A Damage Sensor Associated with the Cuticle Coordinates Three Core Environmental Stress Responses in Caenorhabditis elegans

Extracellular matrix barriers and inducible cytoprotective genes form successive lines of defense against chemical and microbial environmental stressors. The barrier in nematodes is a collagenous extracellular matrix called the cuticle. In , disruption of some cuticle collagen genes activates osmoly...

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Published inGenetics (Austin) Vol. 208; no. 4; pp. 1467 - 1482
Main Authors Dodd, William, Tang, Lanlan, Lone, Jean-Christophe, Wimberly, Keon, Wu, Cheng-Wei, Consalvo, Claudia, Wright, Joni E, Pujol, Nathalie, Choe, Keith P
Format Journal Article
LanguageEnglish
Published United States Genetics Society of America 01.04.2018
Oxford University Press
Subjects
Animals
Antiinfectives and antibacterials
Antioxidants
Biochemistry, Molecular Biology
Caenorhabditis elegans
Caenorhabditis elegans - physiology
Caenorhabditis elegans Proteins - genetics
Caenorhabditis elegans Proteins - metabolism
Cellular stress response
Collagen
Cuticles
Damage
Detoxification
DNA-Binding Proteins - genetics
DNA-Binding Proteins - metabolism
Environment
Environmental stress
Epidermis
Extracellular matrix
Extracellular Matrix - metabolism
Furrows
Gene expression
Gene Expression Profiling
Gene-Environment Interaction
Genes
Genetics
Genomics
Glycerol
High-Throughput Nucleotide Sequencing
Immunology
Inactivation, Metabolic - genetics
Innate immunity
Integrity
Investigations
Kinases
Life Sciences
Mammals
Microorganisms
Nematodes
Osmosis
Pathogens
Proteins
Sensors
Stress response
Stress, Physiological
Stresses
Transcription factors
Transcription Factors - genetics
Transcription Factors - metabolism
Transcriptome
Transgenes
Worms
collagen
antimicrobial response
osmotic stress
damage sensor
detoxification
Damage sensor
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Abstract Extracellular matrix barriers and inducible cytoprotective genes form successive lines of defense against chemical and microbial environmental stressors. The barrier in nematodes is a collagenous extracellular matrix called the cuticle. In , disruption of some cuticle collagen genes activates osmolyte and antimicrobial response genes. Physical damage to the epidermis also activates antimicrobial responses. Here, we assayed the effect of knocking down genes required for cuticle and epidermal integrity on diverse cellular stress responses. We found that disruption of specific bands of collagen, called annular furrows, coactivates detoxification, hyperosmotic, and antimicrobial response genes, but not other stress responses. Disruption of other cuticle structures and epidermal integrity does not have the same effect. Several transcription factors act downstream of furrow loss. SKN-1/Nrf and ELT-3/GATA are required for detoxification, SKN-1/Nrf is partially required for the osmolyte response, and STA-2/Stat and ELT-3/GATA for antimicrobial gene expression. Our results are consistent with a cuticle-associated damage sensor that coordinates detoxification, hyperosmotic, and antimicrobial responses through overlapping, but distinct, downstream signaling.
AbstractList Abstract Although extracellular matrices function as protective barriers to many types of environmental insult, their role in sensing stress and regulating adaptive gene induction responses has not been studied carefully... Extracellular matrix barriers and inducible cytoprotective genes form successive lines of defense against chemical and microbial environmental stressors. The barrier in nematodes is a collagenous extracellular matrix called the cuticle. In Caenorhabditis elegans, disruption of some cuticle collagen genes activates osmolyte and antimicrobial response genes. Physical damage to the epidermis also activates antimicrobial responses. Here, we assayed the effect of knocking down genes required for cuticle and epidermal integrity on diverse cellular stress responses. We found that disruption of specific bands of collagen, called annular furrows, coactivates detoxification, hyperosmotic, and antimicrobial response genes, but not other stress responses. Disruption of other cuticle structures and epidermal integrity does not have the same effect. Several transcription factors act downstream of furrow loss. SKN-1/Nrf and ELT-3/GATA are required for detoxification, SKN-1/Nrf is partially required for the osmolyte response, and STA-2/Stat and ELT-3/GATA for antimicrobial gene expression. Our results are consistent with a cuticle-associated damage sensor that coordinates detoxification, hyperosmotic, and antimicrobial responses through overlapping, but distinct, downstream signaling.
Although extracellular matrices function as protective barriers to many types of environmental insult, their role in sensing stress and regulating adaptive gene induction responses has not been studied carefully... Extracellular matrix barriers and inducible cytoprotective genes form successive lines of defense against chemical and microbial environmental stressors. The barrier in nematodes is a collagenous extracellular matrix called the cuticle. In Caenorhabditis elegans , disruption of some cuticle collagen genes activates osmolyte and antimicrobial response genes. Physical damage to the epidermis also activates antimicrobial responses. Here, we assayed the effect of knocking down genes required for cuticle and epidermal integrity on diverse cellular stress responses. We found that disruption of specific bands of collagen, called annular furrows, coactivates detoxification, hyperosmotic, and antimicrobial response genes, but not other stress responses. Disruption of other cuticle structures and epidermal integrity does not have the same effect. Several transcription factors act downstream of furrow loss. SKN-1 /Nrf and ELT-3 /GATA are required for detoxification, SKN-1 /Nrf is partially required for the osmolyte response, and STA-2 /Stat and ELT-3 /GATA for antimicrobial gene expression. Our results are consistent with a cuticle-associated damage sensor that coordinates detoxification, hyperosmotic, and antimicrobial responses through overlapping, but distinct, downstream signaling.
Although extracellular matrices function as protective barriers to many types of environmental insult, their role in sensing stress and regulating adaptive gene induction responses has not been studied carefully...Extracellular matrix barriers and inducible cytoprotective genes form successive lines of defense against chemical and microbial environmental stressors. The barrier in nematodes is a collagenous extracellular matrix called the cuticle. In Caenorhabditis elegans, disruption of some cuticle collagen genes activates osmolyte and antimicrobial response genes. Physical damage to the epidermis also activates antimicrobial responses. Here, we assayed the effect of knocking down genes required for cuticle and epidermal integrity on diverse cellular stress responses. We found that disruption of specific bands of collagen, called annular furrows, coactivates detoxification, hyperosmotic, and antimicrobial response genes, but not other stress responses. Disruption of other cuticle structures and epidermal integrity does not have the same effect. Several transcription factors act downstream of furrow loss. SKN-1/Nrf and ELT-3/GATA are required for detoxification, SKN-1/Nrf is partially required for the osmolyte response, and STA-2/Stat and ELT-3/GATA for antimicrobial gene expression. Our results are consistent with a cuticle-associated damage sensor that coordinates detoxification, hyperosmotic, and antimicrobial responses through overlapping, but distinct, downstream signaling.
Extracellular matrix barriers and inducible cytoprotective genes form successive lines of defense against chemical and microbial environmental stressors. The barrier in nematodes is a collagenous extracellular matrix called the cuticle. In Caenorhabditis elegans, disruption of some cuticle collagen genes activates osmolyte and antimicrobial response genes. Physical damage to the epidermis also activates antimicrobial responses. Here, we assayed the effect of knocking down genes required for cuticle and epidermal integrity on diverse cellular stress responses. We found that disruption of specific bands of collagen, called annular furrows, coactivates detoxification, hyperosmotic, and antimicrobial response genes, but not other stress responses. Disruption of other cuticle structures and epidermal integrity does not have the same effect. Several transcription factors act downstream of furrow loss. SKN-1/ Nrf and ELT-3/GATA are required for detoxification, SKN-1/Nrf is partially required for the osmolyte response, and STA-2/Stat and ELT3/GATA for antimicrobial gene expression. Our results are consistent with a cuticle-associated damage sensor that coordinates detoxification, hyperosmotic, and antimicrobial responses through overlapping, but distinct, downstream signaling.
Extracellular matrix barriers and inducible cytoprotective genes form successive lines of defense against chemical and microbial environmental stressors. The barrier in nematodes is a collagenous extracellular matrix called the cuticle. In , disruption of some cuticle collagen genes activates osmolyte and antimicrobial response genes. Physical damage to the epidermis also activates antimicrobial responses. Here, we assayed the effect of knocking down genes required for cuticle and epidermal integrity on diverse cellular stress responses. We found that disruption of specific bands of collagen, called annular furrows, coactivates detoxification, hyperosmotic, and antimicrobial response genes, but not other stress responses. Disruption of other cuticle structures and epidermal integrity does not have the same effect. Several transcription factors act downstream of furrow loss. SKN-1/Nrf and ELT-3/GATA are required for detoxification, SKN-1/Nrf is partially required for the osmolyte response, and STA-2/Stat and ELT-3/GATA for antimicrobial gene expression. Our results are consistent with a cuticle-associated damage sensor that coordinates detoxification, hyperosmotic, and antimicrobial responses through overlapping, but distinct, downstream signaling.
Extracellular matrix barriers and inducible cytoprotective genes form successive lines of defense against chemical and microbial environmental stressors. The barrier in nematodes is a collagenous extracellular matrix called the cuticle. In Caenorhabditis elegans, disruption of some cuticle collagen genes activates osmolyte and antimicrobial response genes. Physical damage to the epidermis also activates antimicrobial responses. Here, we assayed the effect of knocking down genes required for cuticle and epidermal integrity on diverse cellular stress responses. We found that disruption of specific bands of collagen, called annular furrows, coactivates detoxification, hyperosmotic, and antimicrobial response genes, but not other stress responses. Disruption of other cuticle structures and epidermal integrity does not have the same effect. Several transcription factors act downstream of furrow loss. SKN-1/Nrf and ELT-3/GATA are required for detoxification, SKN-1/Nrf is partially required for the osmolyte response, and STA-2/Stat and ELT-3/GATA for antimicrobial gene expression. Our results are consistent with a cuticle-associated damage sensor that coordinates detoxification, hyperosmotic, and antimicrobial responses through overlapping, but distinct, downstream signaling.
Author Lone, Jean-Christophe
Wimberly, Keon
Pujol, Nathalie
Tang, Lanlan
Dodd, William
Wu, Cheng-Wei
Choe, Keith P
Consalvo, Claudia
Wright, Joni E
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  surname: Dodd
  fullname: Dodd, William
  organization: Department of Biology, University of Florida, Gainesville, Florida 32611
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  givenname: Lanlan
  surname: Tang
  fullname: Tang, Lanlan
  organization: Department of Biology, University of Florida, Gainesville, Florida 32611
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  givenname: Jean-Christophe
  surname: Lone
  fullname: Lone, Jean-Christophe
  organization: Aix Marseille University, CNRS, INSERM, CIML, Marseille, France
– sequence: 4
  givenname: Keon
  surname: Wimberly
  fullname: Wimberly, Keon
  organization: Department of Biology, University of Florida, Gainesville, Florida 32611
– sequence: 5
  givenname: Cheng-Wei
  surname: Wu
  fullname: Wu, Cheng-Wei
  organization: Department of Biology, University of Florida, Gainesville, Florida 32611
– sequence: 6
  givenname: Claudia
  surname: Consalvo
  fullname: Consalvo, Claudia
  organization: Department of Biology, University of Florida, Gainesville, Florida 32611
– sequence: 7
  givenname: Joni E
  surname: Wright
  fullname: Wright, Joni E
  organization: Department of Biology, University of Florida, Gainesville, Florida 32611
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  givenname: Nathalie
  orcidid: 0000-0001-8889-3197
  surname: Pujol
  fullname: Pujol, Nathalie
  email: pujol@ciml.univ-mrs.fr, kchoe@ufl.edu
  organization: Aix Marseille University, CNRS, INSERM, CIML, Marseille, France pujol@ciml.univ-mrs.fr kchoe@ufl.edu
– sequence: 9
  givenname: Keith P
  surname: Choe
  fullname: Choe, Keith P
  email: pujol@ciml.univ-mrs.fr, kchoe@ufl.edu
  organization: Department of Biology, University of Florida, Gainesville, Florida 32611 pujol@ciml.univ-mrs.fr kchoe@ufl.edu
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29487136$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright Copyright © 2018 by the Genetics Society of America.
Copyright Genetics Society of America Apr 2018
Distributed under a Creative Commons Attribution 4.0 International License
Copyright © 2018 by the Genetics Society of America 2018
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IEDL.DBID 8C1
ISSN 1943-2631
0016-6731
IngestDate Tue Sep 17 20:35:00 EDT 2024
Thu Oct 03 06:34:22 EDT 2024
Fri Aug 16 10:34:07 EDT 2024
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Tue Aug 27 13:46:08 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
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Issue 4
Keywords collagen
antimicrobial response
osmotic stress
damage sensor
detoxification
Damage sensor
Language English
License Copyright © 2018 by the Genetics Society of America.
Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
Available freely online through the author-supported open access option.
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content type line 23
These authors contributed equally to this work.
ORCID 0000-0001-8889-3197
OpenAccessLink https://pubmed.ncbi.nlm.nih.gov/PMC5887142
PMID 29487136
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Oxford University Press
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Snippet Extracellular matrix barriers and inducible cytoprotective genes form successive lines of defense against chemical and microbial environmental stressors. The...
Abstract Although extracellular matrices function as protective barriers to many types of environmental insult, their role in sensing stress and regulating...
Although extracellular matrices function as protective barriers to many types of environmental insult, their role in sensing stress and regulating adaptive...
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StartPage 1467
SubjectTerms Animals
Antiinfectives and antibacterials
Antioxidants
Biochemistry, Molecular Biology
Caenorhabditis elegans
Caenorhabditis elegans - physiology
Caenorhabditis elegans Proteins - genetics
Caenorhabditis elegans Proteins - metabolism
Cellular stress response
Collagen
Cuticles
Damage
Detoxification
DNA-Binding Proteins - genetics
DNA-Binding Proteins - metabolism
Environment
Environmental stress
Epidermis
Extracellular matrix
Extracellular Matrix - metabolism
Furrows
Gene expression
Gene Expression Profiling
Gene-Environment Interaction
Genes
Genetics
Genomics
Glycerol
High-Throughput Nucleotide Sequencing
Immunology
Inactivation, Metabolic - genetics
Innate immunity
Integrity
Investigations
Kinases
Life Sciences
Mammals
Microorganisms
Nematodes
Osmosis
Pathogens
Proteins
Sensors
Stress response
Stress, Physiological
Stresses
Transcription factors
Transcription Factors - genetics
Transcription Factors - metabolism
Transcriptome
Transgenes
Worms
Title A Damage Sensor Associated with the Cuticle Coordinates Three Core Environmental Stress Responses in Caenorhabditis elegans
URI https://www.ncbi.nlm.nih.gov/pubmed/29487136
https://www.proquest.com/docview/2031266282/abstract/
https://search.proquest.com/docview/2009217411
https://hal.science/hal-02108810
https://pubmed.ncbi.nlm.nih.gov/PMC5887142
Volume 208
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