Heterogeneity among muscle precursor cells in adult skeletal muscles with differing regenerative capacities

Developmental Dynamics

Volumn 212, Issue 4, 1998, Pages 495-508

  Pavlath, Grace K ^a   Thaloor, Deepa ^a   Rando, Thomas A ^b,c   Cheong, Monica ^b,c   English, Arthur W ^a   Zheng, Bin ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Masseter muscle; Muscle precursor cells; Muscle regeneration; Myoblast heterogeneity; Trauma

Indexed keywords

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HETEROGENEITY; CELL POPULATION; CONTROLLED STUDY; CYTOARCHITECTURE; LEG MUSCLE; MALE; MASSETER MUSCLE; MASTICATORY MUSCLE; MOUSE; MUSCLE DEVELOPMENT; MUSCLE GROWTH; MUSCLE INJURY; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; MYOBLAST; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL COUNT; CELL DIFFERENTIATION; MALE; MASSETER MUSCLE; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MUSCLE, SKELETAL; MYOD PROTEIN; REGENERATION; STEM CELLS; WOUNDS AND INJURIES;

ANIMALIA;

EID: 0031881052     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0177(199808)212:4<495::AID-AJA3>3.0.CO;2-C     Document Type: Article

References (65)

1. Anderson JE, Mitehell CM, McGeachie JK, Grounds MD. The time course of basic fibroblast growth factor expression in crush-injured skeletal muscles of SJL/J and BALB/c mice. Exp. Cell Res. 1995;216: 325-334.
2. Anderson JE, Ovalle WK, Bressler BH. Electron microscopic and autoradiographic characterization of hindlimb muscle regeneration in the mdx mouse. Anat. Rec. 1987;219:243-257.
3. Bakke M, Kirkeby S, Jensen BL, Hansen HJ, Kreiborg S, Hjorting-Hansen E, Michler L, Moller E. Structure and function of masticatory muscles in a case of muscular dystrophy. J. Oral Pathol. Med. 1990;19:335-340.
4. Barnard W, Bower J, Brown MA, Murphy M, Austin L. Leukemia inhibitory factor (LIF) infusion stimulates skeletal muscle regeneration after injury: Injured muscle expresses lif mRNA. J. Neurol. Sci. 1994;123:108-113.
5. Bischoff R. A satellite cell mitogen from crushed adult muscle. Dev. Biol. 1986;115:140-147.
6. Blau HM, Webster C. Isolation and characterization of human muscle cells. Proc. Natl. Acad. Sci. USA 1981;78:5623-5627.
7. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976;72:248-254.
8. Cantini M, Carraro U. Macrophage-released factor stimulates selectively myogenic cells in primary muscle culture. J. Neuropathol. Exp. Neurol. 1995;54:121-128.
9. 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. 1994;202:1688-1696.
10. Cantini M, Massimino ML, Rapizzi E, Rossini K, Catani C, Dalla Libera L, Carraro U. Human satellite cell proliferation in vitro is regulated by autocrine secretion of IL-6 stimulated by a soluble factor(s) released by activated monocytes. Biochem. Biophys. Res. Commun. 1995;216:49-53.
11. Cho M, Hughes SM, Karsch-Mizrachi I, Travis M, Leinwand LA, Blau HM. Fast myosin heavy chains expressed in secondary mammalian muscle fibers at the time of their inception. J. Cell. Sci. 1994;107: 2361-2371.
12. 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. 1985;160:403-411.
13. Couly GF, Coltey PM, Le Douarin NM. The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 1992;114: 1-15.
14. Couly F, Coltey PM, Le Douarin NM. The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 1993;117:409-429.
15. Cusella-De Angelis MG, Molinari S, Le Donne A, Coletta M, Vivarelli E, Bouche M, Molinaro M, Ferrari S, Cossu G. Differential response of embryonic and fetal myoblasts to TGF beta: A possible regulatory mechanism of skeletal muscle histogenesis. Development 1994; 120: 925-933.
16. Davis RL, Weintraub H, Lassar AB. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 1987;51:987-1000.
17. Gibson MC, Schultz E. Age-related differences in absolute numbers of skeletal muscle satellite cells. Muscle Nerve 1983;6:574-580.
18. Grounds MD, McGeachie JK. A comparison of muscle precursor replication in crush-injured skeletal muscle of Swiss and BALBc mice. Cell Tissue Res. 1989;255:385-931.
19. Grounds MD, Yablonka-Reuveni Z. Molecular and cell biology of skeletal muscle regeneration. Mol. Cell. Biol. Hum. Dis. Ser. 1993;3: 210-256.
20. Gulati AK. Long-term retention of regenerative capability after denervation of skeletal muscle, and dependency of late differentiation on innervation. Anat. Rec. 1988;220:429-34.
21. Hatta K, Schilling TF, BreMiller RA, Kimmel B. Specification of jaw muscle identity in zebrafish: Correlation with engrailed-homeoprotein expression. Science 1990;250:802-805.
22. Hoh JFY, Hughes S, Kang LHD, Rughani A, and Qin H. The biology of cat jaw-closing muscle cells. J. Comp.-Assist. Microsc. 1993;5: 65-70.
23. Jennische E, Ekberg S, Matejka L. Expression of hepatocyte growth factor in growing and regenerating rat skeletal muscle. Am. J. Physiol. 1993;265:C122-C1228.
24. Jennische E, Matejka GL. IGF-I binding and IGF-I expression in regenerating muscle of normal and hypophysectomized rats. Acta Physiol. Scand. 1992; 146:79-86.
25. Karpati G, Carpenter S, Prescott S. Small-caliber skeletal muscle fibers do not suffer necrosis in mdx mouse dystrophy. Muscle Nerve 1988;11:795-803.
26. Koishi K, Zhang M, McLennan IS, Harris AJ. MyoD protein accumulates in satellite cells and is neurally regulated in regenerating myotubes and skeletal muscle fibers. Dev. Dyn. 1995;202:244-254.
27. Krishan K, Dhoot GK. Changes in some troponin and insulin-like growth factor messenger ribonucleic acids in regenerating and denervated skeletal muscles. J. Muscle Res. Cell Motil. 1996;17:513-521.
28. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-685.
29. Levinovitz A, Jennische E, Oldfors A, Edwall D, Norstedt G. Activation of insulin-like growth factor II expression during skeletal muscle regeneration in the rat: Correlation with myotube formation. Mol. Endocrinol. 1992;6:1227-1234.
30. Maley MA, Fan Y, Beilharz MW, Grounds MD. Intrinsic differences in MyoD and myogenin expression between primary cultures of SJL/J and BALB/C skeletal muscle. Exp. Cell Res. 1994;211:99-107.
31. Maley MA, Davies MJ, Grounds MD. Extracellular matrix, growth factors, genetics: their influence on cell proliferation and myotube formation in primary cultures of adult mouse skeletal muscle. Exp. Cell Res. 1995;219:169-179.
32. Mauro A. Satellite cells of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 1961;9:493-495.
33. McGeachie JK, Grounds MD. Retarded myogenic cell replication in regenerating skeletal muscles of old mice: An autoradiographic study in young and old BALBc and SJL/J mice. Cell Tissue Res. 1995;280:277-282.
34. McLennan IS, Koishi K. Cellular localisation of transforming growth factor-beta 2 and -beta 3 (TGF-beta2, TGF-beta3) in damaged and regenerating skeletal muscles. Dev. Dyn. 1997;208:278-289.
35. Miller JB, Stockdale FE. Developmental origins of skeletal muscle fibers: clonal analysis of myogenic cell lineages based on expression of fast and slow myosin heavy chains. Proc. Nat.l Acad. Sci. USA 1986a;83:3860-3864.
36. Miller JB, Stockdale FE. Developmental regulation of the multiple myogenic cell lineages of the avian embryo. J. Cell. Biol. 1986b; 103: 2197-2208.
37. Mitchell CA, McGeachie JK, Grounds MD. Cellular differences in the regeneration of murine skeletal muscle: A quantitative histological study in SJL/J and BALB/c mice. Cell Tissue Res. 1992;269:159-166.
38. Mitchell CA, Grounds MD, Papadimitriou JM. The genotype of bone marrow-derived inflammatory cells does not account for differences in skeletal muscle regeneration between SJL/J and BALB/c mice. Cell Tissue Res. 1995;280:407-413.
39. Mong FS. Experimental studies on masseter muscle grafts in rats: Comparison of donor muscles. J. Oral Rehabil. 1989;16:315-321.
40. Noden DM. The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Am. J. Anat. 1983; 168: 257-276.
41. Orvis JS, Cardinet GHd. Canine muscle fiber types and susceptibility of masticatory muscles to myositis. Muscle Nerve 1981;4:354-359.
42. Pimorady-Esfahani A, Grounds MD, McMenamin PG. Macrophages and dendritic cells in normal and regenerating murine skeletal muscle. Muscle Nerve 1997;20:158-166.
43. Pullinger AG, Monteiro AA. History factors associated with symptoms of temporomandibular disorders. J. Oral Rehabil. 1988;15:117-124.
44. Pullinger AG, Seligman DA. Trauma history in diagnostic groups of temporomandibular disorders. Oral Surg. Oral Med. Oral Pathol. 1991;71:529-534.
45. Rando TA, Blau HM. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J. Cell Biol. 1994;125:1275-1287.
46. Rich M, Lichtman JW. Motor nerve terminal loss from degenerating muscle fibers. Neuron 1989;3:677-688.
47. Robertson TA, Maley A, Grounds MD, Papadimitriou JM. The role of macrophages in skeletal muscle regeneration with particular reference to chemotaxis. Exp. Cell Res. 1993;207:321-331.
48. Sasagasako N, Yamada T, Kohtake N, Kobayashi T, Goto I. Expression of basic fibroblast growth factor in skeletal muscle after experimentally induced myonecrosis. Muscle Nerve 1994;17:1343-1345.
49. Scher N, Dobleman TJ, Poe DS, Panje WR. Proliferative myositis of the masseter muscle. Laryngoscope 1987;97:591-593.
50. Schmalbruch H, Hellhammer U. The number of nuclei in adult rat muscles with special reference to satellite cells. Anat. Rec. 1977;189: 169-175.
51. Sesodia S, Cullen MJ. The effect of denervation on the morphology of regenerating rat soleus muscles. Acta Neuropathol. (Berl.) 1991;82: 21-32.
52. Sesodia S, Choksi RM, Nemeth PM. Nerve-dependent recovery of metabolic pathways in regenerating soleus muscles. J. Muscle Res. Cell Motil. 1994;15:573-581.
53. Shelton GD, Cardinet GHd, Bandman E. Canine masticatory muscle disorders: A study of 29 cases. Muscle Nerve 1987;10:753-766.
54. Singer A, Chikarmane A, Festoff BW, Ziegler DK. Trismus. An unusual sign in polymyositis. Arch. Neurol. 1985;42:1116-1118.
55. Snow MH. A quantitative ultrastructural analysis of satellite cells in denervated fast and slow muscles of the mouse. Anat. Rec. 1983;207: 593-604.
56. 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.
57. Tal M. The effect of a long-acting local anaesthetic agent (Marcaine) on the masticatory muscle in rats. Int.J. Oral Surg. 1982;11:101-105.
58. Tan SS. Liver-specific and position-effect expression of a retinol-binding protein-lacZ fusion gene (RBP-lacZ) in transgenic mice. Dev. Biol. 1991;146:24-37.
59. Tanabe Y, Esaki K, Nomura T. Skeletal muscle pathology in X chromosome-linked muscular dystrophy (mdx) mouse. Acta Neuropathol. (Berl). 1986;69:91-95.
60. Tidball JG. Inflammatory cell response to acute muscle injury. Med. Sci. Sports Exerc. 1995;27:1022-1032.
61. Vilmann H, Kirkeby S. Histomorphometrical aspects of the postnatal development of masticatory muscle in the muscular dystrophic mouse. Anat. Anz. 1991:172:109-116.
62. Wakeford S, Watt DJ, Partridge, TA. X-irradiation improves mdx mouse muscle as a model of myofiber loss in DMD. Muscle Nerve 1991;14:42-50.
63. 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.
64. Yablonka-Reuveni Z, Seifert RA. Proliferation of chicken myoblasts is regulated by specific isoforms of platelet-derived growth factor: Evidence for differences between myoblasts from mid and late stages of embryogenesis. Dev. Biol. 1993;156:307-318.
65. Young RB, Miller TR, Merkel RA. Clonal analysis of satellite cells in growing mice. J. Anim. Sci. 1978;46:1241-1249.