Differences in locomotor performance between individuals: Importance of parvalbumin, calcium handling and metabolism

Journal of Experimental Biology

Volumn 215, Issue 4, 2012, Pages 663-670

  Seebacher, Frank ^a   Walter, Isabel ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

Author keywords

Dihydropyridine receptor; Electroporation; Gene expression; Ryanodine receptor; SERCA; Sprint performance; Sustained locomotion

Indexed keywords

CALCIUM; CALCIUM CHANNEL L TYPE; CARRIER PROTEIN; CREATINE KINASE; MESSENGER RNA; PARVALBUMIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR COACTIVATOR 1BETA, ZEBRAFISH; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR COACTIVATOR-1BETA, ZEBRAFISH; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA, ZEBRAFISH; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR-1ALPHA, ZEBRAFISH; RYANODINE RECEPTOR; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; TRANSCRIPTION FACTOR; ZEBRAFISH PROTEIN;

ANIMAL; ARTICLE; BIOSYNTHESIS; ELECTROPORATION; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE; SWIMMING; ZEBRA FISH;

ANIMALS; CALCIUM; CALCIUM CHANNELS, L-TYPE; CARRIER PROTEINS; CREATINE KINASE; ELECTROPORATION; ENERGY METABOLISM; GENE EXPRESSION REGULATION; MUSCLE, SKELETAL; PARVALBUMINS; PPAR DELTA; RNA, MESSENGER; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SWIMMING; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

ANIMALIA; DANIO RERIO;

EID: 84856514977     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.066712     Document Type: Article

References (76)

1. Anttila, K., Mänttäri, S. and Järvilehto, M. (2006). Effects of different training protocols on Ca2+ handling and oxidative capacity in skeletal muslce of Antlantic salmon (Salmo salar L.). J. Exp. Biol. 209, 2971-2978. (Pubitemid 44342575)
2. Anttila, K., Mänttäri, S. and Järvilehto, M. (2007). Expression of dihydropyridine and ryanodine receptors in type IIA fibres of rat skeletal muscle. Acta Histochem. Cytochem. 40, 35-41. (Pubitemid 46743500)
3. Anttila, K., Järvilehto, M. and Mänttäri, S. (2008). The swimming performance of brown trout and whitefish: The effects of exercise on Ca2+ handling and oxidative capacity of swimming muscles. J. Comp. Physiol. B 178, 465-475. (Pubitemid 351550305)
4. Arif, S. H. (2008). A Ca2+-binding protein with numerous roles and uses: Parvalbumin in molecular biology and physiology. BioEssays 31, 410-421.
5. Arnold, S. J. (1983). Morphology, performance and fitness. Amer. Zool. 23, 347-361.
6. Bauwens, D., Garland, T., Jr, Castilla, A. M. and Van Damme, R. (1995). Evolution of sprint speed in lacertid lizards: Morphological, physiological and behavioural covariation. Evolution 49, 848-863. (Pubitemid 3002807)
7. Bellinger, A. M., Reiken, S., Dura, M., Murphy, P. W., Deng, S.-X., Landry, D. W., Nieman, D., Lehnart, S. E., Samaru, M., LaCampagne, A. et al. (2008). Remodeling of ryanodine receptor complex causes ?leaky' channels: A molecular mechanism for decreased exercise capacity. Proc. Natl. Acad. Sci. USA 105, 2198-2202. (Pubitemid 351439488)
8. Berchtold, M. W., Brinkmeier, H. and Münterer, M. (2000). Calcium ion in skeletal muscle: Its crucial role for muscle function, plasticity, and disease. Physiol. Rev. 80, 1215-1265. (Pubitemid 30452014)
9. Brett, J. R. (1964). The respiratory metabolism and swimming performance of young sockeye salmon. J. Fish Res. Board Can. 21, 1183-1226.
10. Brownridge, P., Vieira de Mello, L., Peters, M., McLean, L., Claydon, A., Cossins, A. R., Whitfield, P. D. and Young, I. S. (2009). Regional variation in parvalbumin isoform expression correlates with muscle performance in common carp (Cyprinus carpio). J. Exp. Biol. 212, 184-193.
11. Burgomaster, K. A., Howarth, K. R., Phillips, S. M., Rakobowchuk, M., MacDonald, M. J., McGee, S. L. and Gibala, M. J. (2008). Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J. Physiol. 586, 151-160.
12. Cano, J. M. and Nicieza, A. G. (2006). Temperature, metabolic rate, and constraints on locomotor performance in ectotherm vertebrates. Funct. Ecol. 20, 464-470. (Pubitemid 43882827)
13. Chinsomboon, J., Ruas, J., Gupta, R. K., Thom, R., Shoag, J., Rowe, G. C., Sawada, N., Raghuram, S. and Arany, Z. (2009). The transcrioptional coactivator PGC-1a mediates exercise-induced angiogenesis in skeletal muscle. Proc. Natl. Acad. Sci. USA 106, 21401-21406.
14. Clobert, J., Opplinger, A., Sorci, G., Ernande, B., Swallow, J. G. and Garland, T., Jr (2000). Trade-offs in phenotypic traits: Endurance at birth, growth, survival, predation and susceptibility to parasitism in a lizard, Lacerta vivipara. Funct. Ecol. 14, 675-684. (Pubitemid 32044991)
15. Constantin, D., Constantin-Teodosiu, D., Layfield, R., Tsintzas, K., Bennett, A. J. and Greenhaff, P. L. (2007). PPARdelta agonism induces a change in fuel metabolism and activation of an atrophy programme, but does not impair mitochondrial function in rat skeletal muscle. J. Physiol. 583, 381-390. (Pubitemid 47248448)
16. Constantin-Teodosiu, D., Baker, D. J., Constantin, D. and Greenhaff, P. L. (2009). PPARd agonism inhibits skeletal muscle PDC activity, mitochondrial ATP production and force generation during prolonged contraction. J. Physiol. 587, 231-239.
17. Dirkson, R. T. (2009). Checking your SOCCs and feet: The molecular mechanisms of Ca2+ entry in skeletal muscle. J. Physiol. 587, 3139-3147.
18. East, J. M. (2000). Sarco(endo)plasmic reticulum calcium pumps: Recent advances in our understanding of structure/function and biology. Mol. Membr. Biol. 17, 189-200. (Pubitemid 32267316)
19. Eliason, E. J., Clark, T. D., Hague, M. J., Hanson, L. M., Gallagher, Z. S., Jeffries, K. M., Gale, M. K., Patterson, D. A., Hinch, S. G. and Farrell, A. P. (2011). Differences in thermal tolerance among sockeye salmon populations. Science 332, 109-112.
20. 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. 140, 179-185. (Pubitemid 40312822)
21. Farah, C. S. and Reinach, F. C. (1995). The troponin complex and regulation of muscle contraction. FASEB J. 9, 755-767.
22. Fleckenstein, A. (1983). History of calcium antagonists. Circ. Res. 52 Suppl., 3-16.
23. Friedberg, F. (2005). Parvalbumin isoforms in zebrafish. Mol. Biol. Rep. 32, 167-175. (Pubitemid 41374358)
24. Garenc, C., Silversides, F. G. and Guderley, H. (1998). Burst swimming and its enzymatic correlates in the threespine stickleback (Gasterosteus aculeatus): Full-sib heritabilities. Can. J. Zool. 76, 680-688.
25. Garland, T., Jr and Else, P. L. (1987). Seasonal, sexual, and individual variation in endurance and activity metabolism in lizards. Am. J. Physiol. Regul. Integr. Comp. Physiol. 252, R439-R449.
26. Gibb, A. C. and Dickson, K. A. (2002). Functional morphology and biochemical indices of performance: Is there a correlation between metabolic enzyme activity and swimming performance? Integr. Comp. Biol. 42, 199-207.
27. Guderley, H. (2004). Metabolic responses to low temperature in fish muscle. Biol. Rev. 79, 409-427. (Pubitemid 38685147)
28. Gustavsson, M., Traaseth, N. J., Karim, C. B., Lockamy, E. L., Thomas, D. D. and Veglia, G. (2011). Lipid-mediated folding/unfolding of phospholamban as a regulatory mechanism for sarcoplasmic reticulum Ca2+-ATPase. J. Mol. Biol. 408, 755-765.
29. Hirata, H., Watanabe, T., Hatakeyama, J., Sprague, S. M., Saint-Amant, L., Nagashima, A., Cui, W. W., Zhou, W. and Kuwada, J. Y. (2007). Zebrafish relatively relaxed mutants have a ryanodine receptor defect, show slow swimming and provide a model of multi-minicore disease. Development 134, 2771-2781. (Pubitemid 47305052)
30. Hou, T. T., Johnson, J. D. and Rall, J. A. (1991). Parvalbumin content and Ca2+ and Mg2+ dissociation rates correlated with changes in relaxation rate of frog muscle fibres. J. Physiol. 441, 285-304.
31. Husak, J. H., Fox, S. F., Lovern, M. B. and Van Den Bussche, R. A. (2006). Faster lizards sire more offspring: Sexual selection on whole-animal performance. Evolution 60, 2122-2130. (Pubitemid 44808221)
32. Ingham, P. W. (2009). The power of the zebrafish for disease analysis. Human Mol. Genet. 18, R107-R112.
33. Irschick, D. J. and Losos, J. B. (1998). A comparative analysis of the ecological significance of maximal locomotor performance in Caribbean anolis lizards. Evolution 52, 219-226. (Pubitemid 28195161)
34. James, R. S., Altringham, J. D. and Goldspink, D. F. (1995). The mechanical properties of fast and slow skeletal muscles of the mouse in relation to their locomotory function. J. Exp. Biol. 198, 491-502.
35. James, R. S., Wilson, R. S., De Carvalho, J. E., Kohlsdorf, T., Gomes, F. R. and Navas, C. A. (2005). Interindividual differences in leg muscle mass and pyruvate kinase activity correlate with interindividual differences in jumping performance of Hyla multilineata. Physiol. Biochem. Zool. 78, 857-867. (Pubitemid 41292290)
36. James, R. S., Walter, I. and Seebacher, F. (2011). Variation in expression of calcium handling proteins is associated with inter-individual differences in mechanical performance of rat (Rattus norvegicus) skeletal muscle. J. Exp. Biol. 214, 3542-3548.
37. Johnston, I. A. and Temple, G. K. (2002). Thermal plasticity of skeletal muscle phenotype in ectothermic vertebrates and its significance for locomotory behaviour. J. Exp. Biol. 205, 2305-2322.
38. Johnston, I. A. and Walesby, N. J. (1977). Molecular mechanisms of temperature adaptation in fish myofibrillar adenosine triphosphatases. J. Comp. Physiol. 119, 195-206.
39. Joyner, M. J. and Coyle, E. F. (2008). Endurance exercise performance: The physiology of champions. J. Physiol. 586, 35-44.
40. Kretsinger, R. H. (1980). Structure and evolution of calcium-modulated proteins. Crit. Rev. Biochem. 8, 119-174.
41. Lalli, M. J., Yong, J., Prasad, V., Hashimoto, K., Plank, D., Babu, G. J., Kirkpatrick, D., Walsh, R. A., Sussman, M., Yatani, A. et al. (2001). Sarcoplasmic reticulum Ca2+ ATPase (SERCA) 1a structurally substitutes for SERCA2a in the cardiac sarcoplasmic reticulum and increases cardiac Ca2+ handling capacity. Circ. Res. 89, 160-167. (Pubitemid 34135824)
42. Lande, R. and Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution 37, 1210-1226.
43. Langerhans, R. B. and Reznick, D. N. (2008). Ecology and evolution of swimming performance in fishes: Predicting evolution with biomechanics. In Fish Locomotion: An Eco Ethological Perspective (ed. P. Domenici and B. G. Kapoor), pp. 200-248. Enfield: Science Publishers.
44. Lauder, G. V. (2005). Locomotion. In The Physiology of Fishes (ed. D. H. Evans and J. B. Claiborne), pp. 3-46. Boca Raton: CRC Press.
45. Le Galliard, J.-F., Clobert, J. and Ferriére, R. (2004). Physical performance and darwinian fitness in lizards. Nature 432, 502-505. (Pubitemid 39576530)
46. Lelliott, C. J., Medina-Gomez, G., Petrovic, N., Kis, A., Feldmann, H. M., Bjursell, M., Parker, N., Curtis, K., Campbell, M., Hu, P. et al. (2006). Ablation of PGC-1b results in defective mitochondrial activity, thermogenesis, hepatic function, and cardiac performance. PLoS Biol. 4, e369.
47. LeMoine, C. M. R., Lougheed, S. C. and Moyes, C. D. (2010). Molecular evolution of PGC-1a in vertebrates. J. Mol. Evol. 70, 492-505.
48. Lin, J., Wu, H., Tarr, P. T., Zhang, C.-Y., Wu, Z., Boss, O., Michael, L. F., Puigserver, P., Isotani, E., Olson, E. N. et al. (2002a). Transcriptional co-activator PGC-1a drives the formation of slow-twitch muscle fibres. Nature 418, 797-801.
49. Lin, J., Puigserver, P., Donovan, J., Tarr, P. and Spiegelman, B. M. (2002b). Peroxisome proliferator-activated receptor g coactivator 1b (PGC-1b), a novel PGC- 1-related transcription coactivator associated with host cell factor. J. Biol. Chem. 277, 1645-1648. (Pubitemid 34968733)
50. Müntener, M., Käser, 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.
51. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
52. Plomgaard, P., Penkowa, M., Leick, L., Pedersen, B. K., Saltin, B. and Pilegaard, H. (2006). The mRNA expression profile of metabolic genes relative to MHC isoform pattern in human skeletal muscles. J. Appl. Physiol. 101, 817-825. (Pubitemid 44352295)
53. Rambabu, K. M., Rao, S. H. N. and Rao, N. M. (2005). Efficient expression of transgenes in adult zebrafish by electroporation. BMC Biotechnol. 5, 29.
54. Rodgers, J. T., Lerin, C., Gerhart-Hines, Z. and Puigserver, P. (2008). Metabolic adaptations through the PGC-1a and SIRT1 pathways. FEBS Lett. 582, 46-53. (Pubitemid 350297246)
55. Rosenberg, P. B. (2009). Calcium entry in skeletal muscle. J. Physiol. 587, 3149-3151.
56. Saks, V. (2008). The phosphocreatine-creatine kinase system helps to shape muscle cells and keep them healthy and alive. J. Physiol. 586, 2817-2818. (Pubitemid 351837275)
57. Sandri, M., Lin, J., Handschirm, C., Yang, W., Arany, Z. P., Lecker, S. H., Goldberg, A. L. and Spiegelman, B. M. (2006). PGC-1a protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc. Natl. Acad. Sci. USA 103, 16260-16265. (Pubitemid 44715184)
58. Scarpulla, R. C. (2008). Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol. Rev. 88, 611-638. (Pubitemid 351520089)
59. Schoenman, E. R., Chiaro, J. A., Jones, A., Bastin, L. D. and Coughlin, D. J. (2010). A comparative analysis of parvalbumin expression in pinfish (Lagodon rhomboides) and toadfish (Opsanus sp.). Comp. Biochem. Physiol. 156A, 91-99.
60. Seebacher, F. and Glanville, E. J. (2010). Low levels of physical activity increase metabolic responsiveness to cold in a rat (Rattus fuscipes). PLoS ONE 5, e13022.
61. Seebacher, F., Guderley, H., Elsey, R. M. and Trosclair, P. L., III. (2003). Seasonal acclimatisation of muscle metabolic enzymes in a reptile (Alligator mississippiensis). J. Exp. Biol. 206, 1193-1200. (Pubitemid 36409161)
62. Seebacher, F., Brand, M. D., Else, P. L., Guderley, H., Hulbert, A. J. and Moyes, C. D. (2010). Plasticity of oxidative metabolism in variable climates: Molecular mechanisms. Physiol. Biochem. Zool. 83, 721-732.
63. Sinclair, E. L. E., Ward, A. J. W. and Seebacher, F. (2011). Aggression-induced fin damage modulates trade-offs in burst and endurance swimming performance of mosquitofish. J. Zool. 283, 243-248.
64. Steinhausen, M. F., Sandblom, E., Eliason, E. J., Verhille, C. and Farrell, A. P. (2008). The effect of acute temperature increases on the cardiorespiratory performance of resting and swimming sockeye salmon (Oncorhynchus nerka). J. Exp. Biol. 211, 3915-3926.
65. Van Damme, R., Wilson, R. S., Vanhooydonck, B. and Aerts, P. (2002). Performance constraints in decathletes. Nature 415, 755-756.
66. Vanhooydonck, B., Van Damme, R. and Aerts, P. (2001). Speed and stamina tradeoff in lacertid lizards. Evolution 55, 1040-1048. (Pubitemid 32550571)
67. van Winkle, W. B. (1974). Calcium release from skeletal muscle sarcoplasmic reticulum: Site of action of dantrolene sodium? Science 193, 1130-1131.
68. Verboomen, H., Wuytack, F., De Smedt, H., Himpens, B. and Casteels, R. (1992). Functional differences between SERCA2a and SERCA2b Ca2+ pumps and their modulation by phospholamban. Biochem. J. 286, 591-596.
69. Walter, I. and Seebacher, F. (2007). Molecular mechanisms underlying the development of endothermy in birds (Gallus gallus): A new role of PGC-1a? Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R2315-R2322. (Pubitemid 350224025)
70. Walter, I. and Seebacher, F. (2009). Endothermy in birds: Underlying molecular mechanisms. J. Exp. Biol. 212, 2328-2336.
71. Webb, P. W. and Weihs, D. (1983). Fish Biomechanics. New York: Praeger Publishers.
72. Weigl, L. G., Hohenegger, M., Kress, H. G. (2000). Dihydropyridine- induced Ca2+ release from ryanodine-sensitive Ca2+ pools in human skeletal muscle cells. J. Physiol. 525, 461-469. (Pubitemid 30398374)
73. Wilson, R. S. and James, R. S. (2004). Constraints on muscular performance: Tradeoffs between power output and fatigue resistance. Proc. R. Soc. Lond. B 271 Suppl., S222-S225. (Pubitemid 38586399)
74. Wilson, R. S., Condon, C. H., David, G., FitzGibbon, S., Niehaus, A. C. and Pratt, K. (2010). Females prefer athletes, males fear the disadvantaged: Different signals used in female choice and male competition have varied consequences. Proc. R. Soc. Lond. B 277, 1923-1928.
75. 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, 227-237. (Pubitemid 43226746)
76. Zaykin, D. V., Zhivotovsky, L. A., Westfall, P. H. and Weir, B. S. (2002). Truncated product method for combining p-values. Genet. Epidemiol. 22, 170-185. (Pubitemid 34081490)