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J Cell Biol. Oct 1, 1983; 97(4): 957–962.
PMCID: PMC2112627

Changes in the basement membrane zone components during skeletal muscle fiber degeneration and regeneration

Abstract

The basement membrane of skeletal muscle fibers is believed to persist unchanged during myofiber degeneration and act as a tubular structure within which the regeneration of new myofibers occurs. In the present study we describe macromolecular changes in the basement membrane zone during muscle degeneration and regeneration, as monitored by immunofluorescence using specific antibodies against types IV and V collagen, laminin, and heparan sulfate proteoglycan and by the binding of concanavalin A (Con A). Skeletal muscle regeneration was induced by autotransplantation of the extensor digitorum longus muscle in rats. After this procedure, the myofibers degenerate; this is followed by myosatellite cell activation, proliferation, and fusion, resulting in the formation of new myotubes that mature into myofibers. In normal muscle, the distribution of types IV and V collagen, laminin, heparan sulfate proteoglycan, and Con A binding was seen in the pericellular basement membrane region. In autotransplanted muscle, the various components of the basement membrane zone disappeared, leaving behind some unidentifiable component that still bound Con A. Around the regenerated myotubes a new basement membrane (zone) reappeared, which persisted during maturation of the regenerating muscle. The distribution of various basement membrane components in the regenerated myofibers was similar to that seen in the normal muscle. Based on our present and previous study (Gulati, A.K., A.H. Reddi, and A.A. Zalewski, 1982, Anat. Rec. 204:175-183), it appears that some of the original basement membrane zone components disappear during myofiber degeneration and initial regeneration. As a new basement membrane develops, its components reappear and persist in the mature myofibers. We conclude that skeletal muscle fiber basement membrane (zone) is not a static structure as previously thought, but rather that its components change quite rapidly during myofiber degeneration and regeneration.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Allbrook D. Skeletal muscle regeneration. Muscle Nerve. 1981 May-Jun;4(3):234–245. [PubMed]
  • Beach RL, Burton WV, Hendricks WJ, Festoff BW. Extracellular matrix synthesis by skeletal muscle in culture. Proteins and effect of enzyme degradation. J Biol Chem. 1982 Oct 10;257(19):11437–11442. [PubMed]
  • Burden SJ, Sargent PB, McMahan UJ. Acetylcholine receptors in regenerating muscle accumulate at original synaptic sites in the absence of the nerve. J Cell Biol. 1979 Aug;82(2):412–425. [PMC free article] [PubMed]
  • Carlson BM. A review of muscle transplantation in mammals. Physiol Bohemoslov. 1978;27(5):387–400. [PubMed]
  • Carlson BM, Gutmann E. Regneration in free grafts of normal and denervated muscles in the rat: morphology and histochemistry. Anat Rec. 1975 Sep;183(1):47–62. [PubMed]
  • Courtoy PJ, Timpl R, Farquhar MG. Comparative distribution of laminin, type IV collagen, and fibronectin in the rat glomerulus. J Histochem Cytochem. 1982 Sep;30(9):874–886. [PubMed]
  • Duance VC, Restall DJ, Beard H, Bourne FJ, Bailey AJ. The location of three collagen types in skeletal muscle. FEBS Lett. 1977 Jul 15;79(2):248–252. [PubMed]
  • Ekblom P. Formation of basement membranes in the embryonic kidney: an immunohistological study. J Cell Biol. 1981 Oct;91(1):1–10. [PMC free article] [PubMed]
  • Foidart JM, Reddi AH. Immunofluorescent localization of type IV collagen and laminin during endochondral bone differentiation and regulation by pituitary growth hormone. Dev Biol. 1980 Mar;75(1):130–136. [PubMed]
  • Foidart JM, Bere EW, Jr, Yaar M, Rennard SI, Gullino M, Martin GR, Katz SI. Distribution and immunoelectron microscopic localization of laminin, a noncollagenous basement membrane glycoprotein. Lab Invest. 1980 Mar;42(3):336–342. [PubMed]
  • Furcht LT, Wendelschafer-Crabb G, Woodbridge PA. Cell surface changes accompanying myoblast differentiation. J Supramol Struct. 1977;7(3-4):307–322. [PubMed]
  • Gay S, Martinez-Hernandez A, Rhodes RK, Miller EJ. The collagenous exocytoskeleton of smooth muscle cells. Coll Relat Res. 1981 Jul;1(4):377–384. [PubMed]
  • Grant ME, Heathcote JG, Orkin RW. Current concepts of basement-membrane structure and function. Biosci Rep. 1981 Nov;1(11):819–842. [PubMed]
  • Gulati AK, Zalewski AA. Muscle allograft survival after cyclosporin A immunosuppression. Exp Neurol. 1982 Aug;77(2):378–385. [PubMed]
  • Gulati AK, Reddi AH, Zalewski AA. Distribution of fibronectin in normal and regenerating skeletal muscle. Anat Rec. 1982 Nov;204(3):175–183. [PubMed]
  • Gulati AK, Zalewski AA, Reddi AH. An immunofluorescent study of the distribution of fibronectin and laminin during limb regeneration in the adult newt. Dev Biol. 1983 Apr;96(2):355–365. [PubMed]
  • Hansen-Smith FM, Carlson BM. Cellular responses to free grafting of the extensor digitorum longus muscle of the rat. J Neurol Sci. 1979 Apr;41(2):149–173. [PubMed]
  • Hassell JR, Robey PG, Barrach HJ, Wilczek J, Rennard SI, Martin GR. Isolation of a heparan sulfate-containing proteoglycan from basement membrane. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4494–4498. [PMC free article] [PubMed]
  • Kanwar YS, Farquhar MG. Isolation of glycosaminoglycans (heparan sulfate) from glomerular basement membranes. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4493–4497. [PMC free article] [PubMed]
  • Kefalides NA, Alper R, Clark CC. Biochemistry and metabolism of basement membranes. Int Rev Cytol. 1979;61:167–228. [PubMed]
  • Kühl U, Timpl R, von der Mark K. Synthesis of type IV collagen and laminin in cultures of skeletal muscle cells and their assembly on the surface of myotubes. Dev Biol. 1982 Oct;93(2):344–354. [PubMed]
  • Laurie GW, Leblond CP, Martin GR. Localization of type IV collagen, laminin, heparan sulfate proteoglycan, and fibronectin to the basal lamina of basement membranes. J Cell Biol. 1982 Oct;95(1):340–344. [PMC free article] [PubMed]
  • Liotta LA, Goldfarb RH, Brundage R, Siegal GP, Terranova V, Garbisa S. Effect of plasminogen activator (urokinase), plasmin, and thrombin on glycoprotein and collagenous components of basement membrane. Cancer Res. 1981 Nov;41(11 Pt 1):4629–4636. [PubMed]
  • McMahan UJ, Sanes JR, Marshall LM. Cholinesterase is associated with the basal lamina at the neuromuscular junction. Nature. 1978 Jan 12;271(5641):172–174. [PubMed]
  • Martinez-Hernandez A, Gay S, Miller EJ. Ultrastructural localization of type V collagen in rat kidney. J Cell Biol. 1982 Feb;92(2):343–349. [PMC free article] [PubMed]
  • Martinez-Hernandez A, Marsh CA, Clark CC, Macarak EJ, Brownell AG. Fibronectin: its relationship to basement membranes. II. Ultrastructural studies in rat kidney. Coll Relat Res. 1981 Sep;1(5):405–418. [PubMed]
  • Peltonen L, Myllylä R, Tolonen U, Myllylä VV. Changes in collagen metabolism in diseased muscle. II. Immunohistochemical studies. Arch Neurol. 1982 Dec;39(12):756–759. [PubMed]
  • Pena SD, Gordon BB, Karpati G, Carpenter S. Lectin histochemistry of human skeletal muscle. J Histochem Cytochem. 1981 Apr;29(4):542–546. [PubMed]
  • Rao CN, Margulies IM, Tralka TS, Terranova VP, Madri JA, Liotta LA. Isolation of a subunit of laminin and its role in molecular structure and tumor cell attachment. J Biol Chem. 1982 Aug 25;257(16):9740–9744. [PubMed]
  • Risteli L, Risteli J. Basement membrane research. Med Biol. 1981 Aug;59(4):185–189. [PubMed]
  • Rojkind M, Ponce-Noyola P. The extracellular matrix of the liver. Coll Relat Res. 1982 Mar;2(2):151–175. [PubMed]
  • Roll FJ, Madri JA, Albert J, Furthmayr H. Codistribution of collagen types IV and AB2 in basement membranes and mesangium of the kidney. an immunoferritin study of ultrathin frozen sections. J Cell Biol. 1980 Jun;85(3):597–616. [PMC free article] [PubMed]
  • Sanes JR. Laminin, fibronectin, and collagen in synaptic and extrasynaptic portions of muscle fiber basement membrane. J Cell Biol. 1982 May;93(2):442–451. [PMC free article] [PubMed]
  • Sanes JR, Cheney JM. Lectin binding reveals a synapse-specific carbohydrate in skeletal muscle. Nature. 1982 Dec 16;300(5893):646–647. [PubMed]
  • Schmalbruch H. The morphology of regeneration of skeletal muscles in the rat. Tissue Cell. 1976;8(4):673–692. [PubMed]
  • Spiro RG. Nature of the glycoprotein components of basement membranes. Ann N Y Acad Sci. 1978 Jun 20;312:106–121. [PubMed]
  • Stenman S, Vaheri A. Distribution of a major connective tissue protein, fibronectin, in normal human tissues. J Exp Med. 1978 Apr 1;147(4):1054–1064. [PMC free article] [PubMed]
  • Timpl R, Rohde H, Robey PG, Rennard SI, Foidart JM, Martin GR. Laminin--a glycoprotein from basement membranes. J Biol Chem. 1979 Oct 10;254(19):9933–9937. [PubMed]
  • Vracko R. Basal lamina scaffold-anatomy and significance for maintenance of orderly tissue structure. Am J Pathol. 1974 Nov;77(2):314–346. [PMC free article] [PubMed]
  • Vracko R. Basal lamina layering in diabetes mellitus. Evidence for accelerated rate of cell death and cell regeneration. Diabetes. 1974 Feb;23(2):94–104. [PubMed]
  • Vracko R, Benditt EP. Capillary basal lamina thickening. Its relationship to endothelial cell death and replacement. J Cell Biol. 1970 Oct;47(1):281–285. [PMC free article] [PubMed]
  • Vracko R, Benditt EP. Basal lamina: the scaffold for orderly cell replacement. Observations on regeneration of injured skeletal muscle fibers and capillaries. J Cell Biol. 1972 Nov;55(2):406–419. [PMC free article] [PubMed]
  • Yaoita H, Foidart JM, Katz SI. Localization of the collagenous component in skin basement membrane. J Invest Dermatol. 1978 Apr;70(4):191–193. [PubMed]
  • Zimmermann B, Merker HJ, Barrach HJ. Basement membrane alterations after treatment with trypsin, hyaluronidase or collagenase. Virchows Arch B Cell Pathol Incl Mol Pathol. 1982;40(1):9–15. [PubMed]

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