Synergistic modulation of neuroendocrine-inflammation pathway by microRNAs facilitates intertidal adaptation of molluscs

• Published in: Fish & Shellfish Immunology
• Main Authors: Chen, Hao, Wang, Lin, Wang, Lingling, Zhang, Huan, Wang, Hao, Song, Linsheng
• Format: Report
• Language: English
• Published: ACADEMIC PRESS LTD- ELSEVIER SCIENCE LTD 2023
• Subjects: Inflammation response; Calmodulin; Nitrite oxide; Tumor necrosis factor; miRNAs; Aerial exposure; Fisheries; Immunology; Marine & Freshwater Biology; Veterinary Sciences; OYSTER CRASSOSTREA-GIGAS; STRESS-RESPONSE; INVERTEBRATES; DESICCATION; EXPRESSION; HEMOCYTES; TOLERANCE; EXPOSURE; IMMUNITY; GENES; Crassostrea gigas
• Online Access: http://ir.qdio.ac.cn/handle/337002/183887; https://doi.org/10.1016/j.fsi.2023.109165

Neuroendocrine-immune system is an evolution-conserved regulatory network in maintaining the homeostasis of animals. While knowledge on the roles of neuroendocrine-immune system in the disease and stress responses of organisms is growing, the ecological roles of neuroendocrine-immune system, especially how it shapes the unique lifestyle of organisms remain insufficiently investigated. As an endemic and dominant mollusc in intertidal region, oysters have evolved with a primitive neuroendocrine-immune system and with a sessile lifestyle. Recently, a novel neuroendocrine-immune pathway, Ca2+/calmodulin (CaM)-nitrite oxide synthase (NOS)/nitrite oxide (NO)-tumor necrosis factor (TNF) pathway, is identified in oysters and found altered dynamically during aerial exposure, one common but challenging stresses for intertidal organisms and a decisive factor shaping their habitat. Since the pathway proves fatal in prolonged aerial exposure, we hypothesized that the activation/deactivation of pathway could be strictly modulated in adaptation to the sessile lifestyle of oysters. Here, a synergistic modulation on the Ca2+/CaM-NOS/NO-TNF pathway by four members of miR-92 family and two oyster-specific miRNAs was identified, which further hallmarks the resilience and survival strategy of oysters to aerial exposure. Briefly, these six miRNAs were down-regulating CgCaM24243 post-transcriptionally and deactivating the pathway during the early-stage of stress. However, a robust recession of these miRNAs occurred at the late-stage of stress, resulting in the reactivation of pathway and overwhelming accumulation of cytokines. These results demonstrated a complicated interaction between miRNAs and ancient neuroendocrine-immune system, which facilitates the environmental adaptation of intertidal oysters and provides novel insight on the function and evolution of neuroendocrine-immune system in ecological context.