MicroRNAs downregulate Bag of marbles to ensure proper terminal differentiation in the Drosophila male germline

Development (Cambridge)

Volumn 140, Issue 1, 2013, Pages 23-30

  Eun, Suk Ho ^a   Stoiber, Patrick M ^a   Wright, Heather J ^b   McMurdie, Karen E ^a   Choi, Caitlin H ^a   Gan, Qiang ^a,c   Lim, Cindy ^a   Chen, Xin ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SAN JOSE STATE UNIVERSITY   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bag of marbles; Differentiation; Drosophila; MicroRNA; Post transcriptional regulation; Spermatocyte

Indexed keywords

BAG OF MARBLES PROTEIN; CELL PROTEIN; MICRORNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; GENE EXPRESSION; GENE MUTATION; GENE REPRESSION; MALE; NONHUMAN; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; SPERMATID; SPERMATOCYTE; SPERMATOGONIUM; STEM CELL;

ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; DOWN-REGULATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MALE; MICRORNAS; MOLECULAR SEQUENCE DATA; SPERMATIDS;

EID: 84870725410     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.086397     Document Type: Article

References (48)

1. Bartel, D. P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233.
2. Chen, D. and McKearin, D. (2003a). Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr. Biol. 13, 1786-1791.
3. Chen, D. and McKearin, D. M. (2003b). A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development 130, 1159-1170.
4. Chen, X., Hiller, M., Sancak, Y. and Fuller, M. T. (2005). Tissue-specific TAFs counteract Polycomb to turn on terminal differentiation. Science 310, 869-872.
5. Chen, X., Lu, C., Prado, J. R., Eun, S. H. and Fuller, M. T. (2011). Sequential changes at differentiation gene promoters as they become active in a stem cell lineage. Development 138, 2441-2450.
6. Clarke, M. F. and Fuller, M. (2006). Stem cells and cancer: two faces of eve. Cell 124, 1111-1115.
7. Ebert, M. S., Neilson, J. R. and Sharp, P. A. (2007). MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 4, 721-726.
8. Fabrizio, J. J., Hime, G., Lemmon, S. K. and Bazinet, C. (1998). Genetic dissection of sperm individualization in Drosophila melanogaster. Development 125, 1833-1843.
9. Förstemann, K., Tomari, Y., Du, T., Vagin, V. V., Denli, A. M., Bratu, D. P., Klattenhoff, C., Theurkauf, W. E. and Zamore, P. D. (2005). Normal microRNA maturation and germ-line stem cell maintenance requires Loquacious, a double-stranded RNA-binding domain protein. PLoS Biol. 3, e236.
10. Fuller, M. T. (1993). Spermatogenesis. In The Development of Drosophila melanogaster. Vol. I (ed. M. Bate and A. Martinez-Arias), pp. 71-147. Cold Spring Harbor, New York: Cold Spring Harbor Press.
11. Gan, Q., Chepelev, I., Wei, G., Tarayrah, L., Cui, K., Zhao, K. and Chen, X. (2010). Dynamic regulation of alternative splicing and chromatin structure in Drosophila gonads revealed by RNA-seq. Cell Res. 20, 763-783.
12. Gangaraju, V. K. and Lin, H. (2009). MicroRNAs: key regulators of stem cells. Nat. Rev. Mol. Cell Biol. 10, 116-125.
13. Gönczy, P., Matunis, E. and DiNardo, S. (1997). bag-of-marbles and benign gonial cell neoplasm act in the germline to restrict proliferation during Drosophila spermatogenesis. Development 124, 4361-4371.
14. Groth, A. C., Fish, M., Nusse, R. and Calos, M. P. (2004). Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166, 1775-1782.
15. He, L. and Hannon, G. J. (2004). MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 5, 522-531.
16. Hesketh, J. (2004). 3_-Untranslated regions are important in mRNA localization and translation: lessons from selenium and metallothionein. Biochem. Soc. Trans. 32, 990-993.
17. Insco, M. L., Leon, A., Tam, C. H., McKearin, D. M. and Fuller, M. T. (2009). Accumulation of a differentiation regulator specifies transit amplifying division number in an adult stem cell lineage. Proc. Natl. Acad. Sci. USA 106, 22311-22316.
18. Jin, Z. and Xie, T. (2007). Dcr-1 maintains Drosophila ovarian stem cells. Curr. Biol. 17, 539-544.
19. Kawase, E., Wong, M. D., Ding, B. C. and Xie, T. (2004). Gbb/Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development 131, 1365-1375.
20. Kiger, A. A., Jones, D. L., Schulz, C., Rogers, M. B. and Fuller, M. T. (2001). Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science 294, 2542-2545.
21. Knoblich, J. A. (2008). Mechanisms of asymmetric stem cell division. Cell 132, 583-597.
22. Lai, E. C. (2002). Micro RNAs are complementary to 3_ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genet. 30, 363-364.
23. Lee, Y. S., Nakahara, K., Pham, J. W., Kim, K., He, Z., Sontheimer, E. J. and Carthew, R. W. (2004). Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117, 69-81.
24. Li, Y., Minor, N. T., Park, J. K., McKearin, D. M. and Maines, J. Z. (2009). Bam and Bgcn antagonize Nanos-dependent germ-line stem cell maintenance. Proc. Natl. Acad. Sci. USA 106, 9304-9309.
25. Li, Y., Maines, J. Z., Tastan, O. Y., McKearin, D. M. and Buszczak, M. (2012). Mei-P26 regulates the maintenance of ovarian germline stem cells by promoting BMP signaling. Development 139, 1547-1556.
26. Lindsley, D. L. and Tokyuasu, K. T. (1980). Spermatogenesis. In Genetics and Biology of Drosophila (ed. M. Ashburner and. T. R. Wright), pp. 225-294. New York, NY: Academic Press.
27. Loya, C. M., Lu, C. S., Van Vactor, D. and Fulga, T. A. (2009). Transgenic microRNA inhibition with spatiotemporal specificity in intact organisms. Nat. Methods 6, 897-903.
28. Lu, J., Getz, G., Miska, E. A., Alvarez-Saavedra, E., Lamb, J., Peck, D., Sweet-Cordero, A., Ebert, B. L., Mak, R. H., Ferrando, A. A. et al. (2005). MicroRNA expression profiles classify human cancers. Nature 435, 834-838.
29. Markstein, M., Pitsouli, C., Villalta, C., Celniker, S. E. and Perrimon, N. (2008). Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nat. Genet. 40, 476-483.
30. McKearin, D. and Ohlstein, B. (1995). A role for the Drosophila bag-of-marbles protein in the differentiation of cystoblasts from germline stem cells. Development 121, 2937-2947.
31. McKearin, D. M. and Spradling, A. C. (1990). bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev. 4, 2242-2251.
32. Monk, A. C., Siddall, N. A., Volk, T., Fraser, B., Quinn, L. M., McLaughlin, E. A. and Hime, G. R. (2010). HOW is required for stem cell maintenance in the Drosophila testis and for the onset of transit-amplifying divisions. Cell Stem Cell 6, 348-360.
33. Morris, C. A., Benson, E. and White-Cooper, H. (2009). Determination of gene expression patterns using in situ hybridization to Drosophila testes. Nat. Protoc. 4, 1807-1819.
34. Morrison, S. J. and Spradling, A. C. (2008). Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132, 598-611.
35. Noguchi, T. and Miller, K. G. (2003). A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster. Development 130, 1805-1816.
36. Ohlstein, B. and McKearin, D. (1997). Ectopic expression of the Drosophila Bam protein eliminates oogenic germline stem cells. Development 124, 3651-3662.
37. Park, J. K., Liu, X., Strauss, T. J., McKearin, D. M. and Liu, Q. (2007). The miRNA pathway intrinsically controls self-renewal of Drosophila germline stem cells. Curr. Biol. 17, 533-538.
38. Pek, J. W., Lim, A. K. and Kai, T. (2009). Drosophila maelstrom ensures proper germline stem cell lineage differentiation by repressing microRNA-7. Dev. Cell 17, 417-424.
39. Schulz, C., Kiger, A. A., Tazuke, S. I., Yamashita, Y. M., Pantalena-Filho, L. C., Jones, D. L., Wood, C. G. and Fuller, M. T. (2004). A misexpression screen reveals effects of bag-of-marbles and TGF beta class signaling on the Drosophila male germ-line stem cell lineage. Genetics 167, 707-723.
40. Secombe, J., Li, L., Carlos, L. and Eisenman, R. N. (2007). The Trithorax group protein Lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes Dev. 21, 537-551.
41. Sheng, X. R., Brawley, C. M. and Matunis, E. L. (2009). Dedifferentiating spermatogonia outcompete somatic stem cells for niche occupancy in the Drosophila testis. Cell Stem Cell 5, 191-203.
42. Shivdasani, A. A. and Ingham, P. W. (2003). Regulation of stem cell maintenance and transit amplifying cell proliferation by tgf-beta signaling in Drosophila spermatogenesis. Curr. Biol. 13, 2065-2072.
43. Stark, A., Brennecke, J., Bushati, N., Russell, R. B. and Cohen, S. M. (2005). Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3_UTR evolution. Cell 123, 1133-1146.
44. Tokusumi, T., Tokusumi, Y., Hopkins, D. W., Shoue, D. A., Corona, L. and Schulz, R. A. (2011). Germ line differentiation factor Bag of Marbles is a regulator of hematopoietic progenitor maintenance during Drosophila hematopoiesis. Development 138, 3879-3884.
45. Van Doren, M., Williamson, A. L. and Lehmann, R. (1998). Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr. Biol. 8, 243-246.
46. Volinia, S., Calin, G. A., Liu, C. G., Ambs, S., Cimmino, A., Petrocca, F., Visone, R., Iorio, M., Roldo, C., Ferracin, M. et al. (2006). A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. USA 103, 2257-2261.
47. White-Cooper, H. (2010). Molecular mechanisms of gene regulation during Drosophila spermatogenesis. Reproduction 139, 11-21.
48. Yang, L., Chen, D., Duan, R., Xia, L., Wang, J., Qurashi, A., Jin, P. and Chen, D. (2007). Argonaute 1 regulates the fate of germline stem cells in Drosophila. Development 134, 4265-4272.