A genetic program mediates cold-warming response and promotes stress-induced phenoptosis in C. elegans

Elife. 2018 Apr 17:7:e35037. doi: 10.7554/eLife.35037.

Abstract

How multicellular organisms respond to and are impacted by severe hypothermic stress is largely unknown. From C. elegans screens for mutants abnormally responding to cold-warming stimuli, we identify a molecular genetic pathway comprising ISY-1, a conserved uncharacterized protein, and ZIP-10, a bZIP-type transcription factor. ISY-1 gatekeeps the ZIP-10 transcriptional program by regulating the microRNA mir-60. Downstream of ISY-1 and mir-60, zip-10 levels rapidly and specifically increase upon transient cold-warming exposure. Prolonged zip-10 up-regulation induces several protease-encoding genes and promotes stress-induced organismic death, or phenoptosis, of C. elegans. zip-10 deficiency confers enhanced resistance to prolonged cold-warming stress, more prominently in adults than larvae. We conclude that the ZIP-10 genetic program mediates cold-warming response and may have evolved to promote wild-population kin selection under resource-limiting and thermal stress conditions.

Keywords: C. elegans; C. elegans screen; ISY1 or ISY-1; ZIP-10; bZIP transcription factor; chromosomes; forward genetics; gene expression; hypothermia.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic-Leucine Zipper Transcription Factors / metabolism*
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans / radiation effects*
  • Caenorhabditis elegans Proteins / metabolism*
  • Cold Temperature*
  • Gene Expression Regulation*
  • Gene Regulatory Networks
  • Stress, Physiological*

Substances

  • Basic-Leucine Zipper Transcription Factors
  • Caenorhabditis elegans Proteins
  • zip-10 protein, C elegans