Skip to main content
Top
Published in: Medical Molecular Morphology 1/2015

01-03-2015 | Original Paper

Filamentous structures in skeletal muscle: anchors for the subsarcolemmal space

Authors: Astrid Feinisa Khairani, Yuki Tajika, Maiko Takahashi, Hitoshi Ueno, Tohru Murakami, Arifin Soenggono, Hiroshi Yorifuji

Published in: Medical Molecular Morphology | Issue 1/2015

Login to get access

Abstract

In skeletal muscle fibers, intermediate filaments and actin filaments provide structural support to the myofibrils and the sarcolemma. For many years, it was poorly understood from ultrastructural observations that how these filamentous structures were kept anchored. The present study was conducted to determine the architecture of filamentous anchoring structures in the subsarcolemmal space and the intermyofibrils. The diaphragms (Dp) of adult wild type and mdx mice (mdx is a model for Duchenne muscular dystrophy) were subjected to tension applied perpendicular to the long axis of the muscle fibers, with or without treatment with 1 % Triton X-100 or 0.03 % saponin. These experiments were conducted to confirm the presence and integrity of the filamentous anchoring structures. Transmission electron microscopy revealed that these structures provide firm transverse connections between the sarcolemma and peripheral myofibrils. Most of the filamentous structures appeared to be inserted into subsarcolemmal densities, forming anchoring connections between the sarcolemma and peripheral myofibrils. In some cases, actin filaments were found to run longitudinally in the subsarcolemmal space to connect to the sarcolemma or in some cases to connect to the intermyofibrils as elongated thin filaments. These filamentous anchoring structures were less common in the mdx Dp. Our data suggest that the transverse and longitudinal filamentous structures form an anchoring system in the subsarcolemmal space and the intermyofibrils.
Literature
2.
go back to reference O’Neill A, Williams M, Resneck WG, Milner DJ, Capetanaki Y, Bloch RJ (2002) Sarcolemmal organization in skeletal muscle lacking desmin: evidence for cytokeratins associated with the membrane skeleton at costameres. Mol Biol Cell 13:2347–2359CrossRefPubMedCentralPubMed O’Neill A, Williams M, Resneck WG, Milner DJ, Capetanaki Y, Bloch RJ (2002) Sarcolemmal organization in skeletal muscle lacking desmin: evidence for cytokeratins associated with the membrane skeleton at costameres. Mol Biol Cell 13:2347–2359CrossRefPubMedCentralPubMed
3.
go back to reference Capetanaki Y, Bloch RJ, Kouloumenta A, Mavroidis M, Psarras S (2007) Muscle intermediate filaments and their links to membranes and membranous organelles. Exp Cell Res 313:2063–2076CrossRefPubMed Capetanaki Y, Bloch RJ, Kouloumenta A, Mavroidis M, Psarras S (2007) Muscle intermediate filaments and their links to membranes and membranous organelles. Exp Cell Res 313:2063–2076CrossRefPubMed
4.
go back to reference Kee AJ, Gunning PW, Hardeman EC (2009) Diverse roles of the actin cytoskeleton in striated muscle. J Muscle Res Cell Motil 30:187–197CrossRefPubMed Kee AJ, Gunning PW, Hardeman EC (2009) Diverse roles of the actin cytoskeleton in striated muscle. J Muscle Res Cell Motil 30:187–197CrossRefPubMed
5.
go back to reference Clark KA, McElhinny AS, Beckerle MC, Gregorio CC (2002) Striated muscle cytoarchitecture: an intricate web of form and function. Annu Rev Cell Dev Biol 18:637–706CrossRefPubMed Clark KA, McElhinny AS, Beckerle MC, Gregorio CC (2002) Striated muscle cytoarchitecture: an intricate web of form and function. Annu Rev Cell Dev Biol 18:637–706CrossRefPubMed
6.
go back to reference Pardo JV, Siliciano JD, Craig SW (1983) A vinculin-containing cortical lattice in skeletal muscle: transverse lattice elements (“costameres”) mark sites of attachment between myofibrils and sarcolemma. Proc Natl Acad Sci USA 80:1008–1012CrossRefPubMedCentralPubMed Pardo JV, Siliciano JD, Craig SW (1983) A vinculin-containing cortical lattice in skeletal muscle: transverse lattice elements (“costameres”) mark sites of attachment between myofibrils and sarcolemma. Proc Natl Acad Sci USA 80:1008–1012CrossRefPubMedCentralPubMed
7.
go back to reference Bloch RJ, Gonzales-Serratos H (2003) Lateral force transmission across costameres in skeletal muscle. Exerc Sport Sci Rev 31:73–78CrossRefPubMed Bloch RJ, Gonzales-Serratos H (2003) Lateral force transmission across costameres in skeletal muscle. Exerc Sport Sci Rev 31:73–78CrossRefPubMed
8.
go back to reference Ursitti JA, Lee PC, Resneck WG, McNally MM, Bowman AL, O’Neill A, Stone MR, Bloch RJ (2004) Cloning and characterization of cytokeratins 8 and 19 in adult rat striated muscle. Interaction with the dystrophin glycoprotein complex. J Biol Chem 279:41830–41838CrossRefPubMed Ursitti JA, Lee PC, Resneck WG, McNally MM, Bowman AL, O’Neill A, Stone MR, Bloch RJ (2004) Cloning and characterization of cytokeratins 8 and 19 in adult rat striated muscle. Interaction with the dystrophin glycoprotein complex. J Biol Chem 279:41830–41838CrossRefPubMed
9.
go back to reference Ervasti JM (2003) Costameres: the Achilles’ heel of herculean muscle. J Biol Chem 278:13591–13594CrossRefPubMed Ervasti JM (2003) Costameres: the Achilles’ heel of herculean muscle. J Biol Chem 278:13591–13594CrossRefPubMed
10.
go back to reference Craig SW, Pardo JV (1983) Gamma actin, spectrin, and intermediate filament proteins colocalize with vinculin at costameres, myofibril-to-sarcolemma attachment sites. Cell Motil 3:449–462CrossRefPubMed Craig SW, Pardo JV (1983) Gamma actin, spectrin, and intermediate filament proteins colocalize with vinculin at costameres, myofibril-to-sarcolemma attachment sites. Cell Motil 3:449–462CrossRefPubMed
11.
go back to reference Porter GA, Dmytrenko GM, Winkelmann JC, Bloch RJ (1992) Dystrophin colocalizes with β-spectrin in distinct subsarcolemmal domains in mammalian skeletal muscle. J Cell Biol 117:997–1005CrossRefPubMed Porter GA, Dmytrenko GM, Winkelmann JC, Bloch RJ (1992) Dystrophin colocalizes with β-spectrin in distinct subsarcolemmal domains in mammalian skeletal muscle. J Cell Biol 117:997–1005CrossRefPubMed
12.
go back to reference Stone MR, O’Neill A, Lovering RM, Strong J, Resneck WG, Reed PW, Toivola DM, Ursitti JA, Omary MB, Bloch RJ (2007) Absence of keratin 19 in mice causes skeletal myopathy with mitochondrial and sarcolemmal reorganization. J Cell Sci 120:3999–4008CrossRefPubMed Stone MR, O’Neill A, Lovering RM, Strong J, Resneck WG, Reed PW, Toivola DM, Ursitti JA, Omary MB, Bloch RJ (2007) Absence of keratin 19 in mice causes skeletal myopathy with mitochondrial and sarcolemmal reorganization. J Cell Sci 120:3999–4008CrossRefPubMed
13.
go back to reference Williams MW, Bloch RJ (1999) Extensive but coordinated reorganization of the membrane skeleton in myofibers of dystrophic (mdx) mice. J Cell Biol 144:1259–1270CrossRefPubMedCentralPubMed Williams MW, Bloch RJ (1999) Extensive but coordinated reorganization of the membrane skeleton in myofibers of dystrophic (mdx) mice. J Cell Biol 144:1259–1270CrossRefPubMedCentralPubMed
14.
go back to reference Williams MW, Resneck WG, Bloch RJ (2000) Membrane skeleton of innervated and denervated fast- and slow-twitch muscle. Muscle Nerve 23:590–599CrossRefPubMed Williams MW, Resneck WG, Bloch RJ (2000) Membrane skeleton of innervated and denervated fast- and slow-twitch muscle. Muscle Nerve 23:590–599CrossRefPubMed
15.
go back to reference Williams MW, Resneck WG, Kaysser T, Ursitti JA, Birkenmeier CS, Barker JE, Bloch RJ (2001) Na, K-ATPase in skeletal muscle: two populations of β-spectrin control localization in the sarcolemma but not partitioning between the sarcolemma and the transverse tubules. J Cell Sci 114:751–762PubMed Williams MW, Resneck WG, Kaysser T, Ursitti JA, Birkenmeier CS, Barker JE, Bloch RJ (2001) Na, K-ATPase in skeletal muscle: two populations of β-spectrin control localization in the sarcolemma but not partitioning between the sarcolemma and the transverse tubules. J Cell Sci 114:751–762PubMed
16.
go back to reference Pierobon-Bormioli S (1981) Transverse sarcomere filamentous systems: “Z- and M-cables”. J Muscle Res Cell Motil 2:401–413CrossRef Pierobon-Bormioli S (1981) Transverse sarcomere filamentous systems: “Z- and M-cables”. J Muscle Res Cell Motil 2:401–413CrossRef
17.
go back to reference Bard F, Franzini-Armstrong C (1991) Extra actin filaments at the periphery of skeletal muscle myofibrils. Tissue Cell 23:191–197CrossRefPubMed Bard F, Franzini-Armstrong C (1991) Extra actin filaments at the periphery of skeletal muscle myofibrils. Tissue Cell 23:191–197CrossRefPubMed
18.
go back to reference Hijikata T, Murakami T, Imamura M, Fujimaki N, Ishikawa H (1999) Plectin is a linker of intermediate filaments to Z-discs in skeletal muscle fibers. J Cell Sci 112:867–876PubMed Hijikata T, Murakami T, Imamura M, Fujimaki N, Ishikawa H (1999) Plectin is a linker of intermediate filaments to Z-discs in skeletal muscle fibers. J Cell Sci 112:867–876PubMed
19.
go back to reference Street SF (1983) Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 114:346–364CrossRefPubMed Street SF (1983) Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 114:346–364CrossRefPubMed
20.
go back to reference Garamvölgyi N (1965) Inter-Z bridges in the flight muscle of the bee. J Ultrastruct Res 13:435–443CrossRefPubMed Garamvölgyi N (1965) Inter-Z bridges in the flight muscle of the bee. J Ultrastruct Res 13:435–443CrossRefPubMed
21.
go back to reference 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 96:562–570CrossRefPubMed 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 96:562–570CrossRefPubMed
22.
go back to reference Shear CR, Bloch RJ (1985) Vinculin in subsarcolemmal densities in chicken skeletal muscle: localization and relationship to intracellular and extracellular structures. J Cell Biol 101:240–256CrossRefPubMed Shear CR, Bloch RJ (1985) Vinculin in subsarcolemmal densities in chicken skeletal muscle: localization and relationship to intracellular and extracellular structures. J Cell Biol 101:240–256CrossRefPubMed
23.
go back to reference Hijikata T, Murakami T, Ishikawa H, Yorifuji H (2003) Plectin tethers desmin intermediate filaments onto subsarcolemmal dense plaques containing dystrophin and vinculin. Histochem Cell Biol 119:109–123PubMed Hijikata T, Murakami T, Ishikawa H, Yorifuji H (2003) Plectin tethers desmin intermediate filaments onto subsarcolemmal dense plaques containing dystrophin and vinculin. Histochem Cell Biol 119:109–123PubMed
24.
go back to reference Rybakova IN, Patel JR, Ervasti JM (2000) The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J Cell Biol 150:1209–1214CrossRefPubMedCentralPubMed Rybakova IN, Patel JR, Ervasti JM (2000) The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J Cell Biol 150:1209–1214CrossRefPubMedCentralPubMed
25.
go back to reference Hijikata T, Nakamura A, Isokawa K, Imamura M, Yuasa K, Ishikawa R, Kohama K, Takeda S, Yorifuji H (2008) Plectin 1 links intermediate filaments to costameric sarcolemma through β-synemin, α-dystrobrevin and actin. J Cell Sci 121:2062–2074CrossRefPubMed Hijikata T, Nakamura A, Isokawa K, Imamura M, Yuasa K, Ishikawa R, Kohama K, Takeda S, Yorifuji H (2008) Plectin 1 links intermediate filaments to costameric sarcolemma through β-synemin, α-dystrobrevin and actin. J Cell Sci 121:2062–2074CrossRefPubMed
26.
go back to reference Yorifuji H, Hirokawa N (1989) Cytoskeletal architecture of neuromuscular junction: localization of vinculin. J Electron Microsc Tech 12:160–171CrossRefPubMed Yorifuji H, Hirokawa N (1989) Cytoskeletal architecture of neuromuscular junction: localization of vinculin. J Electron Microsc Tech 12:160–171CrossRefPubMed
27.
go back to reference Stedman HH, Sweeney HL, Shrager JB, Maguire HC, Panettieri RA, Petrof B, Narusawa M, Leferovich JM, Sladky JT, Kelly AM (1991) The mdx mouse diaphragm reproduces the degenerative changes of Duchene muscular dystrophy. Nature 352:536–539CrossRefPubMed Stedman HH, Sweeney HL, Shrager JB, Maguire HC, Panettieri RA, Petrof B, Narusawa M, Leferovich JM, Sladky JT, Kelly AM (1991) The mdx mouse diaphragm reproduces the degenerative changes of Duchene muscular dystrophy. Nature 352:536–539CrossRefPubMed
28.
go back to reference Ishizaki M, Suga T, Kimura E, Shiota T, Kawano R, Uchida Y, Uchino K, Yamashita S, Maeda Y, Uchino M (2008) Mdx respiratory impairment following fibrosis of the diaphragm. Neuromuscul Disord 18:342–348CrossRefPubMed Ishizaki M, Suga T, Kimura E, Shiota T, Kawano R, Uchida Y, Uchino K, Yamashita S, Maeda Y, Uchino M (2008) Mdx respiratory impairment following fibrosis of the diaphragm. Neuromuscul Disord 18:342–348CrossRefPubMed
30.
go back to reference Cohen CM, Tyler JM, Branton D (1980) Spectrin-actin associations studied by electron microscopy of shadowed preparations. Cell 21:875–883CrossRefPubMed Cohen CM, Tyler JM, Branton D (1980) Spectrin-actin associations studied by electron microscopy of shadowed preparations. Cell 21:875–883CrossRefPubMed
31.
go back to reference Pons F, Augier N, Heilig R, Léger J, Mornet D, Léger JJ (1990) Isolated dystrophin molecules as seen by electron microscopy. Proc Natl Acad Sci USA 87:7851–7855CrossRefPubMedCentralPubMed Pons F, Augier N, Heilig R, Léger J, Mornet D, Léger JJ (1990) Isolated dystrophin molecules as seen by electron microscopy. Proc Natl Acad Sci USA 87:7851–7855CrossRefPubMedCentralPubMed
32.
go back to reference Lazarides E (1980) Intermediate filaments as mechanical integrators of cellular space. Nature 283:249–256CrossRefPubMed Lazarides E (1980) Intermediate filaments as mechanical integrators of cellular space. Nature 283:249–256CrossRefPubMed
33.
go back to reference Straub V, Bittner RE, Léger JJ, Voit T (1992) Direct visualization of the dystrophin network on skeletal muscle fiber membrane. J Cell Biol 119:1183–1191CrossRefPubMed Straub V, Bittner RE, Léger JJ, Voit T (1992) Direct visualization of the dystrophin network on skeletal muscle fiber membrane. J Cell Biol 119:1183–1191CrossRefPubMed
35.
go back to reference Cullen MJ, Walsh J, Nicholson LVB, Harris JB (1990) Ultrastructural localization of dystrophin in human muscle by using gold immunolabelling. Proc R Soc Lond B Biol Sci 240:197–210CrossRefPubMed Cullen MJ, Walsh J, Nicholson LVB, Harris JB (1990) Ultrastructural localization of dystrophin in human muscle by using gold immunolabelling. Proc R Soc Lond B Biol Sci 240:197–210CrossRefPubMed
36.
go back to reference Harris JB, Cullen MJ (1992) Ultrastructural localization and the possible role of dystrophin. In: Kalkulas BA, Howell JM, Roses AD (eds) Duchenne muscular dystrophy: animal models and genetic manipulation. Raven Press, New York, pp 19–40 Harris JB, Cullen MJ (1992) Ultrastructural localization and the possible role of dystrophin. In: Kalkulas BA, Howell JM, Roses AD (eds) Duchenne muscular dystrophy: animal models and genetic manipulation. Raven Press, New York, pp 19–40
37.
go back to reference Stevenson SA, Cullen MJ, Rothery S, Coppen SR (2005) High-resolution en-face visualization of the cardiomyocyte plasma membrane reveals distinctive distributions of spectrin and dystrophin. Eur J Cell Biol 84:961–971CrossRefPubMed Stevenson SA, Cullen MJ, Rothery S, Coppen SR (2005) High-resolution en-face visualization of the cardiomyocyte plasma membrane reveals distinctive distributions of spectrin and dystrophin. Eur J Cell Biol 84:961–971CrossRefPubMed
38.
go back to reference Jung D, Yang B, Meyer J, Chamberlain JS, Campbell KP (1995) Identification and characterization of the dystrophin anchoring site on β-dystroglycan. J Biol Chem 270:27305–27310CrossRefPubMed Jung D, Yang B, Meyer J, Chamberlain JS, Campbell KP (1995) Identification and characterization of the dystrophin anchoring site on β-dystroglycan. J Biol Chem 270:27305–27310CrossRefPubMed
39.
go back to reference Ervasti JM, Campbell KP (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122:809–823CrossRefPubMed Ervasti JM, Campbell KP (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122:809–823CrossRefPubMed
40.
go back to reference Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to extracellular matrix. Nature 355:696–702CrossRefPubMed Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to extracellular matrix. Nature 355:696–702CrossRefPubMed
41.
go back to reference Hoffman EP, Kunkel LM (1989) Dystrophin abnormalities in Duchenne/Becker muscular dystrophy. Neuron 2:1019–1029CrossRefPubMed Hoffman EP, Kunkel LM (1989) Dystrophin abnormalities in Duchenne/Becker muscular dystrophy. Neuron 2:1019–1029CrossRefPubMed
42.
go back to reference Campbell KP (1995) Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 80:675–679CrossRefPubMed Campbell KP (1995) Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 80:675–679CrossRefPubMed
43.
go back to reference O’Brien KF, Kunkel LM (2001) Dystrophin and muscular dystrophy: past, present, and future. Mol Genet Metab 74:75–88CrossRefPubMed O’Brien KF, Kunkel LM (2001) Dystrophin and muscular dystrophy: past, present, and future. Mol Genet Metab 74:75–88CrossRefPubMed
44.
go back to reference Law DJ, Allen DL, Tidball JG (1994) Talin, vinculin and DRP (utrophin) concentrations are increased at mdx myotendinous junctions following onset of necrosis. J Cell Sci 107:1477–1483PubMed Law DJ, Allen DL, Tidball JG (1994) Talin, vinculin and DRP (utrophin) concentrations are increased at mdx myotendinous junctions following onset of necrosis. J Cell Sci 107:1477–1483PubMed
45.
go back to reference Bellin RM, Huiatt TW, Critchley DR, Robson RM (2001) Synemin may function to directly link muscle cell intermediate filaments to both myofibrillar Z-lines and costameres. J Biol Chem 276:32330–32337CrossRefPubMed Bellin RM, Huiatt TW, Critchley DR, Robson RM (2001) Synemin may function to directly link muscle cell intermediate filaments to both myofibrillar Z-lines and costameres. J Biol Chem 276:32330–32337CrossRefPubMed
Metadata
Title
Filamentous structures in skeletal muscle: anchors for the subsarcolemmal space
Authors
Astrid Feinisa Khairani
Yuki Tajika
Maiko Takahashi
Hitoshi Ueno
Tohru Murakami
Arifin Soenggono
Hiroshi Yorifuji
Publication date
01-03-2015
Publisher
Springer Japan
Published in
Medical Molecular Morphology / Issue 1/2015
Print ISSN: 1860-1480
Electronic ISSN: 1860-1499
DOI
https://doi.org/10.1007/s00795-014-0070-3

Other articles of this Issue 1/2015

Medical Molecular Morphology 1/2015 Go to the issue