Posttranslational modifications of desmin and their implication in biological processes and pathologies

Histochemistry and Cell Biology

Volumn 141, Issue 1, 2014, Pages 1-16

  Winter, Daniel L ^a   Paulin, Denise ^a   Mericskay, Mathias ^a   Li, Zhenlin ^a  

^a SORBONNE UNIVERSITÉ   (France)

Author keywords

ADP ribosylation; Intermediate filaments; Muscle; Myopathy; Phosphorylation; Ubiquitylation

Indexed keywords

DESMIN; ENZYME;

ADENOSINE DIPHOSPHATE RIBOSYLATION; BIOLOGICAL PHENOMENA AND FUNCTIONS CONCERNING THE ENTIRE ORGANISM; CELL DIVISION; HUMAN; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; UBIQUITINATION; ANIMAL; BIOSYNTHESIS; CARDIOMYOPATHY; CHICKEN; CYTOLOGY; GENETICS; HAMSTER; INTERMEDIATE FILAMENT; METABOLISM; MOUSE; MUSCLE; MUSCLE DISEASE; MUSCULAR DYSTROPHY;

ANIMALS; CARDIOMYOPATHIES; CHICKENS; CRICETINAE; DESMIN; HUMANS; INTERMEDIATE FILAMENTS; MICE; MUSCLE CELLS; MUSCLE CONTRACTION; MUSCLES; MUSCULAR DISEASES; MUSCULAR DYSTROPHIES; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84892724559     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-013-1148-z     Document Type: Review

References (143)

1. Ahmed EK, Rogowska-Wrzesinska A, Roepstorff P., Bulteau AL, Friguet B. (2010) Protein modification and replicative senescence of WI-38 human embryonic fibroblasts. Aging Cell 9(2):252-272. doi:10.1111/j.1474-9726.2010.00555.x
2. Attaix D, Ventadour S, Codran A., Bechet D, Taillandier D, Combaret L. (2005) The ubiquitin-proteasome system and skeletal muscle wasting. Essays Biochem 41:173-186. doi:10.1042/EB0410173
3. Bar H, Mucke N, Katus H.A., Aebi U., Herrmann H. (2007) Assembly defects of desmin disease mutants carrying deletions in the alpha-helical rod domain are rescued by wild type protein. J Struct Biol 158(1):107-115. doi:10.1016/j.jsb.2006.10.029
4. Bar H, Schopferer M, Sharma S., Hochstein B, Mucke N, Herrmann H., Willenbacher N. (2010) Mutations in desmin's carboxy-terminal "tail," domain severely modify filament and network mechanics. J Mol Biol 397(5):1188-1198. doi:10.1016/j.jmb.2010.02.024
5. 2+. Biochim Biophys Acta 1134(3):233-241
6. Barany M, Polyak E, Barany K. (1992b) Protein phosphorylation during the contraction-relaxation-contraction cycle of arterial smooth muscle. Arch Biochem Biophys 294(2):571-578
7. Berdeaux R, Stewart R. (2012) cAMP signaling in skeletal muscle adaptation: hypertrophy, metabolism, and regeneration. Am J Physiol Endocrinol Metab 303(1):E1-E17. doi:10.1152/ajpe ndo.00555.2011
8. Birkenberger L, Ip W. (1990) Properties of the desmin tail domain: studies using synthetic peptides and antipeptide antibodies. J Cell Biol 111(5 Pt 1):2063-2075
9. Blose SH (1979) Ten-nanometer filaments and mitosis: maintenance of structural continuity in dividing endothelial cells. Proc Natl Acad Sci USA 76(7):3372-3376
10. Boehm ME, Seidler J, Hahn B., Lehmann W.D. (2012) Site-specific degree of phosphorylation in proteins measured by liquid chromatography-electrospray mass spectrometry. Proteomics 12(13):2167-2178. doi:10.1002/pmic.201100561
11. Breckler J, Lazarides E. (1982) Isolation of a new high molecular weight protein associated with desmin and vimentin filaments from avian embryonic skeletal muscle. J Cell Biol 92(3):795-806
12. Buscemi N, Foster DB, Neverova I, Van Eyk JE (2002) p21-activated kinase increases the calcium sensitivity of rat triton-skinned cardiac muscle fiber bundles via a mechanism potentially involving novel phosphorylation of troponin I. Circ Res 91(6):509-516
13. Capetanaki Y, Milner DJ, Weitzer G. (1997) Desmin in muscle formation and maintenance: knockouts and consequences. Cell Struct Funct 22(1):103-116
14. 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(10):2063-2076. doi:10.1016/j.yexcr.2007.03.033
15. Caron A, Chapon F. (1999) Desmin phosphorylation abnormalities in cytoplasmic body and desmin-related myopathies. Muscle Nerve 22(8):1122-1125
16. Caron A, Gohel C, Mollaret K., Morello R, Chapon F. (1999) Study of some components of the cytoskeleton in muscular disorders with nonspecific cytoplasmic bodies. Acta Neuropathol 97(3):267-274
17. Cartaud A, Jasmin BJ, Changeux J.P., Cartaud J. (1995) Direct involvement of a lamin-B-related (54 kDa) protein in the association of intermediate filaments with the postsynaptic membrane of the Torpedo marmorata electrocyte. J Cell Sci 108(Pt 1): 153-160
18. Cetin N, Balci-Hayta B, Gundesli H., Korkusuz P, Purali N, Talim B., Tan E, Selcen D, Erdem-Ozdamar S, Dincer P (2013) A novel desmin mutation leading to autosomal recessive limb-girdle muscular dystrophy: distinct histopathological outcomes compared with desminopathies. J Med Genet 50(7):437-443. doi:10.1136/jmedgenet-2012-101487
19. Chourbagi O, Bruston F, Carinci M., Xue Z, Vicart P, Paulin D., Agbulut O. (2011) Desmin mutations in the terminal consensus motif prevent synemin-desmin heteropolymer filament assembly. Exp Cell Res 317(6):886-897. doi:10.1016/j.yexcr.2011.01.013
20. Clemen CS, Herrmann H, Strelkov S.V., Schroder R. (2013) Desminopathies: pathology and mechanisms. Acta Neuropathol 125(1):47-75. doi:10.1007/s00401-012- 1057-6
21. Cohen S, Zhai B, Gygi S.P., Goldberg A.L. (2012) Ubiquitylation by Trim32 causes coupled loss of desmin, Z-bands, and thin filaments in muscle atrophy. J Cell Biol 198(4):575-589. doi:10.10 83/jcb.201110067
22. Coletti D, Moresi V, Adamo S., Molinaro M, Sassoon D. (2005) Tumor necrosis factor-alpha gene transfer induces cachexia and inhibits muscle regeneration. Genesis 43(3):120-128. doi:10.1002/gene.20160
23. Cooke P (1976) A filamentous cytoskeleton in vertebrate smooth muscle fibers. J Cell Biol 68(3):539-556
24. Costa ML, Escaleira R, Cataldo A., Oliveira F, Mermelstein C.S. (2004) Desmin: molecular interactions and putative functions of the muscle intermediate filament protein. Braz J Med Biol Res 37(12):1819-1830
25. Diguet N, Mallat Y, Ladouce R., Clodic G, Prola A, Tritsch E., Blanc J, Larcher JC, Delcayre C, Samuel JL, Friguet B, Bolbach G, Li Z, Mericskay M (2011) Muscle creatine kinase deficiency triggers both actin depolymerization and desmin disorganization by advanced glycation end products in dilated cardiomyopathy. J Biol Chem 286(40):35007-35019. doi:10.1074/jbc. M111.252395
26. Drexler HC, Ruhs A, Konzer A., Mendler L, Bruckskotten M, Looso M., Gunther S, Boettger T, Kruger M, Braun T (2012) On marathons and Sprints: an integrated quantitative proteomics and transcriptomics analysis of differences between slow and fast muscle fibers. Mol Cell Proteomics MCP 11(6):M111010801. doi:10.1074/mcp.M111.010801
27. Epstein CJ, de Asua LJ, Rozengurt E. (1975) The role of cyclic AMP in myogenesis. J Cell Physiol 86(1):83-90. doi:10.1002/jcp.1040860110
28. Eriksson JE, Dechat T, Grin B., Helfand B, Mendez M, Pallari H.M., Goldman R.D. (2009) Introducing intermediate filaments: from discovery to disease. J Clin Invest 119(7):1763-1771. doi:10.1172/JCI38339
29. Evans RM (1988) The intermediate-filament proteins vimentin and desmin are phosphorylated in specific domains. Eur J Cell Biol 46(1):152-160
30. Fardeau M, Godet-Guillain J, Tome F.M., Collin H., Gaudeau S, Boffety C, Vernant P. (1978) A new familial muscular disorder demonstrated by the intra-sarcoplasmic accumulation of a granulofilamentous material which is dense on electron microscopy (author's transl). Rev Neurol (Paris) 134(6-7):411-425
31. Fardeau M, Vicart P, Caron A., Chateau D, Chevallay M, Collin H., Chapon F, Duboc D, Eymard B, Tome FM, Dupret JM, Paulin D, Guicheney P (2000) Familial myopathy with desmin storage seen as a granulo-filamentar, electron-dense material with mutation of the alphaB-cristallin gene. Rev Neurol (Paris) 156(5):497-504
32. Foster DB, Shen LH, Kelly J, Thibault P., Van Eyk JE, Mak A.S. (2000) Phosphorylation of caldesmon by p21-activated kinase. Implications for the Ca(2+) sensitivity of smooth muscle contraction. J Biol Chem 275(3):1959-1965
33. Frosk P, Weiler T, Nylen E., Sudha T, Greenberg CR, Morgan K, Fujiwara T.M., Wrogemann K. (2002) Limb-girdle muscular dystrophy type 2H associated with mutation in TRIM32, a putative E3-ubiquitin-ligase gene. Am J Hum Genet 70(3):663-672. doi:10.1086/339083
34. Fukata Y, Amano M, Kaibuchi K. (2001) Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells. Trends Pharmacol Sci 22(1):32-39
35. Furst DO, Osborn M, Weber K. (1989) Myogenesis in the mouse embryo: differential onset of expression of myogenic proteins and the involvement of titin in myofibril assembly. J Cell Biol 109(2):517-527
36. Gannon J, Staunton L, O'Connell K, Doran P, Ohlendieck K. (2008) Phosphoproteomic analysis of aged skeletal muscle. Int J Mol Med 22(1):33-42
37. Gard DL, Lazarides E. (1982) Analysis of desmin and vimentin phos-phopeptides in cultured avian myogenic cells and their modulation by 8-bromo-adenosine 3',5'-cyclic monophosphate. Proc Natl Acad Sci USA 79(22):6912-6916
38. Geisler N, Weber K. (1988) Phosphorylation of desmin in vitro inhibits formation of intermediate filaments; identification of three kinase A sites in the aminoterminal head domain. EMBO J 7(1):15-20
39. Geisler N, Kaufmann E, Weber K. (1982) Proteinchemical characterization of three structurally distinct domains along the protofilament unit of desmin 10 nm filaments. Cell 30(1):277-286
40. Geisler N, Schunemann J, Weber K. (1992) Chemical cross-linking indicates a staggered and antiparallel protofilament of desmin intermediate filaments and characterizes one higher-level complex between protofilaments. Eur J Biochem 206(3): 841-852
41. Georgatos SD, Weber K, Geisler N., Blobel G. (1987) Binding of two desmin derivatives to the plasma membrane and the nuclear envelope of avian erythrocytes: evidence for a conserved site-specificity in intermediate filament-membrane interactions. Proc Natl Acad Sci USA 84(19):6780-6784
42. Getsios S, Huen AC, Green K.J. (2004) Working out the strength and flexibility of desmosomes. Nat Rev Mol Cell Biol 5(4):271-281. doi:10.1038/nrm1356
43. Goldfarb LG, Dalakas M.C. (2009) Tragedy in a heartbeat: malfunctioning desmin causes skeletal and cardiac muscle disease. J Clin Invest 119(7):1806-1813. doi:10.1172/JCI38027
44. Goldie KN, Wedig T, Mitra A.K., Aebi U., Herrmann H, Hoenger A. (2007) Dissecting the 3-D structure of vimentin intermediate filaments by cryo-electron tomography. J Struct Biol 158(3):378-385. doi:10.1016/j.jsb.2006.12.007
45. Goto H, Tanabe K, Manser E., Lim L, Yasui Y, Inagaki M. (2002) Phos-phorylation and reorganization of vimentin by p21-activated kinase (PAK). Genes Cells 7(2):91-97
46. Graves DJ, Huiatt TW, Zhou H, Huang H.Y., Sernett SW, Robson RM, McMahon K.K. (1997) Regulatory role of arginine-specific mono(ADP-ribosyl)transferase in muscle cells. Adv Exp Med Biol 419:305-313
47. Hahn HS, Yussman MG, Toyokawa T, Marreez Y., Barrett TJ, Hilty KC, Osinska H, Robbins J., Dorn GW 2nd (2002) Ischemic protection and myofibrillar cardiomyopathy: dose-dependent effects of in vivo deltaPKC inhibition. Circ Res 91(8):741-748
48. Hein S, Scheffold T, Schaper J. (1995) Ischemia induces early changes to cytoskeletal and contractile proteins in diseased human myocardium. J Thorac Cardiovasc Surg 110(1):89-98
49. Hengel SM, Goodlett D.R. (2012) A Review of Tandem Mass Spectrometry Characterization of Adenosine Diphosphate-Ribosylated Peptides. Int J Mass Spectrom 312:114-121. doi:10.1016/j.ijms.2011.06.003
50. Herrmann H, Aebi U. (2000) Intermediate filaments and their associates: multi-talented structural elements specifying cytoarchitecture and cytodynamics. Curr Opin Cell Biol 12(1):79-90
51. Herrmann H, Haner M, Brettel M., Ku NO, Aebi U. (1999) Characterization of distinct early assembly units of different intermediate filament proteins. J Mol Biol 286(5):1403-1420. doi:10.1006/jmbi 1999.2528
52. Huang HY, Graves DJ, Robson R.M., Huiatt T.W. (1993) ADP-ribosylation of the intermediate filament protein desmin and inhibition of desmin assembly in vitro by muscle ADP-ribosyltransferase. Biochem Biophys Res Commun 197(2):570-577. doi:10.1006/bbrc.1993.2517
53. Huang HY, Zhou H, Huiatt T.W., Graves D.J. (1996) Target proteins for arginine-specific mono(ADP-ribosyl) transferase in membrane fractions from chick skeletal muscle cells. Exp Cell Res 226(1):147-153. doi:10.1006/excr.1996.0213
54. Huang X, Li J, Foster D., Lemanski SL, Dube DK, Zhang C, Lemanski L.F. (2002) Protein kinase C-mediated desmin phosphorylation is related to myofibril disarray in cardiomyopathic hamster heart. Exp Biol Med (Maywood) 227(11):1039-1046
55. Hutchison CJ (2002) Lamins: building blocks or regulators of gene expression? Nat Rev Mol Cell Biol 3(11):848-858. doi:10.1038/nrm950
56. Inada H, Goto H, Tanabe K., Nishi Y, Kaibuchi K, Inagaki M. (1998) Rho-associated kinase phosphorylates desmin, the myogenic intermediate filament protein, at unique amino-terminal sites. Biochem Biophys Res Commun 253(1):21-25. doi:10.1006/b brc.1998.9732
57. Inada H, Togashi H, Nakamura Y., Kaibuchi K, Nagata K, Inagaki M. (1999) Balance between activities of Rho kinase and type 1 protein phosphatase modulates turnover of phosphorylation and dynamics of desmin/vimentin filaments. J Biol Chem 274(49):34932-34939
58. Inagaki M, Gonda Y, Matsuyama M., Nishizawa K, Nishi Y, Sato C. (1988) Intermediate filament reconstitution in vitro. The role of phosphorylation on the assembly-disassembly of desmin. J Biol Chem 263(12):5970-5978
59. Inagaki M, Gonda Y, Ando S., Kitamura S, Nishi Y, Sato C. (1989a) Regulation of assembly-disassembly of intermediate filaments in vitro. Cell Struct Funct 14(3):279-286
60. 2+-dependent deimination-induced disassembly of intermediate filaments involves specific modification of the amino-terminal head domain. J Biol Chem 264(30):18119-18127
61. Janue A, Odena MA, Oliveira E, Olive M., Ferrer I. (2007a) Desmin is oxidized and nitrated in affected muscles in myotilinopathies and desminopathies. J Neuropathol Exp Neurol 66(8):711-723. doi:10.1097/nen. 0b013e3181256b4c
62. Janue A, Olive M, Ferrer I. (2007b) Oxidative stress in desminopa-thies and myotilinopathies: a link between oxidative damage and abnormal protein aggregation. Brain Pathol 17(4):377-388. doi:10.1111/j.1750-3639.2007.00087.x
63. Joanne P, Chourbagi O, Agbulut O. (2011) Desmin filaments and their disorganization associated with myofibrillar myopathies. Biol Aujourdhui 205(3):163-177. doi:10.1051/jbio/2011016
64. Kaufmann E, Weber K, Geisler N. (1985) Intermediate filament forming ability of desmin derivatives lacking either the amino-terminal 67 or the carboxy-terminal 27 residues. J Mol Biol 185(4):733-742
65. Kawajiri A, Yasui Y, Goto H., Tatsuka M, Takahashi M, Nagata K., Inagaki M. (2003) Functional significance of the specific sites phosphorylated in desmin at cleavage furrow: Aurora-B may phosphorylate and regulate type III intermediate filaments during cytokinesis coordinatedly with Rho-kinase. Mol Biol Cell 14(4):1489-1500. doi:10.1091/mbc.E02-09-0612
66. Kay L, Li Z, Mericskay M., Olivares J, Tranqui L, Fontaine E., Tiivel T, Sikk P, Kaambre T, Samuel JL, Rappaport L, Usson Y, Leverve X, Paulin D, Saks VA (1997) Study of regulation of mitochondrial respiration in vivo. An analysis of influence of ADP diffusion and possible role of cytoskeleton. Biochim Biophys Acta 1322(1):41-59
67. Ke Y, Wang L, Pyle W.G., de Tombe PP, Solaro R.J. (2004) Intracellular localization and functional effects of P21-activated kinase-1 (Pak1) in cardiac myocytes. Circ Res 94(2):194-200. doi:10.1161/01.RES.0000111522.02730.56
68. Kharadia SV, Huiatt TW, Huang H.Y., Peterson JE, Graves D.J. (1992) Effect of an arginine-specific ADP-ribosyltransferase inhibitor on differentiation of embryonic chick skeletal muscle cells in culture. Exp Cell Res 201(1):33-42
69. Kimura K, Ito M, Amano M., Chihara K, Fukata Y, Nakafuku M., Yamamori B, Feng J, Nakano T, Okawa K, Iwamatsu A, Kaibuchi K (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273(5272):245-248
70. Kirmse R, Bouchet-Marquis C, Page C., Hoenger A. (2010) Three-dimensional cryo-electron microscopy on intermediate filaments. Methods Cell Biol 96:565-589. doi:10.1016/S0091-679X(10)96023-8
71. Kiss B, Rohlich P, Kellermayer M.S. (2011) Structure and elasticity of desmin protofibrils explored with scanning force microscopy. J Mol Recognit 24(6):1095-1104. doi:10.1002/jmr.1158
72. Kitamura S, Ando S, Shibata M., Tanabe K, Sato C, Inagaki M. (1989) Protein kinase C phosphorylation of desmin at four serine residues within the non-alpha-helical head domain. J Biol Chem 264(10):5674-5678
73. Konieczny P, Fuchs P, Reipert S., Kunz WS, Zeold A, Fischer I, Paulin D., Schroder R, Wiche G (2008) Myofiber integrity depends on desmin network targeting to Z-disks and costameres via distinct plectin isoforms. J Cell Biol 181(4):667-681
74. Kosako H, Goto H, Yanagida M., Matsuzawa K, Fujita M, Tomono Y., Okigaki T, Odai H, Kaibuchi K, Inagaki M (1999) Specific accumulation of Rho-associated kinase at the cleavage furrow during cytokinesis: cleavage furrow-specific phosphorylation of intermediate filaments. Oncogene 18(17):2783-2788. doi:10.10 38/sj.onc.1202633
75. Kouloumenta A, Mavroidis M, Capetanaki Y. (2007) Proper perinuclear localization of the TRIM-like protein myospryn requires its binding partner desmin. J Biol Chem 282(48):35211-35221. doi:10.1074/jbc.M704733200
76. Kudryashova E, Wu J, Havton L.A., Spencer M.J. (2009) Deficiency of the E3 ubiquitin ligase TRIM32 in mice leads to a myopathy with a neurogenic component. Hum Mol Genet 18(7):1353-1367. doi:10.1093/hmg/ddp036
77. Kudryashova E, Struyk A, Mokhonova E., Cannon SC, Spencer M.J. (2011) The common missense mutation D489 N in TRIM32 causing limb girdle muscular dystrophy 2H leads to loss of the mutated protein in knock-in mice resulting in a Trim32-null phenotype. Hum Mol Genet 20(20):3925-3932. doi:10.1093/h mg/ddr311
78. Kureishi Y, Kobayashi S, Amano M., Kimura K, Kanaide H, Nakano T., Kaibuchi K, Ito M (1997) Rho-associated kinase directly induces smooth muscle contraction through myosin light chain phosphorylation. J Biol Chem 272(19):12257-12260
79. Kusubata M, Tokui T, Matsuoka Y., Okumura E, Tachibana K, Hisanaga S., Kishimoto T, Yasuda H, Kamijo M, Ohba Y et al (1992) p13suc1 suppresses the catalytic function of p34cdc2 kinase for intermediate filament proteins, in vitro. J Biol Chem 267(29):20937-20942
80. Kusubata M, Matsuoka Y, Tsujimura K., Ito H, Ando S, Kamijo M., Yasuda H, Ohba Y, Okumura E, Kishimoto T et al (1993) cdc2 kinase phosphorylation of desmin at three serine/threonine residues in the amino-terminal head domain. Biochem Biophys Res Commun 190(3):927-934
81. Langley RC J.r., Cohen C.M. (1986) Association of spectrin with desmin intermediate filaments. J Cell Biochem 30(2):101-109
82. Lapouge K, Fontao L, Champliaud M.F., Jaunin F., Frias MA, Favre B, Paulin D, Green K.J., Borradori L. (2006) New insights into the molecular basis of desmoplakin- and desmin-related cardiomyopathies. J Cell Sci 119(Pt 23):4974-4985. doi:10.1242/jcs.03255
83. Lazarides E, Hubbard B.D. (1976) Immunological characterization of the subunit of the 100 A filaments from muscle cells. Proc Natl Acad Sci USA 73(12):4344-4348
84. Li H, Capetanaki Y. (1993) Regulation of the mouse desmin gene: transactivated by MyoD, myogenin, MRF4 and Myf5. Nucleic Acids Res 21(2):335-343
85. Li H, Choudhary SK, Milner D.J., Munir MI, Kuisk IR, Capetanaki Y. (1994) Inhibition of desmin expression blocks myoblast fusion and interferes with the myogenic regulators MyoD and myogenin. J Cell Biol 124(5):827-841
86. Li S, Iakoucheva LM, Mooney S.D., Radivojac P. (2010) Loss of posttranslational modification sites in disease. Pac Symp Biocomput 337-347
87. Linden M, Li Z, Paulin D., Gotow T, Leterrier J.F. (2001) Effects of desmin gene knockout on mice heart mitochondria. J Bioenerg Biomembr 33(4):333-341
88. Luck S, Sailer M, Schmidt V., Walther P. (2010) Three-dimensional analysis of intermediate filament networks using SEM tomography. J Microsc 239(1):1-16. doi:10.1111/j.1365-2818.2009.03348.x
89. Mabuchi K, Li B, Ip W., Tao T. (1997) Association of calponin with desmin intermediate filaments. J Biol Chem 272(36):22662-22666
90. Marchal S, Cassar-Malek I, Magaud J.P., Rouault JP, Wrutniak C, Cabello G. (1995) Stimulation of avian myoblast differentiation by triiodothyronine: possible involvement of the cAMP pathway. Exp Cell Res 220(1):1-10. doi:10.1006/excr.1995.1285
91. McCullagh KJ, Edwards B, Poon E., Lovering RM, Paulin D, Davies K.E. (2007) Intermediate filament-like protein syncoilin in normal and myopathic striated muscle. Neuromuscul Disord 17(11-12):970-979
92. McFawn PK, Shen L, Vincent S.G., Mak A., Van Eyk JE, Fisher J.T. (2003) Calcium-independent contraction and sensitization of airway smooth muscle by p21-activated protein kinase. Am J Physiol Lung Cell Mol Physiol 284(5):L863-L870. doi:10.1152/ajplung.0.0068.2002
93. McLendon PM, Robbins J. (2011) Desmin-related cardiomyopathy: an unfolding story. Am J Physiol Heart Circ Physiol 301(4):H1220-H1228. doi:10.1152/ajpheart.00601.2011
94. Mittal B, Sanger JM, Sanger J.W. (1989) Visualization of intermediate filaments in living cells using fuorescently labeled desmin. Cell Motil Cytoskeleton 12(3):127-138. doi:10.1002/cm.970120302
95. Moresi V, Garcia-Alvarez G, Pristera A., Rizzuto E, Albertini MC, Rocchi M, Marazzi G., Sassoon D, Adamo S, Coletti D (2009) Modulation of caspase activity regulates skeletal muscle regeneration and function in response to vasopressin and tumor necrosis factor. PLoS ONE 4(5):e5570. doi:10.1371/journal. pone.0005570
96. Mukai A, Hashimoto N. (2008) Localized cyclic AMP-dependent protein kinase activity is required for myogenic cell fusion. Exp Cell Res 314(2):387-397. doi:10.1016/j.yexcr.2007.10.006
97. 2+ sensitization, and contraction activated by protein kinase C in small airway smooth muscle. J Gen Physiol 141(2):165-178. doi:10.1085/jgp.201210876
98. Nakano S, Engel AG, Akiguchi I, Kimura J. (1997) Myofibrillar myopathy. III. Abnormal expression of cyclin-dependent kinases and nuclear proteins. J Neuropathol Exp Neurol 56(8):850-856
99. O'Connor C.M., Gard DL, Lazarides E. (1981) Phosphorylation of intermediate filament proteins by cAMP-dependent protein kinases. Cell 23(1):135-143
100. Ohtakara K, Inada H, Goto H., Taki W, Manser E, Lim L., Izawa I, Inagaki M (2000) p21-activated kinase PAK phosphorylates desmin at sites different from those for Rho-associated kinase. Biochem Biophys Res Commun 272(3):712-716. doi:10.1006/bbrc.2000.2854
101. Park S, Rasmussen H. (1986) Carbachol-induced protein phosphorylation changes in bovine tracheal smooth muscle. J Biol Chem 261(33):15734-15739
102. Paulin D, Li Z. (2004) Desmin: a major intermediate filament protein essential for the structural integrity and function of muscle. Exp Cell Res 301(1):1-7. doi:10.1016/j.yexcr.2004.08.004
103. Paulin D, Huet A, Khanamyrian L., Xue Z. (2004) Desminopathies in muscle disease. J Pathol 204(4):418-427. doi:10.1002/path.1639
104. Peng Y, Yu D, Gregorich Z., Chen X, Beyer AM, Gutterman D.D., Ge Y. (2013) In-depth proteomic analysis of human tropomyosin by top-down mass spectrometry. J Muscle Res Cell Motil. doi:10.1007/s10974-013-9352-y
105. Pica EC, Kathirvel P, Pramono Z.A., Lai PS, Yee W.C. (2008) Characterization of a novel S13F desmin mutation associated with desmin myopathy and heart block in a Chinese family. Neuro-muscul Disord 18(2):178-182. doi:10.1016/j.nmd.2007.09.011
106. Quinlan RA, Hatzfeld M, Franke W.W., Lustig A., Schulthess T, Engel J. (1986) Characterization of dimer subunits of intermediate filament proteins. J Mol Biol 192(2):337-349
107. Rappaport L, Contard F, Samuel J.L., Delcayre C., Marotte F, Tome F, Fardeau M. (1988) Storage of phosphorylated desmin in a familial myopathy. FEBS Lett 231(2):421-425
108. Rasmussen H, Takuwa Y, Park S. (1987) Protein kinase C in the regulation of smooth muscle contraction. FASEB J 1(3):177-185
109. Russell MA, Lund LM, Haber R, McKeegan K., Cianciola N, Bond M. (2006) The intermediate filament protein, synemin, is an AKAP in the heart. Arch Biochem Biophys 456(2):204-215. doi:10.1016/j.abb.2006.06.010
110. Saccone V, Palmieri M, Passamano L., Piluso G, Meroni G, Politano L., Nigro V. (2008) Mutations that impair interaction properties of TRIM32 associated with limb-girdle muscular dystrophy 2H. Hum Mutat 29(2):240-247. doi:10.1002/humu.20633
111. Schoser BG, Frosk P, Engel A.G., Klutzny U., Lochmuller H, Wrogemann K. (2005) Commonality of TRIM32 mutation in causing sarcotubular myopathy and LGMD2H. Ann Neurol 57(4):591-595. doi:10.1002/ana.20441
112. Schweitzer SC, Klymkowsky MW, Bellin R.M., Robson RM, Capetanaki Y, Evans R.M. (2001) Paranemin and the organization of desmin filament networks. J Cell Sci 114(Pt 6):1079-1089
113. Selcen D, Engel A.G. (2011) Myofibrillar myopathies. Handb Clin Neurol 101:143-154. doi:10.1016/B978-0-08-045031-5.00011-6
114. Sharma S, Mucke N, Katus H.A., Herrmann H., Bar H. (2009) Disease mutations in the "head," domain of the extra-sarcomeric protein desmin distinctly alter its assembly and network-forming properties. J Mol Med (Berl) 87(12):1207-1219. doi:10.1007/s00109-009-0521-9
115. Shieh PB, Kudryashova E, Spencer M.J. (2011) Limb-girdle muscular dystrophy 2H and the role of TRIM32. Handb Clin Neurolgy 101:125-133. doi:10.1016/B978-0-08-045031-5.00009-8
116. Singh MV, Anderson M.E. (2011) Is CaMKII a link between inflammation and hypertrophy in heart? J Mol Med (Berl) 89(6):537-543. doi:10.1007/s00109-011- 0727-5
117. Sjoberg G, Jiang WQ, Ringertz N.R., Lendahl U., Sejersen T. (1994) Colocalization of nestin and vimentin/desmin in skeletal muscle cells demonstrated by three-dimensional fluorescence digital imaging microscopy. Exp Cell Res 214(2):447-458
118. Small J.V., Gimona M. (1998) The cytoskeleton of the vertebrate smooth muscle cell. Acta Physiol Scand 164(4):341-348. doi:10.1046/j.1365-201X.1998. 00441.x
119. Small J.V., Sobieszek A. (1977) Studies on the function and composition of the 10-NM(100-A) filaments of vertebrate smooth muscle. J Cell Sci 23:243-268
120. Swaminathan PD, Purohit A, Hund T.J., Anderson M.E. (2012) Calmodulin-dependent protein kinase II: linking heart failure and arrhythmias. Circ Res 110(12):1661-1677. doi:10.1161/CIRCR ESAHA.111.243956
121. Takuwa Y, Kelley G, Takuwa N., Rasmussen H. (1988) Protein phos-phorylation changes in bovine carotid artery smooth muscle during contraction and relaxation. Mol Cell Endocrinol 60(1):71-86
122. Tao JX, Ip W. (1991) Site-specific antibodies block kinase A phospho-rylation of desmin in vitro and inhibit incorporation of myo-blasts into myotubes. Cell Motil Cytoskeleton 19(2):109-120. doi:10.1002/cm.970190206
123. Terman JR, Kashina A. (2013) Post-translational modification and regulation of actin. Curr Opin Cell Biol 25(1):30-38. doi:10.1016/j.ceb.2012.10. 009
124. Thornell LE, Eriksson A. (1981) Filament systems in the Purkinje fibers of the heart. Am J Physiol 241(3):H291-H305
125. Titeux M, Brocheriou V, Xue Z., Gao J, Pellissier JF, Guicheney P, Paulin D., Li Z. (2001) Human synemin gene generates splice variants encoding two distinct intermediate filament proteins. Eur J Biochem 268(24):6435-6449
126. 2+-calmodulin-dependent protein kinase II phos-phorylates various types of non-epithelial intermediate filament proteins. Biochem Biophys Res Commun 169(3):896-904
127. Tolstonog GV, Sabasch M, Traub P. (2002) Cytoplasmic intermediate filaments are stably associated with nuclear matrices and potentially modulate their DNA-binding function. DNA Cell Biol 21(3):213-239. doi:10.1089/ 10445490252925459
128. Toschi A, Severi A, Coletti D., Catizone A, Musaro A, Molinaro M., Nervi C, Adamo S, Scicchitano BM (2011) Skeletal muscle regeneration in mice is stimulated by local overexpression of V1a-vasopressin receptor. Mol Endocrinol 25(9):1661-1673. doi:10.1210/me.2011-1049
129. Traub P, Vorgias C.E. (1984) Differential effect of arginine modification with 1,2-cyclohexanedione on the capacity of vimentin and desmin to assemble into intermediate filaments and to bind to nucleic acids. J Cell Sci 65:1-20
130. 2+-independent contraction of smooth muscle. J Biol Chem 273(36):23433-23439
131. Vattemi G, Tonin P, Mora M., Filosto M, Morandi L, Savio C., Dal Pra I, Rizzuto N, Tomelleri G (2004) Expression of protein kinase C isoforms and interleukin-1beta in myofibrillar myopathy. Neurology 62(10):1778-1782
132. Vicart P, Caron A, Guicheney P., Li Z, Prevost MC, Faure A, Chateau D., Chapon F, Tome F, Dupret JM, Paulin D, Fardeau M (1998) A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet 20(1):92-95
133. Wang Q, Tolstonog GV, Shoeman R, Traub P. (2001) Sites of nucleic acid binding in type I-IV intermediate filament subunit proteins. Biochemistry 40(34):10342-10349
134. Winter B, Braun T, Arnold H.H. (1993) cAMP-dependent protein kinase represses myogenic differentiation and the activity of the muscle-specific helix-loop-helix transcription factors Myf-5 and MyoD. J Biol Chem 268(13):9869-9878
135. Xue ZG, Cheraud Y, Brocheriou V., Izmiryan A, Titeux M, Paulin D., Li Z. (2004) The mouse synemin gene encodes three intermediate filament proteins generated by alternative exon usage and different open reading frames. Exp Cell Res 298(2):431-444. doi:10.1016/j.yexcr.2004.04.023
136. Yau L, Litchie B, Thomas S., Storie B, Yurkova N, Zahradka P. (2003) Endogenous mono-ADP-ribosylation mediates smooth muscle cell proliferation and migration via protein kinase N-dependent induction of c-fos expression. Eur J Biochem 270(1):101-110
137. Yau L, Litchie B, Zahradka P. (2004) MIBG, an inhibitor of arginine-dependent mono(ADP-ribosyl)ation, prevents differentiation of L6 skeletal myoblasts by inhibiting expression of myogenin and p21(cip1). Exp Cell Res 301(2):320-330. doi:10.1016/j.yexcr.2004.08.036
138. Yu JG, Thornell L.E. (2002) Desmin and actin alterations in human muscles affected by delayed onset muscle soreness: a high resolution immunocytochemical study. Histochem Cell Biol 118(2):171-179. doi:10.1007/s00418-002-0427-x
139. Yu JG, Furst DO, Thornell L.E. (2003) The mode of myofibril remodelling in human skeletal muscle affected by DOMS induced by eccentric contractions. Histochem Cell Biol 119(5):383-393. doi:10.1007/s00418-003-0522-7
140. Yu JG, Carlsson L, Thornell L.E. (2004) Evidence for myofibril remodeling as opposed to myofibril damage in human muscles with DOMS: an ultrastructural and immunoelectron microscopic study. Histochem Cell Biol 121(3):219-227. doi:10.1007/s00418-004-0625-9
141. Yuan J, Huiatt TW, Liao C.X., Robson RM, Graves D.J. (1999) The effects of mono-ADP-ribosylation on desmin assembly-disassembly. Arch Biochem Biophys 363(2):314-322
142. Zalin RJ, Montague W. (1974) Changes in adenylate cyclase, cyclic AMP, and protein kinase levels in chick myoblasts, and their relationship to differentiation. Cell 2(2):103-108
143. Zhou H, Huiatt TW, Robson R.M., Sernett SW, Graves D.J. (1996) Characterization of ADP-ribosylation sites on desmin and restoration of desmin intermediate filament assembly by de-ADP-ribosylation. Arch Biochem Biophys 334(2):214-222. doi:10.1 006/abbi.1996.0449