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. 1983 Dec 1;97(6):1860–1874. doi: 10.1083/jcb.97.6.1860

Expression of intermediate filament-associated proteins paranemin and synemin in chicken development

PMCID: PMC2112725  PMID: 6358235

Abstract

The expression of two intermediate filament-associated proteins, paranemin (280,000 mol wt) and synemin (230,000 mol wt), was investigated with respect to the expression of two core intermediate filament proteins, desmin and vimentin, in various embryonic and adult chicken muscle and nonmuscle cells. All developing muscle cells, regardless of their type, simultaneously express desmin, vimentin, paranemin, and synemin. However, a difference is observed in the expression of paranemin in adult muscle. This protein is removed during differentiation of both fast and slow skeletal muscle, visceral smooth muscle, and the smooth muscle of muscular arteries, but remains in mature myocardial cells, cardiac conducting fibers, and the smooth muscle cells of elastic arteries. Some of these cells express vimentin, others desmin, and still others a mixture of the two. On the other hand, synemin is expressed in all the above types of adult muscle cells except myocardial cells. Adult myocardial cells also lack vimentin, and its presence is gradually reduced after hatching. Since in adult striated muscle all expressed intermediate filament proteins are found predominantly in association with the peripheries of myofibrillar Z discs, these results suggest that a change in the composition of skeletal and cardiac muscle Z discs occurs during chicken development and maturation. Erythrocytes that express synemin and vimentin do not express paranemin, while both embryonic and adult Schwann cells co- express paranemin and vimentin, but not synemin. Endothelial cells of muscular vessels express paranemin, while those of elastic vessels do not, and neither contains synemin. Paranemin and synemin are not expressed in neurons, epithelial, and most glial cells, suggesting that these two polypeptides are expressed only in conjunction with desmin or vimentin. These results suggest that the composition of intermediate filaments changes during chicken development, not only with respect to their core subunit proteins but also with respect to two associated polypeptides, particularly in muscle cells.

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Selected References

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  1. Autilio-Gambetti L., Sipple J., Sudilovsky O., Gambetti P. Intermediate filaments of Schwann cells. J Neurochem. 1982 Mar;38(3):774–780. doi: 10.1111/j.1471-4159.1982.tb08698.x. [DOI] [PubMed] [Google Scholar]
  2. Bennett G. S., Fellini S. A., Holtzer H. Immunofluorescent visualization of 100 A filaments in different cultured chick embryo cell types. Differentiation. 1978;12(2):71–82. doi: 10.1111/j.1432-0436.1979.tb00992.x. [DOI] [PubMed] [Google Scholar]
  3. Bennett G. S., Fellini S. A., Toyama Y., Holtzer H. Redistribution of intermediate filament subunits during skeletal myogenesis and maturation in vitro. J Cell Biol. 1979 Aug;82(2):577–584. doi: 10.1083/jcb.82.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Breckler J., Lazarides E. Isolation of a new high molecular weight protein associated with desmin and vimentin filaments from avian embryonic skeletal muscle. J Cell Biol. 1982 Mar;92(3):795–806. doi: 10.1083/jcb.92.3.795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Campbell G. R., Chamley-Campbell J., Gröschel-Stewart U., Small J. V., Anderson P. Antibody staining of 10-nm (100-A) filaments in cultured smooth, cardiac and skeletal muscle cells. J Cell Sci. 1979 Jun;37:303–322. doi: 10.1242/jcs.37.1.303. [DOI] [PubMed] [Google Scholar]
  6. Carlsson E., Kjörell U., Thornell L. E., Lambertsson A., Strehler E. Differentiation of the myofibrils and the intermediate filament system during postnatal development of the rat heart. Eur J Cell Biol. 1982 Apr;27(1):62–73. [PubMed] [Google Scholar]
  7. Chiu F. C., Norton W. T., Fields K. L. The cytoskeleton of primary astrocytes in culture contains actin, glial fibrillary acidic protein, and the fibroblast-type filament protein, vimentin. J Neurochem. 1981 Jul;37(1):147–155. doi: 10.1111/j.1471-4159.1981.tb05302.x. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Eriksson A., Thornell L-E, Stigbrand T. Skeletin immunoreactivity in heart Purkinje fibers from several species. J Histochem Cytochem. 1979 Dec;27(12):1604–1609. doi: 10.1177/27.12.391995. [DOI] [PubMed] [Google Scholar]
  10. Eriksson A., Thornell L. E. Intermediate (skeletin) filaments in heart Purkinje fibers. A correlative morphological and biochemical identification with evidence of a cytoskeletal function. J Cell Biol. 1979 Feb;80(2):231–247. doi: 10.1083/jcb.80.2.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fellini S. A., Bennett G. S., Toyama Y., Holtzer H. Biochemical and immunological heterogeneity of 100 A filament subunits from different chick cell types. Differentiation. 1978;12(2):59–69. doi: 10.1111/j.1432-0436.1979.tb00991.x. [DOI] [PubMed] [Google Scholar]
  12. Frank E. D., Warren L. Aortic smooth muscle cells contain vimentin instead of desmin. Proc Natl Acad Sci U S A. 1981 May;78(5):3020–3024. doi: 10.1073/pnas.78.5.3020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Franke W. W., Schmid E., Osborn M., Weber K. Different intermediate-sized filaments distinguished by immunofluorescence microscopy. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5034–5038. doi: 10.1073/pnas.75.10.5034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Franke W. W., Schmid E., Osborn M., Weber K. Intermediate-sized filaments of human endothelial cells. J Cell Biol. 1979 Jun;81(3):570–580. doi: 10.1083/jcb.81.3.570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fuseler J. W., Shay J. W. The association of desmin with the developing myofibrils of cultured embryonic rat heart myocytes. Dev Biol. 1982 Jun;91(2):448–457. doi: 10.1016/0012-1606(82)90051-3. [DOI] [PubMed] [Google Scholar]
  16. Gabbiani G., Schmid E., Winter S., Chaponnier C., de Ckhastonay C., Vandekerckhove J., Weber K., Franke W. W. Vascular smooth muscle cells differ from other smooth muscle cells: predominance of vimentin filaments and a specific alpha-type actin. Proc Natl Acad Sci U S A. 1981 Jan;78(1):298–302. doi: 10.1073/pnas.78.1.298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. 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]
  20. Granger B. L., Lazarides E. Structural associations of synemin and vimentin filaments in avian erythrocytes revealed by immunoelectron microscopy. Cell. 1982 Aug;30(1):263–275. doi: 10.1016/0092-8674(82)90032-0. [DOI] [PubMed] [Google Scholar]
  21. Granger B. L., Lazarides E. Synemin: a new high molecular weight protein associated with desmin and vimentin filaments in muscle. Cell. 1980 Dec;22(3):727–738. doi: 10.1016/0092-8674(80)90549-8. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Granger B. L., Repasky E. A., Lazarides E. Synemin and vimentin are components of intermediate filaments in avian erythrocytes. J Cell Biol. 1982 Feb;92(2):299–312. doi: 10.1083/jcb.92.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Hynes R. O., Destree A. T. Relationships between fibronectin (LETS protein) and actin. Cell. 1978 Nov;15(3):875–886. doi: 10.1016/0092-8674(78)90272-6. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Lazarides E., Granger B. L., Gard D. L., O'Connor C. M., Breckler J., Price M., Danto S. I. Desmin- and vimentin-containing filaments and their role inthe assembly of the Z disk in muscle cells. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 1):351–378. doi: 10.1101/sqb.1982.046.01.036. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Lazarides E. Intermediate filaments as mechanical integrators of cellular space. Nature. 1980 Jan 17;283(5744):249–256. doi: 10.1038/283249a0. [DOI] [PubMed] [Google Scholar]
  30. Lazarides E. Intermediate filaments: a chemically heterogeneous, developmentally regulated class of proteins. Annu Rev Biochem. 1982;51:219–250. doi: 10.1146/annurev.bi.51.070182.001251. [DOI] [PubMed] [Google Scholar]
  31. Lazarides E. The distribution of desmin (100 A) filaments in primary cultures of embryonic chick cardiac cells. Exp Cell Res. 1978 Mar 15;112(2):265–273. doi: 10.1016/0014-4827(78)90209-4. [DOI] [PubMed] [Google Scholar]
  32. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  33. Oliphant L. W., Loewen R. D. Filament systems in purkinje cells of the sheep heart: possible alterations of myofibrillogenesis. J Mol Cell Cardiol. 1976 Sep;08(9):679–688. doi: 10.1016/0022-2828(76)90010-9. [DOI] [PubMed] [Google Scholar]
  34. Osborn M., Caselitz J., Weber K. Heterogeneity of intermediate filament expression in vascular smooth muscle: a gradient in desmin positive cells from the rat aortic arch to the level of the arteria iliaca communis. Differentiation. 1981;20(3):196–202. doi: 10.1111/j.1432-0436.1981.tb01176.x. [DOI] [PubMed] [Google Scholar]
  35. Osborn M., Ludwig-Festl M., Weber K., Bignami A., Dahl D., Bayreuther K. Expression of glial and vimentin type intermediate filaments in cultures derived from human glial material. Differentiation. 1981;19(3):161–167. doi: 10.1111/j.1432-0436.1981.tb01143.x. [DOI] [PubMed] [Google Scholar]
  36. Richardson F. L., Stromer M. H., Huiatt T. W., Robson R. M. Immunoelectron and immunofluorescence localization of desmin in mature avian muscles. Eur J Cell Biol. 1981 Dec;26(1):91–101. [PubMed] [Google Scholar]
  37. Schmid E., Osborn M., Rungger-Brändle E., Gabbiani G., Weber K., Franke W. W. Distribution of vimentin and desmin filaments in smooth muscle tissue of mammalian and avian aorta. Exp Cell Res. 1982 Feb;137(2):329–340. doi: 10.1016/0014-4827(82)90034-9. [DOI] [PubMed] [Google Scholar]
  38. Schmid E., Tapscott S., Bennett G. S., Croop J., Fellini S. A., Holtzer H., Franke W. W. Differential location of different types of intermediate-sized filaments in various tissues of the chicken embryo. Differentiation. 1979;15(1):27–40. doi: 10.1111/j.1432-0436.1979.tb01031.x. [DOI] [PubMed] [Google Scholar]
  39. Sharp G. A., Shaw G., Weber K. Immunoelectronmicroscopical localization of the three neurofilament triplet proteins along neurofilaments of cultured dorsal root ganglion neurones. Exp Cell Res. 1982 Feb;137(2):403–413. doi: 10.1016/0014-4827(82)90042-8. [DOI] [PubMed] [Google Scholar]
  40. Shaw G., Osborn M., Weber K. An immunofluorescence microscopical study of the neurofilament triplet proteins, vimentin and glial fibrillary acidic protein within the adult rat brain. Eur J Cell Biol. 1981 Dec;26(1):68–82. [PubMed] [Google Scholar]
  41. Shaw G., Weber K. Differential expression of neurofilament triplet proteins in brain development. Nature. 1982 Jul 15;298(5871):277–279. doi: 10.1038/298277a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Shaw G., Weber K. The distribution of the neurofilament triplet proteins within individual neurones. Exp Cell Res. 1981 Nov;136(1):119–125. doi: 10.1016/0014-4827(81)90043-4. [DOI] [PubMed] [Google Scholar]
  43. Small J. V., Sobieszek A. Studies on the function and composition of the 10-NM(100-A) filaments of vertebrate smooth muscle. J Cell Sci. 1977 Feb;23:243–268. doi: 10.1242/jcs.23.1.243. [DOI] [PubMed] [Google Scholar]
  44. Steinert P. M., Cantieri J. S., Teller D. C., Lonsdale-Eccles J. D., Dale B. A. Characterization of a class of cationic proteins that specifically interact with intermediate filaments. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4097–4101. doi: 10.1073/pnas.78.7.4097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tapscott S. J., Bennett G. S., Toyama Y., Kleinbart F., Holtzer H. Intermediate filament proteins in the developing chick spinal cord. Dev Biol. 1981 Aug;86(1):40–54. doi: 10.1016/0012-1606(81)90313-4. [DOI] [PubMed] [Google Scholar]
  46. Travo P., Weber K., Osborn M. Co-existence of vimentin and desmin type intermediate filaments in a subpopulation of adult rat vascular smooth muscle cells growing in primary culture. Exp Cell Res. 1982 May;139(1):87–94. doi: 10.1016/0014-4827(82)90321-4. [DOI] [PubMed] [Google Scholar]
  47. Willard M., Simon C. Antibody decoration of neurofilaments. J Cell Biol. 1981 May;89(2):198–205. doi: 10.1083/jcb.89.2.198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Yen S. H., Fields K. L. Antibodies to neurofilament, glial filament, and fibroblast intermediate filament proteins bind to different cell types of the nervous system. J Cell Biol. 1981 Jan;88(1):115–126. doi: 10.1083/jcb.88.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]

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