Summary
The intracellular distributions of major muscle proteins, myosin, actin, tropomyosin, α-actinin, and desmin, in smooth muscle cells of chicken gizzard at various stages of embryogenesis were investigated by immunofluorescence-labeling of enzyme-dispersed cells cultured up to three hours. These muscle proteins, except some part of myosin, were organized into fibrous structures as soon as synthesis and accumulation of proteins started. As for myosin, a considerable amount of it was dispersed in soluble cytoplasm as well. On the other hand, Ca++-dependent contractility was detected with detergent-extracted myoblasts and glycerinated tissue from embryos older than 7 days. Although the nascent myofibrils bear a resemblance to “stress fibers,” the former could be distinguished from the latter by their high stability in dispersed, spherical cells. The above findings, therefore, show that the synthesis of contractile proteins is followed by immediate assembly of them into functional myofibrils without undergoing any intermediate structure. Based on these findings, the mechanism of myofibril formation in developing smooth muscle cells is discussed.
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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
Bagby RM (1980) Double-immunofluorescent staining of isolated smooth muscle cells. Histochemistry 69:113–130
Bennett T, Cobb JLS (1969) Studies on the avian gizzard: The development of the gizzard and its innervation. Z Zellforsch 98:599–621
Bois RM (1973) The organization of the contractile apparatus of vertebrate smooth muscle. Anat Rec 177:61–78
Bond M, Somlyo AV (1982) Dense bodies and actin polarity in vertebrate smooth muscle. J Cell Biol 95:403–413
Bragina EE, Vasiliev JM, Gelfand IM (1976) Formation of bundles of microfilaments during spreading of fibroblasts on the substrate. Exp Cell Res 97:241–248
Campbell GR, Chamley JH, Burnstock G (1974) Development of smooth muscle cells in tissue culture. J Anat 117:295–312
Cande WZ, Tooth PJ, Kendrick-Jones J (1983) Regulation of contraction and thick filament assembly-disassembly in glycerinated vertebrate smooth muscle cells. J Cell Biol 97:1062–1071
Chamley JH, Campbell GR, Burnstock G (1974) Dedifferentiation redifferentiation and bundle formation of smooth muscle cells in tissue culture: The influence of cell number and nerve fibers. J Embryol Exp Morphol 32:297–323
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
Gard DL, Lazarides E (1980) The synthesis and distribution of desmin and vimentin during myogenesis in vitro. Cell 19:263–275
Goldman RD, Knipe DM (1972) Functions of cytoplasmic fibers in non-muscle cell motility. Cold Spring Harbor Symp Quant Biol 37:523–524
Gröschel-Stewart U, Chamley JH, Campbell GR, Burnstock G (1975) Changes in myosin distribution in dedifferentiating and redifferentiating smooth muscle cells in tissue culture. Cell Tissue Res 165:13–22
Heggeness MH, Wang K, Singer SJ (1977) Intracellular distributions of mechanochemical proteins in cultured fibroblasts. Proc Natl Acad Sci USA 74:3883–3887
Hirabayashi T (1971) Studies on muscle differentiation. III. Immuno-histochemical identification of tropomyosin in skeletal and cardiac muscles of developing chick embryo. Dev Growth Diff 12:241–252
Hirai S, Hirabayashi T (1983) Developmental change of protein constituents in chicken gizzards. Dev Biol 97:483–493
Ishii N, Takahashi K (1983) Polarity of myofilaments in molluscan smooth muscle. Cell Tissue Res 234:533–545
Kelly RE, Rice RV (1968) Localization of myosin filaments in smooth muscle. J Cell Biol 37:105–116
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond) 227:680–684
Langanger G, Mey JD, Moeremans M, Daneels G, Brabander MD, Small JV (1984) Ultrastructural localization of α-actinin and filamin in cultured cells with the immunogold staining (IGS) method. J Cell Biol 99:1324–1334
Lazarides E (1980) Intermediate filaments as mechanical integrators of cellular space. Nature (Lond) 283:249–256
Panner BJ, Honig CR (1970) Locus and state of aggregation of myosin in tissue sections of vertebrate smooth muscle. J Cell Biol 44:52–61
Pollard TD (1981) Cytoplasmic contractile proteins. J Cell Biol 91:156s-165s
Sanger JW, Sanger JM, Jockusch BM (1983) Differences in the stress fibers between fibroblasts and epithelial cells. J Cell Biol 96:961–969
Schollmeyer JE, Furcht LT, Goll DE, Robson RM, Stromer MH (1976) Localization of contractile proteins in smooth muscle cells and in normal and transformed fibroblasts. In: Goldman AR, Pollard T, Rosenbaum J (eds) Cell motility. Cold Spring Harbor Laboratory, New York, pp 361–388
Small JV (1974) Contractile units in vertebrate smooth muscle cells. Nature (Lond) 249:324–327
Small JV (1977) Studies on isolated smooth muscle cells: The contractile apparatus. J Cell Sci 24:327–349
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
Takano-Ohmuro H, Obinata T, Mikawa T, Masaki T (1983) Changes in myosin isozymes during development of chicken gizzard muscle. J Biochem (Tokyo) 93:903–908
Talian JC, Olmsted JB, Goldman RD (1983) A rapid procedure for preparing fluorescein-labeled specific antibodies from whole antiserum: Its use in analyzing cytoskeletal architecture. J Cell Biol 97:1277–1282
Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354
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
Uehara Y, Campbell GR, Burnstock G (1971) Cytoplasmic filaments in developing and adult vertebrate smooth muscle. J Cell Biol 50:484–497
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
Zigmond SH, Otto JJ, Bryan J (1979) Organization of myosin in a submembranous sheath in well-spread human fibroblasts Exp Cell Res 119:205–219
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Hirai, Si., Hirabayashi, T. Development of myofibrils in the gizzard of chicken embryos. Cell Tissue Res. 243, 487–493 (1986). https://doi.org/10.1007/BF00218055
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DOI: https://doi.org/10.1007/BF00218055