A Regulatory Network of Drosophila Germline Stem Cell Self-renewal

Overview

Journal Dev Cell

Publisher Cell Press

Specialties Cell Biology
Reproductive Medicine

Date 2014 Mar 1

PMID 24576427

Citations 87

Authors

Dong Yan

Ralph A Neumuller

Michael Buckner

Kathleen Ayers

Hua Li

Yanhui Hu

Donghui Yang-Zhou

Lei Pan

Xiaoxi Wang

Colleen Kelley

Arunachalam Vinayagam

Richard Binari

Sakara Randklev

Lizabeth A Perkins

Ting Xie

Lynn Cooley

Norbert Perrimon

Affiliations

Soon will be listed here.

Abstract

Stem cells possess the capacity to generate two cells of distinct fate upon division: one cell retaining stem cell identity and the other cell destined to differentiate. These cell fates are established by cell-type-specific genetic networks. To comprehensively identify components of these networks, we performed a large-scale RNAi screen in Drosophila female germline stem cells (GSCs) covering ∼25% of the genome. The screen identified 366 genes that affect GSC maintenance, differentiation, or other processes involved in oogenesis. Comparison of GSC regulators with neural stem cell self-renewal factors identifies common and cell-type-specific self-renewal genes. Importantly, we identify the histone methyltransferase Set1 as a GSC-specific self-renewal factor. Loss of Set1 in neural stem cells does not affect cell fate decisions, suggesting a differential requirement of H3K4me3 in different stem cell lineages. Altogether, our study provides a resource that will help to further dissect the networks underlying stem cell self-renewal.

Citing Articles

The evolutionary cancer genome theory and its reasoning.

Niculescu V Genet Med Open. 2024; 1(1):100809.

PMID: 39669240 PMC: 11613669. DOI: 10.1016/j.gimo.2023.100809.

The Drosophila histone methyltransferase SET1 coordinates multiple signaling pathways in regulating male germline stem cell maintenance and differentiation.

Vidaurre V, Song A, Li T, Ku W, Zhao K, Qian J Development. 2024; 151(15).

PMID: 39007366 PMC: 11369688. DOI: 10.1242/dev.202729.

A cytological F1 RNAi screen for defects in Drosophila melanogaster female meiosis.

Gilliland W, May D, Bowen A, Conger K, Elrad D, Marciniak M Genetics. 2024; 227(1).

PMID: 38531678 PMC: 11075555. DOI: 10.1093/genetics/iyae046.

The histone methyl-transferase SET1 coordinates multiple signaling pathways in regulating male germline stem cell maintenance and differentiation.

Vidaurre V, Song A, Li T, Ku W, Zhao K, Qian J bioRxiv. 2024; .

PMID: 38405894 PMC: 10888844. DOI: 10.1101/2024.02.14.580277.

Whole transcriptome screening for novel genes involved in meiosis and fertility in Drosophila melanogaster.

Sun S, Defosse T, Boyd A, Sop J, Verderose F, Surray D Sci Rep. 2024; 14(1):3602.

PMID: 38351116 PMC: 10864285. DOI: 10.1038/s41598-024-53346-z.

References

Karpiuk O, Najafova Z, Kramer F, Hennion M, Galonska C, Konig A . The histone H2B monoubiquitination regulatory pathway is required for differentiation of multipotent stem cells. Mol Cell. 2012; 46(5):705-13. DOI: 10.1016/j.molcel.2012.05.022. View

Neumuller R, Betschinger J, Fischer A, Bushati N, Poernbacher I, Mechtler K . Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature. 2008; 454(7201):241-5. PMC: 2988194. DOI: 10.1038/nature07014. View

Ding L, Paszkowski-Rogacz M, Nitzsche A, Slabicki M, Heninger A, de Vries I . A genome-scale RNAi screen for Oct4 modulators defines a role of the Paf1 complex for embryonic stem cell identity. Cell Stem Cell. 2009; 4(5):403-15. DOI: 10.1016/j.stem.2009.03.009. View

Chen D, McKearin D . A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development. 2003; 130(6):1159-70. DOI: 10.1242/dev.00325. View

Ni J, Zhou R, Czech B, Liu L, Holderbaum L, Yang-Zhou D . A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods. 2011; 8(5):405-7. PMC: 3489273. DOI: 10.1038/nmeth.1592. View

Nagengast A, Salz H . The Drosophila U2 snRNP protein U2A' has an essential function that is SNF/U2B" independent. Nucleic Acids Res. 2001; 29(18):3841-7. PMC: 55907. DOI: 10.1093/nar/29.18.3841. View

Schupbach T, Wieschaus E . Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics. 1991; 129(4):1119-36. PMC: 1204776. DOI: 10.1093/genetics/129.4.1119. View

Wang Z, Lin H . Nanos maintains germline stem cell self-renewal by preventing differentiation. Science. 2004; 303(5666):2016-9. DOI: 10.1126/science.1093983. View

Hayles J, Wood V, Jeffery L, Hoe K, Kim D, Park H . A genome-wide resource of cell cycle and cell shape genes of fission yeast. Open Biol. 2013; 3(5):130053. PMC: 3866870. DOI: 10.1098/rsob.130053. View

10.

Minakhina S, Steward R . Hematopoietic stem cells in Drosophila. Development. 2009; 137(1):27-31. PMC: 2796932. DOI: 10.1242/dev.043943. View

11.

Page S, McKim K, Deneen B, Van Hook T, Hawley R . Genetic studies of mei-P26 reveal a link between the processes that control germ cell proliferation in both sexes and those that control meiotic exchange in Drosophila. Genetics. 2000; 155(4):1757-72. PMC: 1461182. DOI: 10.1093/genetics/155.4.1757. View

12.

Wang X, Pan L, Wang S, Zhou J, McDowell W, Park J . Histone H3K9 trimethylase Eggless controls germline stem cell maintenance and differentiation. PLoS Genet. 2012; 7(12):e1002426. PMC: 3245301. DOI: 10.1371/journal.pgen.1002426. View

13.

Park J, Liu X, Strauss T, McKearin D, Liu Q . The miRNA pathway intrinsically controls self-renewal of Drosophila germline stem cells. Curr Biol. 2007; 17(6):533-8. DOI: 10.1016/j.cub.2007.01.060. View

14.

Cooley L, Kelley R, Spradling A . Insertional mutagenesis of the Drosophila genome with single P elements. Science. 1988; 239(4844):1121-8. DOI: 10.1126/science.2830671. View

15.

Tafforeau L, Zorbas C, Langhendries J, Mullineux S, Stamatopoulou V, Mullier R . The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of Pre-rRNA processing factors. Mol Cell. 2013; 51(4):539-51. DOI: 10.1016/j.molcel.2013.08.011. View

16.

Zeitlinger J, Zinzen R, Stark A, Kellis M, Zhang H, Young R . Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes Dev. 2007; 21(4):385-90. PMC: 1804326. DOI: 10.1101/gad.1509607. View

17.

Dietzl G, Chen D, Schnorrer F, Su K, Barinova Y, Fellner M . A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature. 2007; 448(7150):151-6. DOI: 10.1038/nature05954. View

18.

Ohlstein B, McKearin D . Ectopic expression of the Drosophila Bam protein eliminates oogenic germline stem cells. Development. 1997; 124(18):3651-62. DOI: 10.1242/dev.124.18.3651. View

19.

Janic A, Mendizabal L, Llamazares S, Rossell D, Gonzalez C . Ectopic expression of germline genes drives malignant brain tumor growth in Drosophila. Science. 2011; 330(6012):1824-7. DOI: 10.1126/science.1195481. View

20.

Findley S, Tamanaha M, Clegg N, Ruohola-Baker H . Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development. 2003; 130(5):859-71. DOI: 10.1242/dev.00310. View