Effete-mediated degradation of Cyclin A is essential for the maintenance of germline stem cells in Drosophila

Development

Volumn 136, Issue 24, 2009, Pages 4133-4142

  Chen, Dongsheng ^a   Wang, Qi ^a   Huang, Haidong ^a   Xia, Laixin ^a   Jiang, Xiaoyong ^a   Kan, Lijuan ^a   Sun, Qinmiao ^a   Chen, Dahua ^a  

^a INSTITUTE OF ZOOLOGY   (China)

Author keywords

APC C complexes; Cyclin A; Stem cell fate determination; Ubiquitin conjugating enzymes

Indexed keywords

APC PROTEIN; APC2 PROTEIN; CYCLIN A; PROTEIN EFFETE; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANAPHASE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DROSOPHILA; GENE SILENCING; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STEM CELL; UBIQUITINATION;

ANIMALS; CELLS, CULTURED; CYCLIN A; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; HYDROLYSIS; MITOSIS; MUTATION; OVARY; PROTEIN BINDING; STEM CELLS; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITINATION;

MAMMALIA;

EID: 71449116210     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.039032     Document Type: Article

References (48)

1. Aristarkhov, A., Eytan, E., Moghe, A., Admon, A., Hershko, A. and Ruderman, J. V. (1996). E2-C, a cyclin-selective ubiquitin carrier protein required for the destruction of mitotic cyclins. Proc. Natl. Acad. Sci. USA 93, 4294-4299.
2. 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.
3. Castrillon, D. H., Gonczy, P., Alexander, S., Rawson, R., Eberhart, C. G., Viswanathan, S., DiNardo, S. and Wasserman, S. A. (1993). Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics 135, 489-505.
4. Cenci, G., Rawson, R. B., Belloni, G., Castrillon, D. H., Tudor, M., Petrucci, R., Goldberg, M. L., Wasserman, S. A. and Gatti, M. (1997). UbcD1, a Drosophila ubiquitin-conjugating enzyme required for proper telomere behavior. Genes Dev. 11, 863-875.
5. 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.
6. 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.
7. Chen, D. and McKearin, D. (2005). Gene circuitry controlling a stem cell niche. Curr. Biol. 15, 179-184.
8. Cox, D. N., 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.
9. Dawson, I. A., Roth, S. and Artavanis-Tsakonas, S. (1995). The Drosophila cell cycle gene fizzy is required for normal degradation of cyclins A and B during mitosis and has homology to the CDC20 gene of Saccharomyces cerevisiae. J. Cell Biol. 129, 725-737.
10. Forbes, A. and Lehmann, R. (1998). Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 125, 679-690.
11. Glickman, M. H. and Ciechanover, A. (2002). The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82, 373-428.
12. Glotzer, M., Murray, A. W. and Kirschner, M. W. (1991). Cyclin is degraded by the ubiquitin pathway. Nature 349, 132-138.
13. Harper, J. W., Burton, J. L. and Solomon, M. J. (2002). The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev. 16, 2179-2206.
14. Hsu, H. J., LaFever, L. and Drummond-Barbosa, D. (2008). Diet controls normal and tumorous germline stem cells via insulin-dependent and-independent mechanisms in Drosophila Dev. Biol. 313,700-712.
15. Jiang, X., Xia, L., Chen, D., Yang, Y., Huang, H., Yang, L., Zhao, Q., Shen, L., Wang, J. and Chen, D. (2008). Otefin, a nuclear membrane protein, determines the fate of germline stem cells in Drosophila via interaction with Smad complexes. Dev. Cell 14, 494-506.
16. Jin, Z. and Xie, T. (2007). Dcr-1 maintains Drosophila ovarian stem cells. Curr. Biol. 17, 539-544.
17. Kashevsky, H., Wallace, J. A., Reed, B. H., Lai, C., Hayashi-Hagihara, A. and Orr-Weaver, T. L. (2002). The anaphase promoting complex/cyclosome is required during development for modified cell cycles. Proc. Natl. Acad. Sci. USA 99, 11217-11222.
18. King, R. W., Peters, J. M., Tugendreich, S., Rolfe, M., Hieter, P. and Kirschner, M. W. (1995). A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 81, 279-288.
19. Kuo, C. T., Zhu, S., Younger, S., Jan, L. Y. and Jan, Y. N. (2006). Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51, 283-290.
20. Lasko, P. F. and Ashburner, M. (1990). Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev. 4, 905-921.
21. Lilly, M. A., de Cuevas, M. and Spradling, A. C. (2000). Cyclin A associates with the fusome during germline cyst formation in the Drosophila ovary. Dev. Biol. 218, 53-63.
22. Lin, H. and Spradling, A. C. (1997). A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124, 2463-2476.
23. Maines, J. Z., Park, J. K., Williams, M. and McKearin, D. M. (2007). Stonewalling Drosophila stem cell differentiation by epigenetic controls. Development 134, 1471-1479.
24. Mathe, E., Kraft, C., Giet, R., Deak, P., Peters, J. M. and Glover, D. M. (2004). The E2-C vihar is required for the correct spatiotemporal proteolysis of cyclin B and itself undergoes cyclical degradation. Curr. Biol. 14, 1723-1733.
25. Murray, A. W. (2004). Recycling the cell cycle: cyclins revisited. Cell 116, 221-234.
26. 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.
27. Parry, D. H. and O'Farrell, P. H. (2001). The schedule of destruction of three mitotic cyclins can dictate the timing of events during exit from mitosis. Curr. Biol. 11, 671-683.
28. Peters, J. M. (2002). The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 9, 931-943.
29. Rorth, P. (1998). Gal4 in the Drosophila female germline. Mech. Dev. 78, 113-118.
30. Ryoo, H. D., Bergmann, A., Gonen, H., Ciechanover, A. and Steller, H. (2002). Regulation of Drosophila IAP1 degradation and apoptosis by reaper and ubcD1. Nat. Cell Biol. 4, 432-438.
31. Seino, H., Kishi, T., Nishitani, H. and Yamao, F. (2003). Two ubiquitin-conjugating enzymes, UbcP1/Ubc4 and UbcP4/Ubc11, have distinct functions for ubiquitination of mitotic cyclin. Mol. Cell. Biol. 23, 3497-3505.
32. Sigrist, S., Jacobs, H., Stratmann, R. and Lehner, C. F. (1995). Exit from mitosis is regulated by Drosophila fizzy and the sequential destruction of cyclins A, B and B3. EMBO J. 14, 4827-4838.
33. Slack, C., Overton, P., Tuxworth, R. and Chia, W. (2007). Asymmetric localisation of Miranda and its cargo proteins during neuroblast division requires the anaphase-promoting complex/cyclosome. Development 134, 3781-3787.
34. 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.
35. Spradling, A., Drummond-Barbosa, D. and Kai, T. (2001). Stem cells find their niche. Nature 414, 98-104.
36. 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.
37. Tang, A. H., Neufeld, T. P., Kwan, E. and Rubin, G. M. (1997). PHYL acts to downregulate TTK88, a transcriptional repressor of neuronal cell fates, by a SINA-dependent mechanism. Cell 90, 459-467.
38. Tang, Z., Li, B., Bharadwaj, R., Zhu, H., Ozkan, E., Hakala, K., Deisenhofer, J. and Yu, H. (2001). APC2 Cullin protein and APC11 RING protein comprise the minimal ubiquitin ligase module of the anaphase-promoting complex. Mol. Biol. Cell 12, 3839-3851.
39. 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.
40. Wang, Z. and Lin, H. (2005). The division of Drosophila germline stem cells and their precursors requires a specific cyclin. Curr. Biol. 15, 328-333.
41. Wolthuis, R., Clay-Farrace, L., van Zon, W., Yekezare, M., Koop, L., Ogink, J., Medema, R. and Pines, J. (2008). Cdc20 and Cks direct the spindle checkpoint-independent destruction of cyclin A. Mol. Cell 30, 290-302.
42. 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.
43. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
44. 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.
45. Yu, H., King, R. W., Peters, J. M. and Kirschner, M. W. (1996). Identification of a novel ubiquitin-conjugating enzyme involved in mitotic cyclin degradation. Curr. Biol. 6, 455-466.
46. Zaccai, M. and Lipshitz, H. D. (1996). Differential distributions of two adducin-like protein isoforms in the Drosophila ovary and early embryo. Zygote 4, 159-166.
47. Zachariae, W. and Nasmyth, K. (1999). Whose end is destruction: cell division and the anaphase-promoting complex. Genes Dev. 13, 2039-2058.
48. Zhang, Q., Zhang, L., Wang, B., Ou, C. Y., Chien, C. T. and Jiang, J. (2006). A hedgehog-induced BTB protein modulates hedgehog signaling by degrading Ci/Gli transcription factor. Dev. Cell 10, 719-729.