Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function

Kültz, Dietmar

doi:10.1242/jeb.00549

Cited by 304 publications

(265 citation statements)

References 38 publications

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“…In a short‐term response to stress, an upregulation in CSR proteins (or a transcriptomic upregulation of genes coding for them) is expected (Tomanek & Somero, 2000; Kültz, 2003), as has been reported in numerous marine organisms (Lauritano, Procaccini, & Ianora, 2012; Tomanek, 2014; Huth & Place, 2016). However, several studies show both up‐ and downregulation of CSR‐related genes in response to a range of abiotic stressors (Anderson et al., 2015; Goncalves et al., 2016).…”

Section: Discussionmentioning

confidence: 90%

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water

Bailey

Wit

Thor

et al. 2017

Ecology and Evolution

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Ocean acidification is the increase in seawater pCO 2 due to the uptake of atmospheric anthropogenic CO 2, with the largest changes predicted to occur in the Arctic seas. For some marine organisms, this change in pCO 2, and associated decrease in pH, represents a climate change‐related stressor. In this study, we investigated the gene expression patterns of nauplii of the Arctic copepod Calanus glacialis cultured at low pH levels. We have previously shown that organismal‐level performance (development, growth, respiration) of C. glacialis nauplii is unaffected by low pH. Here, we investigated the molecular‐level response to lowered pH in order to elucidate the physiological processes involved in this tolerance. Nauplii from wild‐caught C. glacialis were cultured at four pH levels (8.05, 7.9, 7.7, 7.5). At stage N6, mRNA was extracted and sequenced using RNA‐seq. The physiological functionality of the proteins identified was categorized using Gene Ontology and KEGG pathways. We found that the expression of 151 contigs varied significantly with pH on a continuous scale (93% downregulated with decreasing pH). Gene set enrichment analysis revealed that, of the processes downregulated, many were components of the universal cellular stress response, including DNA repair, redox regulation, protein folding, and proteolysis. Sodium:proton antiporters were among the processes significantly upregulated, indicating that these ion pumps were involved in maintaining cellular pH homeostasis. C. glacialis significantly alters its gene expression at low pH, although they maintain normal larval development. Understanding what confers tolerance to some species will support our ability to predict the effects of future ocean acidification on marine organisms.

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Section: Discussionmentioning

confidence: 90%

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water

Bailey

Wit

Thor

et al. 2017

Ecology and Evolution

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“…3 Despite the global importance of coral reef ecosystems, the cellular mechanisms leading to bleaching remain largely unresolved and a recent review highlighted the need for a better understanding of the process at sublethal temperatures. 4 Kü ltz 5 has recently argued that the cellular stress response is so well conserved because it represents a rapid, transient mechanism for promoting tolerance to temporary environmental extremes, thereby allowing for slower, stressorspecific mechanisms to be upregulated. Programmed cell death (PCD), or apoptosis, is recognised as an important part of the stress response.…”

Section: Introductionmentioning

confidence: 99%

“…Once stabilisation and repair mechanisms have been exhausted or overwhelmed, PCD may mitigate further damage by preventing widespread inflammation and genetic instability. 5 Given this relationship, it is perhaps not surprising that heat shock (stress) proteins are implicated as regulators, usually inhibitors, of PCD and necrosis. [6][7][8] Conversely, reactive oxygen species (ROS), or the stress and cellular damage they cause, are known triggers of PCD.…”

Section: Introductionmentioning

confidence: 99%

Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration

et al. 2004

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Bleaching of reef building corals and other symbiotic cnidarians due to the loss of their dinoflagellate algal symbionts ( ¼ zooxanthellae), and/or their photosynthetic pigments, is a common sign of environmental stress. Mass bleaching events are becoming an increasingly important cause of mortality and reef degradation on a global scale, linked by many to global climate change. However, the cellular mechanisms of stress-induced bleaching remain largely unresolved. In this study, the frequency of apoptosislike and necrosis-like cell death was determined in the symbiotic sea anemone Aiptasia sp. using criteria that had previously been validated for this symbiosis as indicators of programmed cell death (PCD) and necrosis. Results indicate that PCD and necrosis occur simultaneously in both host tissues and zooxanthellae subject to environmentally relevant doses of heat stress. Frequency of PCD in the anemone endoderm increased within minutes of treatment. Peak rates of apoptosis-like cell death in the host were coincident with the timing of loss of zooxanthellae during bleaching. The proportion of apoptosis-like host cells subsequently declined while cell necrosis increased. In the zooxanthellae, both apoptosis-like and necrosis-like activity increased throughout the duration of the experiment (6 days), dependent on temperature dose. A stress-mediated PCD pathway is an important part of the thermal stress response in the sea anemone symbiosis and this study suggests that PCD may play different roles in different components of the symbiosis during bleaching.

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“…total SOD activity versus individual MnSOD and CuZnSOD quantiWcation), the duration of estivation (which varies from »15 days to 180 days), or they may simply reXect diVerences in how particular species adapt to the metabolic stress of estivation. Antioxidant enzymes represent only one facet of the cellular adaptive response that can be recruited in the adaptation to environmental stress (Gracey and Cossins 2003;Kültz 2003).…”

mentioning

confidence: 99%

“…Oxidative stress resistance is often a component of 'multiplex' stress resistance (Miller 2009) that does not appear to be mediated simply by upregulation of antioxidant enzyme levels. Rather, the mechanisms by which multiplex stress resistance is achieved are likely to include a wide range of molecular adaptations (see, for example, Kültz 2003), with speciWc adaptations diVering between species, tissue, and physiological state.…”

mentioning

confidence: 99%

Upregulation of intracellular antioxidant enzymes in brain and heart during estivation in the African lungfish Protopterus dolloi

Page¹,

Salway²,

et al. 2009

J Comp Physiol B

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The African slender lungfish, Protopterus dolloi, is highly adapted to withstand periods of drought by secreting a mucous cocoon and estivating for periods of months to years. Estivation is similar to the diapause and hibernation of other animal species in that it is characterized by negligible activity and a profoundly depressed metabolic rate. As is typically observed in quiescent states, estivating P. dolloi are resistant to environmental stresses. We tested the hypothesis that P. dolloi enhances stress resistance during estivation by upregulating intracellular antioxidant defences in brain and heart tissues. We found that most of the major intracellular antioxidant enzymes, including the mitochondrial superoxide dismutase, cytosolic superoxide dismutase, catalase, glutathione peroxidase and glutathione reductase, were upregulated in brain tissue of lungfish that had estivated for 60 days. Several of these enzymes were also elevated in heart tissue of estivators. These changes wer... Abstract The African slender lungWsh, Protopterus dolloi, is highly adapted to withstand periods of drought by secreting a mucous cocoon and estivating for periods of months to years. Estivation is similar to the diapause and hibernation of other animal species in that it is characterized by negligible activity and a profoundly depressed metabolic rate. As is typically observed in quiescent states, estivating P. dolloi are resistant to environmental stresses. We tested the hypothesis that P. dolloi enhances stress resistance during estivation by upregulating intracellular antioxidant defences in brain and heart tissues. We found that most of the major intracellular antioxidant enzymes, including the mitochondrial superoxide dismutase, cytosolic superoxide dismutase, catalase, glutathione peroxidase and glutathione reductase, were upregulated in brain tissue of lungWsh that had estivated for 60 days. Several of these enzymes were also elevated in heart tissue of estivators. These changes were not due to food deprivation, as they did not occur in a group of Wsh that were deprived of food but maintained in water for the same period of time. We found little evidence of tissue oxidative damage in estivators. Products of lipid peroxidation (4-hydroxynonenal adducts) and oxidative protein damage (carbonylation) were similar in estivating and control lungWsh. However, protein nitrotyrosine levels were elevated in brain tissue of estivators. Taken together, these data indicate that estivating P. dolloi have enhanced oxidative stress resistance in brain and heart due to a signiWcant upregulation of intracellular antioxidant capacity.

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Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function

Cited by 304 publications

References 38 publications

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water

Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration

Upregulation of intracellular antioxidant enzymes in brain and heart during estivation in the African lungfish Protopterus dolloi

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Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function

Cited by 304 publications

References 38 publications

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO2‐acidified sea water

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO2‐acidified sea water

Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration

Upregulation of intracellular antioxidant enzymes in brain and heart during estivation in the African lungfish Protopterus dolloi

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Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water