Thermal acclimation mitigates cold-induced paracellular leak from the Drosophila gut

Abstract Chill susceptible insects suffer tissue damage and die at low temperatures. The mechanisms that cause chilling injury are not well understood but a growing body of evidence suggests that a cold-induced loss of ion and water homeostasis leads to hemolymph hyperkalemia that depolarizes cells,...

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Autores principales:	Heath A. MacMillan, Gil Y. Yerushalmi, Sima Jonusaite, Scott P. Kelly, Andrew Donini
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2017
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/24584995723a4a32be12283a344afb56
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spelling	oai:doaj.org-article:24584995723a4a32be12283a344afb562021-12-02T12:30:37ZThermal acclimation mitigates cold-induced paracellular leak from the Drosophila gut10.1038/s41598-017-08926-72045-2322https://doaj.org/article/24584995723a4a32be12283a344afb562017-08-01T00:00:00Zhttps://doi.org/10.1038/s41598-017-08926-7https://doaj.org/toc/2045-2322Abstract Chill susceptible insects suffer tissue damage and die at low temperatures. The mechanisms that cause chilling injury are not well understood but a growing body of evidence suggests that a cold-induced loss of ion and water homeostasis leads to hemolymph hyperkalemia that depolarizes cells, leading to cell death. The apparent root of this cascade is the net leak of osmolytes down their concentration gradients in the cold. Many insects, however, are capable of adjusting their thermal physiology, and cold-acclimated Drosophila can maintain homeostasis and avoid injury better than warm-acclimated flies. Here, we test whether chilling causes a loss of epithelial barrier function in female adult Drosophila, and provide the first evidence of cold-induced epithelial barrier failure in an invertebrate. Flies had increased rates of paracellular leak through the gut epithelia at 0 °C, but cold acclimation reduced paracellular permeability and improved cold tolerance. Improved barrier function was associated with changes in the abundance of select septate junction proteins and the appearance of a tortuous ultrastructure in subapical intercellular regions of contact between adjacent midgut epithelial cells. Thus, cold causes paracellular leak in a chill susceptible insect and cold acclimation can mitigate this effect through changes in the composition and structure of transepithelial barriers.Heath A. MacMillanGil Y. YerushalmiSima JonusaiteScott P. KellyAndrew DoniniNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 7, Iss 1, Pp 1-11 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Heath A. MacMillan Gil Y. Yerushalmi Sima Jonusaite Scott P. Kelly Andrew Donini Thermal acclimation mitigates cold-induced paracellular leak from the Drosophila gut
description	Abstract Chill susceptible insects suffer tissue damage and die at low temperatures. The mechanisms that cause chilling injury are not well understood but a growing body of evidence suggests that a cold-induced loss of ion and water homeostasis leads to hemolymph hyperkalemia that depolarizes cells, leading to cell death. The apparent root of this cascade is the net leak of osmolytes down their concentration gradients in the cold. Many insects, however, are capable of adjusting their thermal physiology, and cold-acclimated Drosophila can maintain homeostasis and avoid injury better than warm-acclimated flies. Here, we test whether chilling causes a loss of epithelial barrier function in female adult Drosophila, and provide the first evidence of cold-induced epithelial barrier failure in an invertebrate. Flies had increased rates of paracellular leak through the gut epithelia at 0 °C, but cold acclimation reduced paracellular permeability and improved cold tolerance. Improved barrier function was associated with changes in the abundance of select septate junction proteins and the appearance of a tortuous ultrastructure in subapical intercellular regions of contact between adjacent midgut epithelial cells. Thus, cold causes paracellular leak in a chill susceptible insect and cold acclimation can mitigate this effect through changes in the composition and structure of transepithelial barriers.
format	article
author	Heath A. MacMillan Gil Y. Yerushalmi Sima Jonusaite Scott P. Kelly Andrew Donini
author_facet	Heath A. MacMillan Gil Y. Yerushalmi Sima Jonusaite Scott P. Kelly Andrew Donini
author_sort	Heath A. MacMillan
title	Thermal acclimation mitigates cold-induced paracellular leak from the Drosophila gut
title_short	Thermal acclimation mitigates cold-induced paracellular leak from the Drosophila gut
title_full	Thermal acclimation mitigates cold-induced paracellular leak from the Drosophila gut
title_fullStr	Thermal acclimation mitigates cold-induced paracellular leak from the Drosophila gut
title_full_unstemmed	Thermal acclimation mitigates cold-induced paracellular leak from the Drosophila gut
title_sort	thermal acclimation mitigates cold-induced paracellular leak from the drosophila gut
publisher	Nature Portfolio
publishDate	2017
url	https://doaj.org/article/24584995723a4a32be12283a344afb56
work_keys_str_mv	AT heathamacmillan thermalacclimationmitigatescoldinducedparacellularleakfromthedrosophilagut AT gilyyerushalmi thermalacclimationmitigatescoldinducedparacellularleakfromthedrosophilagut AT simajonusaite thermalacclimationmitigatescoldinducedparacellularleakfromthedrosophilagut AT scottpkelly thermalacclimationmitigatescoldinducedparacellularleakfromthedrosophilagut AT andrewdonini thermalacclimationmitigatescoldinducedparacellularleakfromthedrosophilagut
_version_	1718394322276057088

Thermal acclimation mitigates cold-induced paracellular leak from the Drosophila gut

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