Stem cell niche exit in C. elegans via orientation and segregation of daughter cells by a cryptic cell outside the niche

  1. Kacy L Gordon  Is a corresponding author
  2. Jay W Zussman
  3. Xin Li
  4. Camille Miller
  5. David R Sherwood
  1. University of North Carolina at Chapel Hill, United States
  2. Duke University, United States

Abstract

Stem cells reside in and rely upon their niche to maintain stemness but must balance self-renewal with the production of daughters that leave the niche to differentiate. We discovered a mechanism of stem cell niche exit in the canonical C. elegans distal tip cell (DTC) germ stem cell niche mediated by previously unobserved, thin, membranous protrusions of the adjacent somatic gonad cell pair (Sh1). A disproportionate number of germ cell divisions were observed at the DTC-Sh1 interface. Stem-like and differentiating cell fates segregated across this boundary. Spindles polarized, pairs of daughter cells oriented between the DTC and Sh1, and Sh1 grew over the Sh1-facing daughter. Impeding Sh1 growth by RNAi to cofilin and Arp2/3 perturbed the DTC-Sh1 interface, reduced germ cell proliferation, and shifted a differentiation marker. Because Sh1 membrane protrusions eluded detection for decades, it is possible that similar structures actively regulate niche exit in other systems.

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Author details

  1. Kacy L Gordon

    Biology, University of North Carolina at Chapel Hill, Chapel Hill, United States
    For correspondence
    kacy.gordon@unc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0967-4020
  2. Jay W Zussman

    Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Xin Li

    Biology, University of North Carolina at Chapel Hill, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Camille Miller

    Biology, University of North Carolina at Chapel Hill, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. David R Sherwood

    Department of Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2245-2334

Funding

National Institute of General Medical Sciences (R01 GM079320)

  • David R Sherwood

National Institute of General Medical Sciences (R35 MIRA GM118049)

  • David R Sherwood

National Institute of General Medical Sciences (GM121015-01)

  • Kacy L Gordon

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Yukiko M Yamashita, University of Michigan, United States

Version history

  1. Received: February 25, 2020
  2. Accepted: July 17, 2020
  3. Accepted Manuscript published: July 21, 2020 (version 1)
  4. Version of Record published: September 2, 2020 (version 2)

Copyright

© 2020, Gordon et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Kacy L Gordon
  2. Jay W Zussman
  3. Xin Li
  4. Camille Miller
  5. David R Sherwood
(2020)
Stem cell niche exit in C. elegans via orientation and segregation of daughter cells by a cryptic cell outside the niche
eLife 9:e56383.
https://doi.org/10.7554/eLife.56383

Share this article

https://doi.org/10.7554/eLife.56383

Further reading

    1. Developmental Biology
    2. Stem Cells and Regenerative Medicine
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    The Caenorhabditis elegans adult hermaphrodite germline is surrounded by a thin tube formed by somatic sheath cells that support germ cells as they mature from the stem-like mitotic state through meiosis, gametogenesis, and ovulation. Recently, we discovered that the distal Sh1 sheath cells associate with mitotic germ cells as they exit the niche Gordon et al., 2020. Here, we report that these sheath-associated germ cells differentiate first in animals with temperature-sensitive mutations affecting germ cell state, and stem-like germ cells are maintained distal to the Sh1 boundary. We analyze several markers of the distal sheath, which is best visualized with endogenously tagged membrane proteins, as overexpressed fluorescent proteins fail to localize to distal membrane processes and can cause gonad morphology defects. However, such reagents with highly variable expression can be used to determine the relative positions of the two Sh1 cells, one of which often extends further distal than the other.

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