Satellite cells from dystrophic muscle retain regenerative capacity

Stem Cell Research

Volumn 14, Issue 1, 2015, Pages 20-29

  Boldrin, Luisa ^a   Zammit, Peter S ^b   Morgan, Jennifer E ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; DYSTROPHIN; MYOGENIC FACTOR 5; MYOSIN HEAVY CHAIN; NOTEXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL FUNCTION; CELL TRANSPLANTATION; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE REGENERATION; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; REPORTER GENE; SATELLITE CELL; AGING; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DISEASE MODEL; METABOLISM; MUSCLE; MUSCULAR DYSTROPHY, DUCHENNE; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; REGENERATION; SKELETAL MUSCLE SATELLITE CELL; TRANSPLANTATION; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE; ADULT; AGED; CELL ISOLATION; CELL STRESS; HOST CELL; IN VIVO STUDY; REGENERATIVE ABILITY; REGENERATIVE MEDICINE; WILD TYPE; YOUNG ADULT;

AGING; ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MICE, NUDE; MUSCLES; MUSCULAR DYSTROPHY, DUCHENNE; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE;

MUS;

EID: 84911165238     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2014.10.007     Document Type: Article

References (47)

1. Abou-Khalil R., Mounier R., Chazaud B. Regulation of myogenic stem cell behavior by vessel cells: the "menage a trois" of satellite cells, periendothelial cells and endothelial cells. Cell Cycle 2010, 9:892-896.
2. Bankole L.C., Feasson L., Ponsot E., Kadi F. Fibre type-specific satellite cell content in two models of muscle disease. Histopathology 2013, 63:826-832.
3. Beauchamp J.R., Heslop L., Yu D.S., Tajbakhsh S., Kelly R.G., Wernig A., Buckingham M.E., Partridge T.A., Zammit P.S. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J. Cell Biol. 2000, 151:1221-1234.
4. Blaivas M., Carlson B.M. Muscle fiber branching-difference between grafts in old and young rats. Mech. Ageing Dev. 1991, 60:43-53.
5. Boldrin L., Zammit P.S., Muntoni F., Morgan J.E. Mature adult dystrophic mouse muscle environment does not impede efficient engrafted satellite cell regeneration and self-renewal. Stem Cells 2009, 27:2478-2487.
6. Boldrin L., Neal A., Zammit P.S., Muntoni F., Morgan J.E. Donor satellite cell engraftment is significantly augmented when the host niche is preserved and endogenous satellite cells are incapacitated. Stem Cells 2012, 30:1971-1984.
7. Boldrin L., Morgan J.E. Modulation of the host skeletal muscle niche for donor satellite cell grafting. Methods Mol. Biol. 2013, 1035:179-190.
8. Brimah K., Ehrhardt J., Mouly V., Butler-Browne G.S., Partridge T.A., Morgan J.E. Human muscle precursor cell regeneration in the mouse host is enhanced by growth factors. Hum. Gene Ther. 2004, 15:1109-1124.
9. Chamberlain J.S., Metzger J., Reyes M., Townsend D., Faulkner J.A. Dystrophin-deficient mdx mice display a reduced life span and are susceptible to spontaneous rhabdomyosarcoma. FASEB J. 2007, 21:2195-2204.
10. Collins C.A., Zammit P.S. Isolation and grafting of single muscle fibres. Methods Mol. Biol. 2009, 482:319-330.
11. Collins C.A., Olsen I., Zammit P.S., Heslop L., Petrie A., Partridge T.A., Morgan J.E. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 2005, 122:289-301.
12. Dellavalle A., Maroli G., Covarello D., Azzoni E., Innocenzi A., Perani L., Antonini S., Sambasivan R., Brunelli S., Tajbakhsh S., Cossu G. Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat. Commun. 2011, 2:499.
13. Emery A.E. The muscular dystrophies. Lancet 2002, 359:687-695.
14. Gnocchi V.F., Scharner J., Huang Z., Brady K., Lee J.S., White R.B., Morgan J.E., Sun Y.B., Ellis J.A., Zammit P.S. Uncoordinated transcription and compromised muscle function in the lmna-null mouse model of Emery-Emery-Dreyfuss muscular dystrophy. PLoS ONE 2011, 6:e16651.
15. Gross J.G., Morgan J.E. Muscle precursor cells injected into irradiated mdx mouse muscle persist after serial injury. Muscle Nerve 1999, 22:174-185.
16. Harris J.B. Myotoxic phospholipases A2 and the regeneration of skeletal muscles. Toxicon 2003, 42:933-945.
17. Heslop L., Morgan J.E., Partridge T.A. Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J. Cell Sci. 2000, 113(Pt 12):2299-2308.
18. Hoffman E.P., Knudson C.M., Campbell K.P., Kunkel L.M. Subcellular fractionation of dystrophin to the triads of skeletal muscle. Nature 1987, 330:754-758.
19. Hoffman E.P., Morgan J.E., Watkins S.C., Partridge T.A. Somatic reversion/suppression of the mouse mdx phenotype in vivo. J. Neurol. Sci. 1990, 99:9-25.
20. Jiang C., Wen Y., Kuroda K., Hannon K., Rudnicki M.A., Kuang S. Notch signaling deficiency underlies age-dependent depletion of satellite cells in muscular dystrophy. Dis. Model. Mech. 2014, 7:997-1004.
21. Kelly R., Alonso S., Tajbakhsh S., Cossu G., Buckingham M. Myosin light chain 3F regulatory sequences confer regionalized cardiac and skeletal muscle expression in transgenic mice. J. Cell Biol. 1995, 129:383-396.
22. Kottlors M., Kirschner J. Elevated satellite cell number in Duchenne muscular dystrophy. Cell Tissue Res. 2010, 340:541-548.
23. Lu Q.L., Morris G.E., Wilton S.D., Ly T., Artem'yeva O.V., Strong P., Partridge T.A. Massive idiosyncratic exon skipping corrects the nonsense mutation in dystrophic mouse muscle and produces functional revertant fibers by clonal expansion. J. Cell Biol. 2000, 148:985-996.
24. Lu Q.L., Rabinowitz A., Chen Y.C., Yokota T., Yin H., Alter J., Jadoon A., Bou-Gharios G., Partridge T. Systemic delivery of antisense oligoribonucleotide restores dystrophin expression in body-wide skeletal muscles. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:198-203.
25. Mann C.J., Perdiguero E., Kharraz Y., Aguilar S., Pessina P., Serrano A.L., Munoz-Canoves P. Aberrant repair and fibrosis development in skeletal muscle. Skelet. Muscle 2011, 1:21.
26. Mauro A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 1961, 9:493-495.
27. Meng J., Adkin C.F., Xu S.W., Muntoni F., Morgan J.E. Contribution of human muscle-derived cells to skeletal muscle regeneration in dystrophic host mice. PLoS ONE 2011, 6:e17454.
28. Morgan J.E., Zammit P.S. Direct effects of the pathogenic mutation on satellite cell function in muscular dystrophy. Exp. Cell Res. 2010, 316:3100-3108.
29. Morgan J.E., Gross J.G., Pagel C.N., Beauchamp J.R., Fassati A., Thrasher A.J., Di Santo J.P., Fisher I.B., Shiwen X., Abraham D.J., Partridge T.A. Myogenic cell proliferation and generation of a reversible tumorigenic phenotype are triggered by preirradiation of the recipient site. J. Cell Biol. 2002, 157:693-702.
30. Moyle L.A., Zammit P.S. Isolation, culture and immunostaining of skeletal muscle fibres to study myogenic progression in satellite cells, Methods Mol. Biol. 2014, 1210:63-78.
31. Muntoni F., Mateddu A., Marchei F., Clerk A., Serra G. Muscular weakness in the mdx mouse. J. Neurol. Sci. 1993, 120:71-77.
32. Muntoni F., Brockington M., Torelli S., Brown S.C. Defective glycosylation in congenital muscular dystrophies. Curr. Opin. Neurol. 2004, 17:205-209.
33. Neal A., Boldrin L., Morgan J.E. The satellite cell in male and female, developing and adult mouse muscle: distinct stem cells for growth and regeneration. PLoS ONE 2012, 7:e37950.
34. Pastoret C., Sebille A. Further aspects of muscular dystrophy in mdx mice. Neuromuscul. Disord. 1993, 3:471-475.
35. Pastoret C., Sebille A. mdx mice show progressive weakness and muscle deterioration with age. J. Neurol. Sci. 1995, 129:97-105.
36. Pichavant C., Pavlath G.K. Incidence and severity of myofiber branching with regeneration and aging. Skelet. Muscle 2014, 4:9.
37. Relaix F., Zammit P.S. Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 2012, 139:2845-2856.
38. Ross J., Benn A., Jonuschies J., Boldrin L., Muntoni F., Hewitt J.E., Brown S.C., Morgan J.E. Defects in glycosylation impair satellite stem cell function and niche composition in the muscles of the dystrophic large (myd) mouse. Stem Cells 2012, 30:2330-2341.
39. Smythe G.M., Shavlakadze T., Roberts P., Davies M.J., McGeachie J.K., Grounds M.D. Age influences the early events of skeletal muscle regeneration: studies of whole muscle grafts transplanted between young (8weeks) and old (13-21months) mice. Exp. Gerontol. 2008, 43:550-562.
40. Stedman H.H., Sweeney H.L., Shrager J.B., Maguire H.C., Panettieri R.A., Petrof B., Narusawa M., Leferovich J.M., Sladky J.T., Kelly A.M. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 1991, 352:536-539.
41. Tajbakhsh S., Rocancourt D. Buckingham M., Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in myf-5 null mice. Nature 1996, 384:266-270.
42. Wang L., Zhou L., Jiang P., Lu L., Chen X., Lan H., Guttridge D.C., Sun H., Wang H. Loss of miR-29 in myoblasts contributes to dystrophic muscle pathogenesis. Mol. Ther. 2012, 20:1222-1233.
43. Webster C., Blau H.M. 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.
44. Wineinger M.A., Abresch R.T., Walsh S.A., Carter G.T. Effects of aging and voluntary exercise on the function of dystrophic muscle from mdx mice. Am. J. Phys. Med. Rehabil. 1998, 77:20-27.
45. Yablonka-Reuveni Z., Anderson J.E. Satellite cells from dystrophic (mdx) mice display accelerated differentiation in primary cultures and in isolated myofibers. Dev. Dyn. 2006, 235:203-212.
46. Yokota T., Lu Q.L., Morgan J.E., Davies K.E., Fisher R., Takeda S., Partridge T.A. 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.
47. Zammit P.S., Golding J.P., Nagata Y., Hudon V., Partridge T.A., Beauchamp J.R. Muscle satellite cells adopt divergent fates: a mechanism for self-renewal?. J. Cell Biol. 2004, 166:347-357.