Regionalized expression of myosin isoforms in heterotypic myotubes formed from embryonic and fetal rat myoblasts in vitro

Developmental Dynamics

Volumn 208, Issue 3, 1997, Pages 420-431

  Pin, Christopher L ^a,b   Merrifield, Peter A ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b PURDUE UNIVERSITY   (United States)

Author keywords

heterokaryons; myoblast differentiation; myoblast lineages; myogenesis; myosin heavy chain; nuclear domains

Indexed keywords

MYOSIN HEAVY CHAIN;

ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL SPECIFICITY; EMBRYO; EMBRYO DEVELOPMENT; FETUS; FETUS DEVELOPMENT; LIMB DEVELOPMENT; MUSCLE DEVELOPMENT; MUSCLE FIBRIL; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS REGULATION; RAT;

ANIMALS; BROMODEOXYURIDINE; CELL FUSION; CELL LINEAGE; CELL NUCLEUS; CELLS, CULTURED; COCULTURE TECHNIQUES; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; IMMUNOHISTOCHEMISTRY; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 0031042964     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0177(199703)208:3<420::AID-AJA12>3.0.CO;2-3     Document Type: Article

References (56)

1. Bouvagnet, P., Leger, J., Pons, F., Dechesne, C., and Leger, J.J. (1984) Fiber types and myosin types in human atrial and ventricular myocardium. Circ. Res. 55:794-804.
2. Brown, W.E., Salmons, S., and Whalens, R.G. (1983) The sequential replacement of myosin subunit isoforms during muscle type transformation induced by long term electrical stimulation. J. Biol. Chem. 258:14686-14692.
3. Buller, A.J., Eccles, J.C., and Eccles, R.M. (1960) Differentiation of fast and slow muscles in the cat hind limb. J. Physiol. 150:399-416.
4. Burke, R.E. (1986) Physiology of motor units. In: "Myology," Engel, A., and Banker, B.Q. (eds). New York: McGraw-Hill Book Company, Vol. 1, pp. 419-443.
5. Butler, J., and Cosmos, E. (1981) Enzymatic markers to identify muscle-nerve formation during embryogenesis: Modified myosin ATPase and silver-cholinesterase histochemical reactions. Exp. Neurol. 73:831-836.
6. Carraro, U., Catani, C., Belluco, S., Cantini, M., and Marchioro, L. (1986) Slow-like electrostimulation switches on slow myosin in denervated fast muscle. Exp. Neurol. 94:537-553.
7. Condon, K., Silberstein, L., Blau, H.M., and Thompson, W.J. (1990a) Differentiation of fiber types in aneural musculature of the prenatal hindlimb. Dev. Biol. 138:275-295.
8. Condon, K., Silberstein, L., Blau, H.M., and Thompson, W.J. (1990b) Development of muscle fiber type in the prenatal rat hindlimb. Dev. Biol. 138:256-274.
9. DeNardi, C., Ausoni, S., Moretti, P., Gorza, L., Velleca, M., Buckingham, M., and Schiaffino, S. (1993) Type 2× myosin heavy chain is coded by a muscle fiber type specific and developmentally regulated gene. J. Cell Biol. 123:823-835.
10. DiMario, J.X., and Stockdale, F.E. (1995) Differences in the developmental fate of cultured and noncultured myoblasts when transplanted into embryonic limbs. Exp. Cell Res. 216:431-442.
11. DiMario, J.X., Fernyak, S.E., and Stockdale. F.E. (1993) Myoblasts transferred to the limbs of embryos are committed to specific fibre fates. Nature 362:165-167.
12. Donoghue, M.J., and Sanes, J.R. (1994) All muscles are not created equal. Trends in Genetics 10:396-401.
13. Duxson, M. J., and Usson, Y.J. (1989) Cellular insertion of primary and secondary myotubes in embryonic rat muscles. Development 107: 243-251.
14. Duxson, M.J., Usson, Y., and Harris, A.J. (1989) The origin of secondary myotubes in mammalian skeletal muscles: ultrastructural studies. Development 107:743-750.
15. Edom, F., Mouly, V, Barbet, J.P., Fiszman, M.Y., and Butler-Browne, G.S. (1994) Clones of human satellite cells can express in vitro both fast and slow myosin heavy chains. Dev. Biol. 164:219-229.
16. Evans, D., Baillie, H., Caswell,A., and Wigmore, P. (1994) During fetal muscle development, clones of cells contribute to both primary and secondary fibers. Dev. Biol. 162:348-353.
17. Gauthier, G.F. (1986) Skeletal muscle fiber types. In: "Myology," Engel, A., and Banker, B.Q. (eds.) New York: McGraw-Hill Book Company, Vol. 1, pp. 255-283.
18. George-Weinstein, M., Foster, R.F., Gerhart, J.V., and Kaufman, S.J. (1993) In vitro and in vivo expression of α7 integrin and desmin define the primary and secondary myogenic lineages. Dev. Biol. 156:209-229.
19. Gorza, L. (1990) Identification of a novel type 2 fiber population in mammalian skeletal muscle by combined use of histochemical myosin ATPase and anti-myosin monoclonal antibodies. J. Histochem. Cytochem. 38:257-265.
20. Gorza, L., Gundersen, K., Lomo, T., Schiaffino, S., and Westgaard, R.H. (1988) Slow-to-fast transformation of denervated soleus muscles by chronic high-frequency stimulation in the rat. J. Physiol. 402:627-649.
21. Greishammer, U., McGrew, M.J., and Rosenthal, N. (1995) Role of methylation in maintanance of positionally restricted transgene expression in developing muscle. Development 121:2245-2253.
22. Harris, A.J., Duxson, M.J., Fitzsimons, R.B., and Rieger, F. (1989) Myonuclear birthdates distinguish the origin of primary and secondary myotubes in embryonic mammalian skeletal muscles. Development 107:771-784.
23. Hayashi, K., and Ozawa, E. (1991) Vital labelling of somite-derived myogenic cells in the chicken limb bud. Roux Arch. Dev. Biol. 200:188-192.
24. Horan, P.K., and Slezak, S.E. (1989) Stable cell membrane labelling. Nature 340:167-168.
25. Hsu, S.M., Raine, L., and Fanger, H. (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 29:577-580.
26. Hughes, S,M., and Blau, H.M. (1992) Muscle fiber pattern is independent of cell lineage in postnatal rodent development. Cell 68:659-671.
27. Hughes, S.M., Taylor, J.M., Tapscott, S.J., Gurley, C.M., Carter, W.J., and Peterson, C.P. (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.
28. Jolesz, F., and Sreter, F.A. (1981) Development, innervation, and activity-pattern induced changes in skeletal muscle. Annu. Rev. Physiol. 43:531-552.
29. Kalderon, N., and Gilula, N.B. (1979) Membrane events involved in myoblast fusion. J. Cell Biol. 81:411-425.
30. Kelly, A.M., and Zacks, S.I. (1969) The histogenesis of rat intercostal muscle. J. Cell Biol. 42:135-153.
31. Konigsberg, I.R. (1979) Skeletal myoblasts in culture. In: "Method in Enzymology," Jakoby, W., and Pastan, I. (eds) New York: Academic Press, pp. 511-527.
32. Laing, M.N., and Lamb, A.H. (1983) The distribution of muscle fibre types in chick embryo wings transplanted to the pelvic region is normal. J. Embryol. Exp. Morphol. 78:67-82.
33. Miller, S.C., Pavlath, G.K., Blakely, B.T., and Blau, H.M. (1988) Muscle cell components dicatate hepatocyte gene expression and the distribution of the golgi apparatus in heterokaryons. Genes Dev. 2:330-340.
34. Narusawa, M., Fitzsimons, R.B., Izumo, S., Nadal-Ginard, B., Rubinstein, N.A., and Kelly, A.M. (1987) Slow myosin in developing rat skeletal muscle. J. Cell Biol. 104:447-459.
35. Noursadeghi, M., Walsh, F.S., Heiman-Patterson, T., and Dickson, G. (1993) Trans-activation of the murine dystropin gene in human-mouse hybrid myotubes. FEBS Lett. 320:155-159.
36. Papadimitriou, J.M., Robertson, T.A., Mitchell, C.A., and Grounds, M.D. (1990) The process of new plasmalemma formation in focally injured skeletal muscle fibers. J. Struct. Biol. 103:124-134.
37. Pavlath, G.K., Rich, K., Webster, S.G., and Blau, H.M. (1989) Localization of muscle gene products in nuclear domains. Nature 337:570-573.
38. Pette, D., and Düsterhöft, S. (1992) Altered gene expression in fast-twitch muscle induced by chronic low-frequency stimulation. Am. J. Physiol. 262:R333-R338.
39. Pette, D., and Vrbova, G. (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev. Physiol. Biochem. Pharmacol. 120:115-202.
40. Pin, C.L., and Merrifield, P.A. (1993) Embryonic and fetal rat myoblasts express different phenotypes following differentiation in vitro. Dev. Genet. 14:356-368.
41. Ralston, E., and Hall, Z.W. (1989) Intracellular and surface distribution of a membrane protein (CD8) derived from a single nucleus in multinucleated myotubes. J. Cell Biol. 109:2345-2352.
42. Ross, J.J., Duxson, M.J., and Harris, A.J. (1987) Formation of primary and secondary myotubes in rat lumbrical muscles. Development 100:383-394.
43. Sheard, P.W., Duxson, M.J., and Harris, A.J. (1991) Neuromuscular transmission to identified primary and secondary myotubes: A reevaluation of polyneural innervation patterns in rat embryos. Dev. Biol. 148:459-472.
44. Smith, T.H., and Miller, J.B. (1992) Distinct myogenic programs of embryonic and fetal mouse myoblasts cells: Expression of the perinatal myosin heavy chain isoform in vitro. Dev. Biol. 149:16-26.
45. Stockdale, F.E. (1992) Myogenic cell lineages. Dev. Biol. 154:284-298.
46. Stockdale, F.E., and Miller, J.B. (1987) The cellular basis of myosin heavy chain isoform expression during development of avian skeletal muscles. Dev. Biol. 123:1-9.
47. Termin, A., Staron, R.S., and Pette, D. (1989) Changes in myosin heavy chain isoforms during chronic low-frequency stimulation of rat fast hindlimb muscles: A single-fiber study. Eur. J. Biochem. 186:749-754.
48. Thomas, P.E., and Ranatunga, K.W. (1993) Factors affecting muscle fiber transformation in cross-reinnervated muscle. Muscle Nerve 16:193-199.
49. Unguez, G.A., Roy, R.R., Pierotti, D.J., Bodine-Fowler, S., and Edgerton, V.R. (1995) Further evidence of incomplete neural control of muscle properties in cat tibialis anterior motor units. Am. J. Physiol. 37:C527-C534.
50. Van Swearingen, J., and Lance-Jones, C. (1995) Slow and fast muscle fibres are preferentially derived from myoblasts migrating into chick limb buds at different developmental times. Dev. Biol. 170:321-337.
51. Vivarelli, E., Brown, W.E., Whalen, R.G., and Cossu, G. (1988) The expression of slow myosin during mammalian somitogenesis and limb bud differentiation. J. Cell Biol. 107:2191-2197.
52. Voytik, S.L., Przyborski, M., Badylak, S.F., and Konieczny, S.F. (1994) Differential expression of muscle regulatory factor genes in normal and denervated adult rat hindlimb muscles. Dev. Dyn. 198:214-224.
53. Whalen, R.G., Harris, J.B., Butler-Browne, G.S., and Sesodia, S. (1990) Expression of myosin isoforms during notexin-induced regeneration of rat soleus muscles. Dev. Biol. 141:24-40.
54. Wilson, S.J., Ross, J.J., and Harris, A.J. (1988) A critical period for formation of secondary myotubes defined by prenatal undernourishment in rats. Development 102:815-821.
55. Yaffe, D., and Feldman, M. (1965) The formation of hybrid multinucleated muscle fibers from myoblasts of different genetic origin. Dev. Biol. 11:300-317.
56. Zhang, M. and McLennan, I.S. (1995) During secondary myotube formation, primary myotubes preferentially absorb new nuclei at their ends. Dev. Dyn. 204:168-177.