Thyroid hormone regulates muscle function during cold acclimation in zebrafish (Danio rerio)

Journal of Experimental Biology

Volumn 216, Issue 18, 2013, Pages 3514-3521

  Little, Alexander G ^a   Seebacher, Frank ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

3,5,3' triiodothyronine; 3,5 diiodothryronine; Myofibrillar ATPase; SERCA; Swimming performance; T 2; T3

Indexed keywords

LIOTHYRONINE; MESSENGER RNA; MUSCLE FIBRIL ADENOSINE TRIPHOSPHATASE; THYROID HORMONE;

3,5,3′-TRIIODOTHYRONINE, T3; 3,5-DIIODOTHRYRONINE, T2; ACCLIMATIZATION; ANIMAL; ARTICLE; COLD; DIET SUPPLEMENTATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HYPOTHYROIDISM; METABOLISM; MUSCLE; PATHOPHYSIOLOGY; PHYSIOLOGY; SERCA; SWIMMING PERFORMANCE; THYROID GLAND; ZEBRA FISH;

3,5,3′-TRIIODOTHYRONINE, T3; 3,5-DIIODOTHRYRONINE, T2; MYOFIBRILLAR ATPASE; SERCA; SWIMMING PERFORMANCE;

ACCLIMATIZATION; ANIMALS; COLD TEMPERATURE; DIETARY SUPPLEMENTS; GENE EXPRESSION REGULATION; HYPOTHYROIDISM; MUSCLES; RNA, MESSENGER; THYROID GLAND; THYROID HORMONES; TRIIODOTHYRONINE; ZEBRAFISH;

EID: 84883184603     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.089136     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. Arruda, A. P., Nigro, M., Oliveira, G. M. and de Meis, L. (2007). Thermogenic activity of Ca2+-ATPase from skeletal muscle heavy sarcoplasmic reticulum: the role of ryanodine Ca2+ channel. Biochim. Biophys. Acta 1768, 1498-1505.
3. Bal, N. C., Maurya, S. K., Sopariwala, D. H., Sahoo, S. K., Gupta, S. C., Shaikh, S. A., Pant, M., Rowland, L. A., Bombardier, E., Goonasekera, S. A. et al. (2012). Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals. Nat. Med. 18, 1575-1579.
4. Ball, D. and Johnston, I. A. (1996). Molecular mechanisms underlying the plasticity of muscle contractile properties with temperature acclimation in the marine fish Myoxocephalus scorpius. J. Exp. Biol. 199, 1363-1373.
5. Bicudo, J. E., Vianna, C. R. and Chaui-Berlinck, J. G. (2001). Thermogenesis in birds. Biosci. Rep. 21, 181-188.
6. Block, B. A. and Finnerty, J. R. (1994). Endothermy in fishes: a phylogenetic analysis of constraints, predispositions, and selection pressures. Environ. Biol. Fishes 40, 283-302.
7. Bouzaffour, M., Rampon, C., Ramaugé, M., Courtin, F. and Vriz, S. (2010). Implication of type 3 deiodinase induction in zebrafish fin regeneration. Gen. Comp. Endocrinol. 168, 88-94.
8. Brett, J. R. (1965). The relation of size to rate of oxygen consumption and sustained swimming speed of sockeye salmon (Oncorhynchus nerka). J. Fish. Res. Board Can. 22, 1491-1501.
9. Carr, A. N. and Kranias, E. G. (2002). Thyroid hormone regulation of calcium cycling proteins. Thyroid 12, 453-457.
10. Clausen, T., Van Hardeveld, C. and Everts, M. E. (1991). Significance of cation transport in control of energy metabolism and thermogenesis. Physiol. Rev. 71, 733-774.
11. Clobert, J., Oppliger, A., Sorci, G., Ernande, B., Swallow, J. G. and Garland, T. (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.
12. Cooke, R. (2011). The role of the myosin ATPase activity in adaptive thermogenesis by skeletal muscle. Biophys. Rev. 3, 33-45.
13. Deslauriers, D. and Kieffer, J. D. (2012). The effects of temperature on swimming performance of juvenile shortnose sturgeon (Acipenser brevirostrum). J. Appl. Ichthyol. 28, 176-181.
14. 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.
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.
16. Forini, F., Paolicchi, A., Pizzorusso, T., Ratto, G. M., Saviozzi, M., Vanini, V. and Iervasi, G. (2001). 3, 5, 3'-Triiodothyronine deprivation affects phenotype and intracellular [Ca2+]i of human cardiomyocytes in culture. Cardiovasc. Res. 51, 322-330.
17. Goglia, F. (2005). Biological effects of 3, 5-diiodothyronine (T2). Biochemistry (Moscow) 70, 164-172.
18. Guderley, H. (2004a). Locomotor performance and muscle metabolic capacities: impact of temperature and energetic status. Comp. Biochem. Physiol. 139B, 371-382.
19. Guderley, H. (2004b). Metabolic responses to low temperature in fish muscle. Biol. Rev. Camb. Philos. Soc. 79, 409-427.
20. Haldar, S. M., Jeyaraj, D., Anand, P., Zhu, H., Lu, Y., Prosdocimo, D. A., Eapen, B., Kawanami, D., Okutsu, M., Brotto, L. et al. (2012). Kruppel-like factor 15 regulates skeletal muscle lipid flux and exercise adaptation. Proc. Natl. Acad. Sci. USA 109, 6739-6744.
21. Heap, S. P., Watt, P. W. and Goldspink, G. (1985). Consequences of thermal change on the myofibrillar ATPase of five freshwater teleosts. J. Fish Biol. 26, 733-738.
22. Herrel, A. and Bonneaud, C. (2012). Temperature dependence of locomotor performance in the tropical clawed frog, Xenopus tropicalis. J. Exp. Biol. 215, 2465-2470.
23. Hulbert, A. J. (2000). Thyroid hormones and their effects: a new perspective. Biol. Rev. Camb. Philos. Soc. 75, 519-631.
24. Hulbert, A. J. and Else, P. L. (1981). Comparison of the 'mammal machine' and the 'reptile machine': energy use and thyroid activity. Am. J. Physiol. 241, R350-R356.
25. 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.
26. Husak, J. F., Fox, S. F. and Van Den Bussche, R. A. (2008). Faster male lizards are better defenders not sneakers. Anim. Behav. 75, 1725-1730.
27. Hwang, G. C., Watabe, S. and Hashimoto, K. (1990). Changes in carp myosin ATPase induced by temperature acclimation. J. Comp. Physiol. B 160, 233-239.
28. Iordanidou, A., Hadzopoulou-Cladaras, M. and Lazou, A. (2010). Non-genomic effects of thyroid hormone in adult cardiac myocytes: relevance to gene expression and cell growth. Mol. Cell. Biochem. 340, 291-300.
29. Izumo, S., Nadal-Ginard, B. and Mahdavi, V. (1986). All members of the MHC multigene family respond to thyroid hormone in a highly tissue-specific manner. Science 231, 597-600.
30. James, R. S., Walter, I. and Seebacher, F. (2011). Variation in expression of calciumhandling proteins is associated with inter-individual differences in mechanical performance of rat (Rattus norvegicus) skeletal muscle. J. Exp. Biol. 214, 3542-3548.
31. James, R. S., Tallis, J., Herrel, A. and Bonneaud, C. (2012). Warmer is better: thermal sensitivity of both maximal and sustained power output in the iliotibialis muscle isolated from adult Xenopus tropicalis. J. Exp. Biol. 215, 552-558.
32. Johnson, T. and Bennett, A. (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.
33. Johnson, K. M. and Lema, S. C. (2011). Tissue-specific thyroid hormone regulation of gene transcripts encoding iodothyronine deiodinases and thyroid hormone receptors in striped parrotfish (Scarus iseri). Gen. Comp. Endocrinol. 172, 505-517.
34. Johnston, I. A. and Ball, D. (1997). Thermal stress and muscle function in fish. In Global Warming: Implications for Freshwater and Marine Fish (Society for Experimental Biology Seminar Series 61) (ed. C. M. Wood and D. G. McDonald), pp. 70-104. Cambridge: Cambridge University Press.
35. 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.
36. Johnston, I. A., Davison, W. and Goldspink, G. (1975). Adaptations in Mg2+- activated myofibrillar ATPase activity induced by temperature acclimation. FEBS Lett. 50, 293-295.
37. Kahaly, G. J. and Dillmann, W. H. (2005). Thyroid hormone action in the heart. Endocr. Rev. 26, 704-728.
38. Ketzer, L. A., Arruda, A. P., Carvalho, D. P. and de Meis, L. (2009). Cardiac sarcoplasmic reticulum Ca2+-ATPase: heat production and phospholamban alterations promoted by cold exposure and thyroid hormone. Am. J. Physiol. 297, H556-H563.
39. Little, A. G., Lougheed, S. C. and Moyes, C. D. (2010). Evolutionary affinity of billfishes (Xiphiidae and Istiophoridae) and flatfishes (Plueronectiformes): Independent and trans-subordinal origins of endothermy in teleost fishes. Mol. Phylogenet. Evol. 56, 897-904.
40. Little, A. G., Kunisue, T., Kannan, K. and Seebacher, F. (2013). Thyroid hormone actions are temperature-specific and regulate thermal acclimation in zebrafish (Danio rerio). BMC Biol. 11, 26.
41. McCurley, A. T. and Callard, G. V. (2008). Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol. Biol. 9, 102.
42. Morrissette, J. M., Franck, J. P. and Block, B. A. (2003). Characterization of ryanodine receptor and Ca2+-ATPase isoforms in the thermogenic heater organ of blue marlin (Makaira nigricans). J. Exp. Biol. 206, 805-812.
43. Nelson, E. R. and Habibi, H. R. (2009). Thyroid receptor subtypes: structure and function in fish. Gen. Comp. Endocrinol. 161, 90-96.
44. Norris, D. O. (2007). Vertebrate Endocrinology. Amsterdam: Elsevier Academic Press.
45. O'Brien, K. M. (2011). Mitochondrial biogenesis in cold-bodied fishes. J. Exp. Biol. 214, 275-285.
46. Pei, L., Leblanc, M., Barish, G., Atkins, A., Nofsinger, R., Whyte, J., Gold, D., He, M., Kawamura, K., Li, H. R. et al. (2011). Thyroid hormone receptor repression is linked to type I pneumocyte-associated respiratory distress syndrome. Nat. Med. 17, 1466-1472.
47. Prezant, D. J., Richner, B., Valentine, D. E., Aldrich, T. K., Fishman, C. L., Nagashima, H., Chaudhry, I. and Cahill, J. (1990). Temperature dependence of rat diaphragm muscle contractility and fatigue. J. Appl. Physiol. 69, 1740-1745.
48. Purcell, T. J., Naber, N., Franks-Skiba, K., Dunn, A. R., Eldred, C. C., Berger, C. L., Málnási-Csizmadia, A., Spudich, J. A., Swank, D. M., Pate, E. et al. (2011). Nucleotide pocket thermodynamics measured by EPR reveal how energy partitioning relates myosin speed to efficiency. J. Mol. Biol. 407, 79-91.
49. Sänger, A. M. (1993). Limits to the acclimation of fish muscle. Rev. Fish Biol. Fish. 3, 1-15.
50. Schiaffino, S. and Reggiani, C. (2011). Fiber types in mammalian skeletal muscles. Physiol. Rev. 91, 1447-1531.
51. Seebacher, F. and Franklin, C. E. (2011). Physiology of invasion: cane toads are constrained by thermal effects on physiological mechanisms that support locomotor performance. J. Exp. Biol. 214, 1437-1444.
52. Seebacher, F. and James, R. S. (2008). Plasticity of muscle function in a thermoregulating ectotherm (Crocodylus porosus): biomechanics and metabolism. Am. J. Physiol. 294, R1024-R1032.
53. 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.
54. 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.
55. Seebacher, F., Pollard, S. R. and James, R. S. (2012). How well do muscle biomechanics predict whole-animal locomotor performance? The role of Ca2+ handling. J. Exp. Biol. 215, 1847-1853.
56. Simonides, W. S. and van Hardeveld, C. (2008). Thyroid hormone as a determinant of metabolic and contractile phenotype of skeletal muscle. Thyroid 18, 205-216.
57. Simonides, W. S., Thelen, M. H., van der Linden, C. G., Muller, A. and van Hardeveld, C. (2001). Mechanism of thyroid-hormone regulated expression of the SERCA genes in skeletal muscle: implications for thermogenesis. Biosci. Rep. 21, 139-154.
58. Somero, G. N. (1995). Proteins and temperature. Annu. Rev. Physiol. 57, 43-68.
59. Tata, J. R. (2011). Looking for the mechanism of action of thyroid hormone. J. Thyroid Res. 2011, 730630.
60. Tullis, A. and Block, B. A. (1996). Expression of sarcoplasmic reticulum Ca2+-ATPase isoforms in marlin and swordfish muscle and heater cells. Am. J. Physiol. 271, R262-R275.
61. Walter, I. and Seebacher, F. (2009). Endothermy in birds: underlying molecular mechanisms. J. Exp. Biol. 212, 2328-2336.
62. Wang, Y. G., Dedkova, E. N., Fiening, J. P., Ojamaa, K., Blatter, L. A. and Lipsius, S. L. (2003). Acute exposure to thyroid hormone increases Na+ current and intracellular Ca2+ in cat atrial myocytes. J. Physiol. 546, 491-499.
63. Weiss, A. and Leinwand, L. A. (1996). The mammalian myosin heavy chain gene family. Annu. Rev. Cell Dev. Biol. 12, 417-439.
64. Woytanowski, J. R. and Coughlin, D. J. (2013). Thermal acclimation in rainbow smelt, Osmerus mordax, leads to faster myotomal muscle contractile properties and improved swimming performance. Biol. Open 2, 343-350.