Temperature-dependent RNA editing in octopus extensively recodes the neural proteome

Matthew A. Birk, Noa Liscovitch-Brauer, Matthew J. Dominguez, Sean McNeme, Yang Yue, J. Damon Hoff, Itamar Twersky, Kristen J. Verhey, R. Bryan Sutton, Eli Eisenberg, Joshua J.C. Rosenthal

Research output: Contribution to journalArticlepeer-review

Abstract

In poikilotherms, temperature changes challenge the integration of physiological function. Within the complex nervous systems of the behaviorally sophisticated coleoid cephalopods, these problems are substantial. RNA editing by adenosine deamination is a well-positioned mechanism for environmental acclimation. We report that the neural proteome of Octopus bimaculoides undergoes massive reconfigurations via RNA editing following a temperature challenge. Over 13,000 codons are affected, and many alter proteins that are vital for neural processes. For two highly temperature-sensitive examples, recoding tunes protein function. For synaptotagmin, a key component of Ca2+-dependent neurotransmitter release, crystal structures and supporting experiments show that editing alters Ca2+ binding. For kinesin-1, a motor protein driving axonal transport, editing regulates transport velocity down microtubules. Seasonal sampling of wild-caught specimens indicates that temperature-dependent editing occurs in the field as well. These data show that A-to-I editing tunes neurophysiological function in response to temperature in octopus and most likely other coleoids.

Original languageEnglish (US)
Pages (from-to)2544-2555.e13
JournalCell
Volume186
Issue number12
DOIs
StatePublished - Jun 8 2023
Externally publishedYes

Keywords

  • ADAR
  • RNA editing
  • RNA modifications
  • acclimation
  • cephalopod
  • epitranscriptome
  • kinesin
  • neural plasticity
  • synaptotagmin
  • temperature

ASJC Scopus subject areas

  • General Biochemistry, Genetics and Molecular Biology

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