Summary
The Duchenne muscular dystrophy gene product dystrophin has been shown to be located on the inside of the plasma membrane. We investigated the developmental expression of dystrophin on rat skeletal muscle plasma membrane with the antiserum raised against a fragment of the polypeptide predicted from the human dystrophin cDNA map [Koenig et al. (1987) Cell 50: 509–517]. Plasma membrane of primary myotubes of the extensor digitorum longus (EDL) muscle was not initially stained by the antiserum; staining began at day 19 of embryonic life, and plasma membrane of all polynuclear muscle cells including secondary myotubes was uniformly stained by day 5 after birth. These immunohistochemical findings were supported by immunoblot analysis. These results indicate that plasma membrane of myotubes at their first appearance is not lined with dystrophin at the detectable level but becomes lined as their development proceeds.
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References
Adelstein RS, Eisenberg E (1980) Regulation and kinetics of the actin-myosin-ATP interaction. Ann Rev Biochem 49: 921–956
Arahata K, Ishiura S, Ishiguro T, Tsukahara T, Suhara Y, Eguchi C, Ishihara T, Nonaka I, Ozawa E, Sugita H (1988) Immunostaining of skeletal and cardiac muscle surface membrane with antibody against Duchenne muscular dystrophy peptide. Nature 333: 861–863
Bonilla E, Samitt CE, Miranda AF, Hays AP, Salviati IG, DiMauro S, Kunkel LM, Hoffman EP, Rowland LP (1988) Duchenne muscular dystrophy: deficiency of dystrophin at the muscle cell surface. Cell 54: 447–452
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254
Cooper AR, Kurkinen M, Taylor A, Hogan BLM (1981) Studies on the biosynthesis of laminin by murine parietal endoderm cells. Eur J Biochem 119: 189–197
Doucet J-P, Trifaro JM (1988) A discontinuous and highly porous sodium dodecyl sulfate-polyacrylamide slab gel system of high resolution. Anal Biochem 168: 265–271
Hoffman EP, Brown RH Jr, Kunkel LM (1987 a) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51: 919–928
—, Knudson CM, Campbell KP, Kunkel LM (1987 b) Subcellular fractionation of dystrophin to the triad of skeletal muscle. Nature 330: 754–758
—, Fischbeck KH, Brown RH, Johnson M, Medori R, Loike JD, Harris JB, Waterston R, Brooke M, Specht L, Kupsky W, Chamberlain J, Caskey CT, Shapiro F, Kunkel LM (1988 b) Characterization of dystrophin in muscle biopsy specimens from patients with Duchenne's or Becker's muscular dystrophy. N Engl J Med 318: 1363–1368
—, Hudecki MS, Rosenberg PA, Pollina CM, Kunkel LM (1988 a) Cell and fiber-type distribution of dystrophin. Neuron 1: 411–420
Kao L, Krstenansky J, Mendell J, Rammohan KW, Gruenstein E (1988) Immunological identification of a high molecular weight protein as a candidate for the product of the Duchenne muscular dystrophy gene. Proc Natl Acad Sci USA 85: 4491–4495
Kelly AM (1983) Emergence of specialization in skeletal muscle. In: Peachey LD (ed) Handbook of physiology. American Physiological Society, Bethesda, MD, pp 507–538
—, Zacks SI (1969 a) The histogenesis of rat intercostal muscle. J Cell Biol 42: 135–153
— — (1969 b) The fine structure of motor endoplate morphogenesis. J Cell Biol 42: 154–169
Koenig M, Hoffman EP, Bertelson CJ, Monaco AP, Feener C, Kunkel LM (1987) Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50: 509–517
—, Monaco AP, Kunkel LM (1988) The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53: 219–228
Kyhse-Anderson J (1984) Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J Biochem Biophys Methods 10: 203–209
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685
Lev AA, Feener CC, Kunkel LM, Brown RH Jr (1987) Expression of the Duchenne's muscular dystrophy gene in cultured muscle cells. J Biol Chem 262: 15817–15820
Marchesi VT (1985) Stabilizing infrastructure of cell membranes. Ann Rev Cell Biol 1: 531–561
Margossian SS, Lowey S (1982) Preparation of myosin and its subfragments from rabbit skeletal muscle. Methods Enzymol 85: 55–71
Matsuda R, Obinata T, Shimada Y (1981) Types of troponin components during development of chicken skeletal muscle. Dev Biol 82: 11–19
McLachlan J, Wolpert L (1980) The spacial pattern of muscle. development in chick limb. In: Goldspink DF (ed) Development and specialization of skeletal muscle. Cambridge University Press, Cambridge, U.K., pp 1–17
Miranda AF, Bonilla E, Martucci G, Moraes CT, Hays AP, Dimauro S (1988) Immunocytochemical study of dystrophin in muscle cultures from patients with Duchenne muscular dystrophy and unaffected control patients. Am J Pathol 132: 410–415
Miyata Y, Yoshioka K (1980) Selective elimination of motor nerve terminals in the rat soleus muscle during development. J Physiol (Lond) 309: 631–646
Nudel U, Robzyk K, Yaffe D (1988) Expression of the putative Duchenne muscular dystrophy gene in differentiated myogenic cell cultures and in the brain. Nature 331: 635–638
Ross JJ, Duxon MJ, Harris AJ (1987) Formation of primary and secondary myotubes in rat lumbrical muscles. Development 100: 383–394
Rubinstein NA, Kelly AM (1980) Myogenic and neurogenic contributions to the development of fast and slow twitch muscles in rat. Dev Biol 62: 473–485
Scott MO, Sylvester JE, Heiman-Patterson T, Shi Y-J, Fieles W, Stedman H, Burghes A, Ray P, Worton R, Fischbeck KH (1988) Duchenne muscular dystrophy gene expression in normal and diseased human muscle. Science 239: 1418–1420
Shimizu T, Matsumura K, Hashimoto K, Mannen T, Ishiguro T, Eguchi C, Nonaka I, Yosida M, Ozawa E (1988) A monoclonal antibody to a synthetic polypeptide fragment of dystrophin (amino acid sequence from position 215 to 264). Proc Japan Acad 64 B: 205–208
Sugita H, Arahata K, Ishiguro T, Suhara Y, Tsukahara T, Ishiura S, Eguchi C, Nonaka I, Ozawa E (1988) Negative immunostaining of Duchenne muscular dystrophy (DMD) andmdx muscle surface membrane with antibody against synthetic peptide fragment prodicted from DMD cDNA. Proc Japan Acad 64 B: 37–39
Watkins SC, Hoffman EP, Slayter HS, Kunkel LM (1988) Immunoelectron microscopic localization of dystrophin in myofibres. Nature 333: 863–866
Worton RG, Burghes AH (1988) Molecular genetics of Duchenne and Becker muscular dystrophy. Int Rev Neurobiol 29: 1–76
Zubrzycka-Gaarn EE, Bulman DE, Karpati G, Burghes AHM, Belfall B, Klamut HJ, Talbot J, Hodges RS, Ray PN, Worton RG (1988) The Duchenne muscular dystrophy gene product is localized in sarcolemma of human skeletal muscle. Nature 333: 466–469
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Hagiwara, Y., Yoshida, M., Nonaka, I. et al. Developmental expression of dystrophin on the plasma membrane of rat muscle cells. Protoplasma 151, 11–18 (1989). https://doi.org/10.1007/BF01403297
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DOI: https://doi.org/10.1007/BF01403297