Abstract
Ca2+ is a key signal transducer for muscle contraction. Continuous in vivo monitoring of intracellular Ca2+-dynamics in C. elegans pharynx muscle revealed surprisingly complex Ca2+ patterns. Despite the age-dependent decline of pharynx pumping, we observed unaltered fast Ca2+ oscillations both in young and old worms. In addition, sporadic prolonged Ca2+ increases lasting many seconds or minutes were often observed in between periods of fast Ca2+ oscillations. We attribute them to the inhibition of ATP-dependent Ca2+-pumps upon energy depletion. Accordingly, food deprivation largely augmented the frequency of prolonged [Ca2+] increases. However, paradoxically, prolonged [Ca2+] increases were more frequently observed in young worms than in older ones, and less frequently observed in energy-deficient mitochondrial respiratory chain nuo-6 mutants than in wild-type controls. We hypothesize that young animals are more susceptible to energy depletion due to their faster energy consumption rate, while nuo-6 mutants may keep better the energy balance by slowing energy consumption. Our data therefore suggest that the metabolic state of the pharynx during feeding stimulation depends mainly on the delicate balance between the instant rates of energy production and consumption. Thus, in vivo monitoring of muscle Ca2+ dynamics can be used as a novel tool to study cellular energy availability.
Highlights
The nematode C. elegans is one of the leading model organisms for aging research
Pharyngeal muscle activity strongly correlates with aging as decline of pharyngeal pumping directly correlates with a decline in survival probability [7]
Despite the obvious pharynx muscle decline observed during aging, Ca2+ oscillations do not undergo an age-dependent decline
Summary
One of the main advantages of this animal is the availability of well-described mutant strains with shortened or extended life spans, which provides a unique tool to dissect the molecular pathways related to aging [1] Another major advantage is the possibility to visualize physiological alterations over the course of aging, as the normal C. elegans life span is only around two weeks. C. elegans pharynx muscle activity has been shown to progressively decline with worm age [2,3,4,5]. The rate of pharyngeal pumping reaches a maximum of nearly 300 pumps/min for 2 day-old adults, decreasing progressively with age to about 100 pumps/min by day 8, 10 pumps/min by day 12, and essentially no activity after day 14 [7] This pharyngeal pumping decline rate correlates with the longevity of worms. The new technique we show here to study long-lasting pharynx muscle Ca2+ dynamics may provide a novel methodology to in vivo monitor the energy status of the worm
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