Acute heat tolerance of cardiac excitation in the brown trout (Salmo trutta fario)

Journal of Experimental Biology

Volumn 217, Issue 2, 2014, Pages 299-309

  Vornanen, Matti ^a   Haverinen, Jaakko ^a   Egginton, Stuart ^b  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Action potential; Electrocardiogram; Fish heart; High temperature tolerance; Ion current

Indexed keywords

ACTION POTENTIAL; ELECTROCARDIOGRAM; FISH HEART; HIGH TEMPERATURE TOLERANCE; ION CURRENT;

ACCLIMATIZATION; ACTION POTENTIALS; ANIMALS; CALCIUM; HEART; HOT TEMPERATURE; POTASSIUM; SODIUM; TROUT;

EID: 84893363259     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.091272     Document Type: Article

References (54)

1. Aho, E. and Vornanen, M. (2001). Cold acclimation increases basal heart rate but decreases its thermal tolerance in rainbow trout (Oncorhynchus mykiss). J. Comp. Physiol. B 171, 173-179.
2. Altimiras, J., Axelsson, M., Claireaux, G., Lefrancois, C., Mercier, C. and Farrell, A. P. (2002). Cardiorespiratory status of triploid brown trout during swimming at two acclimation temperatures. J. Fish Biol. 60, 102-116.
3. Beitinger, T. L. and Bennett, W. A. (2000). Quantification of the role of acclimation temperature in temperature tolerance of fishes. Environ. Biol. Fishes 58, 277-288.
4. Bennett, W. A. and Beitinger, T. L. (1997). Temperature tolerance of the sheepshead minnow Cyprinodon variegatus. Copeia 1997, 77-87.
5. Bezanilla, F. (2005). Voltage-gated ion channels. IEEE Trans. Nanobioscience 4, 34- 48.
6. Campbell, H. A., Taylor, E. W. and Egginton, S. (2004). The use of power spectral analysis to determine cardiorespiratory control in the short-horned sculpin Myoxocephalus scorpius. J. Exp. Biol. 207, 1969-1976.
7. Campbell, H. A., Klepacki, J. Z. and Egginton, S. (2006). A new method in applying power spectral statistics to examine cardio-respiratory interactions in fish. J. Theor. Biol. 241, 410-419.
8. Collins, C. A. and Rojas, E. (1982). Temperature dependence of the sodium channel gating kinetics in the node of Ranvier. Q. J. Exp. Physiol. 67, 41-55.
9. Cossins, A. R. and Prosser, C. L. (1978). Evolutionary adaptation of membranes to temperature. Proc. Natl. Acad. Sci. USA 75, 2040-2043.
10. Derangeon, M., Montnach, J., Baró, I. and Charpentier, F. (2012). Mouse models of SCN5A-related cardiac arrhythmias. Front. Physiol. 3, 210.
11. Elliott, J. M. and Elliott, J. A. (2010). Temperature requirements of Atlantic salmon Salmo salar, brown trout Salmo trutta and Arctic charr Salvelinus alpinus: predicting the effects of climate change. J. Fish Biol. 77, 1793-1817.
12. Farrell, A. P. (2009). Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids. J. Exp. Biol. 212, 3771-3780.
13. Fields, P. A. (2001). Review: Protein function at thermal extremes: balancing stability and flexibility. Comp. Biochem. Physiol. 129A, 417-431.
14. Ford, T. and Beitinger, T. L. (2005). Temperature tolerance in the goldfish, Carassius auratus. J. Therm. Biol. 30, 147-152.
15. Frederich, M. and Pörtner, H. O. (2000). Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am. J. Physiol. 279, R1531-R1538.
16. Gollock, M. J., Currie, S., Petersen, L. H. and Gamperl, A. K. (2006). Cardiovascular and haematological responses of Atlantic cod (Gadus morhua) to acute temperature increase. J. Exp. Biol. 209, 2961-2970.
17. Golod, D. A., Kumar, R. and Joyner, R. W. (1998). Determinants of action potential initiation in isolated rabbit atrial and ventricular myocytes. Am. J. Physiol. 274, H1902-H1913.
18. Guttman, R. (1962). Effect of temperature on the potential and current thresholds of axon membrane. J. Gen. Physiol. 46, 257-266.
19. Hassinen, M., Paajanen, V., Haverinen, J., Eronen, H. and Vornanen, M. (2007). Cloning and expression of cardiac Kir2.1 and Kir2.2 channels in thermally acclimated rainbow trout. Am. J. Physiol. 292, R2328-R2339.
20. Hassinen, M., Haverinen, J. and Vornanen, M. (2008a). Electrophysiological properties and expression of the delayed rectifier potassium (ERG) channels in the heart of thermally acclimated rainbow trout. Am. J. Physiol. 295, R297-R308.
21. Hassinen, M., Paajanen, V. and Vornanen, M. (2008b). A novel inwardly rectifying K+ channel, Kir2.5, is upregulated under chronic cold stress in fish cardiac myocytes. J. Exp. Biol. 211, 2162-2171.
22. Hassinen, M., Laulaja, S., Paajanen, V., Haverinen, J. and Vornanen, M. (2011). Thermal adaptation of the crucian carp (Carassius carassius) cardiac delayed rectifier current, IKs, by homomeric assembly of Kv7.1 subunits without MinK. Am. J. Physiol. 301, R255-R265.
23. Haverinen, J. and Vornanen, M. (2004). Temperature acclimation modifies Na+ current in fish cardiac myocytes. J. Exp. Biol. 207, 2823-2833.
24. Haverinen, J. and Vornanen, M. (2009). Responses of action potential and K+ currents to temperature acclimation in fish hearts: phylogeny or thermal preferences? Physiol. Biochem. Zool. 82, 468-482.
25. Haverinen, J., Hassinen, M. and Vornanen, M. (2007). Fish cardiac sodium channels are tetrodotoxin sensitive. Acta Physiol. (Oxford) 191, 197-204.
26. Hazel, J. R. and Williams, E. E. (1990). The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog. Lipid Res. 29, 167-227.
27. Heath, A. G. and Hughes, G. M. (1973). Cardiovascular and respiratory changes during heat stress in rainbow trout (Salmo gairdneri). J. Exp. Biol. 59, 323-338.
28. Hochachka, P. W. and Somero, G. N. (1984). Biochemical Adaptation. Princeton, NJ: Princeton University Press.
29. Horoszewicz, L. (1973). Lethal and "disturbing" temperatures in some fish species from lakes with normal and artificially elevated temperature. J. Fish Biol. 5, 165-181.
30. Huxley, A. F. (1959). Ion movements during nerve activity. Ann. New York Acad. Sci. 81, 221-246.
31. Johnston, I. A., Calvo, J., Guderley, H., Fernandez, D. and Palmer, L. (1998). Latitudinal variation in the abundance and oxidative capacities of muscle mitochondria in perciform fishes. J. Exp. Biol. 201, 1-12.
32. Lagerspetz, K. Y. (1987). Temperature effects on different organization levels in animals. Symp. Soc. Exp. Biol. 41, 429-449.
33. Mendonça, P. C. and Gamperl, A. K. (2009). Nervous and humoral control of cardiac performance in the winter flounder (Pleuronectes americanus). J. Exp. Biol. 212, 934-944.
34. Patlak, J. (1991). Molecular kinetics of voltage-dependent Na+ channels. Physiol. Rev. 71, 1047-1080.
35. Precht, H., Christophersen, J. and Hensel, H. (1955). Temperatur und Leben. Berlin: Springer-Verlag.
36. Priede, I. G. (1974). The effect of swimming activity and section of the vagus nerves on heart rate in rainbow trout. J. Exp. Biol. 60, 305-319.
37. Rantin, F. T., Gesser, H., Kalinin, A. L., Querra, C. D. R., De Freitas, J. C. and Driedzic, W. R. (1998). Heart performance, Ca2+ regulation and energy metabolism at high temperatures in Bathygobius soporator, a tropical marine teleost. J. Therm. Biol. 23, 31-39.
38. Rosenthal, J. J. C. and Bezanilla, F. (2002). A comparison of propagated action potentials from tropical and temperate squid axons: different durations and conduction velocities correlate with ionic conductance levels. J. Exp. Biol. 205, 1819- 1830.
39. Seebacher, F., Davison, W., Lowe, C. J. and Franklin, C. E. (2005). A falsification of the thermal specialization paradigm: compensation for elevated temperatures in Antarctic fishes. Biol. Lett. 1, 151-154.
40. Shiels, H. A., Vornanen, M. and Farrell, A. P. (2000). Temperature-dependence of Ltype Ca2+ channel current in atrial myocytes from rainbow trout. J. Exp. Biol. 203, 2771-2780.
41. Shiels, H. A., Vornanen, M. and Farrell, A. P. (2002). The force-frequency relationship in fish hearts - a review. Comp. Biochem. Physiol. 132A, 811-826.
42. Somero, G. N. (1995). Proteins and temperature. Annu. Rev. Physiol. 57, 43-68.
43. 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.
44. Stillman, J. and Somero, G. (1996). Adaptation to temperature stress and aerial exposure in congeneric species of intertidal porcelain crabs (genus Petrolisthes): correlation of physiology, biochemistry and morphology with vertical distribution. J. Exp. Biol. 199, 1845-1855.
45. Talo, A. and Tirri, R. (1991). Temperature acclimation of the perch (Perca fluviatilis L.): changes in duration of cardiac action potential. J. Therm. Biol. 16, 89-92.
46. Verde, C., Parisi, E. and di Prisco, G. (2006). The evolution of thermal adaptation in polar fish. Gene 385, 137-145.
47. Vornanen, M. (1989). Regulation of contractility of the fish (Carassius carassius L.) heart ventricle. Comp. Biochem. Physiol. 94C, 477-483.
48. Vornanen, M. (1997). Sarcolemmal Ca influx through L-type Ca channels in ventricular myocytes of a teleost fish. Am. J. Physiol. 272, R1432-R1440.
49. Vornanen, M. (1998). L-type Ca2+ current in fish cardiac myocytes: effects of thermal acclimation and β-adrenergic stimulation. J. Exp. Biol. 201, 533-547.
50. Vornanen, M., Ryökkynen, A. and Nurmi, A. (2002). Temperature-dependent expression of sarcolemmal K+ currents in rainbow trout atrial and ventricular myocytes. Am. J. Physiol. 282, R1191-R1199.
51. Widmark, J., Sundström, G., Ocampo Daza, D. and Larhammar, D. (2011). Differential evolution of voltage-gated sodium channels in tetrapods and teleost fishes. Mol. Biol. Evol. 28, 859-871.
52. Wood, C. M., Pieprzak, P. and Trott, J. N. (1979). The influence of temperature and anemia on the adrenergic and cholinergic mechanisms controlling heart rate in the rainbow trout. Can. J. Zool. 57, 2440-2447.
53. Závodszky, P., Kardos, J., Svingor, A. and Petsko, G. A. (1998). Adjustment of conformational flexibility is a key event in the thermal adaptation of proteins. Proc. Natl. Acad. Sci. USA 95, 7406-7411.
54. Zheng, H., Liu, W., Anderson, L. Y. and Jiang, Q.-X. (2011). Lipid-dependent gating of a voltage-gated potassium channel. Nat. Commun. 2, 250.