Innexin function dictates the spatial relationship between distal somatic cells in the Caenorhabditis elegans gonad without impacting the germline stem cell pool

Theadora Tolkin, Ariz Mohammad, Todd A. Starich, Ken C.Q. Nguyen, David H. Hall, Tim Schedl, E. Jane Albert Hubbard, David Greenstein

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

Abstract

Gap-junctional signaling mediates myriad cellular interactions in metazoans. Yet, how gap junctions control the positioning of cells in organs is not well understood. Innexins compose gap junctions in invertebrates and affect organ architecture. Here, we investigate the roles of gapjunctions in controlling distal somatic gonad architecture and its relationship to underlying germline stem cells in Caenorhabditis elegans. We show that a reduction of soma–germline gap-junctional activity causes displacement of distal sheath cells (Sh1) towards the distal end of the gonad. We confirm, by live imaging, transmission electron microscopy, and antibody staining, that bare regions—lacking somatic gonadal cell coverage of germ cells—are present between the distal tip cell (DTC) and Sh1, and we show that an innexin fusion protein used in a prior study encodes an antimorphic gap junction subunit that mispositions Sh1. We determine that, contrary to the model put forth in the prior study based on this fusion protein, Sh1 mispositioning does not markedly alter the position of the borders of the stem cell pool nor of the progenitor cell pool. Together, these results demonstrate that gap junctions can control the position of Sh1, but that Sh1 position is neither relevant for GLP-1/Notch signaling nor for the exit of germ cells from the stem cell pool.

Original languageEnglish (US)
Article numbere74955
JournaleLife
Volume11
DOIs
StatePublished - Sep 2022

Bibliographical note

Funding Information:
Funder Grant reference number Author American Cancer Society PF-19-231-01-CSM Theadora Tolkin National Institutes of Health National Institutes of Health National Institutes of Health National Institutes of Health National Institutes of Health National Institutes of Health R35GM134876 R01AG065672 R01GM100756 R01GM57173 R35GM144029 R24OD010943 E Jane Albert Hubbard E Jane Albert Hubbard Tim Schedl David Greenstein David Greenstein David H Hall The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Funding Information:
We thank Gabriela Huelgas-Morales for discussions and constructive suggestions during the course of this work, Swathi Arur for the affinity purified anti-GFP antibody, Verena Jantsch for anti-pSUN-1 antibody, Edward Kipreos for anti-CYE-1 antibody. We thank Michael Cammer and the NYU Langone Microscopy Core for experimental and technical support; the NYU Langone Microscopy Laboratory is partially supported by the Cancer Center Support Grant P30CA016087 at the Laura and Isaac Perl-mutter Cancer Center. We thank WormBase. We thank Kacy Gordon and the CGC (which is funded by NIH Office of Research Infrastructure Programs P40 OD010440), for strains. NIH P30HD071593 and 1S10OD016214-01A1 supports electron microscopy in DHH laboratory.

Publisher Copyright:
© Tolkin, Mohammad et al.

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