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The pattern of organization of intermediate filaments and their asymmetrical association with dense bodies in smooth muscle of an ascidian Halocynthia roretzi

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Summary

An extensive network of intermediate filaments that interconnected cytoplasmic dense bodies and connected the dense bodies to the cell surface was revealed in double-fixed, tannic acid-stained preparations of ascidian smooth muscle. The filament network ran through spaces in the continuous network of myofibrils, connecting them longitudinally, obliquely and transversely to form an intimately associated, dual network. In their transverse passage, the intermediate filaments ran across myofibrils along I-zones exclusively, interconnecting successive dense bodies.

The pattern of attachment of intermediate filaments to dense bodies was predominantly “one-sided.” The filaments, which themselves were not incorporated into the contractile apparatus, remained folded or unfolded between myofibrils and between sarcomere-like structures in synchrony with the contraction-relaxation cycles.

These results suggest that the intermediate filaments mechanically maintain the organization and arrangement of myofibrils via an intimate association with the myofibrils in the regions of the dense bodies, in such a way that the filaments do not impede muscle function.

Based on these observations, a new model for the network of intermediate filaments in smooth muscle cells is proposed.

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References

  • Ashton FT, Somlyo AV, Somlyo AP (1975) The contractile apparatus of vascular smooth muscle: intermediate high voltage stereo electron microscopy. J Mol Biol 98:17–29

    Google Scholar 

  • Bond M, Somlyo AV (1982) Dense bodies and actin polarity in vertebrate smooth muscle. J Cell Biol 95:403–413

    Google Scholar 

  • Campbell GR, Uehara Y, Mark G, Burnstock G (1971) Fine structure of smooth muscle cells grown in tissue culture. J Cell Biol 49:21–34

    Google Scholar 

  • Campbell GR, Chamley-Campbell J, Gröschel-Stewart U, Small JV, Anderson P (1979) Antibody staining of 10-nm (100-Å) filaments in cultured smooth, cardiac and skeletal muscle cells. J Cell Sci 37:303–322

    Google Scholar 

  • Chlebowski JS, Przybylski RJ, Cox PG (1973) Ultrastructural studies of lizard (Anolis carolinensis) myogenesis in vitro. Dev Biol 33:80–99

    Google Scholar 

  • Cooke P (1976) A filamentous cytoskeleton in vertebrate smooth muscle fibers. J Cell Biol 68:539–556

    Google Scholar 

  • Cooke PH, Chase RH (1971) Potassium chloride-insoluble myofilaments in vertebrate smooth muscle cells. Exp Cell Res 66:417–425

    Google Scholar 

  • Cooke PH, Fay FS (1972) Correlation between fiber length, ultrastructure, and the length-tension relationship of mammalian smooth muscle. J Cell Biol 52:105–116

    Google Scholar 

  • Endo T, Masaki T (1984) Differential expression and distribution of chicken skeletal- and smooth-muscle type α-actinins during myogenesis in culture. J Cell Biol 99:2322–2332

    Google Scholar 

  • Fay FS, Fujiwara K, Rees DD, Fogarty KE (1983) Distribution of α-actinin in single isolated smooth muscle cells. J Cell Biol 96:783–795

    Google Scholar 

  • Forbes MS, Sperelakis N (1980) Structures located at the level of the Z bands in mouse ventricular myocardial cells. Tissue Cell 12:467–489

    Google Scholar 

  • Franke WW, Schmid E, Schiller DL, Winter S, Jarasch ED, Moll R, Denk H, Jackson BW, Illmensee K (1982) Differentiationrelated patterns of expression of proteins of intermediate-size filaments in tissues and cultured cells. Cold Spring Harbor Symp Quant Biol 46:431–453

    Google Scholar 

  • Fujimaki N, Kano Y, Ishikawa H (1986) The association of intermediate filaments with the sarcolemma in skeletal muscle fibers. J Electron Microsc 35 [Suppl] 3:2657–2658

    Google Scholar 

  • Gard DL, Lazarides E (1980) The synthesis and distribution of desmin and vimentin during myogenesis in vitro. Cell 19:263–275

    Google Scholar 

  • Geiger B, Dutton AH, Tokuyasu KT, Singer SJ (1981) Immunoelectron microscope studies of membrane-microfilament interactions: distribution of α-actinin, tropomyosin, and vinculin in intestinal epithelial brush border and chicken gizzard smooth muscle cells. J Cell Biol 91:614–628

    Google Scholar 

  • Gross WO (1977) Z-line elementary bodies. Morphological study of sarcomere genesis in chick heart myocytes. J Submicrosc Cytol 9:285–298

    Google Scholar 

  • Holtzer H, Bennett GS, Tapscott SJ, Croop JM, Toyama Y (1982) Intermediate-size filaments: changes in synthesis and distribution in cells of the myogenic and neurogenic lineages. Cold Spring Harbor Symp Quant Biol 46:317–329

    Google Scholar 

  • Ishikawa H (1983) Fine structure of skeletal muscle. In: Dowben RM, Shay JW (eds) Cell and Muscle Motility Vol 4. Plenum Press, New York, pp 1–84

    Google Scholar 

  • Ishikawa H, Bischoff R, Holtzer H (1968) Mitosis and intermediate-sized filaments in developing skeletal muscle. J Cell Biol 38:538–555

    Google Scholar 

  • Kelly DE (1969) Myofibrillogenesis and Z band differentiation. Anat Rec 163:403–426

    Google Scholar 

  • Kilarski W, Kozłowska M (1979) Myofibrillogenesis of the lateral musculature in the trout (Salmo trutta L.). Dev Growth Differ 21:349–360

    Google Scholar 

  • Lazarides E (1980) Intermediate filaments as mechanical integrators of cellular space. Nature 283:249–256

    Google Scholar 

  • Lazarides E (1982) Intermediate filaments: a chemically heterogeneous, developmentally regulated class of proteins. Annu Rev Biochem 51:219–250

    Google Scholar 

  • Lazarides E, Granger BL, Gard DL, O'Conner CM, Breckler J, Price M, Danto SL (1982) Desmin- and vimentin-containing filaments and their role in the assembly of the Z disk in muscle cells. Cold Spring Harbor Symp Quant Biol 46:351–378

    Google Scholar 

  • Lemanski LF (1973) Heart development in the Mexican salamander, Ambystoma mexicanum II. Ultrastructure. Am J Anat 136:487–526

    Google Scholar 

  • Manasek FJ (1968) Embryonic development of the heart I. A light and electron microscopic study of myocardial development in the early chick embryo. J Morphol 125:329–366

    Google Scholar 

  • Nunzi MG, Franzini-Armstrong C (1980) Trabecular network in adult skeletal muscle. J Ultrastruct Res 73:21–26

    Google Scholar 

  • Osborn M, Geisler N, Shaw G, Sharp G, Weber K (1982) Intermediate filaments. Cold Spring Harbor Symp Quant Biol 46:413–429

    Google Scholar 

  • Peng HB, Wolosewick JJ, Cheng P-C (1981) The development of myofibrils in cultured muscle cells: a whole-mount and thin section electron microscopic study. Dev Biol 88:121–136

    Google Scholar 

  • Price M, Sanger JW (1979) Intermediate filaments connect Z-discs in adult chicken muscle. J Exp Zool 208:263–269

    Google Scholar 

  • Price MG, Sanger JW (1983) Intermediate filaments in striated muscle: a review of structural studies in embryonic and adult skeletal muscle. In: Dowben RM, Shay JM (eds) Cell and Muscle Motility Vol 3. Plenum Press, New York, pp 1–40

    Google Scholar 

  • Rönnau K (1977) Myogenesis and contraction in the early embryonic heart of the rainbow-trout. An electron microscopic study. Cell Tissue Res 180:123–132

    PubMed  Google Scholar 

  • Sanger JM, Mittal B, Pochapin MB, Sanger JW (1986) Myofibrillogenesis in living cells microinjected with fluorescently labeled alpha-actinin. J Cell Biol 102:2053–2066

    Google Scholar 

  • Shimada Y, Isobe Y (1986) Cytoskeletal organization in embryonic chick skeletal muscle cells in vitro revealed by the detergent-extraction, freeze-dry methods. In: Emerson C, Fischman DA, Nadal-Ginard B, Siddiqui MAQ (eds) Molecular Biology of Muscle Development. UCLA symposia on molecular and cellular biology. New series. Vol 29. Alan R Liss Inc, New York, pp 725–739

    Google Scholar 

  • Small JV (1974) Contractile units in vertebrate smooth muscle cells. Nature 249:324–327

    Google Scholar 

  • Small JV (1977) Studies on isolated smooth muscle cells: the contractile apparatus. J Cell Sci 24:327–349

    Google Scholar 

  • Small JV (1985) Geometry of actin-membrane attachments in the smooth muscle cell: the localizations of vinculin and α-actinin. EMBO J 4:45–49

    Google Scholar 

  • Small JV, Sobieszek A (1977) Studies on the function and composition of the 10-nm (100-Å) filaments of vertebrate smooth muscle. J Cell Sci 23:243–268

    Google Scholar 

  • Terakado K (1972) Cytological and ultrastructural studies on muscle differentiation in the ascidian, Perophora orientalis. Dev Growth Differ 14:1–23

    Google Scholar 

  • Terakado K (1973) The effects of actinomycin D on muscle cells of ascidian embryo. Dev Growth Differ 15:179–192

    Google Scholar 

  • Terakado K, Obinata T (1987) Structure of multinucleated smooth muscle cells of the ascidian Halocynthia roretzi. Cell Tissue Res 247:85–94

    Google Scholar 

  • Tokuyasu KT, Maher PA, Singer ST (1984) Distributions of vimentin and desmin in developing chick myotubes in vivo. I. Immunofluorescence study. J Cell Biol 98:1961–1972

    Google Scholar 

  • Tsukita S, Tsukita S, Ishikawa H (1983) Association of actin and 10 nm filaments with the dense body in smooth muscle cells of the chicken gizzard. Cell Tissue Res 229:233–242

    Google Scholar 

  • Uehara Y, Campbell GR, Burnstock G (1971) Cytoplasmic filaments in developing and adult vertebrate smooth muscle. J Cell Biol 50:484–497

    Google Scholar 

  • Wang K, Ramirez-Mitchell R (1983) A network of transverse and longitudinal intermediate filaments is associated with sarcomeres of adult vertebrate skeletal muscle. J Cell Biol 96:562–570

    Google Scholar 

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  1. Department of Regulation Biology, Faculty of Science, Saitama University, Urawa, Japan

    K. Terakado

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Terakado, K. The pattern of organization of intermediate filaments and their asymmetrical association with dense bodies in smooth muscle of an ascidian Halocynthia roretzi . Cell Tissue Res. 252, 23–32 (1988). https://doi.org/10.1007/BF00213822

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  • DOI: https://doi.org/10.1007/BF00213822

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