Jak/Stat signalling in niche support cells regulates dpp transcription to control germline stem cell maintenance in the Drosophila ovary

Development

Volumn 135, Issue 3, 2008, Pages 533-540

  López Onieva, Lourdes ^a   Fernández Miñan, Ana ^a,b   González Reyes, Acaimo ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

BMP; Drosophila oogenesis; Germline stem cells; Jak Stat; Niche signalling

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; DECAPENTAPLEGIC PROTEIN; JANUS KINASE; MESSENGER RNA; STAT PROTEIN; DPP PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; HOP PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CANCER STEM CELL; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL DIVISION; CELL LOSS; CELL MATURATION; CELL POPULATION; CELL SURVIVAL; CONTROLLED STUDY; DROSOPHILA; GERM CELL; NONHUMAN; ORTHOLOGY; OVARY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SOMATIC CELL; STEM CELL; STROMA CELL; TRANSCRIPTION REGULATION; ANIMAL; CYTOLOGY; DROSOPHILA MELANOGASTER; ENZYMOLOGY; FEMALE; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; OOCYTE;

ANIMALS; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; JANUS KINASES; OVARY; OVUM; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS; STEM CELLS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 39149098701     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.016121     Document Type: Article

References (50)

1. Agaisse, H., Petersen, U., 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. Bach, E. A., Vincent, S., Zeidler, M. P. and Perrimon, N. (2003). A sensitized genetic screen to identify novel regulators and components of the Drosophila janus kinase/signal transducer and activator of transcription pathway. Genetics 165, 1149-1166.
3. Bach, E. A., Ekas, L. A., Ayala-Camargo, A., Flaherty, M. S., Lee, H., Perrimon, N. and Baeg, G. H. (2007). GFP reporters detect the activation of the Drosophila JAK/STAT pathway in vivo. Gene Expr. Patterns 7, 323-331.
4. Binari, R. and Perrimon, N. (1994). Stripe-specific regulation of pair-rule genes by hopscotch, a putative Jak family tyrosine kinase in Drosophila. Genes Dev. 8, 300-312.
5. Bolívar, J., Pearson, J., López-Onieva, L. and González-Reyes, A. (2006). Genetic dissection of a stem cell niche: the case of the Drosophila ovary. Dev. Dyn. 235, 2969-2979.
6. Brawley, C. and Matunis, E. (2004). Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 304, 1331-1334.
7. Brown, S., Hu, N. and Castelli-Gair Hombria, J. (2001). Identification of the first invertebrate interleukin JAK/STAT receptor, the Drosophila gene domeless. Curr. Biol. 11, 1700-1705.
8. Casanueva, M. and Ferguson, E. (2004). Germline stem cell number in the Drosophila ovary is regulated by redundant mechanisms that control Dpp signalling. Development 131, 1881-1890.
9. 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.
10. Chen, D. and McKearin, D. (2005). Gene circuitry controlling a stem cell niche. Curr. Biol. 15, 179-184.
11. Chen, H., Chen, X., Oh, S., Marinissen, M., Gutkind, J. and Hou, S. (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.
12. Cox, D., Chao, A., Baker, J., Chang, L., Qiao, D. and Lin, H. (1998). A novel class of evolutionary conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 12, 3715-3727.
13. Cox, D., Chao, A. and Lin, H. (2000). piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 127, 503-514.
14. 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.
15. de Cuevas, M. and Spradling, A. (1998). Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125, 2781-2799.
16. de Rooij, D. G. and Russell, L. D. (2000). All you wanted to know about spermatogonia but were afraid to ask. J. Androl. 21, 776-798.
17. Forbes, A., Spradling, A., Ingham, P. and Lin, H. (1996). The role of segment polarity genes during early oogenesis in Drosophila. Development 122, 3284-3294.
18. Fuchs, E., Tumbar, T. and Guasch, G. (2004). Socializing with the neighbors: stem cells and their niche. Cell 116, 769-778.
19. 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.
20. Gilboa, L. and Lehmann, R. (2004). How different is Venus from Mars? The genetics of germ-line stem cells in Drosophila females and males. Development 131, 4895-4905.
21. González-Reyes, A. (2003). Stem cells, niches and cadherins: a view from Drosophila. J. Cell Sci. 116, 949-954.
22. Harrison, D. A., Binari, R., Nahreini, T. S., Gilman, M. and Perrimon, N. (11995). Activation of a Drosophila Janus kinase (JAK) causes hernatopoietic neoplasia and developmental defects. EMBO J. 14, 2857-2865.
23. Harrison, D., McCoon, P., Binari, R., Bilman, M. and Perrimon, N. (1998). Drosophila unpaired encodes a secreted protein that activates the JAK signaling pathway. Genes Dev. 12, 3252-3263.
24. Hombria, J. C.-G., Brown, S., Hader, S. and Zeidler, M. P. (2005). Characterisation of Upd2, a Drosophila JAKISTAT pathway ligand. Dev. Biol. 288, 420-433.
25. Hou, X. S., Melnick, M. B. and Perrimon, N. (1996). Marelle acts downstream of the Drosophila HOP/JAK kinase and encodes a protein similar to the mammalian STATs. Cell 84, 411-419.
26. Kai, T. and Spradling, A. (2003). An empty Drosophila stem cell niche reactivates the proliferation of ectopic cells. Proc. Natl. Acad. Sci. USA 100, 4633-4638.
27. Kai, T. and Spradling, A. (2004). Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 428, 564-569.
28. Kiger, A., Jones, D., Schulz, C., Rogers, M. and Fuller, M. (2001). Stem cell self-renewal specified by JAK-STAT activation in response to a support clue. Science 294, 2542-2545.
29. King, F. and Lin, H. (1999). Somatic signaling mediated by fs(1)Yb is essential for germline stem cell maintenance during Drosophil'a oogenesis. Development 126, 1833-1844.
30. King, F., Szakmary, A., Cox, D. and Lin, H. (2001). Yb modulates the divisions of both germline and somatic stem cells through piwi- and hh-mediated mechanisms in the Drosophila ovary. Mol. Cell 7, 497-508.
31. LaFever, L. and Drummond-Barbosa, D. (2005). Direct control of germline stem cell division and cyst growth by neural insulin in Drosophila. Science 309, 1071-1073.
32. Luo, H., Hanratty, W. P. and Dearolf, C. R. (1995). An amino acid substitution in the Drosophila hopTum-I Jak kinase causes leukemia-like hematopoietic defects. EMBO J. 14, 1412-1420.
33. Perrimon, N. and Mahowald, A. P. (1986). I(1)hopscotch, A larval-pupal zygotic lethal with a specific maternal effect on segmentation in Drosophila. Dev. Biol. 118, 28-41.
34. Scadden, D. T. (2006). The stem-cell niche as an entity of action. Nature 441, 1075-1079.
35. Shi, S., Calhoun, H. C., Xia, F., Li, J., Le, L. and Li, W. X. (2006). JAK signaling globally counteracts heterochromatic gene silencing. Nat. Genet. 38, 1071-1076.
36. Singh, S. R., Zhen, W., Zheng, Z., Wang, H., Oh, S. W., Liu, W., Zbar, B., Schmidt, L. S. and Hou, S. X. (2006). The Drosophila homolog of the human tumor suppressor gene BHD interacts with the JAK-STAT and Dpp signaling pathways in regulating male germline stem cell maintenance. Oncogene 25, 5933-5941.
37. Song, X. and Xie, T. (2003). Wingless signaling regulates the maintenance of ovarian somatic stem cells in Drosophila. Development 130, 3259-3268.
38. Song, X., Wong, M. D., Kawase, E., A, 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.
39. Song, X., Call, G. B., Kirilly, D. and Xie, T. (2007). Notch signaling controls germline stem cell niche formation in the Drosophila ovary. Development 134, 1071-1080.
40. Spradling, A., de Cuevas, M., Drummond-Barbosa, D., Keyes, L., Lilly, M., Pepling, M. and Xie, T. (1997). The Drosophila germarium: stem cells, germ line cysts, and oocytes. Cold Spring Harb. Symp. Quant. Biol. 62, 25-34.
41. Spradling, A., Drummond-Barbosa, D. and Kai, T. (2001). Stem cells find their niche. Nature 414, 98-104.
42. Szakmary, A., Cox, D. N., Wang, Z. and Lin, H. (2005). Regulatory relationship among piwi, pumilio, and bag-of-marbles in Drosophila germline stem cell self-renewal and differentiation. Curr. Biol. 15, 171-178.
43. Tanimoto, H., Itoh, S., ten Dijke, P. and Tabata, T. (2000). Hedgehog creates a gradient of Dpp activity in Drosophila wing imaginal discs. Mol. Cell 5, 59-71.
44. Tulina, N. and Matunis, E. (2001). Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294, 2546-2549.
45. Wieschaus, E., Nüsslein-Volhard, C. and Jürgens, G. (1984), Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster III. Zygotic loci on the X-chromosome and the fourth chromosome. Roux's Arch. Dev. Biol. 193, 296-307.
46. Wong, M. D., Jin, Z. and Xie, T. (2005). Molecular mechanisms of germline stem cell regulation. Annu. Rev. Genet. 39, 173-195.
47. Xi, R., Doan, C., Liu, D. and Xie, T. (2005). Pelota controls self-renewal of germline stem cells by repressing a Bam-independent differentiation pathway. Development 132, 5365-5374.
48. Xie, T. and Spradling, A. (1998). decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell 94, 251-260.
49. Xie, T. and Spradling, A. (2000). A niche maintaining germ line stem cells in the Drosophila ovary. Science 290, 328-330.
50. Zhang, Y. and Kalderon, D. (2001). Hedgehog acts as a somatic stem cell factor in the Drosophila ovary. Nature 410, 599-604.