Skip to main content
Log in

Mitochondria from anoxia-tolerant animals reveal common strategies to survive without oxygen

  • Review
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

The mitochondrion plays a critical role in the development of Oxygen (O2)-related diseases. While research has predominantly focused on hypoxia-sensitive mammals as surrogates for humans, the use of animals which have naturally evolved anoxia tolerance has been largely ignored. Remarkably, some animals can live in the complete absence of O2 for days, months and even years, but surprisingly little is currently known about mitochondrial function in these species. In contrast to mammals, mitochondrial function in anoxia-tolerant animals is relatively insensitive to in vitro anoxia and reoxygenation, suggesting that anoxia tolerance transcends to the level of the mitochondria. Furthermore, long-term anoxia is associated with marked changes in the intrinsic properties of the mitochondria from these species, which may afford protection against anoxia-related damage. In the present review, we highlight some of the strategies anoxia-tolerant animals possess to preserve mitochondrial function in the absence of O2. Specifically, we review mitochondrial Ca2+ regulation, proton leak, redox signaling and mitochondrial permeability transition, in phylogenetically diverse groups of anoxia-tolerant animals. From the strategies they employ, these species emerge as model organisms to illuminate novel interventions to mitigate O2-related mitochondrial dysfunction in humans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adiele RC, Stevens D, Kamunde C (2012) Features of cadmium and calcium uptake and toxicity in rainbow trout (Oncorhynchus mykiss) mitochondria. Toxicol In Vitro 26:164–173

    PubMed  CAS  Google Scholar 

  • Arnaiz SL, Coronel MF, Boveris A (1999) Nitric oxide, superoxide, and hydrogen peroxide production in brain mitochondria after haloperidol treatment. Nitric Oxide 3:235–243

    PubMed  CAS  Google Scholar 

  • Ascensao A, Magalhaes J, Soares JM, Ferreira R, Neuparth MJ, Marques F, Oliveira PJ, Duarte JA (2006) Endurance training limits the functional alterations of rat heart mitochondria submitted to in vitro anoxia-reoxygenation. Int J Cardiol 109:169–178

    PubMed  Google Scholar 

  • Azzolin L, Basso E, Argenton F, Bernardi P (2010) Mitochondrial Ca2+ transport and permeability transition in zebrafish (Danio rerio). Biochim et Biophys Acta 1797:1775–1779

    CAS  Google Scholar 

  • Becker LB, vanden Hoek TL, Shao Z-H, Li C-Q, Schumacker PT (1999) Generation of superoxide in cardiomyocytes during ischemia before reperfusion. Am J Physiol 277:H2240–H2246

    PubMed  CAS  Google Scholar 

  • Bernardi P (1999) Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 79:1127–1155

    PubMed  CAS  Google Scholar 

  • Bickler PE (1992) Cerebral anoxia tolerance in turtles: regulation of intracellular calcium and pH. Am J Physiol 263:R1298–R1302

    PubMed  CAS  Google Scholar 

  • Bickler PE, Buck LT (1998) Adaptations of vertebrate neurons to hypoxia and anoxia: maintaining critical Ca2+ concentrations. J Exp Biol 201:1141–1152

    PubMed  CAS  Google Scholar 

  • Bickler PE, Buck LT (2007) Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69:145–170

    PubMed  CAS  Google Scholar 

  • Bickler PE, Donohoe PH, Buck LT (2000) Hypoxia-induced silencing of NMDA receptors in turtle neurons. J Neurosci 20:3522–3528

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Boveris A, Cadenas E (2000) Mitochondrial production of hydrogen peroxide regulation by nitric oxide and the role of ubisemiquinone. IUBMB Life 50:245–250

    PubMed  CAS  Google Scholar 

  • Brand MD, Nicholls DG (2011) Assessing mitochondrial dysfunction in cells. Biochem J 435:297–312

    PubMed Central  PubMed  CAS  Google Scholar 

  • Brenner C, Moulin M (2012) Physiological roles of the permeability transition pore. Circ Res 111:1237–1247

    PubMed  CAS  Google Scholar 

  • 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 B 119:325–334

    PubMed  CAS  Google Scholar 

  • Buck L, Hogg DWR, Rodgers-Garlick C, Pamenter ME (2012) Oxygen sensitive synaptic neurotransmission in anoxia-tolerant turtle cerebrocortex. In: Nurse CA, Gonzalez C, Peers C, Prabhakar N (eds) Arterial chemoreception. Springer, Netherlands, pp 71–79

    Google Scholar 

  • Burwell LS, Nadtochiy SM, Brookes PS (2009) Cardioprotection by metabolic shut-down and gradual wake-up. J Mol Cell Cardiol 46:804–810

    PubMed Central  PubMed  CAS  Google Scholar 

  • Casey TM, Pakay JL, Guppy M, Arthur PG (2002) Hypoxia causes downregulation of protein and RNA synthesis in noncontracting mammalian cardiomyocytes. Circ Res 90:777–783

    PubMed  CAS  Google Scholar 

  • Chen Q, Moghaddas S, Hoppel CL, Lesnefsky EJ (2008) Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria. Am J Physiol 294:C460–C466

    CAS  Google Scholar 

  • Clegg J (1997) Embryos of Artemia franciscana survive 4 years of continuous anoxia: the case for complete metabolic rate depression. J Exp Biol 200:467–475

    PubMed  Google Scholar 

  • Cross JL, Meloni BP, Bakker AJ, Lee S, Knuckey NW (2010) Modes of neuronal calcium entry and homeostasis following cerebral Ischemia. Stroke Res Treat 2010:316862

    PubMed Central  PubMed  CAS  Google Scholar 

  • Cunha FM, Caldeira da Silva CC, Cerqueira FM, Kowaltowski AJ (2011) Mild mitochondrial uncoupling as a therapeutic strategy. Curr Drug Targets 12:783–789

    Google Scholar 

  • Davidson SM, Duchen MR (2006) Effects of NO on mitochondrial function in cardiomyocytes: pathophysiological relevance. Cardiovasc Res 71:10–21

    PubMed  CAS  Google Scholar 

  • De Zwaan A, Putzer V (1985) Metabolic adaptations of intertidal invertebrates to environmental hypoxia (a comparison of environmental anoxia to exercise anoxia). Symp Soc Exp Biol 39:33–62

    PubMed  Google Scholar 

  • Diaz RJ, Breitburg DL (2009) The hypoxic environment. In: Richards JG, Farrell AP, Brauner CJ (eds) Fish physiology. Elsevier, San Diego, pp 2–17

    Google Scholar 

  • Divakaruni AS, Brand MD (2011) The regulation and physiology of mitochondrial proton leak. Physiology 26:192–205

    PubMed  CAS  Google Scholar 

  • Du G, Mouithys-Mickalad A, Sluse FE (1998) Generation of superoxide anion by mitochondria and impairment of their functions during anoxia and reoxygenation in vitro. Free Radic Biol Med 25:1066–1074

    PubMed  CAS  Google Scholar 

  • Duerr J, Podrabsky J (2010) Mitochondrial physiology of diapausing and developing embryos of the annual killifish Austrofundulus limnaeus: implications for extreme anoxia tolerance. J Comp Physiol B 180:991–1003

    PubMed  Google Scholar 

  • Faccenda D, Campanella M (2012) Molecular regulation of the mitochondrial F1Fo-ATPsynthase: physiological and pathological significance of the inhibitory factor 1 (IF1). Int J Cell Biol 2012:367934

    PubMed Central  PubMed  Google Scholar 

  • Fiskum G, Murphy AN, Beal MF (1999) Mitochondria in neurodegeneration: acute ischemia and chronic neurodegenerative diseases. J Cereb Blood Flow Metab 19:351–369

    PubMed  CAS  Google Scholar 

  • Friberg H, Connern C, Halestrap AP, Wieloch T (1999) Differences in the activation of the mitochondrial permeability transition among brain regions in the rat correlate with selective vulnerability. J Neurochem 72:2488–2497

    PubMed  CAS  Google Scholar 

  • Galli GLJ, Lau GY, Richards JG (2013) Beating oxygen: chronic anoxia exposure reduces mitochondrial F1FO-ATPase activity in turtle (Trachemys scripta) heart. J Exp Biol 216:3283–3293

    PubMed  CAS  Google Scholar 

  • Garcia-Dorado D, Ruiz-Meana M, Inserte J, Rodriguez-Sinovas A, Piper HM (2012) Calcium-mediated cell death during myocardial reperfusion. Cardiovasc Res 94:168–180

    PubMed  CAS  Google Scholar 

  • Garlid KD, Costa ADT, Quinlan CL, Pierre SV, Dos Santos P (2009) Cardioprotective signaling to mitochondria. J Mol Cell Cardiol 46:858–866

    PubMed Central  PubMed  CAS  Google Scholar 

  • Gledhill JR, Walker JE (2006) Inhibitors of the catalytic domain of mitochondrial ATP synthase. Biochem Soc Trans 34:989–992

    PubMed  CAS  Google Scholar 

  • Gouriou Y, Demaurex N, Bijlenga P, De Marchi U (2011) Mitochondrial calcium handling during ischemia-induced cell death in neurons. Biochimie 93:2060–2067

    PubMed  CAS  Google Scholar 

  • Griffiths E (2012) Mitochondria and heart disease. In: Scatena R, Bottoni P, Giardina B (eds) Advances in mitochondrial medicine. Springer, Netherlands, pp 249–267

    Google Scholar 

  • Gross GJ, Auchampach JA (2007) Reperfusion injury: does it exist? J Mol Cell Cardiol 42:12–18

    PubMed Central  PubMed  CAS  Google Scholar 

  • Halestrap AP, Clarke SJ, Javadov SA (2004) Mitochondrial permeability transition pore opening during myocardial reperfusion—a target for cardioprotection. Cardiovasc Res 61:372–385

    PubMed  CAS  Google Scholar 

  • Hand SC, Menze MA (2008) Mitochondria in energy-limited states: mechanisms that blunt the signaling of cell death. J Exp Biol 211:1829–1840

    PubMed  CAS  Google Scholar 

  • Hawrysh PJ, Buck LT (2013) Anoxia-mediated calcium release through the mitochondrial permeability transition pore silences NMDA receptor currents in turtle neurons. J Exp Biol 216:4375–4387

    PubMed  CAS  Google Scholar 

  • Hickey AR, Renshaw GC, Speers-Roesch B, Richards J, Wang Y, Farrell A, Brauner C (2012) 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 182:91–100

    PubMed  Google Scholar 

  • Hochachka PW (1986) Metabolic arrest. Int Care Med 12:127–133

    CAS  Google Scholar 

  • Hochachka PW, Buck LT, Doll CJ, Land SC (1996) Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93:9493–9498

    PubMed Central  PubMed  CAS  Google Scholar 

  • Holman JD, Hand SC (2009) Metabolic depression is delayed and mitochondrial impairment averted during prolonged anoxia in the ghost shrimp, Lepidophthalmus louisianensis (Schmitt, 1935). J Exp Mar Bio Ecol 376:85–93

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hunter DR, Haworth RA (1979) The Ca2+-induced membrane transition in mitochondria: III. transitional Ca2+ release. Arch Biochem Biophys 195:468–477

    PubMed  CAS  Google Scholar 

  • Hunter DR, Haworth RA, Southard JH (1976) Relationship between configuration, function, and permeability in calcium-treated mitochondria. J Biol Chem 251:5069–5077

    PubMed  CAS  Google Scholar 

  • Jackson DC (2000) Living without oxygen: lessons from the freshwater turtle. Comp Biochem Physiol A 125:299–315

    CAS  Google Scholar 

  • Jackson DC (2002) Hibernating without oxygen: physiological adaptations of the painted turtle. J Physiol 543:731–737

    PubMed Central  PubMed  CAS  Google Scholar 

  • Jensen FB, Hansen MN, Montesanti G, Wang T (2014) Nitric oxide metabolites during anoxia and reoxygenation in the anoxia-tolerant vertebrate, Trachemys scripta. J Exp Biol 217:1477–9145

    Google Scholar 

  • Kane LA, Van Eyk JE (2009) Post-translational modifications of ATP synthase in the heart: biology and function. J Bioenerg Biomembr 41:145–150

    PubMed Central  PubMed  CAS  Google Scholar 

  • Kelly RF, Sluiter W, McFalls EO (2008) Hibernating myocardium. Circ Res 102:3–5

    PubMed  CAS  Google Scholar 

  • Kesaraju S, Schmidt-Kastner R, Prentice HM, Milton SL (2009) Modulation of stress proteins and apoptotic regulators in the anoxia tolerant turtle brain. J Neurochem 109:1413–1426

    PubMed Central  PubMed  CAS  Google Scholar 

  • Krivoruchko A, Storey KB (2010) Forever young: mechanisms of natural anoxia tolerance and potential links to longevity. Oxid Med Cell Longev 3:186–198

    Google Scholar 

  • Kurochkin IO, Ivanina AV, Eilers S, Downs CA, May LA, Sokolova IM (2009) Cadmium affects metabolic responses to prolonged anoxia and reoxygenation in eastern oysters (Crassostrea virginica). Am J Physiol 297:R1262–R1272

    CAS  Google Scholar 

  • Kwast KE, Shapiro JI, Rees BB, Hand SC (1995) Oxidative phosphorylation and the realkalinization of intracellular pH during recovery from anoxia in Artemia franciscana embryos. Biochimica et Biophys Acta 1232:5–12

    Google Scholar 

  • Lesnefsky EJ, Chen Q, Moghaddas S, Hassan MO, Tandler B, Hoppel CL (2004) Blockade of electron transport during ischemia protects cardiac mitochondria. J Biol Chem 279:47961–47967

    PubMed  CAS  Google Scholar 

  • Leveelahti L, Rytkönen K, Renshaw GC, Nikinmaa M (2014) Revisiting redox-active antioxidant defenses in response to hypoxic challenge in both hypoxia-tolerant and hypoxia-sensitive fish species. Fish Physiol Biochem 40:183–191

    Google Scholar 

  • Lippe G, Bisetto E, Comelli M, Contessi S, Di Pancrazio F, Mavelli I (2009) Mitochondrial and cell-surface F0F1ATPsynthase in innate and acquired cardioprotection. J Bioenerg Biomembr 41:151–157

    PubMed  CAS  Google Scholar 

  • Lushchak VI, Lushchak LP, Mota AA, Hermes-Lima M (2001) Oxidative stress and antioxidant defenses in goldfish Carassius auratus during anoxia and reoxygenation. Am J Physiol 280:R100–R107

    CAS  Google Scholar 

  • Lutz PL (1992) Mechanisms for anoxic survival in the vertebrate brain. Annu Rev Physiol 54:601–618

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Manzanero S, Santro T, Arumugam TV (2013) Neuronal oxidative stress in acute ischemic stroke: sources and contribution to cell injury. Neurochem Int 62:712–718

    PubMed  CAS  Google Scholar 

  • Menze MA, Hutchinson K, Laborde SM, Hand SC (2005) Mitochondrial permeability transition in the crustacean Artemia franciscana: absence of a calcium-regulated pore in the face of profound calcium storage. Am J Physiol 289:R68–R76

    CAS  Google Scholar 

  • Milerova M, Charvatova Z, Skarka L, Ostadalova I, Drahota Z, Fialova M, Ostadal B (2010) Neonatal cardiac mitochondria and ischemia/reperfusion injury. Mol Cell Biochem 335:147–153

    PubMed  CAS  Google Scholar 

  • Milton SL, Prentice HM (2007) Beyond anoxia: the physiology of metabolic downregulation and recovery in the anoxia-tolerant turtle. Comp Biochem Physiol A 147:277–290

    Google Scholar 

  • Milton SL, Nayak G, Kesaraju S, Kara L, Prentice HM (2007) Suppression of reactive oxygen species production enhances neuronal survival in vitro and in vivo in the anoxia-tolerant turtle Trachemys scripta. J Neurochem 101:993–1001

    PubMed  CAS  Google Scholar 

  • Murillo D, Kamga C, Mo L, Shiva S (2011) Nitrite as a mediator of ischemic preconditioning and cytoprotection. Nitric Oxide 25:70–80

    PubMed Central  PubMed  CAS  Google Scholar 

  • Murphy E, Steenbergen C (2008) Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 88:581–609

    PubMed Central  PubMed  CAS  Google Scholar 

  • Murphy E, Steenbergen C (2011) What makes the mitochondria a killer? Can we condition them to be less destructive? Biochim et Biophys Acta 1813:1302–1308

    CAS  Google Scholar 

  • Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124–1136

    PubMed  CAS  Google Scholar 

  • Murry CE, Richard VJ, Reimer KA, Jennings RB (1990) Ischemic preconditioning slows energy metabolism and delays ultrastructural damage during a sustained ischemic episode. Circ Res 66:913–931

    PubMed  CAS  Google Scholar 

  • Myers GS (1952) Annual fishes. Aquarium J 23:125–141

    Google Scholar 

  • Nadtochiy SM, Tompkins AJ, Brookes PS (2006) Different mechanisms of mitochondrial proton leak in ischaemia/reperfusion injury and preconditioning: implications for pathology and cardioprotection. Biochem J 395:611–618

    PubMed Central  PubMed  CAS  Google Scholar 

  • Nayak GH, Prentice HM, Milton SL (2011) Neuroprotective signaling pathways are modulated by adenosine in the anoxia tolerant turtle. J Cereb Blood Flow 31:467–475

    CAS  Google Scholar 

  • Nico LG, Thomerson JE (1989) Ecology, food habits and spatial interactions of Orinoco Basin annual killifish. Acta Biol Venez 12:106–120

    Google Scholar 

  • Nilsson GE, Lutz PL (2004) Anoxia tolerant brains. J Cereb Blood Flow 24:475–486

    Google Scholar 

  • Nilsson GE, Renshaw GM (2004) Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. J Exp Biol 207:3131–3139

    PubMed  CAS  Google Scholar 

  • Ostadal B, Ostadalova I, Kolar F, Charvatova Z, Netuka I (2009) Ontogenetic development of cardiac tolerance to oxygen deprivation—possible mechanisms. Phys Res 58(Suppl 2):S1–S12

    Google Scholar 

  • Ott M, Gogvadze V, Orrenius S, Zhivotovsky B (2007) Mitochondria, oxidative stress and cell death. Apoptosis Int J Program Cell Death 12:913–922

    CAS  Google Scholar 

  • Ozcan C, Holmuhamedov EL, Jahangir A, Terzic A (2001) Diazoxide protects mitochondria from anoxic injury: implications for myopreservation. J Thorac Cardiovasc Surg 121:298–306

    PubMed  CAS  Google Scholar 

  • Pagliaro P, Moro F, Tullio F, Perrelli MG, Penna C (2011) Cardioprotective pathways during reperfusion: focus on redox signaling and other modalities of cell signaling. Antioxid Redox Signal 14:833–850

    PubMed  CAS  Google Scholar 

  • Pamenter M, Richards M, Buck L (2007) Anoxia-induced changes in reactive oxygen species and cyclic nucleotides in the painted turtle. J Comp Physiol B 177:473–481

    PubMed  CAS  Google Scholar 

  • Pamenter ME, Shin DS-H, Cooray M, Buck LT (2008) Mitochondrial ATP-sensitive K+ channels regulate NMDAR activity in the cortex of the anoxic western painted turtle. J Physiol 586:1043–1058

    PubMed Central  PubMed  CAS  Google Scholar 

  • Pamenter ME, Hogg DW, Gu XQ, Buck LT, Haddad GG (2012) Painted turtle cortex is resistant to an in vitro mimic of the ischemic mammalian penumbra. J Cereb Blood Flow 32:2033–2043

    CAS  Google Scholar 

  • Papa S, Martino PL, Capitanio G, Gaballo A, De Rasmo D, Signorile A, Petruzzella V (2012) The oxidative phosphorylation system in mammalian mitochondria. Adv Exp Med Biol 942:3–37

    PubMed  CAS  Google Scholar 

  • Penna C, Perrelli MG, Pagliaro P (2013) Mitochondrial pathways, permeability transition pore, and redox signaling in cardioprotection: therapeutic implications. Antioxid Redox Signal 18:556–599

    PubMed  CAS  Google Scholar 

  • Perez-Pinzon MA, Lutz PL, Sick TJ, Rosenthal M (1997) Metabolic mechanisms of anoxia tolerance in the turtle brain. Adv Exp Med Biol 411:75–81

    PubMed  CAS  Google Scholar 

  • Pinder AW, Storey KB, Ultsch GR (1992) Environmental Biology of the Amphibia. University Chicage Press, Chicago

  • Podrabsky JE, Hand SC (1999) The bioenergetics of embryonic diapause in an annual killifish, Austrofundulus limnaeus. J Exp Biol 202(Pt 19):2567–2580

    PubMed  CAS  Google Scholar 

  • Podrabsky JE, Menze MA, Hand SC (2012) Long-term survival of anoxia despite rapid ATP decline in embryos of the annual killifish Austrofundulus limnaeus. J Exp Zool 317:524–532

    CAS  Google Scholar 

  • Quarrie R, Cramer BM, Lee DS, Steinbaugh GE, Erdahl W, Pfeiffer DR, Zweier JL, Crestanello JA (2011) Ischemic preconditioning decreases mitochondrial proton leak and reactive oxygen species production in the postischemic heart. J Surg Res 165:5–14

    PubMed Central  PubMed  CAS  Google Scholar 

  • Racay P, Tatarkova Z, Chomova M, Hatok J, Kaplan P, Dobrota D (2009) Mitochondrial calcium transport and mitochondrial dysfunction after global brain ischemia in rat hippocampus. Neurochem Res 34:1469–1478

    PubMed  CAS  Google Scholar 

  • Raedschelders K, Ansley DM, Chen DDY (2012) The cellular and molecular origin of reactive oxygen species generation during myocardial ischemia and reperfusion. Pharmacol Ther 133:230–255

    PubMed  CAS  Google Scholar 

  • Renshaw GMC, Kutek AK, Grant GD, Anoopkumar-Dukie S (2012) Forecasting elasmobranch survival following exposure to severe stressors. Comp Biochem Physiol A 162:101–112

    CAS  Google Scholar 

  • Rice ME (2011) H2O2: a dynamic neuromodulator. Neuroscience 17:389–406

    CAS  Google Scholar 

  • Rice ME, Lee EJK, Choy Y (1995) High levels of ascorbic acid, not glutathione, in the CNS of anoxia-tolerant reptiles contrasted with levels in anoxia-intolerant species. J Neurochem 64:1790–1799

    PubMed  CAS  Google Scholar 

  • Richards JG (2011) Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J Exp Biol 214:191–199

    PubMed  Google Scholar 

  • Rouslin W, Broge CW, Grupp IL (1990) ATP depletion and mitochondrial functional loss during ischemia in slow and fast heart-rate hearts. Am J Physiol 259:H1759–H1766

    PubMed  CAS  Google Scholar 

  • Sanderson TH, Reynolds CA, Kumar R, Przyklenk K, Huttemann M (2013) Molecular mechanisms of ischemia-reperfusion injury in brain: pivotal role of the mitochondrial membrane potential in reactive oxygen species generation. Mol Neurobiol 47:9–23

    PubMed Central  PubMed  CAS  Google Scholar 

  • Sandvik GK, Nilsson GE, Jensen FB (2012) Dramatic increase of nitrite levels in hearts of anoxia-exposed crucian carp supporting a role in cardioprotection. Am J Physiol 302:R468–R477

    CAS  Google Scholar 

  • Savina MV, Emel’ianova LV, Brailovskaia IV (2009) Bioenergetics of the lower vertebrates. Mechanisms of adaptations to anoxia and hypoxia. Zh Evol Biokhim Fiziol 45:157–168

    PubMed  CAS  Google Scholar 

  • Sciamanna MA, Zinkel J, Fabi AY, Lee CP (1992) Ischemic injury to rat forebrain mitochondria and cellular calcium homeostasis. Biochim Biophys Acta 1134:223–232

    PubMed  CAS  Google Scholar 

  • Shin DS, Buck LT (2003) Effect of anoxia and pharmacological anoxia on whole-cell NMDA receptor currents in cortical neurons from the Western painted turtle. Physiol Biochem Zool 76:41–51

    PubMed  CAS  Google Scholar 

  • Simpson BRC (1979) The phenology of annual killifishes. Symp Zool Soc Lond 44:243–261

    Google Scholar 

  • Smith RW, Cash P, Ellefsen S, Nilsson GE (2009) Proteomic changes in the crucian carp brain during exposure to anoxia. Proteome 9:2217–2229

    CAS  Google Scholar 

  • Sokolova IM, Evans S, Hughes FM (2004) Cadmium-induced apoptosis in oyster hemocytes involves disturbance of cellular energy balance but no mitochondrial permeability transition. J Exp Biol 207:3369–3380

    PubMed  CAS  Google Scholar 

  • Stamm C, Friehs I, Choi Y-H, Zurakowski D, McGowan FX, del Nido PJ (2003) Cytosolic calcium in the ischemic rabbit heart: assessment by pH- and temperature-adjusted rhod-2 spectrofluorometry. Cardiovasc Res 59:695–704

    PubMed  CAS  Google Scholar 

  • Stecyk JAW, Paajanen V, Farrell AP, Vornanen M (2007) Effect of temperature and prolonged anoxia exposure on electrophysiological properties of the turtle (Trachemys scripta) heart. Am J Physiol 293:R421–R437

    CAS  Google Scholar 

  • Stecyk JAW, Galli GL, Shiels HA, Farrell AP (2008) Cardiac survival in anoxia-tolerant vertebrates: an electrophysiological perspective. Comp Biochem Physiol C 148:339

    Google Scholar 

  • Stecyk JAW, Bock C, Overgaard J, Wang T, Farrell AP, Portner H-O (2009) Correlation of cardiac performance with cellular energetic components in the oxygen-deprived turtle heart. Am J Physiol 297:R756–R768

    CAS  Google Scholar 

  • Storey KB (1996) Oxidative stress: animal adaptations in nature. Brazilian J Med Biol Res 29:1715–1733

    CAS  Google Scholar 

  • Storey KB, Storey JM (1990) Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. Q Rev Biol 65:145–174

    PubMed  CAS  Google Scholar 

  • St-Pierre J, Boutilier RG (2001) Aerobic capacity of frog skeletal muscle during hibernation. Phys Biochem Zool 74:390–397

    CAS  Google Scholar 

  • St-Pierre J, Brand MD, Boutilier RG (2000a) The effect of metabolic depression on proton leak rate in mitochondria from hibernating frogs. J Exp Biol 203:1469–1476

    PubMed  CAS  Google Scholar 

  • St-Pierre J, Brand MD, Boutilier RG (2000b) Mitochondria as ATP consumers: cellular treason in anoxia. Proc Natl Acad Sci USA 97:8670–8674

    PubMed Central  PubMed  CAS  Google Scholar 

  • Stuart JA, Gillis TE, Ballantyne JS (1998) Compositional correlates of metabolic depression in the mitochondrial membranes of estivating snails. Am J Physiol 275:R1977–R1982

    PubMed  CAS  Google Scholar 

  • Sun J, Morgan M, Shen RF, Steenbergen C, Murphy E (2007) Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ Res 101:1155–1163

    PubMed  CAS  Google Scholar 

  • Szczepanek K, Chen Q, Larner AC, Lesnefsky EJ (2012) Cytoprotection by the modulation of mitochondrial electron transport chain: the emerging role of mitochondrial STAT3. Mitochondrion 12:180–189

    PubMed Central  PubMed  CAS  Google Scholar 

  • Tattersall GJ, Ultsch GR (2008) Physiological ecology of aquatic overwintering in ranid frogs. Biol Rev Camb Philos Soc 83:119–140

    PubMed  Google Scholar 

  • Toninello A, Salvi M, Colombo L (2000) The membrane permeability transition in liver mitochondria of the great green goby Zosterisessor ophiocephalus (Pallas). J Exp Biol 203:3425–3434

    PubMed  CAS  Google Scholar 

  • Van Den Thillart G, Van Den Waarde A (1991) Physiological strategies for gas exchange and metabolism, Cambridge, UK

  • van den Thillart G, van Waarde A, Muller HJ, Erkelens C, Addink A, Lugtenburg J (1989) Fish muscle energy metabolism measured by in vivo 31P-NMR during anoxia and recovery. Am J Physiol 256:R922–R929

    PubMed  Google Scholar 

  • Vanden Hoek TL, Li C, Shao Z, Schumacker PT, Becker LB (1997) Significant levels of oxidants are generated by isolated cardiomyocytes during ischemia prior to reperfusion. J Mol Cell Cardiol 29:2571–2583

    PubMed  CAS  Google Scholar 

  • Vander Heide RS, Hill ML, Reimer KA, Jennings RB (1996) Effect of reversible ischemia on the activity of the mitochondrial ATPase: relationship to ischemic preconditioning. J Mol Cell Cardiol 28:103–112

    PubMed  CAS  Google Scholar 

  • Venkataraman R, Holcomb MR, Harder R, Knollmann BC, Baudenbacher F (2012) Ratiometric imaging of calcium during ischemia-reperfusion injury in isolated mouse hearts using Fura-2. Biomed Eng 11:39

    Google Scholar 

  • Walters AM, Porter GA, Brookes PS (2012) Mitochondria as a drug target in ischemic heart disease and cardiomyopathy. Circ Res 111:1222–1236

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wasser JS, Inman KC, Arendt EA, Lawler RG, Jackson DC (1990) 31P-NMR measurements of pHi and high-energy phosphates in isolated turtle hearts during anoxia and acidosis. Am J Physiol 259:R521–R530

    PubMed  CAS  Google Scholar 

  • Willet K, Detry O, Lambermont B, Meurisse M, Defraigne JO, Sluse-Goffart C, Sluse FE (2000) Effects of cold and warm ischemia on the mitochondrial oxidative phosphorylation of swine lung. Transplantation 69:582–588

    PubMed  CAS  Google Scholar 

  • Willmore WG, Storey KB (1997) Antioxidant systems and anoxia tolerance in a freshwater turtle Trachemys scripta elegans. Mol Cell Biochem 170:177–185

    PubMed  CAS  Google Scholar 

  • Ylitalo KV, Ala-Rämi A, Liimatta EV, Peuhkurinen KJ, Hassinen IE (2000) Intracellular free calcium and mitochondrial membrane potential in ischemia/reperfusion and preconditioning. J Mol Cell Cardiol 32:1223–1238

    PubMed  CAS  Google Scholar 

  • Zini R, Morin C, Bertelli A, Bertelli AAE, Tillement J-P (2002) Resveratrol-induced limitation of dysfunction of mitochondria isolated from rat brain in an anoxia-reoxygenation model. Life Sci 71:3091–3108

    PubMed  CAS  Google Scholar 

  • Zweier JL, Wang P, Kuppusamy P (1995a) Direct measurement of nitric oxide generation in the ischemic heart using electron paramagnetic resonance spectroscopy. J Biol Chem 270:304–307

    PubMed  CAS  Google Scholar 

  • Zweier JL, Wang P, Samouilov A, Kuppusamy P (1995b) Enzyme-independent formation of nitric oxide in biological tissues. Nature Med 1:804–809

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gina L. J. Galli.

Additional information

Communicated by I.D. Hume.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Galli, G.L.J., Richards, J.G. Mitochondria from anoxia-tolerant animals reveal common strategies to survive without oxygen. J Comp Physiol B 184, 285–302 (2014). https://doi.org/10.1007/s00360-014-0806-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-014-0806-3

Keywords

Navigation