Lateral transmission of force is impaired in skeletal muscles of dystrophic mice and very old rats

Journal of Physiology

Volumn 589, Issue 5, 2011, Pages 1195-1208

  Ramaswamy, Krishnan S ^a   Palmer, Mark L ^a,e   Van Der Meulen, Jack H ^b   Renoux, Abigail ^c   Kostrominova, Tatiana Y ^c   Michele, Daniel E ^c,d   Faulkner, John A ^a,c  

^a Department of Biomedical Engineering ^*  (United States)

^b Department of Surgery   (United States)

^c Molecular and Integrative Physiology   (United States)

^d Internal Medicine in the Medical School   (United States)

^e UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; GLYCOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; EPIMYSIUM; EXTENSOR DIGITORUM LONGUS MUSCLE; EXTRACELLULAR MATRIX; GENE DISRUPTION; GENE MUTATION; MALE; MOUSE; MUSCLE FORCE; MUSCULAR DYSTROPHY; MUSCULOSKELETAL FUNCTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TIBIALIS ANTERIOR MUSCLE;

AGING; ANIMALS; BLOTTING, WESTERN; DYSTROPHIN; MALE; MICE; MICE, INBRED MDX; MUSCLE CONTRACTION; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; RATS;

EID: 79951974764     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.201921     Document Type: Article

References (54)

1. Abmayr S & Chamberlain JS (2006). The structure and function of dystrophin. In The Molecular Mechanisms of Muscular Dystrophy, ed. Winder S, Landes Bioscience, Georgetown.
2. Anastasi G, Cutroneo G, Santoro G, Arco A, Rizzo G, Bramanti P, Rinaldi C, Sidoti A, Amato A & Favaloro A (2008). Costameric proteins in human skeletal muscle during muscular inactivity. J Anat 213, 284-295.
3. Bansal D, Miyake K, Vogel SS, Groh S, Chen CC, Williamson R, McNeil PL & Campbell KP (2003). Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 423, 168-172.
4. Bloch RJ & Gonzalez-Serratos H (2003). Lateral force transmission across costameres in skeletal muscle. Exerc Sport Sci Rev 31, 73-78.
5. Bloch RJ, Reed P, O'Neill A, Strong J, Williams M, Porter N & Gonzalez-Serratos H (2004). Costameres mediate force transduction in healthy skeletal muscle and are altered in muscular dystrophies. J Muscle Res Cell Motil 25, 590-592.
6. Brooks SV & Faulkner JA (1988). Contractile properties of skeletal muscles from young, adult and aged mice. J Physiol 404, 71-82.
7. Brooks SV & Faulkner JA (1996). The magnitude of the initial injury induced by stretches of maximally activated muscle fibres of mice and rats increases in old age. J Physiol 497, 573-580.
8. Burkholder TJ, Fingado B, Baron S & Lieber RL (1994). Relationship between muscle fiber types and sizes and muscle architectural properties in the mouse hindlimb. J Morphol 221, 177-190.
9. Campbell MJ, McComas AJ & Petito F (1973). Physiological changes in aging muscles. J Neurol Neurosurg Psych 36, 174-182.
10. Campbell KP & Stull JT (2003). Skeletal muscle basement membrane-sarcolemma-cytoskeleton interaction minireview series. J Biol Chem 278, 12599-12600.
11. Carlson BM, Borisov AB, Dedkov EI, Khalyfa A, Kostrominova TY, Macpherson PC, Wang E & Faulkner JA (2002). Effects of long-term denervation on skeletal muscle in old rats. J Gerontol A Biol Sci Med Sci 57, B366-B374.
12. Claflin DR & Brooks SV (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.
13. Dedrick ME & Clarkson PM (1990). The effects of eccentric exercise on motor performance in young and older women. Eur J Appl Physiol Occup Physiol 60, 183-186.
14. DelloRusso C, Crawford RW, Chamberlain JS & Brooks SV (2001). Tibialis anterior muscles in mdx mice are highly susceptible to contraction-induced injury. J Muscle Res Cell Motil 22, 467-475.
15. Doherty TJ, Vandervoort AA, Taylor AW & Brown WF (1993). Effects of motor unit losses on strength in older men and women. J Appl Physiol 74, 868-874.
16. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
17. Ervasti JM (2003). Costameres: the Achilles' heel of Herculean muscle. J Biol Chem 278, 13591-13594.
18. Ervasti JM & Campbell KP (1991). Membrane organization of the dystrophin-glycoprotein complex. Cell 66, 1121-1131.
19. Ervasti JM & Campbell KP (1993). A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122, 809-823.
20. Ervasti JM, Ohlendieck K, Kahl SD, Gaver MG & Campbell KP (1990). Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 345, 315-319.
21. Faulkner JA (2003). Terminology for contractions of muscles during shortening, while isometric, and during lengthening. J Appl Physiol 95, 455-459.
22. Faulkner JA, Davis CS, Mendias CL & Brooks SV (2008). The aging of elite male athletes: age-related changes in performance and skeletal muscle structure and function. Clin J Sport Med 18, 501-507.
23. Frontera WR, Hughes VA, Lutz KJ & Evans WJ (1991). A cross-sectional study of muscle strength and mass in 45- to 78-yr-old men and women. J Appl Physiol 71, 644-650.
24. Gao Y, Kostrominova TY, Faulkner JA & Wineman AS (2008a). Age-related changes in the mechanical properties of the epimysium in skeletal muscles of rats. J Biomech 41, 465-469.
25. Gao Y, Waas AM, Faulkner JA, Kostrominova TY & Wineman AS (2008b). Micromechanical modeling of the epimysium of the skeletal muscles. J Biomech 41, 1-10.
26. Gordon AM, Huxley AF & Julian FJ (1966). The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184, 170-192.
27. Grimby G & Saltin B (1983). The ageing muscle. Clin Physiol 3, 209-218.
28. 2+ homeostasis during fatigue. Exp Physiol 95, 641-656.
29. Henry MD & Campbell KP (1996). Dystroglycan: an extracellular matrix receptor linked to the cytoskeleton. Curr Opin Cell Biol 8, 625-631.
30. Hoffman EP, Brown RH Jr & Kunkel LM (1987). Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51, 919-928.
31. Huijing PA (2003). Muscular force transmission necessitates a multilevel integrative approach to the analysis of function of skeletal muscle. Exerc Sport Sci Rev 31, 167-175.
32. Kanda K, Hashizume K, Nomoto E & Asaki S (1986). The effects of aging on physiological properties of fast and slow twitch motor units in the rat gastrocnemius. Neurosci Res 3, 242-246.
33. Kjaer M (2004). Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84, 649-698.
34. Lapidos KA, Kakkar R & McNally EM (2004). The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ Res 94, 1023-1031.
35. Larsson L, Ansved T, Edstrom L, Gorza L & Schiaffino S (1991). Effects of age on physiological, immunohistochemical and biochemical properties of fast-twitch single motor units in the rat. J Physiol 443, 257-275.
36. Lexell J, Taylor CC & Sjostrom M (1988). What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84, 275-294.
37. Li S, Kimura E, Ng R, Fall BM, Meuse L, Reyes M, Faulkner JA & Chamberlain JS (2006). A highly functional mini-dystrophin/GFP fusion gene for cell and gene therapy studies of Duchenne muscular dystrophy. Hum Mol Genet 15, 1610-1622.
38. Lynch GS, Hinkle RT, Chamberlain JS, Brooks SV & Faulkner JA (2001). Force and power output of fast and slow skeletal muscles from mdx mice 6-28 months old. J Physiol 535, 591-600.
39. Macpherson PC, Dennis RG & Faulkner JA (1997). Sarcomere dynamics and contraction-induced injury to maximally activated single muscle fibres from soleus muscles of rats. J Physiol 500, 523-533.
40. Michele DE & Campbell KP (2003). Dystrophin-glycoprotein complex: post-translational processing and dystroglycan function. J Biol Chem 278, 15457-15460.
41. Panchangam A, Claflin DR, Palmer ML & Faulkner JA (2008). Magnitude of sarcomere extension correlates with initial sarcomere length during lengthening of activated single fibers from soleus muscle of rats. Biophys J 95, 1890-1901.
42. 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 U S A 80, 1008-1012.
43. Pastoret C & Sebille A (1995). Mdx mice show progressive weakness and muscle deterioration with age. J Neurol Sci 129, 97-105.
44. Patel TJ & Lieber RL (1997). Force transmission in skeletal muscle: from actomyosin to external tendons. Exerc Sport Sci Rev 25, 321-363.
45. Paul AC, Sheard PW, Kaufman SJ & Duxson MJ (2002). Localization of α7 integrins and dystrophin suggests potential for both lateral and longitudinal transmission of tension in large mammalian muscles. Cell Tissue Res 308, 255-265.
46. Pirozzolo FJ & Maletta GJ (1982). The Aging Motor System. Praeger Publishers, New York.
47. Ploutz-Snyder LL, Giamis EL, Formikell M & Rosenbaum AE (2001). Resistance training reduces susceptibility to eccentric exercise-induced muscle dysfunction in older women. J Gerontol A Biol Sci Med Sci 56, B384-B390.
48. Rader EP, Song W, Van Remmen H, Richardson A & Faulkner JA (2006). Raising the antioxidant levels within mouse muscle fibres does not affect contraction-induced injury. Exp Physiol 91, 781-789.
49. Renganathan M, Messi ML & Delbono O (1997). Dihydropyridine receptor-ryanodine receptor uncoupling in aged skeletal muscle. J Membr Biol 157, 247-253.
50. 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, 1209-1214.
51. Street SF (1983). Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 114, 346-364.
52. Worton R (1995). Muscular dystrophies: diseases of the dystrophin-glycoprotein complex. Science 270, 755-756.
53. Young A, Stokes M & Crowe M (1984). Size and strength of the quadriceps muscles of old and young women. Eur J Clin Invest 14, 282-287.
54. Young A, Stokes M & Crowe M (1985). The size and strength of the quadriceps muscles of old and young men. Clin Physiol 5, 145-154.