Do Mitochondria Limit Hot Fish Hearts? Understanding the Role of Mitochondrial Function with Heat Stress in Notolabrus celidotus

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Iftikar, Fathima I ^a   Hickey, Anthony J R ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CITRATE SYNTHASE; CYTOCHROME C; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; LACTATE DEHYDROGENASE; LACTIC ACID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD OXYGEN TENSION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENVIRONMENTAL TEMPERATURE; ENZYME SYNTHESIS; FISH; FLUOROMETRY; HEART FAILURE; HEART FUNCTION; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART RATE; HEAT STRESS; IN VIVO STUDY; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL PERMEABILITY; NONHUMAN; NOTOLABRUS CELIDOTUS; PROTEIN SECRETION; RESPIROMETRY;

ADAPTATION, PHYSIOLOGICAL; ADENOSINE TRIPHOSPHATE; ANIMALS; CELL RESPIRATION; ENERGY METABOLISM; FISHES; GLYCOLYSIS; HEART; HEART FAILURE; HEART FUNCTION TESTS; HEAT STRESS DISORDERS; HEMOGLOBINS; HOT TEMPERATURE; MITOCHONDRIA, HEART; NEW ZEALAND; OXYGEN; PERMEABILITY; REACTIVE OXYGEN SPECIES;

ANIMALIA; NOTOLABRUS CELIDOTUS;

EID: 84878382914     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064120     Document Type: Article

References (105)

1. Perry AL, Low PJ, Ellis JR, Reynolds JD, (2005) Climate change and distribution shifts in marine fishes. Science 308: 1912-1915.
2. Pörtner HO, Farrell AP, (2008) Physiology and climate change. Science 322: 690-692.
3. Walther GR, Post E, Convey P, Menzel A, Parmesan C, et al. (2002) Ecological responses to recent climate change. Nature 416: 389-395.
4. Galli GLJ, Richards JG, (2012) The effect of temperature on mitochondrial respiration in permeabilized cardiac fibres from the freshwater turtle, Trachemys scripta. J Therm Biol 37: 195-200.
5. Farrell AP, Eliason EJ, Sandblom E, Clark TD, (2009) Fish cardiorespiratory physiology in an era of climate change. Can J Zool 87: 835-851.
6. Stillman JH, (2003) Acclimation capacity underlies susceptibility to climate change. Science 301: 65.
7. Hochachka PW, Somero GN (2002) Biochemical adaptation; mechanism and process in physiological evolution. New York: Oxford University Press. 466 p.
8. Somero GN, (2002) Thermal physiology and vertical zonation of intertidal animals: Optima, limits, and costs of living. Integr Comp Biol 42: 780-789.
9. Somero GN, (2011) Comparative physiology: a "crystal ball" for predicting consequences of global change. Am J Physiol-Reg I 301: R1-R14.
10. Hochachka PW, Somero GN, (1968) The adaptation of enzymes to temperature. Comp Biochem Physiol 27: 659-668.
11. Somero GN, Dahlhoff E, Lin JJ (1996) Stenotherms and eurytherms: mechanisms establishing thermal optima and tolerance ranges. In: Johnston IA, Bennett AF, editors. Animals and Temperature; Phenotypic and Evolutionary Adaptation. Cambridge: Cambridge University Press.
12. Portner HO, Knust R, (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315: 95-97.
13. Portner 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.
14. Willmer P, Stone G, Johnston I (2005) Environmental physiology of animals. Oxford, U.K: Blackwell Publishing.
15. Verberk WCEP, Bilton DT, Calosi P, Spicer JI, (2011) Oxygen supply in aquatic ectotherms: Partial pressure and solubility together explain biodiversity and size patterns. Ecology 92: 1565-1572.
16. Harper A, Newton I, Watt P, (1995) The effect of temperature on spontaneous action potential discharge of the isolated sinus venosus from winter and summer plaice (Pleuronectes platessa). J Exp Biol 198: 137-140.
17. Farrell AP (1997) Effects of temperature on cardiovascular performance. In: Wood CM, McDonald DG, editors. Global Warming: Implications for Freshwater and Marine Fish. Cambridge: Cambridge University Press. 135-158.
18. Shiels HA, Vornanen M, Farrell AP, (2003) Acute temperature change modulates the response of ICa to adrenergic stimulation in fish cardiomyocytes. Physiol Biochem Zool 76: 816-824.
19. Lesnefsky EJ, Moghaddas S, Tandler B, Kerner J, Hoppel CL, (2001) Mitochondrial dysfunction in cardiac disease: ischemia-reperfusion, aging, and heart failure. J Mol Cell Cardiol 33: 1065-1089.
20. Huss JM, Kelly DP, (2005) Mitochondrial energy metabolism in heart failure: a question of balance. J Clin Invest 115: 547-555.
21. Lane N (2005) Power, sex and suicide: mitochondria and the meaning of life. Oxford: Oxford University Press.
22. Steinlechner-Maran R, Eberl T, Kunc M, Schröcksnadel H, Margreiter R, et al. (1997) Respiratory defect as an early event in preservation-reoxygenation injury of endothelial cells 1. Transplantation 63: 136-142.
23. Stadlmann S, Renner K, Pollheimer J, Moser P, Zeimet A, et al. (2006) Preserved coupling of oxidative phosphorylation but decreased mitochondrial respiratory capacity in IL-1β-treated human peritoneal mesothelial cells. Cell Biochem Biophys 44: 179-186.
24. Grieshaber MK, Hardewig I, Kreutzer U, Pörtner HO, (1994) Physiological and metabolic responses to hypoxia in invertebrates. Rev Physiol Biochem Pharmacol 125: 44-129.
25. Hochachka P (1994) Muscles as molecular and metabolic machines. Boca Raton: CRC Press.
26. Mootha VK, Bunkenborg J, Olsen JV, Hjerrild M, Wisniewski JR, et al. (2003) Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115: 629-640.
27. Cereghetti GM, Scorrano L, (2006) The many shapes of mitochondrial death. Oncogene 25: 4717-4724.
28. Benard G, Faustin B, Passerieux E, Galinier A, Rocher C, et al. (2006) Physiological diversity of mitochondrial oxidative phosphorylation. Am J Physiol Cell Physiol 291: C1172-1182.
29. Borutaite V, Brown GC, (2003) Mitochondria in apoptosis of ischemic heart FEBS Letters. 541: 1-5.
30. 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.
31. Brand MD, Nicholls DG, (2011) Assessing mitochondrial dysfunction in cells. Biochem J 435: 297-312.
32. Lemieux H, Semsroth S, Antretter H, Höfer D, Gnaiger E, (2011) Mitochondrial respiratory control and early defects of oxidative phosphorylation in the failing human heart. Int J Biochem Cell Biol 43: 1729-1738.
33. Lemieux H, Tardif J-C, Dutil J-D, Blier PU, (2010) Thermal sensitivity of cardiac mitochondrial metabolism in an ectothermic species from a cold environment, Atlantic wolffish (Anarhichas lupus). J Exp Mar Biol Ecol 384: 113-118.
34. Moyes CD, (1996) Cardiac metabolism in high performance fish. Comp Biochem Physiol A 113: 69-75.
35. Somero GN, (2002) Thermal physiology and vertical zonation of intertidal animals:optima, limits, and costs of living. Intergrative and Comparative Biology 42: 780-789.
36. Qian L, Song X, Ren H, Gong J, Cheng S, (2004) Mitochondrial mechanism of heat stress-induced injury in rat cardiomyocyte. Cell Stress Chaperon 9: 281-293.
37. Turrens JF, (2003) Mitochondrial formation of reactive oxygen species. J Physiol (Lond) 552: 335-344.
38. 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.
39. Johnston IA, Helga G, Franklin CE, Crockford T, Collins K, (1994) Are mitochondria subject to evolutionary temperature adaptation? J Exp Biol 195: 293-306.
40. Blier PU, Lemieux H, (2001) The impact of the thermal sensitivity of cytochrome c oxidase on the respiration rate of Arctic charr red muscle mitochondria. J Comp Physiol B 171: 247-253.
41. Birkedal R, Gesser H, (2004) Regulation of mitochondrial energy production in cardiac cells of rainbow trout (Oncorhynchus mykiss). J Comp Physiol B 174: 255-262.
42. Birkedal R, Gesser H, (2003) Creatine kinase and mitochondrial respiration in hearts of trout, cod and freshwater turtle. J Comp Physiol B 173: 493-499.
43. 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.
44. Ansaldo M, Luquet CM, Evelson PA, Polo JM, Llesuy S, (2000) Antioxidant levels from different Antarctic fish caught around South Georgia Island and Shag Rocks. Polar Biol 23: 160-165.
45. Hardewig I, Pörtner HO, Peck LS, (1999) Thermal sensitivity of mitochondrial function in the Antarctic Notothenioid Lepidonotothen nudifrons. J Comp Physiol B 169: 597-604.
46. Hilton Z, Clements KD, Hickey AJ, (2010) Temperature sensitivity of cardiac mitochondria in intertidal and subtidal triplefin fishes. J Comp Physiol B 180: 979-990.
47. Iftikar FI, MacDonald J, Hickey AJR, (2010) Thermal limits of portunid crab heart mitochondria: Could more thermo-stable mitochondria advantage invasive species? J Exp Mar Biol Ecol 395: 232-239.
48. Francis MP, Morrison MA, Leathwick J, Walsh C, Middleton C, (2005) Predictive models of small fish presence and abundance in northern New Zealand harbours. Estuar Coast Shelf S 64: 419-435.
49. Lane N, Martin W, (2010) The energetics of genome complexity. Nature 467: 929-934.
50. Tarba C, Cracium C, (1990) A comparative study of the effects of procaine, lidocaine, tetracaine and dibucaine on the functions and ultrastructure of isolated rat liver mitochondria. Biochim Biophys Acta 1019: 19-28.
51. Wells RMG, McNeil H, MacDonald JA, (2005) Fish hypnosis: Induction of an atonic immobility reflex. Mar Freshw Behav Phy 38: 71-78.
52. Gollock MJ, Kennedy CR, Brown JA, (2005) Physiological responses to acute temperature increase in European eels Anguilla anguilla infected with Anguillicola crassus. Dis Aquat Org 64: 223-228.
53. Pörtner HO, Berdal B, Blust R, Brix O, Colosimo A, et al. (2001) Climate induced temperature effects on growth performance, fecundity and recruitment in marine fish: developing a hypothesis for cause and effect relationships in Atlantic cod (Gadus morhua) and common eelpout (Zoarces viviparus). Cont Shelf Res 21: 1975-1997.
54. Zakhartsev MV, Wachter B, Sartoris FJ, Pörtner HO, Blust R, (2003) Thermal physiology of the common eelpout (Zoarces viviparus). J Comp Physiol B 173: 365-378.
55. Zijlstra WG, Buursma A, Meeuwsen-van der Roest WP, (1991) Absorption spectra of human fetal and adult oxyhemoglobin, de-oxyhemoglobin, carboxyhemoglobin, and methemoglobin. Clin Chem 37: 1633-1638.
56. Villas-Bôas SG, Delicado DG, Åkesson M, Nielsen J, (2003) Simultaneous analysis of amino and nonamino organic acids as methyl chloroformate derivatives using gas chromatography-mass spectrometry. Anal Biochem 322: 134-138.
57. Howald H, Hoppeler H, Claassen H, Mathieu O, Straub R, (1985) Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflügers Archiv 403: 369-376.
58. Srere PA (1969) [1] Citrate synthase: [EC 4.1.3.7. Citrate oxaloacetate-lyase (CoA-acetylating)]. In: John ML, editor. Method Enzymol: Academic Press. 3-11.
59. Hochachka PW, Stanley C, Merkt J, Sumar-Kalinowski J, (1983) Metabolic meaning of elevated levels of oxidative enzymes in high altitude adapted animals: an interpretive hypothesis. Respir Physiol 52: 303-313.
60. Hickey AJ, Clements KD, (2003) Key metabolic enzymes and muscle structure in triplefin fishes (Tripterygiidae): a phylogenetic comparison. J Comp Physiol B 173: 113-123.
61. Newsholme EA, Crabtree B, (1986) Maximum catalytic activity of some key enzymes in provision of physiologically useful information about metabolic fluxes. J Exp Zool 239: 159-167.
62. McClelland GB, Craig PM, Dhekney K, Dipardo S, (2006) Temperature- and exercise-induced gene expression and metabolic enzyme changes in skeletal muscle of adult zebrafish (Danio rerio). J Physiol 577: 739-751.
63. Gnaiger E, Kuznetsov AV, Schneeberger S, Seiler R, Brandacher G, et al. (2000) Mitochondria in the cold. In: Heldmaier M, Klingenspor M, editors. Life in the cold. Heidelberg: Springer. 431-442.
64. Gnaiger E, (2009) Capacity of oxidative phosphorylation in human skeletal muscle: New perspectives of mitochondrial physiology. Int J Biochem Cell B 41: 1837-1845.
65. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, et al. (2008) Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 3: 965-976.
66. Hickey A, Renshaw G, Speers-Roesch B, Richards J, Wang Y, et al. (2011) A radical approach to beating hypoxia: depressed free radical release from heart fibres of the hypoxia-tolerant epaulette shark (Hemiscyllum ocellatum). J Comp Physiol B: 1-10.
67. Chinopoulos C, Vajda S, Csanády L, Mándi M, Mathe K, et al. (2009) A novel kinetic assay of mitochondrial ATP-ADP exchange rate mediated by the ANT. Biophys J 96: 2490-2504.
68. Aggio R, Villas-Bôas SG, Ruggiero K, (2011) Metab: an R package for high-throughput analysis of metabolomics data generated by GC-MS. Bioinformatics 27: 2316-2318.
69. Domenis R, Comelli M, Bisetto E, Mavelli I, (2011) Mitochondrial bioenergetic profile and responses to metabolic inhibition in human hepatocarcinoma cell lines with distinct differentiation characteristics. J Bioenerg Biomembr 43: 493-505.
70. Zukiene R, Nauciene Z, Ciapaite J, Mildaziene V, (2010) Acute temperature resistance threshold in heart mitochondria: Febrile temperature activates function but exceeding it collapses the membrane barrier. Int J Hyperther 26: 56-66.
71. Fink MP, (2001) Cytopathic Hypoxia: Mitochondrial Dysfunction as Mechanism Contributing to Organ Dysfunction in Sepsis. Crit Care Clin 17: 219-237.
72. Fink MP, (2002) Cytopathic hypoxia. Is oxygen use impaired in sepsis as a result of an acquired intrinsic derangement in cellular respiration? Crit Care Clin 18: 165-175.
73. Farrell AP, Jones DR (1992) The Heart. In: Hoar WS, Randall DJ, Farrell AP, editors. Fish Physiology. San Diego: Academic Press. 1-88.
74. Clark TD, Sandblom E, Cox GK, Hinch SG, Farrell AP, (2008) Circulatory limits to oxygen supply during an acute temperature increase in the Chinook salmon (Oncorhynchus tshawytscha). Am J Physiol-Reg I 295: R1631-R1639.
75. Frederich M, Pörtner HO, (2000) Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am J Physiol-Reg I 279: R1531-R1538.
76. Pörtner HP, (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88: 137-146.
77. Zielinski S, Pörtner H-O, (2000) Oxidative stress and antioxidative defense in cephalopods: a function of metabolic rate or age? Comp Biochem Physiol B 125: 147-160.
78. Feidantsis K, Pörtner H, Lazou A, Kostoglou B, Michaelidis B, (2009) Metabolic and molecular stress responses of the gilthead seabream Sparus aurata during long-term exposure to increasing temperatures. Mar Biol 156: 797-809.
79. Van Dijk PLM, Tesch C, Hardewig I, Pörtner HO, (1999) Physiological disturbances at critically high temperatures: A comparison between stenothermal Antarctic and eurythermal temperate eelpouts (Zoarcidae). J Exp Biol 202: 3611-3621.
80. Podrabsky JE, Lopez JP, Fan TWM, Higashi R, Somero GN, (2007) Extreme anoxia tolerance in embryos of the annual killifish Austrofundulus limnaeus: insights from a metabolomics analysis. J Exp Biol 210: 2253-2266.
81. Murphy MP, (2009) How mitochondria produce reactive oxygen species. Biochem J 417: 1-13.
82. Brand MD, (1990) The proton leak across the mitochondrial inner membrane. Biochim Biophys Acta 1018: 128-133.
83. Seebacher F, Brand MD, Else PL, Guderley HE, Hulbert AJ, et al. (2010) Plasticity of oxidative metabolism in variable climates: Molecular mechanisms. Physiol Biochem Zool 83: 721-732.
84. Hand SC, Menze MA, (2008) Mitochondria in energy-limited states: mechanisms that blunt the signaling of cell death. J Exp Biol 211: 1829-1840.
85. Mailer K, (1990) Superoxide radical as electron donor for oxidative phosphorylation of ADP. Biochem Bioph Res Co 170: 59-64.
86. Ide T, Tsutsui H, Kinugawa S, Utsumi H, Kang D, et al. (1999) Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circ Res 85: 357-363.
87. Sorescu D, Griendling KK, (2002) Reactive oxygen species, mitochondria, and NAD(P)H oxidases in the development and progression of heart failure. Congest Heart Fail 8: 132-140.
88. Hickey AJR, Chai CC, Choong SY, de Freitas Costa S, Skea GL, et al. (2009) Impaired ATP turnover and ADP supply depress cardiac mitochondrial respiration and elevate superoxide in nonfailing spontaneously hypertensive rat hearts. Am J Physiol-Cell Ph 297: C766-C774.
89. Gnaiger E, Kuznetsov AV, (2002) Mitochondrial respiration at low levels of oxygen and cytochrome c. Biochem Soc Trans 30: 252-258.
90. Lemieux H, Tardif J-C, Dutil J-D, Blier PU, (2010) Thermal sensitivity of cardiac mitochondrial metabolism in an ectothermic species from a cold environment, Atlantic wolffish (Anarhichas lupus). J Exp Mar Biol Ecol 384: 113-118.
91. Brown GC, (2001) Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim Biophys Acta 1504: 46-57.
92. Calvert JW, Jha S, Gundewar S, Elrod JW, Ramachandran A, et al. (2009) Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ Res 105: 365-374.
93. Boveris A, Costa LE, Poderoso JJ, Carreras MC, Cadenas E, (2000) Regulation of mitochondrial respiration by oxygen and nitric oxide. Ann NY Acad Sci 899: 121-135.
94. Gnaiger E, Lassnig B, Kuznetsov A, Rieger G, Margreiter R, (1998) Mitochondrial oxygen affinity, respiratory flux control and excess capacity of cytochrome c oxidase. J Exp Biol 201: 1129-1139.
95. Oellermann M, Pörtner HO, Mark FC, (2012) Mitochondrial dynamics underlying thermal plasticity of cuttlefish (Sepia officinalis) hearts. J Exp Biol 215: 2992-3000.
96. Hilton Z, Clements KD, Hickey AJR (2010) Temperature sensitivity of cardiac mitochondria in intertidal and subtidal triplefin fishes. Comp Biochem Physiol Submitted.
97. Ventura-Clapier R, Garnier A, Veksler V, (2004) Energy metabolism in heart failure. J Physiol 555: 1-13.
98. Guderley HE, Rojas FM, Nusetti OA, (1995) Metabolic specialization of mitochondria from scallop phasic muscles. Mar Biol 122: 409-416.
99. Moyes CD, Schulte PM, Hochachka PW, (1992) Recovery metabolism of trout white muscle: role of mitochondria. Am J Physiol-Reg I 262: R295-R304.
100. Blier PU, Guderley HE, (1993) Effects of pH and temperature on the kinetics of pyruvate oxidation by muscle mitochondria from rainbow trout (Oncorhynchus mykiss). Physiol Zool 66: 474-489.
101. Lemieux H, Blier PU, Tardif JC, (2008) Does membrane fatty acid composition modulate mitochondrial functions and their thermal sensitivities? Comp Biochem Physiol A 149: 20-29.
102. Mourik J, (1983) Oxidations in the tricarboxylic acid cycle by intact mitochondria isolated from the lateral red muscle of goldfish (Carassius auratus L.). Effects of anoxia on the oxidation of pyruvate and glutamate. Comp Biochem Physiol B 76: 851-859.
103. Lemieux H, Tardif J-C, Blier PU, (2010) Thermal sensitivity of oxidative phosphorylation in rat heart mitochondria: Does pyruvate dehydrogenase dictate the response to temperature? J Therm Biol 35: 105-111.
104. Somero GN, Dahlhoff E, Lin JJ (1996) Stenotherms and eurytherms: mechanisms establishing thermal optima and tolerance ranges. In: Johnston IA, Bennett AF, editors. Animals and Temperature; Phenotypic and Evolutionary Adaptation. Cambridge: Cambridge University Press.
105. Neubauer S, (2007) The Failing Heart - An Engine Out of Fuel. New Eng J Med 356: 1140-1151.