Maintenance of Drosophila germline stem cell sexual identity in oogenesis and tumorigenesis

Development (Cambridge)

Volumn 142, Issue 6, 2015, Pages 1073-1082

  Shapiro Kulnane, Laura ^a   Smolko, Anne Elizabeth ^a   Salz, Helen Karen ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Germline tumors; Jak Stat; Oogenesis; Phf7; Sxl

Indexed keywords

JANUS KINASE; PROTEIN; STAT PROTEIN; SXL PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN; PHF7 PROTEIN, DROSOPHILA; RNA BINDING PROTEIN; SXL PROTEIN, DROSOPHILA;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL MUTANT; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVATION; FEMALE; GENDER IDENTITY; GENE EXPRESSION; GERM CELL; GERM CELL TUMOR; GERMLINE STEM CELL; MALE; NONHUMAN; OOCYTE DEVELOPMENT; OVARY TUMOR; PARACRINE SIGNALING; PHENOTYPE; PHF7 GENE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SRY GENE; TESTIS; TUMOR MICROENVIRONMENT; ADULT STEM CELL; ANIMAL; CYTOLOGY; DROSOPHILA MELANOGASTER; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HOMEOSTASIS; IMAGE PROCESSING; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SEXUAL DEVELOPMENT;

ADULT STEM CELLS; ANIMALS; CARCINOGENESIS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; GERM CELLS; HOMEODOMAIN PROTEINS; HOMEOSTASIS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MICROSCOPY, FLUORESCENCE; OOGENESIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA-BINDING PROTEINS; SEQUENCE ANALYSIS, RNA; SEX CHARACTERISTICS; TESTIS;

EID: 84930532282     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.116590     Document Type: Article

References (70)

1. Agaisse, H., Petersen, U.-M., Boutros, M., Mathey-Prevot, B. and Perrimon, N. (2003). Signaling role of hemocytes in Drosophila JAK/STAT-dependent response to septic injury. Dev. Cell 5, 441-450.
2. Amoyel, M., Anderson, A. M. and Bach, E. A. (2014). JAK/STAT pathway dysregulation in tumors: a Drosophila perspective. Semin. Cell Dev. Biol. 28, 96-103.
3. Aoyagi, N. and Wassarman, D. A. (2000). Genes encoding Drosophila melanogaster RNA polymerase II general transcription factors: diversity in TFIIA and TFIID components contributes to gene-specific transcriptional regulation. J. Cell Biol. 150, F45-F50.
4. Bellott, D. W., Hughes, J. F., Skaletsky, H., Brown, L. G., Pyntikova, T., Cho, T.-J., Koutseva, N., Zaghlul, S., Graves, T., Rock, S. et al. (2014). Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature 508, 494-499.
5. Bergner, L. M., Hickman, F. E., Wood, K. H., Wakeman, C. M., Stone, H. H., Campbell, T. J., Lightcap, S. B., Favors, S. M., Aldridge, A. C. and Hales, K. G. (2010). A novel predicted bromodomain-related protein affects coordination between meiosis and spermiogenesis in Drosophila and is required for male meiotic cytokinesis. DNA Cell Biol. 29, 487-498.
6. Brown, J. B., Boley, N., Eisman, R., May, G. E., Stoiber, M. H., Duff, M. O., Booth, B. W., Wen, J., Park, S., Suzuki, A. M. et al. (2014). Diversity and dynamics of the Drosophila transcriptome. Nature 512, 393-399.
7. Cabrera, G. R., Godt, D., Fang, P.-Y., Couderc, J.-L. and Laski, F. A. (2002). Expression pattern of Gal4 enhancer trap insertions into the bric à brac locus generated by P element replacement. Genesis 34, 62-65.
8. Casper, A. L. and van Doren, M. (2009). The establishment of sexual identity in the Drosophila germline. Development 136, 3821-3830.
9. Chau, J., Kulnane, L. S. and Salz, H. K. (2009). Sex-lethal facilitates the transition from germline stem cell to committed daughter cell in the Drosophila ovary. Genetics 182, 121-132.
10. Chau, J., Kulnane, L. S. and Salz, H. K. (2012). Sex-lethal enables germline stem cell differentiation by down-regulating Nanos protein levels during Drosophila oogenesis. Proc. Natl. Acad. Sci. USA 109, 9465-9470.
11. 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.
12. 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.
13. Chen, D. and McKearin, D. (2005). Gene circuitry controlling a stem cell niche. Curr. Biol. 15, 179-184.
14. Chen, H.-W., Chen, X., Oh, S.-W., Marinissen, M. J., Gutkind, J. S. and Hou, S. X. (2002). mom identifies a receptor for the Drosophila JAK/STAT signal transduction pathway and encodes a protein distantly related to the mammalian cytokine receptor family. Genes Dev. 16, 388-398.
15. Chen, X., Oh, S.-W., Zheng, Z., Chen, H.-W., Shin, H.-H. and Hou, S. X. (2003). Cyclin D-Cdk4 and cyclin E-Cdk2 regulate the Jak/STAT signal transduction pathway in Drosophila. Dev. Cell 4, 179-190.
16. 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.
17. 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.
18. Forbes, A. A. and Lehmann, R. R. (1998). Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 125, 679-690.
19. Friedmann-Morvinski, D. and Verma, I. M. (2014). Dedifferentiation and reprogramming: origins of cancer stem cells. EMBO Rep. 15, 244-253.
20. 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.
21. Gilbert, M. M., Weaver, B. K., Gergen, J. P. and Reich, N. C. (2005). A novel functional activator of the Drosophila JAK/STAT pathway, unpaired2, is revealed by an in vivo reporter of pathway activation. Mech. Dev. 122, 939-948.
22. Gilboa, L. and Lehmann, R. (2004). Repression of primordial germ cell differentiation parallels germ line stem cell maintenance. Curr. Biol. 14, 981-986.
23. Harris, R. E., Pargett, M., Sutcliffe, C., Umulis, D. and Ashe, H. L. (2011). Brat promotes stem cell differentiation via control of a bistable switch that restricts BMP signaling. Dev. Cell 20, 72-83.
24. Hernańdez, G., Han, H., Gandin, V., Fabian, L., Ferreira, T., Zuberek, J., Sonenberg, N., Brill, J. A. and Lasko, P. (2012). Eukaryotic initiation factor 4E-3 is essential for meiotic chromosome segregation, cytokinesis and male fertility in Drosophila. Development 139, 3211-3220.
25. Hersmus, R., Stoop, H., White, S. J., Drop, S. L. S., Oosterhuis, J. W., Incrocci, L., Wolffenbuttel, K. P. and Looijenga, L. H. J. (2012). Delayed recognition of disorders of sex development (DSD): a missed opportunity for early diagnosis of malignant germ cell tumors. Int. J. Endocrinol. 2012, 671209.
26. Hombrıá, J. C.-G., Brown, S., Häder, S. and Zeidler, M. P. (2005). Characterisation of Upd2, a Drosophila JAK/STAT pathway ligand. Dev. Biol. 288, 420-433.
27. Horabin, J. I., Bopp, D., Waterbury, J. and Schedl, P. (1995). Selection and maintenance of sexual identity in the Drosophila germline. Genetics 141, 1521-1535.
28. Hudson, A. M. and Cooley, L. (2014). Methods for studying oogenesis. Methods 68, 207-217.
29. Kai, T., Williams, D. and Spradling, A. C. (2005). The expression profile of purified Drosophila germline stem cells. Dev. Biol. 283, 486-502.
30. Kanetsky, P. A., Mitra, N., Vardhanabhuti, S., Vaughn, D. J., Li, M., Ciosek, S. L., Letrero, R., D’Andrea, K., Vaddi, M., Doody, D. R. et al. (2011). A second independent locus within DMRT1 is associated with testicular germ cell tumor susceptibility. Hum. Mol. Genet. 20, 3109-3117.
31. 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.
32. Koster, R., Mitra, N., D’Andrea, K., Vardhanabhuti, S., Chung, C. C., Wang, Z., Erickson, R. L., Vaughn, D. J., Litchfield, K., Rahman, N. et al. (2014). Pathway-based analysis of GWAs data identifies association of sex determination genes with susceptibility to testicular germ cell tumors. Hum. Mol. Genet. 23, 6061-6068.
33. Kraggerud, S. M., Hoei-Hansen, C. E., Alagaratnam, S., Skotheim, R. I., Abeler, V. M., Rajpert-De Meyts, E. and Lothe, R. A. (2013). Molecular characteristics of malignant ovarian germ cell tumors and comparison with testicular counterparts: implications for pathogenesis. Endocr. Rev. 34, 339-376.
34. Leatherman, J. L. and DiNardo, S. (2008). Zfh-1 controls somatic stem cell selfrenewal in the Drosophila testis and nonautonomously influences germline stem cell self-renewal. Cell Stem Cell 3, 44-54.
35. 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.
36. Leser, K., Awe, S., Barckmann, B., Renkawitz-Pohl, R. and Rathke, C. (2012). The bromodomain-containing protein tBRD-1 is specifically expressed in spermatocytes and is essential for male fertility. Biol. Open 1, 597-606.
37. 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.
38. Li, Y., Zhang, Q., Carreira-Rosario, A., Maines, J. Z., McKearin, D. M. and Buszczak, M. (2013). Mei-p26 cooperates with bam, bgcn and sxl to promote early germline development in the Drosophila ovary. PLoS ONE 8, e58301.
39. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
40. Loṕez-Onieva, L., Fernańdez-Miñań, A. and Gonzaĺez-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.
41. Matson, C. K., Murphy, M. W., Sarver, A. L., Griswold, M. D., Bardwell, V. J. and Zarkower, D. (2011). DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 476, 101-104.
42. McGuire, S. E., Le, P. T., Osborn, A. J., Matsumoto, K. and Davis, R. L. (2003). Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302, 1765-1768.
43. 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.
44. 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.
45. Nagengast, A. A., Stitzinger, S. M., Tseng, C.-H., Mount, S. M. and Salz, H. K. (2003). Sex-lethal splicing autoregulation in vivo: interactions between SEXLETHAL, the U1 snRNP and U2AF underlie male exon skipping. Development 130, 463-471.
46. Nakada, D., Oguro, H., Levi, B. P., Ryan, N., Kitano, A., Saitoh, Y., Takeichi, M., Wendt, G. R. and Morrison, S. J. (2014). Oestrogen increases haematopoietic stem-cell self-renewal in females and during pregnancy. Nature 505, 555-558.
47. Ni, J.-Q., Zhou, R., Czech, B., Liu, L.-P., Holderbaum, L., Yang-Zhou, D., Shim, H.-S., Tao, R., Handler, D., Karpowicz, P. et al. (2011). A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat. Methods 8, 405-407.
48. Pleskacova, J., Hersmus, R., Oosterhuis, J. W., Setyawati, B. A., Faradz, S. M., Cools, M., Wolffenbuttel, K. P., Lebl, J., Drop, S. L. and Looijenga, L. H. (2010). Tumor risk in disorders of sex development. Sex. Dev. 4, 259-269.
49. Ronen, D. and Benvenisty, N. (2014). Sex-dependent gene expression in human pluripotent stem cells. Cell Rep. 8, 923-932.
50. Salz, H. K. (2011). Sex determination in insects: a binary decision based on alternative splicing. Curr. Opin. Genet. Dev. 21, 395-400.
51. Salz, H. K. and Erickson, J. W. (2010). Sex determination in Drosophila: the view from the top. Fly (Austin) 4, 60-70.
52. Song, X. and Xie, T. (2003). Wingless signaling regulates the maintenance of ovarian somatic stem cells in Drosophila. Development 130, 3259-3268.
53. Song, X., Wong, M. D., Kawase, E., Xi, R., Ding, B. C., McCarthy, J. J. and Xie, T. (2004). 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 131, 1353-1364.
54. Spradling, A., Fuller, M. T., Braun, R. E. and Yoshida, S. (2011). Germline stem cells. Cold Spring Harb. Perspect. Biol. 3, a002642–a002642.
55. Staab, S., Heller, A. and Steinmann-Zwicky, M. (1996). Somatic sex-determining signals act on XX germ cells in Drosophila embryos. Development 122, 4065-4071.
56. Steinmann-Zwicky, M. (1994). Sex determination of the Drosophila germ line: tra and dsx control somatic inductive signals. Development 120, 707-716.
57. Tipping, M. and Perrimon, N. (2014). Drosophila as a model for context-dependent tumorigenesis. J. Cell. Physiol. 229, 27-33.
58. Trapnell, C., Pachter, L. and Salzberg, S. L. (2009). TopHat: discovering splice junctions with RNA-Seq. J. Gerontol. 25, 1105-1111.
59. Trapnell, C., Williams, B. A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M. J., Salzberg, S. L., Wold, B. J. and Pachter, L. (2010). Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515.
60. Tulina, N. and Matunis, E. (2001). Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294, 2546-2549.
61. Turnbull, C., Rapley, E. A., Seal, S., Pernet, D., Renwick, A., Hughes, D., Ricketts, M., Linger, R., Nsengimana, J., Deloukas, P. et al. (2010). Variants near DMRT1, TERT and ATF7IP are associated with testicular germ cell cancer. Nat. Genet. 42, 604-607.
62. 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.
63. Wang, Z. and Lin, H. (2004). Nanos maintains germline stem cell self-renewal by preventing differentiation. Science 303, 2016-2019.
64. 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.
65. Wawersik, M., Milutinovich, A., Casper, A. L., Matunis, E., Williams, B. and van Doren, M. (2005). Somatic control of germline sexual development is mediated by the JAK/STAT pathway. Nature 436, 563-567.
66. Wei, G., Oliver, B., Pauli, D. and Mahowald, A. P. (1994). Evidence for sex transformation of germline cells in ovarian tumor mutants of drosophila. Dev. Biol. 161, 318-320.
67. White-Cooper, H. (2010). Molecular mechanisms of gene regulation during Drosophila spermatogenesis. Reproduction 139, 11-21.
68. Yan, D., Neumüller, R. A., Buckner, M., Ayers, K., Li, H., Hu, Y., Yang-Zhou, D., Pan, L., Wang, X., Kelley, C. et al. (2014). A regulatory network of Drosophila germline stem cell self-renewal. Dev. Cell 28, 459-473.
69. Yang, S. Y., Baxter, E. M. and van Doren, M. (2012). Phf7 controls male sex determination in the Drosophila germline. Dev. Cell 22, 1041-1051.
70. Zeeberg, B. R., Qin, H., Narasimhan, S., Sunshine, M., Cao, H., Kane, D. W., Reimers, M., Stephens, R. M., Bryant, D., Burt, S. K. et al. (2005). High-throughput GoMiner, an “industrial-strength” integrative gene ontology tool for interpretation of multiple-microarray experiments, with application to studies of common variable immune deficiency (CVID). BMC Bioinformatics 6, 168.