Common variants of drosophila melanogaster Cyp6d2 cause camptothecin sensitivity and synergize with loss of Brca2

G3: Genes, Genomes, Genetics

Volumn 3, Issue 1, 2013, Pages 91-99

  Thomas, Adam M ^a   Hui, Carrie ^a   South, Adam ^a   McVey, Mitch ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

Breaks; Chemotherapeutics; Cytochrome p450; Double strand; Homologous; Recombination

Indexed keywords

BRCA2 PROTEIN; CAMPTOTHECIN; CYTOCHROME; CYTOCHROME P450 6D2; DOUBLE STRANDED DNA; IRINOTECAN; OXIDOREDUCTASE; TOPOTECAN; UNCLASSIFIED DRUG; CYTOCHROME P 450 CYP6D2; CYTOCHROME P-450 CYP6D2; CYTOCHROME P450; DNA TOPOISOMERASE INHIBITOR; DROSOPHILA PROTEIN; DRUG DERIVATIVE; INSECT PROTEIN; PRIMER DNA;

ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME 2; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DROSOPHILA MELANOGASTER; DRUG SENSITIVITY; FEMALE; GENE LOSS; GENE MUTATION; IONIZING RADIATION; LETHAL DOSE; MALE; NONHUMAN; POINT MUTATION; RADIOSENSITIVITY; TRANSPOSON; ANIMAL; CHEMOTHERAPY; DOUBLE-STRAND BREAKS; DRUG EFFECT; DRUG SCREENING; GENETIC COMPLEMENTATION; GENETIC POLYMORPHISM; GENETICS; HOMOLOGOUS RECOMBINATION; METABOLISM; METHODOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

DROSOPHILA MELANOGASTER;

CHEMOTHERAPEUTICS; CYTOCHROME P450; DOUBLE-STRAND BREAKS; HOMOLOGOUS RECOMBINATION;

ANIMALS; BRCA2 PROTEIN; CAMPTOTHECIN; CYTOCHROME P-450 ENZYME SYSTEM; DNA DAMAGE; DNA PRIMERS; DNA REPAIR; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; DRUG EVALUATION, PRECLINICAL; GENETIC COMPLEMENTATION TEST; INSECT PROTEINS; POLYMORPHISM, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TOPOISOMERASE I INHIBITORS; TOPOTECAN;

MLCS; MLOWN;

EID: 84883179594     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.112.003996     Document Type: Article

References (57)

1. Adams, M. D., S. E. Celniker, R. A. Holt, C. A. Evans, J. D. Gocayne et al., 2000 The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.
2. Amichot, M., S. Tarès, A. Brun-Barale, L. Arthaud, J.-M. Bride et al., 2004 Point mutations associated with insecticide resistance in the Drosophila cytochrome P450 Cyp6a2 enable DDT metabolism. Eur. J. Biochem. 271: 1250-1257.
3. Bergé, J. B., R. Feyereisen, and M. Amichot, 1998 Cytochrome P450 monooxygenases and insecticide resistance in insects. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353: 1701-1705.
4. Bischof, J., R. K. Maeda, M. Hediger, F. Karch, and K. Basler, 2007 An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104: 3312-3317.
5. Boulton, S. J., 2006 Cellular functions of the BRCA tumour-suppressor proteins. Biochem. Soc. Trans. 34: 633-645.
6. Boyd, J. B., and R. B. Setlow, 1976 Characterization of postreplication repair in mutagen-sensitive strains of Drosophila melanogaster. Genetics 84: 507-526.
7. Brough, R., D. Wei, S. Leulier, C. J. Lord, Y. S. Rong et al., 2008 Functional analysis of Drosophila melanogaster BRCA2 in DNA repair. DNA Repair (Amst.) 7: 10-19.
8. Buchon, N., N. A. Broderick, M. Poidevin, S. Pradervand, and B. Lemaitre, 2009 Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 5: 200-211.
9. Chan, S. H., A. M. Yu, and M. McVey, 2010 Dual roles for DNA polymerase theta in alternative end-joining repair of double-strand breaks in drosophila ed. R.S. Hawley. PLoS Genet. 6: e1001005.
10. Chintapalli, V. R., J. Wang, and J. A. T. Dow, 2007 Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 39: 715-720.
11. Coon, M. J., X. X. Ding, S. J. Pernecky, and A. D. Vaz, 1992 Cytochrome P450: progress and predictions. FASEB J. 6: 669-673.
12. Coon, M. J., A. D. Vaz, and L. L. Bestervelt, 1996 Cytochrome P450 2: peroxidative reactions of diversozymes. FASEB J. 10: 428-434.
13. Davies, A. A., J. Y. Masson, M. J. McIlwraith, A. Z. Stasiak, A. Stasiak et al., 2001 Role of BRCA2 in control of the RAD51 recombination and DNA repair protein. Mol. Cell 7: 273-282.
14. Edwards, A., M. Gladstone, P. Yoon, D. Raben, B. Frederick et al., 2011 Combinatorial effect of maytansinol and radiation in Drosophila and human cancer cells. Dis Model Mech 4: 496-503.
15. Ferguson, L. R., and A. E. Pearson, 1996 The clinical use of mutagenic anticancer drugs. Mutat. Res. 355: 1-12.
16. Gateff, E., 1978 Malignant neoplasms of genetic origin in Drosophila melanogaster. Science 200: 1448-1459.
17. Gateff, E., and H. A. Schneiderman, 1974 Developmental capacities of benign and malignant neoplasms of Drosophila. Dev. Genes Evol. 176: 23-65.
18. Giraudo, M., G. C. Unnithan, G. Le Goff, and R. Feyereisen, 2010 Regulation of cytochrome P450 expression in Drosophila: Genomic insights. Pestic. Biochem. Physiol. 97: 115-122.
19. Gladstone, M., and T. T. Su, 2011 Chemical genetics and drug screening in Drosophila cancer models. J. Genet. Genomics 38: 497-504.
20. Gruenewald, C., J. A. Botella, F. Bayersdorfer, J. A. Navarro, and S. Schneuwly, 2009 Hyperoxia-induced neurodegeneration as a tool to identify neuroprotective genes in Drosophila melanogaster. Free Radic. Biol. Med. 46: 1668-1676.
21. Guengerich, F. P., 1999 Cytochrome P-450 3A4: regulation and role in drug metabolism. Annu. Rev. Pharmacol. Toxicol. 39: 1-17.
22. Hollenberg, P. F., 1992 Mechanisms of cytochrome P450 and peroxidasecatalyzed xenobiotic metabolism. FASEB J. 6: 686-694.
23. Holm, C., J. M. Covey, D. Kerrigan, and Y. Pommier, 1989 Differential requirement of DNA replication for the cytotoxicity of DNA topoisomerase I and II inhibitors in Chinese hamster DC3F cells. Cancer Res. 49: 6365-6368.
24. Hsiang, Y. H., and L. F. Liu, 1988 Identification of mammalian DNA topoisomerase I as an intracellular target of the anticancer drug camptothecin. Cancer Res. 48: 1722-1726.
25. Hsiang, Y. H., R. Hertzberg, S. Hecht, and L. F. Liu, 1985 Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J. Biol. Chem. 260: 14873-14878.
26. Hsiang, Y. H., M. G. Lihou, and L. F. Liu, 1989 Arrest of replication forks by drug-stabilized topoisomerase I-DNA cleavable complexes as a mechanism of cell killing by camptothecin. Cancer Res. 49: 5077-5082.
27. Jaklevic, B., L. Uyetake, W. Lemstra, J. Chang, W. Leary et al., 2006 Contribution of growth and cell cycle checkpoints to radiation survival in Drosophila. Genetics 174: 1963-1972.
28. Kane, D. P., M. Shusterman, Y. Rong, and M. McVey, 2012 Competition between replicative and translesion polymerases during homologous recombination repair in Drosophila ed. R.S. Hawley. PLoS Genet. 8: e1002659.
29. Klovstad, M., U. Abdu, and T. Schüpbach, 2008 Drosophila brca2 is required for mitotic and meiotic DNA repair and efficient activation of the meiotic recombination checkpoint. PLoS Genet. 4: e31.
30. Koster, D. A., K. Palle, E. S. M. Bot, M.-A. Bjornsti, and N. H. Dekker, 2007 Antitumour drugs impede DNA uncoiling by topoisomerase I. Nature 448: 213-217.
31. Kunimoto, T., K. Nitta, T. Tanaka, N. Uehara, H. Baba et al., 1987 Antitumor activity of 7-ethyl-10-[4-(1-piperidino)-1-piperidino] carbonyloxy-camptothec in, a novel water-soluble derivative of camptothecin, against murine tumors. Cancer Res. 47: 5944-5947.
32. Lawley, P. D., and D. H. Phillips, 1996 DNA adducts from chemotherapeutic agents. Mutat. Res. 355: 13-40.
33. Legarza, K., and L.-X. Yang, 2006 New molecular mechanisms of action of camptothecin-type drugs. Anticancer Res. 26: 3301-3305.
34. Maekawa, K., N. Harakawa, T. Yoshimura, S.-R. Kim, Y. Fujimura et al., 2010 CYP3A4*16 and CYP3A4*18 alleles found in East Asians exhibit differential catalytic activities for seven CYP3A4 substrate drugs. Drug Metab. Dispos. 38: 2100-2104.
35. Mattern, M. R., G. A. Hofmann, F. L. McCabe, and R. K. Johnson, 1991 Synergistic cell killing by ionizing radiation and topoisomerase I inhibitor topotecan (SK&F 104864). Cancer Res. 51: 5813-5816.
36. Plant, N., 2007 The human cytochrome P450 sub-family: transcriptional regulation, inter-individual variation and interaction networks. Biochim. Biophys. Acta 1770: 478-488.
37. Pommier, Y., 2006 Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer 6: 789-802.
38. Pommier, Y., 2009 DNA Topoisomerase I Inhibitors. Chemistry, Biology, and Interfacial Inhibition. 109: 2894-2902.
39. Radcliffe, C. M., E. A. Silva, and S. D. Campbell, 2002 A method for assaying the sensitivity of Drosophilareplication checkpoint mutants to anti-cancer and DNA-damaging drugs. Genome 45: 881-889.
40. Ray Chaudhuri, A., Y. Hashimoto, R. Herrador, K. J. Neelsen, D. Fachinetti et al., 2012 Topoisomerase I poisoning results in PARP-mediated replication fork reversal. Nat. Struct. Mol. Biol. 19: 417-423.
41. Roseman, R. R., E. A. Johnson, C. K. Rodesch, M. Bjerke, R. N. Nagoshi et al., 1995 A P element containing suppressor of hairy-wing binding regions has novel properties for mutagenesis in Drosophila melanogaster. Genetics 141: 1061-1074.
42. Rubin, G. M., 2000 Comparative Genomics of the Eukaryotes. Science 287: 2204-2215.
43. Rudrapatna, V. A., R. L. Cagan, and T. K. Das, 2012 Drosophila cancer models. Dev. Dyn. 241: 107-118.
44. Ryder, E., F. Blows, M. Ashburner, R. Bautista-Llacer, D. Coulson et al., 2004 The DrosDel collection: a set of P-element insertions for generating custom chromosomal aberrations in Drosophila melanogaster. Genetics 167: 797-813.
45. Smith, D. A., M. J. Ackland, and B. C. Jones, 1997 Properties of cytochrome P450 isoenzymes and their substrates part 2: properties of cytochrome P450 substrates. Drug Discov. Today 2: 479-486.
46. Strumberg, D., A. A. Pilon, M. Smith, R. Hickey, L. Malkas et al., 2000 Conversion of topoisomerase I cleavage complexes on the leading strand of ribosomal DNA into 59-phosphorylated DNA double-strand breaks by replication runoff. Mol. Cell. Biol. 20: 3977-3987.
47. Su, T. T., 2011 Safeguarding genetic information in Drosophila. Chromosoma 120: 547-555.
48. Sung, P., 1994 Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265: 1241-1243.
49. Thorslund, T., and S. C. West, 2007 BRCA2: a universal recombinase regulator. Oncogene 26: 7720-7730.
50. Tijet, N., C. Helvig, and R. Feyereisen, 2001 The cytochrome P450 gene superfamily in Drosophila melanogaster: annotation, intron-exon organization and phylogeny. Gene 262: 189-198.
51. Tsao, Y. P., A. Russo, G. Nyamuswa, R. Silber, and L. F. Liu, 1993 Interaction between replication forks and topoisomerase I-DNA cleavable complexes: studies in a cell-free SV40 DNA replication system. Cancer Res. 53: 5908-5914.
52. Tu, C. P. D., and B. Akgül, 2005 Drosophila glutathione S-transferases. Methods Enzymol. 401: 204-226.
53. van Bergeijk, P., J. Heimiller, L. Uyetake, and T. T. Su, 2012 Genome-wide expression analysis identifies a modulator of ionizing radiation-induced p53-independent apoptosis in Drosophila melanogaster. PLoS ONE 7: e36539.
54. Wall, M. E., and M. C. Wani, 1995 Camptothecin and taxol: discovery to clinic-thirteenth Bruce F. Cain Memorial Award Lecture. Cancer Res. 55: 753-760.
55. Wooster, R., G. Bignell, J. Lancaster, S. Swift, S. Seal et al., 1995 Identification of the breast cancer susceptibility gene BRCA2. Nature 378: 789-792.
56. Yang, J, C. McCart, D. J. Woods, S. Terhzaz, K. G. Greenwood, R. H. ffrench-Constant, and J. A. T. Dow, 2007 A Drosophila systems approach to xenobiotic metabolism. Physiol. Genomics 30: 223-231.
57. Zijlstra, J. A., and E. W. Vogel, 1988 Metabolic inactivation of mutagens in Drosophila melanogaster. Mutat. Res. 198: 73-83