Myofiber branching rather than myofiber hyperplasia contributes to muscle hypertrophy in mdx mice

Skeletal Muscle

Volumn 4, Issue 1, 2014, Pages

  Faber, Rachel M ^a   Hall, John K ^a   Chamberlain, Jeffrey S ^a,b   Banks, Glen B ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

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

Author keywords

Duchenne muscular dystrophy; Fiber branching; Hypertrophy; Inflammation; Innervation; Neuromuscular synapse; Skeletal muscle

Indexed keywords

EID: 84902072635     PISSN: None     EISSN: 20445040     Source Type: Journal    
DOI: 10.1186/2044-5040-4-10     Document Type: Article

References (51)

1. Hoffman EP, Brown RH, Kunkel LM. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 1987, 51:919-928. 10.1016/0092-8674(87)90579-4, 3319190.
2. Koenig M, Hoffman EP, Bertelson CJ, Monaco AP, Feener C, Kunkel LM. Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 1987, 50:509-517. 10.1016/0092-8674(87)90504-6, 3607877.
3. Jones DA, Round JM, Edwards RH, Grindwood SR, Tofts PS. Size and composition of the calf and quadriceps muscles in Duchenne muscular dystrophy. A tomographic and histochemical study. J Neurol Sci 1983, 60:307-322. 10.1016/0022-510X(83)90071-0, 6886735.
4. Reimers CD, Schlotter B, Eicke BM, Witt TN. Calf enlargement in neuromuscular diseases: a quantitative ultrasound study in 350 patients and review of the literature. J Neurol Sci 1996, 143:46-56. 10.1016/S0022-510X(96)00037-8, 8981297.
5. Kornegay JN, Childers MK, Bogan DJ, Bogan JR, Nghiem P, Wang J, Fan Z, Howard JF, Schatzberg SJ, Dow JL, Grange RW, Styner MA, Hoffman EP, Wagner KR. The paradox of muscle hypertrophy in muscular dystrophy. Phys Med Rehabil Clin N Am 2012, 23:149-172. xii, 10.1016/j.pmr.2011.11.014, 22239881.
6. Blau HM, Webster C, Pavlath GK. Defective myoblasts identified in Duchenne muscular dystrophy. Proc Natl Acad Sci U S A 1983, 80:4856-4860. 10.1073/pnas.80.15.4856, 384144, 6576361.
7. Webster C, Blau HM. Accelerated age-related decline in replicative life-span of Duchenne muscular dystrophy myoblasts: implications for cell and gene therapy. Somat Cell Mol Genet 1990, 16:557-565. 10.1007/BF01233096, 2267630.
8. Mouly V, Aamiri A, Bigot A, Cooper RN, Di Donna S, Furling D, Gidaro T, Jacquemin V, Mamchaoui K, Negroni E, Perie S, Renault V, Silva-Barbosa SD, Butler-Browne GS. The mitotic clock in skeletal muscle regeneration, disease and cell mediated gene therapy. Acta Physiol Scand 2005, 184:3-15. 10.1111/j.1365-201X.2005.01417.x, 15847639.
9. Sacco A, Mourkioti F, Tran R, Choi J, Llewellyn M, Kraft P, Shkreli M, Delp S, Pomerantz JH, Artandi SE, Blau HM. Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 2010, 143:1059-1071. 10.1016/j.cell.2010.11.039, 3025608, 21145579.
10. Coulton GR, Curtin NA, Morgan JE, Partridge TA. The mdx mouse skeletal muscle myopathy: II, Contractile properties. Neuropathol Appl Neurobiol 1988, 14:299-314. 10.1111/j.1365-2990.1988.tb00890.x, 3221977.
11. Coulton GR, Morgan JE, Partridge TA, Sloper JC. The mdx mouse skeletal muscle myopathy: I. A histological, morphometric and biochemical investigation. Neuropathol Appl Neurobiol 1988, 14:53-70. 10.1111/j.1365-2990.1988.tb00866.x, 2967442.
12. Pagel CN, Partridge TA. Covert persistence of mdx mouse myopathy is revealed by acute and chronic effects of irradiation. J Neurol Sci 1999, 164:103-116. 10.1016/S0022-510X(99)00061-1, 10402020.
13. Lynch GS, Hinkle RT, Chamberlain JS, Brooks SV, Faulkner JA. Force and power output of fast and slow skeletal muscles from mdx mice 6-28 months old. J Physiol 2001, 535:591-600. 10.1111/j.1469-7793.2001.00591.x, 2278782, 11533147.
14. Banks GB, Judge LM, Allen JM, Chamberlain JS. The polyproline site in hinge 2 influences the functional capacity of truncated dystrophins. PLoS Genet 2010, 6:e1000958. 10.1371/journal.pgen.1000958, 2873924, 20502633.
15. Bockhold KJ, Rosenblatt JD, Partridge TA. Aging normal and dystrophic mouse muscle: analysis of myogenicity in cultures of living single fibers. Muscle Nerve 1998, 21:173-183. 10.1002/(SICI)1097-4598(199802)21:2<173::AID-MUS4>3.0.CO;2-8, 9466592.
16. Crawford GE, Lu QL, Partridge TA, Chamberlain JS. Suppression of revertant fibers in mdx mice by expression of a functional dystrophin. Hum Mol Genet 2001, 10:2745-2750. 10.1093/hmg/10.24.2745, 11734539.
17. Yokota T, Lu QL, Morgan JE, Davies KE, Fisher R, Takeda S, Partridge TA. 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 2006, 119:2679-2687. 10.1242/jcs.03000, 16757519.
18. Sacco A, Doyonnas R, Kraft P, Vitorovic S, Blau HM. Self-renewal and expansion of single transplanted muscle stem cells. Nature 2008, 456:502-506. 10.1038/nature07384, 2919355, 18806774.
19. Verze L, Buffo A, Rossi F, Oestreicher AB, Gispen WH, Strata P. Increase of B-50/GAP-43 immunoreactivity in uninjured muscle nerves of MDX mice. Neuroscience 1996, 70:807-815. 10.1016/S0306-4522(96)83017-X, 9045090.
20. Snow MH. Satellite cell distribution within the soleus muscle of the adult mouse. Anat Rec 1981, 201:463-469. 10.1002/ar.1092010303, 7305027.
21. Distefano G, Ferrari RJ, Weiss C, Deasy BM, Boninger ML, Fitzgerald GK, Huard J, Ambrosio F. Neuromuscular electrical stimulation as a method to maximize the beneficial effects of muscle stem cells transplanted into dystrophic skeletal muscle. PLoS One 2013, 8:e54922. 10.1371/journal.pone.0054922, 3602431, 23526927.
22. Hijikata T, Ishikawa H. Functional morphology of serially linked skeletal muscle fibers. Acta Anat (Basel) 1997, 159:99-107. 10.1159/000147972, 9575360.
23. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000, 28:41-51. 10.1016/S0896-6273(00)00084-2, 11086982.
24. Banks GB, Combs AC, Chamberlain JS. Sequencing protocols to genotype mdx, mdx(4cv), and mdx(5cv) mice. Muscle Nerve 2010, 42:268-270. 10.1002/mus.21700, 3155817, 20544945.
25. Banks GB, Kanjhan R, Wiese S, Kneussel M, Wong LM, O'Sullivan G, Sendtner M, Bellingham MC, Betz H, Noakes PG. Glycinergic and GABAergic synaptic activity differentially regulate motoneuron survival and skeletal muscle innervation. J Neurosci 2005, 25:1249-1259. 10.1523/JNEUROSCI.1786-04.2005, 15689563.
26. Balice-Gordon RJ, Thompson WJ. The organization and development of compartmentalized innervation in rat extensor digitorum longus muscle. J Physiol 1988, 398:211-231. 1191769, 3392671.
27. Leite PE, Lagrota-Candido J, Moraes L, D'Elia L, Pinheiro DF, da Silva RF, Yamasaki EN, Quirico-Santos T. Nicotinic acetylcholine receptor activation reduces skeletal muscle inflammation of mdx mice. J Neuroimmunol 2010, 227:44-51. 10.1016/j.jneuroim.2010.06.005, 20615555.
28. Marques MJ, Conchello JA, Lichtman JW. From plaque to pretzel: fold formation and acetylcholine receptor loss at the developing neuromuscular junction. J Neurosci 2000, 20:3663-3675.
29. Deschenes MR, Hurst TE, Ramser AE, Sherman EG. Presynaptic to postsynaptic relationships of the neuromuscular junction are held constant across age and muscle fiber type. Dev Neurobiol 2013, 73:744-753. 10.1002/dneu.22095, 23696094.
30. Lyons PR, Slater CR. Structure and function of the neuromuscular junction in young adult mdx mice. J Neurocytol 1991, 20:969-981. 10.1007/BF01187915, 1686056.
31. Banks GB, Chamberlain JS, Froehner SC. Truncated dystrophins can influence neuromuscular synapse structure. Mol Cell Neurosci 2009, 40:433-441. 10.1016/j.mcn.2008.12.011, 2826111, 19171194.
32. White RB, Bierinx AS, Gnocchi VF, Zammit PS. Dynamics of muscle fibre growth during postnatal mouse development. BMC Dev Biol 2010, 10:21. 10.1186/1471-213X-10-21, 2836990, 20175910.
33. Lovering RM, Michaelson L, Ward CW. Malformed mdx myofibers have normal cytoskeletal architecture yet altered EC coupling and stress-induced Ca2+ signaling. Am J Physiol Cell Physiol 2009, 297:C571-C580. 10.1152/ajpcell.00087.2009, 2740390, 19605736.
34. Anderson JE. A role for nitric oxide in muscle repair: nitric oxide-mediated activation of muscle satellite cells. Mol Biol Cell 2000, 11:1859-1874. 10.1091/mbc.11.5.1859, 14889, 10793157.
35. McCarthy JJ, Mula J, Miyazaki M, Erfani R, Garrison K, Farooqui AB, Srikuea R, Lawson BA, Grimes B, Keller C, Van Zant G, Campbell KS, Esser KA, Dupont-Versteedgen EE, Peterson CA. Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development 2011, 138:3657-3666. 10.1242/dev.068858, 3152923, 21828094.
36. Pastoret C, Sebille A. Age-related differences in regeneration of dystrophic (mdx) and normal muscle in the mouse. Muscle Nerve 1995, 18:1147-1154. 10.1002/mus.880181011, 7659109.
37. Pastoret C, Sebille A. mdx mice show progressive weakness and muscle deterioration with age. J Neurol Sci 1995, 129:97-105. 10.1016/0022-510X(94)00276-T, 7608742.
38. Partridge TA. The mdx mouse model as a surrogate for Duchenne muscular dystrophy. FEBS J 2013, 280:4177-4186. 10.1111/febs.12267, 23551987.
39. Bishop DL, Misgeld T, Walsh MK, Gan WB, Lichtman JW. Axon branch removal at developing synapses by axosome shedding. Neuron 2004, 44:651-661. 10.1016/j.neuron.2004.10.026, 15541313.
40. Vetrone SA, Montecino-Rodriguez E, Kudryashova E, Kramerova I, Hoffman EP, Liu SD, Miceli MC, Spencer MJ. Osteopontin promotes fibrosis in dystrophic mouse muscle by modulating immune cell subsets and intramuscular TGF-beta. J Clin Invest 2009, 119:1583-1594. 10.1172/JCI37662, 2689112, 19451692.
41. Tamaki T, Sekine T, Akatsuka A, Uchiyama S, Nakano S. Three-dimensional cytoarchitecture of complex branched fibers in soleus muscle from mdx mutant mice. Anat Rec 1993, 237:338-344. 10.1002/ar.1092370307, 8291687.
42. Knuesel I, Mastrocola M, Zuellig RA, Bornhauser B, Schaub MC, Fritschy JM. Short communication: altered synaptic clustering of GABAA receptors in mice lacking dystrophin (mdx mice). Eur J Neurosci 1999, 11:4457-4462. 10.1046/j.1460-9568.1999.00887.x, 10594673.
43. Banks GB, Chamberlain JS. The value of mammalian models for duchenne muscular dystrophy in developing therapeutic strategies. Curr Top Dev Biol 2008, 84:431-453.
44. Cox GA, Cole NM, Matsumura K, Phelps SF, Hauschka SD, Campbell KP, Faulkner JA, Chamberlain JS. Overexpression of dystrophin in transgenic mdx mice eliminates dystrophic symptoms without toxicity. Nature 1993, 364:725-729. 10.1038/364725a0, 8355788.
45. Chan S, Head SI, Morley JW. Branched fibers in dystrophic mdx muscle are associated with a loss of force following lengthening contractions. Am J Physiol Cell Physiol 2007, 293:C985-C992. 10.1152/ajpcell.00128.2007, 17567750.
46. Chan S, Head SI. The role of branched fibres in the pathogenesis of Duchenne muscular dystrophy. Exp Physiol 2011, 96:564-571.
47. Head SI. Branched fibres in old dystrophic mdx muscle are associated with mechanical weakening of the sarcolemma, abnormal Ca2+ transients and a breakdown of Ca2+ homeostasis during fatigue. Exp Physiol 2010, 95:641-656. 10.1113/expphysiol.2009.052019, 20139167.
48. Kimura E, Han JJ, Li S, Fall B, Ra J, Haraguchi M, Tapscott SJ, Chamberlain JS. Cell-lineage regulated myogenesis for dystrophin replacement: a novel therapeutic approach for treatment of muscular dystrophy. Hum Mol Genet 2008, 17:2507-2517. 10.1093/hmg/ddn151, 2574879,2574879, 18511457.
49. Cerletti M, Jurga S, Witczak CA, Hirshman MF, Shadrach JL, Goodyear LJ, Wagers AJ. Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 2008, 134:37-47. 10.1016/j.cell.2008.05.049, 3665268, 18614009.
50. Filareto A, Parker S, Darabi R, Borges L, Iacovino M, Schaaf T, Mayerhofer T, Chamberlain JS, Ervasti JM, McIvor RS, Kyba M, Perlingeiro RC. An ex vivo gene therapy approach to treat muscular dystrophy using inducible pluripotent stem cells. Nat Commun 2013, 4:1549. 3595133, 23462992.
51. Hall JK, Banks GB, Chamberlain JS, Olwin BB. Prevention of muscle aging by myofiber-associated satellite cell transplantation. Sci Transl Med 2010, 2:57ra-83ra.