Temperature sensitivity of cardiac mitochondria in intertidal and subtidal triplefin fishes

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 180, Issue 7, 2010, Pages 979-990

  Hilton, Z ^a   Clements, Kendall D ^a   Hickey, Anthony J R ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Ectotherm; Fish; Heart failure; Mitochondria; Temperature

Indexed keywords

CYTOCHROME C OXIDASE; OXYGEN; SEA WATER;

ACCLIMATIZATION; ANIMAL; ANOXIA; ARTICLE; BLOOD; BODY WEIGHT; BREATHING; COMPARATIVE STUDY; HEART; HEART FAILURE; HEART MITOCHONDRION; HEART VENTRICLE FUNCTION; METABOLISM; ORGAN SIZE; OXIDATIVE PHOSPHORYLATION; PATHOPHYSIOLOGY; PERCIFORMES; PHYSIOLOGY; TEMPERATURE;

ACCLIMATIZATION; ANIMALS; ANOXIA; BODY WEIGHT; ELECTRON TRANSPORT COMPLEX IV; HEART; HEART FAILURE; MITOCHONDRIA, HEART; ORGAN SIZE; OXIDATIVE PHOSPHORYLATION; OXYGEN; PERCIFORMES; RESPIRATION; SEAWATER; TEMPERATURE; VENTRICULAR FUNCTION;

ANIMALIA; BELLAPISCIS MEDIUS; FORSTERYGION VARIUM; PISCES;

EID: 77956771710     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-010-0477-7     Document Type: Article

References (82)

1. Abele D, Philipp E, González PM, Puntarulo S (2007) Marine invertebrate mitochondria and oxidative stress. Front Biosci 12: 933-946.
2. Almeida-Val VMF, Buck LT, Hochachka PW (1994) Substrate and acute temperature effects on turtle heart and liver mitochondria. Am J Physiol 266R: 858-862.
3. Antunes F, Boveris A, Cadenas E (2004) On the mechanism and biology of cytochrome oxidase inhibition by nitric oxide. PNAS 101: 16774-16779.
4. Benard G, Faustin B, Passerieux E, Galinier A, Rocher C, Bellance N, Delage J-P, Casteilla L, Letellier T, Rossignol R (2006) Physiological diversity of mitochondrial oxidative phosphorylation. Am J Physiol 291C: 1172-1182.
5. Birkedal R, Gesser H (2003) Creatine kinase and mitochondrial respiration in hearts of trout, cod and freshwater turtle. J Comp Physiol 173B: 493-499.
6. Borutaite V, Brown G (1996) Rapid reduction of nitric oxide by mitochondria, and reversible inhibition of mitochondrial respiration by nitric oxide. Biochem J 315: 295-299.
7. Boushel R, Gnaiger E, Schjerling P, Skovbro M, Kraunsoe R, Dela F (2007) Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetalogia 50: 790-796.
8. Brand MD, Chien L-F, Ainscow EK, Rolfe DFS, Porter RK (1994) The causes and functions of mitochondrial proton leak. Biochim Biophys Acta 1187: 132-139.
9. Brookes PS, Buckingham JA, Tenreiro AM, Hulbert AJ, Brand MD (1998) The proton permeability of the inner membrane of liver mitochondria from ectothermic and endothermic vertebrates and from obese rats: correlations with standard metabolic rate and phospholipid fatty acid composition. Comp Biochem Physiol 119B: 325-334.
10. Cadenas S, Buckingham J, St Pierre J, Dickinson K, Jones R, Brand M (2000) AMP decreases the efficiency of skeletal-muscle mitochondria. Biochem J 351: 307-311.
11. Caldwell RS, Vernberg FJ (1970) The influence of acclimation temperature on the lipid composition of fish gill mitochondria. Comp Biochem Physiol 34: 179-191.
12. Campian JL, Gao X, Qian M, Eaton JW (2007) Cytochrome c oxidase activity and oxygen tolerance. J Biol Chem 282: 12430-12438.
13. Cereghetti GM, Scorrano L (2006) The many shapes of mitochondrial death. Oncogene 25: 4717-4724.
14. Chance B, Hagihara B (1962) Activation and inhibition of succinate oxidation following adenosine diphosphate supplements to pigeon heart mitochondria. J Biol Chem 237: 3540-3545.
15. Chemnitius J, Manglitz T, Kloeppel M, Doenst T, Schwartz P, Kreuzer H, Zech R (1993) Rapid preparation of subsarcolemmal and interfibrillar mitochondrial subpopulations from cardiac muscle. Int J Biochem 25: 589-596.
16. Clements KD (2003) Triplefins. In: Andrew N, Francis MP (eds) The living reef: the ecology of New Zealand's rocky reefs. Craig Potton Publishing, Nelson, pp 160-167.
17. Cossins AR, Kent J, Prosser CL (1980) A steady state and differential polarised phase fluorimetric study of the liver microsomal and mitochondrial membranes of thermally acclimated green sunfish (Lepomis cyanellus). Biochim Biophys Acta 599: 341-358.
18. Dahlhoff E, Somero GN (1993) Effects of temperature on mitochondria from abalone (Genus Haliotis): adaptive plasticity and its limits. J Exp Biol 185: 151-168.
19. Das NB (1937) Studies on the inhibition of the succinic and lactic-malic dehydrogenases. Biochem J 31: 1124-1130.
20. Davidson S, Duchen M (2006) Effects of NO on mitochondrial function in cardiomyocytes: pathophysiological relevance. Cardiovasc Res 71: 10-21.
21. Di Paola M, Lorusso M (2006) Interaction of free fatty acids with mitochondria: coupling, uncoupling and permeability transition. Biochim Biophys Acta 1757: 1330-1337.
22. Farrell AP (1997) Effects of temperature on cardiovascular performance. In: Wood CM, Mc Donald DG (eds) Global warming: implications for freshwater and marine fish. Cambridge University Press, Cambridge, pp 135-158.
23. Farrell AP (2002) Cardiorespiratory performance in salmonids during exercise at high temperature: insights into cardiovascular design limitations in fishes. Comp Biochem Physiol 132A: 797-810.
24. Feary DA, Clements KD (2006) Habitat use by triplefin fishes (Family Trypterygiidae) on rocky reefs in New Zealand. J Fish Biol 69: 1031-1046.
25. Frederich M, Pörtner HO (2000) Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am J Physiol 279R: 1531-1538.
26. Glanville EJ, 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.
27. Gnaiger E (2003) Oxygen conformity of cellular respiration; a perspective of mitochondrial physiology. Kluwer Academic/Plenum Publishers, New York.
28. Gnaiger E (2008) Polarographic oxygen sensors, the oxygraph, and high-resolution respirometry to assess mitochondrial function. In: Dykens J, Will Y (eds) Drug-induced mitochondrial dysfunction. John Wiley & Sons, Inc.
29. Gnaiger E (2009) Capacity of oxidative phosphorylation in human skeletal muscle: new perspectives of mitochondrial physiology. Int J Biochem Cell Biol 41: 1837-1845.
30. Gnaiger E, Lassnig B, Kuznetsov AV, Rieger G, Raimund M (1998) Mitochondrial oxygen affinity, respiratory flux control and excess capacity of cytochrome c oxidase. J Exp Biol 201: 1129-1139.
31. Gnaiger E, Kuznetsov AV, Schneeberger S, Seiler R, Brandacher G, Steurer W, Margreiter R (2000) Mitochondria in the cold. In: Heldmaier M, Klingenspor M (eds) Life in the cold. Springer, Heidelberg, pp 431-442.
32. Guderley H, St Pierre J (2002) Going with the flow or life in the fast lane: contrasting mitochondrial responses to thermal change. J Exp Biol 205: 2237-2249.
33. Hardewig I, Peck LS, Pörtner HO (1999) Thermal sensitivity of mitochondrial function in the Antarctic Notothenioid Lepidonotothen nudifrons. J Comp Physiol 169B: 597-604.
34. Hazel JR, Williams EE (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.
35. Hickey AJR, Clements KD (2003) Key metabolic enzymes and muscle structure in triplefin fishes (Tripterygiidae): a phylogenetic comparison. J Comp Physiol 173B: 113-123.
36. Hickey AJR, Clements KD (2005) Genome size evolution in New Zealand triplefin fishes. J Hered 96: 356-362.
37. Hickey AJR, Chai CC, Choong SY, de Freitas Costa S, Skea GL, Phillips ARJ, Cooper GJS (2009a) Impaired ATP turnover and ADP supply depress cardiac mitochondrial respiration and elevate superoxide in nonfailing spontaneously hypertensive rat hearts. Am J Physiol 297: C766-C774.
38. Hickey AJR, Lavery SD, Hannan DA, Baker SC, Clements KD (2009b) New Zealand triplefin fishes (Family Tripterygiidae): contrasting population structure and mtDNA diversity within a marine species flock. Mol Ecol 18: 680-696.
39. Hillar M, Lott V, Lennox B (1975) Correlation of the effects of citric acid cycle metabolites on succinate oxidation by rat liver mitochondria and submitochondrial particles. Bioenergetics 7: 1-16.
40. Hilton Z, Wellenreuther M, Clements KD (2008) Physiology underpins habitat partitioning in a sympatric sister-species pair of intertidal fishes. Funct Ecol 22: 1108-1117.
41. Hochachka PW, Somero GN (2002) Biochemical adaptation. Mechanism and process in physiological evolution. Oxford University Press, New York.
42. Hulbert AJ, Else PL (2000) Mechanisms underlying the cost of living in animals. Annu Rev Physiol 62: 207-235.
43. Irving DO, Watson K (1976) Mitochondrial enzymes of tropical fish: a comparison with fish from cold waters. Comp Biochem Physiol 54B: 81-92.
44. Johnston IA, Guderley H, Franklin CE, Crockford T, Kamunde C (1994) Are mitochondria subject to evolutionary temperature adaptation? J Exp Biol 195: 293-306.
45. Jüllig M, Hickey AJR, Chai CC, Skea GL, Middleditch MJ, Costa S, Choong SY, Philips AJC, Cooper GJS (2008) Is the failing heart out of fuel or a worn engine running rich? A study of mitochondria in old spontaneously hypertensive rats. Proteomics 8: 2556-2572.
46. Kunz WS, Kudin A, Vielhaber S, Elger CE, Attardi G, Villani G (2000) Flux control of cytochrome c oxidase in human skeletal muscle. J Biol Chem 275: 27741-27745.
47. Kuznetsov A, Tiivel T, Sikk P, Kaambre T, Kay L, Daneshrad Z, Rossi A, Kadaja L, Peet N, Seppet E, Saks V (1996) Striking differences between the kinetics of regulation of respiration by ADP in slow-twitch and fast-twitch muscles in vivo. Eur J Biochem 241: 909-915.
48. Kuznetsov AV, Schneeberger S, Seiler R, Brandacher G, Mark W, Steurer W, Saks V, Usson Y, Margreiter R, Gnaiger E (2004) Mitochondrial defects and heterogenous cytochrome c release after cardiac cold ischemia and reperfusion. Am J Physiol 286H: 1633-1641.
49. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, Kunz WS (2008) Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 3: 965-976.
50. Leary SC, Lyons CN, Rosenberger AG, Ballantyne JS, Stillman J, Moyes CD (2003) Fiber-type differences in muscle mitochondrial profiles. Am J Physiol 285R: 817-826.
51. Mootha VK, Bunkenborg J, Olsen JV, Hjerrild M, Wisniewski JR, Stahl E, Bolouri MS, Ray HN, Sihag S, Kamal M (2003) Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115: 629-640.
52. Moyes CD, Mathieu-Costello OA, Brill RW, Hochachka PW (1992) Mitochondrial metabolism of cardiac and skeletal muscles from a fast (Katsuwonus pelamis) and a slow (Cyprinus carpio) fish. Can J Zool 70: 1246-1253.
53. Murphy M (2009) How mitochondria produce reactive oxygen species. Biochem J 417: 1-13.
54. Oosterbaan RJ (1994) Frequency and regression analysis. In: Ritzema HP (ed) Drainage principles and applications. ILRI Publication 16, Wageningen, The Netherlands, pp 175-223.
55. Pardee AB, Potter VR (1948) Inhibition of succinate dehydrogenase by oxaloacetate. J Biol Chem 176: 1085-1094.
56. Park K-S, Jo I, Pak Y, Bae S-W, Rhim H, Suh S-H, Park S, Zhu M, So I, Kim K (2002) FCCP depolarizes plasma membrane potential by activating proton and Na+ currents in bovine aortic endothelial cells. Pflügers Arch Eur J Physiol 443: 344-352.
57. Paulus W, Bronzwaer J (2004) Nitric oxide's role in the heart: control of beating or breathing? Am J Physiol 287: H8-H13.
58. Pörtner HO (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88: 137-146.
59. Pörtner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol 132A: 739-761.
60. Pörtner HO (2006) Climate-dependent evolution of Antarctic ectotherms: an integrative analysis. Deep Sea Res Part II: Top Stud Oceanogr 53: 1071-1104.
61. Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315: 95-97.
62. Pörtner HO, Hardewig I, Peck LS (1999) Mitochondrial function and critical temperature in the Antarctic bivalve, Laternula elliptica. Comp Biochem Physiol 124A: 179-189.
63. Pörtner HO, Mark FC, Bock C (2004) Oxygen limited thermal tolerance in fish? Answers obtained by nuclear magnetic resonance techniques. Respir Physiol Neurobiol 141: 243-260.
64. Pörtner HO, Lucassen M, Storch D (2005) Metabolic biochemistry: it's role in thermal tolerance and the capacities of physiological and ecological function. The physiology of polar fishes. Elsevier, New York, pp 79-154.
65. Saks V, Belikova Y, Kuznetsov A (1991) In vivo regulation of mitochondrial respiration in cardiomyocytes: specific restrictions for intracellular diffusion of ADP. Biochim Biophys Acta 1074: 302-311.
66. Saks V, Vasil'eva E, Belikova Y, Kuznetsov A, Lyapina S, Petrova L (1993) Retarded diffusion of ADP in cardiomyocytes: possible role of mitochondrial outer membrane and creatine kinase in cellular regulation of oxidative phosphorylation. Biochim Biophys Acta 1144: 134-148.
67. Saks VA, Veksler VI, Kuznetsov AV, Kay L, Sikk P, Tiivel T, Tranqui L, Olivares J, Winkler K, Wiedemann F, Kunz WS (1998) Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol Cell Biochem 184: 81-100.
68. Samartsev VN, Smirnov AV, Zeldi IP, Markova OV, Mokhova EN, Skulachev VP (1997) Involvement of aspartate/glutamate antiporter in fatty-acid-induced uncoupling of liver mitochondria. Biochim Biophys Acta 1319: 251-257.
69. Sheeran FL, Pepe S (2006) Energy deficiency in the failing heart: linking increased reactive oxygen species and disruption of oxidative phosphorylation rate. Biochim Biophys Acta 1757: 543-552.
70. Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integ Comp Physiol 42: 780-789.
71. Sommer A, Klein B, Pörtner HO (1997) Temperature induced anaerobiosis in two populations of the polychaete worm Arenicola marina (L). J Comp Physiol 167B: 25-35.
72. Stillman J, Somero GN (2000) A comparative analysis of the upper thermal tolerance limits of eastern pacific porcelain crabs, genus Petrolisthes: influences of latitude, vertical zonation, acclimation, and phylogeny. Physiol Biochem Zool 73: 200-208.
73. Stuart JA, Cadenas S, Jekabsons MB, Roussel D, Brand MD (2001) Mitochondrial proton leak and the uncoupling protein 1 homologues. Biochim Biophys Acta 1504: 144-158.
74. Trigari G, Pirini M, Ventrella V, Pagliarani A, Trombetti F, Borgatti AR (1992) Lipid composition and mitochondrial respiration in warm- and cold-adapted sea bass. Lipids 27: 371-377.
75. Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552: 335-344.
76. van den Thillart G, De Bruin G (1981) Influence of environmental temperature on mitochondrial membranes. Biochim Biophys Acta 640: 439-447.
77. van den Thillart G, Modderkolk J (1978) The effect of acclimation temperature on the activation energies of state III respiration and on the unsaturation of membrane lipids of goldfish mitochondria. Biochim Biophys Acta 510: 38-51.
78. Vandenheede JR, Criddle RC, Ahmed AI, Feeney RE (1973) Heart mitochondrial oxidations of an Antarctic fish. Comp Biochem Physiol 46B: 313-319.
79. Veksler VI, Kuznetsov AV, Sharov VG, Kapelko VI, Saks VA (1987) Mitochondrial respirometry parameters in cardiac tissue: a novel method of assessment by using saponin-skinned fibers. Biochim Biophys Acta 892: 191-196.
80. Weinstein RB, Somero GN (1998) Effects of temperature on mitochondrial function in the Antarctic fish Trematomus bernacchii. J Comp Physiol 168B: 190-196.
81. Wellenreuther M, Barrett PT, Clements KD (2007) Ecological diversification in habitat use by subtidal triplefin fishes (Tripterygiidae). Mar Ecol Prog Ser 330: 235-246.
82. Wieckowski MR, Wojtczak L (1997) Involvement of the dicarboxylate carrier in the protonophoric action of long-chain fatty acids in mitochondria. Biochem Biophys Res Commun 232: 414-417.