Reduced L-type Ca2+ current and compromised excitability induce loss of skeletal muscle function during acute cooling in locust

TY - JOUR

T1 - Reduced L-type Ca2+ current and compromised excitability induce loss of skeletal muscle function during acute cooling in locust

AU - Findsen, Anders

AU - Overgaard, Johannes

AU - Pedersen, Thomas Holm

N1 - © 2016. Published by The Company of Biologists Ltd.

PY - 2016/8/1

Y1 - 2016/8/1

N2 - Low temperature causes most insects to enter a state of neuromuscular paralysis, termed chill coma. The susceptibility of insect species to chill coma is tightly correlated to their distribution limits and for this reason it is important to understand the cellular processes that underlie chill coma. It is known that muscle function is markedly depressed at low temperature and this suggests that chill coma is partly caused by impairment in the muscle per se. To find the cellular mechanism(s) underlying muscle dysfunction at low temperature, we examined the effect of low temperature (5°C) on several events in excitation-contraction coupling in the migratory locust (Locusta migratoria). Intracellular membrane potential recordings during single nerve stimulations showed that 70% of fibers at 20°C produced an action potential (AP), while only 55% of fibers were able to fire an AP at 5°C. Reduced excitability at low temperature was caused by an ∼80% drop in L-type Ca(2+) current and a depolarizing shift in its activation of around 20 mV, which means that a larger endplate potential would be needed to activate the muscle AP at low temperature. In accordance, we showed that intracellular Ca(2+) transients were largely absent at low temperature following nerve stimulation. In contrast, maximum contractile force was unaffected by low temperature in chemically skinned muscle bundles, which demonstrates that the function of the contractile filaments is preserved at low temperature. These findings demonstrate that reduced L-type Ca(2+) current is likely to be the most important factor contributing to loss of muscle function at low temperature in locust.

AB - Low temperature causes most insects to enter a state of neuromuscular paralysis, termed chill coma. The susceptibility of insect species to chill coma is tightly correlated to their distribution limits and for this reason it is important to understand the cellular processes that underlie chill coma. It is known that muscle function is markedly depressed at low temperature and this suggests that chill coma is partly caused by impairment in the muscle per se. To find the cellular mechanism(s) underlying muscle dysfunction at low temperature, we examined the effect of low temperature (5°C) on several events in excitation-contraction coupling in the migratory locust (Locusta migratoria). Intracellular membrane potential recordings during single nerve stimulations showed that 70% of fibers at 20°C produced an action potential (AP), while only 55% of fibers were able to fire an AP at 5°C. Reduced excitability at low temperature was caused by an ∼80% drop in L-type Ca(2+) current and a depolarizing shift in its activation of around 20 mV, which means that a larger endplate potential would be needed to activate the muscle AP at low temperature. In accordance, we showed that intracellular Ca(2+) transients were largely absent at low temperature following nerve stimulation. In contrast, maximum contractile force was unaffected by low temperature in chemically skinned muscle bundles, which demonstrates that the function of the contractile filaments is preserved at low temperature. These findings demonstrate that reduced L-type Ca(2+) current is likely to be the most important factor contributing to loss of muscle function at low temperature in locust.

KW - Journal Article

UR - http://www.scopus.com/inward/record.url?scp=84982946677&partnerID=8YFLogxK

U2 - 10.1242/jeb.137604

DO - 10.1242/jeb.137604

M3 - Journal article

C2 - 27247315

SN - 0022-0949

VL - 219

SP - 2340

EP - 2348

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

IS - Pt 15

ER -