Cyclin E controls Drosophila female germline stem cell maintenance independently of its role in proliferation by modulating responsiveness to niche signals

Development (Cambridge)

Volumn 140, Issue 3, 2013, Pages 530-540

  Ables, Elizabeth T ^a   Drummond Barbosa, Daniela ^a,b  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b Johns Hopkins University   (United States)

Author keywords

BMP signaling; Cdk2; Cell cycle; Cyclin E; Drosophila; Germline stem cell

Indexed keywords

CYCLIN DEPENDENT KINASE 2; CYCLIN E;

ANIMAL CELL; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CELL PROLIFERATION; CONFERENCE PAPER; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENE MUTATION; GERMLINE STEM CELL; INTRACELLULAR SIGNALING; MOSAICISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEM CELL; STEM CELL NICHE;

ALLELES; ANIMALS; APOPTOSIS; CELL DIVISION; CELL PROLIFERATION; CYCLIN B; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; G2 PHASE; GERM CELLS; GREEN FLUORESCENT PROTEINS; INTERCELLULAR JUNCTIONS; MUTATION; PHENOTYPE; SIGNAL TRANSDUCTION; STEM CELL NICHE; STEM CELLS;

EID: 84872068577     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.088583     Document Type: Conference Paper

References (74)

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. Ables, E. T., Laws, K. M. and Drummond-Barbosa, D. (2012). Control of adult stem cells in vivo by a dynamic physiological environment: diet-dependent systemic factors in Drosophila and beyond. WIREs Dev Biol 1, 657-674.
3. Ashburner, M. and Drysdale, R. (1994). FlyBase - the Drosophila genetic database. Development 120, 2077-2079.
4. Ballabeni, A., Park, I. H., Zhao, R., Wang, W., Lerou, P. H., Daley, G. Q. and Kirschner, M. W. (2011). Cell cycle adaptations of embryonic stem cells. Proc. Natl. Acad. Sci. USA 108, 19252-19257.
5. Berger, C., Pallavi, S. K., Prasad, M., Shashidhara, L. S. and Technau, G. M. (2005). A critical role for cyclin E in cell fate determination in the central nervous system of Drosophila melanogaster. Nat. Cell Biol. 7, 56-62.
6. Berger, C., Kannan, R., Myneni, S., Renner, S., Shashidhara, L. S. and Technau, G. M. (2010). Cell cycle independent role of Cyclin E during neural cell fate specification in Drosophila is mediated by its regulation of Prospero function. Dev. Biol. 337, 415-424.
7. Brodigan, T. M., Liu, J., Park, M., Kipreos, E. T. and Krause, M. (2003). Cyclin E expression during development in Caenorhabditis elegans. Dev. Biol. 254, 102-115.
8. Brumby, A., Secombe, J., Horsfield, J., Coombe, M., Amin, N., Coates, D., Saint, R. and Richardson, H. (2004). A genetic screen for dominant modifiers of a cyclin E hypomorphic mutation identifies novel regulators of S-phase entry in Drosophila. Genetics 168, 227-251.
9. Calvi, B. R., Lilly, M. A. and Spradling, A. C. (1998). Cell cycle control of chorion gene amplification. Genes Dev. 12, 734-744.
10. Chen, D., Wang, Q., Huang, H., Xia, L., Jiang, X., Kan, L., Sun, Q. and Chen, D. (2009). Effete-mediated degradation of Cyclin A is essential for the maintenance of germline stem cells in Drosophila. Development 136, 4133-4142.
11. Chen, S., Wang, S. and Xie, T. (2011). Restricting self-renewal signals within the stem cell niche: multiple levels of control. Curr. Opin. Genet. Dev. 21, 684-689.
12. Choi, J. H., Banks, A. S., Estall, J. L., Kajimura, S., Boström, P., Laznik, D., Ruas, J. L., Chalmers, M. J., Kamenecka, T. M., Blüher, M. et al. (2010). Anti-diabetic drugs inhibit obesity-linked phosphorylation of PPARgamma by Cdk5. Nature 466, 451-456.
13. Davis, F. M., Tsao, T. Y., Fowler, S. K. and Rao, P. N. (1983). Monoclonal antibodies to mitotic cells. Proc. Natl. Acad. Sci. USA 80, 2926-2930.
14. de Cuevas, M. and Spradling, A. C. (1998). Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125, 2781-2789.
15. de Nooij, J. C., Letendre, M. A. and Hariharan, I. K. (1996). A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell 87, 1237-1247.
16. Doronkin, S., Djagaeva, I. and Beckendorf, S. K. (2003). The COP9 signalosome promotes degradation of Cyclin E during early Drosophila oogenesis. Dev. Cell 4, 699-710.
17. Duman-Scheel, M., Weng, L., Xin, S. and Du, W. (2002). Hedgehog regulates cell growth and proliferation by inducing Cyclin D and Cyclin E. Nature 417, 299-304.
18. Duronio, R. J. and O'Farrell, P. H. (1995). Developmental control of the G1 to S transition in Drosophila: cyclin Eis a limiting downstream target of E2F. Genes Dev. 9, 1456-1468.
19. Duronio, R. J., Bonnette, P. C. and O'Farrell, P. H. (1998). Mutations of the Drosophila dDP, dE2F, and cyclin E genes reveal distinct roles for the E2F-DP transcription factor and cyclin E during the G1-S transition. Mol. Cell. Biol. 18, 141-151.
20. Escudero, L. M. and Freeman, M. (2007). Mechanism of G1 arrest in the Drosophila eye imaginal disc. BMC Dev. Biol. 7, 13.
21. Firth, L. C. and Baker, N. E. (2005). Extracellular signals responsible for spatially regulated proliferation in the differentiating Drosophila eye. Dev. Cell 8, 541-551.
22. Fox, P. M., Vought, V. E., Hanazawa, M., Lee, M. H., Maine, E. M. and Schedl, T. (2011). Cyclin E and CDK-2 regulate proliferative cell fate and cell cycle progression in the C. elegans germline. Development 138, 2223-2234.
23. Gilboa, L., Forbes, A., Tazuke, S. I., Fuller, M. T. and Lehmann, R. (2003). Germ line stem cell differentiation in Drosophila requires gap junctions and proceeds via an intermediate state. Development 130, 6625-6634.
24. Hong, A., Lee-Kong, S., Iida, T., Sugimura, I. and Lilly, M. A. (2003). The p27cip/kip ortholog dacapo maintains the Drosophila oocyte in prophase of meiosis I. Development 130, 1235-1242.
25. Hsu, H. J. and Drummond-Barbosa, D. (2009). Insulin levels control female germline stem cell maintenance via the niche in Drosophila. Proc. Natl. Acad. Sci. USA 106, 1117-1121.
26. 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.
27. Inaba, M., Yuan, H. and Yamashita, Y. M. (2011). String (Cdc25) regulates stem cell maintenance, proliferation and aging in Drosophila testis. Development 138, 5079-5086.
28. Jacobs, H. W., Knoblich, J. A. and Lehner, C. F. (1998). Drosophila Cyclin B3 is required for female fertility and is dispensable for mitosis like Cyclin B. Genes Dev. 12, 3741-3751.
29. Jeong, J., Verheyden, J. M. and Kimble, J. (2011). Cyclin E and Cdk2 control GLD-1, the mitosis/meiosis decision, and germline stem cells in Caenorhabditis elegans. PLoS Genet. 7, e1001348.
30. 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.
31. LaFever, L., Feoktistov, A., Hsu, H. J. and Drummond-Barbosa, D. (2010). Specific roles of Target of rapamycin in the control of stem cells and their progeny in the Drosophila ovary. Development 137, 2117-2126.
32. Lange, C. and Calegari, F. (2010). Cdks and cyclins link G1 length and differentiation of embryonic, neural and hematopoietic stem cells. Cell Cycle 9, 1893-1900.
33. Lantz, V., Chang, J. S., Horabin, J. I., Bopp, D. and Schedl, P. (1994). The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev. 8, 598-613.
34. Li, V. C., Ballabeni, A. and Kirschner, M. W. (2012). Gap 1 phase length and mouse embryonic stem cell self-renewal. Proc. Natl. Acad. Sci. USA 109, 12550-12555.
35. Lilly, M. A. and Spradling, A. C. (1996). The Drosophila endocycle is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion. Genes Dev. 10, 2514-2526.
36. 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.
37. Loeb, K. R., Kostner, H., Firpo, E., Norwood, T., Tsuchiya, K. D., Clurman, B. E. and Roberts, J. M. (2005). A mouse model for cyclin E-dependent genetic instability and tumorigenesis. Cancer Cell 8, 35-47.
38. Minella, A. C., Welcker, M. and Clurman, B. E. (2005). Ras activity regulates cyclin E degradation by the Fbw7 pathway. Proc. Natl. Acad. Sci. USA 102, 9649-9654.
39. Minella, A. C., Loeb, K. R., Knecht, A., Welcker, M., Varnum-Finney, B. J., Bernstein, I. D., Roberts, J. M. and Clurman, B. E. (2008). Cyclin E phosphorylation regulates cell proliferation in hematopoietic and epithelial lineages in vivo. Genes Dev. 22, 1677-1689.
40. Möröy, T. and Geisen, C. (2004). Cyclin E. Int. J. Biochem. Cell Biol. 36, 1424-1439.
41. Myster, D. L., Bonnette, P. C. and Duronio, R. J. (2000). A role for the DP subunit of the E2F transcription factor in axis determination during Drosophila oogenesis. Development 127, 3249-3261.
42. Narbonne-Reveau, K. and Lilly, M. (2009). The Cyclin-dependent kinase inhibitor Dacapo promotes genomic stability during premeiotic S phase. Mol. Biol. Cell 20, 1960-1969.
43. Neganova, I., Zhang, X., Atkinson, S. and Lako, M. (2009). Expression and functional analysis of G1 to S regulatory components reveals an important role for CDK2 in cell cycle regulation in human embryonic stem cells. Oncogene 28, 20-30.
44. Neumüller, R. A., Betschinger, J., Fischer, A., Bushati, N., Poernbacher, I., Mechtler, K., Cohen, S. M. and Knoblich, J. A. (2008). Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature 454, 241-245.
45. Nicholson, S. C., Nicolay, B. N., Frolov, M. V. and Moberg, K. H. (2011). Notch- dependent expression of the archipelago ubiquitin ligase subunit in the Drosophila eye. Development 138, 251-260.
46. Ninov, N., Manjón, C. and Martín-Blanco, E. (2009). Dynamic control of cell cycle and growth coupling by ecdysone, EGFR, and PI3K signaling in Drosophila histoblasts. PLoS Biol. 7, e1000079.
47. Odajima, J., Wills, Z. P., Ndassa, Y. M., Terunuma, M., Kretschmannova, K., Deeb, T. Z., Geng, Y., Gawrzak, S., Quadros, I. M., Newman, J. et al. (2011). Cyclin E constrains Cdk5 activity to regulate synaptic plasticity and memory formation. Dev. Cell 21, 655-668.
48. Ohlmeyer, J. T. and Schüpbach, T. (2003). Encore facilitates SCF-Ubiquitin- proteasome-dependent proteolysis during Drosophila oogenesis. Development 130, 6339-6349.
49. Ohtsubo, M. and Roberts, J. M. (1993). Cyclin-dependent regulation of G1 in mammalian fibroblasts. Science 259, 1908-1912.
50. Orford, K. W. and Scadden, D. T. (2008). Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat. Rev. Genet. 9, 115-128.
51. Park, E. A., Macalpine, D. M. and Orr-Weaver, T. L. (2007). Drosophila follicle cell amplicons as models for metazoan DNA replication: a cyclinE mutant exhibits increased replication fork elongation. Proc. Natl. Acad. Sci. USA 104, 16739-16746.
52. 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.
53. Resnitzky, D., Gossen, M., Bujard, H. and Reed, S. I. (1994). Acceleration of the G1/S phase transition by expression of cyclins D1 and E with an inducible system. Mol. Cell. Biol. 14, 1669-1679.
54. Richardson, H. E., O'Keefe, L. V., Reed, S. I. and Saint, R. (1993). A Drosophila G1-specific cyclin E homolog exhibits different modes of expression during embryogenesis. Development 119, 673-690.
55. Richardson, H., O'Keefe, L. V., Marty, T. and Saint, R. (1995). Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc. Development 121, 3371-3379.
56. Salomoni, P. and Calegari, F. (2010). Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol. 20, 233-243.
57. Sauer, K., Knoblich, J. A., Richardson, H. and Lehner, C. F. (1995). Distinct modes of cyclin E/cdc2c kinase regulation and S-phase control in mitotic and endoreduplication cycles of Drosophila embryogenesis. Genes Dev. 9, 1327-1339.
58. Singh, A. M. and Dalton, S. (2009). The cell cycle and Myc intersect with mechanisms that regulate pluripotency and reprogramming. Cell Stem Cell 5, 141-149.
59. Siu, K. T., Rosner, M. R. and Minella, A. C. (2012). An integrated view of cyclin E function and regulation. Cell Cycle 11, 57-64.
60. Song, X., Zhu, C. H., Doan, C. and Xie, T. (2002). Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science 296, 1855-1857.
61. Spruck, C. H., Won, K. A. and Reed, S. I. (1999). Deregulated cyclin E induces chromosome instability. Nature 401, 297-300.
62. Strohmaier, H., Spruck, C. H., Kaiser, P., Won, K. A., Sangfelt, O. and Reed, S. I. (2001). Human F-box protein hCdc4 targets cyclin E for proteolysis and is mutated in a breast cancer cell line. Nature 413, 316-322.
63. Sukhanova, M. J. and Du, W. (2008). Control of cell cycle entry and exiting from the second mitotic wave in the Drosophila developing eye. BMC Dev. Biol. 8, 7.
64. Thomer, M., May, N. R., Aggarwal, B. D., Kwok, G. and Calvi, B. R. (2004). Drosophila double-parked is sufficient to induce re-replication during development and is regulated by cyclin E/CDK2. Development 131, 4807-4818.
65. Ugland, H., Boquest, A. C., Naderi, S., Collas, P. and Blomhoff, H. K. (2008). cAMP-mediated induction of cyclin E sensitizes growth-arrested adipose stem cells to DNA damage-induced apoptosis. Mol. Biol. Cell 19, 5082-5092.
66. Wang, Z. A. and Kalderon, D. (2009). Cyclin E-dependent protein kinase activity regulates niche retention of Drosophila ovarian follicle stem cells. Proc. Natl. Acad. Sci. USA 106, 21701-21706.
67. 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.
68. White, A. E., Leslie, M. E., Calvi, B. R., Marzluff, W. F. and Duronio, R. J. (2007). Developmental and cell cycle regulation of the Drosophila histone locus body. Mol. Biol. Cell 18, 2491-2502.
69. Whittaker, A. J., Royzman, I. and Orr-Weaver, T. L. (2000). Drosophila double parked: a conserved, essential replication protein that colocalizes with the origin recognition complex and links DNA replication with mitosis and the down- regulation of S phase transcripts. Genes Dev. 14, 1765-1776.
70. Xi, R. and Xie, T. (2005). Stem cell self-renewal controlled by chromatin remodeling factors. Science 310, 1487-1489.
71. 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.
72. 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.
73. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
74. Yu, S. Y., Yoo, S. J., Yang, L., Zapata, C., Srinivasan, A., Hay, B. A. and Baker, N. E. (2002). A pathway of signals regulating effector and initiator caspases in the developing Drosophila eye. Development 129, 3269-3278.