Cul4 and DDB1 regulate Orc2 localization, BrdU incorporation and Dup stability during gene amplification in Drosophila follicle cells

Journal of Cell Science

Volumn 122, Issue 14, 2009, Pages 2393-2401

  Lin, Hsiu Chen ^a,b   Wu, June Tai ^c,d   Tan, Bertrand Chin Ming ^e   Chien, Cheng Ting ^a,b  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

Cdt1; Chorion gene amplification; Cul4; DDB1; DNA replication; Dup; Orc2; Pre RC; Proliferation

Indexed keywords

BROXURIDINE; CULLIN 4; DNA DAMAGE BINDING PROTEIN 1; DOUBLE PARKED PROTEIN; DROSOPHILA PROTEIN; GENOMIC DNA; ORIGIN RECOGNITION COMPLEX 2 PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CELL PROLIFERATION; CHORION; CONTROLLED STUDY; DNA REPLICATION; DROSOPHILA; GENE AMPLIFICATION; INSECT CELL; LARVAL STAGE; NONHUMAN; OVARY FOLLICLE CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY;

ANIMALS; BROMODEOXYURIDINE; CELL CYCLE PROTEINS; CELL PROLIFERATION; CHORION; CULLIN PROTEINS; DNA REPLICATION; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE AMPLIFICATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; MUTATION; ORIGIN RECOGNITION COMPLEX; OVARIAN FOLLICLE; PROTEIN STABILITY;

EUKARYOTA;

EID: 69649103008     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.042861     Document Type: Article

References (57)

1. Abbas, T., Sivaprasad, U., Terai, K., Amador, V., Pagano, M. and Dutta, A. (2008). PCNA-dependent regulation of p21 ubiquitylation and degradation via the CRL4Cdt2 ubiquitin ligase complex. Genes Dev. 22, 2496-2506.
2. Aggarwal, B. D. and Calvi, B. R. (2004). Chromatin regulates origin activity in Drosophila follicle cells. Nature 430, 372-376.
3. Aggarwal, P., Lessie, M. D., Lin, D. I., Pontano, L., Gladden, A. B., Nuskey, B., Goradia, A., Wasik, M. A., Klein-Szanto, A. J., Rustgi, A. K. et al. (2007). Nuclear accumulation of cyclin D1 during S phase inhibits Cul4-dependent Cdt1 proteolysis and triggers p53-dependent DNA rereplication. Genes Dev. 21, 2908-2922.
4. Arias, E. E. and Walter, J. C. (2006). PCNA functions as a molecular platform to trigger Cdt1 destruction and prevent re-replication. Nat. Cell Biol. 8, 84-90.
5. Arias, E. E. and Walter, J. C. (2007). Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 21, 497-518.
6. Austin, R. J., Orr-Weaver, T. L. and Bell, S. P. (1999). Drosophila ORC specifically binds to ACE3, an origin of DNA replication control element. Genes Dev. 13, 2639-2649.
7. Baker, N. E. and Rubin, G. M. (1992). Ellipse mutations in the Drosophila homologue of the EGF receptor affect pattern formation, cell division, and cell death in eye imaginal discs. Dev. Biol. 150, 381-396.
8. Beall, E. L., Manak, J. R., Zhou, S., Bell, M., Lipsick, J. S. and Botchan, M. R. (2002). Role for a Drosophila Myb-containing protein complex in site-specific DNA replication. Nature 420, 833-837.
9. Beall, E. L., Bell, M., Georlette, D. and Botchan, M. R. (2004). Dm-myb mutant lethality in Drosophila is dependent upon mip130: positive and negative regulation of DNA replication. Genes Dev. 18, 1667-1680.
10. Blow, J. J. and Dutta, A. (2005). Preventing re-replication of chromosomal DNA. Nat. Rev. Mol. Cell. Biol. 6, 476-486.
11. Bosco, G., Du, W. and Orr-Weaver, T. L. (2001). DNA replication control through interaction of E2F-RB and the origin recognition complex. Nat. Cell Biol. 3, 289-295.
12. Callus, B. A. and Vaux, D. L. (2007). Caspase inhibitors: viral, cellular and chemical. Cell Death Differ. 14, 73-78.
13. Calvi, B. R. and Spradling, A. C. (1999). Chorion gene amplification in Drosophila: a model for metazoan origins of DNA replication and S-phase control. Methods 18, 407-417.
14. Calvi, B. R., Lilly, M. A. and Spradling, A. C. (1998). Cell cycle control of chorion gene amplification. Genes Dev. 12, 734-744.
15. Cavaliere, V., Bernardi, F., Romani, P., Duchi, S. and Gargiulo, G. (2008). Building up the Drosophila eggshell: first of all the eggshell genes must be transcribed. Dev. Dyn. 237, 2061-2072.
16. Cayirlioglu, P., Bonnette, P. C., Dickson, M. R. and Duronio, R. J. (2001). Drosophila E2f2 promotes the conversion from genomic DNA replication to gene amplification in ovarian follicle cells. Development 128, 5085-5098.
17. Cayirlioglu, P., Ward, W. O., Silver Key, S. C. and Duronio, R. J. (2003). Transcriptional repressor functions of Drosophila E2F1 and E2F2 cooperate to inhibit genomic DNA synthesis in ovarian follicle cells. Mol. Cell. Biol. 23, 2123-2134.
18. Chen, C. K. and Chien, C. T. (1999). Negative regulation of atonal in proneural cluster formation of Drosophila R8 photoreceptors. Proc. Natl. Acad. Sci. USA 96, 5055-5060.
19. Claycomb, J. M. and Orr-Weaver, T. L. (2005). Developmental gene amplification: insights into DNA replication and gene expression. Trends Genet. 21, 149-162.
20. Claycomb, J. M., MacAlpine, D. M., Evans, J. G., Bell, S. P. and Orr-Weaver, T. L. (2002). Visualization of replication initiation and elongation in Drosophila. J. Cell Biol. 159, 225-236.
21. Claycomb, J. M., Benasutti, M., Bosco, G., Fenger, D. D. and Orr-Weaver, T. L. (2004). Gene amplification as a developmental strategy: isolation of two developmental amplicons in Drosophila. Dev. Cell 6, 145-155.
22. Dai, Q. and Wang, H. (2006). Cullin 4 makes its mark on chromatin. Cell Div. 1, 14.
23. Delidakis, C. and Kafatos, F. C. (1989). Amplification enhancers and replication origins in the autosomal chorion gene cluster of Drosophila. EMBO J. 8, 891-901.
24. DePamphilis, M. L. (2003). The 'ORC cycle': a novel pathway for regulating eukaryotic DNA replication. Gene 310, 1-15.
25. He, Y. J., McCall, C. M., Hu, J., Zeng, Y. and Xiong, Y. (2006). DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev. 20, 2949-2954.
26. Higa, L. A., Wu, M., Ye, T., Kobayashi, R., Sun, H. and Zhang, H. (2006a). CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol. 8, 1277-1283.
27. Higa, L. A., Yang, X., Zheng, J., Banks, D., Wu, M., Ghosh, P., Sun, H. and Zhang, H. (2006b). Involvement of CUL4 ubiquitin E3 ligases in regulating CDK inhibitors Dacapo/p27Kip1 and cyclin E degradation. Cell Cycle 5, 71-77.
28. Hong, E. J., Villen, J., Gerace, E. L., Gygi, S. P. and Moazed, D. (2005). A cullin E3 ubiquitin ligase complex associates with Rik1 and the Clr4 histone H3-K9 methyltransferase and is required for RNAi-mediated heterochromatin formation. RNA Biol. 2, 106-111.
29. Hu, J., Zacharek, S., He, Y. J., Lee, H., Shumway, S., Duronio, R. J. and Xiong, Y. (2008). WD40 protein FBW5 promotes ubiquitination of tumor suppressor TSC2 by DDB1-CUL4-ROC1 ligase. Genes Dev. 22, 866-871.
30. Jia, S., Kobayashi, R. and Grewal, S. I. (2005). Ubiquitin ligase component Cul4 associates with Clr4 histone methyltransferase to assemble heterochromatin. Nat. Cell Biol. 7, 1007-1013.
31. Kapetanaki, M. G., Guerrero-Santoro, J., Bisi, D. C., Hsieh, C. L., Rapic-Otrin, V. and Levine, A. S. (2006). The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc. Natl. Acad. Sci. USA 103, 2588-2593.
32. Kim, Y. and Kipreos, E. T. (2007). The Caenorhabditis elegans replication licensing factor CDT-1 is targeted for degradation by the CUL-4/DDB-1 complex. Mol. Cell. Biol. 27, 1394-1406.
33. Kim, Y., Starostina, N. G. and Kipreos, E. T. (2008). The CRL4Cdt2 ubiquitin ligase targets the degradation of p21Cip1 to control replication licensing. Genes Dev. 22, 2507-2519.
34. Labib, K. and Gambus, A. (2007). A key role for the GINS complex at DNA replication forks. Trends Cell Biol. 17, 271-278.
35. Lee, J. and Zhou, P. (2007). DCAFs, the missing link of the CUL4-DDB1 ubiquitin ligase. Mol. Cell 26, 775-780.
36. Lee, T. and Luo, L. (2001). Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24, 251-254.
37. Lee, T., Winter, C., Marticke, S. S., Lee, A. and Luo, L. (2000). Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25, 307-316.
38. 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.
39. Lu, L., Zhang, H. and Tower, J. (2001). Functionally distinct, sequence-specific replicator and origin elements are required for Drosophila chorion gene amplification. Genes Dev. 15, 134-146.
40. Machida, Y. J., Hamlin, J. L. and Dutta, A. (2005). Right place, right time, and only once: replication initiation in metazoans. Cell 123, 13-24.
41. May, N. R., Thomer, M., Murnen, K. F. and Calvi, B. R. (2005). Levels of the origin-binding protein Double parked and its inhibitor Geminin increase in response to replication stress. J. Cell Sci. 118, 4207-4217.
42. Nishitani, H., Sugimoto, N., Roukos, V., Nakanishi, Y., Saijo, M., Obuse, C., Tsurimoto, T., Nakayama, K. I., Nakayama, K., Fujita, M. et al. (2006). Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBO J. 25, 1126-1136.
43. Nishitani, H., Shiomi, Y., Iida, H., Michishita, M., Takami, T. and Tsurimoto, T. (2008). CDK inhibitor p21 is degraded by a PCNA coupled Cul4-DDB1Cdt2 pathway during S phase and after UV irradiation. J. Biol. Chem. 283, 29045-29052.
44. Prober, D. A. and Edgar, B. A. (2000). Ras1 promotes cellular growth in the Drosophila wing. Cell 100, 435-446.
45. Royzman, I., Austin, R. J., Bosco, G., Bell, S. P. and Orr-Weaver, T. L. (1999). ORC localization in Drosophila follicle cells and the effects of mutations in dE2F and dDP. Genes Dev. 13, 827-840.
46. Saxena, S. and Dutta, A. (2005). Geminin-Cdt1 balance is critical for genetic stability. Mutat. Res. 569, 111-121.
47. Senga, T., Sivaprasad, U., Zhu, W., Park, J. H., Arias, E. E., Walter, J. C. and Dutta, A. (2006). PCNA is a cofactor for Cdt1 degradation by CUL4/DDB1-mediated N-terminal ubiquitination. J. Biol. Chem. 281, 6246-6252.
48. Shibutani, S. T., de la Cruz, A. F., Tran, V., Turbyfill, W. J., 3rd, Reis, T., Edgar, B. A. and Duronio, R. J. (2008). Intrinsic negative cell cycle regulation provided by PIP box-and Cul4Cdt2-mediated destruction of E2f1 during S phase. Dev. Cell 15, 890-900.
49. Spradling, A. C. (1981). The organization and amplification of two chromosomal domains containing Drosophila chorion genes. Cell 27, 193-201.
50. Sun, J., Smith, L., Armento, A. and Deng, W. M. (2008). Regulation of the endocycle/gene amplification switch by Notch and ecdysone signaling. J. Cell Biol. 182, 885-896.
51. Tower, J. (2004). Developmental gene amplification and origin regulation. Annu. Rev. Genet. 38, 273-304.
52. Wang, H., Zhai, L., Xu, J., Joo, H. Y., Jackson, S., Erdjument-Bromage, H., Tempst, P., Xiong, Y. and Zhang, Y. (2006). Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol. Cell 22, 383-394.
53. 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.
54. Wohlschlegel, J. A., Dwyer, B. T., Dhar, S. K., Cvetic, C., Walter, J. C. and Dutta, A. (2000). Inhibition of eukaryotic DNA replication by geminin binding to Cdt1. Science 290, 2309-2312.
55. Xouri, G., Dimaki, M., Bastiaens, P. I. and Lygerou, Z. (2007). Cdt1 interactions in the licensing process: a model for dynamic spatiotemporal control of licensing. Cell Cycle 6, 1549-1552.
56. Zhang, H. and Tower, J. (2004). Sequence requirements for function of the Drosophila chorion gene locus ACE3 replicator and ori-beta origin elements. Development 131, 2089-2099.
57. Zhou, Q., Krebs, J. F., Snipas, S. J., Price, A., Alnemri, E. S., Tomaselli, K. J. and Salvesen, G. S. (1998). Interaction of the baculovirus anti-apoptotic protein p35 with caspases. Specificity, kinetics, and characterization of the caspase/p35 complex. Biochemistry 37, 10757-10765.