The Na+-K+-ATPase is needed in glia of touch receptors for responses to touch in C. elegans

J Neurophysiol. 2020 May 1;123(5):2064-2074. doi: 10.1152/jn.00636.2019. Epub 2020 Apr 15.

Abstract

Four of the five types of mammalian mechanosensors are composed of nerve endings and accessory cells. In Caenorhabditis elegans we showed that glia support the function of nose touch neurons via the activity of glial Na+ and K+ channels. We show here that a third regulator of Na+ and K+, the Na+-K+-ATPase, is needed in glia of nose touch neurons for touch. Importantly, we show that two Na+-K+-ATPase genes are needed for the function rather than structural integrity and that their ion transport activity is crucial for touch. Finally, when glial Na+-K+-ATPase genes are knocked out, touch can be restored by activation of a third Na+-K+-ATPase. Taken together, these data show the requirement in glia of touch neurons of the function of the Na+-K+-ATPase. These data underscore the importance of the homeostasis of Na+ and K+, most likely in the space surrounding touch neurons, in touch sensation, a function that might be conserved across species.NEW & NOTEWORTHY Increasing evidence supports that accessory cells in mechanosensors regulate neuronal output; however, the glial molecular mechanisms that control this regulation are not fully understood. We show here in Caenorhabditis elegans that specific glial Na+-K+-ATPase genes are needed for nose touch-avoidance behavior. Our data support the requirement of these Na+-K+-ATPases for homeostasis of Na+ and K+ in nose touch receptors. Our data add to our understanding of glial regulation of mechanosensors.

Keywords: C. elegans; Na+-K+-ATPase; glia; mechanosensation; touch.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Behavior, Animal / physiology*
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / genetics
  • Neuroglia / enzymology
  • Neuroglia / metabolism*
  • Potassium / metabolism*
  • Sensory Receptor Cells / physiology*
  • Sodium / metabolism*
  • Sodium-Potassium-Exchanging ATPase / metabolism*
  • Touch / physiology*

Substances

  • Caenorhabditis elegans Proteins
  • Sodium
  • Sodium-Potassium-Exchanging ATPase
  • Potassium