Cyclin G is involved in meiotic recombination repair in Drosophila Melanogaster

Journal of Cell Science

Volumn 125, Issue 22, 2012, Pages 5555-5563

  Nagel, Anja C ^a   Fischer, Patrick ^a   Szawinski, Jutta ^a   La Rosa, Martina K ^a   Preiss, Anette ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

9 1 1 complex; BRCA2; Cyclin G; Double strand break repair; DSB; Meiotic checkpoint

Indexed keywords

BRCA2 PROTEIN; CYCLIN G; DOUBLE STRANDED DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN RAD9;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; DROSOPHILA MELANOGASTER; EGG SHELL; GENE; IN VIVO STUDY; MEIOSIS; NONHUMAN; OOCYTE DEVELOPMENT; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; BODY PATTERNING; CYCLIN G; DNA BREAKS, DOUBLE-STRANDED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOPRECIPITATION; MALE; MEIOSIS; MUTANT PROTEINS; MUTATION; OOCYTES; OVARY; OVIPOSITION; OVUM; PROTEIN BINDING; RECOMBINATIONAL DNA REPAIR; REPRODUCIBILITY OF RESULTS;

EID: 84873551026     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.113902     Document Type: Article

References (50)

1. Abdu, U., Brodsky, M. and Schüpbach, T. (2002). Activation of a meiotic checkpoint during Drosophila oogenesis regulates the translation of Gurken through Chk2/Mnk. Curr. Biol. 12, 1645-1651.
2. Abdu, U., Klovstad, M., Butin-Israeli, V., Bakhrat, A. and Schüpbach, T. (2007). An essential role for Drosophila hus1 in somatic and meiotic DNA damage responses. J. Cell Sci. 120, 1042-1049.
3. Alexiadis, V., Lusser, A. and Kadonaga, J. T. (2004). A conserved N-terminal motif in Rad54 is important for chromatin remodeling and homologous strand pairing. J. Biol. Chem. 279, 27824-27829.
4. Bennin, D. A., Don, A. S., Brake, T., McKenzie, J. L., Rosenbaum, H., Ortiz, L., DePaoli-Roach, A. A. and Horne, M. C. (2002). Cyclin G2 associates with protein phosphatase 2A catalytic and regulatory B' subunits in active complexes and induces nuclear aberrations and a G1/S phase cell cycle arrest. J. Biol. Chem. 277, 27449-27467.
5. Brough, R., Wei, D., Leulier, S., Lord, C. J., Rong, Y. S. and Ashworth, A. (2008). Functional analysis of Drosophila melanogaster BRCA2 in DNA repair. DNA Repair (Amst.) 7, 10-19.
6. Chen, X. (2002). Cyclin G: a regulator of the p53-Mdm2 network. Dev. Cell 2, 518-519. Chou, T. B. and Perrimon, N. (1992). Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131, 643-653.
7. Chou, T. B. and Perrimon, N. (1992). Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131, 643-653.
8. Chowdhury, D., Keogh, M. C., Ishii, H., Peterson, C. L., Buratowski, S. and Lieberman, J. (2005). c-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell 20, 801-809.
9. Esashi, F., Christ, N., Gannon, J., Liu, Y., Hunt, T., Jasin, M. and West, S. C. (2005). CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 434, 598-604.
10. Faradji, F., Bloyer, S., Dardalhon-Cuménal, D., Randsholt, N. B. and Peronnet, F. (2011). Drosophila melanogaster Cyclin G coordinates cell growth and cell proliferation. Cell Cycle 10, 805-818.
11. Forget, A. L. and Kowalczykowski, S. C. (2010). Single-molecule imaging brings Rad51 nucleoprotein filaments into focus. Trends Cell Biol. 20, 269-276.
12. Ghabrial, A. and Schüpbach, T. (1999). Activation of a meiotic checkpoint regulates translation of Gurken during Drosophila oogenesis. Nat. Cell Biol. 1, 354-357.
13. Ghabrial, A., Ray, R. P. and Schüpbach, T. (1998). okra and spindle-B encode components of the RAD52 DNA repair pathway and affect meiosis and patterning in Drosophila oogenesis. Genes Dev. 12, 2711-2723.
14. Giot, L., Bader, J. S., Brouwer, C., Chaudhuri, A., Kuang, B., Li, Y., Hao, Y. L., Ooi, C. E., Godwin, B., Vitols, E. et al. (2003). A protein interaction map of Drosophila melanogaster. Science 302, 1727-1736.
15. González-Reyes, A., Elliott, H. and St Johnston, D. (1997). Oocyte determination and the origin of polarity in Drosophila: the role of the spindle genes. Development 124, 4927-4937.
16. Jang, J. K., Sherizen, D. E., Bhagat, R., Manheim, E. A. and McKim, K. S. (2003). Relationship of DNA double-strand breaks to synapsis in Drosophila. J. Cell Sci. 116, 3069-3077.
17. Johnstone, O. and Lasko, P. (2004). Interaction with eIF5B is essential for Vasa function during development. Development 131, 4167-4178.
18. Joyce, E. F., Pedersen, M., Tiong, S., White-Brown, S. K., Paul, A., Campbell, S. D. and McKim, K. S. (2011). Drosophila ATM and ATR have distinct activities in the regulation of meiotic DNA damage and repair. J. Cell Biol. 195, 359-367.
19. Kanaoka, Y., Kimura, S. H., Okazaki, I., Ikeda, M. and Nojima, H. (1997). GAK: a cyclin G associated kinase contains a tensin/auxilin-like domain. FEBS Lett. 402, 73-80.
20. Kimura, S. H., Ikawa, M., Ito, A., Okabe, M. and Nojima, H. (2001). Cyclin G1 is involved in G2/M arrest in response to DNA damage and in growth control after damage recovery. Oncogene 20, 3290-3300.
21. Klattenhoff, C., Bratu, D. P., McGinnis-Schultz, N., Koppetsch, B. S., Cook, H. A. and Theurkauf, W. E. (2007). Drosophila rasiRNA pathway mutations disrupt embryonic axis specification through activation of an ATR/Chk2 DNA damage response. Dev. Cell 12, 45-55.
22. Klattenhoff, C., Xi, H., Li, C., Lee, S., Xu, J., Khurana, J. S., Zhang, F., Schultz, N., Koppetsch, B. S., Nowosielska, A. et al. (2009). The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 138, 1137-1149.
23. Klovstad, M., Abdu, U. and Schüpbach, T. (2008). Drosophila brca2 is required for mitotic and meiotic DNA repair and efficient activation of the meiotic recombination checkpoint. PLoS Genet. 4, e31.
24. Lancaster, O. M., Breuer, M., Cullen, C. F., Ito, T. and Ohkura, H. (2010). The meiotic recombination checkpoint suppresses NHK-1 kinase to prevent reorganisation of the oocyte nucleus in Drosophila. PLoS Genet. 6, e1001179.
25. Maier, D., Stumm, G., Kuhn, K. and Preiss, A. (1992). Hairless, a Drosophila gene involved in neural development, encodes a novel, serine rich protein. Mech. Dev. 38, 143-156.
26. McKim, K. S. and Hayashi-Hagihara, A. (1998). mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev. 12, 2932-2942.
27. McKim, K. S., Joyce, E. F. and Jang, J. K. (2009). Cytological analysis of meiosis in fixed Drosophila ovaries. Methods Mol. Biol. 558, 197-216.
28. Mehrotra, S. and McKim, K. S. (2006). Temporal analysis of meiotic DNA doublestrand break formation and repair in Drosophila females. PLoS Genet. 2, e200.
29. Morris, J. and Lehmann, R. (1999). Drosophila oogenesis: versatile spn doctors. Curr. Biol. 9, R55-R58.
30. Murali, T., Pacifico, S., Yu, J., Guest, S., Roberts, G. G., 3rd and Finley, R. L., Jr (2011). DroID 2011: a comprehensive, integrated resource for protein, transcription factor, RNA and gene interactions for Drosophila. Nucleic Acids Res. 39, D736-D743.
31. Nagel, A. C., Szawinski, J., Fischer, P., Maier, D., Wech, I. and Preiss, A. (2012). Dorso-ventral axis formation of the Drosophila oocyte requires Cyclin G. Hereditas 149, 186-196.
32. Naito, Y., Shimizu, H., Kasama, T., Sato, J., Tabara, H., Okamoto, A., Yabuta, N. and Nojima, H. (2012). Cyclin G-associated kinase regulates protein phosphatase 2A by phosphorylation of its B'c subunit. Cell Cycle 11, 604-616.
33. Okamoto, K., Li, H., Jensen, M. R., Zhang, T., Taya, Y., Thorgeirsson, S. S. and Prives, C. (2002). Cyclin G recruits PP2A to dephosphorylate Mdm2. Mol. Cell 9, 761-771.
34. Pardo, B., Gómez-González, B. and Aguilera, A. (2009). DNA repair in mammalian cells: DNA double-strand break repair: how to fix a broken relationship. Cell. Mol. Life Sci. 66, 1039-1056.
35. Peretz, G., Arie, L. G., Bakhrat, A. and Abdu, U. (2009). The Drosophila hus1 gene is required for homologous recombination repair during meiosis. Mech. Dev. 126, 677-686.
36. Petersen, P., Chou, D. M., You, Z., Hunter, T., Walter, J. C. and Walter, G. (2006). Protein phosphatase 2A antagonizes ATM and ATR in a Cdk2-and Cdc7-independent DNA damage checkpoint. Mol. Cell. Biol. 26, 1997-2011.
37. Rong, Y. S., Titen, S. W., Xie, H. B., Golic, M. M., Bastiani, M., Bandyopadhyay, P., Olivera, B. M., Brodsky, M., Rubin, G. M. and Golic, K. G. (2002). Targeted mutagenesis by homologous recombination in D. melanogaster. Genes Dev. 16, 1568-1581.
38. Rørth, P. (1998). Gal4 in the Drosophila female germline. Mech. Dev. 78, 113-118. Rubin, G. M. and Spradling, A. C. (1982). Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353.
39. Rubin, G. M. and Spradling, A. C. (1982). Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353.
40. Salvaing, J., Nagel, A. C., Mouchel-Vielh, E., Bloyer, S., Maier, D., Preiss, A. and Peronnet, F. (2008a). The enhancer of Trithorax and Polycomb Corto interacts with Cyclin G in Drosophila. PLoS One 3, e1658.
41. Salvaing, J., Mouchel-Vielh, E., Bloyer, S., Preiss, A. and Peronnet, F. (2008b). Regulation of Abd-B expression by Cyclin G and Corto in the abdominal epithelium of Drosophila. Hereditas 145, 138-146.
42. Sarkaria, J. N., Busby, E. C., Tibbetts, R. S., Roos, P., Taya, Y., Karnitz, L. M. and Abraham, R. T. (1999). Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 59, 4375-4382
43. Schüpbach, T (1987). Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of egg shell and embryo in Drosophila melanogaster. Cell 49, 699-707.
44. Shiloh, Y. (2006). The ATM-mediated DNA-damage response: taking shape. Trends Biochem. Sci. 31, 402-410.
45. Staeva-Vieira, E., Yoo, S. and Lehmann, R. (2003). An essential role of DmRad51/ SpnA in DNA repair and meiotic checkpoint control. EMBO J. 22, 5863-5874.
46. Stanyon, C. A., Liu, G., Mangiola, B. A., Patel, N., Giot, L., Kuang, B., Zhang, H., Zhong, J. and Finley, R. L., Jr (2004). A Drosophila protein-interaction map centered on cell-cycle regulators. Genome Biol. 5, R96.
47. Summers, K. C., Shen, F., Sierra Potchanant, E. A., Phipps, E. A., Hickey, R. J. and Malkas, L. H. (2011). Phosphorylation: the molecular switch of double-strand break repair. Int. J. Proteomics 2011, doi:10.1155/2011/373816.
48. Tautz, D. and Pfeifle, C. (1989). A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81-85.
49. Van der Meer, J. (1977). Optical clean and permanent whole mount preparations for phasecontrast microscopy of cuticular structures of insect larvae. Drosoph. Inf. Serv. 52, 160.
50. Yu, J., Pacifico, S., Liu, G. and Finley, R. L., Jr (2008). DroID: the Drosophila Interactions Database, a comprehensive resource for annotated gene and protein interactions. BMC Genomics 9, 461.