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PreprintCited by 35Developmental Biology and Gene RegulationGenetics, Aging, and Longevity in Model OrganismsNuclear Receptors and Signaling

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NHR-23 activity is necessary for C. elegans developmental progression and apical extracellular matrix structure and function

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Johnson, Londen C., Vo, An A., Clancy, John C., Myles, Krista M., Pooranachithra, Murugesan, Aguilera, Joseph, Levenson, Max T., Wohlenberg, Chloe, Rechtsteiner, Andreas, Ragle, James Matthew, Chisholm, Andrew D., Ward, Jordan D.·2021·Development
DOI 10.1101/2021.10.27.465992PMC PMC10233720

Preprint — published as 10.1242/dev.201085

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Abstract

SUMMARY STATEMENT: This work shows how a C. elegans transcription factor controls remodeling of the apical extracellular matrix during development and in which tissues it acts. Nematode molting is a remarkable process where animals must repeatedly build a new apical extracellular matrix (aECM) beneath a previously built aECM that is subsequently shed. The nuclear hormone receptor NHR-23/NR1F1 is an important regulator of C. elegans molting. NHR-23 expression oscillates in the epidermal epithelium, and soma-specific NHR-23 depletion causes severe developmental delay and death. Tissue-specific RNAi suggests that nhr-23 acts primarily in seam and hypodermal cells. NHR-23 coordinates the expression of factors involved in molting, lipid transport/metabolism, and remodeling of the aECM. NHR-23 depletion causes dampened expression of a nas-37 promoter reporter and a loss of reporter oscillation. The cuticle collagen ROL-6 and zona pellucida protein NOAH-1 display aberrant annular localization and severe disorganization over the seam cells following NHR-23 depletion, while the expression of the adult-specific cuticle collagen BLI-1 is diminished and frequently found in patches. Consistent with these localization defects, the cuticle barrier is severely compromised when NHR-23 is depleted. Together, this work provides insight into how NHR-23 acts in the seam and hypodermal cells to coordinate aECM regeneration during development.

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Metadata

Authors
Johnson, L. C., Vo, A. A., Clancy, J. C., Myles, K. M., Pooranachithra, M., Aguilera, J., Levenson, M. T., Wohlenberg, C., Rechtsteiner, A., Ragle, J. M., Chisholm, A. D., & Ward, J. D.
Affiliations
  • University of California, Santa Cruz (US)
  • University of California San Diego (US)
Corresponding author
Ward, Jordan D.
ORCID
Venue
Development
Publisher
openRxiv
Published
2021-10-27
Volume
150
Issue
10
ISSN
0950-1991 (ISSN-L)
DOI
10.1101/2021.10.27.465992
PMC
PMC10233720
OpenAlex
W4367668415
Cited by
35
References
1
Citations by year
2026: 7 · 2025: 10 · 2024: 10 · 2023: 6 · 2022: 2
FWCI
2.94
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Development (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by)
Funders
  • National Institutes of Health (R21OD033663, IA 52242, OD010440, P40OD010440)
  • NIH Office of the Director (R21OD033663)
  • National Institute of General Medical Sciences (R01GM138701, R35GM134970, R00GM107345, T32GM133391)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Receptors and Signaling
Keywords
nuclear receptors, Caenorhabditis elegans, molting, apical extracellular matrix, seam cells, subcutaneous tissue, epidermis, cuticle collagen, lipid transport
MeSH terms
Animals, Epithelium, Extracellular Matrix, Transcription Factors, Caenorhabditis elegans, Receptors, Cytoplasmic and Nuclear, Caenorhabditis elegans Proteins

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