Without children is required for stat-mediated zfh1 transcription and for germline stem cell differentiation

Development (Cambridge)

Volumn 141, Issue 13, 2014, Pages 2602-2610

  Maimon, Iris ^a   Popliker, Malka ^a   Gilboa, Lilach ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Drosophila; GSC; Niche; Stat92E; Woc; Zfh1; ZMYM

Indexed keywords

DROSOPHILA PROTEIN; JANUS KINASE; STAT PROTEIN; STAT92E PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZFH1; UNCLASSIFIED DRUG; WITHOUT CHILDREN PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL RENEWAL; CELL STRUCTURE; CONTROLLED STUDY; DAUGHTER CELL; FEMALE; GERM CELL; GERMLINE STEM CELL; HAPLOINSUFFICIENCY; MALE; NONHUMAN; PHENOTYPE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SOMATIC CELL; UPREGULATION;

DROSOPHILA; GSC; NICHE; STAT92E; WOC; ZFH1; ZMYM;

ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; DNA PRIMERS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; OVARY; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; STAT TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84903129571     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.109611     Document Type: Article

References (48)

1. Ables, E. T. and Drummond-Barbosa, D. (2010). The steroid hormone ecdysone functions with intrinsic chromatin remodeling factors to control female germline stem cells in Drosophila. Cell Stem Cell 7, 581-592.
2. Baeg, G.-H., Zhou, R. and Perrimon, N. (2005). Genome-wide RNAi analysis of JAK/STAT signaling components in Drosophila. Genes Dev. 19, 1861-1870.
3. Brawley, C. and Matunis, E. (2004). Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 304, 1331-1334.
4. Buszczak, M., Paterno, S., Lighthouse, D., Bachman, J., Planck, J., Owen, S., Skora, A. D., Nystul, T. G., Ohlstein, B., Allen, A. et al. (2007). The Carnegie protein trap library: a versatile tool for Drosophila developmental studies. Genetics 175, 1505-1531.
5. Chen, D. and McKearin, D.(2003). Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr. Biol. 13, 1786-1791.
6. Chen, D. and McKearin, D. M. (2003). A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development 130, 1159-1170.
7. Decotto, E. and Spradling, A. C. (2005). The Drosophila ovarian and testis stem cell niches: similar somatic stem cells and signals. Dev. Cell 9, 501-510.
8. Flaherty, M. S., Salis, P., Evans, C. J., Ekas, L. A., Marouf, A., Zavadil, J., Banerjee, U. and Bach, E. A. (2010). Chinmo is a functional effector of the JAK/STAT pathway that regulates eye development, tumor formation, and stem cell self-renewal in Drosophila. Dev. Cell 18, 556-568.
9. Font-Burgada, J., Rossell, D., Auer, H. and Azorin, F. (2008). Drosophila HP1c isoform interacts with the zinc-finger proteins WOC and Relative-of-WOC to regulate gene expression. Genes Dev. 22, 3007-3023.
10. Fortini, M. E., Lai, Z. C. and Rubin, G. M. (1991). The Drosophila zfh-1 and zfh-2 genes encode novel proteins containing both zinc-finger and homeodomain motifs. Mech. Dev. 34, 113-122.
11. Fuller, M. T. and Spradling, A. C. (2007). Male and female Drosophila germline stem cells: two versions of immortality. Science 316, 402-404.
12. Gancz, D. and Gilboa, L. (2013). Insulin and Target of rapamycin signaling orchestrate the development of ovarian niche-stem cell units in Drosophila. Development 140, 4145-4154.
13. Gancz, D., Lengil, T. and Gilboa, L. (2011). Coordinated regulation of niche and stem cell precursors by hormonal signaling. PLoS Biol. 9, e1001202.
14. Gilboa, L. and Lehmann, R. (2006). Soma-germline interactions coordinate homeostasis and growth in the Drosophila gonad. Nature 443, 97-100.
15. Gilboa, L., Forbes, A., Tazuke, S. I., Fuller, M. T. and Lehmann, R. (2003). Germline stem cell differentiation in Drosophila requires gap junctions and proceeds via an intermediate state. Development 130, 6625-6634.
16. Harris, R.E. and Ashe, H.L.(2011). Cease and desist: modulating short-range Dpp signalling in the stem-cell niche. EMBO Rep. 12, 519-526.
17. Issigonis, M., Tulina, N., de Cuevas, M., Brawley, C., Sandler, L. and Matunis, E. (2009). JAK-STAT signal inhibition regulates competition in the Drosophila testis stem cell niche. Science 326, 153-156.
18. Jin, Z., Flynt, A. S. and Lai, E. C. (2013). Drosophila piwi mutants exhibit germline stem cell tumors that are sustained by elevated Dpp signaling. Curr. Biol. 23, 1442-1448.
19. Karsten, P., Hader, S. and Zeidler, M. P. (2002). Cloning and expression of Drosophila SOCS36E and its potential regulation by the JAK/STAT pathway. Mech. Dev. 117, 343-346.
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. Kirilly, D. and Xie, T. (2007). The Drosophila ovary: an active stem cell community. Cell Res. 17, 15-25.
22. Kirilly, D., Wang, S. and Xie, T. (2011). Self-maintained escort cells form a germline stem cell differentiation niche. Development 138, 5087-5097.
23. Leatherman, J. L. and Dinardo, S. (2008). Zfh-1 controls somatic stem cell self-renewal in the Drosophila testis and nonautonomously influences germline stem cell self-renewal. Cell Stem Cell 3, 44-54.
24. Leatherman, J. L. and Dinardo, S. (2010). Germline self-renewal requires cyst stem cells and stat regulates niche adhesion in Drosophila testes. Nat. Cell Biol. 12, 806-811.
25. Li, M. A., Alls, J. D., Avancini, R. M., Koo, K. and Godt, D. (2003). The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila. Nat. Cell Biol. 5, 994-1000.
26. Lim, J. G. Y. and Fuller, M. T. (2012). Somatic cell lineage is required for differentiation and not maintenance of germline stem cells in Drosophila testes. Proc. Natl. Acad. Sci. U.S.A. 109, 18477-18481.
27. Lopez-Onieva, L., Fernandez-Minan, A. and Gonzalez-Reyes, A. (2008). Jak/Stat signalling in niche support cells regulates dpp transcription to control germline stem cell maintenance in the Drosophila ovary. Development 135, 533-540.
28. Maimon, I. and Gilboa, L. (2011). Dissection and staining of Drosophila larval ovaries. J. Vis. Exp. e2537.
29. Morris, L. X. and Spradling, A. C. (2011). Long-term live imaging provides new insight into stem cell regulation and germline-soma coordination in the Drosophila ovary. Development 138, 2207-2215.
30. Newsome, T. P., Asling, B. and Dickson, B. J. (2000). Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127, 851-860.
31. Ohlstein, B. and McKearin, D. (1997). Ectopic expression of the Drosophila Bam protein eliminates oogenic germline stem cells. Development 124, 3651-3662.
32. Postigo, A. A. and Dean, D. C. (1999). ZEB represses transcription through interaction with the corepressor CtBP. Proc. Natl. Acad. Sci. U.S.A. 96, 6683-6688.
33. Raffa, G. D., Cenci, G., Siriaco, G., Goldberg, M. L. and Gatti, M. (2005). The putative Drosophila transcription factor woc is required to prevent telomeric fusions. Mol. Cell 20, 821-831.
34. Rangan, P., Malone, C. D., Navarro, C., Newbold, S. P., Hayes, P. S., Sachidanandam, R., Hannon, G. J. and Lehmann, R. (2011). piRNA production requires heterochromatin formation in Drosophila. Curr. Biol. 21, 1373-1379.
35. Rojas-Rios, P., Guerrero, I. and Gonzalez-Reyes, A. (2012). Cytoneme-mediated delivery of hedgehog regulates the expression of bone morphogenetic proteins to maintain germline stem cells in Drosophila. PLoS Biol. 10, e1001298.
36. Saito, K., Inagaki, S., Mituyama, T., Kawamura, Y., Ono, Y., Sakota, E., Kotani, H., Asai, K., Siomi, H. and Siomi, M. C. (2009). A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 461, 1296-1299.
37. Schulz, C., Wood, C. G., Jones, D. L., Tazuke, S. I. and Fuller, M. T. (2002). Signaling from germ cells mediated by the rhomboid homolog stet organizes encapsulation by somatic support cells. Development 129, 4523-4534.
38. Shields, A. R., Spence, A. C., Yamashita, Y. M., Davies, E. L. and Fuller, M. T. (2014). The actin-binding protein profilin is required for germline stem cell maintenance and germ cell enclosure by somatic cyst cells. Development 141, 73-82.
39. Singh, S. R., Zheng, Z., Wang, H., Oh, S. W., Chen, X. and Hou, S. X. (2010). Competitiveness for the niche and mutual dependence of the germline and somatic stem cells in the Drosophila testis are regulated by the JAK/STAT signaling. J. Cell Physiol. 223, 500-510.
40. Smedley, D., Hamoudi, R., Lu, Y.-J., Cooper, C. and Shipley, J. (1999). Cloning and mapping of members of the MYM family. Genomics 60, 244-247.
41. Spradling, A., Fuller, M. T., Braun, R. E. and Yoshida, S. (2011). Germline stem cells. Cold Spring Harb. Perspect. Biol. 3, a002642.
42. Tulina, N. and Matunis, E. (2001). Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294, 2546-2549.
43. Wang, L., Li, Z. and Cai, Y. (2008). The JAK/STAT pathway positively regulates DPP signaling in the Drosophila germline stem cell niche. J. Cell Biol. 180, 721-728.
44. Warren, J. T., Wismar, J., Subrahmanyam, B. and Gilbert, L. I. (2001). Woc (without children) gene control of ecdysone biosynthesis in Drosophila melanogaster. Mol. Cell. Endocrinol. 181, 1-14.
45. Wismar, J., Habtemichael, N., Warren, J. T., Dai, J.-D., Gilbert, L.I. and Gateff, E. (2000). The mutation without children(rgl) causes ecdysteroid deficiency in third-instar larvae of Drosophila melanogaster. Dev. Biol. 226, 1-17.
46. Xie, T. and Spradling, A. C. (1998). decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell 94, 251-260.
47. Xie, T. and Spradling, A. C. (2000). A niche maintaining germline stem cells in the Drosophila ovary. Science 290, 328-330.
48. Zweier, C., Albrecht, B., Mitulla, B., Behrens, R., Beese, M., Gillessen-Kaesbach, G., Rott, H. D. and Rauch, A. (2002). "Mowat-Wilson" syndrome with and without Hirschsprung disease is a distinct, recognizable multiple congenital anomalies-mental retardation syndrome caused by mutations in the zinc finger homeo box 1B gene. Am. J. Med. Genet. 108, 177-181.