Abstract
The decline of aging C. elegans male's mating behavior is correlated with the increased excitability of the cholinergic circuitry that executes copulation. In this study, we show that the mating circuits' functional durability depends on the metabolic regulator SIR-2.1, a NAD(+)-dependent histone deacetylase. Aging sir-2.1(0) males display accelerated mating behavior decline due to premature hyperexcitability of cholinergic circuits used for intromission and ejaculation. In sir-2.1(0) males, the hypercontraction of the spicule-associated muscles pinch the vas deferens opening, thus blocking sperm release. The hyperexcitability is aggravated by reactive oxygen species (ROS). Our genetic, pharmacological, and behavioral analyses suggest that in sir-2.1(0) and older wild-type males, enhanced catabolic enzymes expression, coupled with the reduced expression of ROS-scavengers contribute to the behavioral decline. However, as a compensatory response to reduce altered catabolism/ROS production, anabolic enzymes expression levels are also increased, resulting in higher gluconeogenesis and lipid synthesis. DOI: http://dx.doi.org/10.7554/eLife.01730.001.
Highlights
Lifespan is well studied in the model organism Caenorhabditis elegans (Kenyon, 2010), the aging process per se is still under intense research (Jin, 2010)
We reported that C. elegans male mating behavior deteriorates during early aging
Relative mRNA expression level of genes involved in metabolic processes such as glycolysis (A), TCA cycle (B), fatty acid oxidation(C), Gluconeogenesis/glyceroneogenesis/lipid synthesis (D), Glyoxylate cycle (E), and electron transport chain (ETC) (F) in 2-day-old wild type, 1-day-old, and 2-day-old sir-2.1(0) males relative to 1-day-old wild type. d1 WT refers to day1 wild type; d2 WT refers to day 2 wild type; d1 s2 refers to day1 sir-2.1(0); d2 s2 refers to day 2 sir-2.1(0)
Summary
Lifespan is well studied in the model organism Caenorhabditis elegans (Kenyon, 2010), the aging process per se is still under intense research (Jin, 2010). The decline could be due to physiological alterations toward a non-optimal state, which leads to the failure of proper behavioral execution. It is urgent to uncover the molecular mechanism(s) underlying the physiological changes, so that certain actions could prevent or postpone the non-optimal modifications that occur during aging. Our previous studies used C. elegans males to establish a behavioral model for studying physiological alterations that occur during early aging (Guo et al, 2012). The spicule intromission motor step, which occurs during C. elegans male copulation, is sensitive to changes that occur during early aging (Garcia et al, 2001; Garcia and Sternberg, 2003). Optogenetics, and genetic analyses, we found a correlation between the increased excitability of the spicule intromission circuit and the decline of mating at early adulthood (Guo et al, 2012).
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