The Drosophila homolog of MCPH1, a human microcephaly gene, is required for genomic stability in the early embryo

Journal of Cell Science

Volumn 120, Issue 20, 2007, Pages 3565-3577

  Rickmyre, Jamie L ^a   DasGupta, Shamik ^b   Ooi, Danny Liang Yee ^c   Keel, Jessica ^a   Lee, Ethan ^a   Kirschner, Marc W ^c   Waddell, Scott ^b   Lee, Laura A ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

BRCT domain; Cell cycle; DNA checkpoint; Drosophila; Embryogenesis; Microcephaly; Mitosis

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CYCLIN DEPENDENT KINASE 1; MICROCEPHALIN; NUCLEAR PROTEIN; UNCLASSIFIED DRUG;

ANAPHASE; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CENTROSOME; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; ENZYME PHOSPHORYLATION; FEMALE; GENE IDENTIFICATION; GENE MUTATION; GENETIC CONSERVATION; GENETIC SCREENING; GENOMIC INSTABILITY; MALE; MICROCEPHALY; MITOSIS INHIBITION; MITOSIS SPINDLE; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PREMATURE CHROMOSOME CONDENSATION; PRIORITY JOURNAL;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CHROMATIN; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GENES, INSECT; GENOMIC INSTABILITY; MITOSIS; MUSHROOM BODIES; MUTATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES;

BASIDIOMYCOTA;

EID: 36248952558     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.016626     Document Type: Article

References (68)

1. Abdu, U., Brodsky, M. and Schupbach, T. (2002). Activation of a meiotic checkpoint during Drosophila oogenesis regulates the translation of Gurken through Chk2/Mnk. Curr. Biol. 12, 1645-1651.
2. Alderton, G. K., Galbiati, L., Griffith, E., Surinya, K. H., Neitzel, H., Jackson, A. P., Jeggo, P. A. and O'Driscoll, M. (2006). Regulation of mitotic entry by microcephalin and its overlap with ATR signalling. Nat. Cell Biol. 8, 725-733.
3. Ballinger, D. G. and Benzer, S. (1989). Targeted gene mutations in Drosophila. Proc. Natl. Acad. Sci. USA 86, 9402-9406.
4. Bartek, J. (2006). Microcephalin guards against small brains, genetic instability, and cancer. Cancer Cell 10, 91-93.
5. Basto, R., Lou, J., Vinogradova, T., Gardiol, A., Woods, C. G., Khodjakov, A. and Raff, J. W. (2006). Flies without centrioles. Cell 125, 1375-1386.
6. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
7. Brodsky, M. H., Sekelsky, J. J., Tsang, G., Hawley, R. S. and Rubin, G. M. (2000). mus304 encodes a novel DNA damage checkpoint protein required during Drosophila development. Genes Dev. 14, 666-678.
8. Brodsky, M. H., Weinert, B. T., Tsang, G., Rong, Y. S., McGinnis, N. M., Golic, K. G., Rio, D. C. and Rubin, G. M. (2004). Drosophila melanogaster MNK/Chk2 and p53 regulate multiple DNA repair and apoptotic pathways following DNA damage. Mol. Cell. Biol. 24, 1219-1231.
9. Chen, B., Chu, T., Harms, E., Gergen, J. P. and Strickland, S. (1998). Mapping of Drosophila mutations using site-specific male recombination. Genetics 149, 157-163.
10. Cox, J., Jackson, A. P., Bond, J. and Woods, C. G. (2006). What primary microcephaly can tell us about brain growth. Trends Mol. Med. 12, 358-366.
11. Crittenden, J. R., Skoulakis, E. M., Han, K. A., Kalderon, D. and Davis, R. L. (1998). Tripartite mushroom body architecture revealed by antigenic markers. Learn. Mem. 5, 38-51.
12. de Belle, J. S. and Heisenberg, M. (1994). Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692-695.
13. do Carmo Avides, M. and Glover, D. M. (1999). Abnormal spindle protein, Asp, and the integrity of mitotic centrosomal microtubule organizing centers. Science 283, 1733-1735.
14. Fenger, D. D., Carminati, J. L., Burney-Sigman, D. L., Kashevsky, H., Dines, J. L., Elfring, L. K. and Orr-Weaver, T. L. (2000). PAN GU: a protein kinase that inhibits S phase and promotes mitosis in early Drosophila development. Development 127, 4763-4774.
15. Foe, V. E., Odell, G. M. and Edgar, B. A. (1993). Mitosis and morphogenesis in the Drosophila embryo: point and counterpoint. In The Development of Drosaphila melanogaster (ed. M. Bate and A. Martinez Arias), pp. 149-300. Cold Spring Harbor, NY. Cold Spring Harbor Laboratory Press.
16. Fogarty, P., Campbell, S. D., Abu-Shumays, R., Phalle, B. S., Yu, K. R., Uy, G. L., Goldberg, M. L. and Sullivan, W. (1997). Tne Drosophila grapes gene is related to checkpoint gene chk1/rad27 and is required for late syncytial division fidelity. Curr. Biol. 7, 418-426.
17. Freeman, M., Nusslein-Volhard, C. and Glover, D. M. (1986). The dissociation of nuclear and centrosomal division in gnu, a mutation causing giant nuclei in Drosophila. Cell 46, 457-468.
18. Glover, D. M., Leibowitz, M. H., McLean, D. A. and Parry, H. (1995). Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles. Cell 81, 95-105.
19. Glover, J. N., Williams, R. S. and Lee, M. S. (2004). Interactions between BRCT repeats and phosphoproteins: tangled up in two. Trends Biochem. Sci. 29, 579-585.
20. Greenspan, R. J. (2004). Fly Pushing: The Theory and Practice of Drosophila Genetics. Cold Spring Harbor, NY. Cold Spring Harbor Laboratory Press.
21. Grenningloh, G., Rehm, E. J. and Goodman, C. S. (1991). Genetic analysis of growth cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule. Cell 67, 45-57.
22. Grumbling, G. and Strelets, V. (2006). FlyBase: anatomical data, images and queries. Nucleic Acids Res. 34, D484-D488.
23. Huyton, T., Bates, P. A., Zhang, X., Sternberg, M. J. and Freemont, P. S. (2000). The BRCA1 C-terminal domain: structure and function. Mutat. Res. 460, 319-332.
24. Jackson, A. P., Eastwood, H., Bell, S. M., Adu, J., Toomes, C., Carr, I. M., Roberts, E., Hampshire, D. J., Crow, Y. J., Mighell, A. J. et al. (2002). Identification of microcephalin, a protein implicated in determining the size of the human brain. Am. J. Hum. Genet. 71, 136-142.
25. Jaklevic, B. R. and Su, T. T. (2004). Relative contribution of DNA repair, cell cycle checkpoints, and cell death to survival after DNA damage in Drosophila larvae. Curr. Biol. 14, 23-32.
26. Jeffers, L. J., Coull, B. J., Stack, S. J. and Morrison, C. G. (2007). Distinct BRCT domains in Mcph1/Brit1 mediate ionizing radiation-induced focus formation and centrosomal localization. Oncogene doi:10.1038/sj.onc.1210595.
27. Koundakjian, E. J., Cowan, D. M., Hardy, R. W. and Becker, A. H. (2004). The Zuker collection: a resource for the analysis of autosomal gene function in Drosophila melanogaster. Genetics 167, 203-206.
28. Kramer, A., Mailand, N., Lukas, C., Syljuasen, R. G., Wilkinson, C. J., Niggg, E. A., Bartek, J. and Lukas, J. (2004). Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase. Nat. Cell Biol. 6, 884-891.
29. Krashes, M. J., Keene, A. C., Leung, B., Armstrong, J. D. and Waddell, S. (2007). Sequential use of mushroom body neuron subsets during drosophila odor memory processing. Neuron 53, 103-115.
30. Larocque, J. R., Jaklevic, B. R., So, T. T. and Sekelsky, J. (2007). Drosophila ATR in double-strand break repair. Genetics 175, 1023-1033.
31. Lee, L. A. and Orr-Weaver, T. L. (2003). Regulation of cell cycles in Drosophila development: intrinsic and extrinsic cues. Annu. Rev. Genet. 37, 545-578.
32. Lee, L. A., Van Hoewyk, D. and Orr-Weaver, T. L. (2003). The Drosophila cell cycle kinase PAN GU forms an active complex with PLUTONIUM and GNU to regulate embryonic divisions. Genes Dev. 17, 2979-2991.
33. Li, K. and Kaufman, T. C. (1996). The homeotic target gene centrosomin encodes an essential centrosomal component. Cell 85, 585-596.
34. Lin, S. Y. and Elledge, S. J. (2003). Multiple tumor suppressor pathways negatively regulate telomerase. Cell 113, 881-889.
35. Lin, S. Y., Rai, R., Li, K., Xu, Z. X. and Elledge, S. J. (2005). BRIT1/MCPH1 is a DNA damage responsive protein that regulates the Brca1-Chk1 pathway, implicating checkpoint dysfunction in microcephaly. Proc. Natl. Acad. Sci. USA 102, 15105-15109.
36. Masrouha, N., Yang, L., Hijal, S., Larochelle, S. and Suter, B. (2003). The Drosophila chk2 gene loki is essential for embryonic DNA double-strand-break checkpoints induced in S phase or G2. Genetics 163, 973-982.
37. Megraw, T. L., Li, K., Kao, L. R. and Kaufman, T. C. (1999). The centrosomin protein is required for centrosome assembly and function during cleavage in Drosophila. Development 126, 2829-2839.
38. Nyberg, K. A., Michelson, R. J., Putnam, C. W. and Weinert, T. A. (2002). Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36, 617-656.
39. O'Driscoll, M., Ruiz-Perez, V. L., Woods, C. G., Jeggo, P. A. and Goodship, J. A. (2003). A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat. Genet. 33, 497-501.
40. O'Farrell, F. H., Stumpff, J. and Su. T. T. (2004). Embryonic cleavage cycles: how is a mouse like a fly? Curr. Biol. 14, R35-R45.
41. Oh, S. W., Kingsley, T., Shin, H. H., Zheng, Z., Chen, H. W., Chen, X., Wang, H., Ruan, P., Moody, M. and Hou, S. X. (2003). A P-element insertion screen identified mutations in 455 novel essential genes in Drosophila. Genetics 163, 195-201.
42. Oikemus, S. R., McGinnis, N., Queiroz-Machado, J., Takachinsky, H., Takada, S., Sunkel, C. E. and Brodsky, M. H. (2004). Drosophila atm/ telomere fusion is required for telomefic localization of HP1 and telomere position effect. Genes Dev. 18, 1850-1861.
43. Petermann, E. and Caldecott, K. W. (2006). Evidence that the ATR/ Chk1 pathway maintains normal replication fork progression during unperturbed S phase. Cell Cycle 5, 2203-2209.
44. Price, D., Rabinovitch, S., O'Farrell, P. H. and Campbell, S. D. (2000). Drosophila weel has an essential role in the nuclear divisions of early embryogenesis. Genetics 155, 159-166.
45. Purdy, A., Uyetake, L., Cordeiro, M. G. and Su, T. T. (2005). Regulation of mitosis in response to damaged or incompletely replicated DNA require different levels of Grapes (Drosophila Chk1). J. Cell Sci. 118, 3305-3315.
46. Raff, J. W. and Glover, D. M. (1988). Nuclear and cytoplasmic mitotic cycles continue in Drosophila embryos in which DNA synthesis is inhibited with aphidicolin. J. Cell Biol. 107, 2009-2019.
47. Rai, R., Dai, H., Multani, A. S., Li, K., Chin, K., Gray, J., Lahad, J. P., Liang, J., Mills, G. B., Merie-Bernstam, F. et al. (2006). BRIT1 regulates early DNA damage response, chromosomal integrity, and cancer. Cancer Cell 10, 145-157.
48. Renault, A. D., Zhang, X. H., Alphey, L. S., Frenz, L. M., Glover, D. M., Saunders, R. D. and Axton, J. M. (2003). giant nuclei is essential in the cell cycle transition from meiosis to mitosis. Development 130, 2997-3005.
49. Rorth, P. (1998). Gal4 in the Drosophila female germline. Mech. Dev. 78, 113-118.
50. Rothwell, W. F. and Sullivan, W. (2000). Fluorescent analysis of Drosophila embryos. In Drosophila Protocols (ed. W. Sullivan, M. Ashburner and R. S. Hawley), pp. 141-157. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
51. Sibon, O. C., Stevenson, V. A. and Theurkauf, W. E. (1997). DNA-replication checkpoint control at the Drosophila midblastula transition. Nature 388, 93-97.
52. Sibon, O. C., Laurencon, A., Hawley, R. and Theurkauf, W. E. (1999). The Drosophila ATM homologue Mei-41 has an essential checkpoint function at the midblastula transition. Curr. Biol. 9, 302-312.
53. Sibon, O. C., Kelkar, A., Lemstra, W. and Theurkauf, W. E. (2000). DNA-replication/DNA-damage-dependent centrosome inactivation in Drosophila embryos. Nat. Cell Biol. 2, 90-95.
54. Spradling, A. C. (1986). P-element-mediated transformation. In Drosophila: A Practical Approach (ed. D. B. Roberts), pp. 175-197. Oxford: IRL Press.
55. Stumpff, J., Duncan, T., Homola, E., Campbell, S. D. and Su, T. T. (2004). Drosophila. Weel kinase regulates Cdk1 and mitotic entry during embryogenesis. Curr. Biol. 14, 2143-2148.
56. So, T. T., Campbell, S. D. and O'Farrell, P. H. (1999). Drosophila grapes/CHK1 mutants are defective in cyclin proteolysis and coordination of mitotic events. Curr. Biol. 9, 919-922.
57. Sullivan, K. M., Scott, K., Zuker, C. S. and Rubin, G. M. (2000). The ryanodine receptor is essential for larval development in Drosophila melanogaster. Proc. Natl. Acad Sci. USA 97, 5942-5947.
58. Takada, S., Kelkar, A. and Theurkauf, W. E. (2003). Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity. Cell 113, 87-99.
59. Takada, S., Kwak, S., Koppetsch, B. S. and Theurkauf, W. E. (2007). grp (chk1) replication-checkpoint mutations and DNA damage trigger a Chk2-dependent block at the Drosophila midblastula transition. Development 134, 1737-1744.
60. Tang, T. T., Bickel, S. E., Young, L. M. and Orr-Weaver, T. L. (1998). Maintenance of sister-chromatid cohesion at the centromere by the Drosophila MEI-S332 protein. Genes Dev. 12, 3843-3856.
61. Trimborn, M., Bell, S. M., Felix, C., Rashid, Y., Jafri, H., Griffiths, P. D., Neumann, L. M., Krebs, A., Reis, A., Sperling, K. et al. (2004). Mutations in microcephalin cause aberrant regulation of chromosome condensation. Am. J. Hum Genet. 75, 261-266.
62. Trimborn, M., Schindler, D., Neltzel, H. and Hirano, T. (2006). Misregulated chromosome condensation in MCPH1 primary microcephaly is mediated by condensin II. Cell Cycle 5, 322-326.
63. Wakefield, J. G., Bonaccorsi, S. and Gatti, M. (2001). The drosophila protein asp is involved in microtubule organization during spindle formation and cytokinesis. J. Cell Biol. 153, 637-648.
64. Woods, C. G., Bond, J. and Enard, W. (2005). Autosomal recessive primary microcephaly (MCPH): a review of clinical, molecular, and evolutionary findings. Am. J. Hum. Genet. 76, 717-728.
65. Xu, J., Xin, S. and Do, W. (2001). Drosophila Chk2 is required for DNA damage-mediated cell cycle arrest and apoptosis. FEBS Lett. 508, 394-398.
66. Xu, X., Lee, J. and Stern, D. F. (2004). Microcephalin is a DNA damage response protein involved in regulation of CHK1 and BRCA1. J. Biol. Chem 279, 34091-34094.
67. Yu, K. R., Saint, R. B. and Sullivan, W. (2000). The Grapes checkpoint coordinates nuclear envelope breakdown and chromosome condensation. Nat. Cell Biol. 2, 609-615.
68. Zhong, X., Pfeifer, G. P. and Xu, X. (2006). Microcephalin encodes a centrosomal protein. Cell Cycle 5, 457-458.