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. 1983 Sep 1;97(3):818–823. doi: 10.1083/jcb.97.3.818

Highly homologous filamin polypeptides have different distributions in avian slow and fast muscle fibers

PMCID: PMC2112561  PMID: 6350321

Abstract

The high molecular weight actin-binding protein filamin is located at the periphery of the Z disk in the fast adult chicken pectoral muscle (Gomer, R. H., and E. Lazarides, 1981, Cell, 23: 524-532). In contrast, we have found that in the slow anterior latissimus dorsi (ALD) muscle, filamin was additionally located throughout the l band as judged by immunofluorescence with affinity-purified antibodies on myofibrils and cryosections. The Z line proteins desmin and alpha-actinin, however, had the same distribution in ALD as they do in pectoral muscle. Quantitation of filamin and actin from the two muscle types showed that there was approximately 10 times as much filamin per actin in ALD myofibrils as in pectoral myofibrils. Filamin immunoprecipitated from ALD had an electrophoretic mobility in SDS polyacrylamide gels identical to that of pectoral myofibril filamin and slightly greater than that of chicken gizzard filamin. Two-dimensional peptide maps of filamin immunoprecipitated and labeled with 125I showed that ALD myofibril filamin was virtually identical to pectoral myofibril filamin and was distinct from chicken gizzard filamin.

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Selected References

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  1. BARANY M., BARANY K., RECKARD T., VOLPE A. MYOSIN OF FAST AND SLOW MUSCLES OF THE RABBIT. Arch Biochem Biophys. 1965 Jan;109:185–191. doi: 10.1016/0003-9861(65)90304-8. [DOI] [PubMed] [Google Scholar]
  2. BULLER A. J., LEWIS D. M. FURTHER OBSERVATIONS ON MAMMALIAN CROSS-INNERVATED SKELETAL MUSCLE. J Physiol. 1965 May;178:343–358. doi: 10.1113/jphysiol.1965.sp007631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bechtel P. J. Identification of a high molecular weight actin-binding protein in skeletal muscle. J Biol Chem. 1979 Mar 25;254(6):1755–1758. [PubMed] [Google Scholar]
  4. Bronson D. D., Schachat F. H. Heterogeneity of contractile proteins. Differences in tropomyosin in fast, mixed, and slow skeletal muscles of the rabbit. J Biol Chem. 1982 Apr 10;257(7):3937–3944. [PubMed] [Google Scholar]
  5. Brotschi E. A., Hartwig J. H., Stossel T. P. The gelation of actin by actin-binding protein. J Biol Chem. 1978 Dec 25;253(24):8988–8993. [PubMed] [Google Scholar]
  6. Bárány M. ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol. 1967 Jul;50(6 Suppl):197–218. doi: 10.1085/jgp.50.6.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bárány M., Close R. I. The transformation of myosin in cross-innervated rat muscles. J Physiol. 1971 Mar;213(2):455–474. doi: 10.1113/jphysiol.1971.sp009393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cummins P., Perry S. V. Chemical and immunochemical characteristics of tropomyosins from striated and smooth muscle. Biochem J. 1974 Jul;141(1):43–49. doi: 10.1042/bj1410043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. DAWSON D. M., ROMANUL F. C. ENZYMES IN MUSCLES. II. HISTOCHEMICAL AND QUANTITATIVE STUDIES. Arch Neurol. 1964 Oct;11:369–378. doi: 10.1001/archneur.1964.00460220031004. [DOI] [PubMed] [Google Scholar]
  10. Davies P. J., Wallach D., Willingham M. C., Pastan I., Yamaguchi M., Robson R. M. Filamin-actin interaction. Dissociation of binding from gelation by Ca2+-activated proteolysis. J Biol Chem. 1978 Jun 10;253(11):4036–4042. [PubMed] [Google Scholar]
  11. Davies P., Bechtel P., Pastan I. Filamin inhibits actin activation of heavy meromyosin ATPase. FEBS Lett. 1977 May 15;77(2):228–232. doi: 10.1016/0014-5793(77)80240-8. [DOI] [PubMed] [Google Scholar]
  12. Dhoot G. K., Perry S. V. Distribution of polymorphic forms of troponin components and tropomyosin in skeletal muscle. Nature. 1979 Apr 19;278(5706):714–718. doi: 10.1038/278714a0. [DOI] [PubMed] [Google Scholar]
  13. Elder J. H., Pickett R. A., 2nd, Hampton J., Lerner R. A. Radioiodination of proteins in single polyacrylamide gel slices. Tryptic peptide analysis of all the major members of complex multicomponent systems using microgram quantities of total protein. J Biol Chem. 1977 Sep 25;252(18):6510–6515. [PubMed] [Google Scholar]
  14. GREENWOOD F. C., HUNTER W. M., GLOVER J. S. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY. Biochem J. 1963 Oct;89:114–123. doi: 10.1042/bj0890114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gard D. L., Lazarides E. The synthesis and distribution of desmin and vimentin during myogenesis in vitro. Cell. 1980 Jan;19(1):263–275. doi: 10.1016/0092-8674(80)90408-0. [DOI] [PubMed] [Google Scholar]
  16. Gomer R. H., Lazarides E. Switching of filamin polypeptides during myogenesis in vitro. J Cell Biol. 1983 Feb;96(2):321–329. doi: 10.1083/jcb.96.2.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gomer R. H., Lazarides E. The synthesis and deployment of filamin in chicken skeletal muscle. Cell. 1981 Feb;23(2):524–532. doi: 10.1016/0092-8674(81)90148-3. [DOI] [PubMed] [Google Scholar]
  18. Granger B. L., Lazarides E. Desmin and vimentin coexist at the periphery of the myofibril Z disc. Cell. 1979 Dec;18(4):1053–1063. doi: 10.1016/0092-8674(79)90218-6. [DOI] [PubMed] [Google Scholar]
  19. Granger B. L., Lazarides E. The existence of an insoluble Z disc scaffold in chicken skeletal muscle. Cell. 1978 Dec;15(4):1253–1268. doi: 10.1016/0092-8674(78)90051-x. [DOI] [PubMed] [Google Scholar]
  20. HESS A. Structural differences of fast and slow extrafusal muscle fibres and their nerve endings in chickens. J Physiol. 1961 Jul;157:221–231. doi: 10.1113/jphysiol.1961.sp006717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. HUXLEY H. E. ELECTRON MICROSCOPE STUDIES ON THE STRUCTURE OF NATURAL AND SYNTHETIC PROTEIN FILAMENTS FROM STRIATED MUSCLE. J Mol Biol. 1963 Sep;7:281–308. doi: 10.1016/s0022-2836(63)80008-x. [DOI] [PubMed] [Google Scholar]
  22. Hartwig J. H., Stossel T. P. Interactions of actin, myosin, and an actin-binding protein of rabbit pulmonary macrophages. III. Effects of cytochalasin B. J Cell Biol. 1976 Oct;71(1):295–303. doi: 10.1083/jcb.71.1.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hartwig J. H., Stossel T. P. Isolation and properties of actin, myosin, and a new actinbinding protein in rabbit alveolar macrophages. J Biol Chem. 1975 Jul 25;250(14):5696–5705. [PubMed] [Google Scholar]
  24. Hess A. Vertebrate slow muscle fibers. Physiol Rev. 1970 Jan;50(1):40–62. doi: 10.1152/physrev.1970.50.1.40. [DOI] [PubMed] [Google Scholar]
  25. Hoh J. F., Yeoh G. P. Rabbit skeletal myosin isoenzymes from fetal, fast-twitch and slow-twitch muscles. Nature. 1979 Jul 26;280(5720):321–323. doi: 10.1038/280321a0. [DOI] [PubMed] [Google Scholar]
  26. Hubbard B. D., Lazarides E. Copurification of actin and desmin from chicken smooth muscle and their copolymerization in vitro to intermediate filaments. J Cell Biol. 1979 Jan;80(1):166–182. doi: 10.1083/jcb.80.1.166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. KATZ A. M., DREYER W. J., ANFINSEN C. B. Peptide separation by two-dimensional chromatography and electrophoresis. J Biol Chem. 1959 Nov;234:2897–2900. [PubMed] [Google Scholar]
  28. Kessler S. W. Cell membrane antigen isolation with the staphylococcal protein A-antibody adsorbent. J Immunol. 1976 Nov;117(5 Pt 1):1482–1490. [PubMed] [Google Scholar]
  29. Kessler S. W. Rapid isolation of antigens from cells with a staphylococcal protein A-antibody adsorbent: parameters of the interaction of antibody-antigen complexes with protein A. J Immunol. 1975 Dec;115(6):1617–1624. [PubMed] [Google Scholar]
  30. Koteliansky V. E., Glukhova M. A., Shirinsky V. P., Babaev V. R., Kandalenko V. F., Rukosuev V. S., Smirnov V. N. Identification of a filamin-like protein in chicken heart muscle. FEBS Lett. 1981 Mar 9;125(1):44–48. doi: 10.1016/0014-5793(81)80992-1. [DOI] [PubMed] [Google Scholar]
  31. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  32. Lazarides E., Hubbard B. D. Immunological characterization of the subunit of the 100 A filaments from muscle cells. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4344–4348. doi: 10.1073/pnas.73.12.4344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Maruyama K., Ohashi K. Tropomyosin inhibits the interaction of F-actin and filamin. J Biochem. 1978 Oct;84(4):1017–1019. doi: 10.1093/oxfordjournals.jbchem.a132184. [DOI] [PubMed] [Google Scholar]
  34. Mommaerts W. F., Buller A. J., Seraydarian K. The modification of some biochemical properties of muscle by cross-innervation. Proc Natl Acad Sci U S A. 1969 Sep;64(1):128–133. doi: 10.1073/pnas.64.1.128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Montarras D., Fiszman M. Y., Gros F. Characterization of the tropomyosin present in various chick embryo muscle types and in muscle cells differentiated in vitro. J Biol Chem. 1981 Apr 25;256(8):4081–4086. [PubMed] [Google Scholar]
  36. Nunnally M. H., Powell L. D., Craig S. W. Reconstitution and regulation of actin gel-sol transformation with purified filamin and villin. J Biol Chem. 1981 Mar 10;256(5):2083–2086. [PubMed] [Google Scholar]
  37. Page S. G. Structure and some contractile properties of fast and slow muscles of the chicken. J Physiol. 1969 Nov;205(1):131–145. doi: 10.1113/jphysiol.1969.sp008956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Prewitt M. A., Salafsky B. Effect of cross innervation on biochemical characteristics of skeletal muscles. Am J Physiol. 1967 Jul;213(1):295–300. doi: 10.1152/ajplegacy.1967.213.1.295. [DOI] [PubMed] [Google Scholar]
  39. REVEL J. P. The sarcoplasmic reticulum of the bat cricothroid muscle. J Cell Biol. 1962 Mar;12:571–588. doi: 10.1083/jcb.12.3.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Reinach F. C., Masaki T., Shafiq S., Obinata T., Fischman D. A. Isoforms of C-protein in adult chicken skeletal muscle: detection with monoclonal antibodies. J Cell Biol. 1982 Oct;95(1):78–84. doi: 10.1083/jcb.95.1.78. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Robson R. M., Zeece M. G. Comparative studies of -actinin from porcine cardiac and skeletal muscle. Biochim Biophys Acta. 1973 Jan 25;295(1):208–224. doi: 10.1016/0005-2795(73)90088-3. [DOI] [PubMed] [Google Scholar]
  42. Rosenberg S., Stracher A. Effect of actin-binding protein on the sedimentation properties of actin. J Cell Biol. 1982 Jul;94(1):51–55. doi: 10.1083/jcb.94.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. STEIN J. M., PADYKULA H. A. Histochemical classification of individual skeletal muscle fibers of the rat. Am J Anat. 1962 Mar;110:103–123. doi: 10.1002/aja.1001100203. [DOI] [PubMed] [Google Scholar]
  44. Samaha F. J., Guth L., Albers R. W. The neural regulation of gene expression in the muscle cell. Exp Neurol. 1970 May;27(2):276–282. doi: 10.1016/0014-4886(70)90220-7. [DOI] [PubMed] [Google Scholar]
  45. Schiaffino S., Hanzlíková V., Pierobon S. Relations between structure and function in rat skeletal muscle fibers. J Cell Biol. 1970 Oct;47(1):107–119. doi: 10.1083/jcb.47.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Shizuta Y., Shizuta H., Gallo M., Davies P., Pastan I. Purification and properties of filamin, and actin binding protein from chicken gizzard. J Biol Chem. 1976 Nov 10;251(21):6562–6567. [PubMed] [Google Scholar]
  47. Spudich J. A., Watt S. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J Biol Chem. 1971 Aug 10;246(15):4866–4871. [PubMed] [Google Scholar]
  48. Spudich J. A., Watt S. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J Biol Chem. 1971 Aug 10;246(15):4866–4871. [PubMed] [Google Scholar]
  49. Sreter F. A., Seidel J. C., Gergely J. Studies on myosin from red and white skeletal muscles of the rabbit. I. Adenosine triphosphatase activity. J Biol Chem. 1966 Dec 25;241(24):5772–5776. [PubMed] [Google Scholar]
  50. Stossel T. P., Hartwig J. H. Interactions of actin, myosin, and a new actin-binding protein of rabbit pulmonary macrophages. II. Role in cytoplasmic movement and phagocytosis. J Cell Biol. 1976 Mar;68(3):602–619. doi: 10.1083/jcb.68.3.602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Tomanek R. J., Asmundson C. R., Cooper R. R., Barnard R. J. Fine structure of fast-twitch and slow-twitch guinea pig muscle fibers. J Morphol. 1973 Jan;139(1):47–65. doi: 10.1002/jmor.1051390104. [DOI] [PubMed] [Google Scholar]
  52. Wang K., Ash J. F., Singer S. J. Filamin, a new high-molecular-weight protein found in smooth muscle and non-muscle cells. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4483–4486. doi: 10.1073/pnas.72.11.4483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Wang K. Filamin, a new high-molecular-weight protein found in smooth muscle and nonmuscle cells. Purification and properties of chicken gizzard filamin. Biochemistry. 1977 May 3;16(9):1857–1865. doi: 10.1021/bi00628a015. [DOI] [PubMed] [Google Scholar]
  54. Wang K., Singer S. J. Interaction of filamin with f-actin in solution. Proc Natl Acad Sci U S A. 1977 May;74(5):2021–2025. doi: 10.1073/pnas.74.5.2021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Zeece M. G., Robson R. M., Bechtel P. J. Interaction of alpha-actinin, filamin and tropomyosin with F-actin. Biochim Biophys Acta. 1979 Dec 14;581(2):365–370. doi: 10.1016/0005-2795(79)90258-7. [DOI] [PubMed] [Google Scholar]

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