{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,12]],"date-time":"2026-04-12T08:36:41Z","timestamp":1775983001221,"version":"3.50.1"},"reference-count":57,"publisher":"The Royal Society","issue":"1941","license":[{"start":{"date-parts":[[2020,12,16]],"date-time":"2020-12-16T00:00:00Z","timestamp":1608076800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/royalsociety.org\/-\/media\/journals\/author\/Licence-to-Publish-20062019-final.pdf"},{"start":{"date-parts":[[2020,12,16]],"date-time":"2020-12-16T00:00:00Z","timestamp":1608076800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/royalsociety.org\/journals\/ethics-policies\/data-sharing-mining\/"}],"funder":[{"name":"Canada Foundation for Innovation"},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"crossref","award":["RGPIN-2018-05322"],"award-info":[{"award-number":["RGPIN-2018-05322"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["royalsocietypublishing.org"],"crossmark-restriction":true},"short-container-title":["Proc. R. Soc. B."],"published-print":{"date-parts":[[2020,12,23]]},"abstract":"<jats:p>\n                    There is a growing appreciation that insect distribution and abundance are associated with the limits of thermal tolerance, but the physiology underlying thermal tolerance remains poorly understood. Many insects, like the migratory locust (\n                    <jats:italic>Locusta migratoria<\/jats:italic>\n                    ), suffer a loss of ion and water balance leading to hyperkalaemia (high extracellular [K\n                    <jats:sup>+<\/jats:sup>\n                    ]) in the cold that indirectly causes cell death. Cells can die in several ways under stress, and how they die is of critical importance to identifying and understanding the nature of thermal adaptation. Whether apoptotic or necrotic cell death pathways are responsible for low-temperature injury is unclear. Here, we use a caspase-3 specific assay to indirectly quantify apoptotic cell death in three locust tissues (muscle, nerves and midgut) following prolonged chilling and recovery from an injury-inducing cold exposure. Furthermore, we obtain matching measurements of injury, extracellular [K\n                    <jats:sup>+<\/jats:sup>\n                    ] and muscle caspase-3 activity in individual locusts to gain further insight into the mechanistic nature of chilling injury. We found a significant increase in muscle caspase-3 activity, but no such increase was observed in either nervous or gut tissue from the same animals, suggesting that chill injury primarily relates to muscle cell death. Levels of chilling injury measured at the whole animal level, however, were strongly correlated with the degree of haemolymph hyperkalaemia, and not apoptosis. These results support the notion that cold-induced ion balance disruption triggers cell death but also that apoptosis is not the main form of cell damage driving low-temperature injury.\n                  <\/jats:p>","DOI":"10.1098\/rspb.2020.1663","type":"journal-article","created":{"date-parts":[[2020,12,16]],"date-time":"2020-12-16T02:53:13Z","timestamp":1608087193000},"page":"20201663","update-policy":"https:\/\/doi.org\/10.1098\/crossmark-policy","source":"Crossref","is-referenced-by-count":18,"title":["Hyperkalaemia, not apoptosis, accurately predicts insect chilling injury"],"prefix":"10.1098","volume":"287","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0382-3673","authenticated-orcid":true,"given":"Jessica","family":"Carrington","sequence":"first","affiliation":[{"name":"Department of Biology, Carleton University, Ottawa, Canada, K1S 5B6"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6215-8941","authenticated-orcid":true,"given":"Mads Kuhlmann","family":"Andersen","sequence":"additional","affiliation":[{"name":"Department of Biology, Carleton University, Ottawa, Canada, K1S 5B6"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kaylen","family":"Brzezinski","sequence":"additional","affiliation":[{"name":"Department of Biology, Carleton University, Ottawa, Canada, K1S 5B6"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7598-3273","authenticated-orcid":true,"given":"Heath A.","family":"MacMillan","sequence":"additional","affiliation":[{"name":"Department of Biology, Carleton University, Ottawa, Canada, K1S 5B6"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"175","published-online":{"date-parts":[[2020,12,16]]},"reference":[{"key":"e_1_3_5_2_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-physiol-022516-034142"},{"key":"e_1_3_5_3_2","doi-asserted-by":"publisher","DOI":"10.1086\/662642"},{"key":"e_1_3_5_4_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.179598"},{"key":"e_1_3_5_5_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-017-10586-6"},{"key":"e_1_3_5_6_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0306-4565(98)00020-5"},{"key":"e_1_3_5_7_2","doi-asserted-by":"publisher","DOI":"10.1152\/jn.00724.2019"},{"key":"e_1_3_5_8_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cbpb.2005.11.005"},{"key":"e_1_3_5_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jinsphys.2010.10.004"},{"key":"e_1_3_5_10_2","doi-asserted-by":"publisher","DOI":"10.1006\/cryo.1996.0045"},{"key":"e_1_3_5_11_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cryobiol.2004.01.004"},{"key":"e_1_3_5_12_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-017-08926-7"},{"key":"e_1_3_5_13_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.168518"},{"key":"e_1_3_5_14_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.00923"},{"key":"e_1_3_5_15_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.051540"},{"key":"e_1_3_5_16_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2015.1483"},{"key":"e_1_3_5_17_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.107516"},{"key":"e_1_3_5_18_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.150813"},{"key":"e_1_3_5_19_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1813532115"},{"key":"e_1_3_5_20_2","doi-asserted-by":"crossref","first-page":"3171","DOI":"10.1242\/jeb.204.18.3171","article-title":"Mechanisms of cell survival in hypoxia and hypothermia","volume":"204","author":"Boutilier RG","year":"2001","journal-title":"J. Exp. Biol."},{"key":"e_1_3_5_21_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10495-010-0570-0"},{"key":"e_1_3_5_22_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.140152"},{"key":"e_1_3_5_23_2","doi-asserted-by":"publisher","DOI":"10.1152\/ajpregu.00465.2014"},{"key":"e_1_3_5_24_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.174904"},{"key":"e_1_3_5_25_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.213934"},{"key":"e_1_3_5_26_2","doi-asserted-by":"publisher","DOI":"10.1038\/srep18607"},{"key":"e_1_3_5_27_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.123760"},{"key":"e_1_3_5_28_2","first-page":"R823","article-title":"Cold-acclimation increases depolarization resistance and tolerance in muscle fibers from a chill-susceptible insect, Locusta migratoria","volume":"308","author":"Bayley JS","year":"2020","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"e_1_3_5_29_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1503456112"},{"key":"e_1_3_5_30_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0022-1910(03)00168-9"},{"key":"e_1_3_5_31_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10495-006-0048-2"},{"key":"e_1_3_5_32_2","doi-asserted-by":"crossref","first-page":"1465","DOI":"10.1016\/0270-9139(95)90071-3","article-title":"In situ detection of fragmented DNA (tunel assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note","volume":"21","author":"Grasl-Kraupp B","year":"1995","journal-title":"Hepatology"},{"key":"e_1_3_5_33_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jinsphys.2015.03.007"},{"key":"e_1_3_5_34_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10495-009-0322-1"},{"key":"e_1_3_5_35_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.immuni.2016.01.020"},{"key":"e_1_3_5_36_2","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.201107133"},{"key":"e_1_3_5_37_2","doi-asserted-by":"publisher","DOI":"10.1038\/sj.cdd.4402060"},{"key":"e_1_3_5_38_2","doi-asserted-by":"publisher","DOI":"10.1038\/cdd.2014.216"},{"key":"e_1_3_5_39_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2016.11.047"},{"key":"e_1_3_5_40_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2009.08.042"},{"key":"e_1_3_5_41_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.215475"},{"key":"e_1_3_5_42_2","first-page":"1","article-title":"The thoracic mechanism of a grasshopper, and its antecedents","volume":"82","author":"Snodgrass RE","year":"1929","journal-title":"Smithson. Misc. Collect."},{"key":"e_1_3_5_43_2","volume-title":"R: a language and environment for statistical computing","author":"R Development Core Team","year":"2019"},{"key":"e_1_3_5_44_2","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1242\/jeb.177.1.201","article-title":"Calcium channel currents in neurones from locust (Schistocerca gregaria) thoracic ganglia","volume":"177","author":"Pearson HA","year":"1993","journal-title":"J. Exp. Biol."},{"key":"e_1_3_5_45_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jinsphys.2019.03.003"},{"key":"e_1_3_5_46_2","unstructured":"Quintavalle A. 2013 Voltage-gated calcium channels in honey bees: physiological roles and potential targets for insecticides. MSc thesis ENS de Lyon France."},{"key":"e_1_3_5_47_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0001366"},{"key":"e_1_3_5_48_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.218750"},{"key":"e_1_3_5_49_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.2417316"},{"key":"e_1_3_5_50_2","doi-asserted-by":"publisher","DOI":"10.1007\/s12028-019-00776-7"},{"key":"e_1_3_5_51_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cbpa.2015.10.020"},{"key":"e_1_3_5_52_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.191593"},{"key":"e_1_3_5_53_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ceca.2011.03.003"},{"key":"e_1_3_5_54_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.73.4.1907-1916.2005"},{"key":"e_1_3_5_55_2","doi-asserted-by":"publisher","DOI":"10.3923\/ijzr.2018.49.60"},{"key":"e_1_3_5_56_2","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1242\/jeb.95.1.61","article-title":"Mechanisms of ionic homeostasis in the central nervous system of an insect","volume":"95","author":"Treherne J","year":"1981","journal-title":"J. Exp. Biol."},{"key":"e_1_3_5_57_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0040-8166(73)80056-4"},{"key":"e_1_3_5_58_2","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1242\/jcs.18.1.179","article-title":"Insect peripheral nerves: accessibility of neurohaemal regions to lanthanum","volume":"18","author":"Lane NJ","year":"1975","journal-title":"J. Cell Sci."}],"container-title":["Proceedings of the Royal Society B: Biological Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rspb.2020.1663","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/full-xml\/10.1098\/rspb.2020.1663","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rspb.2020.1663","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,5]],"date-time":"2022-12-05T02:27:05Z","timestamp":1670207225000},"score":1,"resource":{"primary":{"URL":"https:\/\/royalsocietypublishing.org\/doi\/10.1098\/rspb.2020.1663"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,12,16]]},"references-count":57,"journal-issue":{"issue":"1941","published-print":{"date-parts":[[2020,12,23]]}},"alternative-id":["10.1098\/rspb.2020.1663"],"URL":"https:\/\/doi.org\/10.1098\/rspb.2020.1663","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.07.03.186759","asserted-by":"object"}]},"ISSN":["0962-8452","1471-2954"],"issn-type":[{"value":"0962-8452","type":"print"},{"value":"1471-2954","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,12,16]]},"assertion":[{"value":"2020-07-10","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2020-11-21","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2020-12-16","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}