Stage-specific Differences in the Requirements for Germline Stem Cell Maintenance in the Drosophila Ovary

Overview

Journal Cell Stem Cell

Publisher Cell Press

Specialty Cell Biology

Date 2008 Jan 24

PMID 18213359

Citations 35

Authors

Halyna R Shcherbata

Ellen J Ward

Karin A Fischer

Jenn-Yah Yu

Steven H Reynolds

Chun-Hong Chen

Peizhang Xu

Bruce A Hay

Hannele Ruohola-Baker

Affiliations

Soon will be listed here.

Abstract

In this study, we uncover a role for microRNAs in Drosophila germline stem cell (GSC) maintenance. Disruption of Dicer-1 function in GSCs during adult life results in GSC loss. Surprisingly, however, loss of Dicer-1 during development does not result in a GSC maintenance defect, although a defect is seen if both Dicer-1 and Dicer-2 function are disrupted. Loss of the bantam microRNA mimics the Dicer-1 maintenance defect when induced in adult GSCs, suggesting that bantam plays a key role in GSC self-renewal. Mad, a component of the TGF-beta pathway, behaves similarly to Dicer-1: adult GSC maintenance requires Mad if it is lost during adult life, but not if it is lost during pupal development. Overall, these results show stage-specific differential sensitivity of GSC maintenance to certain perturbations, and suggest that there may be Dcr-2 dependent redundancy of GSC maintenance mechanisms during development that is lost in later life.

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References

Bilen J, Liu N, Burnett B, Pittman R, Bonini N . MicroRNA pathways modulate polyglutamine-induced neurodegeneration. Mol Cell. 2006; 24(1):157-63. DOI: 10.1016/j.molcel.2006.07.030. View

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

Xie T, Spradling A . decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell. 1998; 94(2):251-60. DOI: 10.1016/s0092-8674(00)81424-5. View

Xu T, Rubin G . Analysis of genetic mosaics in developing and adult Drosophila tissues. Development. 1993; 117(4):1223-37. DOI: 10.1242/dev.117.4.1223. View

Boiani M, Gentile L, Gambles V, Cavaleri F, Redi C, Scholer H . Variable reprogramming of the pluripotent stem cell marker Oct4 in mouse clones: distinct developmental potentials in different culture environments. Stem Cells. 2005; 23(8):1089-104. DOI: 10.1634/stemcells.2004-0352. View

Meshorer E, Yellajoshula D, George E, Scambler P, Brown D, Misteli T . Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell. 2006; 10(1):105-16. PMC: 1868458. DOI: 10.1016/j.devcel.2005.10.017. View

Pal-Bhadra M, Leibovitch B, Gandhi S, Chikka M, Rao M, Bhadra U . Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science. 2004; 303(5658):669-72. DOI: 10.1126/science.1092653. View

Nolo R, Morrison C, Tao C, Zhang X, Halder G . The bantam microRNA is a target of the hippo tumor-suppressor pathway. Curr Biol. 2006; 16(19):1895-904. DOI: 10.1016/j.cub.2006.08.057. View

Shcherbata H, Hatfield S, Ward E, Reynolds S, Fischer K, Ruohola-Baker H . The MicroRNA pathway plays a regulatory role in stem cell division. Cell Cycle. 2005; 5(2):172-5. DOI: 10.4161/cc.5.2.2343. View

10.

Jordan K, Clegg N, Blasi J, Morimoto A, Sen J, Stein D . The homeobox gene mirror links EGF signalling to embryonic dorso-ventral axis formation through notch activation. Nat Genet. 2000; 24(4):429-33. DOI: 10.1038/74294. View

11.

Li Z, Li L . Understanding hematopoietic stem-cell microenvironments. Trends Biochem Sci. 2006; 31(10):589-95. DOI: 10.1016/j.tibs.2006.08.001. View

12.

Fuchs E, Tumbar T, Guasch G . Socializing with the neighbors: stem cells and their niche. Cell. 2004; 116(6):769-78. DOI: 10.1016/s0092-8674(04)00255-7. View

13.

Brennecke J, Hipfner D, Stark A, Russell R, Cohen S . bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell. 2003; 113(1):25-36. DOI: 10.1016/s0092-8674(03)00231-9. View

14.

Thompson B, Cohen S . The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell. 2006; 126(4):767-74. DOI: 10.1016/j.cell.2006.07.013. View

15.

Ward E, Shcherbata H, Reynolds S, Fischer K, Hatfield S, Ruohola-Baker H . Stem cells signal to the niche through the Notch pathway in the Drosophila ovary. Curr Biol. 2006; 16(23):2352-8. DOI: 10.1016/j.cub.2006.10.022. View

16.

Zhu C, Xie T . Clonal expansion of ovarian germline stem cells during niche formation in Drosophila. Development. 2003; 130(12):2579-88. DOI: 10.1242/dev.00499. View

17.

Song X, Wong M, Kawase E, Xi R, Ding B, McCarthy J . Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development. 2004; 131(6):1353-64. DOI: 10.1242/dev.01026. View

18.

Li L, Xie T . Stem cell niche: structure and function. Annu Rev Cell Dev Biol. 2005; 21:605-31. DOI: 10.1146/annurev.cellbio.21.012704.131525. View

19.

Karres J, Hilgers V, Carrera I, Treisman J, Cohen S . The conserved microRNA miR-8 tunes atrophin levels to prevent neurodegeneration in Drosophila. Cell. 2007; 131(1):136-45. DOI: 10.1016/j.cell.2007.09.020. View

20.

Peng J, Karpen G . H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability. Nat Cell Biol. 2006; 9(1):25-35. PMC: 2819265. DOI: 10.1038/ncb1514. View