Literature DB >> 26577869

Cell cycle features of C. elegans germline stem/progenitor cells vary temporally and spatially.

Debasmita Roy1, David Michaelson1, Tsivia Hochman2, Anthony Santella3, Zhirong Bao3, Judith D Goldberg2, E Jane Albert Hubbard4.   

Abstract

Many organisms accumulate a pool of germline stem cells during development that is maintained in later life. The dynamics of establishment, expansion and homeostatic maintenance of this pool are subject to both developmental and physiological influences including the availability of a suitable niche microenvironment, nutritional status, and age. Here, we investigated the dynamics of germline proliferation during stages of expansion and homeostasis, using the C. elegans germ line as a model. The vast majority of germ cells in the proliferative zone are in interphase stages of mitosis (G1, S, G2) rather than in the active mitotic (M) phase. We examined mitotic index and DNA content, comparing different life stages, mutants, and physiological conditions. We found that germ cells in larval stages cycle faster than in adult stages, but that this difference could not be attributed to sexual fate of the germ cells. We also found that larval germ cells exhibit a lower average DNA content compared to adult germ cells. We extended our analysis to consider the effects of distance from the niche and further found that the spatial pattern of DNA content differs between larval and adult stages in the wild type and among mutants in pathways that interfere with cell cycle progression, cell fate, or both. Finally, we characterized expansion of the proliferative pool of germ cells during adulthood, using a regeneration paradigm (ARD recovery) in which animals are starved and re-fed. We compared adult stage regeneration and larval stage expansion, and found that the adult germ line is capable of rapid accumulation but does not sustain a larval-level mitotic index nor does it recapitulate the larval pattern of DNA content. The regenerated germ line does not reach the number of proliferative zone nuclei seen in the continuously fed adult. Taken together, our results suggest that cell cycle dynamics are under multiple influences including distance from the niche, age and/or maturation of the germ line, nutrition and, possibly, latitude for physical expansion.
Copyright © 2015 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Adult reproductive diapause; Cell fate; Insulin; Irises; Notch; S6 Kinase

Mesh:

Substances:

Year:  2015        PMID: 26577869      PMCID: PMC4827254          DOI: 10.1016/j.ydbio.2015.10.031

Source DB:  PubMed          Journal:  Dev Biol        ISSN: 0012-1606            Impact factor:   3.582


  39 in total

Review 1.  Maintenance of C. elegans.

Authors:  Theresa Stiernagle
Journal:  WormBook       Date:  2006-02-11

2.  Cyclin E and CDK-2 regulate proliferative cell fate and cell cycle progression in the C. elegans germline.

Authors:  Paul M Fox; Valarie E Vought; Momoyo Hanazawa; Min-Ho Lee; Eleanor M Maine; Tim Schedl
Journal:  Development       Date:  2011-06       Impact factor: 6.868

3.  Isolation and characterization of mutations causing abnormal eversion of the vulva in Caenorhabditis elegans.

Authors:  G Seydoux; C Savage; I Greenwald
Journal:  Dev Biol       Date:  1993-06       Impact factor: 3.582

4.  Insulin signaling promotes germline proliferation in C. elegans.

Authors:  David Michaelson; Dorota Z Korta; Yossi Capua; E Jane Albert Hubbard
Journal:  Development       Date:  2010-02       Impact factor: 6.868

5.  Cellular analyses of the mitotic region in the Caenorhabditis elegans adult germ line.

Authors:  Sarah L Crittenden; Kimberly A Leonhard; Dana T Byrd; Judith Kimble
Journal:  Mol Biol Cell       Date:  2006-05-03       Impact factor: 4.138

6.  Progression from a stem cell-like state to early differentiation in the C. elegans germ line.

Authors:  Olivier Cinquin; Sarah L Crittenden; Dyan E Morgan; Judith Kimble
Journal:  Proc Natl Acad Sci U S A       Date:  2010-01-13       Impact factor: 11.205

7.  Analysis of Germline Stem Cell Differentiation Following Loss of GLP-1 Notch Activity in Caenorhabditis elegans.

Authors:  Paul M Fox; Tim Schedl
Journal:  Genetics       Date:  2015-07-08       Impact factor: 4.562

8.  Germline stem cells and their regulation in the nematode Caenorhabditis elegans.

Authors:  Aaron Kershner; Sarah L Crittenden; Kyle Friend; Erika B Sorensen; Douglas F Porter; Judith Kimble
Journal:  Adv Exp Med Biol       Date:  2013       Impact factor: 2.622

9.  The genetics of Caenorhabditis elegans.

Authors:  S Brenner
Journal:  Genetics       Date:  1974-05       Impact factor: 4.562

10.  Control of Caenorhabditis elegans germ-line stem-cell cycling speed meets requirements of design to minimize mutation accumulation.

Authors:  Michael Chiang; Amanda Cinquin; Adrian Paz; Edward Meeds; Christopher A Price; Max Welling; Olivier Cinquin
Journal:  BMC Biol       Date:  2015-07-18       Impact factor: 7.431

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  14 in total

Review 1.  Starvation Responses Throughout the Caenorhabditis elegans Life Cycle.

Authors:  L Ryan Baugh; Patrick J Hu
Journal:  Genetics       Date:  2020-12       Impact factor: 4.562

2.  Rapid population-wide declines in stem cell number and activity during reproductive aging in C. elegans.

Authors:  Zuzana Kocsisova; Kerry Kornfeld; Tim Schedl
Journal:  Development       Date:  2019-04-23       Impact factor: 6.868

Review 3.  The Interaction Between Niche and Hematopoietic Stem Cells.

Authors:  Chaoyu Wang; Chen Tian; Yizhuo Zhang
Journal:  Indian J Hematol Blood Transfus       Date:  2016-01-12       Impact factor: 0.900

Review 4.  Developmental Control of the Cell Cycle: Insights from Caenorhabditis elegans.

Authors:  Edward T Kipreos; Sander van den Heuvel
Journal:  Genetics       Date:  2019-03       Impact factor: 4.562

5.  Dafachronic acid inhibits C. elegans germ cell proliferation in a DAF-12-dependent manner.

Authors:  Madhumati Mukherjee; Snehal N Chaudhari; Riju S Balachandran; Alexandra S Vagasi; Edward T Kipreos
Journal:  Dev Biol       Date:  2017-10-21       Impact factor: 3.582

6.  Identification of regulators of germ stem cell enwrapment by its niche in C. elegans.

Authors:  Lara M Linden; Kacy L Gordon; Ariel M Pani; Sara G Payne; Aastha Garde; Dane Burkholder; Qiuyi Chi; Bob Goldstein; David R Sherwood
Journal:  Dev Biol       Date:  2017-06-23       Impact factor: 3.582

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

Authors:  Kacy L Gordon; Jay W Zussman; Xin Li; Camille Miller; David R Sherwood
Journal:  Elife       Date:  2020-07-21       Impact factor: 8.140

8.  Antagonistic control of Caenorhabditis elegans germline stem cell proliferation and differentiation by PUF proteins FBF-1 and FBF-2.

Authors:  Xiaobo Wang; Mary Ellenbecker; Benjamin Hickey; Nicholas J Day; Emily Osterli; Mikaya Terzo; Ekaterina Voronina
Journal:  Elife       Date:  2020-08-17       Impact factor: 8.140

Review 9.  Biology of the Caenorhabditis elegans Germline Stem Cell System.

Authors:  E Jane Albert Hubbard; Tim Schedl
Journal:  Genetics       Date:  2019-12       Impact factor: 4.562

Review 10.  Germline Stem and Progenitor Cell Aging in C. elegans.

Authors:  Theadora Tolkin; E Jane Albert Hubbard
Journal:  Front Cell Dev Biol       Date:  2021-07-08
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