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Cited by 5Developmental Biology and Gene RegulationWnt/β-catenin signaling in development and cancerGenomics and Chromatin Dynamics

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Dynamic compartmentalization of the pro-invasive transcription factor NHR-67 reveals a role for Groucho in regulating a proliferative-invasive cellular switch in C. elegans

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Medwig-Kinney, Taylor N, Kinney, Brian A, Martinez, Michael AQ, Yee, Callista, Sirota, Sydney S, Mullarkey, Angelina A, Somineni, Neha, Hippler, Justin, Zhang, Wan, Shen, Kang, Hammell, Christopher, Pani, Ariel M, Matus, David Q·2023·eLife
DOI 10.7554/elife.84355.3

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Abstract

A growing body of evidence suggests that cell division and basement membrane invasion are mutually exclusive cellular behaviors. How cells switch between proliferative and invasive states is not well understood. Here, we investigated this dichotomy in vivo by examining two cell types in the developing Caenorhabditis elegans somatic gonad that derive from equipotent progenitors, but exhibit distinct cell behaviors: the post-mitotic, invasive anchor cell and the neighboring proliferative, non-invasive ventral uterine (VU) cells. We show that the fates of these cells post-specification are more plastic than previously appreciated and that levels of NHR-67 are important for discriminating between invasive and proliferative behavior. Transcription of NHR-67 is downregulated following post-translational degradation of its direct upstream regulator, HLH-2 (E/Daughterless) in VU cells. In the nuclei of VU cells, residual NHR-67 protein is compartmentalized into discrete punctae that are dynamic over the cell cycle and exhibit liquid-like properties. By screening for proteins that colocalize with NHR-67 punctae, we identified new regulators of uterine cell fate maintenance: homologs of the transcriptional co-repressor Groucho (UNC-37 and LSY-22), as well as the TCF/LEF homolog POP-1. We propose a model in which the association of NHR-67 with the Groucho/TCF complex suppresses the default invasive state in non-invasive cells, which complements transcriptional regulation to add robustness to the proliferative-invasive cellular switch in vivo.

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Metadata

Authors
Medwig-Kinney, T. N., Kinney, B. A., Martinez, M. A., Yee, C., Sirota, S. S., Mullarkey, A. A., Somineni, N., Hippler, J., Zhang, W., Shen, K., Hammell, C., Pani, A. M., & Matus, D. Q.
Affiliations
  • Stony Brook University (US)
  • Cold Spring Harbor Laboratory (US)
  • Howard Hughes Medical Institute (US)
  • University of Virginia (US)
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2023-12-01
Volume
12
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.84355.3
OpenAlex
W4389236467
Cited by
5
References
5
Citations by year
2026: 3 · 2025: 1 · 2024: 1
FWCI
0.44
Type
journal article
Language
en
Open access
Licence
Locations
eLife (publishedVersion, cc-by)
Funders
  • National Institutes of Health (R01GM121597, F31HD100091, F30CA257383, R01GM117406, R35GM142880)
  • Damon Runyon Cancer Research Foundation (DRR-47-17)
  • Stony Brook University (Presidential Critical Research Funds)
  • Human Frontier Science Program (LTF000127/2016-L)
  • Howard Hughes Medical Institute (Investigator)
  • National Science Foundation (2217560)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords
Groucho, POP-1, anchor cell, basement membrane invasion, nuclear compartmentalization, corepressors, cell fate maintenance, Caenorhabditis elegans

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