Nonrandom Sister Chromatid Segregation of Sex Chromosomes in Drosophila Male Germline Stem Cells

Overview

Journal Chromosome Res

Date 2013 May 18

PMID 23681657

Citations 6

Authors

Yukiko M Yamashita

Affiliations

Soon will be listed here.

Abstract

Sister chromatids are the product of DNA replication, which is assumed to be a very precise process. Therefore, sister chromatids should be exact copies of each other. However, reports have indicated that sister chromatids are segregated nonrandomly during cell division, suggesting that sister chromatids are not the same, although their DNA sequences are the same. Researchers have speculated that stem cells may retain template strands to avoid replication-induced mutations. An alternative proposal is that cells may segregate distinct epigenetic information carried on sister chromatids. Recently, we found that Drosophila male germline stem cells segregate sister chromatids of X and Y chromosomes with a strong bias. We discuss this finding in relation to existing models for nonrandom sister chromatid segregation.

Citing Articles

A genome-wide library of MADM mice for single-cell genetic mosaic analysis.

Contreras X, Amberg N, Davaatseren A, Hansen A, Sonntag J, Andersen L Cell Rep. 2021; 35(12):109274.

PMID: 34161767 PMC: 8317686. DOI: 10.1016/j.celrep.2021.109274.

Asymmetric Histone Inheritance in Asymmetrically Dividing Stem Cells.

Wooten M, Ranjan R, Chen X Trends Genet. 2019; 36(1):30-43.

PMID: 31753528 PMC: 6925335. DOI: 10.1016/j.tig.2019.10.004.

Asymmetric Centromeres Differentially Coordinate with Mitotic Machinery to Ensure Biased Sister Chromatid Segregation in Germline Stem Cells.

Ranjan R, Snedeker J, Chen X Cell Stem Cell. 2019; 25(5):666-681.e5.

PMID: 31564548 PMC: 6842444. DOI: 10.1016/j.stem.2019.08.014.

As the fat flies: The dynamic lipid droplets of Drosophila embryos.

Welte M Biochim Biophys Acta. 2015; 1851(9):1156-85.

PMID: 25882628 PMC: 4516585. DOI: 10.1016/j.bbalip.2015.04.002.

Gathering up meiotic telomeres: a novel function of the microtubule-organizing center.

Yamamoto A Cell Mol Life Sci. 2014; 71(11):2119-34.

PMID: 24413667 PMC: 11113538. DOI: 10.1007/s00018-013-1548-1.

References

Tulin A, Kogan G, Filipp D, Balakireva M, Gvozdev V . Heterochromatic Stellate gene cluster in Drosophila melanogaster: structure and molecular evolution. Genetics. 1997; 146(1):253-62. PMC: 1207940. DOI: 10.1093/genetics/146.1.253. View

Morrison S, Spradling A . Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell. 2008; 132(4):598-611. PMC: 4505728. DOI: 10.1016/j.cell.2008.01.038. View

Falconer E, Chavez E, Henderson A, Poon S, McKinney S, Brown L . Identification of sister chromatids by DNA template strand sequences. Nature. 2009; 463(7277):93-7. PMC: 3757939. DOI: 10.1038/nature08644. View

Conboy M, Karasov A, Rando T . High incidence of non-random template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS Biol. 2007; 5(5):e102. PMC: 1852584. DOI: 10.1371/journal.pbio.0050102. View

Fung J, Marshall W, Dernburg A, Agard D, Sedat J . Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations. J Cell Biol. 1998; 141(1):5-20. PMC: 2132734. DOI: 10.1083/jcb.141.1.5. View

Razafsky D, Hodzic D . Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J Cell Biol. 2009; 186(4):461-72. PMC: 2733748. DOI: 10.1083/jcb.200906068. View

Malik H, Henikoff S . Major evolutionary transitions in centromere complexity. Cell. 2009; 138(6):1067-82. DOI: 10.1016/j.cell.2009.08.036. View

Leatherman J, DiNardo S . Germline self-renewal requires cyst stem cells and stat regulates niche adhesion in Drosophila testes. Nat Cell Biol. 2010; 12(8):806-11. PMC: 2917891. DOI: 10.1038/ncb2086. View

Zemach A, McDaniel I, Silva P, Zilberman D . Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science. 2010; 328(5980):916-9. DOI: 10.1126/science.1186366. View

10.

Losick V, Morris L, Fox D, Spradling A . Drosophila stem cell niches: a decade of discovery suggests a unified view of stem cell regulation. Dev Cell. 2011; 21(1):159-71. PMC: 6894370. DOI: 10.1016/j.devcel.2011.06.018. View

11.

Schepers A, Vries R, van den Born M, van de Wetering M, Clevers H . Lgr5 intestinal stem cells have high telomerase activity and randomly segregate their chromosomes. EMBO J. 2011; 30(6):1104-9. PMC: 3061032. DOI: 10.1038/emboj.2011.26. View

12.

Yamashita Y, Fuller M . Asymmetric centrosome behavior and the mechanisms of stem cell division. J Cell Biol. 2008; 180(2):261-6. PMC: 2213579. DOI: 10.1083/jcb.200707083. View

13.

Cairns J . Mutation selection and the natural history of cancer. Nature. 1975; 255(5505):197-200. DOI: 10.1038/255197a0. View

14.

Fei J, Huttner W . Nonselective sister chromatid segregation in mouse embryonic neocortical precursor cells. Cereb Cortex. 2009; 19 Suppl 1:i49-54. DOI: 10.1093/cercor/bhp043. View

15.

Merok J, Lansita J, Tunstead J, Sherley J . Cosegregation of chromosomes containing immortal DNA strands in cells that cycle with asymmetric stem cell kinetics. Cancer Res. 2002; 62(23):6791-5. View

16.

Yamashita Y, Mahowald A, Perlin J, Fuller M . Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science. 2007; 315(5811):518-21. PMC: 2563045. DOI: 10.1126/science.1134910. View

17.

Tran V, Lim C, Xie J, Chen X . Asymmetric division of Drosophila male germline stem cell shows asymmetric histone distribution. Science. 2012; 338(6107):679-82. PMC: 3532436. DOI: 10.1126/science.1226028. View

18.

Quyn A, Appleton P, Carey F, Steele R, Barker N, Clevers H . Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell. 2010; 6(2):175-81. DOI: 10.1016/j.stem.2009.12.007. View

19.

Yadlapalli S, Yamashita Y . Chromosome-specific nonrandom sister chromatid segregation during stem-cell division. Nature. 2013; 498(7453):251-4. PMC: 3711665. DOI: 10.1038/nature12106. View

20.

Shinin V, Gayraud-Morel B, Gomes D, Tajbakhsh S . Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol. 2006; 8(7):677-87. DOI: 10.1038/ncb1425. View