. An electron microscope study of myofibril formation in embryonic chick skeletal muscle. J Cell Biol. 1967 Mar;32(3):557–575. doi: 10.1083/jcb.32.3.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. GODMAN G. C. The effect of colchicine on striated muscle in tissue culture. Exp Cell Res. 1955 Jun;8(3):488–499. doi: 10.1016/0014-4827(55)90125-7. [DOI] [PubMed] [Google Scholar]
  12. HANSON J., HUXLEY H. E. Quantitative studies on the structure of cross-striated myofibrils. II. Investigations by biochemical techniques. Biochim Biophys Acta. 1957 Feb;23(2):250–260. doi: 10.1016/0006-3002(57)90326-8. [DOI] [PubMed] [Google Scholar]
  13. HAY E. D. The fine structure of differentiating muscle in the salamander tail. Z Zellforsch Mikrosk Anat. 1963;59:6–34. doi: 10.1007/BF00321005. [DOI] [PubMed] [Google Scholar]
  14. HOLTZER H., MARSHALL J. M., Jr, FINCK H. An analysis of myogenesis by the use of fluorescent antimyosin. J Biophys Biochem Cytol. 1957 Sep 25;3(5):705–724. doi: 10.1083/jcb.3.5.705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. ISHIKAWA H. THE FINE STRUCTURE OF MYO-TENDON JUNCTION IN SOME MAMMALIAN SKELETAL MUSCLES. Arch Histol Jpn. 1965 Feb;25:275–296. doi: 10.1679/aohc1950.25.275. [DOI] [PubMed] [Google Scholar]
  16. Inoué S., Sato H. Cell motility by labile association of molecules. The nature of mitotic spindle fibers and their role in chromosome movement. J Gen Physiol. 1967 Jul;50(6 Suppl):259–292. [PMC free article] [PubMed] [Google Scholar]
  17. Ishikawa H. Formation of elaborate networks of T-system tubules in cultured skeletal muscle with special reference to the T-system formation. J Cell Biol. 1968 Jul;38(1):51–66. doi: 10.1083/jcb.38.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Manasek F. J. Mitosis in developing cardiac muscle. J Cell Biol. 1968 Apr;37(1):191–196. doi: 10.1083/jcb.37.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nagai R., Rebhun L. I. Cytoplasmic microfilaments in streaming Nitella cells. J Ultrastruct Res. 1966 Mar;14(5):571–589. doi: 10.1016/s0022-5320(66)80083-7. [DOI] [PubMed] [Google Scholar]
  20. O'Brien T. P., Thimann K. V. Intracellular fibers in oat coleoptile cells and their possible significance in cytoplasmic streaming. Proc Natl Acad Sci U S A. 1966 Sep;56(3):888–894. doi: 10.1073/pnas.56.3.888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Obinata T., Yamamoto M., Maruyama K. The identification of randomly formed thin filaments in differentiating muscle cells of the chick embryo. Dev Biol. 1966 Oct;14(2):192–213. doi: 10.1016/0012-1606(66)90013-3. [DOI] [PubMed] [Google Scholar]
  22. Okazaki K., Holtzer H. An analysis of myogenesis in vitro using fluorescein-labeled antimyosin. J Histochem Cytochem. 1965 Nov-Dec;13(8):726–739. doi: 10.1177/13.8.726. [DOI] [PubMed] [Google Scholar]
  23. Okazaki K., Holtzer H. Myogenesis: fusion, myosin synthesis, and the mitotic cycle. Proc Natl Acad Sci U S A. 1966 Nov;56(5):1484–1490. doi: 10.1073/pnas.56.5.1484. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. PREER J. R., Jr A quantitative study of a technique of double diffusion in agar. J Immunol. 1956 Jul;77(1):52–60. [PubMed] [Google Scholar]
  25. PRICE H. M., HOWES E. L., Jr, BLUMBERG J. M. ULTRASTRUCTURAL ALTERATIONS IN SKELETAL MUSCLE FIBERS INJURED BY COLD. II. CELLS ON THE SARCOLEMMAL TUBE: OBSERVATIONS ON "DISCONTINUOUS" REGENERATION AND MYOFIBRIL FORMATION. Lab Invest. 1964 Oct;13:1279–1302. [PubMed] [Google Scholar]
  26. Przybylski R. J., Blumberg J. M. Ultrastructural aspects of myogenesis in the chick. Lab Invest. 1966 May;15(5):836–863. [PubMed] [Google Scholar]
  27. ROBBINS E., GONATAS N. K. HISTOCHEMICAL AND ULTRASTRUCTURAL STUDIES ON HELA CELL CULTURES EXPOSED TO SPINDLE INHIBITORS WITH SPECIAL REFERENCE TO THE INTERPHASE CELL. J Histochem Cytochem. 1964 Sep;12:704–711. doi: 10.1177/12.9.704. [DOI] [PubMed] [Google Scholar]
  28. STOCKDALE F. E., HOLTZER H. DNA synthesis and myogenesis. Exp Cell Res. 1961 Sep;24:508–520. doi: 10.1016/0014-4827(61)90450-5. [DOI] [PubMed] [Google Scholar]
  29. STOCKDALE F., OKAZAKI K., NAMEROFF M., HOLTZER H. 5-BROMODEOXYURIDINE: EFFECT ON MYOGENESIS IN VITRO. Science. 1964 Oct 23;146(3643):533–535. doi: 10.1126/science.146.3643.533. [DOI] [PubMed] [Google Scholar]
  30. STREHLER B. L., KONIGSBERG I. R., KELLEY J. E. PLOIDY OF MYOTUBE NUCLEI DEVELOPING IN VITRO AS DETERMINED WITH A RECORDING DOUBLE BEAM MICRO-SPECTROPHOTOMETER. Exp Cell Res. 1963 Nov;32:232–241. doi: 10.1016/0014-4827(63)90098-3. [DOI] [PubMed] [Google Scholar]
  31. SZENT-GYORGYI A. G. A new method for the preparation of actin. J Biol Chem. 1951 Sep;192(1):361–369. [PubMed] [Google Scholar]
  32. Shafiq S. A., Gorycki M. A., Milhorat A. T. An electron microscopic study of regeneration and satellite cells in human muscle. Neurology. 1967 Jun;17(6):567–passim. doi: 10.1212/wnl.17.6.567. [DOI] [PubMed] [Google Scholar]
  33. TANAKA Y. FIBRILLAR STRUCTURES IN THE CELLS OF BLOODFORMING ORGANS. J Natl Cancer Inst. 1964 Sep;33:467–485. [PubMed] [Google Scholar]
  34. Taylor A. C. Microtubules in the microspikes and cortical cytoplasm of isolated cells. J Cell Biol. 1966 Feb;28(2):155–168. doi: 10.1083/jcb.28.2.155. [DOI] [PMC free article] [PubMed] [Google Scholar]

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