Interaction of oxygen supply, oxidative stress, and molecular defence systems during temperature stress in fishes.

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Oxygen is the essential substrate for oxidativeenergy production, but oxygen exposure has to belimited because of the damaging effects of reactiveoxygen specie (ROS). Thus, the regulation of oxygenhomeostasis within a narrow physiological range iscrucial for all aerobic life. In marine ectotherms,temperatures outside the species specific optimumrange, which is enclosed by the pejus temperatures(Tp), are supposed to cause progressively decreasingoxygen levels in body fluids and tissues, i.e.functional hypoxia. When critical temperatures (Tc)are reached, transition to anaerobic energyproduction can be observed. In my doctoral study Itested the hypothesis that temperature inducedhypoxia entails oxidative stress, i.e. unbalancedROS production. Moreover, temperature-inducedhypoxia was suggested to induce physiologicaladjustments mediated by the hypoxia inducibletranscription factor (HIF-1), i.e. the masterregulator of oxygen homeostasis.I investigated the long-term influence ofenvironmental temperature and the short-term effectof graded temperature stress on oxidative stressmarkers and the HIF-1 response in the liver ofmarine fish from different latitudes under in vivoconditions.The Antarctic zoarcid Pachycara brachycephalum, keptat control temperature (0°C) was compared to winteracclimatised (6°C) con-familial temperate Zoarcesviviparus. A highly oxidised glutathione redox ratioand elevated microsomal lipid radical formationrates in P. brachycephalum reflected the increasedsusceptibility of polar animals for oxidative stressand lipid peroxidation. However, high glutathionelevels appeared to buffer elevated lipid radicalformation in P. brachycephalum and to charge theliver tissue with a high antioxidant capacity.Consequently, oxidative damage markers were lowunder control conditions (0°C) as well as duringwarm acclimation to 5°C, when compared to thetemperate species. In line with cold enhancedoxidative stress, seasonal temperature changeswithin the natural temperature range of thetemperate Z. viviparus caused higher levels ofoxidative stress in cold acclimated specimens (6°C)collected in winter than in animals collected insummer (12°C). Thus, in the zoarcids, both coldadaptation and cold acclimatisation were associatedwith elevated oxidative stress levels.Sequence determination of the hypoxia-induciblesubunit HIF-1α from the temperate Zoarces viviparusand four cold-adapted Antarctic fishes (Zoarcidae:Pachycara brachycephalum, Notothenioidei: Trematomushansoni, T. pennellii, and Chionodraco myersi)demonstrated remarkable differences in the deducedpeptide sequences compared with mammals andnon-polar fishes. In P. brachycephalum HIF-1α theN-terminal functional proline of theoxygen-dependent degradation domain was substitutedby leucine, which is so far the first report of thisphenotype. As the HIF-1α sequences from the threenotothenioids contained both functional prolineresidues, Pro-Leu substitution cannot be considereda specific polar adaptation. Lack of one functionalproline may cause higher resistance of HIF-1α toprolyl hydroxylases and proteasomal degradation.Thus, it can only be speculated that HIF-1α isregulated mainly via transactivation and not so muchvia degradation / stabilisation in the Antarcticzoarcid.Increased HIF-1 DNA binding in 5°C acclimated P.brachycephalum versus control fish kept at 0°Cindicated that at least at the level of dimerformation HIF-1 was still functional, despitePro-Leu substitution and despite the highly oxidisedredox environment. Whereas in P. brachycephalumHIF-1 DNA binding was higher at the respectivewarmer water temperature (5°C versus. 0°C), in thetemperate Z. viviparus it was higher in cold winter(6°C) versus summer animals (12°C). In both species,HIF-1 may play a physiological role to adjust tissueoxygen supply to the tolerated temperature range.Moreover, HIF-1 DNA binding occurred at a highlyoxidised cellular redox environment in both, P.brachycephalum and winter animals of Z. viviparus.In contrast to seasonal cold acclimatisation, acutecold exposure of Z. viviparus (2 h) to 1 and 5°C ledto a more reduced cellular redox environment, whichwas accompanied by increased HIF-1 DNA binding.Oxidative damage was increased following 24 hrecovery at control temperature. Thus, effects ofacute cold exposure and recovery, i.e. cold-inducedhypoxia and reoxygenation are reminiscent ofischemia / reperfusion events well described inmammals. Acute heat exposure and recovery causedsimilar biochemical effects. However, oxidativestress markers were elevated only during earlyrecovery (8 12 h). Thus, repair of oxidativedamage may be faster following heat than followingcold stress.Moreover, acute cold and heat stress had opposingimpacts on the cellular redox balance with coldstress causing a more reduced, and critical heatstress a more oxidised cellular redox environment.The more oxidised conditions during critical heatstress seemed to interfere with the HIF response asreflected in weak HIF-1 signals in EMSA assays.HIF-1 may thus have different functions duringlong-term (seasonal) and short-term (acute stress)changes of environmental temperatures in thetemperate eelpout Z. viviparus, and the redoxpotential may be the modulating factor.

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Thesis (PhD)
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Heise, K. (2005): Interaction of oxygen supply, oxidative stress, and molecular defence systems during temperature stress in fishes. , PhD thesis, Universität Bremen.

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