Pheromone-based communication influences the production of somatic extracellular vesicles in C. elegans

Extracellular vesicles (EVs) play vital roles in various biological processes, yet understanding how environmental factors and social interactions influence EV-regulated systems remains a challenge. A recent study by researchers at the Polish Academy of Sciences conducted in Caenorhabditis elegans sheds light on this intriguing phenomenon, focusing on the role of large EVs, known as exophers, in maternal somatic tissue resource management and their impact on offspring development.

Exophers are evolutionarily conserved structures in C. elegans that contribute to the efficient allocation of resources within maternal somatic tissues, resulting in faster development of offspring. The research aims to decipher the intricate interplay of environmental cues and social dynamics that govern exophergenesis in this model organism.

The study identifies the primary male pheromone, ascr#10, as a key regulator of exopher production in hermaphrodites. This effect is mediated through the G-protein-coupled receptor STR-173 located in ASK sensory neurons. Interestingly, while ascr#10 enhances exophergenesis, pheromone produced by other hermaphrodites, specifically ascr#3, inhibits exopher production within the population.

Further investigation reveals a regulatory network involving neuropeptides FLP-8 and FLP-21, originating from different sensory neurons, in modulating exophergenesis. Specifically, FLP-8 from URX neurons and FLP-21 from AQR/PQR/URX neurons play distinct roles in mediating the effects of social signals on exopher production.

Model

Fig. 8

Males produce ascarosides, including ascr#10, which promote exopher production through ASK, ADL, and AWB signaling, whereby the ASK-expressed STR-173 GPCR enhances exopher production in response to ascr#10. In contrast, hermaphrodites release a different set of ascarosides, dominated by ascr#3, which reduces exopher production, primarily acting via the ASI, ASH, and ASK sensory neurons. The AQR/PQR/URX neurons in the pseudocoelomic cavity release FLP-8 and FLP-21 neuropeptides, negatively regulating exophergenesis. This modulation is critical for decreasing exophergenesis due to hermaphrodite pheromones but not for the increase driven by male pheromones.

These findings highlight a fascinating regulatory mechanism wherein the nervous system responds to social cues to modulate the production of somatic EVs. By unraveling the intricate inter-tissue and social dynamics governing exophergenesis, this research provides valuable insights into how environmental factors and social interactions influence EV-regulated systems.

Understanding the mechanisms underlying EV regulation in response to social signals not only advances our knowledge of fundamental biological processes but also opens new avenues for research in fields such as developmental biology and neurobiology. Moreover, insights gained from studies in model organisms like C. elegans may have broader implications for understanding similar processes in more complex organisms, including humans.

Szczepańska A, Olek K, Kołodziejska K, Yu J, Ibrahim AT, Adamkiewicz L, Schroeder FC, Pokrzywa W, Turek M. (2024) Pheromone-based communication influences the production of somatic extracellular vesicles in C. elegans. Nat Commun 15(1):2715. [article]

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