Myopathic changes in murine skeletal muscle lacking synemin

American Journal of Physiology - Cell Physiology

Volumn 308, Issue 6, 2015, Pages C448-C462

  García Pelagio, Karla P ^a   Muriel, Joaquin ^a   O’Neill, Andrea ^a   Desmond, Patrick F ^a   Lovering, Richard M ^a   Lund, Linda ^b   Bond, Meredith ^c   Bloch, Robert J ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BALTIMORE   (United States)

^c CLEVELAND STATE UNIVERSITY   (United States)

Author keywords

Biomechanical properties; Costameres; Cytoskeleton; Desmin; Elastimetry

Indexed keywords

ALPHA ACTININ; ALPHA SYNEMIN; BETA GALACTOSIDASE; BETA SYNEMIN; DESMIN; DYSTROPHIN; INTERMEDIATE FILAMENT PROTEIN; OBSCURIN; SYNEMIN; UNCLASSIFIED DRUG; SYNEMIN PROTEIN, MOUSE;

ACTIN MYOSIN INTERACTION; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CONTROLLED STUDY; COSTAMERE; FAST MUSCLE; FATIGUE; GENOTYPE; HOMOLOGOUS RECOMBINATION; IMMUNOFLUORESCENCE; MALE; MORPHOMETRICS; MOUSE; MUSCLE CELL; MUSCLE FIBRIL; MUSCLE INJURY; MUSCLE ISOMETRIC CONTRACTION; MUSCLE MASS; MUSCLE STRENGTH; MUSCLE TETANIC CONTRACTION; MUSCLE TWITCH; MYOPATHY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SARCOLEMMA; SKELETAL MUSCLE; TREADMILL; TREADMILL EXERCISE; WESTERN BLOTTING; ANIMAL; BIOMECHANICS; C57BL MOUSE; DEFICIENCY; FAST MUSCLE FIBER; GENETICS; KNOCKOUT MOUSE; METABOLISM; MUSCLE FATIGUE; MUSCULAR DISEASES; PATHOLOGY; PATHOPHYSIOLOGY; RUNNING;

MURINAE; MUS;

ANIMALS; BIOMECHANICAL PHENOMENA; COSTAMERES; GENOTYPE; INTERMEDIATE FILAMENT PROTEINS; ISOMETRIC CONTRACTION; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE FATIGUE; MUSCLE FIBERS, FAST-TWITCH; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DISEASES; PHENOTYPE; RUNNING; SARCOLEMMA;

EID: 84924911606     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00331.2014     Document Type: Article

References (96)

1. Agbulut O, Li Z, Perie S. Lack of desmin results in abortive muscle regeneration and modifications in synaptic structure. Cell Motil Cytoskeleton49: 51–66, 2001.
2. Anastasi G, Cutroneo G, Santoro G, Arco A, Rizzo G, Bramanti P, Rinaldi C, Sidoti A, Amato A, Favaloro A. Costameric proteins in human skeletal muscle during muscular inactivity. J Anat213: 284–295, 2008.
3. Becker B, Bellin RM, Sernett SW, Huiatt TW, Robson RM. Synemin contains the rod domain of intermediate filaments. Biochem Biophys Res Commun213: 796–802, 1995.
4. Bellin R, Huiatt W, Critchley R, Robson M. Synemin may function to directly link muscle cell intermediate filaments to both myofibrillar Z-lines and costameres. J Biol Chem276: 32330–32337, 2001.
5. Bellin RM, Sernett SW, Becker B, Ip W, Huiatt TW, Robson RM. Molecular characteristics and interactions of the intermediate filament protein synemin. Interactions with alpha-actinin may anchor synemincontaining heterofilaments. J Biol Chem274: 29493–29499, 1999.
6. Bhat HF, Adams ME, Khandayc FA. Syntrophin proteins as Santa Claus: role(s) in cell signal transduction. Cell Mol Life Sci70: 2533–2554, 2013.
7. Bhosle RC, Michele D, Campbell KP, Li Z, Robson RM. Interactions of intermediate filament protein synemin with dystrophin and utrophin. Biochem Biophys Res Commun346: 768–777, 2006.
8. Bilak SR, Sernett SW, Bilak MM, Bellin RM, Stromer MH, Huiatt TW, Robson RM. Properties of the novel intermediate filament protein synemin and its identification in mammalian muscle. Arch Biochem Biophys355: 63–76, 1998.
9. Blaauw B, Schiaffino S, Reggiani C. Mechanisms modulating skeletal muscle phenotype. Compr Physiol13: 1645–1687, 2013.
10. Blake DJ, Martin-Rendon E. Intermediate filaments and the function of the dystrophin-protein complex. Trends Cardiovasc Med12: 224–228, 2002.
11. Bloch RJ, Capetanaki Y, O’Neill A, Reed P, Williams M, Resneck W, Porter N, Ursitti J. Costameres: repeating structures at the sarcolemma of skeletal muscle. Clin Orthop Relat Res403: S203–S210, 2002.
12. Bloch RJ, González-Serratos H. Lateral force transmission across costameres in skeletal muscle. Exerc Sport Sci Rev31: 73–78, 2003.
13. Briguet A, Courdier-Fruh I, Foster M, Meier T, Magyar JP. Histological parameters for the quantitative assessment of muscular dystrophy in the mdx mouse. Neuromuscul Disord14: 675–682, 2004.
14. Brooks NE, Myburgh KH. Skeletal muscle wasting with disuse atrophy is multi-dimensional: the response and interaction of myonuclei, satellite cells and signaling pathways. Front Physiol5: 99, 2014.
15. Campbell K, Stull T. Skeletal muscle basement membrane-sarcolemmacytoskeleton interaction minireview series. J Biol Chem278: 12599–12600, 2003.
16. Capetanaki Y, Bloch RJ, Kouloumenta A, Mavroidis M, Psarras S. Muscle intermediate filaments and their links to membranes and membranous organelles. Exp Cell Res313: 2063–2076, 2007.
17. Carlsson L, Li Z, Paulin D, Price M, Breckler J, Robson R, Wiche G, Thornell LE. Differences in the distribution of synemin, paranemin, and plectin in skeletal muscles of wild-type and desmin knock-out mice. Histochem Cell Biol114: 39–47, 2000.
18. Coulombe PA, Bousquet O, Ma L, Yamada S, Wirtz D. The “ins” and “outs” of IF organization. Trends Cell Biol10: 420–428, 2000.
19. Dalakas M, Park KY, Semino-Mora C, Lee HS, Sivakumar K, Goldfarb L. Desmin myopathy, a skeletal myopathy with cardiomyopathy caused by mutations in the desmin gene. N Engl J Med342: 770–780, 2000.
20. De Bleecker JL, Ertl BB, Engel AG. Patterns of abnormal protein expression in target formation and unstructured cores. Neuromuscul Disord6: 339–349, 1996.
21. Diviani D, Maric D, Pérez López I, Cavin S, Del Vescovo CD. A-kinase anchoring proteins: molecular regulators of the cardiac stress response. Biochim Biophys Acta1833: 901–908, 2013.
22. Dulhunty AF, Franzini-Armstrong C. The relative contribution of the folds and caveolae to the surface membrane of frog skeletal muscle fibers at different sarcomere length. J Physiol250: 513–539, 1975.
23. Durbeej M, Campbell KP. Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr Opin Genet Dev12: 349–361, 2002.
24. Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab17: 164–184, 2013.
25. Eriksson JE, Dechat T, Grin B, Helfand B, Mendez M, Pallari HM, Goldman R. Introducing intermediate filaments: from discovery to disease. J Clin Invest119: 1763–1771, 2009.
26. Ervasti J, Campbell K. Membrane organization of the dystrophinglycoprotein complex. Cell66: 1121–1131, 1991.
27. Ervasti J. Costameres: the Achilles’ heel of herculean muscle. J Biol Chem278: 13591–13594, 2003.
28. Frimel TN, Walter GA, Gibbs JD, Gaidosh GS, Vandenborne K. Noninvasive monitoring of muscle damage during reloading following limb disuse. Muscle Nerve32: 605–612, 2005.
29. Garcia-Pelagio K, Bloch R, Ortega A, Gonzalez-Serratos H. Biomechanics of the sarcolemma and costameres in single skeletal muscle fibers from normal and dystrophin-null mice. J Muscle Res Cell Motil31: 323–336, 2011.
30. Garcia-Pelagio K, Bloch R, Ortega A, Gonzalez-Serratos H. Elastic properties of the sarcolemma-costamere complex of muscle cells in normal mice. AIP Conf Proc854: 51–53, 2006.
31. García-Pelagio K, Muriel J, O’Neill A, Desmond P, Lovering R, Lund L, Bond M, Bloch R. Characterization of skeletal muscle in the synemin knock-out mouse. AIP Conf Proc1626: 67, 2014.
32. Goebel HH. Congenital myopathies with inclusion bodies: a brief review. Neuromuscul Disord8: 162–168, 1998.
33. Goldman R, Khuon S, Chou Y, Opal P, Steinert P. The function of intermediate filaments in cell shape and cytoskeletal integrity. J Cell Biol134: 971–983, 1996.
34. Goto H, Inagaki M. New insights into roles of intermediate filament phosphorylation and progeria pathogenesis. IUBMB Life 2014 Mar 23 [Epub ahead of print].
35. Granger BL, Lazarides E. Synemin: a new high molecular weight protein associated with desmin and vimentin filaments in muscle. Cell22: 727–738, 1980.
36. Helfand B, Chang L, Goldman R. Intermediate filaments are dynamic and motile elements of cellular architecture. J Cell Sci117: 133–141, 2004.
37. Herrmann H, Strelkov SV, Burkhard P, Aebi U. Intermediate filaments: primary determinants of cell architecture and plasticity. J Clin Invest119: 1772–1783, 2009.
38. Hesse M, Franz T, Tamai Y, Taketo MM, Magin TM. Targeted deletion of keratins 18 and 19 leads to trophoglast fragility and early embryonic lethality. EMBO J19: 5060–5070, 2000.
39. Hesse M, Magin T, Weber K. Genes for intermediate filament proteins and the draft sequence of the human genome: novel keratin genes and a surprisingly high number of pseudogenes related to keratin genes 8 and 18. J Cell Sci114: 2569–2575, 2001.
40. Hijikata T, Nakamura A, Isokawa K, Imamura M, Yuasa K, Ishikawa R, Kohama K, Takeda S, Yorifuji H. Plectin 1 links intermediate filaments to costameric sarcolemma through beta-synemin, alpha-dystrobrevin and actin. J Cell Sci121: 2062–2074, 2008.
41. Hoffman EP, Brown R, Kunkel L. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell51: 919–928, 1987.
42. Holland A, Carberry S, Ohlendieck K. Proteomics of the dystrophinglycoprotein complex and dystrophinopathy. Curr Protein Pept Sci14: 680–697, 2013.
43. Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature355: 696–702, 1992.
44. Janmey P, Euteneuer U, Traub P, Schliwa M. Viscoelastic properties of vimentin compared with other filamentous biopolymer networks. J Cell Biol113: 155–160, 1991.
45. Jing R, Pizzolato G, Robson RM, Gabbiani G, Skalli O. Intermediate filament protein synemin is present in human reactive and malignant astrocytes and associates with ruffled membranes in astrocytoma cells. Glia50: 107–120, 2005.
46. Kontrogianni-Konstantopoulos A, Jones EM, Van Rossum DB, Bloch RJ. Obscurin is a ligand for small ankyrin 1 in skeletal muscle. Mol Biol Cell14: 1138–1148, 2003.
47. Kreplak L, Bär H, Leterrier JF, Hermann H, Aebi U. Exploring the mechanical behavior of single intermediate filaments. J Mol Biol354: 569–577, 2005.
48. Lapidos KA, Kakkar R, McNally EM. The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ Res94: 1023–1031, 2004.
49. Lazarides E, Hubbard B. Immunological characterization of the subunit of the 100 A filaments from muscle cells. Proc Natl Acad Sci USA73: 4344–4348, 1976.
50. Lepinoux-Chambaud C, Eyer J. Review on intermediate filaments of the nervous system and their pathological alterations. Histochem Cell Biol140: 13–22, 2013.
51. Li Z, Colucci-Guyon E, Pincon-Raymond M, Mericshay M, Pourin S, Paulin D, Babinet C. Cardiovascular lesions and skeletal myopathy in mice lacking desmin. Dev Biol175, 362–366, 1996.
52. Lou J, Bi W, Zhao Y, Liu S, Zheng J, Yan C. Muscle injury induced by different types of contractions in dystrophic mdx mice. J Muscle Res Cell Motil32: 411–419, 2012.
53. Lovering R, De Deyne P. Contractile function, sarcolemma integrity and the loss of dystrophin after skeletal muscle eccentric contraction-induced injury. Am J Physiol Cell Physiol286: C230–C238, 2004.
54. Lovering R, O’Neill A, Muriel J, Prosser B, Strong J, Bloch RJ. Physiology, structure, and susceptibility to injury of skeletal muscle in mice lacking keratin 19-based and desmin-based intermediate filaments. Am J Physiol Cell Physiol300: C803–C813, 2011.
55. Luna G, Lewis GP, Banna CD, Skalli O, Fisher SK. Expression profiles of nestin and synemin in reactive astrocytes and Müller cells following retinal injury: a comparison with glial fibrillar acidic protein and vimentin. Mol Vis16: 2511–2523, 2010.
56. Lund M, Kerr J, Lupinetti J, Zhang Y, Russell M, Bloch R, Bond M. Synemin isoforms differentially organize cell junctions and desmin filaments in neonatal cardiomyocytes. FASEB J1: 137–148, 2011.
57. Manal K, Roberts D, Buchanan T. Optimal pennation angle of the primary ankle plantar and dorsiflexors: variations with sex, contraction intensity, and limb. J Appl Biomech22: 255–263, 2006.
58. McConnachie G, Langeberg LK, Scott JD. AKAP signaling complexes: getting to the heart of matter. Trends Mol Med12: 317–323, 2006.
59. Mizuno Y, Thompson TG, Guyon JR, Lidov HG, Brosius M, Imamura M, Ozawa E, Watkins SC, Kunkel LM. Desmuslin, an intermediate filament protein that interacts with alpha-dystrobrevin and desmin. Proc Natl Acad Sci USA98: 6156–6161, 2001.
60. Nigro V, Savarese M. Genetic basis of limb-girdle muscular dystrophies: the 2014 update. Acta Myol33: 1–12, 2014.
61. Noetzel E, Rose M, Sevinc E, Hilgers RD, Hartmann A, Naami A, Knüchel R, Dahl E. Intermediate filament dynamics and breast cancer: aberrant promoter methylation of the synemin gene is associated with early tumor relapse. Oncogene29: 4814–4825, 2010.
62. O’Neill A, Williams M, Resneck W, Milner D, Capetanaki Y, Bloch RJ. Sarcolemmal organization in skeletal muscle lacking desmin: evidence for cytokeratins associated with the membrane skeleton at costameres. Mol Biol Cell13: 2347–2359, 2002.
63. Ozawa E. From dystrophinopathy to sarcoglycanopathy: evolution of a concept of muscular dystrophy. Muscle Nerve21: 421–438, 1998.
64. Pan X, Hobbs RP, Coulombe PA. The expanding significance of keratin intermediate filaments in normal and diseased epithelia. Curr Opin Cell Biol25: 47–56, 2013.
65. Paramio J, Jorcano L. Beyond structure: do intermediate filaments modulate cell signaling? Bioassays24: 836–844, 2002.
66. Pardo JV, Siliciano J, Craig S. A vinculin-containing cortical lattice in skeletal muscle: transverse lattice elements (“costameres”) mark sites of attachment between myofibrils and sarcolemma. Proc Natl Acad Sci USA80: 1008–1012, 1983.
67. Patel TJ, Lieber RL. Force transmission in skeletal muscle: from actomyosin to external tendons. Exerc Sport Sci Rev25: 321–363, 1997.
68. Paulin D, Li Zhenlin. Desmin: a major intermediate filament protein essential for the structural integrity and function of muscle. Exp Cell Res301: 1–7, 2004.
69. Pekny T, Faiz M, Wilhelmsson U, Curtis MA, Matej R, Skalli O, Pekny M. Synemin is expressed in reactive astrocytes and Rosenthal fibers in Alexander disease. APMIS122: 76–80, 2014.
70. Pitre A, Davis N, Paul M, Orr AW, Skalli O. Synemin promotes AKT-dependent glioblastoma cell proliferation by antagonizing PP2. Mol Biol Cell23: 1243–1253, 2012.
71. Porter GA, Dmytrenko GM, Winkelmann JC, Bloch RJ. Dystrophin colocalizes with beta-spectrin in distinct subsarcolemmal domains in mammalian skeletal muscle. J Cell Biol117: 997–1005, 1992.
72. Pratt SJ, Shah SB, Ward CW, Kerr JP, Stains JP, Lovering RM. Recovery of altered neuromuscular junction morphology and muscle function in mdx mice after injury. Cell Mol Life Sci72: 153–164, 2015.
73. Price MG, Lazarides E. Expression of intermediate filament/associated proteins paranemin and synemin in chicken development. J Cell Biol97: 1860–1874, 1983.
74. Rando TA. The dystrophin-glycoprotein complex, cellular signaling, and the regulation of cell survival in the muscular dystrophies. Muscle Nerve24: 1575–1594, 2001.
75. Rapoport S. Mechanical properties of the sarcolemma and myoplasm in frog muscle as a function of sarcomere length. J Gen Physiol59: 559–585, 1972.
76. Reed PW, Mathews KD, Mills KA, Bloch RJ. The sarcolemma in the Large(myd) mouse. Muscle Nerve30: 585–595, 2004.
77. Roche JA, Lovering RM, Roche R, Ru L, Reed PW, Bloch R. Extensive mononuclear infiltration and myogenesis characterize recovery of dysferlin-null skeletal muscle from contraction induced injuries. Am J Physiol Cell Physiol298: C298–C312, 2010.
78. Roche JA, Ru LW, Bloch RJ. Distinct effects of contraction-induced injury in vivo on four different murine models of dysferlinopathy. J Biomed Biotechnol2012: 13403, 2012.
79. Rudolf R, Khan MM, Lustrino D, Labeit S, Kettelhut IC, Navegantes LC. Alterations of cAMP-dependent signaling in dystrophic skeletal muscle. Front Physiol4: 290, 2013.
80. Rusell AP. Molecular regulation of skeletal muscle mass. Clin Exp Pharmacol Physiol37: 378–384, 2009.
81. Russell MA, Lund LM, Haber R, McKeegan K, Cianciola N, Bond M. The intermediate filament protein, synemin, is an AKAP in the heart. Arch Biochem Biophys456: 204–215, 2006.
82. Rybakova I, Patel J, Ervasti J. The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J Cell Biol150: 1209–1214, 2000.
83. Sandoval IV, Colaco CA, Lazarides E. Purification of the intermediate filament-associated protein, synemin, from chicken smooth muscle. Studies on its physicochemical properties, interaction with desmin, and phosphorylation. J Biol Chem258: 2568–2576, 1983.
84. Schmitt-Graeff A, Jing R, Nitschke R, Desmoulière A, Skalli O. Synemin expression is widespread in liver fibrosis and is induced in proliferating and malignant biliary epithelial cells. Hum Pathol37: 1200–1210, 2006.
85. Sejersen T, Lendahl U. Transient expression of the intermediate filament nestin during skeletal muscle development. J Cell Sci106: 1291–1300, 1993.
86. Shah SB, Davis J, Weisleder N, Kostavassili I, McCulloch AD, Raiston E, Capetanaki Y, Lieber RL. Structural and functional roles of desmin in mouse skeletal muscle during passive deformation. Biophys J86: 2993–3008, 2004.
87. Shear CR, Bloch RJ. Vinculin in subsarcolemmal densities in chicken skeletal muscle: localization and relationship to intracellular and extracellular structures. J Cell Biol101: 240–256, 1985.
88. Stone MR, O’Neill A, Lovering RM, Strong J, Resneck WG, Reed PW, Toivola DM, Ursitti JA, Omary MB, Bloch RJ. Absence of keratin 19 in mice causes skeletal myopathy with mitochondrial and sarcolemmal reorganization. J Cell Sci120: 3999–4008, 2007.
89. Street SE. Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol114: 346–364, 1983.
90. Sun N, Critchley D, Paulin D, Li Z, Robson R. Human alpha-synemin interacts directly with vinculin and metavinculin. Biochem J409: 657–667, 2008.
91. Sun N, Critchley D, Paulin D, Li Z, Robson R. Identification of a repeated domain within mammalian alpha-synemin that interacts directly with talin. Exp Cell Res314: 1839–1849, 2008.
92. Ursitti JA, Lee PC, Resneck WG, McNally MM, Bowman AL, O’Neill A, Stone MR, Bloch RJ. Cloning and characterization of cytokeratins 8 and 19 in adult rat striated muscle. Interaction with the dystrophin glycoprotein complex. J Biol Chem279: 41830–41838, 2004.
93. Williams W, Bloch RJ. Differential distribution of dystrophin, and _-spectrin at the sarcolemma of fast twitch skeletal muscle fibers. J Muscle Res Cell Motil20: 383–393, 1999.
94. Yang J, Dominguez B, de Winter F, Gould T, Eriksson J, Lee K. Nestin negatively regulates postsynaptic differentiation of the neuromuscular synapse. Nat Neurosci14: 324–330, 2011.
95. Yurchenco PD, Cheng YS, Campbell K, Li S. Loss of basement membrane, receptor and cytoskeletal lattices in a laminin-deficient muscular dystrophy. J Cell Sci117: 735–742, 2004.
96. Zhenlin L, Parlakian A, Coletti D, Alonso-Martin S, Hourdé C, Joanne P, Gao-Li J, Blanc J, Ferry A, Paulin D, Xue Z, Agbulut O. Synemin acts as a regulator of signaling molecules in skeletal muscle hypertrophy. J Cell Sci127: 4589–4601, 2014.