Fiber polymorphism in skeletal muscles of the American lobster, Homarus americanus: Continuum between slow-twitch (S1) and slow-tonic (S 2) fibers

Journal of Experimental Biology

Volumn 207, Issue 16, 2004, Pages 2755-2767

  Medler, Scott ^a   Lilley, Travis ^a   Mykles, Donald L ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Actin; Arthropoda; Crustacea; Homarus americanus; Isoform; Lobster; Myosin heavy chain; Skeletal muscle

Indexed keywords

COMPLEMENTARY DNA; MESSENGER RNA; MYOSIN HEAVY CHAIN; PRIMER DNA; TROPOMYOSIN;

AMINO ACID SEQUENCE; ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; COMPARATIVE STUDY; CYTOLOGY; DNA SEQUENCE; GENETICS; HISTOLOGY; METABOLISM; MOLECULAR GENETICS; MUSCLE CELL; MUSCLE FIBRIL; NEPHROPIDAE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SKELETAL MUSCLE;

AMINO ACID SEQUENCE; ANALYSIS OF VARIANCE; ANIMALS; BASE SEQUENCE; DNA PRIMERS; DNA, COMPLEMENTARY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MOLECULAR SEQUENCE DATA; MUSCLE FIBERS; MUSCLE, SKELETAL; MYOFIBRILS; MYOSIN HEAVY CHAINS; NEPHROPIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TROPOMYOSIN;

ANIMALIA; ARTHROPODA; CRUSTACEA; HOMARUS; HOMARUS AMERICANUS; INVERTEBRATA; LOBSTER; NEPHROPIDAE;

EID: 4344632209     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.01094     Document Type: Article

References (60)

1. Ahn, A. N., Monti, R. J. and Biewener, A. A. (2003). In vivo and in vitro heterogeneity of segment length changes in the semimembranosus muscle of the toad. J. Physiol. 549, 877-888.
2. Allen, D. L., Roy, R. R. and Edgerton, V. R. (1999). Myonuclear domains in muscle adaptation and disease. Muscle Nerve 22, 1350-1360.
3. Ariano, M. A., Armstrong, R. B. and Edgerton, V. R. (1973). Hindlimb muscle fiber populations of five mammals. J. Histochem. Cytochem. 21, 51-55.
4. Atwood, H. L. (1976). Organization and synaptic physiology of crustacean neuromuscular systems. Prog. Neurobiol. 7, 291-391.
5. Bandman, E. and Rosser, B. W. C. (2000). Evolutionary significance of myosin heavy chain heterogeneity in birds. Microsc. Res. Tech. 50, 473-491.
6. Barnard, J., Edgerton, V. R., Furukawa, T. and Peter, J. B. (1971). Histochemical, biochemical, and contractile properties of red, white, and intermediate fibers. Am. J. Physiol. 220, 410-414.
7. Basi, G. S., Boardman, M. and Storti, R. V. (1984). Alternative splicing of a Drosophila tropomyosin gene generates muscle tropomyosin isoforms with different carboxy-terminal ends. Mol. Cell. Biol. 4, 2828-2836.
8. Blough, E. R., Rennie, E. R., Zhang, F. and Reiser, P. J. (1996). Enhanced electrophoretic separation and resolution of myosin heavy chains in mammalian and avian skeletal muscles. Anal. Biochem. 233, 31-35.
9. Bolster, D. R., Kimball, S. R. and Jefferson, L. S. (2003). Translational control mechanisms modulate skeletal muscle gene expression during hypertrophy. Exerc. Sort Sci. Rev. 31, 111-116.
10. Bottinelli, R. (2001). Functional heterogeneity of mammalian single muscle fibres: do myosin isoforms tell the whole story? Pflügers Arch. 443, 6-17.
11. Brooke, M. H. and Kaiser, K. K. (1970). Muscle fiber types: how many and what kind? Arch. Neurol. 23, 369-379.
12. Caiozzo, V. J. (2002). Plasticity of skeletal muscle phenotype: mechanical consequences. Muscle Nerve 26, 740-768.
13. Caiozzo, V. J., Baker, M. J., Huang, K., Chou, H., Wu, Y. Z. and Baldwin, K. M. (2003). Single-fiber myosin heavy chain polymorphism: how many patterns and what proportions? Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R570-R580.
14. Cho, Y. J. and Hitchcock-DeGregori, S. E. (1991). Relationship between alternatively spliced exons and functional domains of tropomyosin. Proc. Natl. Acad. Sci. USA 88, 10153-10157.
15. Clark, K. A., McElninny, A. S., Beckerle, M. C. and Gregorio, C. C. (2002). Striated muscle cytoarchitecture: an intricate web of form and function. Annu. Rev. Cell Dev. Biol. 18, 637-706.
16. Cotton, J. L. S. and Mykles, D. L. (1993). Cloning of a crustacean myosin heavy chain isoform: exclusive expression in fast muscle. J. Exp. Zool. 267, 578-586.
17. Covi, J. A., Belote, J. M. and Mykles, D. L. (1999). Subunit compositions and catalytic properties of proteasomes from developmental temperature- sensitive mutants of Drosophila melanogaster. Arch. Biochem. Biophys. 368, 85-97.
18. Edman, E. A. P., Reggiani, C. and teKronnie, G. (1985). Differences in maximum velocity of shortening along single muscle fibres of the frog. J. Physiol. 365, 147-163.
19. 2+-sensitivity and twitch contraction kinetics in dragonfly flight muscle. J. Exp. Biol. 200, 1473-1482.
20. Fowler, W. S. and Neil, D. M. (1992). Histochemical heterogeneity of fibers in the abdominal superficial flexor muscles of the Norway lobster, Nephrops norvegicus (L.). J. Exp. Zool. 264, 406-418.
21. Holmes, J. M., Hilber, K., Galler, S. and Neil, D. M. (1999). Shortening properties of two biochemically defined muscle fibre types of the Norway lobster, Nephrops norvegicus L. J. Muscle Res. Cell Motil. 20, 265-278.
22. Jahromi, S. S. and Atwood, H. L. (1969). Correlation of structure, speed of contraction, and total tension in fast and slow abdominal muscle fibers of the lobster (Homarus americanus). J. Exp. Zool. 171, 25-38.
23. Jahromi, S. S. and Atwood, H. L. (1971). Structural and contractile properties of lobster leg-muscle fibers. J. Exp. Zool. 176, 475-486.
24. Jefferson, L. S. and Kimball, S. R. (2001). Translational control of protein synthesis: Implications for understanding changes in skeletal muscle mass. Int. J. Sport Nut. Exerc Metab. 11, S143-S149.
25. LaFramboise, W. A., Griffis, B., Bonner, P., Warren, W., Scalise, D., Guthrie, R. D. and Cooper, R. L. (2000). Muscle type-specific myosin isoforms in crustacean muscles. J. Exp. Zool. 286, 36-48.
26. Li, X. and Wang, X. (2000). Application of real-time polymerase chain reaction for the quantitation of interleukin-1β mRNA upregulation in brain ischemic tolerance. Brain Res. Protocols 5, 211-217.
27. Lutz, G. J., Cuizon, D. B., Ryan, A. F. and Lieber, R. L. (1998). Four novel myosin heavy chain transcripts define a molecular basic for muscle fibre types in Rana pipiens. J. Physiol. 508, 667-680.
28. Lutz, G. J., Bremner, S. N., Bade, M. J. and Lieber, R. L. (2001). Identification of myosin light chains in Rana pipiens skeletal muscle and their expression patterns along single fibers. J. Exp. Biol. 204, 4237-4248.
29. Marden, J. H., Fitzhugh, G. H., Wolf, M. R., Arnold, K. D. and Rowan, B. (1999). Alternative splicing, muscle calcium sensitivity, and the modulation of dragonfly flight performance. Proc. Natl. Acad. Sci. USA 96, 15304-15309.
30. 2+-sensitivity and the force and power output of dragonfly flight muscles during oscillatory contraction. J. Exp. Biol. 204, 3457-3470.
31. Medler, S. and Mykles, D. L. (2003). Analysis of myofibrillar proteins and transcripts in adult skeletal muscles of the American lobster Homarus americanus: variable expression of myosins, actin and troponins in fast, slow-twitch and slow-tonic fibres. J. Exp. Biol. 206, 3557-3567.
32. Mykles, D. L. (1985a). Heterogeneity of myofibrillar proteins in lobster fast and slow muscles: variants of troponin, paramyosin, and myosin light chains comprise four distinct protein assemblages. J. Exp. Zool. 234, 23-32.
33. Mykles, D. L. (1985b). Multiple variants of myofibrillar proteins in single fibers of lobster claw muscles: evidence for two types of slow fibers in the cutter closer muscle. Biol. Bull. 169, 476-483.
34. Mykles, D. L. (1988). Histochemical and biochemical characterization of two slow fiber types in decapod crustacean muscles. J. Exp. Zool. 245, 232-243.
35. Mykles, D. L. (1997). Crustacean muscle plasticity: molecular mechanisms determining mass and contractile properties. Comp. Biochem. Physiol. B 117, 367-378.
36. Mykles, D. L., Cotton, J. L. S., Taniguchi, H., Sano, K. I. and Maeda, Y. (1998). Cloning of tropomyosins from lobster (Homarus americanus) striated muscles: fast and slow isoforms may be generated from the same transcript. J. Muscle Res. Cell. Mot. 19, 105-115.
37. Mykles, D. L., Medler, S., Koenders, A. and Cooper, R. L. (2002). Myofibrillar protein isoform expression is correlated with synaptic efficacy in slow fibres of the claw and leg opener muscles of crayfish and lobster. J. Exp. Biol. 205, 513-522.
38. Neil, D. M., Fowler, W. S. and Tobasnik, G. (1993). Myofibrillar protein composition correlates with histochemistry in fibres of the abdominal flexor muscles of the Norway lobster. J. Exp. Biol. 183, 185-201.
39. Neter, J., Wasserman, W. and Kutner, M. H. (1990). Applied Linear Statistical Models: Regression, Analysis of Variance, and Experimental Designs. 3rd edition. Boston: Irwin.
40. Newlands, S. L., Levitt, L. K., Robinson, C. S., Karpf, A. B. C., Hodgson, V. R. H., Wade, R. P. and Hardeman, E. C. (1998). Transcription occurs in pulses in muscle fibers. Genes Dev. 12, 2748-2758.
41. 2+-stimulated activity in single fibres of toad rectus abdominus muscle. J. Muscle Res. Cell. Motil. 23, 147-156.
42. Ogonowski, M. M. and Lang, F. (1979). Histochemical evidence for enzyme differences in crustacean fast and slow muscle. J. Exp. Zool. 207, 143-151.
43. Perry, S. V. (2001). Vertebrate tropomyosin: distribution, properties and function. J. Muscle Res. Cell. Motil. 22, 5-49.
44. Peter, J. B., Barnard, R. J., Edgerton, V. R., Gillespie, C. A. and Stempel, K. E. (1972). Metabolic profiles of three fiber types of skeletal muscle in guinea pigs and rabbits. Biochemistry 11, 2627-2633.
45. Pette, D. (2001). Plasticity in skeletal, cardiac, and smooth muscle - historical perspective: plasticity of mammalian skeletal muscle. J. Appl. Physiol. 90, 1119-1124.
46. Pette, D. and Staron, R. S. (2000). Myosin isoforms, muscle fiber types, and transitions. Microsc. Res. Tech. 50, 500-509.
47. Pette, D., Peuker, H. and Staron, R. S. (1999). The impact of biochemical methods for single muscle fibre analysis. Acta. Physiol. Scand. 166, 261-277.
48. Peuker, H. and Pette, D. (1997). Quantitative analysis of myosin heavy-chain mRNA and protein isoforms in single fibers reveal a pronounced fiber heterogeneity in normal rabbit muscles. Eur. J. Biochem. 247, 30-36.
49. Rome, L. C., Funke R. P., Alexander, R. M., Lutz, G. J., Aldridge, F. S. and Freadman, M. (1988). Why animals have different muscle fibre types. Nature 355, 824-827.
50. Rome, L. C. and Lindstedt, S. L. (1997). Mechanical and metabolic design of the muscular system in vertebrates. In Comparative Physiology (ed. W. H. Dantzler), pp. 1587-1651. New York: Oxford University Press.
51. Schiaffino, S. and Reggiani, C. (1996). Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol. Rev. 76, 371-423.
52. Silverman, H., Costello, W. J. and Mykles, D. L. (1987). Morphological fiber type correlates of physiological and biochemical properties in crustacean muscle. Am. Zool. 27, 1011-1019.
53. Sohn, J., Mykles, D. L. and Cooper, R. L. (2000). Characterization of muscles associated with the articular membrane in the dorsal surface of the crayfish abdomen. J. Exp. Zool. 287, 353-377.
54. Stephenson, G. M. M. (2001). Hybrid skeletal muscle fibres: a rare or common phenomenon? Clin. Exp. Pharmacol. Physiol. 28, 692-702.
55. Stevens, L., Gohlsch, B., Mounier, Y. and Pette, D. (1999). Changes in myosin heavy chain mRNA and protein isoforms in single fibers of unloaded rat soleus muscle. FEBS Lett. 463, 15-18.
56. Sweeney, H. L., Feng, H. S., Yang, Z. and Watkins, H. (1998). Functional analyses of troponin T mutations that cause hypertrophic cardiomyopathy: insights into disease pathogenesis and troponin function. Proc. Natl. Acad. Sci. USA 95, 14406-14410.
57. Talmadge, R. J. and Roy, R. R. (1993). Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J. Appl. Physiol. 75, 2337-2340.
58. West, J. M. (1997). Ultrastructural and contractile activation properties of crustacean muscle fibers over the moult cycle. Comp. Biochem. Physiol. B 117, 333-345.
59. Wray, W., Boulikas, T., Wray, V. P. and Hancock, R. (1981). Silver staining of proteins in polyacrylamide gels. Anal. Biochem. 118, 197-203.
60. Yu, X. L. and Mykles, D. L. (2003). Cloning of a muscle-specific calpain from the American lobster, Homarus americanus: expression associated with muscle atrophy and restoration during moulting. J. Exp. Biol. 206, 561-575.