MyoD and myogenin protein expression in skeletal muscles of senile rats

Cell and Tissue Research

Volumn 311, Issue 3, 2003, Pages 401-416

  Dedkov, Eduard I ^a   Kostrominova, Tatiana Y ^a,b   Borisov, Andrei B ^a   Carlson, Bruce M ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Aging; Muscle fibers; MyoD; Myogenin; Rat (WI HicksCar); Satellite cells; Skeletal muscles

Indexed keywords

ANTIBODY; MYOD PROTEIN; MYOGENIC FACTOR; MYOGENIN;

AGED; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL NUCLEUS; CONTROLLED STUDY; EXTENSOR DIGITORUM LONGUS MUSCLE; GASTROCNEMIUS MUSCLE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MUSCLE DENERVATION; NERVE FIBER; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; SATELLITE CELL; SENILITY; SKELETAL MUSCLE; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

ANIMALIA;

EID: 0037361978     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-002-0686-9     Document Type: Article

References (51)

1. Abu-Hatoum O, Gross-Mesilaty S, Breitschopf K, Hoffman A, Gonen H, Ciechanover A, Bengal E (1998) Degradation of myogenic transcription factor MyoD by the ubiquitine pathway in vivo and in vitro: regulation by specific DNA binding. Mol Cell Biol 18:5670-5677
2. Adams L, Carlson BM, Henderson L, Goldman D (1995) Adaptation of nicotinic acetylcholine receptor, myogenin, and MRF4 gene expression to long-term muscle denervation. J Cell Biol 131:1341-1349
3. Alway SE, Lowe DA, Chen KD (2001) The effects of age and hindlimb suspension on the levels of expression of the myogenic regulatory factors MyoD and myogenin in rat fast and slow skeletal muscles. Exp Physiol 86:509-517
4. Alway SE, Degens H, Lowe DA, Krishnamurthy G (2002) Increased myogenic repressor Id mRNA and protein levels in hindlimb muscles of aged rats. Am J Physiol Regul Integrative Comp Physiol 282:R411-R422
5. Breitschopf K, Bengal E, Ziv T, Admon A, Ciechanover A (1998) A novel site for ubiquitination: the N-terminal residue, and not internal lysines of MyoD, is essential for conjugation and degradation of the protein. EMBO J 17:5964-5973
6. Buonanno A, Cheng J, Venepally P, Weis J, Calvo S (1998) Activity-dependent regulation of muscle genes: repressive and stimulatory effects of innervation. Acta Physiol Scand 163:S17-S26
7. Caccia MR, Harris JB, Johnson MA (1979) Morphology and physiology of skeletal muscle in aging rodents. Muscle Nerve 2:202-212
8. Carlson BM (1995) Factors influencing the repair and adaptation of muscles in aged individuals: satellite cells and innervation. J Gerontol Biol Sci 50A:96-100
9. Carlson BM, Dedkov EI, Borisov AB, Faulkner JA (2001) Skeletal muscle regeneration in very old rats. J Gerontol Biol Sci 56A:B224-B233
10. Cooper RN, Tajbakhsh S, Mouly V, Cossu G, Buckingham M, Butler-Browne GS (1999) In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J Cell Sci 112:2895-2901
11. Creuzet S, Lescaudron L, Li Z, Fontaine-Perus J (1998) MyoD, myogenin, and desmin-nls-lacZ transgene emphasize the distinct patterns of satellite cell activation in growth and regeneration. Exp Cell Res 243:241-253
12. Daniloff JK, Levi G, Grumet M, Rieger F, Edelman GM (1986) Altered expression of neuronal cell adhesion molecules induced by nerve injury and repair. J Cell Biol 103:929-945
13. Dedkov EI, Kostrominova TY, Borisov AB, Carlson BM (2001) Reparative myogenesis in long-term denervated skeletal muscles of adult rats results in a reduction of the satellite cell population. Anat Rec 263:139-154
14. Dias P, Parham DM, Shapiro DN, Tapscott SJ, Houghton PJ (1992) Monoclonal antibodies to the myogenic regulatory protein MyoD1: epitope mapping and diagnostic utility. Cancer Res 52:6431-6439
15. Duclert A, Piette J, Changeux J-P (1991) Influence of innervation of myogenic factors and acetylcholine receptor α-subunit mRNAs. NeuroReport 2:25-28
16. Dupont-Versteegden EE, Houle JD, Gurley CM, Peterson CA (1998) Early changes in muscle fiber size and gene expression in response to spinal cord transection and exercise. Am J Physiol Cell Physiol 275:C1124-C1133
17. Edmondson DG, Olson EN (1993) Helix-loop-helix proteins as regulators of muscle-specific transcription. J Biol Chem 268:755-758
18. Eftimie R, Brenner HR, Buonanno A (1991) Myogenin and MyoD join a family of skeletal muscle genes regulated by electrical activity. Proc Natl Acad Sci USA 88:1349-1353
19. Faulkner JA, Brooks SV, Zebra E (1995) Muscle atrophy and weakness with aging: contraction-induced injury as an underlying mechanism. J Gerontol Biol Sci 50A:124-129
20. Füchtbauer E-M, Westphal H (1992) MyoD and myogenin are coexpressed in regenerating skeletal muscle of the mouse. Dev Dyn 193:34-39
21. Fujisawa K (1974) Some observations on the skeletal musculature of aged rats. J Neurol Sci 22:353-366
22. Funk WD, Ouellette M, Wright WE (1991) Molecular biology of myogenic regulatory factors. Mol Biol Med 8:185-195
23. Gomes RR Jr, Booth FW (1998) Expression of acetylcholine receptor mRNAs in atrophying and non-atrophying skeletal muscles of old rats. J Appl Physiol 85:1903-1908
24. Grounds MD, Garrett KL, Lai MC, Wright WE, Beilharz MW (1992) Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell Tissue Res 267:99-104
25. Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91:534-551
26. Hughes SM, Koishi K, Rudnicki M, Maggs AM (1997) MyoD protein is differentially accumulated in fast and slow skeletal muscle fibers and required for normal fiber type balance in rodents. Mech Dev 61:151-163
27. Irintchev A, Zeschnigk M, Starzinski-Powitz A, Wernig A (1994) Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev Dyn 199:326-337
28. Kami K, Noguchi K, Senba E (1995) Localization of myogenin, c-fos, c-jun, and muscle-specific gene mRNAs in regenerating rat skeletal muscle. Cell Tissue Res 280:11-19
29. Kaufmann U, Martin B, Link D, Witt K, Zeitler R, Reinhard S, Starzinski-Powitz A (1999) M-cadherin and its sisters in development of striated muscle. Cell Tissue Res 296:191-198
30. Koishi K, Zhang M, McLennan IS, Harris AJ (1995) MyoD protein accumulates in satellite cells and is neurally regulated in regenerating myotubes and skeletal muscle fibers. Dev Dyn 202:244-254
31. Kostrominova TY, Macpherson PCD, Carlson BM, Goldman D (2000) Regulation of myogenin protein expression in denervated muscles from young and old rats. Am J Physiol Regul Integrative Comp Physiol 279:R179-R188
32. Larsson L (1982) Aging in mammalian skeletal muscle. In: Mortimer JA, Pirozzolo FJ, Maletta GJ (eds) The aging motor system. Praeger, New York, pp 60-97
33. Larsson L, Ramamurthy B (2000) Aging-related changes in skeletal muscle. Drugs Aging 17:303-316
34. Launay T, Armand A-S, Charbonnier F, Mira J-C, Donsez E, Gallien CL, Chanoine C (2001) Expression and neural control of myogenic regulatory factor genes during regeneration of mouse soleus. J Histochem Cytochem 49:887-899
35. Lowe DA, Lund T, Always SE (1998) Hypertrophy-stimulated myogenic regulatory factor mRNA increases are attenuated in fast muscle of aged quails. Am J Physiol 275 (Cell Physiol 44):C155-C162
36. Marsh DR, Criswell DS, Carson JA, Booth FW (1997) Myogenic regulatory factors during regeneration of skeletal muscle in young, adult, and old rats. J Appl Physiol 83:1270-1275
37. Moore SE, Walsh FS (1986) Nerve dependent regulation of neural cell adhesion molecule expression in skeletal muscle. Neurosci 18:499-505
38. Musaro A, Cusella De Angelis MG, Germani A, Ciccarelli C, Molinaro M, Zani BM (1995) Enhanced expression of myogenic regulatory genes in aging skeletal muscle. Exp Cell Res 221:241-248
39. Navarro A, Lopez-Cepero JM, Sanchez del Pino MJ (2001) Skeletal muscle and aging. Front Biosci 6:D26-D44
40. Neville C, Rosenthal N (1996) Transcriptional regulation of skeletal myogenesis. In: Goodbourn S (ed) Eukariotic gene transcription. Oxford University Press, Oxford, pp 192-233
41. Puri PL, Sartorelli V (2000) Regulation of muscle regulatory factors by DNA-binding, interacting proteins, and post-transcriptional modifications. J Cell Physiol 185:155-173
42. Robertson TA, Grounds MD, Mitchell CA, Papadimitriou JM (1990) Fusion between myogenic cells in vivo: an ultrastructural study in regenerating murine skeletal muscle. J Struct Biol 105:170-182
43. Sabourin LA, Rudnicki MA (2000) The molecular regulation of myogenesis. Clin Genet 57:16-25
44. Sakuma K, Watanabe K, Sano M, Uramoto I (1999) The adaptive response of MyoD family proteins in overloaded, regenerating and denervated rat muscles. Biochim Biophys Acta 1428:284-292
45. Sanes JR, Schachner M, Covault J (1986) Expression of several adhesive macromolecules (N-CAM, L1, J1, NILE, uvomorulin, laminin, fibronectin, and a heparan sulfate proteoglycan) in embryonic, adult, and denervated adult skeletal muscle. J Cell Biol 102:420-431
46. Schmalbruch H, Lewis DM (2000) Dynamics of nuclei of muscle fibers and connective tissue cells in normal and denervated rat muscles. Muscle Nerve 23:617-626
47. Tamaki T, Uchiyama S, Uchiyama Y, Akatsuka A, Yoshimura S, Roy RR, Edgerton VR (2000) Limited myogenic response to a single bout of weight-lifting exercise in old rats. Am J Physiol Cell Physiol 278:C1143-C1152
48. Tapscott SJ, Davis RL, Thayer MJ, Cheng P-F, Weintraub H, Lassar AB (1988) MyoD1: a nuclear phosphoprotein requiring a myc homology region to convert fibroblasts to myoblasts. Science 242:405-411
49. Voytik SL, Przyborski M, Badylak SF, Konieczny SF (1993) Differential expression of muscle regulatory factor genes in normal and denervated adult rat hindlimb muscles. Dev Dyn 198:214-224
50. Weis J (1994) Jun, Fos, MyoD1 and myogenin proteins are increased in skeletal muscle fiber nuclei after denervation. Acta Neuropathol 87:63-70
51. Witzemann V, Sakmann B (1991) Differential regulation of MyoD and myogenin mRNA levels by nerve induced muscle activity. FEBS Lett 282:259-264