Muscular dystrophy begins early in embryonic development deriving from stem cell loss and disrupted skeletal muscle formation

DMM Disease Models and Mechanisms

Volumn 2, Issue 7-8, 2009, Pages 374-388

  Merrick, Deborah ^a,b   Stadler, Lukas Kurt Josef ^a   Larner, Dean ^a   Smith, Janet ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 3; DYSTROPHIN; MYOSIN HEAVY CHAIN; TRANSCRIPTION FACTOR PAX7;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; EMBRYO DEVELOPMENT; GENE DISRUPTION; GENE MUTATION; INTERCOSTAL MUSCLE; LIMB GIRDLE MUSCULAR DYSTROPHY; MOUSE; MUSCLE DEVELOPMENT; MUSCULAR DYSTROPHY; MYOBLAST; MYOTUBE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SKELETAL MUSCLE; STEM CELL; ANIMAL; C57BL MOUSE; CYTOLOGY; DISEASE MODEL; EMBRYONIC STEM CELL; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; HEART; PATHOPHYSIOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; CAVEOLIN 3; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DYSTROPHIN; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC PREDISPOSITION TO DISEASE; HEART; MICE; MICE, INBRED C57BL; MUSCLE FIBERS, SKELETAL; MUSCULAR DYSTROPHIES; PHENOTYPE; STEM CELLS;

EID: 70349758560     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.001008     Document Type: Article

References (71)

1. Agbulut, O., Noirez, P., Beaumont, F. and Butler-Browne, G. (2003). Myosin heavy chain isoforms in postnatal muscle development of mice. Biol. Cell 95, 399-406. (Pubitemid 37220806)
2. Anderson, C., Winder, S. J. and Borycki, A. G. (2007). Dystroglycan protein distribution coincides with basement membranes and muscle differentiation during mouse embryogenesis. Dev. Dyn. 236, 2627-2635. (Pubitemid 47450951)
3. Aravamudan, B., Volonte, D., Ramani, R., Gursoy, E., Lisanti, M. P., London, B. and Galbiati, F. (2003). Transgenic overexpression of caveolin-3 in the heart induces a cardiomyopathic phenotype. Hum. Mol. Genet. 12, 2777-2788. (Pubitemid 37407114)
4. Armand, O., Boutineau, A. M., Mauger, A., Pautou, M. P. and Kieny, M. (1983). Origin of satellite cells in avian skeletal muscles. Arch. Anat. Microsc. Morphol. Exp. 72, 163-181. (Pubitemid 14239540)
5. Baghdiguian, S., Martin, M., Richard, I., Pons, F., Astier, C., Bourg, N., Hay, R. T., Chemaly, R., Halaby, G., Loiselet, J. et al. (1999). Calpain 3 deficiency is associated with myonuclear apoptosis and profound perturbation of the IkappaB alpha/NF-kappaB pathway in limb-girdle muscular dystrophy type 2A. Nat. Med. 5, 503-511. (Pubitemid 29220208)
6. Bassett, D. I., Bryson-Richardson, R. J., Daggett, D. F., Gautier, P., Keenan, D. G. and Currie, P. D. (2003). Dystrophin is required for the formation of stable muscle attachments in the zebrafish embryo. Development 130, 5851-5860. (Pubitemid 37540857)
7. Biederer, C. H., Ries, S. J., Moser, M., Florio, M., Israel, M. A., McCormick, F. and Buettner, R. (2000). The basic helix-loop-helix transcription factors myogenin and Id2 mediate specific induction of caveolin-3 gene expression during embryonic development. J. Biol. Chem. 275, 26245-26251. (Pubitemid 30676673)
8. Chamberlain, J. S., Metzger, J., Reyes, M., Townsend, D. and Faulkner, J. A. (2007). Dystrophin-deficient mdx mice display a reduced life span and are susceptible to spontaneous rhabdomyosarcoma. FASEB J. 21, 2195-2204. (Pubitemid 47026454)
9. Chan, S., Head, S. and Morley, J. (2007). Branched fibers in dystrophic mdx muscle are associated with a loss of force following lengthening contractions. Am. J. Physiol. Cell Physiol. 293, C985-C992.
10. Cho, M., Hughes, S. M., Karsch-Mizrachi, I., Travis, M., Leinwand, L. A. and Blau, H. M. (1994). Fast myosin heavy chains expressed in secondary mammalian muscle fibers at the time of their inception. J. Cell Sci. 107, 2361-2371. (Pubitemid 24292485)
11. Cossu, G., Tajbakhsh, S. and Buckingham, M. (1996). How is myogenesis initiated in the embryo? Trends Genet. 12, 218-223. (Pubitemid 26163010)
12. Cox, G. F. and Kunkel, L. M. (1997). Dystrophies and heart disease. Curr. Opin. Cardiol. 12, 329-343.
13. Cuda, G., Fananapazir, L., Zhu, W. S., Sellers, J. R. and Epstein, N. D. (1993). Skeletal muscle expression and abnormal function of beta-myosin in hypertrophic cardiomyopathy. J. Clin. Invest. 91, 2861-2865. (Pubitemid 23182546)
14. Cusella-De Angelis, M. G., Lyons, G., Sonnino, C., De Angelis, L., Vivarelli, E., Farmer, K., Wright, W. E., Molinaro, M., Bouche, M., Buckingham, M. et al. (1992). MyoD, myogenin independent differentiation of primordial myoblasts in mouse somites. J. Cell Biol. 116, 1243-1255.
15. Ervasti, J. and Campbell, K. (1993). A role for the dystrophin- glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122, 809-823. (Pubitemid 23241091)
16. Finsterer, J., Gelpi, E. and Stollberger, C. (2005). Left ventricular hypertrabeculation/noncompaction as a cardiac manifestation of Duchenne muscular dystrophy under non-invasive positive-pressure ventilation. Acta Cardiol. 60, 445-448. (Pubitemid 41133960)
17. Frock, R. L., Kudlow, B. A., Evans, A. M., Jameson, S. A., Hauschka, S. D. and Kennedy, B. K. (2006). Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes Dev. 20, 486-500.
18. Galbiati, F., Volonte, D., Chu, J. B., Li, M., Fine, S. W., Fu, M., Bermudez, J., Pedemonte, M., Weidenheim, K. M., Pestell, R. G. et al. (2000). Transgenic overexpression of caveolin-3 in skeletal muscle fibers induces a Duchenne-like muscular dystrophy phenotype. Proc. Natl. Acad. Sci. USA 97, 9689-9694.
19. Galbiati, F., Engleman, J., Volonte, D., Zhang, X., Minetti, C., Li, M., Hou, H., Kneitz, B., Edelmann, W. and Lisanti, M. (2001). Caveolin-3 null mice show a loss of caveolae, changes in the microdomain distribution of the dystrophin-glycoprotein complex, and T-tubule abnormalities. J. Biol. Chem. 276, 21425-21433. (Pubitemid 33648999)
20. Geisterfer-Lowrance, A. A., Kass, S., Tanigawa, G., Vosberg, H. P., McKenna, W., Seidman, C. E. and Seidman, J. G. (1990). A molecular basis for familial hypertrophic cardiomyopathy: a beta cardiac myosin heavy chain gene missense mutation. Cell 62, 999-1006. (Pubitemid 20269146)
21. Glass, D. (2005). A signalling role for dystrophin: inhibiting skeletal muscle atrophy pathways. Cancer Cell 5, 351-352.
22. Gros, J., Scaal, M. and Marcelle, C. (2004). A two-step mechanism for myotome formation in chick. Dev. Cell 6, 875-882. (Pubitemid 38745421)
23. Gross, M. K., Moran-Rivard, L., Velasquez, T., Nakatsu, M. N., Jagla, K. and Goulding, M. (2000). Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development 127, 413-424. (Pubitemid 30087976)
24. Hadchouel, J., Carvajal, J. J., Daubas, P., Bajard, L., Chang, T., Rocancourt, D., Cox, D., Summerbell, D., Tajbakhsh, S., Rigby, P. W. et al. (2003). Analysis of a key regulatory region upstream of the Myf5 gene reveals multiple phases of myogenesis, orchestrated at each site by a combination of elements dispersed throughout the locus. Development 130, 3415-3426. (Pubitemid 37010005)
25. Hagiwara, Y., Sasaoka, T., Araishi, K., Imamura, M., Yorifuji, H., Nonaka, I., Ozawa, E. and Kikuchi, T. (2000). Caveolin-3 deficiency causes muscle degeneration in mice. Hum. Mol. Genet. 9, 3047-3054. (Pubitemid 32000778)
26. Harper, S. Q., Hauser, M. A., DelloRusso, C., Duan, D., Crawford, R. W., Phelps, S. F., Harper, H. A., Robinson, A. S., Engelhardt, J. F., Brooks, S. V. et al. (2002). Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy. Nat. Med. 8, 253-261. (Pubitemid 34250103)
27. Hayashi, T., Arimura, T., Ueda, K., Shibata, H., Hohda, S., Takahashi, M., Hori, H., Koga, Y., Oka, N., Imaizumi, T. et al. (2004). Identification and functional analysis of a caveolin-3 mutation associated with familial hypertrophic cardiomyopathy. Biochem. Biophys. Res. Commun. 313, 178-184. (Pubitemid 37524041)
28. Hoffman, E., Brown, R. and Kunkel, L. (1987). Dystrophin: the protein product of the Duchenne Muscular Dystrophy locus. Cell 51, 919-928. (Pubitemid 18099471)
29. Hollway, G. E. and Currie, P. D. (2003). Myotome meanderings: cellular morphogenesis and the making of muscle. EMBO Rep. 4, 855-860.
30. Houzelstein, D., Lyons, G. E., Chamberlain, J. and Buckingham, M. E. (1992). Localization of dystrophin gene transcripts during mouse embryogenesis. J. Cell Biol. 119, 811-821.
31. Huang, X., Poy, F., Zhang, R., Joachimiak, A., Sudol, M. and Eck, M. (2000). Structure of a WW domain-containing fragment of dystrophin complexed with beta - dystroglycan. Nat. Struct. Biol. 7, 634-638. (Pubitemid 30636672)
32. Ilsley, J. L., Sudol, M. and Winder, S. J. (2002). The WW domain: linking cell signalling to the membrane cytoskeleton. Cell. Signal. 14, 183-189. (Pubitemid 34102446)
33. Jung, D., Yang, B., Meyer, J., Chamberlain, J. and Campbell, K. (1995). Identification and characterization of the dystrophin anchoring site on beta-dystroglycan. J. Biol. Chem. 270, 27305-27310.
34. Kaufman, M. (1995). The Atlas of Mouse Development. 2nd edn. London: Academic Press.
35. Lehmann, R. (2001). Cell migration in invertebrates: clues from border and distal tip cells. Curr. Opin. Genet. Dev. 11, 457-463.
36. Lindon, C., Montarras, D. and Pinset, C. (1998). Cell cycle-regulated expression of the muscle determination factor Myf5 in proliferating myoblasts. J. Cell Biol. 140, 111-118. (Pubitemid 28070899)
37. Merrick, D., Ting, T., Stadler, L. and Smith, J. (2007). A role for Insulin-like growth factor 2 in specification of the fast skeletal muscle fibre. BMC Dev. Biol. 7, 65. (Pubitemid 47033854)
38. Minetti, C., Bado, M., Broda, P., Sotgia, F., Bruno, C., Galbiati, F., Volonte, D., Lucania, G., Pavan, A., Bonilla, E. et al. (2002). Impairment of caveolae formation and T-system disorganization in human muscular dystrophy with caveolin-3 deficiency. Am. J. Pathol. 160, 265-270. (Pubitemid 34052287)
39. Nixon, S. J., Wegner, J., Ferguson, C., Mery, P. F., Hancock, J. F., Currie, P. D., Key, B., Westerfield, M. and Parton, R. G. (2005). Zebrafish as a model for caveolinassociated muscle disease; caveolin-3 is required for myofibril organization and muscle cell patterning. Hum. Mol. Genet. 14, 1727-1743. (Pubitemid 41418046)
40. Ohlendieck, K., Matsumura, K., Ionasescu, V. V., Towbin, J. A., Bosch, E. P., Weinstein, S. L., Sernett, S. W. and Campbell, K. P. (1993). Duchenne muscular dystrophy: deficiency of dystrophin-associated proteins in the sarcolemma. Neurology 43, 795-800. (Pubitemid 23121977)
41. Ott, M. O., Bober, E., Lyons, G., Arnold, H. and Buckingham, M. (1991). Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111, 1097-1107. (Pubitemid 21900264)
42. Oustanina, S., Hause, G. and Braun, T. (2004). Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J. 23, 3430-3439.
43. Parsons, M. J., Campos, I., Hirst, E. M. and Stemple, D. L. (2002). Removal of dystroglycan causes severe muscular dystrophy in zebrafish embryos. Development 129, 3505-3512. (Pubitemid 34906134)
44. Quinlan, J. G., Hahn, H. S., Wong, B. L., Lorenz, J. N., Wenisch, A. S. and Levin, L. S. (2004). Evolution of the mdx mouse cardiomyopathy: physiological and morphological findings. Neuromuscul. Disord. 14, 491-496.
45. Razani, B., Park, D. S., Miyanaga, Y., Ghatpande, A., Cohen, J., Wang, X. B., Scherer, P. E., Evans, T. and Lisanti, M. P. (2002). Molecular cloning and developmental expression of the caveolin gene family in the amphibian Xenopus laevis. Biochemistry 41, 7914-7924. (Pubitemid 34655156)
46. Reimann, J., Irintchev, A. and Wernig, A. (2000). Regenerative capacity and the number of satellite cells in soleus muscles of normal and mdx mice. Neuromuscul. Disord. 10, 276-282.
47. Relaix, F., Montarras, D., Zaffran, S., Gayraud-Morel, B., Rocancourt, D., Tajbakhsh, S., Mansouri, A., Cumano, A. and Buckingham, M. (2006). Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J. Cell Biol. 172, 91-102. (Pubitemid 43042632)
48. Roig, M., Roma, J., Fargas, A. and Munell, F. (2004). Longitudinal pathologic study of the gastrocnemius muscle group in mdx mice. Acta Neuropathol. 107, 27-34. (Pubitemid 38088272)
49. Roma, J., Munell, F., Fargas, A. and Roig, M. (2004). Evolution of pathological changes in the gastrocnemius of the mdx mice correlate with utrophin and betadystroglycan expression. Acta Neuropathol. 108, 443-452. (Pubitemid 39462356)
50. Schofield, J., Houzelstein, D., Davies, K., Buckingham, M. and Edwards, Y. H. (1993). Expression of the dystrophin-related protein (utrophin) gene during mouse embryogenesis. Dev. Dyn. 198, 254-264. (Pubitemid 24036648)
51. Schofield, J. N., Gorecki, D. C., Blake, D. J., Davies, K. and Edwards, Y. H. (1995). Dystroglycan mRNA expression during normal and mdx mouse embryogenesis: a comparison with utrophin and the apo-dystrophins. Dev. Dyn. 204, 178-185.
52. Seale, P., Sabourin, L. A., Girgis-Gabardo, A., Mansouri, A., Gruss, P. and Rudnicki, M. A. (2000). Pax7 is required for the specification of myogenic satellite cells. Cell 102, 777-786.
53. Shin, D. H., Kim, J. S., Kwon, B. S., Lee, K. S., Kim, J. W., Kim, M. H., Cho, S. S. and Lee, W. J. (2003). Caveolin-3 expression during early chicken development. Brain Res. Dev. Brain Res. 141, 83-89. (Pubitemid 36315695)
54. Smith, J. (1996). Muscle Growth factors, ubiquitin and apoptosis in dystrophic muscle: apoptosis declines with age in the mdx mouse. Basic Appl. Myol. 6, 279-284.
55. Smith, J. and Schofield, P. N. (1994). The effects of fibroblast growth factors in longterm primary culture of dystrophic (mdx) mouse muscle myoblasts. Exp. Cell Res. 210, 86-93. (Pubitemid 24168499)
56. Smith, J. and Schofield, P. N. (1997). Stable integration of an mdx skeletal muscle cell line into dystrophic (mdx) skeletal muscle: evidence for stem cell status. Cell Growth Differ. 8, 927-934. (Pubitemid 27355466)
57. Smith, J. and Merrick, D. (2008). Embryonic Skeletal Muscle Micro-Explant Culture and Isolation of Skeletal Muscle Stem Cells. Totowa, NJ: Humana Press.
58. Smith, J., Fowke, G. and Schofield, P. (1995). Programmed cell death in dystrophic (mdx) muscle is inhibited by IGF-II. Cell Death Differ. 2, 243-251.
59. Smith, J., Goldsmith, C., Ward, A. and LeDieu, R. (2000). IGF-II ameliorates the dystrophic phenotype and coordinately down-regulates programmed cell death. Cell Death Differ. 7, 1109-1118. (Pubitemid 30952845)
60. Smythe, G. M., Eby, J. C., Disatnik, M. H. and Rando, T. A. (2003). A caveolin-3 mutant that causes limb girdle muscular dystrophy type 1C disrupts Src localization and activity and induces apoptosis in skeletal myotubes. J. Cell Sci. 116, 4739-4749.
61. Sotgia, F., Lee, J., Das, K., Bedford, M., Petrucci, T., Macioce, P., Sargiacomo, M., Dagna Bricarelli, F., Minetti, C., Sudol, M. et al. (2000). Caveolin-3 directly interacts with the C-terminal tail of β-dystroglycan. J. Biol. Chem. 275, 38048-38058.
62. Spencer, M. J., Walsh, C. M., Dorshkind, K. A., Rodriguez, E. M. and Tidball, J. G. (1997). Myonuclear apoptosis in dystrophic mdx muscle occurs by perforin-mediated cytotoxicity. J. Clin. Invest. 99, 2745-2751. (Pubitemid 27259822)
63. Vaghy, P., Frang, J., Wu, W. and Vaghy, L. (1998). Increased caveolin-3 levels in mdx mouse muscles. FEBS Lett. 431, 125-127. (Pubitemid 28330866)
64. Volonte, D., Peoples, A. J. and Galbiati, F. (2003). Modulation of myoblast fusion by caveolin-3 in dystrophic skeletal muscle cells: implications for Duchenne muscular dystrophy and limb-girdle muscular dystrophy-1C. Mol. Biol. Cell 14, 4075-4088. (Pubitemid 37186310)
65. Webster, C., Silberstein, L., Hays, A. P. and Blau, H. M. (1988). Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell 52, 503-513. (Pubitemid 18067515)
66. Weir, A. P., Morgan, J. E. and Davies, K. E. (2004). A-utrophin up-regulation in mdx skeletal muscle is independent of regeneration. Neuromuscul. Disord. 14, 19-23.
67. Wilding, J., Jürgen, E., Schneider, A., Sang, E., Davies, K., Neubauer, S. and Clarke, K. (2005). Dystrophin- and MLP-deficient mouse hearts: marked differences in morphology and function, but similar accumulation of cytoskeletal proteins. FASEB J. 19, 79-81. (Pubitemid 40069924)
68. Williamson, R. A., Henry, M. D., Daniels, K. J., Hrstka, R. F., Lee, J. C., Sunada, Y., Ibraghimov-Beskrovnaya, O. and Campbell, K. P. (1997). Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum. Mol. Genet. 6, 831-841. (Pubitemid 27239066)
69. Woodman, S. E., Park, D. S., Cohen, A. W., Cheung, M. W., Chandra, M., Shirani, J., Tang, B., Jelicks, L. A., Kitsis, R. N., Christ, G. J. et al. (2002). Caveolin-3 knock-out mice develop a progressive cardiomyopathy and show hyperactivation of the p42/44 MAPK cascade. J. Biol. Chem. 277, 38988-38997.
70. Yue, Y., Li, Z., Harper, S. Q., Davisson, R. L., Chamberlain, J. S. and Duan, D. (2003). Microdystrophin gene therapy of cardiomyopathy restores dystrophin-glycoprotein complex and improves sarcolemma integrity in the mdx mouse heart. Circulation 108, 1626-1632. (Pubitemid 37187791)
71. Zammit, P. S., Partridge, T. A. and Yablonka-Reuveni, Z. (2006). The skeletal muscle satellite cell: the stem cell that came in from the cold. J. Histochem. Cytochem. 54, 1177-1191. (Pubitemid 44623339)