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Protein synthesis is defended in the mitochondrial fraction of gill but not heart in cunner (Tautogolabrus adspersus) exposed to acute hypoxia and hypothermia

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Abstract

The cunner, Tautogolabrus adspersus, is a north-temperate teleost which relies upon metabolic depression to survive the extreme low water temperatures of its habitat during the winter. Previous study has demonstrated a decrease in protein synthesis accompanies the metabolic depression observed at the whole animal level during seasonal low temperature exposure. As such, the objective of the current study was to determine: (i) if the response of decreased protein synthesis is conserved across environmental stressors and (ii) if the response of metabolic depression is conserved across levels of cellular organization. This was accomplished through the measurement of in vivo protein synthesis rates in the whole tissue, cytosolic and mitochondrial protein pools (reflective of nuclear encoded proteins imported into mitochondria) of heart and gill in cunner exposed to either acute low temperature (8–4°C) or acute hypoxia (10% O2 saturation). In both heart and gill, rates of protein synthesis in the whole tissue and cytosolic protein pools were substantially depressed by 80% in response to acute hypothermia. In hypoxic heart, protein synthesis was significantly decreased by 50–60% in the whole tissue, cytosolic and mitochondrial pools; however, in gill there was no significant difference in rates of protein synthesis in any cellular fraction between normoxic and hypoxic groups. Most strikingly the rate of new protein accumulation in the mitochondrial fraction of gill did not change in response to either a decrease in temperature or hypoxia. The defense of protein synthesis in the gill is most likely associated with the importance of maintaining ionic regulation and the oxidative capacity in this front line organ for gas and ion exchange.

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References

  • Bailey JR, Driedzic WR (1996) Decreased total ventricular and mitochondrial protein synthesis during extended anoxia in turtle heart. Am J Physiol Regul Integr Comp Physiol 271:R1660–R1667

    CAS  Google Scholar 

  • Ballantyne JS (1994) Fish mitochondria. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes: Analytical techniques, vol 3. Elsevier Science, New York, pp 487–502

    Google Scholar 

  • Barger JL, Brand BM, Boyer BB (2003) Tissue-specific depression of mitochondrial proton leak and substrate oxidation in hibernating arctic ground squirrels. Am J Physiol Regul Integr Comp Physiol 284:R1306–R1313

    CAS  PubMed  Google Scholar 

  • Birkedal R, Gesser H (2004) Effects of hibernation on mitochondrial regulation and metabolic capacities in mycardium of painted turtle (Chrysemys picta). Comp Biochem Physiol A Mol Integr Physiol 139:285–291

    Article  PubMed  Google Scholar 

  • Bishop T, St.Pierre J, Brand MD (2002) Primary causes of decreased mitochondrial oxygen consumption during metabolic depression in snail cells. Am J Physiol Regul Integr Comp Physiol 282:R372–R382

    CAS  PubMed  Google Scholar 

  • Boutilier RG (2001) Mechanisms of cell survival in hypoxia and hypothermia. J Exp Biol 204:3171–3181

    CAS  PubMed  Google Scholar 

  • Brooks GA (2002) Lactate shuttles in nature. Biochem Soc Trans 30:258–264

    Article  CAS  PubMed  Google Scholar 

  • Brooks SPJ, Storey KB (1993) De novo protein synthesis and protein phosphorylation during anoxia and recovery in the red-eared turtle. Am J Physiol Regul Integr Comp Physiol 265:R1380–R1386

    CAS  Google Scholar 

  • Brooks GA, Dubouchaud H, Brown M, Sicurello JP, Butz CE (1999) Role of mitochondrial lactate dehydrogenase and lactate oxidation in the intracellular lactate shuttle. Proc Natl Acad Sci USA 96:1129–1134

    Article  CAS  PubMed  Google Scholar 

  • Brustovetsky NN, Mayevsky EI, Grishina EV, Gogvadze VG, Amerkhanov ZG (1989) Regulation of the rate of respiration and oxidative phosphorylation in liver mitochondria from hibernating ground squirrels, Citellus undulates. Comp Biochem Physiol 94B:537–541

    Google Scholar 

  • Fraser KPP, Houlihan DF, Lutz PL, Leone-Kabler S, Manuel L, Brechin JG (2001) Complete suppression of protein synthesis during anoxia with no post-anoxia protein synthesis debt in the red-eared slider turtle Trachemys scripta elegans. J Exp Biol 204:4353–4360

    CAS  PubMed  Google Scholar 

  • Garlick PJ, McNurlan MA, Preedy VR (1980) A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of [3H] phenylalanine. Biochem J 192:719–723

    CAS  PubMed  Google Scholar 

  • Gerasimova NS, Steklova IV, Tuuminen T (1989) Fluorometric method for phenylalanine microplate assay adapted for phenylketonuria screening. Clin Chem 35:2112–2115

    CAS  PubMed  Google Scholar 

  • Green JM, Farwell M (1971) Winter habits of the cunner, Tautogolabrus adspersus (Walbaum 1792), in Newfoundland. Can J Zool 49:1497–1499

    Article  Google Scholar 

  • Guppy M (2004) The biochemistry of metabolic depression: a history of perceptions. Comp Biochem Physiol 139B:435–442

    CAS  Google Scholar 

  • Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 77:1–40

    Article  Google Scholar 

  • Guppy M, Fuery CJ, Flanigan JE (1994) Biochemical principles of metabolic depression. Comp Biochem Physiol 109B:175–189

    CAS  Google Scholar 

  • Hand SC, Hardewig I (1996) Downregulation of cellular metabolism during environmental stress: mechanisms and implications. Annu Rev Physiol 58:539–563

    Article  CAS  PubMed  Google Scholar 

  • Haugaard N, Irving L (1943) The influence of temperature upon the oxygen consumption of the cunner (Tautogolabrus adspersus Walbaum) in summer and in winter. J Cell Comp Physiol 21:19–26

    Article  Google Scholar 

  • Hochachka PW, Lutz PL (2001) Mechanism, origin and evolution of anoxia tolerance in animals. Comp Biochem Physiol 130B:435–459

    CAS  Google Scholar 

  • King TE (1967) Preparation of succinate dehydrogenase and reconstruction of succinate oxidase. In: Pullman ME, Estabrook RW (eds) Methods in enzymology, vol 10. Academic Press, New York, pp 322–331

    Google Scholar 

  • Kwast KE, Hand SC (1993) Regulatory features of protein synthesis in isolated mitochondria from Artemia embryos. Am J Physiol Regul Integr Comp Physiol 265:R1238–R1246

    CAS  Google Scholar 

  • Kwast KE, Hand SC (1996a) Oxygen and pH regulation of protein synthesis in mitochondria from Artemia franciscana embryos. Biochem J 313:207–214

    CAS  PubMed  Google Scholar 

  • Kwast KE, Hand SC (1996b) Acute depression of mitochondrial protein synthesis during anoxia. J Biol Chem 271:7313–7319

    Article  CAS  PubMed  Google Scholar 

  • Lewis JM, Driedzic WR (2007) Tissue specific changes in protein synthesis associated with seasonal metabolic depression and recovery in the north temperature labrid, Tautogolabrus adspersus. Am J Physiol Regul Integr Comp Physiol 293:R474–R481

    CAS  PubMed  Google Scholar 

  • Lewis JM, Costa I, Val AL, Almeida-Val VMF, Gamperl AK, Driedzic WR (2007) Responses to hypoxia and recovery: repayment of oxygen debt is not associated with compensatory protein synthesis in the Amazonian cichlid, Astronotus ocellatus. J Exp Biol 210:1935–1943

    Article  CAS  PubMed  Google Scholar 

  • Lutz PL, Nilsson GE (1997) Contrasting strategies for anoxic brain survival—glycolysis up or down. J Exp Biol 200:411–419

    CAS  PubMed  Google Scholar 

  • Lyndon AR, Houlihan DF (1998) Gill protein turnover: costs of adaptation. Comp Biochem Physiol 119A:27–34

    CAS  Google Scholar 

  • MacCormack TJ, Driedzic WR (2007) The impact of hypoxia on in vivo glucose uptake in a hypoglycemic fish, Myoxocephalus scorpius. Am J Physiol Regul Integr Comp Phys 292:R1033–R1042

    CAS  Google Scholar 

  • Martin SL, Maniero GD, Carery C, Hand SC (1999) Reversible depression of oxygen consumption in isolated liver mitochondria during hibernation. Physiol Biochem Zool 72:255–264

    Article  CAS  PubMed  Google Scholar 

  • Matey V, Richards JG, Wang Y, Wood CM, Rogers J, Davies R, Murray BW, Du CJ, Brauner CJ (2008) The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii. J Exp Biol 211:1063–1074

    Article  CAS  PubMed  Google Scholar 

  • Mattisson AGM, Johansson RG, Bostrom SL (1972) The cellular localization of lactate dehydrogenase in skeletal muscle of eel (Anguilla anguilla). Comp Biochem Physiol 41B:475–482

    Google Scholar 

  • Muleme HM, Walpole AC, Staples JF (2006) Mitochondrial metabolism in hibernation: metabolic suppression, temperature effects, and substrate preferences. Physiol Biochem Zool 79:474–483

    Article  CAS  PubMed  Google Scholar 

  • Muusze B, Marcon J, van den Thillart G, Almeida-Val VMF (1998) Hypoxia tolerance of Amazon fish. Respirometry and energy metabolism of the cichlid Astronotus Ocellatus. Comp Biochem Physiol 120A:151–156

    CAS  Google Scholar 

  • Perry S (1998) Relationships between branchial chloride cells and gas transfer in freshwater fish. Comp Biochem Physiol 119A:9–16

    CAS  Google Scholar 

  • Poyton RO, McEwen JE (1996) Crosstalk between nuclear and mitochondrial genomes. Annu Rev Biochem 65:563–607

    Article  CAS  PubMed  Google Scholar 

  • Rolfe DFS, Brown CG (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758

    CAS  PubMed  Google Scholar 

  • Smith RW, Houlihan DF, Nilsson GE, Brechin JG (1996) Tissue-specific changes in protein synthesis rates in vivo during anoxia in crucian carp. Am J Physiol Regul Integr Comp Physiol 271:R897–R904

    CAS  Google Scholar 

  • Sollid J, Nilsson GE (2006) Plasticity of respiratory structures: adaptive remodeling of fish gills induced by ambient oxygen and temperature. Respir Physiol Neurobiol 154:241–251

    Article  CAS  PubMed  Google Scholar 

  • Sollid J, De Angelis P, Gundersen K, Nilsson GE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667–3673

    Article  PubMed  Google Scholar 

  • St. Pierre J, Brand MD, Boutilier RG (2000a) Metabolic depression and enhanced O2 affinity of mitochondria in hypoxic hypometabolism. Am J Physiol Regul Integr Comp Physiol 279:R1205–R1214

    CAS  PubMed  Google Scholar 

  • St. Pierre J, Brand MD, Boutilier RG (2000b) Mitochondria as ATP consumers: cellular treason in anoxia. PNAS 97:8670–8674

    Article  CAS  PubMed  Google Scholar 

  • Storey KB (1988) Suspended animation: the molecular basis of metabolic depression. Can J Zool 66:124–132

    Article  CAS  Google Scholar 

  • Storey KB (2002) Life in the slow lane: molecular mechanisms of estivation. Comp Biochem Physiol 133A:733–754

    CAS  Google Scholar 

  • Storey KB, Storey JM (2004) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev 79:207–233

    Article  PubMed  Google Scholar 

  • Storey KB, Storey JM (2007) Tribute to P.L. Lutz: putting life on ‘pause’—molecular regulation of hypometabolism. J Exp Biol 210:1700–1714

    Article  CAS  PubMed  Google Scholar 

  • Treberg JR, Hall JR, Driedzic WR (2005) Enhanced protein synthesis capacity in Atlantic cod (Gadus morhua) is associated with temperature-induced compensatory growth. Am J Physiol Regul Integr Comp Physiol 288:R205–R211

    CAS  PubMed  Google Scholar 

  • Treberg JR, Crockett EL, Driedzic WR (2006) Activation of liver carnitine palmitoyltransferase-1 and mitochondrial acetoacetyl-CoA thiolase is associated with elevated ketone body levels in the elasmobranch Squalus acanthias. Physiol Biochem Zool 79:899–908

    Article  CAS  PubMed  Google Scholar 

  • van Breukelen F, Martin SL (2001) Translational initiation is uncoupled from elongation at 18°C during mammalian hibernation. Am J Physiol Regul Integr Comp Physiol 281:R1374–R1379

    PubMed  Google Scholar 

  • van Breukelen F, Sonenberg N, Martin SL (2004) Seasonal and state-dependent changes of eIF4E and 4E-BP1 during mammalian hibernation: implications for the control of translation during torpor. Am J Physiol Regul Integr Comp Physiol 287:R349–R353

    PubMed  Google Scholar 

  • van der Meer DLM, van den Thillart GEEJM, Witte F, de Bakker MAG, Besser J, Richardson MK, Spaink HP, Leito JTD, Bagowski CP (2005) Gene expression profiling of the long-term adaptive response to hypoxia in the gills of adult zebrafish. Am J Physiol Regul Integr Comp Physiol 289:R1512–R1519

    PubMed  Google Scholar 

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Acknowledgments

This work was funded by a Natural Sciences and Engineering Research Council (NSERC) Discovery Grant to WRD, who holds the Canada Research Chair in Marine Bioscience. JML was supported by and NSERC postgraduate fellowship. The authors would like to thank the Field Services Division of the Ocean Sciences Centre for the collection of animals and would like to acknowledge the technical support of Jason Treberg and Connie Short.

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Correspondence to Johanne M. Lewis.

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Communicated by H. V. Carey.

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Lewis, J.M., Driedzic, W.R. Protein synthesis is defended in the mitochondrial fraction of gill but not heart in cunner (Tautogolabrus adspersus) exposed to acute hypoxia and hypothermia. J Comp Physiol B 180, 179–188 (2010). https://doi.org/10.1007/s00360-009-0396-7

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  • DOI: https://doi.org/10.1007/s00360-009-0396-7

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