Neuronal control of myogenic regulatory factor accumulation in fetal muscle

Developmental Dynamics

Volumn 236, Issue 3, 2007, Pages 732-745

  Washabaugh, Charles H ^a,b   Ontell, Martin P ^a   Shand, Stuart H ^a   Bradbury, Neil ^a,c   Kant, Jeffrey A ^a   Ontell, Marcia ^a  

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

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^c ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

Competitive PCR; Crural muscles; Fetal denervation; MRF mRNA and protein; Myogenesis

Indexed keywords

MESSENGER RNA; MYOD PROTEIN; MYOGENIC FACTOR; MYOGENIC FACTOR 5; MYOGENIC REGULATORY FACTOR 4; MYOGENIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; EXTENSOR DIGITORUM LONGUS MUSCLE; FETUS; FETUS DEVELOPMENT; GENE EXPRESSION REGULATION; MOLECULAR CLONING; MOUSE; MUSCLE DENERVATION; MUSCLE DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; SOLEUS MUSCLE;

ANIMALS; BLOTTING, WESTERN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; MICE; MICROSCOPY, CONFOCAL; MUSCLE DENERVATION; MUSCLES; MYOD PROTEIN; MYOGENIC REGULATORY FACTORS; PREGNANCY; RNA, MESSENGER;

MUS;

EID: 33947402680     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21078     Document Type: Article

References (55)

1. 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.
2. Braun T, Buschhausen-Denker G, Bober E, Tannich E, Arnold HH. 1989. A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO J 8:701-709.
3. Braun T, Bober E, Winter B, Rosenthal N, Arnold HH. 1990. Myf-6, a new member of the human gene family of myogenic determination factors: evidence for a gene cluster on chromosome 12. EMBO J 9:821-831.
4. Brennan TJ, Edmondson DG, Olson EN. 1990. Aberrant regulation of MyoD1 contributes to the partially defective myogenic phenotype of BC3H1 Cells. J Cell Biol 110:929-937.
5. Buckingham ME. 1994. Muscle: the regulation of myogenesis. Curr Opin Genet Dev 4:745-751.
6. Buonanno A, Apone L, Morasso MI, Beers R, Brenner HR, Eftimie R. 1992. The MyoD family of myogenic factors is regulated by electrical activity: isolation and characterization of a mouse myf-5 cDNA. Nucleic Acids Res 20:539-544.
7. Byers TJ, Kunkel LM, Watkins SC. 1991. The subcellular distribution of dystrophin in mouse skeletal, cardiac and smooth muscle. J Cell Biol 115:411-421.
8. Clark G, Sperry M. 1945. A simplified Nissl stain with thionin. Stain Technol 20:23-24.
9. Davis RL, Weintraub H, Lassar AB. 1987. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51: 987-1000.
10. Duclert A, Piette J, Changeux JP. 1991. Influence of innervation of myogenic factors and AChR alpha-subunit mRNAs. Neuroreport 2:25-28.
11. Edmondson DG, Olson EN. 1989. A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program. Genes Dev 3:628-640.
12. Eftimie R, Brenner H, Buonanno A. 1991. Myogenin and MyoD join a family of muscle genes regulated by electrical activity. Proc Natl Acad Sci U S A 88:1349-1353.
13. Esser K, Gunning P, Hardman E. 1993. Nerve-dependent and -independent patterns of mRNA expression in regenerating skeletal muscle. Dev Biol 159:173-183.
14. Fujisawa-Sehara A, Nabeshima Y, Komiya T, Uetsuki T, Asakura A, Nabeshima Y. 1992. Differential trans-activation of muscle-specific regulatory elements including the mysosin light chain box by chicken MyoD, myogenin, and MRF4. J Biol Chem 267:10031-10038.
15. Hinterberger TJ, Sassoon DA, Rhodes SJ, Konieczny SF. 1991. Expression of the muscle regulatory factor MRF4 during somite and skeletal myofiber development. Dev Biol 147:144-156.
16. Hughes D. 1992. The development of mammalian skeletal muscle in the absence of innervation. Ph.D. Dissertation. University of Pittsburgh School of Medicine.
17. Hughes D, Ontell M. 1992. Morphometric analysis of the developing murine aneural soleus muscle. Dev Dyn 193:175-184.
18. Hughes D, Schade R, Ontell M. 1992. Ablation of the fetal mouse spinal cord: the effect on soleus muscle cytoarchitecture. Dev Dyn 193:164-174.
19. Hughes SM, Taylor JM, Tapscott SJ, Gurley CM, Carter WJ, Peterson CA. 1993. Selective accumulation of MyoD and myogenin mRNAs in fast and slow adult skeletal muscle is controlled by innervation and hormones. Development 118: 1137-1147.
20. Hughes SM, Kioshi K, Rudnicki MA, Maggs AM. 1997. MyoD protein is differentially accumulated in fast and slow skeletal muscle fibers and required for normal fibre type balance in rodents. Mech Dev 61:151-163.
21. Hyatt J-PK, Roy RR, Baldwin KM, Edgerton VR. 2003. Nerve activity-independent regulation of skeletal muscle atrophy: role of MyoD and myogenin in satellite cells and myonuclei. Am J Physiol Cell Physiol 285:C1161-C1173.
22. Ishido M, Kami K, Masuhara M. 2004. In vivo expression patterns of MyoD, p21, and Rb proteins in myonuclei and satellite cells of denervated rat skeletal muscle. Am J Phsiol Cell Physiol 287:C484-C493.
23. Kostrominova T, Macpherson PCD, Carlson BM, Goldman D. 2000. Regulation of myogenin protein expression in denervated muscle from young and old rats. Am J Physiol Regul Integr Comp Physiol 279:R179-R188.
24. Kraus B, Pette D. 1997. Quantification of MyoD, myogenin, MRF4 and Id-1 by reverse-transcriptase polymerase chain reaction in rat muscles: effects of hypothyroidism and chronic low-frequency stimulation. Eur J Biochem 247:98-106.
25. Lassar AB, Buskin JN, Lockshon D, Davis RL, Apone S, Hauschka SD, Weintraub H. 1989. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle specific creatine kinase enhancer. Cell 58:823-831.
26. Lin H, Yutzey KE, Konieczny SF. 1991. Muscle-specific expression of the troponin I gene requires interactions between helix-loop-helix muscle regulatory factors and ubiquitous transcription factors. Mol Cell Biol 11:267-280.
27. McHanwell S, Biscoe TJ. 1981. The localization of motoneurons supplying the hindlimb muscles of the mouse. Philos Trans R Soc Lond 293:477-508.
28. Miner JH, Wold B. 1990. Herculin, a fourth member of the MyoD family of myogenic regulatory genes. Proc Natl Acad Sci U S A 87:1089-1093.
29. Moschella M, Ontell M. 1987. Transient and chronic neonatal denervation of murine muscle: a procedure to modify the phenotypic expression of muscular dystrophy. J Neurosci 7:2145-2152.
30. Ontell M, Kozeka K. 1984a. The organogenesis of murine striated muscle: a cytoartchitectural study. Am J Anat 171: 133-148.
31. Ontell M, Kozeka K. 1984b. The organogenesis of the mouse extensor digitorum longus striated muscle: a quantitative study. Am J Anat 171:149-162.
32. Ontell M, Bourke D, Hughes D. 1988a. Cytoarchitecture of the fetal murine soleus muscle. Am J Anat 181:267-278.
33. Ontell M, Hughes D, Bourke D. 1988b. Morphometric analysis of the developing mouse soleus muscle. Am J Anat 181: 279-288.
34. Ontell MP, Sopper M, Lyons G, Buckingham M, Ontell M. 1993. Modulation of contractile protein gene expression in fetal murine crural muscles: emergence of muscle diversity. Dev Dyn 198:203-213.
35. Ontell M, Ontell MP, Buckingham M. 1995. Muscle-specific gene expression during myogenesis in the mouse. Microsc Res Tech 30:354-365.
36. Rhodes SJ, Konieczny SF. 1989. Identification of MRF4: a new member of the muscle regulatory factor gene family. Genes Dev 3:2050-2061.
37. Rosenthal N, Berglund EB, Wentworth BM, Donoghue M, Winter B, Bober E, Braun T, Arnold HH. 1990. A highly conserved enhancer downstream of the human MLC1/3 locus is a target for multiple myogenic determining factors. Nucleic Acids Res 18:6239-6246.
38. Sabourin LA, Rudnicki MA. 2000. The molecular regulation of myogenesis. Clin Genet 57:16-25.
39. Snedecor GW, Cochran WG. 1980. Statistical methods. 7th ed. Ames, IA: The Iowa State University Press.
40. Sunyer T, Merlie JP. 1993. Cell type and differentiation-dependent expression from the mouse acetylcholine receptor epsilon-subunit promoter. J Neurosci Res 36: 224-234.
41. Tajbakhsh S, Buckingham M. 2000. The birth of muscle progenitor cells in the mouse: spatiotemporal considerations. In: Ordahl CP, editor. Somitogenesis, current topics in developmental biology. Vol. 47. London: Academic Press. p 225-268.
42. Tang H, Veldman B, Goldman D. 2006. Characterization of a muscle-specific enhancer in human MuSK promoter reveals the essential role of myogenin in controlling activity-dependent gene regulation. J Biol Chem 281:3943-3953.
43. Thomas D, Kleuber K, Bourke D, Ontell M. 1984. The size of myofibers in mature grafts of the mouse extensor digitorum longus muscle. Muscle Nerve 7:226-231.
44. Voytik SL, Przyborski M, Badylak SF, Konieczny SF. 1993. Differential expression of muscle regulatory factor genes in normal and denervated adult rat hind-limb muscles. Dev Dyn 198:214-224.
45. Wagner M, Perry RP. 1985. Characterization of the multigene family encoding the mouse S16 ribosomal protein: strategy for distinguishing an expressed gene from its processed pseudogene counterparts by an analysis of total genomic DNA. Mol Cell Biol 5:3560-3576.
46. Wang ZZ, Washabaugh CH, Yao Y, Wang JM, Zhang L, Ontell MP, Watkins SC, Rudnicki MA, Ontell M. 2003. Abberant development of motor axons and neuromuscular synapses in MyoD-null mice. J Neurosci 23:5161-5169.
47. Washabaugh CH, Ontell MP, Shan Z, Hoffman EP, Ontell M. 1998. Role of the nerve in determining fetal skeletal muscle phenotype. Dev Dyn 211:177-190.
48. Washabaugh CH, Ontell MP, Kant JA, Ontell M. 1999. Creatine kinase transcript accumulation: effect of the nerve during muscle development. Dev Dyn 215:285-296.
49. Weis J. 1994. Jun, Fos, MyoD1 and myogenin proteins are increased in skeletal muscle fiber nuclei after denervation. Act Neuropathol (Berl) 87:63-70.
50. Weis J, Kaussen M, Calvo S, Buonanno A. 2000. Denervation induces a rapid nuclear accumulation of MRF4 in mature myofibers. Dev Dyn 218:438-451.
51. Wigston DJ, English AW. 1992. Fiber-type proportions in mammalian soleus muscle during postnatal development. J Neurobiol 23:61-70.
52. Wirtz P, Loermans HMT, Peer PGM, Reinjes AGM. 1983. Postnatal growth and differentiation of muscle fibers in the mouse. I. A histochemical and morphological investigation of normal muscle. J Anat 137:109-126.
53. Witzemann V, Sakmann B. 1991. Differential regulation of MyoD and myogenin mRNA levels by nerve induced muscle activity. FEBS Lett 282:259-264.
54. Wright WE, Sassoon DA, Lin VK. 1989. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD1. Cell 56:607-617.
55. Yutzey KE, Rhodes SJ, Konieczny SF. 1990. Differential trans activation associated with the muscle regulatory factors MyoD1, myogenin, and MRF4. Mol Cell Biol 10:3934-3944.