Literature DB >> 32008902

Niche Cell Wrapping Ensures Primordial Germ Cell Quiescence and Protection from Intercellular Cannibalism.

Daniel C McIntyre1, Jeremy Nance2.   

Abstract

Niche cells often wrap membrane extensions around stem cell surfaces. Niche wrapping has been proposed to retain stem cells in defined positions and affect signaling [e.g., 1, 2]. To test these hypotheses and uncover additional functions of wrapping, we investigated niche wrapping of primordial germ cells (PGCs) in the C. elegans embryonic gonad primordium. The gonad primordium contains two PGCs that are wrapped individually by two somatic gonad precursor cells (SGPs). SGPs are known to promote PGC survival during embryogenesis and exit from quiescence after hatching, although how they do so is unknown [3]. Here, we identify two distinct functions of SGP wrapping that are critical for PGC quiescence and survival. First, niche cell wrapping templates a laminin-based basement membrane around the gonad primordium. Laminin and the basement membrane receptor dystroglycan function to maintain niche cell wrapping, which is critical for normal gonad development. We find that laminin also preserves PGC quiescence during embryogenesis. Exit from quiescence following laminin depletion requires glp-1/Notch and is accompanied by inappropriate activation of the GLP-1 target sygl-1 in PGCs. Independent of basement membrane, SGP wrapping performs a second, crucial function to ensure PGC survival. Endodermal cells normally engulf and degrade large lobes extended by the PGCs [4]. When SGPs are absent, we show that endodermal cells can inappropriately engulf and cannibalize the PGC cell body. Our findings demonstrate how niche cell wrapping protects germ cells by manipulating their signaling environment and by shielding germ cells from unwanted cellular interactions that can compromise their survival.
Copyright © 2019 Elsevier Ltd. All rights reserved.

Entities:  

Keywords:  Notch; basement membrane; cell death; dystroglycan; laminin; niche; primordial germ cell; quiescence; stem cell; wrapping

Mesh:

Year:  2020        PMID: 32008902      PMCID: PMC7044025          DOI: 10.1016/j.cub.2019.12.021

Source DB:  PubMed          Journal:  Curr Biol        ISSN: 0960-9822            Impact factor:   10.834


  36 in total

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Journal:  Development       Date:  2003-07       Impact factor: 6.868

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Journal:  Development       Date:  2012-04-25       Impact factor: 6.868

4.  Canonical notch signaling functions as a commitment switch in the epidermal lineage.

Authors:  Cédric Blanpain; William E Lowry; H Amalia Pasolli; Elaine Fuchs
Journal:  Genes Dev       Date:  2006-11-01       Impact factor: 11.361

5.  A possible role for FRM-1, a C. elegans FERM family protein, in embryonic development.

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Journal:  Mol Cells       Date:  2011-03-24       Impact factor: 5.034

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Authors:  Kaleb M Naegeli; Eric Hastie; Aastha Garde; Zheng Wang; Daniel P Keeley; Kacy L Gordon; Ariel M Pani; Laura C Kelley; Meghan A Morrissey; Qiuyi Chi; Bob Goldstein; David R Sherwood
Journal:  Dev Cell       Date:  2017-11-20       Impact factor: 12.270

7.  Roles of the Wnt effector POP-1/TCF in the C. elegans endomesoderm specification gene network.

Authors:  Melissa Owraghi; Gina Broitman-Maduro; Thomas Luu; Heather Roberson; Morris F Maduro
Journal:  Dev Biol       Date:  2009-10-07       Impact factor: 3.582

8.  Genetic control of programmed cell death in the nematode C. elegans.

Authors:  H M Ellis; H R Horvitz
Journal:  Cell       Date:  1986-03-28       Impact factor: 41.582

9.  The union of somatic gonad precursors and primordial germ cells during Caenorhabditis elegans embryogenesis.

Authors:  Monica R Rohrschneider; Jeremy Nance
Journal:  Dev Biol       Date:  2013-04-04       Impact factor: 3.582

10.  Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences.

Authors:  C C Mello; J M Kramer; D Stinchcomb; V Ambros
Journal:  EMBO J       Date:  1991-12       Impact factor: 11.598

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Journal:  Nat Commun       Date:  2021-11-25       Impact factor: 14.919

2.  Independent regulation of mitochondrial DNA quantity and quality in Caenorhabditis elegans primordial germ cells.

Authors:  Aaron Z A Schwartz; Nikita Tsyba; Yusuff Abdu; Maulik R Patel; Jeremy Nance
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3.  DAF-18/PTEN inhibits germline zygotic gene activation during primordial germ cell quiescence.

Authors:  Amanda L Fry; Amy K Webster; Julia Burnett; Rojin Chitrakar; L Ryan Baugh; E Jane Albert Hubbard
Journal:  PLoS Genet       Date:  2021-07-21       Impact factor: 5.917

  3 in total

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