Short‐term starvation stress at young adult stages enhances meiotic activity of germ cells to maintain spermatogenesis in aged male Caenorhabditis elegans

• Published in: Aging cell Vol. 18; no. 3; pp. e12930 - n/a
• Main Authors: Chou, Wan‐Yi, Lin, Yu‐Chun, Lee, Ying‐Hue
• Format: Journal Article
• Language: English
• Published: England John Wiley & Sons, Inc 01.06.2019; John Wiley and Sons Inc
• Subjects: Aging; Aging - genetics; Anaphase; Anaphase-promoting complex; anaphase‐promoting complex/cyclosome (APC/C); Animals; Caenorhabditis elegans; Caenorhabditis elegans - cytology; Caenorhabditis elegans - genetics; Caenorhabditis elegans - growth & development; CDC‐20; Genetic engineering; Germ cells; Germ Cells - cytology; Germ Cells - metabolism; Male; Males; Meiosis; Meiosis - genetics; Mitosis; Nematodes; Original; Physiological aspects; short‐term starvation; Spermatogenesis; Spermatogenesis - genetics; Starvation; Starvation - genetics; stress response hormesis; Stress, Physiological - genetics; Teenagers; Ubiquitin; Ubiquitin-protein ligase; Young adults; Youth; spermatogenesis; stress response hormesis; meiosis; CDC-20; short-term starvation; anaphase-promoting complex/cyclosome (APC/C)
• ISSN: 1474-9718; 1474-9726
• DOI: 10.1111/acel.12930

To survive and reproduce, living organisms must evolve numerous mechanisms to re‐adjust their physiology when encountering adverse conditions that subject them to severe stress. We found that short‐term starvation (STS) stress in young adult male Caenorhabditis elegans can significantly improve their vitality (relative to nonstressed males) when they are aged. In addition, we found that stress‐treated aged males maintained reproductive activity equivalent to young males, whereas nonstressed aged males quickly lost reproductive ability. STS stress can preserve sperm number and quality in aged male worms. Spermatogenesis involves germ cell mitosis and meiosis. We found that germ cell meiotic activity is more sensitive to aging than mitotic activity and is declining rapidly with age. We examined the role of numerous factors important for spermatogenesis on STS‐preserved spermatogenesis during aging. Our results show that mutant strains deficient in anaphase‐promoting complex/cyclosome (APC/C) function fail to exhibit the STS stress‐enhanced spermatogenesis found in wild‐type N2 worms, suggesting that the mechanism underlying starvation‐induced spermatogenesis involves the APC/C complex, a conserved ubiquitin‐protein ligase E3 complex. Furthermore, transgenic expression of FZY‐1/CDC‐20, a coactivator of APC/C, ameliorated the age‐associated decline of meiosis, similar to the hormetic effect of STS. A short‐term starvation (STS) treatment in young adult male Caenorhabditis elegans significantly improves their reproduction fitness when they are aged. STS stress preserves sperm number and quality in aged male worms, and the mechanism underlying requires anaphase‐promoting complex/cyclosome (APC/C) activity crucial for meiotic division to produce sperms. STS‐induced hormetic effects prevent the age‐associated decline of FZY‐1/CDC‐20 expression, which in turn maintains APC/C activity from decline with age.