Disease course in mdx:Utrophin+/− mice: comparison of three mouse models of duchenne muscular dystrophy

Physiological Reports

Volumn 3, Issue 4, 2015, Pages

  McDonald, Abby A ^a   Hebert, Sadie L ^a   Kunz, Matthew D ^a   Ralles, Steven J ^a   McLoon, Linda K ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Collagen; Dystrophin; Fibrosis; Mouse models; Muscle disease; Muscle function; Muscular dystrophy; Skeletal muscle; Utrophin

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 4; DYSTROPHIN; TRANSCRIPTION FACTOR PAX7; UTROPHIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; FEMALE; FIBROSIS; GENOTYPE; GRIP STRENGTH TEST; IMMUNOHISTOCHEMISTRY; MALE; MORPHOMETRICS; MOUSE; MUSCLE FUNCTION; NONHUMAN; PROTEIN EXPRESSION; ROTAROD TEST;

EID: 85003689164     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12391     Document Type: Article

References (70)

1. Anderson, B. C., S. P. Christiansen, S. Grandt, R. W. Grange, and L. K. McLoon. 2006. Increased extraocular muscle strength with direct injection of insulin-like growth factor-1. Invest. Ophthalmol. Vis. Sci. 47:2461–2467.
2. Arechavala-Gomeza, V., M. Kinali, L. Feng, M. Guglieri, G. Edge, M. Main, et al. 2010. Revertant fibres and dystrophin traces in Duchenne muscular dystrophy: implication for clinical trials. Neuromuscul. Disord. 20:295–301.
3. Baker, P. E., J. A. Kearney, B. Gong, A. P. Merriam, D. E. Kuhn, J. D. Porter, et al. 2006. Analysis of gene expression differences between utrophin/dystrophin-deficient vs mdx skeletal muscle reveals a specific upregulation of slow muscle genes in limb muscles. Neurogenetics 7: 1–91.
4. Brooks, S. V., and J. A. Faulkner. 1990. Contraction-induced injury: recovery of skeletal muscles in young and old mice. Am. J. Physiol. 258:C436–C442
5. Bulfield, G., W. G. Siller, P. A. L. Wight, and K. J. Moore. 1984. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl Acad. Sci. USA 81:1189–1192.
6. Campbell, K. P., and S. D. Kahl. 1989. Association of dystrophin and an integral membrane glycoprotein. Nature 338:259–262.
7. Carnwath, J. W., and D. M. Shotton. 1987. Muscular dystrophy in the mdx mouse: histopathology of the soleus and extensor digitorum longus muscles. J. Neurol. Sci. 80:39–54.
8. Connolly, A. M., R. M. Keeling, S. Mehta, A. Pestronk, and J. R. Sanes. 2001. Three mouse models of muscular dystrophy: the natural history of strength and fatigue in dystrophin-, dystrophin/utrophin-, and laminin a2-deficient mice. Neuromuscul. Disord. 11:703–712.
9. Coulton, G. R., N. A. Curtin, J. E. Morgan, and T. A. Partridge. 1988a. The mdx mouse skeletal muscle myopathy: II Contractile properties. Neuropathol. Appl. Neurobiol. 14:299–314.
10. Coulton, G. R., J. E. Morgan, T. A. Partridge, and J. C. Sloper. 1988b. The mdx mouse skeletal muscle myopathy: I. A histological, morphometric and biochemical investigation. Neuropathol. Appl. Neurobiol. 14:53–70.
11. Dangain, J., and G. Vrbova. 1984. Muscle development in mdx mutant mice. Muscle Nerve 7:700–704.
12. Deconinck, A. E., J. A. Rafael, J. A. Skinner, S. C. Brown, A. C. Potter, L. Metzinger, et al. 1997. Utrophin-dystrophin- deficient mice as a model for Duchenne muscular dystrophy. Cell 90:717–727.
13. Deconinck, N., J. A. Rafael, G. Beckers-Bleukx, D. Kahn, A. E. Deconinck, K. E. Davies, et al. 1998. 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.
14. Dellorusso, C., R. W. Crawford, J. S. Chamberlain, and S. V. Brooks. 2001. Tibialis anterior muscles in mdx mice are highly susceptible to contraction-induced injury. J. Muscle Res. Cell Motil. 22:467–475.
15. DiMario, J. X., A. Uzman, and R. C. Strohman. 1991. Fiber regeneration is not persistent in dystrophic (mdx) mouse skeletal muscle. Dev. Biol. 148:314–321.
16. Dupont-Versteegden, E. E., and R. J. McCarter. 1992. Differential expression of muscular dystrophy in diaphragm versus hindlimb muscles of mdx mice. Muscle Nerve 15:1105–1110.
17. Earnshaw, J. C., P. Kyprianou, K. Krishan, and G. K. Dhoot. 2002. Differentiation of original and regenerated skeletal muscle fibres in mdx dystrophic muscles. Histochem. Cell Biol. 118:19–27.
18. Emery, A. E. 1991. Population frequencies of inherited neuromuscular diseases–a world survey. Neuromuscul. Disord. 1:19–29.
19. Fairclough, R. J., A. Bareja, and K. E. Davies. 2011. Progress in therapy for Duchenne muscular dystrophy. Exp. Physiol. 96:1101–1113.
20. Gillies, A. R., and R. L. Lieber. 2011. Structure and function of the skeletal muscle extracellular matrix. Muscle Nerve 44:318–331.
21. Gomez, C. M., R. Maselli, J. E. Gundeck, M. Chao, J. W. Day, S. Tamamizu, et al. 1997. Slow-channel transgenic mice: a model of postsynaptic organellar degeneration at the neuromuscular junction. J. Neurosci. 17:4170–4179.
22. Grady, R. M., H. Teng, M. C. Nichol, J. C. Cunningham, R. S. Wilkinson, and J. R. Sanes. 1997. Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90:729–738.
23. Helliwell, T. R., N. T. Man, G. E. Morris, and K. E. Davies. 1992. The dystrophin-related protein, utrophin, is expressed on the sarcolemma of regenerating human skeletal muscle fibres in dystrophies and inflammatory myopathies. Neuromuscul. Disord. 2:177–184.
24. +/−mice. Muscle Nerve 43:263–267.
25. Huebner, K. D., D. S. Jassal, O. Halevy, M. Pines, and J. E. Anderson. 2008. Functional resolution of fibrosis in mdx mouse dystrophic heart and skeletal muscle by halofuginone. Am. J. Physiol. Heart Circ. Physiol. 294:H1550–H1561
26. Janssen, P. M., N. Hiranandani, T. A. Mays, and J. A. Rafael- Fortney. 2005. Utrophin deficiency worsens cardiac contractile dysfunction present in dystrophin-deficient mdx mice. Am. J. Physiol. Heart Circ. Physiol. 289:H2373–H2378
27. Kaspar, B. K., J. Llado, N. Sherkat, J. D. Rothstein, and F. H. Gage. 2003. Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 301:839–842.
28. Khurana, T. S., S. C. Watkins, P. Chafey, J. Chelly, F. Tome, M. Fardeau, et al. 1991. Immunolocalization and developmental expression of dystrophin related protein in skeletal muscle. Neuromuscul. Disord. 1:185–194.
29. Klein, S. M., J. Vykoukal, P. Lechler, K. Zeitler, S. Gehmert, S. Schreml, et al. 2012. Noninvasive in vivo assessment of muscle impairment in the mdx mouse model–A comparison of two common wire hanging methods with two different results. J. Neurosci. Methods 203: 292–297.
30. Kunkel, L. M., J. F. Hejtmanciks, C. T. Caskey, A. Speer, A. P. Monaco, W. Middlesworth, et al. 1986. Analysis of deletions in DNA from patients with Becker and Duchenne muscular dystrophy. Nature 322:73–77.
31. Lefaucheur, J. P., C. Pastoret, and A. Sebille. 1995. Phenotype of dystrophinopathy in old mdx mice. Anat. Rec. 242:70–76.
32. −/− mice. Hum. Mol. Genet. 23:4786–4800.
33. Lynch, G. S., R. T. Hinkle, J. S. Chamberlain, S. V. Brooks, and J. A. Faulkner. 2001. Force and power output of fast and slow skeletal muscles from mdx mice 6-28 months old. J. Physiol. 535:591–600.
34. Mariani, J. F., F. Pons, J. Leger, N. Loffreda, M. Anoal, M. Chevallay, et al. 1991. Expression of myosin heavy chain isoforms in Duchenne muscular dystrophy. Neuromuscul. Disord. 1:397–409.
35. Matsumura, K., and K. P. Campbell. 1994. Dystrophin- glycoprotein complex: its role in the molecular pathogenesis of muscular dystrophies. Muscle Nerve 17:2–15.
36. McNally, E. M., and P. Pytel. 2007. Muscle diseases: the muscular dystrophies. Annu. Rev. Pathol. 2:87–109.
37. Muller, J., N. Vayssiere, M. Royuela, M. E. Leger, A. Mutter, F. Bacou, et al. 2001. Comparative evolution of muscular dystrophy in diaphragm, gastrocnemius and masseter muscles from old male mdx mice. J. Muscle Res. Cell Motil. 22:133–139.
38. Muntoni, F., A. Mateddu, F. Marchei, A. Clerk, and G. Serra. 1993. Muscular weakness in the mdx mouse. J. Neurol. Sci. 120:71–77.
39. Musaro, A., K. McCullagh, A. Paul, L. Houghton, G. Dobrowolny, M. Molinaro, et al. 2001. Localized IGF-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat. Genet. 27:195–200.
40. Pane, M., E. S. Mazzone, L. Fanelli, R. De Sanctis, F. Bianco, S. Sivo, et al. 2014. Reliability of the performance of upper limb assessment in Duchenne muscular dystrophy. Neuromuscul. Disord. 24:201–206.
41. Pastoret, C., and A. Sebille. 1995. mdx mice show progressive weakness and muscle deterioration with age. J. Neurol. Sci. 129:97–105.
42. Pessina, P., D. Cabrera, M. G. Morales, C. A. Riquelme, J. Guitierrez, A. L. Serrano, et al. 2014. Novel and optimized strategies for inducing fibrosis in vivo: focus on Duchenne Muscular Dystrophy. Skelet Muscle 4:7. doi: 10.1186/2044-5040-4-7.
43. Pichavant, C., A. Aartsma-Rus, P. R. Clemens, K. E. Davies, G. Dickson, S. Takeda, et al. 2011. Current status of pharmaceutical and genetic therapeutic approaches to treat DMD. Mol. Ther. 19:830–840.
44. Quinlan, J. G., S. R. Johnson, M. K. McKee, and S. P. Lyden. 1992. Twitch and tetanus in mdx mouse muscle. Muscle Nerve 15:837–842.
45. Rafael, J. A., J. M. Tinsley, A. C. Potter, A. E. Deconinck, and K. E. Davies. 1998. Skeletal muscle-specific expression of a utrophin transgene rescues utrophin-dystrophin deficient mice. Nature 19:79–82.
46. Reiser, P. J., R. L. Moss, G. G. Giulian, and M. L. Greaser. 1985. Shortening velocity in single fibers from adult rabbit soleus muscles is correlated with myosin heavy chain composition. J. Biol. Chem. 260:9077–9080.
47. Renault, V., G. Prion-Hamelin, C. Forestier, S. DiDonna, S. Decary, F. Hentati, et al. 2000. Skeletal muscle regeneration and the mitotic clock. Exp. Gerontol. 35:711–719.
48. Ricard-Blum, S., and F. Ruggierio. 2005. The collagen superfamily: from extracellular matrix to the cell membrane. Pathol. Biol. 53:430–442.
49. Schleip, R., I. L. Naylor, D. Ursu, W. Melzer, A. Zorn, H. J. Wilke, et al. 2006. Passive muscle stiffness may be influenced by active contractility of intramuscular connective tissue. Med. Hypotheses 66:66–71.
50. Seale, P., L. A. Sabourin, A. Girgis-Gabardo, A. Mansouri, P. Gruss, and M. A. Rudnicki. 2000. Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–786.
51. Sicinski, P., Y. Geng, A. S. Ryder-Cook, E. A. Barnard, M. Darlison, and P. J. Barnard. 1989. The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244:1578–1580.
52. Snow, L. M., L. K. McLoon, and L. V. Thompson. 2005. Adult and developmental myosin heavy chain isoforms in soleus muscle of aging Fischer Brown Norway rat. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 286:866–873.
53. Spassov, A., T. Gredes, T. Gedrange, S. Lucke, S. Morgenstern, D. Pavlovic, et al. 2013. Differential expression of myosin heavy chain isoforms in the masticatory muscles of dystrophin-deficient mice. Eur. J. Orthod. 33:613–619.
54. Spurney, C. F., H. Gordish-Dressman, A. D. Guerron, A. Sali, G. S. Pandey, R. Rawat, et al. 2009. Preclinical drug trials in the mdx mouse: assessment of reliable and sensitive outcome measures. Muscle Nerve 39:591–602.
55. Stedman, H. H., H. L. Sweeney, J. B. Shrager, H. C. Maguire, R. A. Panettieri, B. Petrof, et al. 1991. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352: 536–539.
56. Steinberger, M., M. F ӧ ller, S. Vogelgesang, M. Krautwald, M. Landsberger, C. K. Winkler, et al. 2014. Lack of the serum- and glucocorticoid-inducible kinase SGK1 improves muscle force characteristics and attenuates fibrosis in dystrophic mdx mouse muscle. Pflugers Arch. doi: 10.1007/s00424-014-1645-5 [Epub ahead of print]
57. Sweeney, H. L., M. J. Kushmerick, K. Mabuchi, J. Gergely, and F. A. Sreter. 1986. Velocity of shortening and myosin isozymes in two types of rabbit fast-twitch muscle fibers. Am. J. Physiol. 251:C431–C434
58. Swiderski, K., M. Todorov, S. M. Gehring, T. Naim, A. Chee, D. I. Stapleton, et al. 2014. Transilast administration reduces fibrosis and improves fatigue resistance in muscles of mdx dystrophic mice. Fibrogenesis Tissue Repair 7:1. doi: 10.1186/1755-1536-7-1.
59. Tan, N., and J. B. Lansman. 2014. Utrophin regulates modal gating of mechanosensitive ion channels in dystrophic skeletal muscle. J. Physiol. 15:3303–3323.
60. Tanganyika-deWinter, C. L., H. Heemskerk, T. G. Karnaoukh, M. van Putten, S. J. de Kimpe, J. van Deutekom, et al. 2012. Long-term exon skipping studies with 2 0 -P-methyl phosphorothioate antisense oligonucleotides in dystrophic mouse models. Mol. Ther. Nucleic. Acids 1:e66
61. Tinsley, J. M., A. C. Potter, S. R. Phelps, R. Fisher, J. I. Trickett, and K. E. Davies. 1996. Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature 384:349–353.
62. Tinsley, J., N. Deconinck, R. Fisher, D. Kahn, S. Phelps, J. M. Gillis, et al. 1998. Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat. Med. 4:1441–1444.
63. Turgeman, T., Y. Hagai, K. Huebner, D. S. Jassal, J. E. Anderson, O. Genin, et al. 2008. Prevention of muscle fibrosis and improvement in muscle performance in the mdx mouse by halofuginone. Neuromuscul. Disord. 18: 857–868
64. van Putten, M., C. de Winter, W. van Roon-Mom, G. J. van Ommen, P. A. C. ‘t Hoen, and A. Aartsma-Rus. 2010. A 3-months mild functional test regime does not affect disease parameters in young mdx mice. Neuromuscul. Disord. 20:273–280
65. van Putten, M., D. Kumar, M. Hulsker, W. M. H. Hoogaars, J. J. Plomp, A. van Opstal, et al. 2012. Comparison of skeletal muscle pathology and motor function of dystrophin and utrophin deficient mouse strains. Neuromuscul. Disord. 22:406–417.
66. Wakefield, P. M., J. M. Tinsley, M. J. Wood, R. Gilbert, G. Karpati, and K. E. Davies. 2000. Prevention of the dystrophic phenotype in dystrophin/utrophin-deficient muscle following adenovirus-mediated transfer of an utrophin minigene. Gene Ther. 7:201–204.
67. Webster, C., L. Silberstein, A. P. Hays, and H. M. Blau. 1988. Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell 52:503–513.
68. Wilton, S. D., D. E. Dye, L. M. Blechynden, and N. G. Laing. 1997. Revertant fibres: a possible genetic therapy for Duchenne muscular dystrophy? Neuromuscul. Disord. 7:329–335.
69. Yokota, T., Q. L. Lu, J. E. Morgan, K. E. Davies, R. Fisher, S. Takeda, et al. 2006. Expansion of revertant fibers in dystrophic mdx muscles reflects activity of muscle precursor cells and serves as an index of muscle regeneration. J. Cell Sci. 119:2679–2687.
70. Zhou, L., J. A. Rafael-Fortney, P. Huang, X. S. Zhao, G. Cheng, X. Zhou, et al. 2008. Haploinsufficiency of utrophin gene worsens skeletal muscle inflammation and fibrosis in mdx mice. J. Neurol. Sci. 264:106–111.