A new look at the origin, function, and 'stem-cell' status of muscle satellite cells

Developmental Biology

Volumn 218, Issue 2, 2000, Pages 115-124

  Seale, Patrick ^a   Rudnicki, Michael A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Muscle regeneration; Myf5; MyoD; Myogenic stem cells; Satellite cells

Indexed keywords

BETA1 INTEGRIN; CALCINEURIN; CYTOKINE; DESMIN; DNA; DYSTROPHIN; INTERMEDIATE FILAMENT PROTEIN; MESSENGER RNA; NUCLEAR FACTOR; PROTEIN TYROSINE KINASE INHIBITOR; SCATTER FACTOR; VASCULAR CELL ADHESION MOLECULE 1;

CELL DIFFERENTIATION; GENE; MUSCLE; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SATELLITE CELL; STEM CELL;

EID: 0034651562     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9565     Document Type: Review

References (80)

1. Adams G. R., Haddad F. The relationships among IGF1, DNA content, and protein accumulation during skeletal muscle hypertrophy. J. Appl. Physiol. 81:1996;2509-2516.
2. Adams G. R., McCue S. A. Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats. J. Appl. Physiol. 84:1998;1716-1722.
3. Allen R. E., Sheehan S. M., Taylor R. G., Kendall T. L., Rice G. M. Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J. Cell. Physiol. 165:1995;307-312.
4. Anastasi S., Giordano S., Sthandier O., Gambarotta G., Maione R., Comoglio P., Amati P. A natural hepatocyte growth factor/scatter factor autocrine loop in myoblast cells and the effect of the constitutive Met kinase activation on myogenic differentiation. J. Cell Biol. 137:1997;1057-1068.
5. Appell H. J., Forsberg S., Hollmann W. Satellite cell activation in human skeletal muscle after training: Evidence for muscle fiber neoformation. Int. J. Sports Med. 9:1988;297-299.
6. Armand O., Boutineau A. M., Mauger A., Pautou M. P., Kieny M. Origin of satellite cells in avian skeletal muscles. Arch. Anat. Microsc. Morphol. Exp. 72:1983;163-181.
7. Arnold H. H., Winter B. Muscle differentiation: More complexity to the network of myogenic regulators. Curr. Opin. Genet. Dev. 8:1998;539-544.
8. Austin L., Bower J., Kurek J., Vakakis N. Effects of leukaemia inhibitory factor and other cytokines on murine and human myoblast proliferation. J. Neurol. Sci. 112:1992;185-191.
9. Bianco P., Cossu G. Uno, nessuno, e centomila. Searching for the identity of mesodermal progenitors. Exp. Cell. Res. 251:1999;257-263.
10. Birchmeier C., Gherardi E. Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol. 8:1998;404-410.
11. Bischoff R. Interaction between satellite cells and skeletal muscle fibers. Development. 109:1990;943-952.
12. Bischoff R. The satellite cell and muscle regeneration. Engel A. G., Franszini-Armstrong C. Myogenesis. 1994;97-118 McGraw-Hill, New York.
13. Bischoff R. Chemotaxis of skeletal muscle satellite cells. Dev. Dyn. 208:1997;505-515.
14. Bittner R. E., Schofer C., Weipoltshammer K., Ivanova S., Streubel B., Hauser E., Freilinger M., Hoger H., Elbe-Burger A., Wachtler F. Recruitment of bone-marrow-derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice. Anat. Embryol. 199:1999;391-396.
15. Bjornson C. R., Rietze R. L., Reynolds B. A., Magli M. C., Vescovi A. L. Turning brain into blood: A hematopoietic fate adopted by adult neural stem cells in vivo. Science. 283:1999;534-537.
16. Braun T., Rudnicki M. A., Arnold H. H., Jaenisch R. Targeted inactivation of the muscle regulatory gene Myf5 results in abnormal rib development and perinatal death. Cell. 71:1992;369-382.
17. Bulfield G., Siller W. G., Wight P. A., Moore K. J. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl. Acad. Sci. USA. 81:1984;1189-1192.
18. Cantini M., Carraro U. Macrophage-released factor stimulates selectively myogenic cells in primary muscle culture. J. Neuropathol. Exp. Neurol. 54:1995;121-128.
19. Cantini M., Massimino M. L., Bruson A., Catani C., Dalla Libera L., Carraro U. Macrophages regulate proliferation and differentiation of satellite cells. Biochem. Biophys. Res. Commun. 202:1994;1688-1696.
20. Cornelison D. D., Wold B. J. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol. 191:1997;270-283.
21. Cossu G., Cicinelli P., Fieri C., Coletta M., Molinaro M. Emergence of TPA-resistant 'satellite' cells during muscle histogenesis of human limb. Exp. Cell Res. 160:1985;403-411.
22. Darr K. C., Schultz E. Exercise-induced satellite cell activation in growing and mature skeletal muscle. J. Appl. Physiol. 63:1987;1816-1821.
23. DeAngelis L. D., Berghella L., Coletta M., DeAngelis M. G. C., Lattanzi L., Ponzetto C., Cossu G. Skeletal myogenic progenitors originating from embryonic dorsal aorta co-express endothelial and myogenic markers and contribute to post-natal muscle growth and regeneration. J. Cell Biol. 147:1999;869-878.
24. Dzierzak E. Embryonic beginnings of definitive hematopoietic stem cells. Ann. N. Y. Acad. Sci. 872:1999;256-262.
25. Edwall D., Schalling M., Jennische E., Norstedt G. Induction of insulin-like growth factor I messenger ribonucleic acid during regeneration of rat skeletal muscle. Endocrinology. 124:1989;820-825.
26. Eglitis M. A., Mezey E. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc. Natl. Acad. Sci. USA. 94:1997;4080-4085.
27. Emery A. E. The muscular dystrophies. BMJ. 317:1998;991-995.
28. Feldman J. L., Stockdale F. E. Skeletal muscle satellite cell diversity: Satellite cells form fibers of different types in cell culture. Dev. Biol. 143:1991;320-334.
29. Feldman J. L., Stockdale F. E. Temporal appearance of satellite cells during myogenesis. Dev. Biol. 153:1992;217-226.
30. Ferrari G., Cusella-De Angelis G., Coletta M., Paolucci E., Stornaiuolo A., Cossu G., Mavilio F. Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 279:1998;1528-1530.
31. Floss T., Arnold H. H., Braun T. A role for FGF-6 in skeletal muscle regeneration. Genes Dev. 11:1997;2040-2051.
32. Gal-Levi R., Leshem Y., Aoki S., Nakamura T., Halevy O. Hepatocyte growth factor plays a dual role in regulating skeletal muscle satellite cell proliferation and differentiation. Biochim. Biophys. Acta. 1402:1998;39-51.
33. Gibson M. C., Schultz E. Age-related differences in absolute numbers of skeletal muscle satellite cells. Muscle Nerve. 6:1983;574-580.
34. Goodell M. A., Brose K., Paradis G., Conner A. S., Mulligan R. C. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp. Med. 183:1996;1797-1806.
35. Goodell M. A., Rosenzweig M., Kim H., Marks D. F., DeMaria M., Paradis G., Grupp S. A., Sieff C. A., Mulligan R. C., Johnson R. P. Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat. Med. 3:1997;1337-1345.
36. Grounds M. D. Age-associated changes in the response of skeletal muscle cells to exercise and regeneration. Ann. N. Y. Acad. Sci. 854:1998;78-91.
37. Grounds M. D., Yablonka-Reuveni Z. Molecular and cell biology of skeletal muscle regeneration. Mol. Cell. Biol. Hum. Dis. Ser. 3:1993;210-256.
38. Gussoni E., Soneoka Y., Strickland C. D., Buzney E. A., Khan M. K., Flint A. F., Kunkel L. M., Mulligan R. C. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature. 401:1999;390-394.
39. Hartley R. S., Bandman E., Yablonka-Reuveni Z. Skeletal muscle satellite cells appear during late chicken embryogenesis. Dev. Biol. 153:1992;206-216.
40. Hoh J. F., Hughes S. Expression of superfast myosin in aneural regenerates of cat jaw muscle. Muscle Nerve. 14:1991;316-325.
41. Hughes S. M., Blau H. M. Migration of myoblasts across basal lamina during skeletal muscle development. Nature. 345:1990;350-353.
42. Irintchev A., Zeschnigk M., Starzinski-Powitz A., Wernig A. Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev. Dyn. 199:1994;326-337.
43. Jackson K. O., Mi T., Goodell M. A. Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc. Natl. Acad. Sci. USA. 1999.
44. Jesse T. L., LaChance R., Iademarco M. F., Dean D. C. Interferon regulatory factor-2 is a transcriptional activator in muscle where it regulates expression of vascular cell adhesion molecule-1. J. Cell Biol. 140:1998;1265-1276.
45. Kaufmann U., Martin B., Link D., Witt K., Zeitler R., Reinhard S., Starzinski-Powitz A. M-cadherin and its sisters in development of striated muscle. Cell Tissue Res. 296:1999;191-198.
46. Kurek J. B., Nouri S., Kannourakis G., Murphy M., Austin L. Leukemia inhibitory factor and interleukin-6 are produced by diseased and regenerating skeletal muscle. Muscle Nerve. 19:1996;1291-1301.
47. Lescaudron L., Peltekian E., Fontaine-Perus J., Paulin D., Zampieri M., Garcia L., Parrish E. Blood borne macrophages are essential for the triggering of muscle regeneration following muscle transplant. Neuromuscul. Disord. 9:1999;72-80.
48. Matsuda R., Spector D. H., Strohman R. C. Regenerating adult chicken skeletal muscle and satellite cell cultures express embryonic patterns of myosin and tropomyosin isoforms. Dev. Biol. 100:1983;478-488.
49. Mauro A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9:1961;493-495.
50. Megeney L. A., Kablar B., Garrett K., Anderson J. E., Rudnicki M. A. MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev. 10:1996;1173-1183.
51. Megeney L. A., Rudnicki M. A. Determination versus differentiation and the MyoD family of transcription factors. Biochem. Cell Biol. 73:1995;723-732.
52. Merly F., Lescaudron L., Rouaud T., Crossin F., Gardahaut M. F. Macrophages enhance muscle satellite cell proliferation and delay their differentiation. Muscle Nerve. 22:1999;724-732.
53. Musaro A., McCullagh K. J., Naya F. J., Olson E. N., Rosenthal N. IGF1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1. Nature. 400:1999;581-585.
54. Orimo S., Hiyamuta E., Arahata K., Sugita H. Analysis of inflammatory cells and complement C3 in bupivacaine-induced myonecrosis. Muscle Nerve. 14:1991;515-520.
55. Pardanaud L., Dieterlen-Lievre F. Manipulation of the angiopoietic/hemangiopoietic commitment in the avian embryo. Development. 126:1999;617-627.
56. Pardanaud L., Luton D., Prigent M., Bourcheix L. M., Catala M., Dieterlen-Lievre F. Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis. Development. 122:1996;1363-1371.
57. Rosen G. D., Sanes J. R., LaChance R., Cunningham J. M., Roman J., Dean D. C. Roles for the integrin VLA-4 and its counter receptor VCAM-1 in myogenesis. Cell. 69:1992;1107-1119.
58. Rosenblatt J. D., Parry D. J., Partridge T. A. Phenotype of adult mouse muscle myoblasts reflects their fiber type of origin. Differentiation. 60:1996;39-45.
59. Rosenblatt J. D., Yong D., Parry D. J. Satellite cell activity is required for hypertrophy of overloaded adult rat muscle. Muscle Nerve. 17:1994;608-613.
60. Rudnicki M. A., Braun T., Hinuma S., Jaenisch R. Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf5 and results in apparently normal muscle development. Cell. 71:1992;383-390.
61. Sabourin L. A., Girgis-Gabardo A., Seale P., Asakura A., Rudnicki M. A. Reduced differentiation potential of primary MyoD-/- myogenic cells derived from adult skeletal muscle. J. Cell Biol. 144:1999;631-643.
62. Schultz E. Fine structure of satellite cells in growing skeletal muscle. Am. J. Anat. 147:1976;49-70.
63. Schultz E. Satellite cell behavior during skeletal muscle growth and regeneration. Med. Sci. Sports Exerc. 21:1989;S181-186.
64. Schultz E. Satellite cell proliferative compartments in growing skeletal muscles. Dev. Biol. 175:1996;84-94.
65. Schultz E., Albright D. J., Jaryszak D. L., David T. L. Survival of satellite cells in whole muscle transplants. Anat. Rec. 222:1988;12-17.
66. Schultz E., Jaryszak D. L. Effects of skeletal muscle regeneration on the proliferation potential of satellite cells. Mech. Ageing Dev. 30:1985;63-72.
67. Schultz E., Jaryszak D. L., Gibson M. C., Albright D. J. Absence of exogenous satellite cell contribution to regeneration of frozen skeletal muscle. J. Muscle Res. Cell Motil. 7:1986;361-367.
68. Schultz E., Jaryszak D. L., Valliere C. R. Response of satellite cells to focal skeletal muscle injury. Muscle Nerve. 8:1985;217-222.
69. Sheehan S. M., Allen R. E. Skeletal muscle satellite cell proliferation in response to members of the fibroblast growth factor family and hepatocyte growth factor. J. Cell. Physiol. 181:1999;499-506.
70. Shibasaki F., Price E. R., Milan D., McKeon F. Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature. 382:1996;370-373.
71. Sicinski P., Geng Y., Ryder-Cook A. S., Barnard E. A., Darlison M. G., Barnard P. J. The molecular basis of muscular dystrophy in the mdx mouse: A point mutation. Science. 244:1989;1578-1580.
72. Smith C. K. 2nd, 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. 159:1994;379-385.
73. Tatsumi R., Anderson J. E., Nevoret C. J., Halevy O., Allen R. E. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev. Biol. 194:1998;114-128.
74. Tidball J. G. Inflammatory cell response to acute muscle injury. Med. Sci. Sports Exerc. 27:1995;1022-1032.
75. Watt D. J., Morgan J. E., Clifford M. A., Partridge T. A. The movement of muscle precursor cells between adjacent regenerating muscles in the mouse. Anat. Embryol. 175:1987;527-536.
76. Webster C., Blau H. M. Accelerated age-related decline in replicative life-span of Duchenne muscular dystrophy myoblasts: Implications for cell and gene therapy. Somatic Cell Mol. Genet. 16:1990;557-565.
77. Yablonka-Reuveni Z., Rivera A. J. Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev. Biol. 164:1994;588-603.
78. Yablonka-Reuveni Z., Rudnicki M. A., Rivera A. J., Primig M., Anderson J. E., Natanson P. The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD. Dev. Biol. 210:1999;440-455.
79. Yang J. T., Rando T. A., Mohler W. A., Rayburn H., Blau H. M., Hynes R. O. Genetic analysis of alpha 4 integrin functions in the development of mouse skeletal muscle. J. Cell Biol. 135:1996;829-835.
80. Zeschnigk M., Kozian D., Kuch C., Schmoll M., Starzinski-Powitz A. Involvement of M-cadherin in terminal differentiation of skeletal muscle cells. J. Cell Sci. 108:1995;2973-2981.