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Early-life stress triggers long-lasting organismal resilience and longevity via tetraspanin.

ABSTRACT: Early-life stress experiences can produce lasting impacts on organismal adaptation and fitness. How transient stress elicits memory-like physiological effects is largely unknown. Here we show that early-life thermal stress strongly up-regulates tsp-1, a gene encoding the conserved transmembrane tetraspanin in C. elegans. TSP-1 forms prominent multimers and stable web-like structures critical for membrane barrier functions in adults and during aging. The up-regulation of TSP-1 persists even after transient early-life stress. Such regulation requires CBP-1, a histone acetyl-transferase that facilitates initial tsp-1 transcription. Tetraspanin webs form regular membrane structures and mediate resilience-promoting effects of early-life thermal stress. Gain-of-function TSP-1 confers marked C. elegans longevity extension and thermal resilience in human cells. Together, our results reveal a cellular mechanism by which early-life thermal stress produces long-lasting memory-like impact on organismal resilience and longevity.

SUBMITTER: Jiang WI

PROVIDER: S-EPMC10402089 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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Early-life stress triggers long-lasting organismal resilience and longevity via tetraspanin.

Jiang Wei I WI De Belly Henry H Wang Bingying B Wong Andrew A Kim Minseo M Oh Fiona F DeGeorge Jason J Huang Xinya X Guang Shouhong S Weiner Orion D OD Ma Dengke K DK

bioRxiv : the preprint server for biology 20231217

Early-life stress experiences can produce lasting impacts on organismal adaptation and fitness. How transient stress elicits memory-like physiological effects is largely unknown. Here we show that early-life thermal stress strongly up-regulates <i>tsp-1</i>, a gene encoding the conserved transmembrane tetraspanin in <i>C. elegans</i>. TSP-1 forms prominent multimers and stable web-like structures critical for membrane barrier functions in adults and during aging. The up-regulation of TSP-1 persi ...[more]

PMID: 37546737

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Project description:The olfactory system is a niche of continuous structural plasticity, holding postnatal proliferative neurogenesis in the olfactory bulbs and a population of immature neurons in the piriform cortex. These neurons in the piriform cortex are generated during embryonic development, retain the expression of immaturity markers such as doublecortin, and slowly mature and integrate into the olfactory circuit as the animal ages. To study how early life experiences affect this population of cortical immature neurons, we submitted mice of the C57/Bl6J strain to a protocol of maternal separation for 3 h per day from postnatal day 3 to postnatal day 21. Control mice were continuously with their mothers. After weaning, mice were undisturbed until 6 weeks of age, when they were weighted and tested in the elevated plus-maze, a standard test for anxiety-like behavior, to check for phenotypical effects. Mice were then perfused, and their brains processed for the immunofluorescent detection of doublecortin and the endogenous proliferation marker Ki67. We found that maternal separation induced a significant increase in the body weight of males, but not females. Further, maternally separated mice displayed increased exploratory-like behavior (i.e., head dipping, velocity and total distance traveled in the elevated plus maze), but no significant differences in anxiety-like behavior or corticosterone levels after behavioral testing. Finally, we observed a significant increase in the number of complex doublecortin neurons in the piriform cortex, but not in the olfactory bulbs, of mice submitted to maternal separation. Interestingly, most doublecortin neurons in the piriform cortex, but not the olfactory bulb, express the epigenetic reader MeCP2. In summary, mild early life stress results, during adolescence, in a male-specific increase in body weight, alteration of the exploratory behaviors, and an increase in doublecortin neurons in the piriform cortex, suggesting an alteration in their maturation process.

Dataset Information

Early-life stress triggers long-lasting organismal resilience and longevity via tetraspanin.

Publications

Early-life stress triggers long-lasting organismal resilience and longevity via tetraspanin.

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