Biomechanics of the sarcolemma and costameres in single skeletal muscle fibers from normal and dystrophin-null mice

Journal of Muscle Research and Cell Motility

Volumn 31, Issue 5-6, 2011, Pages 323-336

  Garcia Pelagio K P ^a   Bloch, R J ^b   Ortega, A ^a   Gonzalez Serratos H ^b  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

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

Author keywords

Costamere; Dystrophic muscle; mdx; Muscle mechanics; Muscular dystrophy; Superficial tension

Indexed keywords

DYSTROPHIN;

ANIMAL; ARTICLE; C57BL MOUSE; COSTAMERE; METABOLISM; MOUSE; MOUSE MUTANT; SARCOLEMMA; SKELETAL MUSCLE;

ANIMALS; COSTAMERES; DYSTROPHIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE FIBERS, SKELETAL; SARCOLEMMA;

MAMMALIA; MUS;

EID: 79952310518     PISSN: 01424319     EISSN: 15732657     Source Type: Journal    
DOI: 10.1007/s10974-011-9238-9     Document Type: Article

References (78)

1. DG Allen GD Lamb H Westerblad 2008 Skeletal muscle fatigue: cellular mechanisms Physiol Rev 88 287 332 1:CAS:528:DC%2BD1cXitVKgtrg%3D 10.1152/physrev.00015.2007 18195089
2. G Anastasi G Cutroneo G Santoro A Arco G Rizzo P Bramanti C Rinaldi A Sidoti A Amato A Favaloro 2008 Costameric proteins in human skeletal muscle during muscular inactivity J Anat 213 3 284 295 1:CAS:528:DC%2BD1cXhtFylsL7O 10.1111/j.1469-7580.2008.00921.x 18537849
3. G Ayalon J Davis P Scotland V Bennett 2008 An ankyrin-based mechanism for functional organization of dystrophin and dystroglycan Cell 135 7 1189 1200 1:CAS:528:DC%2BD1MXisFyjtg%3D%3D 10.1016/j.cell.2008.10.018 19109891
4. E Barton 2006 Impact of Sarcoglycan complex on mechanical signal transduction in murine skeletal muscle Am J Physiol Cell Physiol 290 2 C411 C419 1:CAS:528:DC%2BD28XhsFKhsr4%3D 10.1152/ajpcell.00192.2005 16162659
5. A Beedle P Nienaber K Campbell 2007 Fukutin-related protein associates with the sarcolemmal dystrophin-glycoprotein complex J Biol Chem 282 23 16713 16717 1:CAS:528:DC%2BD2sXmt1ahu7c%3D 10.1074/jbc.C700061200 17452335 (Pubitemid 47093191)
6. R Bhosle D Michele K Campbell Z Li R Robson 2006 Interactions of intermediate filament protein synemin with dystrophin and utrophin Biochem Biophys Res Commun 346 3 768 777 1:CAS:528:DC%2BD28XmtlWrsLc%3D 10.1016/j.bbrc.2006.05.192 16777071 (Pubitemid 44192512)
7. B Blaauw C Mammucari L Toniolo L Agatea R Abraham M Sandri C Reggiani S Schaffino 2008 Akt activation prevents the force drop induced by eccentric contractions in dystrophin-deficient skeletal muscle Hum Mol Genet 17 23 3686 3696 1:CAS:528:DC%2BD1cXhtlGis77K 10.1093/hmg/ddn264 18753145
8. B Blaauw L Agate L Toniolo M Canato M Quarta K Dyar D Danieli-Betto R Betto S Schiaffino C Reggiani 2010 Eccentric contractions lead to myofibrillar dysfunction in muscular dystrophy J Appl Physiol 108 1 105 111 1:CAS:528:DC%2BC3cXitFGgs70%3D 10.1152/japplphysiol.00803.2009 19910334
9. R Bloch H Gonzalez-Serratos 2003 Lateral force transmission across costameres in skeletal muscle Exerc Sport Sci Rev 31 2 73 78 10.1097/00003677-200304000-00004 12715970 (Pubitemid 36443764)
10. R Bloch Y Capetanaki A O'Neill P Reed MW Williams W Resneck N Porter J Ursitti 2002 Costameres: repeating structures at the sarcolemma of skeletal muscle Clin Orthop Relat Res 403S S203 S210 10.1097/00003086-200210001-00024
11. Boal D (2006) Mechanics of the cell. Cambridge University Press, Cambridge
12. J Bobet RF Mooney T Gordon 1998 Force and stiffness of old dystrophic (mdx) mouse skeletal muscles Muscle Nerve 21 4 536 539 1:STN:280: DyaK1c7pt1Cktw%3D%3D 10.1002/(SICI)1097-4598(199804)21:4<536::AID-MUS15>3. 0.CO;2-V 9533791 (Pubitemid 28145333)
13. J Brenman D Chao H Xia K Aldape D Bredt 1995 Nitric oxide synthase complexed with dystrophin and absent from skeletal muscles sarcolemma in Duchenne muscular dystrophy Cell 82 5 743 752 1:CAS:528:DyaK2MXotFahu7Y%3D 10.1016/0092-8674(95)90471-9 7545544
14. Bull H (1964) An introduction to physical biochemistry. Davis Co, Philadelphia
15. K Campbell T Stull 2003 Skeletal muscle basement membrane-sarcolemma- cytoskeleton interaction minireview series J Biol Chem 278 15 12599 12600 1:CAS:528:DC%2BD3sXislGrsro%3D 10.1074/jbc.R300005200 12556456 (Pubitemid 36800016)
16. C Caputo P Bolaños 1994 Fluo-3 signals associated with potassium contractures in single amphibian muscle fibers J Physiol 481 119 128 1:CAS:528:DyaK2MXisVWmtLo%3D 7853234 (Pubitemid 24361352)
17. D Claffin S Brooks 2008 Direct observation of failing fibers in muscles of dystrophic mice provides mechanistic insight into muscular dystrophy Am J Physiol Cell Physiol 294 C651 C658 10.1152/ajpcell.00244.2007 (Pubitemid 351264415)
18. G Dmytrenko D Pumplin R Bloch 1993 Dystrophin in membrane skeletal network: localization and comparison to other proteins J Neurosci 13 2 547 558 1:CAS:528:DyaK3sXhs1GksL4%3D 8426227 (Pubitemid 23045138)
19. AF Dulhunty C Franzini-Armstrong 1975 The relative contribution of the folds and caveolae to the surface membrane of frog skeletal muscle fibers at different sarcomere length J Physiol 250 513 539 1:STN:280: DyaE28%2FislSntA%3D%3D 1080806
20. Dull RW (1941) Mathematics for engineers. McGraw-Hill Book Company, New York
21. S Ehmer H Herrmann R Bittner T Voit 1997 Spatial distribution of beta-spectrin in normal and dystrophic human skeletal muscle Acta Neuropathol 94 3 240 246 1:CAS:528:DyaK2sXltlaisL4%3D 10.1007/s004010050699 9292693 (Pubitemid 27395325)
22. J Ervasti 2003 Costameres: the Achilles' heel of herculean muscle J Biol Chem 278 16 13591 13594 1:CAS:528:DC%2BD3sXjtVSisLg%3D 10.1074/jbc.R200021200 12556452 (Pubitemid 36799888)
23. J Ervasti 2007 Dystrophin, its interactions with other proteins, and implications for muscular dystrophy Biochem Biophys Acta 1772 2 108 117 1:CAS:528:DC%2BD2sXpvVynug%3D%3D 16829057 (Pubitemid 46123911)
24. J Ervasti K Campbell 1991 Membrane organization of the dystrophin-glycoprotein complex Cell 66 6 1121 1131 1:CAS:528:DyaK3MXmtVCisLk%3D 10.1016/0092-8674(91)90035-W 1913804 (Pubitemid 121001402)
25. J Ervasti K Campbell 1993 A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin J Cell Biol 122 809 823 1:CAS:528:DyaK3sXltFWks7k%3D 10.1083/jcb.122.4.809 8349731 (Pubitemid 23241091)
26. E Evans M Hochmuth 1976 Membrane viscoelasticity Biophys J 16 1 1 11 1:STN:280:DyaE28%2FovFemtQ%3D%3D 10.1016/S0006-3495(76)85658-5 1244886
27. E Evans A Yeung 1989 Apparent viscosity and cortical tension of blood granulocytes determined by micropipette aspiration Biophys J 56 151 160 1:STN:280:DyaL1MzitlaqsA%3D%3D 10.1016/S0006-3495(89)82660-8 2752085 (Pubitemid 19175791)
28. Fonbrune P (1949) Technique de Micromanipulation. Massonn et Cie, Paris
29. K Garcia-Pelagio R Bloch A Ortega H Gonzalez-Serratos 2006 Elastic properties of the sarcolemma-costamere complex of muscle cells in normal mice AIP Conf Proc 854 51 53 10.1063/1.2356399
30. K Garcia-Pelagio R Bloch A Ortega H Gonzalez-Serratos 2008 Passive viscoelastic properties of costameres in EDL muscle in normal and dystrophin null mice AIP Conf Proc 1032 268 271 10.1063/1.2979289
31. G Goldspink K Fernandes PE Williams DJ Wells 1994 Age-related changes in collagen gene expression in the muscles of mdx dystrophic and normal mice Neuromuscul Disord 4 3 183 191 1:STN:280:DyaK2M%2FgtlKrtw%3D%3D 10.1016/0960-8966(94)90019-1 7919967 (Pubitemid 24171292)
32. H Gonzalez-Serratos 1971 Inward spread of activation in vertebrate muscle fibres J Physiol 212 3 777 799 1:CAS:528:DyaE3MXosFaktg%3D%3D 5557071
33. AM Gordon AF Huxley FJ Julian 1966 The variation in isometric tension with sarcomere length in vertebrate muscle fibers J Physiol 184 170 192 1:STN:280:DyaF2s%2Fit1WjsA%3D%3D 5921536
34. M Hochmuth 2000 Micropipette aspiration of living cells J Biomech 33 15 22 1:STN:280:DC%2BD3c%2FnsFKjtw%3D%3D 10.1016/S0021-9290(99)00175-X 10609514
35. EP Hoffman R Brown L Kunkel 1987 Dystrophin: the protein product of the Duchenne muscular dystrophy locus Cell 51 919 928 1:CAS:528:DyaL1cXntlWqug%3D%3D 10.1016/0092-8674(87)90579-4 3319190
36. OF Hutter FL Burton DL Bovell 1991 Mechanical properties of normal and mdx mouse sarcolemma: bearing on function of dystrophin J Muscle Res Cell Motil 12 585 589 1:STN:280:DyaK387msF2qtA%3D%3D 10.1007/BF01738447 1791198
37. K Lapidos R Kakkar M McNally 2004 The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma Circ Res 94 1023 1031 1:CAS:528:DC%2BD2cXjt1yksr4%3D 10.1161/01.RES.0000126574.61061.25 15117830 (Pubitemid 38579696)
38. Leckie FA, Dal Bello DJ (2009) Strength and stiffness of engineering systems. Springer, New York
39. C Minetti G Cordone F Beltrame M Bado E Bonilla 1998 Disorganization of dystrophin costameric lattice in Becker muscular dystrophy Muscle Nerve 21 2 211 216 1:STN:280:DyaK1c7is1SksA%3D%3D 10.1002/(SICI)1097-4598(199802)21:2<211:: AID-MUS8>3.0.CO;2-E 9466596 (Pubitemid 28079740)
40. JM Mitchison 1953 The thickness of the sea urchin fertilization membrane Exp Cell Res 5 2 536 538 1:STN:280:DyaG2c%2Fjsl2rtw%3D%3D 10.1016/0014-4827(53) 90240-7 13117023
41. S Na F Chowdhury B Tay M Ouyang M Gregor Y Wang G Wiche N Wang 2009 Plectin contributes to mechanical properties of living cells Am J Physiol Cell Physiol 296 4 C868 C877 1:CAS:528:DC%2BD1MXkvVyhsb4%3D 10.1152/ajpcell.00604. 2008 19244477
42. D Needham M Hochmuth 1992 A sensitive measure of surface stress in the resting neutrophil Biophys J 61 6 1664 1670 1:STN:280:DyaK38zhsVeguw%3D%3D 10.1016/S0006-3495(92)81970-7 1617145
43. Nelkon M (1979) Scholarship physics. Hienemann Educational Publishers, London
44. V Nigro G Piluso A Belsito L Politano, et al. 1996 Identification of a novel sarcoglycan gene at 5q33 encoding a sarcolemmal 35 kDa glycoprotein Hum Mol Genet 5 8 1179 1186 1:CAS:528:DyaK28XkslSqsrw%3D 10.1093/hmg/5.8.1179 8842738 (Pubitemid 26318558)
45. K Nowak K Davies 2004 Duchenne muscular dystrophy and dystrophin: pathogenesis and opportunities for treatment EMBO Rep 5 872 876 1:CAS:528:DC%2BD2cXot1Kgtrw%3D 10.1038/sj.embor.7400221 15470384 (Pubitemid 350011231)
46. A O'Neill MW Williams W Resneck D Milner Y Capetanaki RJ Bloch 2002 Sarcolemmal organization in skeletal muscle lacking desmin: evidence for cytokeratins associated with membrane skeleton at costameres Mol Biol Cell 13 2347 2359 10.1091/mbc.01-12-0576 12134074 (Pubitemid 34831339)
47. SA Oak YW Zhou HW Jarrett 2003 Skeletal muscle signaling pathway through the dystrophin glycoprotein complex and Rac1 J Biol Chem 278 41 39287 39295 1:CAS:528:DC%2BD3sXnvFansbo%3D 10.1074/jbc.M305551200 12885773 (Pubitemid 37248483)
48. K Ohlendieck J Ervasti J Snook K Campbell 1991 Dystrophin-glycoprotein complex is highly enriched in isolated skeletal muscle sarcolemma J Cell Biol 112 135 148 1:CAS:528:DyaK3MXjvFOktw%3D%3D 10.1083/jcb.112.1.135 1986002 (Pubitemid 21909606)
49. E Ozawa 1998 From dystrophinopathy to sarcoglycanopathy: evolution of a concept of muscular dystrophy Muscle Nerve 21 421 438 1:STN:280: DyaK1c7pt1Clsw%3D%3D 10.1002/(SICI)1097-4598(199804)21:4<421::AID-MUS1>3. 0.CO;2-B 9533777 (Pubitemid 28145319)
50. C Pasternak E Elson 1985 Lymphocyte mechanical response triggered by cross-linking surface receptors J Cell Biol 100 860 872 1:CAS:528: DyaL2MXhsVOgtLo%3D 10.1083/jcb.100.3.860 4038710 (Pubitemid 15135347)
51. C Pasternak S Wong E Elson 1995 Mechanical function of dystrophin in muscle cells J Cell Biol 128 3 355 361 1:CAS:528:DyaK2MXjt1Cju7s%3D 10.1083/jcb.128.3.355 7844149
52. J Pellicer V García-Morales MJ Hernández 2000 On the demonstration of the Young-Laplace equation in introductory physics courses Phys Educ 35 2 126 129 10.1088/0031-9120/35/2/309
53. N Petersen W McConnaughey E Elson 1982 Dependence of locally measured cellular deformability on position on the cell, temperature, and cytochalasin B Proc Natl Acad Sci USA 79 5327 5331 1:STN:280:DyaL3s%2FjvFelsA%3D%3D 10.1073/pnas.79.17.5327 6957866 (Pubitemid 12002205)
54. B Petrof J Shrager H Stedman A Kelly L Sweeney 1993 Dystrophin protect the sarcolemma from stresses developed during muscle contraction Proc Natl Acad Sci USA 90 3710 3714 1:CAS:528:DyaK3sXktVKnsb4%3D 10.1073/pnas.90.8.3710 8475120 (Pubitemid 23111437)
55. G Porter G Dmytrenko J Winkelmann R Bloch 1992 Dystrophin colocalizes with beta-spectrin in distinct subsarcolemmal domains in mammalian skeletal muscle J Cell Biol 117 5 997 1005 1:CAS:528:DyaK38XktVGntLc%3D 10.1083/jcb.117.5.997 1577872
56. NL Quach TA Rando 2006 Focal adhesion kinase is essential for costamerogenesis in cultured skeletal muscle cells Dev Biol 293 38 52 1:CAS:528:DC%2BD28XjvVGit7c%3D 10.1016/j.ydbio.2005.12.040 16533505
57. RP Rand 1964 Mechanical properties of the red cell membrane Biophys J 4 303 316 1:STN:280:DyaF2M%2Fgt1WlsA%3D%3D 10.1016/S0006-3495(64)86784-9 14197789
58. S Rapoport 1972 Mechanical properties of the sarcolemma and myoplasm in frog muscle as a function of sarcomere length J Gen Physiol 59 559 585 10.1085/jgp.59.5.559 4537306
59. P Reed RJ Bloch 2005 Postnatal changes in sarcolemmal organization in mdx mouse Neuromuscul Disord 15 8 552 561 10.1016/j.nmd.2005.03.007 16051092 (Pubitemid 41033010)
60. I Rybakova J Patel J Ervasti 2000 The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin J Cell Biol 150 5 1209 1214 1:CAS:528:DC%2BD3cXmtlegtb8%3D 10.1083/jcb.150.5.1209 10974007
61. S Shah J Davis N Weisleder I Kostavassili A McCulloch E Raltson Y Capetanaki R Lieber 2004 Structural and functional roles of desmin in mouse skeletal muscle during passive deformation Biophys J 86 2993 3008 1:CAS:528:DC%2BD2cXjvVyjurc%3D 10.1016/S0006-3495(04)74349-0 15111414 (Pubitemid 38552702)
62. MR Stone A O'Neill R Lovering J Strong WG Resneck PW Reed D Toivola J Ursitti BM Omary RJ Bloch 2007 Absence of keratin 19 in mice causes skeletal myopathy with mitochondrial and sarcolemmal reorganization J Cell Sci 120 22 3999 4008 1:CAS:528:DC%2BD2sXhsVOru73M 10.1242/jcs.009241 17971417 (Pubitemid 350269405)
63. V Straub R Bittner J Leger T Voit 1991 Direct visualization of the dystrophin network on skeletal muscle fiber membrane J Cell Biol 119 5 1183 1191 10.1083/jcb.119.5.1183
64. SE Street 1983 Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters J Cell Physiol 114 346 364 1:STN:280:DyaL3s7mtFektg%3D%3D 10.1002/jcp.1041140314 6601109 (Pubitemid 13161556)
65. Taylor R (2005) Classical mechanics. University Science Books, Sausalito
66. O Thoumine O Cardoso JJ Meister 1999 Changes in the mechanical properties of fibroblasts during spreading: a micromanipulation study Eur Biophys J 28 3 222 234 1:STN:280:DyaK1M3gvFSitA%3D%3D 10.1007/s002490050203 10192936 (Pubitemid 29225600)
67. R Trans-Son-Tay D Needham A Yeung M Hochmuth 1991 Time-dependent recovery of passive neutrophils after large deformation Biophys J 60 4 856 866 10.1016/S0006-3495(91)82119-1
68. M Tsai R Frank R Waugh 1993 Passive mechanical behavior of human neutrophils: power law fluid Biophys J 65 2078 2088 1:STN:280: DyaK2c7ivVyqtg%3D%3D 10.1016/S0006-3495(93)81238-4 8298037 (Pubitemid 23334875)
69. JA Ursitti PC Lee WG Resneck MM McNally AL Bowman A O'Neill MR Stone RJ Bloch 2004 Cloning and characterization of cytokeratins 8 and 19 in adult rat striated muscle. Interaction with the dystrophin glycoprotein complex J Biol Chem 279 40 41830 41838 1:CAS:528:DC%2BD2cXnvFWgurg%3D 10.1074/jbc.M400128200 15247274 (Pubitemid 39313631)
70. E Waugh E Evans 1979 Thermoelasticity of red blood cell membrane Biophys J 26 115 132 1:STN:280:DyaL3M3ls1ymug%3D%3D 10.1016/S0006-3495(79)85239-X 262408
71. S Wieneke R Stehle Z Li H Jockusch 2000 Generation of tension by skinned fibers and intact skeletal muscles from desmin-deficient mice Biochem Biophys Res Commun 278 419 425 1:CAS:528:DC%2BD3cXotlKksb4%3D 10.1006/bbrc.2000.3810 11097852
72. MW Williams RJ Bloch 1999 Extensive but coordinate reorganization of the membrane skeleton in myofibers of dystrophic (mdx) mice J Cell Biol 144 1259 1270 1:CAS:528:DyaK1MXitVKjtbg%3D 10.1083/jcb.144.6.1259 10087268 (Pubitemid 29157303)
73. MW Williams RJ Bloch 1999 Differential distribution of dystrophin and beta-spectrin at the sarcolemma of fast twitch skeletal muscle fibers J Muscle Res Cell Motil 20 383 393 1:CAS:528:DyaK1MXntFOntbs%3D 10.1023/A:1005512217552 10531619 (Pubitemid 29457250)
74. S Winder 1997 The membrane-cytoskeleton interface: the role of dystrophin and utrophin J Muscle Res Cell Motil 18 617 629 1:CAS:528:DyaK1cXjvFOnuw%3D%3D 10.1023/A:1018627705273 9429156 (Pubitemid 27519512)
75. E Wojcikiewicz X Zhang V Moy 2004 Force and compliance measurements on living cells using Atomic Force Microscopy (AFM) Biol Proced Online 6 1 9 1:CAS:528:DC%2BD2cXktVKlt7c%3D 10.1251/bpo67 14737221 (Pubitemid 38597698)
76. AV Wolff AK Niday KA Voelker JA Call NP Evans KP Granata RW Grange 2006 Passive mechanical properties of maturing extensor digitorum longus are not affected by lack of dystrophin Muscle Nerve 34 3 304 312 1:CAS:528: DC%2BD28XpvVems7Y%3D 10.1002/mus.20588 16770793 (Pubitemid 44300161)
77. Q Zhang X Wang X Wei W Chen 2007 Characterization of viscoelastic properties of normal and osteoarthritic chondrocytes in experimental rabbit model Osteoarthr Cartil 16 7 837 840 1:CAS:528:DC%2BD2sXmsVWntr0%3D 10.1016/j.joca.2007.09.016 18032072
78. E Zubrzycka-Gaarn D Bulman G Karpati, et al. 1988 The Duchenne muscular dystrophy gene product is localized in sarcolemma of human skeletal muscle Nature 333 6172 466 469 1:CAS:528:DyaL1cXlt1Krt78%3D 10.1038/333466a0 3287171