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Quantitative model analysis of the resting membrane potential in insect skeletal muscle: Implications for low temperature tolerance

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Quantitative model analysis of the resting membrane potential in insect skeletal muscle : Implications for low temperature tolerance. / Bayley, Jeppe Seamus; Overgaard, Johannes; Pedersen, Thomas Holm.

I: Comparative Biochemistry and Physiology -Part A : Molecular and Integrative Physiology, Bind 257, 110970, 07.2021.

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avisTidsskriftartikelForskningpeer review

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Bayley, Jeppe Seamus ; Overgaard, Johannes ; Pedersen, Thomas Holm. / Quantitative model analysis of the resting membrane potential in insect skeletal muscle : Implications for low temperature tolerance. I: Comparative Biochemistry and Physiology -Part A : Molecular and Integrative Physiology. 2021 ; Bind 257.

Bibtex

@article{f3655a42fd3e4771b9434964d43f6a29,
title = "Quantitative model analysis of the resting membrane potential in insect skeletal muscle: Implications for low temperature tolerance",
abstract = "Abiotic stressors, such as cold exposure, can depolarize insect cells substantially causing cold coma and cell death. During cold exposure, insect skeletal muscle depolarization occurs through a 2-stage process. Firstly, short-term cold exposure reduces the activity of electrogenic ion pumps, which depolarize insect muscle markedly. Secondly, during long-term cold exposure, extracellular ion homeostasis is disrupted causing further depolarization. Consequently, many cold hardy insects improve membrane potential stability during cold exposure through adaptations that secure maintenance of ion homeostasis during cold exposure. Less is known about the adaptations permitting cold hardy insects to maintain membrane potential stability during the initial phase of cold exposure, before ion balance is disrupted. To address this problem it is critical to understand the membrane components (channels and transporters) that determine the membrane potential and to examine this question the present study constructed a mathematical “charge difference” model of the insect muscle membrane potential. This model was parameterized with known literature values for ion permeabilities, ion concentrations and membrane capacitance and the model was then further developed by comparing model predictions against empirical measurements following pharmacological inhibitors of the Na+/K+ ATPase, Cl− channels and symporters. Subsequently, we compared simulated and recorded membrane potentials at 0 and 31 °C and at 10–50 mM extracellular [K+] to examine if the model could describe membrane potentials during the perturbations occurring during cold exposure. Our results confirm the importance of both Na+/K+ ATPase activity and ion-selective Na+, K+ and Cl− channels, but the model also highlights that additional electroneutral flux of Na+ and K+ is needed to describe how membrane potentials respond to temperature and [K+] in insect muscle. While considerable further work is still needed, we argue that this “charge difference” model can be used to generate testable hypotheses of how insects can preserve membrane polarization in the face of stressful cold exposure.",
keywords = "Cold exposure, Depolarization, Electrogenic ion transport, Insect, Membrane potential",
author = "Bayley, {Jeppe Seamus} and Johannes Overgaard and Pedersen, {Thomas Holm}",
note = "Publisher Copyright: {\textcopyright} 2021 Elsevier Inc.",
year = "2021",
month = jul,
doi = "10.1016/j.cbpa.2021.110970",
language = "English",
volume = "257",
journal = "Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology",
issn = "1095-6433",
publisher = "Elsevier",

}

RIS

TY - JOUR

T1 - Quantitative model analysis of the resting membrane potential in insect skeletal muscle

T2 - Implications for low temperature tolerance

AU - Bayley, Jeppe Seamus

AU - Overgaard, Johannes

AU - Pedersen, Thomas Holm

N1 - Publisher Copyright: © 2021 Elsevier Inc.

PY - 2021/7

Y1 - 2021/7

N2 - Abiotic stressors, such as cold exposure, can depolarize insect cells substantially causing cold coma and cell death. During cold exposure, insect skeletal muscle depolarization occurs through a 2-stage process. Firstly, short-term cold exposure reduces the activity of electrogenic ion pumps, which depolarize insect muscle markedly. Secondly, during long-term cold exposure, extracellular ion homeostasis is disrupted causing further depolarization. Consequently, many cold hardy insects improve membrane potential stability during cold exposure through adaptations that secure maintenance of ion homeostasis during cold exposure. Less is known about the adaptations permitting cold hardy insects to maintain membrane potential stability during the initial phase of cold exposure, before ion balance is disrupted. To address this problem it is critical to understand the membrane components (channels and transporters) that determine the membrane potential and to examine this question the present study constructed a mathematical “charge difference” model of the insect muscle membrane potential. This model was parameterized with known literature values for ion permeabilities, ion concentrations and membrane capacitance and the model was then further developed by comparing model predictions against empirical measurements following pharmacological inhibitors of the Na+/K+ ATPase, Cl− channels and symporters. Subsequently, we compared simulated and recorded membrane potentials at 0 and 31 °C and at 10–50 mM extracellular [K+] to examine if the model could describe membrane potentials during the perturbations occurring during cold exposure. Our results confirm the importance of both Na+/K+ ATPase activity and ion-selective Na+, K+ and Cl− channels, but the model also highlights that additional electroneutral flux of Na+ and K+ is needed to describe how membrane potentials respond to temperature and [K+] in insect muscle. While considerable further work is still needed, we argue that this “charge difference” model can be used to generate testable hypotheses of how insects can preserve membrane polarization in the face of stressful cold exposure.

AB - Abiotic stressors, such as cold exposure, can depolarize insect cells substantially causing cold coma and cell death. During cold exposure, insect skeletal muscle depolarization occurs through a 2-stage process. Firstly, short-term cold exposure reduces the activity of electrogenic ion pumps, which depolarize insect muscle markedly. Secondly, during long-term cold exposure, extracellular ion homeostasis is disrupted causing further depolarization. Consequently, many cold hardy insects improve membrane potential stability during cold exposure through adaptations that secure maintenance of ion homeostasis during cold exposure. Less is known about the adaptations permitting cold hardy insects to maintain membrane potential stability during the initial phase of cold exposure, before ion balance is disrupted. To address this problem it is critical to understand the membrane components (channels and transporters) that determine the membrane potential and to examine this question the present study constructed a mathematical “charge difference” model of the insect muscle membrane potential. This model was parameterized with known literature values for ion permeabilities, ion concentrations and membrane capacitance and the model was then further developed by comparing model predictions against empirical measurements following pharmacological inhibitors of the Na+/K+ ATPase, Cl− channels and symporters. Subsequently, we compared simulated and recorded membrane potentials at 0 and 31 °C and at 10–50 mM extracellular [K+] to examine if the model could describe membrane potentials during the perturbations occurring during cold exposure. Our results confirm the importance of both Na+/K+ ATPase activity and ion-selective Na+, K+ and Cl− channels, but the model also highlights that additional electroneutral flux of Na+ and K+ is needed to describe how membrane potentials respond to temperature and [K+] in insect muscle. While considerable further work is still needed, we argue that this “charge difference” model can be used to generate testable hypotheses of how insects can preserve membrane polarization in the face of stressful cold exposure.

KW - Cold exposure

KW - Depolarization

KW - Electrogenic ion transport

KW - Insect

KW - Membrane potential

UR - http://www.scopus.com/inward/record.url?scp=85105264694&partnerID=8YFLogxK

U2 - 10.1016/j.cbpa.2021.110970

DO - 10.1016/j.cbpa.2021.110970

M3 - Journal article

C2 - 33932565

AN - SCOPUS:85105264694

VL - 257

JO - Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology

JF - Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology

SN - 1095-6433

M1 - 110970

ER -