The Bantam MicroRNA is Associated with Drosophila Fragile X Mental Retardation Protein and Regulates the Fate of Germline Stem Cells

Overview

Journal PLoS Genet

Specialty Genetics

Date 2009 Apr 4

PMID 19343200

Citations 61

Authors

Yingyue Yang

Shunliang Xu

Laixin Xia

Jun Wang

Shengmei Wen

Peng Jin

Dahua Chen

Affiliations

Soon will be listed here.

Abstract

Fragile X syndrome, a common form of inherited mental retardation, is caused by the loss of fragile X mental retardation protein (FMRP). We have previously demonstrated that dFmr1, the Drosophila ortholog of the fragile X mental retardation 1 gene, plays a role in the proper maintenance of germline stem cells in Drosophila ovary; however, the molecular mechanism behind this remains elusive. In this study, we used an immunoprecipitation assay to reveal that specific microRNAs (miRNAs), particularly the bantam miRNA (bantam), are physically associated with dFmrp in ovary. We show that, like dFmr1, bantam is not only required for repressing primordial germ cell differentiation, it also functions as an extrinsic factor for germline stem cell maintenance. Furthermore, we find that bantam genetically interacts with dFmr1 to regulate the fate of germline stem cells. Collectively, our results support the notion that the FMRP-mediated translation pathway functions through specific miRNAs to control stem cell regulation.

Citing Articles

Communication between the stem cell niche and an adjacent differentiation niche through miRNA and EGFR signaling orchestrates exit from the stem cell state in the Drosophila ovary.

Chen J, Li C, Sheng Y, Zhang J, Pang L, Dong Z PLoS Biol. 2024; 22(3):e3002515.

PMID: 38512963 PMC: 10986965. DOI: 10.1371/journal.pbio.3002515.

Yang D, Xiao F, Li J, Wang S, Fan X, Ni Q Front Genet. 2023; 14:1096902.

PMID: 36926584 PMC: 10012872. DOI: 10.3389/fgene.2023.1096902.

Noncoding RNA Regulation of Hormonal and Metabolic Systems in the Fruit Fly .

Chan K, Chan T, Bendena W, Hui J Metabolites. 2023; 13(2).

PMID: 36837772 PMC: 9967906. DOI: 10.3390/metabo13020152.

Drosophila FMRP controls miR-276-mediated regulation of nejire mRNA for space-filling dendrite development.

Li H, Gavis E G3 (Bethesda). 2022; 12(11).

PMID: 36102801 PMC: 9635640. DOI: 10.1093/g3journal/jkac239.

Evidence of the Physical Interaction between Rpl22 and the Transposable Element , a Heterochromatic Transposon of .

Berloco M, Minervini C, Moschetti R, Palazzo A, Viggiano L, Marsano R Genes (Basel). 2021; 12(12).

PMID: 34946947 PMC: 8701128. DOI: 10.3390/genes12121997.

References

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

Xu K, Bogert B, Li W, Su K, Lee A, Gao F . The fragile X-related gene affects the crawling behavior of Drosophila larvae by regulating the mRNA level of the DEG/ENaC protein pickpocket1. Curr Biol. 2004; 14(12):1025-34. DOI: 10.1016/j.cub.2004.05.055. View

Zhang Y, Bailey A, Matthies H, Renden R, Smith M, Speese S . Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell. 2001; 107(5):591-603. DOI: 10.1016/s0092-8674(01)00589-x. View

Jin P, Alisch R, Warren S . RNA and microRNAs in fragile X mental retardation. Nat Cell Biol. 2004; 6(11):1048-53. DOI: 10.1038/ncb1104-1048. View

Lin H . The stem-cell niche theory: lessons from flies. Nat Rev Genet. 2002; 3(12):931-40. DOI: 10.1038/nrg952. View

Jin Z, Xie T . Dcr-1 maintains Drosophila ovarian stem cells. Curr Biol. 2007; 17(6):539-44. DOI: 10.1016/j.cub.2007.01.050. View

Hatfield S, Shcherbata H, Fischer K, Nakahara K, Carthew R, Ruohola-Baker H . Stem cell division is regulated by the microRNA pathway. Nature. 2005; 435(7044):974-8. DOI: 10.1038/nature03816. View

Lin H . Cell biology of stem cells: an enigma of asymmetry and self-renewal. J Cell Biol. 2008; 180(2):257-60. PMC: 2213586. DOI: 10.1083/jcb.200712159. View

Alisch R, Jin P, Epstein M, Caspary T, Warren S . Argonaute2 is essential for mammalian gastrulation and proper mesoderm formation. PLoS Genet. 2008; 3(12):e227. PMC: 2323323. DOI: 10.1371/journal.pgen.0030227. View

10.

Penagarikano O, Mulle J, Warren S . The pathophysiology of fragile x syndrome. Annu Rev Genomics Hum Genet. 2007; 8:109-29. DOI: 10.1146/annurev.genom.8.080706.092249. View

11.

Zarnescu D, Jin P, Betschinger J, Nakamoto M, Wang Y, Dockendorff T . Fragile X protein functions with lgl and the par complex in flies and mice. Dev Cell. 2004; 8(1):43-52. DOI: 10.1016/j.devcel.2004.10.020. View

12.

Costa A, Wang Y, Dockendorff T, Erdjument-Bromage H, Tempst P, Schedl P . The Drosophila fragile X protein functions as a negative regulator in the orb autoregulatory pathway. Dev Cell. 2005; 8(3):331-42. DOI: 10.1016/j.devcel.2005.01.011. View

13.

Ishizuka A, Siomi M, Siomi H . A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 2002; 16(19):2497-508. PMC: 187455. DOI: 10.1101/gad.1022002. View

14.

Spradling A, Kai T . Stem cells find their niche. Nature. 2001; 414(6859):98-104. DOI: 10.1038/35102160. View

15.

Jin P, Zarnescu D, Ceman S, Nakamoto M, Mowrey J, Jongens T . Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat Neurosci. 2004; 7(2):113-7. DOI: 10.1038/nn1174. View

16.

Lin H . Stem cells: to be and not to be. Nature. 2003; 425(6956):353-5. DOI: 10.1038/425353a. View

17.

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

18.

Dockendorff T, Su H, McBride S, Yang Z, Choi C, Siwicki K . Drosophila lacking dfmr1 activity show defects in circadian output and fail to maintain courtship interest. Neuron. 2002; 34(6):973-84. DOI: 10.1016/s0896-6273(02)00724-9. View

19.

Chen D, McKearin D . Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr Biol. 2003; 13(20):1786-91. DOI: 10.1016/j.cub.2003.09.033. View

20.

Garber K, Smith K, Reines D, Warren S . Transcription, translation and fragile X syndrome. Curr Opin Genet Dev. 2006; 16(3):270-5. DOI: 10.1016/j.gde.2006.04.010. View