Concurrent effects of cold and hyperkalaemia cause insect chilling injury

MacMillan, Heath A.; Baatrup, Erik; Overgaard, Johannes

doi:10.1098/rspb.2015.1483

Cited by 72 publications

(98 citation statements)

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“…S1). Further studies are needed to investigate these sources of variation, but here we clearly demonstrate a relationship between in vitro cell viability and polarization that reinforces the hypothesized model in which depolarization initiates an apoptotic/necrotic cascade (Hochachka, 1986;Boutilier, 2001;MacMillan et al, 2015c;Overgaard and MacMillan, 2017). These results also raise three important questions: (1) why might the V m of cold-acclimated cells be less affected by hyperkalemia?…”

Section: Cold Acclimation Improves Ion Homeostasis During Cold Stresssupporting

confidence: 46%

“…Consistent with this idea we found that cold-acclimated locusts maintained polarization of V m better, and the same animals also showed improved cellular and organismal survival. In a previous study by MacMillan et al (2015c) we showed that only the combined effect of hyperkalemia and chilling causes injury, which suggested that V m must be depolarized past a critical threshold level to induce necrotic/apoptotic events. Our results support the hypothesis that by maintaining low hemolymph [K + ] during cold stress, cold-acclimated locusts better preserve V m , which ensures that cellular viability and organismal performance is maintained during chilling.…”

Section: Cold Acclimation Improves Ion Homeostasis During Cold Stressmentioning

confidence: 99%

“…Tissue damage was estimated in muscle tissue as described in MacMillan et al (2015c). The head and extremities were removed and a longitudinal incision was made on the ventral side of the thorax to expose the mesothoracic posterior tergocoxal muscle (M90; Snodgrass, 1929).…”

Section: Cellular Viability After Cold Exposurementioning

confidence: 99%

“…The increased intracellular [Ca 2+ ] subsequently causes an activation of Ca 2+ -dependent lipases and proteases, resulting in cell death (McConkey and Orrenius, 1996;Demaurex and Distelhorst, 2003). In a recent study, MacMillan et al (2015c) investigated the separate and combined effects of hyperkalemia and low temperature (which both depolarize V m ) on chilling injury in locust muscle and showed that cell death only occurred when the in vitro muscle preparations were exposed to both factors simultaneously. Hyperkalemia and low temperature depolarized V m additively, and only induced injury when applied together.…”

Section: Introductionmentioning

confidence: 99%

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Cold-acclimation improves chill tolerance in the migratory locust through preservation of ion balance and membrane potential

Andersen

Folkersen

MacMillan

et al. 2016

Journal of Experimental Biology

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Most insects have the ability to alter their cold tolerance in response to temporal temperature fluctuations, and recent studies have shown that insect cold tolerance is closely tied to the ability to maintain transmembrane ion gradients that are important for the maintenance of cell membrane potential (V m ). Several studies have therefore suggested a link between preservation of V m and cellular survival after cold stress, but none has measured V m in this context. We tested this hypothesis by acclimating locusts (Locusta migratoria) to high (31°C) and low temperature (11°C) for 4 days before exposing them to cold stress (0°C) for up to 48 h and subsequently measuring ion balance, cell survival, muscle V m , and whole animal performance. Cold stress caused gradual muscle cell death, which coincided with a loss of ion balance and depolarization of muscle V m . The loss of ion balance and cell polarization were, however, dampened markedly in cold-acclimated locusts such that the development of chill injury was reduced. To further examine the association between cellular injury and V m we exposed in vitro muscle preparations to cold buffers with low, intermediate, or. These experiments revealed that cellular injury during cold exposure occurs when V m becomes severely depolarized. Interestingly, we found that cellular sensitivity to hypothermic hyperkalaemia was lower in cold-acclimated locusts that were better able to defend V m whilst exposed to high extracellular [K + ]. Together these results demonstrate a mechanism of cold acclimation in locusts that improves survival after cold stress: increased cold tolerance is accomplished by preservation of V m through maintenance of ion homeostasis and decreased K + sensitivity.

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Section: Cold Acclimation Improves Ion Homeostasis During Cold Stresssupporting

confidence: 46%

Section: Cold Acclimation Improves Ion Homeostasis During Cold Stressmentioning

confidence: 99%

Section: Cellular Viability After Cold Exposurementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Cold-acclimation improves chill tolerance in the migratory locust through preservation of ion balance and membrane potential

Andersen

Folkersen

MacMillan

et al. 2016

Journal of Experimental Biology

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“…Following an intense cold exposure (longer duration 56 and/or lower temperature), chill-susceptible insects acquire irreversible injuries and eventually 57 die (Koštál et al, 2004;Koštál et al, 2006;Rojas and Leopold, 1996) and rates of survival 58 following chilling are also regularly used as a measure of insect cold tolerance (Andersen et al,59 2015; MacMillan et al, 2015a; Sinclair et al, 2015). While there is often a high degree of 60 covariance in these three metrics, the mechanisms that underlie each of them is different and 61 in hemolymph water content (Koštál et induced hyperkalemia further depolarizes resting membrane potential by reducing the K + 107 gradient necessary for passive K + leak, and it is these cumulative short-and long-term 108 depolarizations that has been linked to cellular damage in locusts (MacMillan et al, 2015c). 109…”

Section: Chill Susceptibility In Insects 45mentioning

confidence: 99%

Functional Plasticity of the gut and the Malpighian tubules underlies cold acclimation and mitigates cold-induced hyperkalemia inDrosophila melanogaster

Yerushalmi

Misyura

MacMillan

et al. 2017

Preprint

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(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint . http://dx.doi.org/10.1101/224832 doi: bioRxiv preprint first posted online 2 Abstract 22At low temperatures, Drosophila, like most insects, lose the ability to regulate ion and water 23 balance across the gut epithelia, which can lead to a lethal increase of [K + ] in the hemolymph 24 (hyperkalemia). Cold-acclimation, the physiological response to low temperature exposure, can 25 mitigate or entirely prevent these ion imbalances, but the physiological mechanisms that 26 facilitate this process are not well understood. Here, we test whether plasticity in the 27 ionoregulatory physiology of the gut and Malpighian tubules of Drosophila may aid in 28 preserving ion homeostasis in the cold. Upon adult emergence, D. melanogaster females were 29 subjected to seven days at warm (25°C) or cold (10°C) acclimation conditions. The cold 30 acclimated flies had a lower critical thermal minimum (CTmin), recovered from chill coma more 31 quickly, and better maintained hemolymph K + balance in the cold. The improvements in chill 32 tolerance coincided with increased Malpighian tubule fluid secretion and better maintenance of 33 K + secretion rates in the cold, as well as reduced rectal K + reabsorption in cold-acclimated flies. 34To test whether modulation of ion-motive ATPases, the main drivers of epithelial transport in the 35 alimentary canal, mediate these changes, we measured the activities of Na + -K + -ATPase and V-36 type H + -ATPase at the Malpighian tubules, midgut, and hindgut. Na + /K + -ATPase and V-type H + -37ATPase activities were lower in the midgut and the Malpighian tubules of cold-acclimated flies, 38 but unchanged in the hindgut of cold acclimated flies, and were not predictive of the observed 39 alterations in K + transport. Our results suggest that modification of Malpighian tubule and gut 40 ion and water transport likely prevents cold-induced hyperkalemia in cold-acclimated flies and 41 that this process is not directly related to the activities of the main drivers of ion transport in 42 these organs, Na + /K + -and V-type H + -ATPases. 43All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.

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Bigger isn't always better: Challenging assumptions about the associations between diapause, body weight, and overwintering survival

Short,

Walters,

Hahn

2024

Ecology and Evolution

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During the winter, animals face limited food availability. Many animals enter dormancy to reduce their winter energy expenditure. Most insects spend the winter in diapause, a state of programmed dormancy. It is often assumed that diapausing insects need nutrient stores to fuel their many months of basal metabolism and must grow heavier than their non‐diapause‐programmed counterparts. However, the extent to which food limitation affects body weight during overwintering preparation as well as the likelihood and duration of diapause remains unclear. We limited the duration of the feeding period and thus the total quantity of food available to diapause‐destined larvae of the pupal‐diapausing flesh fly, Sarcophaga crassipalpis, to test how food limitation affects body weight in the context of diapause programming. We also tested the extent to which food deprivation and body weight affect the likelihood and duration of diapause. We hypothesized that diapause‐destined larvae grow more quickly and pupariate at a heavier body weight than non‐diapause larvae. We also hypothesized that body weight is more dramatically reduced by food limitations when a larva is programmed for diapause. Finally, we hypothesized that larvae with lighter body weight (i.e., food limited) are less likely to enter pupal diapause and also stay in diapause for a shorter duration than heavier, well‐fed, individuals. Contrary to our hypotheses that diapausing insects are heavier than their non‐diapausing counterparts, we found diapausing pupae weighed less than non‐diapausing pupae, especially when larvae received limited food. We found light pupae did not abort their diapause program. In both diapausing and non‐diapausing pupae, body weight was positively correlated with simulated winter survival. However, above a weight threshold, body weight no longer affected simulated winter survival in diapausing pupae. Contrary to our predictions and the general consensus in much of the diapause literature, we also found that lighter pupae stayed in diapause longer than heavier pupae. Overall, our results challenge the precept that body weight and diapause are positively associated. The relationship between body weight and diapause is complex and may be affected by the availability of food before and after winter, the availability of high‐quality overwintering sites, and the life history of a particular insect.

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Concurrent effects of cold and hyperkalaemia cause insect chilling injury

Cited by 72 publications

References 50 publications

Cold-acclimation improves chill tolerance in the migratory locust through preservation of ion balance and membrane potential

Cold-acclimation improves chill tolerance in the migratory locust through preservation of ion balance and membrane potential

Functional Plasticity of the gut and the Malpighian tubules underlies cold acclimation and mitigates cold-induced hyperkalemia inDrosophila melanogaster

Bigger isn't always better: Challenging assumptions about the associations between diapause, body weight, and overwintering survival

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