Hypoxia Tolerance in Animals: Biology and Application

Gorr, Thomas A.; Wichmann, Daniela; Hu, Jingyu; Hermes‐Lima, Marcelo; Welker, Alexis F.; Terwilliger, Nora B.; Wren, Jodie F; Viney, Mark; Morris, Steve; Nilsson, Göran; Deten, Alexander; Soliz, Jorge; Gassmann, Max

doi:10.1086/648581

Cited by 106 publications

(59 citation statements)

References 177 publications

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“…The comparison of a hypoxia-sensitive mollusc, the bay scallop, with the better studied mammalian models (Honda et al, 2005;Gorr et al, 2010;Di Lisa et al, 2011;Kadenbach et al, 2011;Hüttemann et al, 2012;Pamenter, 2014) reveals similarities of the H/R-induced mitochondrial pathology in hypoxia-sensitive organisms, including the loss of ETS function, protein damage and collapse of the normal control over the mitochondrial OXPHOS flux. Thus, the mitochondrial OXPHOS capacity of scallops quickly and dramatically decreased during reoxygenation, as reflected in the loss of the ETS activity and mitochondrial depolarization.…”

Section: Discussion H/r-induced Mitochondrial Reorganization Correlatmentioning

confidence: 99%

Intermittent hypoxia leads to functional reorganization of mitochondria and affects cellular bioenergetics in marine molluscs

Ivanina

Nesmelova

Leamy

et al. 2016

Journal of Experimental Biology

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Fluctuations in oxygen (O 2 ) concentrations represent a major challenge to aerobic organisms and can be extremely damaging to their mitochondria. Marine intertidal molluscs are well-adapted to frequent O 2 fluctuations, yet it remains unknown how their mitochondrial functions are regulated to sustain energy metabolism and prevent cellular damage during hypoxia and reoxygenation (H/ R). We used metabolic control analysis to investigate the mechanisms of mitochondrial responses to H/R stress (18 h at <0.1% O 2 followed by 1 h of reoxygenation) using hypoxia-tolerant intertidal clams Mercenaria mercenaria and hypoxia-sensitive subtidal scallops Argopecten irradians as models. We also assessed H/R-induced changes in cellular energy balance, oxidative damage and unfolded protein response to determine the potential links between mitochondrial dysfunction and cellular injury. Mitochondrial responses to H/R in scallops strongly resembled those in other hypoxia-sensitive organisms. Exposure to hypoxia followed by reoxygenation led to a strong decrease in the substrate oxidation (SOX) and phosphorylation (PHOS) capacities as well as partial depolarization of mitochondria of scallops. Elevated mRNA expression of a reactive oxygen speciessensitive enzyme aconitase and Lon protease (responsible for degradation of oxidized mitochondrial proteins) during H/R stress was consistent with elevated levels of oxidative stress in mitochondria of scallops. In hypoxia-tolerant clams, mitochondrial SOX capacity was enhanced during hypoxia and continued rising during the first hour of reoxygenation. In both species, the mitochondrial PHOS capacity was suppressed during hypoxia, likely to prevent ATP wastage by the reverse action of F O ,F 1 -ATPase. The PHOS capacity recovered after 1 h of reoxygenation in clams but not in scallops. Compared with scallops, clams showed a greater suppression of energy-consuming processes (such as protein turnover and ion transport) during hypoxia, indicated by inactivation of the translation initiation factor EIF-2α, suppression of 26S proteasome activity and a dramatic decrease in the activity of Na + /K + -ATPase. The steady-state levels of adenylates were preserved during H/R exposure and AMP-dependent protein kinase was not activated in either species, indicating that the H/R exposure did not lead to severe energy deficiency. Taken together, our findings suggest that mitochondrial reorganizations sustaining high oxidative phosphorylation flux during recovery, combined with the ability to suppress ATP-demanding cellular functions during hypoxia, may contribute to high resilience of clams to H/R stress and help maintain energy homeostasis during frequent H/R cycles in the intertidal zone.

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Section: Discussion H/r-induced Mitochondrial Reorganization Correlatmentioning

confidence: 99%

Intermittent hypoxia leads to functional reorganization of mitochondria and affects cellular bioenergetics in marine molluscs

Ivanina

Nesmelova

Leamy

et al. 2016

Journal of Experimental Biology

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“…This pattern of vertical distribution in response to the pressure exposure may represent a form of behavioural homeostasis (Johnson et al, 1992) in which the shrimp are actively seeking lower pressures (shallower waters) to counteract the negative physiological effects of the increased pressure exposure. Behavioural homeostasis has been shown in marine ectotherms in response to hypoxia (Gorr et al, 2010), whereby organisms actively seek cooler water where oxygen saturation is higher because of the temperature effect. Behavioural homeostasis is a whole-organism response to a stressor such as pressure, which, if successful, will have effects on other aspects of the stress response, thus negating the need for a pronounced CSR.…”

Section: Discussionmentioning

confidence: 99%

Characterising multi-level effects of an acute pressure exposure on a shallow-water invertebrate: insights into the kinetics and hierarchy of the stress response

Morris

Thatje

Ravaux

et al. 2015

Journal of Experimental Biology

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Hydrostatic pressure is an important, ubiquitous, environmental variable of particular relevance in the marine environment. However, it is widely overlooked despite recent evidence that some marine ectotherms may be demonstrating climate-driven bathymetric range shifts. Wide-ranging effects of increased hydrostatic pressure have been observed from the molecular through to the behavioural level. Still, no study has simultaneously examined these multiple levels of organisation in a single experiment in order to understand the kinetics, hierarchy and interconnected nature of such responses during an acute exposure, and over a subsequent recovery period. Here, we quantify the transcription of a set of previously characterised genes during and after acute pressure exposure in adults of the shrimp Palaemonetes varians. Further, we perform respiratory rate and behavioural analysis over the same period. Increases in expression of genes associated with stress and metabolism were observed during and after high-pressure exposure. Respiratory rate increased during exposure and into the recovery period. Finally, differential behaviour was observed under elevated hydrostatic pressure in comparison to ambient pressure. Characterising generalised responses to acute elevated pressure is a vital precursor to longer-term, acclimation-based pressure studies. Results provide a novel insight into what we term the overall stress response (OSR) to elevated pressure; a concept that we suggest to be applicable to other environmental stressors. We highlight the importance of considering more than a single component of the stress response in physiological studies, particularly in an era where environmental multi-stressor studies are proliferating.

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“…The scope of these contingency plans is highly variable from a few short minutes of survival in highly active mammalian tissues such as the brain and the heart to extended (weeks-months) anoxemia that is tolerated by lower vertebrates such as the crucian carp and turtle (48). Initial sensing and coping mechanisms reflected in response to ischemia/reperfusion injury and pre-and postconditioning are only briefly discussed here in the context of acute O 2 sensing.…”

Section: O 2 -Sensing Tissuesmentioning

confidence: 99%

Hydrogen sulfide as an oxygen sensor

Olson

2013

Clinical Chemistry and Laboratory Medicine

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Significance: Although oxygen (O 2 )-sensing cells and tissues have been known for decades, the identity of the O 2 -sensing mechanism has remained elusive. Evidence is accumulating that O 2 -dependent metabolism of hydrogen sulfide (H 2 S) is this enigmatic O 2 sensor. Recent Advances: The elucidation of biochemical pathways involved in H 2 S synthesis and metabolism have shown that reciprocal H 2 S/O 2 interactions have been inexorably linked throughout eukaryotic evolution; there are multiple foci by which O 2 controls H 2 S inactivation, and the effects of H 2 S on downstream signaling events are consistent with those activated by hypoxia. H 2 S-mediated O 2 sensing has been demonstrated in a variety of O 2 -sensing tissues in vertebrate cardiovascular and respiratory systems, including smooth muscle in systemic and respiratory blood vessels and airways, carotid body, adrenal medulla, and other peripheral as well as central chemoreceptors. Critical Issues: Information is now needed on the intracellular location and stoichometry of these signaling processes and how and which downstream effectors are activated by H 2 S and its metabolites. Future Directions: Development of specific inhibitors of H 2 S metabolism and effector activation as well as cellular organelle-targeted compounds that release H 2 S in a timeor environmentally controlled way will not only enhance our understanding of this signaling process but also provide direction for future therapeutic applications. Antioxid. Redox Signal. 22, 377-397.

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Hypoxia Tolerance in Animals: Biology and Application

Cited by 106 publications

References 177 publications

Intermittent hypoxia leads to functional reorganization of mitochondria and affects cellular bioenergetics in marine molluscs

Intermittent hypoxia leads to functional reorganization of mitochondria and affects cellular bioenergetics in marine molluscs

Characterising multi-level effects of an acute pressure exposure on a shallow-water invertebrate: insights into the kinetics and hierarchy of the stress response

Hydrogen sulfide as an oxygen sensor

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