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Journal of Comparative Physiology B

, Volume 182, Issue 1, pp 91–100 | Cite as

A radical approach to beating hypoxia: depressed free radical release from heart fibres of the hypoxia-tolerant epaulette shark (Hemiscyllum ocellatum)

  • Anthony J. R. Hickey
  • Gillian M. C. Renshaw
  • Ben Speers-Roesch
  • Jeffrey G. Richards
  • Yuxiang Wang
  • Anthony P. Farrell
  • Colin J. Brauner
Original Paper

Abstract

Hypoxia and warm ischemia are primary concerns in ischemic heart disease and transplant and trauma. Hypoxia impacts tissue ATP supply and can induce mitochondrial dysfunction that elevates reactive species release. The epaulette shark, Hemiscyllum ocellatum, is remarkably tolerant of severe hypoxia at temperatures up to 34°C, and therefore provides a valuable model to study warm hypoxia tolerance. Mitochondrial function was tested in saponin permeabilised ventricle fibres using high-resolution respirometry coupled with purpose-built fluorospectrometers. Ventricular mitochondrial function, stability and reactive species production of the epaulette shark was compared with that of the hypoxia-sensitive shovelnose ray, Aptychotrema rostrata. Fibres were prepared from each species acclimated to normoxic water conditions, or following a 2 h, acute hypoxic exposure at levels representing 40% of each species’ critical oxygen tension. Although mitochondrial respiratory fluxes for normoxia-acclimated animals were similar for both species, reactive species production in the epaulette shark was approximately half that of the shovelnose ray under normoxic conditions, even when normalised to tissue oxidative phosphorylation flux. The hypoxia-sensitive shovelnose ray halved oxidative phosphorylation flux and cytochrome c oxidase flux was depressed by 34% following hypoxic stress. In contrast, oxidative phosphorylation flux of the epaulette shark ventricular fibres isolated from acute hypoxia exposed the animals remained similar to those from normoxia-acclimated animals. However, uncoupling of respiration revealed depressed electron transport systems in both species following hypoxia exposure. Overall, the epaulette shark ventricular mitochondria showed greater oxidative phosphorylation stability and lower reactive species outputs with hypoxic exposure, and this may protect cardiac bioenergetic function in hypoxic tropical waters.

Keywords

Mitochondria Hypoxia tolerance Shark 

Abbreviations

CI

Complex I

CII

Complex II

CCO

Cytochrome c oxidase

ETS

Electron Transport System

OXP

Oxidative phosphorylation system

NO

Nitric oxide

RCR

Respiratory control ratio

RS

Reactive species

%RS/O2

The percentage of reactive species relative to oxygen consumed

Notes

Acknowledgments

This research was supported by Natural Science and Engineering Research Council Discovery grants to JGR, YW, APF and CJB. CJB was supported by a Killam Faculty Research Fellowship. AJRH was supported by the University of Auckland Early Career Excellence Award. BS-R was supported by a Journal of Experimental Biology Travelling Fellowship from the Company of Biologists, a Comparative Physiology and Biochemistry Student Research Grant from the Canadian Society of Zoologists, and a Graduate Travel Award from the Department of Zoology, University of British Columbia. We thank Kevin and Kathy Townsend at the Moreton Bay Research Station for all their efforts during our stay.

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Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Anthony J. R. Hickey
    • 1
  • Gillian M. C. Renshaw
    • 2
  • Ben Speers-Roesch
    • 3
  • Jeffrey G. Richards
    • 3
  • Yuxiang Wang
    • 4
  • Anthony P. Farrell
    • 3
    • 5
  • Colin J. Brauner
    • 3
  1. 1.School of Biological SciencesThe University of AucklandAucklandNew Zealand
  2. 2.Hypoxia and Ischemia Research Unit, School of Physiotherapy and Exercise ScienceGriffith UniversityBrisbaneAustralia
  3. 3.Department of ZoologyUniversity of British ColumbiaVancouverCanada
  4. 4.Department of BiologyQueens UniversityKingstonCanada
  5. 5.Faculty of Land and Food SystemsUniversity of British ColumbiaVancouverCanada

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