Regional variation in parvalbumin isoform expression correlates with muscle performance in common carp (Cyprinus carpio)

Journal of Experimental Biology

Volumn 212, Issue 2, 2009, Pages 184-193

  Brownridge, Philip ^a   De Mello, Luciane Vieira ^a   Peters, Mary ^a   McLean, Lynn ^a   Claydon, Amy ^a   Cossins, Andrew R ^a   Whitfield, Phillip D ^a   Young, Iain S ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Activation; Isometric force; Muscle; Parvalbumin; Proteomics; Relaxation; Swimming

Indexed keywords

ISOPROTEIN; PARVALBUMIN;

ANIMAL; ARTICLE; BIOMECHANICS; CARP; CHEMISTRY; FAST MUSCLE FIBER; GENE EXPRESSION PROFILING; GENETICS; HISTOLOGY; METABOLISM; PHYSIOLOGY;

ANIMALS; BIOMECHANICS; CARPS; GENE EXPRESSION PROFILING; MUSCLE FIBERS, FAST-TWITCH; PARVALBUMINS; PROTEIN ISOFORMS;

CYPRINIDAE; CYPRINUS CARPIO;

EID: 58149358980     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.021857     Document Type: Article

References (53)

1. Altringham, J. D. and Ellerby, D. J. (1999). Fish swimming: patterns in muscle function. J. Exp. Biol. 202, 3397-3403.
2. Altringham, J. D., Wardle, C. S. and Smith, C. I. (1993). Myotomal muscle function at different locations in the body of a swimming fish. J. Exp. Biol. 182, 191-206.
3. 2+ binding and diffusion, during activation of frog skeletal muscle. J. Gen. Physiol. 112, 297-316.
4. Benzonan, G., Capony, J. P. and Pechere, J. F. (1972). Binding of calcium to muscular parvalbumins. Biochim. Biophys. Acta 278, 110-116.
5. Beynon, R. J. (2005). A simple tool for drawing proteolytic peptide maps. Bioinformatics 21, 674-675.
6. Bland, J. M. and Altman, D. G. (1995). Statistics notes: multiple significance tests: the Bonferroni method. Br. Med. J. 310, 170.
7. Bottinelli, R., Schiaffino, S. and Reggiani, C. (1991). Force-velocity relations and myosin heavy-chain isoform compositions of skinned fibers from Rat Skeletal-Muscle. J. Physiol. (Lond.) 437, 655-672.
8. Brandts, J. F., Brennan, M. and Lin, L. N. (1977). Unfolding and refolding occur much faster for a proline-free protein than for most proline-containing proteins. Proc. Natl. Acad. Sci. USA 74, 4178-4181.
9. Candiano, G., Bruschi, M., Musante, L., Santucci, L., Ghiggeri, G. M., Carnemolla, B., Orecchia, P., Zardi, L. and Righetti, P. G. (2004). Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25, 1327-1333.
10. Carver, T. and Bleasby, A. (2003). The design of Jemboss: a graphical user interface to EMBOSS. Bioinformatics 19, 1837-1843.
11. Celio, M. R. and Heizmann, C. W. (1982). Calcium-binding protein parvalbumin is associated with fast contracting muscle-fibers. Nature 297, 504-506.
12. Clamp, M., Cuff, J., Searle, S. M. and Barton, G. J. (2004). The Jalview Java alignment editor. Bioinformatics 20, 426-427.
13. Clark, M. S., Edwards, Y. J. K., Peterson, D., Clifton, S. W., Thompson, A. J., Sasaki, M., Suzuki, Y., Kikuchi, K., Watabe, S., Kawakami, K. et al. (2003). Fugu ESTs: new resources for transcription analysis and genome annotation. Genome Res. 13, 2747-2753.
14. Coffee, C. J. and Bradshaw, R. A. (1973). Carp muscle calcium-binding protein.1. characterization of tryptic peptides and complete amino-acid sequence of component-B. J. Biol. Chem. 248, 3305-3312.
15. Coffee, C. J., Bradshaw, R. A. and Kretsinger, R. H. (1974). The coordination of calcium ions by carp muscle calcium binding proteins A, B and C. Adv. Exp. Med. Biol. 48, 211-233.
16. Coughlin, D. J., Solomon, S. and Wilwert, J. L. (2007). Parvalbumin expression in trout swimming muscle correlates with relaxation rate. Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 147, 1074-1082.
17. Davies, M. L. F., Johnston, I. A. and Vandewal, J. (1995). Muscle-fibers in rostral and caudal myotomes of the atlantic cod (Gadus-morhua L) have different mechanical-properties. Physiol. Zool. 68, 673-697.
18. Ellerby, D. J. and Altringham, J. D. (2001). Spatial variation in fast muscle function of the rainbow trout Oncorhynchus mykiss during fast-starts and sprinting. J. Exp. Biol. 204, 2239-2250.
19. Erickson, J. R., Sidell, B. D. and Moerland, T. S. (2005). Temperature sensitivity of calcium binding for parvalbumins from Antarctic and temperate zone teleost fishes. Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 140, 179-185.
20. Felsenstein, J. (1989). PHYLIP-Phylogeny Inference Package (Version 3.2). Cladistics 5, 164-166.
21. Friedberg, F. (2005). Parvalbumin isoforms in zebrafish. Mol. Biol. Rep. 32, 167-175.
22. Gracey, A. Y., Fraser, E. J., Li, W. Z., Fang, Y. X., Taylor, R. R., Rogers, J., Brass, A. and Cossins, A. R. (2004). Coping with cold: an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc. Natl. Acad. Sci. USA 101, 16970-16975.
23. Grzyb, K. and Skorkowski, E. F. (2005). Characterization of creatine kinase isoforms in herring (Clupea harengus) skeletal muscle. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 140, 629-634.
24. Henzl, M. T., Agah, S. and Larson, J. D. (2004). Rat alpha- and beta-parvalbumins: comparison of their pentacarboxylate and site-interconversion variants. Biochemistry 43, 9307-9319.
25. Hsiao, C. D., Tsai, W. Y. and Tsai, H. J. (2002). Isolation and expression of two zebrafish homologues of parvalbumin genes related to chicken CPV3 and mammalian oncomodulin. Mech. Dev. 119, S161-S166.
26. Huriaux, F., Collin, S., Vandewalle, P., Philippart, J. C. and Focant, B. (1997). Characterization of parvalbumin isotypes in white muscle from the barbel and expression during development. J. Fish Biol. 50, 821-836.
27. Iio, T. and Hoshihara, Y. (1984). Static and kinetic-studies on carp muscle parvalbumins. J. Biochem. 96, 321-328.
28. 2+-ATPase is inhibited. Am. J. Physiol., Cell Physiol. 39, C411-C417.
29. 2+] on tension generation in fibers of skinned frog skeletal-muscle and mechanically disrupted rat ventricular cardiac-muscle. Pflugers Arch. 358, 195-201.
30. Klug, G. A., Leberer, E., Leisner, E., Simoneau, J. A. and Pette, D. (1988). Relationship between parvalbumin content and the speed of relaxation in chronically stimulated rabbit fast-twitch muscle. Pflugers Arch. 411, 126-131.
31. Kumar, V. D., Lee, L. and Edwards, B. F. P. (1990). Refined crystal-structure of calcium-liganded carp parvalbumin 4.25 at 1.5-Å resolution. Biochemistry 29, 1404-1412.
32. Lannergren, J., Elzinga, G. and Stienen, G. J. M. (1993). Force relaxation, labile heat and parvalbumin content of skeletal-muscle fibers of Xenopus-laevis. J. Physiol. (Lond.) 463, 123-140.
33. Mclean, L., Young, I. S., Doherty, M. K., Robertson, D. H. L., Cossins, A. R., Gracey, A. Y., Beynon, R. J. and Whitfield, P. D. (2007). Global cooling: cold acclimation and the expression of soluble proteins in carp skeletal muscle. Proteomics 7, 2667-2681.
34. Moeschler, H. J., Schaer, J. J. and Cox, J. A. (1980). A thermodynamic analysis of the binding of calcium and magnesium-ions to parvalbumin. Eur. J. Biochem. 111, 73-78.
35. Muntener, M., Kaser, L., Weber, J. and Berchtold, M. W. (1995). Increase of skeletal-muscle relaxation speed by direct-injection of parvalbumin cDNA. Proc. Natl. Acad. Sci. USA 92, 6504-6508.
36. 2+-specific site. Eur. J. Biochem. 242, 249-255.
37. Pechere, J. F., Demaille, J. and Capony, J. P. (1971). Muscular parvalbumins-preparative and analytical methods of general applicability. Biochim. Biophys. Acta 236, 391-408.
38. Perkins, D. N., Pappin, D. J. C., Creasy, D. M. and Cottrell, J. S. (1999). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567.
39. Permyakov, E. A., Medvedkin, V. N., Mitin, Y. V. and Kretsinger, R. H. (1991). Noncovalent complex between domain AB and domains CD*EF of parvalbumin. Biochim. Biophys. Acta 1076, 67-70.
40. Rasband, W. S. (1997-2007). ImageJ. http://rsb.info.nih.gov/ij/.
41. Rodnick, K. J. and Sidell, B. D. (1995). Effects of body-size and thermal-acclimation on parvalbumin concentration in white muscle of striped bass. J. Exp. Zool. 272, 266-274.
42. Rome, L. C., Syme, D. A., Hollingworth, S., Lindstedt, S. L. and Baylor, S. M. (1996). The whistle and the rattle: the design of sound producing muscles. Proc. Natl. Acad. Sci. USA 93, 8095-8100.
43. Schwaller, B., Dick, J., Dhoot, G., Carroll, S., Vrbova, G., Nicotera, P., Pette, D., Wyss, A., Bluethmann, H., Hunziker, W. et al. (1999). Prolonged contraction-relaxation cycle of fast-twitch muscles in parvalbumin knockout mice. Am. J. Physiol., Cell Physiol. 276, C395-C403.
44. Swank, D. M., Zhang, G. X. and Rome, L. C. (1997). Contraction kinetics of red muscle in scup: Mechanism for variation in relaxation rate along the length of the fish. J. Exp. Biol. 200, 1297-1307.
45. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). Clustal-W-improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
46. Thys, T. M., Blank, J. M. and Schachat, F. H. (1998). Rostral-caudal variation in troponin T and parvalbumin correlates with differences in relaxation rates of cod axial muscle. J. Exp. Biol. 201, 2993-3001.
47. Thys, T. M., Blank, J. M., Coughlin, D. J. and Schachat, F. (2001). Longitudinal variation in muscle protein expression and contraction kinetics of largemouth bass axial muscle. J. Exp. Biol. 204, 4249-4257.
48. Verrez-Bagnis, V., Ladrat, C., Morzel, M., Noel, J. and Fleurence, J. (2001). Protein changes in post mortem sea bass (Dicentrarchus labrax) muscle monitored by one-and two-dimensional gel electrophoresis. Electrophoresis 22, 1539-1544.
49. Vornanen, M., Tiitu, V., Kakela, R. and Aho, E. (1999). Effects of thermal acclimation on the relaxation system of crucian carp white myotomal muscle. J. Exp. Zool. 284, 241-251.
50. Wardle, C. S., Videler, J. J., Arimoto, T., Franco, J. M. and He, P. (1989). The muscle twitch and the maximum swimming speed of giant bluefin tuna, Thunnusthynnus. J. Fish Biol. 35, 129-137.
51. Wilwert, J. L., Madhoun, N. M. and Coughlin, D. J. (2006). Parvalbumin correlates with relaxation rate in the swimming muscle of sheepshead and kingfish. J. Exp. Biol. 209 (2), 227-237.
52. Winnard, P., Cashon, R. E., Sidell, B. D. and Vayda, M. E. (2003). Isolation, characterization and nucleotide sequence of the muscle isoforms of creatine kinase from the Antarctic teleost Chaenocephalus aceratus. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 134, 651-667.
53. Wnuk, W., Cox, J. A. and Stein, E. A. (1982). Parvalbumins and other soluble high-affinity calcium-binding proteins from muscle In Calcium and Cell Function, vol. 2 (ed. W. Y. Cheung), pp. 243-278. New York: Academic Press.