Head-tail-head neural wiring underlies gut fat storage in Caenorhabditis elegans temperature acclimation

Proc Natl Acad Sci U S A. 2022 Aug 9;119(32):e2203121119. doi: 10.1073/pnas.2203121119. Epub 2022 Aug 1.

Abstract

Animals maintain the ability to survive and reproduce by acclimating to environmental temperatures. We showed here that Caenorhabditis elegans exhibited temperature acclimation plasticity, which was regulated by a head-tail-head neural circuitry coupled with gut fat storage. After experiencing cold, C. elegans individuals memorized the experience and were prepared against subsequent cold stimuli. The cyclic adenosine monophosphate (cAMP) response element-binding protein (CREB) regulated temperature acclimation in the ASJ thermosensory neurons and RMG head interneurons, where it modulated ASJ thermosensitivity in response to past cultivation temperature. The PVQ tail interneurons mediated the communication between ASJ and RMG via glutamatergic signaling. Temperature acclimation occurred via gut fat storage regulation by the triglyceride lipase ATGL-1, which was activated by a neuropeptide, FLP-7, downstream of CREB. Thus, a head-tail-head neural circuit coordinated with gut fat influenced experience-dependent temperature acclimation.

Keywords: CREB; Caenorhabditis elegans; neural circuit; neuropeptide; temperature acclimation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acclimatization* / physiology
  • Adipose Tissue* / metabolism
  • Animals
  • Caenorhabditis elegans Proteins / metabolism
  • Caenorhabditis elegans* / anatomy & histology
  • Caenorhabditis elegans* / physiology
  • Cold Temperature*
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Digestive System* / metabolism
  • Glutamic Acid / metabolism
  • Head* / innervation
  • Interneurons / metabolism
  • Lipase / metabolism
  • Neural Pathways*
  • Neuropeptides / metabolism
  • Tail* / innervation
  • Thermosensing

Substances

  • Caenorhabditis elegans Proteins
  • Cyclic AMP Response Element-Binding Protein
  • FLP-7 protein, C elegans
  • Neuropeptides
  • Glutamic Acid
  • ATGL-1 protein, C elegans
  • Lipase