Differential expression of myosin heavy chain mRNA and protein isoforms in four functionally diverse rabbit skeletal muscles during pre- and postnatal development

Developmental Dynamics

Volumn 211, Issue 3, 1998, Pages 193-203

  Mckoy, Godfrina ^a   Léger, Marie Eva ^b   Bacou, Francis ^b   Goldspink, Geoffrey ^a,c  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b CEMAGREF   (France)

^c ROYAL FREE HOSPITAL   (United Kingdom)

Author keywords

3' untranslated region; Development; Gene expression; Myosin; Myosin heavy chain genes; Nucleotide sequences; Protein isoforms; Skeletal muscle

Indexed keywords

MYOSIN HEAVY CHAIN;

ANIMAL TISSUE; ARTICLE; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; SKELETAL MUSCLE;

ANIMALS; BASE SEQUENCE; DIAPHRAGM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES; MOLECULAR SEQUENCE DATA; MUSCLE DEVELOPMENT; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; RABBITS; RNA, MESSENGER; VARIATION (GENETICS);

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0031947778     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0177(199803)211:3<193::AID-AJA1>3.0.CO;2-C     Document Type: Article

References (56)

1. Aigner S, Gohlsch B, Hamalainen N, Staron RS, Über A, Wehrle U, Pette D. Fast myosin heavy chain diversity in skeletal muscles of the rabbit: Heavy chain IId, not IIb predominates. Eur. J. Biochem. 1993;211:367-372.
2. Bacou F, Rouanet P, Barjot C, Janmot C, Vigneron P, d'Albis A. Expression of myosin isoforms in denervated, cross-reinnervated and electrically stimulated rabbit muscles. Eur. J. Biochem. 1996; 236:539-547.
3. Barany M. ATPase activity of myosin correlated with speed of muscle shortening. J. Gen. Physiol. 1967;50:197-216.
4. Barjot C, Cotten ML, Goblet C, Whalen RG, Bacou F. Expression of myosin heavy chain and of myogenic regulatory factor genes in fast or slow rabbit muscle satellite cell cultures. J. Muscle Res. Cell Motil. 1995;16:619-628.
5. Bottinelli R, Schiaffino S, Reggiani C. Force-velocity relations and myosin heavy chain isoform compositions of skinned fibres from rat skeletal muscle. J. Physiol. 1991;437:655-672.
6. Bottinelli R, Betto R, Schiaffino S, Reggiani C. Maximum shortening velocity and coexistence of myosin heavy chain isoforms in single skinned fast fibres of rat skeletal muscle. J. Muscle Res. Cell Motil. 1994;15:413-419.
7. Briand M, Boissonnet G, Laplace-Marieze V, Briand Y. Metabolic and contractile differentiation of rabbit muscles during growth. Int. J. Biochem. 1993;25:1881-1887.
8. Butler-Brown GS, Whalen, RG. Myosin isozyme transitions occurring during the postnatal development of the rat soleus muscle. Dev. Biol. 1984;102:324-334.
9. Caiozzo VJ, Haddad F, Baker MJ, Baldwin KM. Influence of mechanical loading on myosin heavy-chain protein and mRNA isoform expression. J. Appl. Physiol. 1996;80:1503-1512.
10. Chizzonite RA, Everett AW, Clark WA, Jakovcic S, Rabinowitz M, Zak R. Isolation and characterization of two molecular variants of myosin heavy chain from rabbit ventricle. Change in their content during normal growth and after treatment with thyroid hormone. J. Biol. Chem. 1982;257:2056-2065.
11. Chomczynski P, Sacchi N. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987;162:156-159.
12. Chou M, Webster SG, Blau HM. Evidence for myoblast-extrinsic regulation of slow myosin heavy chain expression during muscle fibre formation in embryonic development. J. Cell Biol. 1993;121:795-810.
13. d'Albis A, Pantaloni C, Béchet JJ An electrophoretic study of native myosin isozymes and of their subunit content. Eur. J. Biochem. 1979;99:261-272.
14. DeNardi C, Ausoni S, Moretti P, Gorza L, Velleca M, Buckingham M, Schiaffino S. Type 2X-myosin heavy chain is coded by a muscle fibre type specific and developmentally regulated gene. J. Cell Biol. 1993;123:823-835.
15. Ennion S, Sant'ana Pereira J, Sargeant AJ, Young A, Goldspink G. Characterization of human skeletal muscle fibres according to the myosin heavy chains they express. J. Muscle Res. Cell Motil. 1995a;16:35-43.
16. Ennion S, Gauvry L, Butterworth P, Goldspink G. Small-diameter white myotomal muscle fibres associated with growth hyperplasia in the carp (Cyprinus carpio) express a distinct myosin heavy chain gene. J. Expt. Biol. 1995b;198:1603-1611.
17. Gambke B, Lyons GE, Haselgrove J, Kelly AM, Rubinstein NA. Thyroidal and neural control of myosin transition during development of rat fast and slow muscles. FEBS Lett. 1983;156:335-339.
18. Goldfine SM, Einheber S, Fischman DA. Cell free incorporation of newly synthesized myosin subunits into thick myofilaments. J. Muscle Res. Cell Motil. 1991;12:161-170.
19. Goldspink G. Muscle energetics and animal locomotion. In: Alexander RM, Goldspink G, eds. Mechanics and Energetics of Animal Locomotion. London: Chapman and Hall, 1977:57-81.
20. Goldspink G. Malleability of the motor system: A comparative approach. J. Exp. Biol. 1985;115:375-391.
21. Goldspink G, Scutt A, Loughna P, Wells D, Jaenicke T, Gerlach GF. Gene expression in skeletal muscle in response to mechanical signals. Am. J. Physiol. 1992;262:R326-R363 .
22. Gondret F, Lefaucheur L, d'Albis A, Bonneau M. Myosin isoform transitions in four rabbit muscles during postnatal growth. J. Muscle Res. Cell Motil. 1996;17:657-667.
23. Harvey RJ, Vereugdenhil E, Zaman SE, Bhandal NS, Usherwood PNR, Barnard EA, Darlinson MG. Sequence of a functional invertebrate GABAA receptor subunit which can form a chimeric receptor with a vertebrate alpha subunit. EMBO J. 1991;10:3239-3254.
24. Jackson RL. Cytoplasmic regulation of mRNA function: The importance of the 3′ untranslated region. Cell 1993;74:9-14.
25. LaFramboise WA, Daood MJ, Guthrie RD, Schiaffino S, Moretti P, Brozanski B, Ontell MP, Butler-Brown GS, Whalen RG, Ontell M. Emergence of the mature myosin phenotype in the rat diaphragm muscle. Dev. Biol. 1991;144:1-15.
26. Larsson L, Moss RL. Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J. Physiol. 1993;472:595-614.
27. Leferovich JM, Rubinstein NA, Kelly AM. Expression of slow and fast myosin heavy chains in overloaded muscles of the developing rat. J. Muscle Res. Cell Motil. 1991;12:247-253.
28. Loughna PT, Izumo S, Goldspink G, Nadal-Ginard B. Disuse and passive stretch cause rapid alterations in expression of developmental and adult contractile protein genes in skeletal muscle. Development 1990;109:217-223.
29. Lyons GE, Ontell M, Cox R, Sasoon D, Buckingham M. The expression of myosin genes in developing skeletal muscle in the mouse embryo. J. Cell Biol. 1990;111:1465-1476.
30. Mahdavi V, Strehler E, Periasamy M, Wieczorek DF, Izumo S, Nadal-Gianrd B. Sacromeric myosin heavy chain gene family: Organisation and pattern of expression. Med. Sci. Sports Exerc. 1986;18:229-308.
31. Mahdavi V, Izumo S, Nadal-Gianrd B. Developmental and hormonal regulation of sacromeric myosin heavy chain gene family. Circ. Res. 1987;60:804-814.
32. Merati AL, Bodine SC, Bennett T, Hak-Hyun J, Hiroshi F, Ryan AF Identification of a novel myosin heavy chain gene expressed in the rat larynx. Biochim. Biophy. Acta 1996;1306:153-159.
33. Miller JB, Stockdale FE. Developmental origins of skeletal muscle fibres: Clonal analysis of myogenic cell lineages based on expression of fast and slow myosin heavy chain genes. Proc. Natl. Acad. Sci. USA 1986;83:3860-3864.
34. Molkentin JD, Olson EN Combinatorial control of muscle development by basic helix-loop-helix and MADS-box transcription factors. Proc. Natl. Acad. Sci. USA 1996;93:9366-9373.
35. Muntz L. Cellular and biochemical aspects of muscle differentiation. Comp. Biochem. Physiol. 1990;97B:215-225.
36. Parker-Thornburg J, Bauer B, Palermo J, Robbins J. Structural and developmental analysis of two linked myosin heavy chain genes. Dev. Biol. 1992;150:99-107.
37. Pette D, Vrbova G. Adaptation of mammalian skeletal muscle fibres to chronic electrical stimulation. Rev. Physiol. Biochem. Pharmacol. 1992;120:115-202.
38. Reiser PJ, Moss RL, Giulian GC, Greaser ML. Shortening velocity in single fibres from adult rabbit soleus muscle is correlated with and myosin heavy chain composition. J. Biol. Chem. 1985;260:9077-9080.
39. Reiser PJ, Greaser ML, Moss RL. Myosin heavy chain composition of single cells from avian slow skeletal muscle is strongly correlated with velocity of shortening during development. Dev. Biol. 1988;129: 400-407
40. Rome LC, Sosnicki AA, Goble DO. Maximum velocity of shortening of three fibre types from horse soleus muscle: Implications for scaling to body size. J. Physiol. 1990;431:173-185.
41. Russell B, Wenderoth MP, Goldspink PH. Remodelling of myofibrils: Subcellular distribution of myosin heavy chain mRNA and protein. Am. J. Physiol. 1992;262:R339-R345.
42. Russell SD, Cambon N, Nadal-Ginard B, Whalen RG. Thyroid hormone induces a nerve-independent precocious expression of fast myosin heavy chain mRNA in rat hindlimb skeletal muscle. J. Biol. Chem. 1988;263:6370-6374.
43. Russell SD, Cambon N, Whalen RG. Two types of neonatal-to-adult fast myosin heavy chain transitions in rat hindlimb muscle fibres. Dev. Biol. 1993;157:359-370.
44. Schiaffino S, Reggiani C. Molecular diversity of myofibrillar proteins: Gene regulation and functional significance. Physiol. Rev. 1996;76: 371-423.
45. Smerdu V, Karsch-Mizrachi I, Campione M, Leinwand L, Schiaffino S. Type IIx myosin heavy chain transcripts are expressed in type IIb fibres of human skeletal muscle. Am. J. Physiol. 1994;267:C1723-C1728.
46. Soussi-Yanicostas N, Whalen RG, Petit C. Five skeletal myosin heavy chain genes are organized as a multigene complex in the human genome. Hum. Mol. Genet. 1993;2:563-569
47. Staron RS, Johnson P. Mini review. Myosin polymorphism and differential expression in adult human skeletal muscle. Comp. Biochem. Physiol. 1993;106B:463-475.
48. Talmadge RJ, Roy RR. Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J. Appl. Physiol. 1993;75:2337-2340.
49. Thompson W. Synapse elimination in neonatal rat muscle is sensitive to pattern of muscle use. Nature 1983;302:614-686.
50. Van Essen DC, Gordon H, Soha JM, Fraser SE. Synaptic dynamics at the neuromuscular junction: Mechanisms and models. J. Neurobiol. 1990;21:223-249.
51. Vincent S, Marty L, Fort P. S26 ribosomal protein RNA: An invariant control for gene regulation experiments in eucaryotic cells and tissues. Nucleic. Acids Res. 1993;21:1498.
52. Weiss A, Leinwand LA. The mammalian myosin heavy chain gene family. Ann. Rev. Cell Dev. Biol. 1996;12:417-439.
53. Weydert A, Daubas P, Lazaridis I, Barton P, Garner I, Leader DP, Bonhomme F, Catalan J, Simon D, Guenet JL, Gros F, Buckingham ME. Gene for skeletal muscle myosin heavy chain are clustered and are not located on the same mouse chromosome as a cardiac myosin heavy chain gene. Proc. Natl. Acad. Sci. USA 1985;82:7183-7187.
54. Whalen RG. Myosin isoenzymes as molecular markers for muscle physiology. J. Exp. Biol. 1985;115:43-53.
55. Whalen RG, Sell SM, Butler-Browne GS, Schwartz K, Bouveret P, Pinset-Harstrom I. Three myosin heavy-chain isoenzymes appear sequentially in rat muscle development. Nature 1981;292:805-809.
56. Wydro RM, Nguyen HT, Gubits RM, Nadal-Ginard B. Characterisation of sacromeric myosin heavy chain genes. J. Biol. Chem. 1983;258:670-678.