Extraocular muscle satellite cells are high performance myo-engines retaining efficient regenerative capacity in dystrophin deficiency

Developmental Biology

Volumn 397, Issue 1, 2015, Pages 31-44

  Stuelsatz, Pascal ^a   Shearer, Andrew ^a   Li, Yunfei ^a   Muir, Lindsey A ^a   Ieronimakis, Nicholas ^a   Shen, Qingwu W ^a   Kirillova, Irina ^a   Yablonka Reuveni, Zipora ^a  

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

Author keywords

Clonal growth; Cre loxP; Duchenne muscular dystrophy; Engraftment; Extraocular muscles; FACS; Mdx4cv; Myf5; MyoD; Myosin light chain 3F nLacZ; Nestin GFP; Pax3; Pax7; Renewal; Retractor bulbi; Satellite cells

Indexed keywords

DYSTROPHIN; GREEN FLUORESCENT PROTEIN; KI 67 ANTIGEN; MYOD PROTEIN; MYOGENIC FACTOR 5; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR PAX7;

ADULT; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CELL GROWTH; CELL LINEAGE; CELL PROLIFERATION; CELL RENEWAL; DIAPHRAGM MUSCLE; EXTRAOCULAR MUSCLE; FEMALE; LIMB; MALE; MOUSE; MUSCLE REGENERATION; NONHUMAN; PROGENY; SKELETAL MUSCLE SATELLITE CELL; SOMITE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE; ANIMAL; C57BL MOUSE; CELL SEPARATION; CELL TRANSPLANTATION; CYTOLOGY; DEFICIENCY; DISEASE MODEL; DUCHENNE MUSCULAR DYSTROPHY; EMBRYOLOGY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; PHYSIOLOGY; REGENERATION; SKELETAL MUSCLE; STEM CELL; TRANSGENIC MOUSE;

ANIMALS; CELL LINEAGE; CELL PROLIFERATION; CELL SEPARATION; CELL TRANSPLANTATION; DISEASE MODELS, ANIMAL; DYSTROPHIN; EXTREMITIES; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE; STEM CELLS;

EID: 84915813637     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.08.035     Document Type: Article

References (107)

1. Andrade F.H., Porter J.D., Kaminski H.J. Eye muscle sparing by the muscular dystrophies: lessons to be learned?. Microsc. Res. Tech. 2000, 48:192-203.
2. Arpke R.W., Darabi R., Mader T.L., Zhang Y., Toyama A., Lonetree C.L., Nash N., Lowe D.A., Perlingeiro R.C., Kyba M. A new immuno-, dystrophin-deficient model, the NSG-mdx(4Cv) mouse, provides evidence for functional improvement following allogeneic satellite cell transplantation. Stem Cells 2013, 31:1611-1620.
3. Banks G.B., Combs A.C., Chamberlain J.S. Sequencing protocols to genotype mdx, mdx(4cv), and mdx(5cv) mice. Muscle Nerve 2010, 42:268-270.
4. Banks G.B., Combs A.C., Odom G.L., Bloch R.J., Chamberlain J.S. Muscle structure influences utrophin expression in mdx mice. PLoS Genet. 2014, 10:e1004431.
5. 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.
6. Beauchamp J.R., Morgan J.E., Pagel C.N., Partridge T.A. Dynamics of myoblast transplantation reveal a discrete minority of precursors with stem cell-like properties as the myogenic source. J. Cell Biol. 1999, 144:1113-1122.
7. Chang N.C., Rudnicki M.A. Satellite cells: the architects of skeletal muscle. Curr. Top. Dev. Biol. 2014, 107:161-181.
8. Chapman V.M., Miller D.R., Armstrong D., Caskey C.T. Recovery of induced mutations for X chromosome-linked muscular dystrophy in mice. Proc. Natl. Acad. Sci. U.S.A 1989, 86:1292-1296.
9. 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.
10. Couly G.F., Coltey P.M., Le Douarin N.M. The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 1992, 114:1-15.
11. da Silva Costa R.M., Kung J., Poukens V., Demer J.L. Nonclassical innervation patterns in mammalian extraocular muscles. Curr. Eye Res. 2012, 37:761-769.
12. Dai D.F., Santana L.F., Vermulst M., Tomazela D.M., Emond M.J., MacCoss M.J., Gollahon K., Martin G.M., Loeb L.A., Ladiges W.C., Rabinovitch P.S. Overexpression of catalase targeted to mitochondria attenuates murine cardiac aging. Circulation 2009, 119:2789-2797.
13. Danko I., Chapman V., Wolff J.A. The frequency of revertants in mdx mouse genetic models for Duchenne muscular dystrophy. Pediatr. Res. 1992, 32:128-131.
14. Danoviz M.E., Yablonka-Reuveni Z. Skeletal muscle satellite cells: background and methods for isolation and analysis in a primary culture system. Methods Mol. Biol. 2012, 798:21-52.
15. Day K., Paterson B., Yablonka-Reuveni Z. A distinct profile of myogenic regulatory factor detection within Pax7+ cells at S phase supports a unique role of Myf5 during posthatch chicken myogenesis. Dev. Dyn. 2009, 238:1001-1009.
16. Day K., Shefer G., Richardson J.B., Enikolopov G., Yablonka-Reuveni Z. Nestin-GFP reporter expression defines the quiescent state of skeletal muscle satellite cells. Dev. Biol. 2007, 304:246-259.
17. Day K., Shefer G., Shearer A., Yablonka-Reuveni Z. The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny. Dev. Biol. 2010, 340:330-343.
18. Decrouy A., Renaud J.M., Davis H.L., Lunde J.A., Dickson G., Jasmin B.J. Mini-dystrophin gene transfer in mdx4cv diaphragm muscle fibers increases sarcolemmal stability. Gene Ther. 1997, 4:401-408.
19. Demer J.L. Mechanics of the orbita. Dev. Ophthalmol. 2007, 40:132-157.
20. Engleka K.A., Gitler A.D., Zhang M., Zhou D.D., High F.A., Epstein J.A. Insertion of Cre into the Pax3 locus creates a new allele of Splotch and identifies unexpected Pax3 derivatives. Dev. Biol. 2005, 280:396-406.
21. Fischer E.H., Charbonneau H., Tonks N.K. Protein tyrosine phosphatases: a diverse family of intracellular and transmembrane enzymes. Science 1991, 253:401-406.
22. Goulding M., Lumsden A., Paquette A.J. Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 1994, 120:957-971.
23. Grounds M.D., Shavlakadze T. Growing muscle has different sarcolemmal properties from adult muscle: a proposal with scientific and clinical implications: reasons to reassess skeletal muscle molecular dynamics, cellular responses and suitability of experimental models of muscle disorders. Bioessays 2011, 33:458-468.
24. Grounds M.D., Yablonka-Reuveni Z. Molecular and cell biology of skeletal muscle regeneration. Mol. Cell Biol. Hum. Dis. Ser. 1993, 3:210-256.
25. Halevy O., Piestun Y., Allouh M.Z., Rosser B.W., Rinkevich Y., Reshef R., Rozenboim I., Wleklinski-Lee M., Yablonka-Reuveni Z. Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev. Dyn. 2004, 231:489-502.
26. Harel I., Nathan E., Tirosh-Finkel L., Zigdon H., Guimaraes-Camboa N., Evans S.M., Tzahor E. Distinct origins and genetic programs of head muscle satellite cells. Dev. Cell 2009, 16:822-832.
27. Hawke T.J., Garry D.J. Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol. 2001, 91:534-551.
28. He S., Yoon H.S., Suh B.J., Eccles M.R. PAX3 Is extensively expressed in benign and malignant tissues of the melanocytic lineage in humans. J. Investig. Dermatol. 2010, 130:1465-1468.
29. Head S.I., Williams D.A., Stephenson D.G. Abnormalities in structure and function of limb skeletal muscle fibres of dystrophic mdx mice. Proc. Biol. Sci. 1992, 248:163-169.
30. Hebert S.L., Daniel M.L., McLoon L.K. The role of Pitx2 in maintaining the phenotype of myogenic precursor cells in the extraocular muscles. PLoS One 2013, 8:e58405.
31. 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.
32. Horst D., Ustanina S., Sergi C., Mikuz G., Juergens H., Braun T., Vorobyov E. Comparative expression analysis of Pax3 and Pax7 during mouse myogenesis. Int. J. Dev. Biol. 2006, 50:47-54.
33. Ieronimakis N., Balasundaram G., Rainey S., Srirangam K., Yablonka-Reuveni Z., Reyes M. Absence of CD34 on murine skeletal muscle satellite cells marks a reversible state of activation during acute injury. PloS One 2010, 5:e10920.
34. Im W.B., Phelps S.F., Copen E.H., Adams E.G., Slightom J.L., Chamberlain J.S. Differential expression of dystrophin isoforms in strains of mdx mice with different mutations. Hum Mol Genet 1996, 5:1149-1153.
35. 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.
36. Judge L.M., Haraguchiln M., Chamberlain J.S. Dissecting the signaling and mechanical functions of the dystrophin-glycoprotein complex. J. Cell Sci. 2006, 119:1537-1546.
37. Kallestad K.M., Hebert S.L., McDonald A.A., Daniel M.L., Cu S.R., McLoon L.K. Sparing of extraocular muscle in aging and muscular dystrophies: a myogenic precursor cell hypothesis. Exp. Cell Res. 2011, 317:873-885.
38. Kallestad K.M., McLoon L.K. Defining the heterogeneity of skeletal muscle-derived side and main population cells isolated immediately ex vivo. J. Cell Physiol 2010, 222:676-684.
39. Kaminski H.J., al-Hakim M., Leigh R.J., Katirji M.B., Ruff R.L. Extraocular muscles are spared in advanced Duchenne dystrophy. Ann. Neurol. 1992, 32:586-588.
40. Kaminski H.J., Richmonds C.R., Kusner L.L., Mitsumoto H. Differential susceptibility of the ocular motor system to disease. Ann. N. Y. Acad. Sci. 2002, 956:42-54.
41. Kanisicak O., Mendez J.J., Yamamoto S., Yamamoto M., Goldhamer D.J. Progenitors of skeletal muscle satellite cells express the muscle determination gene, MyoD. Dev. Biol. 2009, 332:131-141.
42. Kassar-Duchossoy L., Gayraud-Morel B., Gomes D., Rocancourt D., Buckingham M., Shinin V., Tajbakhsh S. Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice. Nature 2004, 431:466-471.
43. Kastner S., Elias M.C., Rivera A.J., Yablonka-Reuveni Z. Gene expression patterns of the fibroblast growth factors and their receptors during myogenesis of rat satellite cells. J. Histochem. Cytochem. 2000, 48:1079-1096.
44. Keire P., Shearer A., Shefer G., Yablonka-Reuveni Z. Isolation and culture of skeletal muscle myofibers as a means to analyze satellite cells. Methods Mol. Biol. 2013, 946:431-468.
45. 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.
46. Khurana T.S., Prendergast R.A., Alameddine H.S., Tome F.M., Fardeau M., Arahata K., Sugita H., Kunkel L.M. Absence of extraocular muscle pathology in Duchenne[U+05F3]s muscular dystrophy: role for calcium homeostasis in extraocular muscle sparing. J. Exp. Med. 1995, 182:467-475.
47. Kirillova I., Gussoni E., Goldhamer D.J., Yablonka-Reuveni Z. Myogenic reprogramming of retina-derived cells following their spontaneous fusion with myotubes. Dev. Biol. 2007, 311:449-463.
48. Konieczny P., Swiderski K., Chamberlain J.S. Gene and cell-mediated therapies for muscular dystrophy. Muscle Nerve 2013, 47:649-663.
49. Kuang S., Kuroda K., Le Grand F., Rudnicki M.A. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 2007, 129:999-1010.
50. Lagrota-Candido J., Vasconcellos R., Cavalcanti M., Bozza M., Savino W., Quirico-Santos T. Resolution of skeletal muscle inflammation in mdx dystrophic mouse is accompanied by increased immunoglobulin and interferon-gamma production. Int. J. Exp. Pathol. 2002, 83:121-132.
51. LifeMap, LifeMap Sciences, Inc., 2013. http://discovery.lifemapsc.com/library/images/extraocular-skeletal-muscle-anatomy.
52. Lu Q.L., Morris G.E., Wilton S.D., Ly T., Artemyeva 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.
53. Marques M.J., Pertille A., Carvalho C.L., Santo Neto H. Acetylcholine receptor organization at the dystrophic extraocular muscle neuromuscular junction. Anat. Rec. 2007, 290:846-854.
54. Mauro A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 1961, 9:493-495.
55. McDonald A.A., Kunz M.D., McLoon L.K. Dystrophic changes in extraocular muscles after gamma irradiation in mdx:utrophin(+/-) mice. PLoS One 2014, 9:e86424.
56. McGeachie J.K., Grounds M.D., Partridge T.A., Morgan J.E. Age-related changes in replication of myogenic cells in mdx mice: quantitative autoradiographic studies. J. Neurol. Sci. 1993, 119:169-179.
57. McLoon L.K., Wirtschafter J. Activated satellite cells are present in uninjured extraocular muscles of mature mice. Trans. Am. Ophthalmol. Soc. 2002, 100:119-123. (discussion 123-114).
58. Mignone J.L., Kukekov V., Chiang A.S., Steindler D., Enikolopov G. Neural stem and progenitor cells in nestin-GFP transgenic mice. J. Comp. Neurol. 2004, 469:311-324.
59. Miller R.G., Sharma K.R., Pavlath G.K., Gussoni E., Mynhier M., Lanctot A.M., Greco C.M., Steinman L., Blau H.M. Myoblast implantation in Duchenne muscular dystrophy: the San Francisco study. Muscle Nerve 1997, 20:469-478.
60. Mombaerts P., Iacomini J., Johnson R.S., Herrup K., Tonegawa S., Papaioannou V.E. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 1992, 68:869-877.
61. Montarras D., LHonore A., Buckingham M. Lying low but ready for action: the quiescent muscle satellite cell. FEBS J. 2013, 280:4036-4050.
62. Morrison J., Lu Q.L., Pastoret C., Partridge T., Bou-Gharios G. T-cell-dependent fibrosis in the mdx dystrophic mouse. Lab. Investig. 2000, 80:881-891.
63. Moss F.P., Leblond C.P. Satellite cells as the source of nuclei in muscles of growing rats. Anat. Rec. 1971, 170:421-435.
64. Muzumdar M.D., Tasic B., Miyamichi K., Li L., Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007, 45:593-605.
65. Negroni E., Vallese D., Vilquin J.T., Butler-Browne G., Mouly V., Trollet C. Current advances in cell therapy strategies for muscular dystrophies. Expert Opin. Biol. Ther. 2011, 11:157-176.
66. Noden D.M., Francis-West P. The differentiation and morphogenesis of craniofacial muscles. Dev. Dyn. 2006, 235:1194-1218.
67. Ono Y., Boldrin L., Knopp P., Morgan J.E., Zammit P.S. Muscle satellite cells are a functionally heterogeneous population in both somite-derived and branchiomeric muscles. Dev. Biol. 2010, 337:29-41.
68. Pacheco-Pinedo E.C., Budak M.T., Zeiger U., Jorgensen L.H., Bogdanovich S., Schroder H.D., Rubinstein N.A., Khurana T.S. Transcriptional and functional differences in stem cell populations isolated from extraocular and limb muscles. Physiol. Genomics 2009, 37:35-42.
69. Porter J.D. Commentary: extraocular muscle sparing in muscular dystrophy: a critical evaluation of potential protective mechanisms. Neuromuscul. Disord. 1998, 8:198-203.
70. Porter J.D., Israel S., Gong B., Merriam A.P., Feuerman J., Khanna S., Kaminski H.J. Distinctive morphological and gene/protein expression signatures during myogenesis in novel cell lines from extraocular and hindlimb muscle. Physiol. Genomics 2006, 24:264-275.
71. Porter J.D., Karathanasis P. Extraocular muscle in merosin-deficient muscular dystrophy: cation homeostasis is maintained but is not mechanistic in muscle sparing. Cell Tissue Res. 1998, 292:495-501.
72. Porter J.D., Merriam A.P., Hack A.A., Andrade F.H., McNally E.M. Extraocular muscle is spared despite the absence of an intact sarcoglycan complex in gamma- or delta-sarcoglycan-deficient mice. Neuromuscul. Disord. 2001, 11:197-207.
73. Sacco A., Doyonnas R., Kraft P., Vitorovic S., Blau H.M. Self-renewal and expansion of single transplanted muscle stem cells. Nature 2008, 456:502-506.
74. Sambasivan R., Gayraud-Morel B., Dumas G., Cimper C., Paisant S., Kelly R.G., Tajbakhsh S. Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Dev. Cell 2009, 16:810-821.
75. Schoser B.G., Pongratz D. Extraocular mitochondrial myopathies and their differential diagnoses. Strabismus 2006, 14:107-113.
76. Schultz E., Gibson M.C., Champion T. Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J. Exp. Zool. 1978, 206:451-456.
77. Seale P., Sabourin L.A., Girgis-Gabardo A., Mansouri A., Gruss P., Rudnicki M.A. Pax7 is required for the specification of myogenic satellite cells. Cell 2000, 102:777-786.
78. Shefer G., Rauner G., Stuelsatz P., Benayahu D., Yablonka-Reuveni Z. Moderate-intensity treadmill running promotes expansion of the satellite cell pool in young and old mice. FEBS J. 2013, 280:4063-4073.
79. Shefer G., Van de Mark D.P., Richardson J.B., Yablonka-Reuveni Z. Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev. Biol. 2006, 294:50-66.
80. Shefer G., Wleklinski-Lee M., Yablonka-Reuveni Z. Skeletal muscle satellite cells can spontaneously enter an alternative mesenchymal pathway. J. Cell Sci. 2004, 117:5393-5404.
81. Shefer G., Yablonka-Reuveni Z. Isolation and culture of skeletal muscle myofibers as a means to analyze satellite cells. Basic Cell Culture Protocols 2005, Vol. 290:281-304. Humana Press, Totowa, NJ.
82. Smith C.K., Janney M.J., Allen R.E. Temporal expression of myogenic regulatory genes during activation, proliferation, and differentiation of rat skeletal muscle satellite cells. J. Cell Physiol. 1994, 159:379-385.
83. Spencer M.J., Montecino-Rodriguez E., Dorshkind K., Tidball J.G. Helper (CD4(+)) and cytotoxic (CD8(+)) T cells promote the pathology of dystrophin-deficient muscle. Clin. Immunol. 2001, 98:235-243.
84. Spencer R.F., Porter J.D. Biological organization of the extraocular muscles. Prog. Brain Res. 2006, 151:43-80.
85. Stuelsatz P., Keire P., Almuly R., Yablonka-Reuveni Z. A contemporary atlas of the mouse diaphragm: myogenicity, vascularity, and the Pax3 connection. J. Histochem. Cytochem. 2012, 60:638-657.
86. Stuelsatz P., Shearer A., Yablonka-Reuveni Z. Ancestral Myf5 gene activity in periocular connective tissue identifies a subset of fibro/adipogenic progenitors but does not connote a myogenic origin. Dev. Biol 2014, 385:366-379.
87. 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.
88. Tajbakhsh S., Rocancourt D., Cossu G., Buckingham M. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 1997, 89:127-138.
89. Tedesco F.S., Cossu G. Stem cell therapies for muscle disorders. Curr. Opin. Neurol. 2012, 25:597-603.
90. Tremblay J.P., Malouin F., Roy R., Huard J., Bouchard J.P., Satoh A., Richards C.L. Results of a triple blind clinical study of myoblast transplantations without immunosuppressive treatment in young boys with Duchenne muscular dystrophy. Cell Transplant. 1993, 2:99-112.
91. Valdez G., Tapia J.C., Lichtman J.W., Fox M.A., Sanes J.R. Shared resistance to aging and ALS in neuromuscular junctions of specific muscles. PloS One 2012, 7:e34640.
92. Villalta S.A., Nguyen H.X., Deng B., Gotoh T., Tidball J.G. Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum. Mol. Genet. 2009, 18:482-496.
93. 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.
94. White R.B., Bierinx A.S., Gnocchi V.F., Zammit P.S. Dynamics of muscle fibre growth during postnatal mouse development. BMC Dev. Biol. 2010, 10:21.
95. Williams D.A., Head S.I., Lynch G.S., Stephenson D.G. Contractile properties of skinned muscle fibres from young and adult normal and dystrophic (mdx) mice. J. Physiol. 1993, 460:51-67.
96. Wilschut K.J., Ling V.B., Bernstein H.S. Concise review: stem cell therapy for muscular dystrophies. Stem Cells Transl. Med. 2012, 1:833-842.
97. Yablonka-Reuveni Z. Discrimination of myogenic and nonmyogenic cells from embryonic skeletal muscle by 90 degrees light scattering. Cytometry 1988, 9:121-125.
98. Yablonka-Reuveni Z. Isolation and culture of myogenic stem cells. Handbook of Stem Cells 2004, Vol. 2:571-580. Elsevier: Academic Press, San Diego.
99. Yablonka-Reuveni Z. The skeletal muscle satellite cell: still young and fascinating at 50. J. Histochem. Cytochem. 2011, 59:1041-1059.
100. 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.
101. Yang J., Ontell M.P., Kelly R., Watkins S.C., Ontell M. Limitations of nls beta-galactosidase as a marker for studying myogenic lineage or the efficacy of myoblast transfer. Anat. Rec. 1997, 248:40-50.
102. 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.
103. Yu Wai Man C.Y., Chinnery P.F., Griffiths P.G. Extraocular muscles have fundamentally distinct properties that make them selectively vulnerable to certain disorders. Neuromuscul. Disord.: NMD 2005, 15(17-23).
104. 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.
105. Zammit P.S., Partridge T.A., Yablonka-Reuveni Z. The skeletal muscle satellite cell: the stem cell that came in from the cold. J. Histochem. Cytochem. 2006, 54:1177-1191.
106. Zeiger U., Mitchell C.H., Khurana T.S. Superior calcium homeostasis of extraocular muscles. Exp. Eye Res. 2010, 91:613-622.
107. Zhou Y., Liu D., Kaminski H.J. Myosin heavy chain expression in mouse extraocular muscle: more complex than expected. Investig. Ophthalmol. Vis. Sci. 2010, 51:6355-6363.