How well do muscle biomechanics predict whole-animal locomotor performance? The role of Ca2+ handling

Journal of Experimental Biology

Volumn 215, Issue 11, 2012, Pages 1847-1853

  Seebacher, Frank ^a   Pollard, Samuel R ^b   James, Rob S ^b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b Institute for Clean Growth and Future Mobility   (United Kingdom)

Author keywords

Dihydropyridine receptor; Fatigue resistance; Ryanodine receptor; SERCA; Sprint performance; Swimming kinematics

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; NIFEDIPINE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; THAPSIGARGIN;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIOMECHANICS; CALCIUM SIGNALING; CARP; DRUG ANTAGONISM; DRUG EFFECT; IN VITRO STUDY; LOCOMOTION; MUSCLE CONTRACTION; MUSCLE FATIGUE; PHYSIOLOGY; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE; SWIMMING;

ANIMALS; BIOMECHANICS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CARPS; LOCOMOTION; MODELS, BIOLOGICAL; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE, SKELETAL; NIFEDIPINE; SARCOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SWIMMING; THAPSIGARGIN;

ANIMALIA; CYPRINIDAE; CYPRINUS CARPIO;

EID: 84861651044     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.067918     Document Type: Article

References (64)

1. Allen, D. G., Lamb, G. D. and Westerblad, H. (2008). Skeletal muscle fatigue: cellular mechanisms Physiol. Rev. 88, 287-332.
2. 2+ handling and oxidative capacity in skeletal muscle of Atlantic salmon (Salmo salar L.). J. Exp. Biol. 209, 2971-2978. (Pubitemid 44342575)
3. Antilla, K., Mänttäri, S. and Järvilehto, M. (2007). Expression of dihyrdopyridine and ryanodine receptors in type IIA fibres of rat skeletal muscle. Acta Histochem. Cytochem. 40, 35-41. (Pubitemid 46743500)
4. 2+-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. Am. Zool. 23, 347-361.
6. 2+ entry. J. Gen. Physiol. 133, 79-91.
7. Bennett, A. F. (1991). The evolution of activity capacity. J. Exp. Biol. 160, 1-23.
8. Berchtold, M. W., Brinkmeier, H. and Müntener, 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. Claireaux, G. and Lefrançois, C. (2007). Linking environmental variability and fish performance: integration through the concept of scope for activity. Phil. Trans. R. Soc. B 362, 2031-2041. (Pubitemid 350058107)
11. Dickinson, M. H., Farley, C. T., Full, R. J., Koehl, M. A. R., Kram, R. and Lehman, S. (2000). How animals move: an integrative view. Science 288, 100-106. (Pubitemid 30203037)
12. 2+ entry in skeletal muscle. J. Physiol. 587, 3139-3147.
13. Dykes, M. H. M. (1975). Evaluation of a muscle relaxant: dantrolene sodium (dantrium). JAMA 231, 862-864.
14. Fleckenstein, A. (1983). History of calcium antagonists. Circ. Res. 52(Suppl. 1), 3-16.
15. Fleming, J. R., Crockford, T., Altringham, J. D. and Johnston, I. A. (1990). effects of temperature acclimation on muscle relaxation in the carp: a mechanical, biochemical, and ultrastructural study. J. Exp. Zool. 255, 286-295. (Pubitemid 20305907)
16. Foster, T. S., Hamann, S. R., Richards, V. R., Bryant, P. J., Graves, D. A. and McAllister, R. G. (1983). Nifedipine kinetics and bioavailability after single intravenous and oral doses in normal subjects. J. Clin. Pharmacol. 23, 161-170. (Pubitemid 13131441)
17. 2+ release by direct and specific action at skeletal muscle ryanodine receptors. J. Biol. Chem. 272, 26965-26971. (Pubitemid 27452649)
18. Galli, G. L. J., Taylor, E. W. and Shiels, H. A. (2006). Calcium flux in turtle ventricular myocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291, R1781-R1789. (Pubitemid 44904147)
19. Garland, T., Jr, Hankins, E. and Huey, R. B. (1990). Locomotor capacity and social dominance in male lizards. Funct. Ecol. 4, 243-250. (Pubitemid 20428306)
20. 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.
21. Glanville, E. J. and Seebacher, F. (2006). Compensation for environmental change by complementary shifts of thermal sensitivity and thermoregulatory behaviour in an ectotherm. J. Exp. Biol. 209, 4869-4877. (Pubitemid 46166714)
22. Hammer, C. (1995). Fatigue and exercise tests with fish. Comp. Biochem. Physiol. 112 A, 1-20.
23. Heap, S. P. and Goldspinck, G. (1986). Alterations to the swimming performance of carp, Cyprinus carpio, as a result of temperature acclimation. J. Fish Biol. 29, 747-753.
24. 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 ryanodine receptor defect, show slow swimming and provide a model of multi-minicore disease. Development 134, 2771-2781. (Pubitemid 47305052)
25. Houston, M. C. (1986). Treatment of hypertensive urgencies and emergencies with nifedipine. Am. Heart J. 111, 963-969. (Pubitemid 16092962)
26. Husak, J. F., 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)
27. Irschick, D. J. and Garland, T., Jr (2001). Integrating function and ecology in studies of adaptation: investigations of locomotor capacity as a model system. Annu. Rev. Ecol. Syst. 32, 367-396. (Pubitemid 34043166)
28. Irschick, D. J., Meyers, J. J., Husak, J. F. and LeGalliard, J.-F. (2008). How does selection operate on whole-organism functional capacities? A review and synthesis. Evol. Ecol. Res. 10, 177-196. (Pubitemid 351501876)
29. James, R. S., Navas, C. A. and Herrel, A. (2007). How important are skeletal muscle mechanics in setting limits on jumping performance? J. Exp. Biol. 210, 923-933. (Pubitemid 46650596)
30. 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.
31. Johnson, T. P. and Bennett, A. F. (1995). The thermal acclimation of burst escape performance in fish: an integrated study of molecular and cellular physiology and organismal performance. J. Exp. Biol. 198, 2165-2175.
32. 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.
33. Johnston, I. A., Sidell, B. D. and Driedzig, W. R. (1985). Force-velocity characteristics and metabolism of carp muscle fibres following temperature acclimation. J. Exp. Biol. 119, 239-249. (Pubitemid 16185498)
34. Joyner, M. J. and Coyle, E. F. (2008). Endurance exercise performance: the physiology of champions. J. Physiol. 586, 35-44.
35. Krause, T., Gerbershagen, M. U., Fiege, M., Weisshorn, R. and Wappler, F. (2004). Dantrolene-a review of its pharmacology, therapeutic use and new developments. Anaesthesia 59, 364-373. (Pubitemid 38489297)
36. 2+ entry into mouse skeletal muscle fibres. J. Physiol. 533, 185-199. (Pubitemid 32499371)
37. Lande, R. and Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution 37, 1210-1226.
38. Langerhans, R. B. (2009). Morphology, performance, fitness: functional insights into a post-Pleistocene radiation of mosquitofish. Biol. Lett. 5, 488-491.
39. Lee, Y. S., Ondrias, K., Duhl, A. J., Ehrlich, B. E. and Kim, D. H. (1991). Comparison of calcium release from sarcoplasmic reticulum of slow and fast twitch muscles. J. Membrane Biol. 122, 155-163.
40. Le Galliard, J.-F., Clobert, J. and Ferriere, R. (2004). Physical performance and darwinian fitness in lizards. Nature 432, 502-505. (Pubitemid 39576530)
41. 2+ release channels and their regulation by endogenous effectors. Annu. Rev. Physiol. 56, 485-508.
42. Nakai, J., Dirksen, R. T., Nguyen, H. T., Pessah, I. N., Beam, K. G. and Allen, P. D. (1996). Enhanced dihydropyridine receptor channel activity in the presence of ryanodine receptor. Nature 380, 72-75. (Pubitemid 26076239)
43. Pan, Z., Yang, D., Nagaraj, R. Y., Nosek, T. A., Nishi, M., Takeshima, H., Cheng, H. and Ma, J. (2002). Dysfunction of store-operated calcium channel in muscle cells lacking mg29. Nat. Cell Biol. 4, 379-383. (Pubitemid 34521034)
44. Perry, G. (1999). The evolution of search modes: ecological versus phylogenetic perspectives. Am. Nat. 153, 98-109. (Pubitemid 29284827)
45. Seebacher, F. and Walter, I. (2012). Differences in locomotor performance between individuals: importance of parvalbumin, calcium handling, and metabolism. J. Exp. Biol. 215, 663-670.
46. Shiels, H. A., Freund, E. V., Farrell, A. P. and Block, B. A. (1999). The sarcoplasmic reticulum plays a major role in isometric contraction in atrial muscle of yellowfin tuna. J. Exp. Biol. 202, 881-890. (Pubitemid 29194832)
47. 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.
48. Sjåland, C., Lunde, P. K., Swift, F., Munkvik, M., Ericsson, M., Lunde, M., Boye, S., Christensen, G., Ellingsen, O., Sejersted, O. M. et al. (2011). Slowed relaxation and preserved maximal force in soleus muscles of mice with targeted disruption of the Serca2 gene in skeletal muscle. J. Physiol. 589, 6139-6155.
49. Spierts, I. L. Y. and Van Leeuwen, J. L. (1999). Kinematics and muscle dynamics of C-and S-starts of carp (Cyprinus carpio L.). J. Exp. Biol. 202, 393-406. (Pubitemid 29120430)
50. 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.
51. Stephenson, D. G., Lamb, G. D. and Stephenson, G. M. M. (1998). Events of the excitation-contraction-relaxation (E-C-R) cycle in fast-and slow-twitch mammalian muscle fibres relevant to muscle fatigue. Acta Physiol. Scand. 162, 229-245. (Pubitemid 28121401)
52. Syme, D. A. and Tonks, D. M. (2004). Fatigue and recovery dynamic and steady-state performance in frog skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286, R916-R926. (Pubitemid 38506839)
53. Tiitu, V. and Vornanen, M. (2003). Ryanodine and dihydropyridine receptor binding in ventricular cardiac muscle of fish with different temperature preferences. J. Comp. Physiol. B 173, 285-291. (Pubitemid 36832226)
54. Van Damme, R., Wilson, R. S., Vanhooydonck, B. and Aerts, P. (2002). Evolutionary biology: performance constraints in decathletes. Nature 415, 755-756. (Pubitemid 34150490)
55. Vanhooydonck, B., Van Damme, R. and Aerts, P. (2001). Speed and stamina trade-off in lacertid lizards. Evolution 55, 1040-1048. (Pubitemid 32550571)
56. Van Winkle, W. B. (1976). Calcium release from skeletal muscle sarcoplasmic reticulum: site of action of dantrolene sodium? Science 193, 1130-1131.
57. Vornanen, M. (1997). Sarcolemmal Ca influx through L-type Ca channels in ventricular myocytes of a teleost fish. Am. J. Physiol. Regul. Integr. Comp. Physiol. 272, R1432-R1440.
58. Wakeling, J. M., Cole, N. J., Kemp, K. M. and Johnston, I. A. (2000). The biomechanics and evolutionary significance of thermal acclimation in the common carp Cyprinus carpio. Am. J. Physiol. 279, R657-R665.
59. Walker, J. A., Ghalambor, C., Griset, O., McKenney, D. and Reznick, D. N. (2005). Do faster starts increase the probability of evading predators? Funct. Ecol. 19, 808-815. (Pubitemid 44933505)
60. Wardle, C. S. (1975). Limit of fish swimming speed. Nature 255, 725-727.
61. 2+ pools in human skeletal muscle cells. J. Physiol. 525, 461-469. (Pubitemid 30398374)
62. Wilson, R. S., James, R. S., Bywater, C. and Seebacher, F. (2009). Costs and benefits of increased weapon size differ between sexes of the slender crayfish, Cherax dispar. J. Exp. Biol. 212, 853-858.
63. 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.
64. 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)