Collagen content does not alter the passive mechanical properties of fibrotic skeletal muscle in mdx mice

American Journal of Physiology - Cell Physiology

Volumn 306, Issue 10, 2014, Pages

  Smith, Lucas R ^a   Barton, Elisabeth R ^a  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

Collagen; Fibrosis; Passive mechanics; Skeletal muscle

Indexed keywords

COLLAGEN; HYDROXYPROLINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIAPHRAGM MUSCLE; EXTENSOR DIGITORUM LONGUS MUSCLE; FIBROSIS; MALE; MECHANICS; MICROSCOPY; MOUSE; MOUSE MODEL; MUSCLE RIGIDITY; MUSCLE STRENGTH; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE; SOLEUS MUSCLE; VISCOSITY;

COLLAGEN; FIBROSIS; PASSIVE MECHANICS; SKELETAL MUSCLE;

ANIMALS; BIOMECHANICAL PHENOMENA; COLLAGEN; DIAPHRAGM; DISEASE MODELS, ANIMAL; ELASTICITY; EXTRACELLULAR MATRIX; FIBROSIS; HYDROXYPROLINE; MALE; MICE; MICE, INBRED MDX; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; VISCOSITY;

EID: 84900540434     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00383.2013     Document Type: Article

References (55)

1. Abbott BC, Lowy J. Stress relaxation in muscle. Proc R Soc Lond B Biol Sci 146: 281-288, 1956.
2. Acuna MJ, Pessina P, Olguin H, Cabrera D, Vio CP, Bader M, Munoz-Canoves P, Santos RA, Cabello-Verrugio C, Brandan E. Restoration of muscle strength in dystrophic muscle by angiotensin-1-7 through inhibition of TGF-beta signalling. Hum Mol Genet 25: 1237-1249, 2014.
3. Ardite E, Perdiguero E, Vidal B, Gutarra S, Serrano AL, Munoz-Canoves P. PAI-1-regulated miR-21 defines a novel age-associated fibrogenic pathway in muscular dystrophy. J Cell Biol 196: 163-175, 2012.
4. Avery NC, Bailey AJ. Enzymic and non-enzymic cross-linking mechanisms in relation to turnover of collagen: relevance to aging and exercise. Scand J Med Sci Sports 15: 231-240, 2005.
5. Barton ER, Morris L, Kawana M, Bish LT, Toursel T. Systemic administration of L-arginine benefits mdx skeletal muscle function. Muscle Nerve 32: 751-760, 2005.
6. Berquin A, Schmit P, Moens P, Lebacq J. Compliance of normal, dystrophic and transplanted mouse muscles. J Biomech 27: 1331-1337, 1994.
7. Bobet J, Mooney RF, Gordon T. Force and stiffness of old dystrophic (mdx) mouse skeletal muscles. Muscle Nerve 21: 536-539, 1998.
8. Bulfield G, Siller WG, Wight PA, Moore KJ. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81: 1189-1192, 1984.
9. Burkholder TJ, Lieber RL. Sarcomere length operating range of vertebrate muscles during movement. J Exp Biol 204: 1529-1536, 2001.
10. de Jong S, van Veen TA, de Bakker JM, van Rijen HV. Monitoring cardiac fibrosis: a technical challenge. Neth Heart J 20: 44-48, 2012.
11. Flesch M, Schiffer F, Zolk O, Pinto Y, Rosenkranz S, Hirth-Dietrich C, Arnold G, Paul M, Bohm M. Contractile systolic and diastolic dysfunction in renin-induced hypertensive cardiomyopathy. Hypertension 30: 383-391, 1997.
12. Garlich MW, Baltgalvis KA, Call JA, Dorsey LL, Lowe DA. Plantarflexion contracture in the mdx mouse. Am J Phys Med Rehabil 89: 976-985, 2010.
13. Gillies AR, Lieber RL. Structure and function of the skeletal muscle extracellular matrix. Muscle Nerve 44: 318-331, 2011.
14. Gillies AR, Smith LR, Lieber RL, Varghese S. Method for decellularizing skeletal muscle without detergents or proteolytic enzymes. Tissue Eng Part C Methods 17: 383-389, 2011.
15. Gindre J, Takaza M, Moerman KM, Simms CK. A structural model of passive skeletal muscle shows two reinforcement processes in resisting deformation. J Mech Behav Biomed Mater 22: 84-94, 2013.
16. Gosselin LE, Martinez DA, Vailas AC, Sieck GC. Passive length-force properties of senescent diaphragm: relationship with collagen characteristics. J Appl Physiol 76: 2680-2685, 1994.
17. Hakim CH, Duan D. Gender differences in contractile and passive properties of mdx extensor digitorum longus muscle. Muscle Nerve 45: 250-256, 2012.
18. Hakim CH, Duan D. Truncated dystrophins reduce muscle stiffness in the extensor digitorum longus muscle of mdx mice. J Appl Physiol 114: 482-489, 2013.
19. Hakim CH, Grange RW, Duan D. The passive mechanical properties of the extensor digitorum longus muscle are compromised in 2-to 20-mo-old mdx mice. J Appl Physiol 110: 1656-1663, 2011.
20. Haslett JN, Kang PB, Han M, Kho AT, Sanoudou D, Volinski JM, Beggs AH, Kohane IS, Kunkel LM. The influence of muscle type and dystrophin deficiency on murine expression profiles. Mamm Genome 16: 739-748, 2005.
21. Haus JM, Carrithers JA, Trappe SW, Trappe TA. Collagen, crosslinking, and advanced glycation end products in aging human skeletal muscle. J Appl Physiol 103: 2068-2076, 2007.
22. Heydemann A, Huber JM, Demonbreun A, Hadhazy M, McNally EM. Genetic background influences muscular dystrophy. Neuromuscul Disord 15: 601-609, 2005.
23. Klingler W, Jurkat-Rott K, Lehmann-Horn F, Schleip R. The role of fibrosis in Duchenne muscular dystrophy. Acta Myol 31: 184-195, 2012.
24. Kumar A, Khandelwal N, Malya R, Reid MB, Boriek AM. Loss of dystrophin causes aberrant mechanotransduction in skeletal muscle fibers. FASEB J 18: 102-113, 2004.
25. Law DJ, Caputo A, Tidball JG. Site and mechanics of failure in normal and dystrophin-deficient skeletal muscle. Muscle Nerve 18: 216-223, 1995.
26. Lieber RL, Ward SR. Cellular mechanisms of tissue fibrosis. 4. Structural and functional consequences of skeletal muscle fibrosis. Am J Physiol Cell Physiol 305: C241-C252, 2013.
27. MacKenna DA, Omens JH, McCulloch AD, Covell JW. Contribution of collagen matrix to passive left ventricular mechanics in isolated rat hearts. Am J Physiol Heart Circ Physiol 266: H1007-H1018, 1994.
28. Magnusson SP. Passive properties of human skeletal muscle during stretch maneuvers. A review. Scand J Med Sci Sports 8: 65-77, 1998.
29. Mann CJ, Perdiguero E, Kharraz Y, Aguilar S, Pessina P, Serrano AL, Munoz-Canoves P. Aberrant repair and fibrosis development in skeletal muscle. Skelet Muscle 1: 21, 2011.
30. Mendez J, Keys A. Density and composition of mammalian muscle. Metabolism 9: 184-188, 1960.
31. Meyer GA, Lieber RL. Elucidation of extracellular matrix mechanics from muscle fibers and fiber bundles. J Biomech 44: 771-773, 2011.
32. Moorwood C, Liu M, Tian Z, Barton ER. Isometric and eccentric force generation assessment of skeletal muscles isolated from murine models of muscular dystrophies. J Vis Exp 71: e50036, 2013.
33. Murray JD, Canan BD, Martin CD, Stangland JE, Rastogi N, Rafael-Fortney JA, Janssen PM. The force-temperature relationship in healthy and dystrophic mouse diaphragm; implications for translational study design. Front Physiol 3: 422, 2012.
34. Nyska A, Dayan D. Ameloblastic fibroma in a young cat. J Oral Pathol Med 24: 233-236, 1995.
35. Palokangas H, Kovanen V, Duncan A, Robins SP. Age-related changes in the concentration of hydroxypyridinium crosslinks in functionally different skeletal muscles. Matrix 12: 291-296, 1992.
36. Petrof BJ, Stedman HH, Shrager JB, Eby J, Sweeney HL, Kelly AM. Adaptations in myosin heavy chain expression and contractile function in dystrophic mouse diaphragm. Am J Physiol Cell Physiol 265: C834-C841, 1993.
37. Pierard GE. Sirius red polarization method is useful to visualize the organization of connective tissues but not the molecular composition of their fibrous polymers. Matrix 9: 68-71, 1989.
38. Prado LG, Makarenko I, Andresen C, Kruger M, Opitz CA, Linke WA. Isoform diversity of giant proteins in relation to passive and active contractile properties of rabbit skeletal muscles. J Gen Physiol 126: 461-480, 2005.
39. Provenzano PP, Vanderby R Jr. Collagen fibril morphology and organization: implications for force transmission in ligament and tendon. Matrix Biol 25: 71-84, 2006.
40. Rich L, Whittaker P. Collagen and picosirius red staining: a polarized light assessment of fibrillar hue and spatial distribution. Braz J Morphol Sci 22: 97-104, 2005.
41. Shirani J, Pick R, Roberts WC, Maron BJ. Morphology and significance of the left ventricular collagen network in young patients with hypertrophic cardiomyopathy and sudden cardiac death. J Am Coll Cardiol 35: 36-44, 2000.
42. Smith LR, Lee KS, Ward SR, Chambers HG, Lieber RL. Hamstring contractures in children with spastic cerebral palsy result from a stiffer extracellular matrix and increased in vivo sarcomere length. J Physiol 589: 2625-2639, 2011.
43. Stedman HH, Sweeney HL, Shrager JB, Maguire HC, Panettieri RA, Petrof B, Narusawa M, Leferovich JM, Sladky JT, Kelly AM. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352: 536-539, 1991.
44. Swaggart KA, Heydemann A, Palmer AA, McNally EM. Distinct genetic regions modify specific muscle groups in muscular dystrophy. Physiol Genomics 43: 24-31, 2011.
45. Tabel GM, Whittaker P, Vlachonassios K, Sonawala M, Chandraratna PA. Collagen fiber morphology determines echogenicity of myocardial scar: implications for image interpretation. Echocardiography 23: 103-107, 2006.
46. Tirrell TF, Cook MS, Carr JA, Lin E, Ward SR, Lieber RL. Human skeletal muscle biochemical diversity. J Exp Biol 215: 2551-2559, 2012.
47. Trensz F, Haroun S, Cloutier A, Richter MV, Grenier G. A muscle resident cell population promotes fibrosis in hindlimb skeletal muscles of mdx mice through the Wnt canonical pathway. Am J Physiol Cell Physiol 299: C939-C947, 2010.
48. Vij R, Vij H, Rao NN. Evaluation of collagen in connective tissue walls of odontogenic cysts-a histochemical study. J Oral Pathol Med 40: 257-262, 2011.
49. Wang K, McCarter R, Wright J, Beverly J, Ramirez-Mitchell R. Regulation of skeletal muscle stiffness and elasticity by titin isoforms: a test of the segmental extension model of resting tension. Proc Natl Acad Sci USA 88: 7101-7105, 1991.
50. Ward SR, Tomiya A, Regev GJ, Thacker BE, Benzl RC, Kim CW, Lieber RL. Passive mechanical properties of the lumbar multifidus muscle support its role as a stabilizer. J Biomech 42: 1384-1389, 2009.
51. Whittaker P, Boughner DR, Kloner RA. Analysis of healing after myocardial infarction using polarized light microscopy. Am J Pathol 134: 879-893, 1989.
52. Whittaker P, Kloner RA, Boughner DR, Pickering JG. Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light. Basic Res Cardiol 89: 397-410, 1994.
53. Wolff AV, Niday AK, Voelker KA, Call JA, Evans NP, Granata KP, Grange RW. Passive mechanical properties of maturing extensor digitorum longus are not affected by lack of dystrophin. Muscle Nerve 34: 304-312, 2006.
54. Zhou L, Lu H. Targeting fibrosis in Duchenne muscular dystrophy. J Neuropathol Exp Neurol 69: 771-776, 2010.
55. Zou Y, Zwolanek D, Izu Y, Gandhy S, Schreiber G, Brockmann K, Devoto M, Tian Z, Hu Y, Veit G, Meier M, Stetefeld J, Hicks D, Straub V, Voermans NC, Birk DE, Barton ER, Koch M, Bonnemann CG. Recessive and dominant mutations in COL12A1 cause a novel EDS/myopathy overlap syndrome in humans and mice. Hum Mol Genet 2014 Jan 20 [Epub ahead of print].