Syncoilin is required for generating maximum isometric stress in skeletal muscle but dispensable for muscle cytoarchitecture

American Journal of Physiology - Cell Physiology

Volumn 294, Issue 5, 2008, Pages

  Zhang, Jianlin ^a,d   Bang, Marie Louise ^a,e   Gokhin, David S ^b   Lu, Yingchun ^a,f   Cui, Li ^c   Li, Xiaodong ^a   Gu, Yusu ^a   Dalton, Nancy D ^a   Scimia, Maria Cecilia ^a,e   Peterson, Kirk L ^a   Lieber, Richard L ^b   Chen, Ju ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d WUHAN UNIVERSITY   (China)

^e IRCCS MULTIMEDICA   (Italy)

^f NONE   (United States)

Author keywords

Intermediate filament; Mutant mouse; Sarcomere

Indexed keywords

CYTOSKELETON PROTEIN; DESMIN; DOBUTAMINE; DYSTROBREVIN; DYSTROPHIN ASSOCIATED PROTEIN COMPLEX; MUSCLE PROTEIN; SYNCOILIN; UNCLASSIFIED DRUG; INTERMEDIATE FILAMENT PROTEIN; PRIMER DNA; SYNC PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; GENE TARGETING; HEART MUSCLE; MOUSE; MUSCLE CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SKELETAL MUSCLE; UPREGULATION; ANIMAL; CYTOLOGY; GENETICS; HEART LEFT VENTRICLE FUNCTION; HEMODYNAMICS; HINDLIMB; MECHANICAL STRESS; MOUSE MUTANT; MUSCLE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; RESTRICTION MAPPING;

MUS;

ANIMALS; DESMIN; DNA PRIMERS; HEMODYNAMICS; HINDLIMB; INTERMEDIATE FILAMENT PROTEINS; MICE; MICE, KNOCKOUT; MUSCLE CONTRACTION; MUSCLE FIBERS; MUSCLE PROTEINS; MUSCLE, SKELETAL; RESTRICTION MAPPING; STRESS, MECHANICAL; VENTRICULAR FUNCTION, LEFT;

EID: 48249120408     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00049.2008     Document Type: Article

References (35)

1. Albrecht DE, Froehner SC. DAMAGE, a novel α-dystrobrevin- associated MAGE protein in dystrophin complexes. J Biol Chem 279: 7014-7023, 2004.
2. Arber S, Hunter JJ, Ross J Jr, Hongo M, Sansig G, Borg J, Perriard JC, Chien KR, Caroni P. MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure. Cell 88: 393-403, 1997.
3. Bach JP, Borta H, Ackermann W, Faust F, Borchers O, Schrader M. The secretory granule protein syncollin localizes to HL-60 cells and neutrophils. J Histochem Cytochem 54: 877-888, 2006.
4. Barash IA, Bang ML, Mathew L, Greaser ML, Chen J, Lieber RL. Structural and regulatory roles of muscle ankyrin repeat protein family in skeletal muscle. Am J Physiol Cell Physiol 293: C218-C227, 2007.
5. Benson MA, Newey SE, Martin-Rendon E, Hawkes R, Blake DJ. Dysbindin, a novel coiled-coil-containing protein that interacts with the dystrobrevins in muscle and brain. J Biol Chem 276: 24232-24241, 2001.
6. Blake DJ. Dystrobrevin dynamics in muscle-cell signalling: a possible target for therapeutic intervention in Duchenne muscular dystrophy? Neuromuscul Disord 12, Suppl 1: S110-S117, 2002.
7. Blake DJ, Nawrotzki R, Loh NY, Gorecki DC, Davies KE. β-Dystrobrevin, a member of the dystrophin-related protein family. Proc Natl Acad Sci USA 95: 241-246, 1998.
8. Brown SC, Torelli S, Ugo I, De Biasia F, Howman EV, Poon E, Britton J, Davies KE, Muntoni F. Syncoilin upregulation in muscle of patients with neuromuscular disease. Muscle Nerve 32: 715-725, 2005.
9. Chleboun GS, Patel TJ, Lieber RL. Skeletal muscle architecture and fiber-type distribution with the multiple bellies of the mouse extensor digitorum longus muscle. Acta Anat (Basel) 159: 147-155, 1997.
10. Deconinck N, Rafael JA, Beckers-Bleukx G, Kahn D, Deconinck AE, Davies KE, Gillis JM. Consequences of the combined deficiency in dystrophin and utrophin on the mechanical properties and myosin composition of some limb and respiratory muscles of the mouse. Neuromuscul Disord 8: 362-370, 1998.
11. Dellorusso C, Crawford RW, Chamberlain JS, Brooks SV. Tibialis anterior muscles in mdx mice are highly susceptible to contraction-induced injury. J Muscle Res Cell Motil 22: 467-475, 2001.
12. DeSantiago J, Maier LS, Bers DM. Frequency-dependent acceleration of relaxation in the heart depends on CaMKII, but not phospholamban. J Mol Cell Cardiol 34: 975-984, 2002.
13. 2+-sensitive manner. Cell 90: 325-333, 1997.
14. Ervasti JM, Campbell KP. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122: 809-823, 1993.
15. Ervasti JM, Campbell KP. Membrane organization of the dystrophin-glycoprotein complex. Cell 66: 1121-1131, 1991.
16. Feick P, Foisner R, Wiche G. Immunolocalization and molecular properties of a high molecular weight microtubule-bundling protein (syncolin) from chicken erythrocytes. J Cell Biol 112: 689-699, 1991.
17. Friden J, Lieber RL. Spastic muscle cells are shorter and stiffer than normal cells. Muscle Nerve 27: 157-164, 2003.
18. Howman EV, Sullivan N, Poon EP, Britton JE, Hilton-Jones D, Davies KE. Syncoilin accumulation in two patients with desmin-related myopathy. Neuromuscul Disord 13: 42-48, 2003.
19. Li Z, Mericskay M, Agbulut O, Butler-Browne G, Carlsson L, Thornell LE, Babinet C, Paulin D. Desmin is essential for the tensile strength and integrity of myofibrils but not for myogenic commitment, differentiation, and fusion of skeletal muscle. J Cell Biol 139: 129-144, 1997.
20. Lieber RL, Friden J. Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 23: 1647-1666, 2000.
21. Lynch GS, Hinkle RT, Chamberlain JS, Brooks SV, Faulkner JA. Force and power output of fast and slow skeletal muscles from mdx mice 6-28 months old. J Physiol 535: 591-600, 2001.
22. McCullagh KJ, Edwards B, Poon E, Lovering RM, Paulin D, Davies KE. Intermediate filament-like protein syncoilin in normal and myopathic striated muscle. Neuromuscul Disord 2007.
23. Milner DJ, Weitzer G, Tran D, Bradley A, Capetanaki Y. Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J Cell Biol 134: 1255-1270, 1996.
24. 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 α-dystrobrevin and desmin. Proc Natl Acad Sci USA 98: 6156-6161, 2001.
25. Moens P, Baatsen PH, Marechal G. Increased susceptibility of EDL muscles from mdx mice to damage induced by contractions with stretch. J Muscle Res Cell Motil 14: 446-451, 1993.
26. Newey SE, Howman EV, Ponting CP, Benson MA, Nawrotzki R, Loh NY, Davies KE, Blake DJ. Syncoilin, a novel member of the intermediate filament superfamily that interacts with α-dystrobrevin in skeletal muscle. J Biol Chem 276: 6645-6655, 2001.
27. Patel ND, Jannapureddy SR, Hwang W, Chaudhry I, Boriek AM. Altered muscle force and stiffness of skeletal muscles in alpha-sarcoglycan-deficient mice. Am J Physiol Cell Physiol 284: C962-C968, 2003.
28. Perriard JC, Hirschy A, Ehler E. Dilated cardiomyopathy: a disease of the intercalated disc? Trends Cardiovasc Med 13: 30-38, 2003.
29. Poon E, Howman EV, Newey SE, Davies KE. Association of syncoilin and desmin: linking intermediate filament proteins to the dystrophin-associated protein complex. J Biol Chem 277: 3433-3439, 2002.
30. Rockman HA, Ono S, Ross RS, Jones LR, Karimi M, Bhargava V, Ross J Jr, Chien KR. Molecular and physiological alterations in murine ventricular dysfunction. Proc Natl Acad Sci USA 91: 2694-2698, 1994.
31. Sam M, Shah S, Friden J, Milner DJ, Capetanaki Y, Lieber RL. Desmin knockout muscles generate lower stress and are less vulnerable to injury compared with wild-type muscles. Am J Physiol Cell Physiol 279: C1116-C1122, 2000.
32. Shah SB, Su FC, Jordan K, Milner DJ, Friden J, Capetanaki Y, Lieber RL. Evidence for increased myofibrillar mobility in desmin-null mouse skeletal muscle. J Exp Biol 205: 321-325, 2002.
33. Tanaka N, Dalton N, Mao L, Rockman HA, Peterson KL, Gottshall KR, Hunter JJ, Chien KR, Ross J Jr. Transthoracic echocardiography in models of cardiac disease in the mouse. Circulation 94: 1109-1117, 1996.
34. Wilding JR, Schneider JE, Sang AE, Davies KE, Neubauer S, Clarke K. Dystrophin- and MLP-deficient mouse hearts: marked differences in morphology and function, but similar accumulation of cytoskeletal proteins. FASEB J 19: 79-81, 2005.
35. Yoshida M, Suzuki A, Yamamoto H, Noguchi S, Mizuno Y, Ozawa E. Dissociation of the complex of dystrophin and its associated proteins into several unique groups by n-octyl β-D-glucoside. Eur J Biochem 222: 1055-1061, 1994.