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

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

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 bZI...

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Main Authors: Wei Jiang, Yuehua Wei, Yong Long, Arthur Owen, Bingying Wang, Xuebing Wu, Shuo Luo, Yongjun Dang, Dengke K Ma
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-04-01
Series:eLife
Subjects:
hypothermia
bZIP transcription factor
ISY1 or ISY-1
ZIP-10
C. elegans screen
forward genetics
Online Access:https://elifesciences.org/articles/35037
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record_format Article
spelling doaj-d57a8eae22bf44a185594635bba730c72021-05-05T15:48:34ZengeLife Sciences Publications LtdeLife2050-084X2018-04-01710.7554/eLife.35037A genetic program mediates cold-warming response and promotes stress-induced phenoptosis in C. elegansWei Jiang0https://orcid.org/0000-0001-7615-0900Yuehua Wei1Yong Long2Arthur Owen3Bingying Wang4Xuebing Wu5https://orcid.org/0000-0003-0369-5269Shuo Luo6Yongjun Dang7https://orcid.org/0000-0001-7237-1132Dengke K Ma8https://orcid.org/0000-0002-5619-7485Cardiovascular Research Institute, University of California, San Francisco, San Francisco, United States; Key Laboratory of Metabolism and Molecular Medicine, The Ministry of Education, Fudan University, Shanghai, China; Department of Biochemistry and Molecular Biology, Shanghai Medical College, Fudan University, Shanghai, China; Department of Physiology, University of California, San Francisco, San Francisco, United StatesCardiovascular Research Institute, University of California, San Francisco, San Francisco, United States; Department of Physiology, University of California, San Francisco, San Francisco, United StatesCardiovascular Research Institute, University of California, San Francisco, San Francisco, United States; Department of Physiology, University of California, San Francisco, San Francisco, United States; State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaDepartment of Molecular Cell Biology, University of California, Berkeley, Berkeley, United StatesCardiovascular Research Institute, University of California, San Francisco, San Francisco, United States; Department of Physiology, University of California, San Francisco, San Francisco, United StatesWhitehead Institute for Biomedical Research, Massachusetts Institute of Technology, Cambridge, United StatesWhitehead Institute for Biomedical Research, Massachusetts Institute of Technology, Cambridge, United StatesKey Laboratory of Metabolism and Molecular Medicine, The Ministry of Education, Fudan University, Shanghai, China; Department of Biochemistry and Molecular Biology, Shanghai Medical College, Fudan University, Shanghai, ChinaCardiovascular Research Institute, University of California, San Francisco, San Francisco, United States; Department of Physiology, University of California, San Francisco, San Francisco, United StatesHow 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.https://elifesciences.org/articles/35037hypothermiabZIP transcription factorISY1 or ISY-1ZIP-10C. elegans screenforward genetics
collection DOAJ
language English
format Article
sources DOAJ
author Wei Jiang
Yuehua Wei
Yong Long
Arthur Owen
Bingying Wang
Xuebing Wu
Shuo Luo
Yongjun Dang
Dengke K Ma
spellingShingle Wei Jiang
Yuehua Wei
Yong Long
Arthur Owen
Bingying Wang
Xuebing Wu
Shuo Luo
Yongjun Dang
Dengke K Ma
A genetic program mediates cold-warming response and promotes stress-induced phenoptosis in C. elegans
eLife
hypothermia
bZIP transcription factor
ISY1 or ISY-1
ZIP-10
C. elegans screen
forward genetics
author_facet Wei Jiang
Yuehua Wei
Yong Long
Arthur Owen
Bingying Wang
Xuebing Wu
Shuo Luo
Yongjun Dang
Dengke K Ma
author_sort Wei Jiang
title A genetic program mediates cold-warming response and promotes stress-induced phenoptosis in C. elegans
title_short A genetic program mediates cold-warming response and promotes stress-induced phenoptosis in C. elegans
title_full A genetic program mediates cold-warming response and promotes stress-induced phenoptosis in C. elegans
title_fullStr A genetic program mediates cold-warming response and promotes stress-induced phenoptosis in C. elegans
title_full_unstemmed A genetic program mediates cold-warming response and promotes stress-induced phenoptosis in C. elegans
title_sort genetic program mediates cold-warming response and promotes stress-induced phenoptosis in c. elegans
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2018-04-01
description 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.
topic hypothermia
bZIP transcription factor
ISY1 or ISY-1
ZIP-10
C. elegans screen
forward genetics
url https://elifesciences.org/articles/35037
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