Endoribonuclease ENDU-2 regulates multiple traits including cold tolerance via cell autonomous and nonautonomous controls in Caenorhabditis elegans

Tomoyo Ujisawa, Akane Ohta, Tatsuya Ii, Yohei Minakuchi, Atsushi Toyoda, Miki Ii, and Atsushi Kuhara
PNAS August 28, 2018 115 (35) 8823-8828; published ahead of print August 13, 2018 https://doi.org/10.1073/pnas.1808634115

  1. Edited by Martin Chalfie, Columbia University, New York, NY, and approved July 24, 2018 (received for review May 24, 2018)

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Significance

Environmental temperature acclimation is essential to animal survival, yet thermoregulation mechanisms remain poorly understood. In this study, we describe Ca2+-dependent endoribonuclease (EndoU) ENDU-2 located in ADL chemosensory neurons and specific muscle cells as a regulator of multiple pleiotropic phenomena including cold tolerance, life span, and brood size through cell-autonomous and cell-nonautonomous pathways in nematode Caenorhabditis elegans. Ca2+ imaging revealed ADL temperature response to be the result of transient receptor potential (TRP) channel activity and regulated by ENDU-2 via cell-autonomous and cell-nonautonomous pathways. Transcriptome analysis revealed that ENDU-2 influences expression of the caspase gene ced-3. Moreover, ENDU-2 downregulates cold tolerance and synaptic remodeling in the dorsal nerve cord through caspase signaling. We therefore propose a model for cold tolerance regulation that occurs via EndoU action.

Abstract

Environmental temperature acclimation is essential to animal survival, yet thermoregulation mechanisms remain poorly understood. We demonstrate cold tolerance in Caenorhabditis elegans as regulated by paired ADL chemosensory neurons via Ca2+-dependent endoribonuclease (EndoU) ENDU-2. Loss of ENDU-2 function results in life span, brood size, and synaptic remodeling abnormalities in addition to enhanced cold tolerance. Enzymatic ENDU-2 defects localized in the ADL and certain muscle cells led to increased cold tolerance in endu-2 mutants. Ca2+ imaging revealed ADL neurons were responsive to temperature stimuli through transient receptor potential (TRP) channels, concluding that ADL function requires ENDU-2 action in both cell-autonomous and cell-nonautonomous mechanisms. ENDU-2 is involved in caspase expression, which is central to cold tolerance and synaptic remodeling in dorsal nerve cord. We therefore conclude that ENDU-2 regulates cell type-dependent, cell-autonomous, and cell-nonautonomous cold tolerance.

Footnotes

  • ↵1Present address: Exploratory Research Center on Life and Living Systems, National Institutes of Natural Sciences, Okazaki, Aichi 444-8787, Japan.

  • ↵2To whom correspondence may be addressed. Email: aohta{at}center.konan-u.ac.jp or atsushi_kuhara{at}me.com.

  • ↵3Present address: Department of Biology, New Mexico Highlands University, Las Vegas, NM 87701.

  • Author contributions: T.U., A.O., A.T., M.I., and A.K. designed research; T.U., A.O., T.I., Y.M., A.T., M.I., and A.K. performed research; T.I., Y.M., A.T., M.I., and A.K. contributed new reagents/analytic tools; T.U., A.O., Y.M., A.T., M.I., and A.K. analyzed data; and T.U., A.O., A.T., M.I., and A.K. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The RNA-seq data reported in this paper have been deposited in the DNA Data Bank of Japan Sequence Read Archive (accession no. DRA006152).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1808634115/-/DCSupplemental.

Published under the PNAS license.

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Endoribonuclease ENDU-2 regulates multiple traits including cold tolerance via cell autonomous and nonautonomous controls in Caenorhabditis elegans
Tomoyo Ujisawa, Akane Ohta, Tatsuya Ii, Yohei Minakuchi, Atsushi Toyoda, Miki Ii, Atsushi Kuhara
Proceedings of the National Academy of Sciences Aug 2018, 115 (35) 8823-8828; DOI: 10.1073/pnas.1808634115
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