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Journal of Nucleic Acids
Volume 2010, Article ID 456487, 9 pages
http://dx.doi.org/10.4061/2010/456487
Research Article

Aflatoxin B1-Associated DNA Adducts Stall S Phase and Stimulate Rad51 foci in Saccharomyces cerevisiae

1Ordway Research Institute, Center for Medical Sciences, 150 New Scotland Avenue, Albany, NY 12209, USA
2Department of Biomedical Sciences, State University of New York at Albany, 150 New Scotland Avenue, Albany, NY 12209, USA
3Albany Medical College, 47 New Scotland Avenue, Albany, NY 12208, USA
4Bloomberg School of Public Health, Johns Hopkins University, 615 North Wolfe Street, Baltimore, MD 21205, USA

Received 15 August 2010; Accepted 9 September 2010

Academic Editor: Ashis Basu

Copyright © 2010 Michael Fasullo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. A. Hussain, D. R. Ferry, G. El-Gazzaz et al., “Hepatocellular carcinoma,” Annals of Oncology, vol. 12, no. 2, pp. 161–172, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Jemal, R. Siegael, J. Xu, and E. Ward, “Cancer statistics,” CA A Cancer Journal for Clinicians, vol. 60, no. 5, pp. 277–300, 2010. View at Google Scholar
  3. K. A. McGlynn and W. T. London, “Epidemiology and natural history of hepatocellular carcinoma,” Best Practice and Research, vol. 19, no. 1, pp. 3–23, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. M. C. Kew, “Synergistic interaction between aflatoxin B1 and hepatitis B virus in hepatocarcinogenesis,” Liver International, vol. 23, no. 6, pp. 405–409, 2003. View at Google Scholar · View at Scopus
  5. D. Moradpour and H. E. Blum, “Pathogenesis of hepatocellular carcinoma,” European Journal of Gastroenterology and Hepatology, vol. 17, no. 5, pp. 477–483, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. P. Pineau, S. Volinia, K. McJunkin et al., “miR-221 overexpression contributes to liver tumorigenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 1, pp. 264–269, 2010. View at Google Scholar
  7. F. Fornari, L. Gramantieri, M. Ferracin et al., “MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma,” Oncogene, vol. 27, no. 43, pp. 5651–5661, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. I. C. Hsu, R. A. Metcalf, T. Sun, J. A. Welsh, N. J. Wang, and C. C. Harris, “Mutational hotspot in the p53 gene in human hepatocellular carcinomas,” Nature, vol. 350, no. 6317, pp. 427–428, 1991. View at Publisher · View at Google Scholar · View at Scopus
  9. H.-M. Shen and C.-N. Ong, “Mutations of the p53 tumor suppressor gene and ras oncogenes in aflatoxin hepatocarcinogenesis,” Mutation Research, vol. 366, no. 1, pp. 23–44, 1996. View at Publisher · View at Google Scholar · View at Scopus
  10. G. N. Wogan, “Aflatoxin as a human carcinogen,” Hepatology, vol. 30, no. 2, pp. 573–575, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. V. Paget, F. Sichel, D. Garon, and M. Lechevrel, “Aflatoxin B1-induced TP53 mutational pattern in normal human cells using the FASAY (Functional Analysis of Separated Alleles in Yeast),” Mutation Research, vol. 656, no. 1-2, pp. 55–61, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. D. B. Zimonjic, M. E. Durkin, C. L. Keck-Waggoner, S.-W. Park, S. S. Thorgeirsson, and N. C. Popescu, “SMAD5 gene expression, rearrangements, copy number, and amplification at fragile site FRA5C in human hepatocellular carcinoma,” Neoplasia, vol. 5, no. 5, pp. 390–396, 2003. View at Google Scholar · View at Scopus
  13. E. Pang, N. Wong, P. B.-S. Lai, K.-F. To, W.-Y. Lau, and P. J. Johnson, “Consistent chromosome 10 rearrangements in four newly established human hepatocellular carcinoma cell lines,” Genes Chromosomes and Cancer, vol. 33, no. 2, pp. 150–159, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. P. Pineau, A. Marchio, C. Battiston et al., “Chromosome instability in human hepatocellular carcinoma depends on p53 status and aflatoxin exposure,” Mutation Research, vol. 653, no. 1-2, pp. 6–13, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. D. L. Eaton and E. P. Gallagher, “Mechanisms of aflatoxin carcinogenesis,” Annual Review of Pharmacology and Toxicology, vol. 34, pp. 135–172, 1994. View at Google Scholar · View at Scopus
  16. C. N. Martin and R. C. Garner, “Aflatoxin B oxide generated by chemical or enzymic oxidation of aflatoxin B1 causes guanine substitution in nucleic acids,” Nature, vol. 267, no. 5614, pp. 863–865, 1977. View at Google Scholar · View at Scopus
  17. M. E. Smela, M. L. Hamm, P. T. Henderson, C. M. Harris, T. M. Harris, and J. M. Essigmann, “The aflatoxin B1 formamidopyrimidine adduct plays a major role in causing the types of mutations observed in human hepatocellular carcinoma,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 10, pp. 6655–6660, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. O. Alekseyev, M. L. Hamm, and J. M. Essigmann, “Aflatoxin B1 formamidopyrimidine adducts are preferentially repaired by the nucleotide excision repair pathway in vivo,” Carcinogenesis, vol. 25, no. 6, pp. 1045–1051, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. L. L. Bedard and T. E. Massey, “Aflatoxin B1-induced DNA damage and its repair,” Cancer Letters, vol. 241, no. 2, pp. 174–183, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. K. L. Brown, M. W. Voehler, S. M. Magee, C. M. Harris, T. M. Harris, and M. P. Stone, “Structural perturbations induced by the α-anomer of the aflatoxin B1 formamidopyrimidine adduct in duplex and single-strand DNA,” Journal of the American Chemical Society, vol. 131, no. 44, pp. 16096–16107, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Manuguerra, F. Saletta, M. R. Karagas et al., “XRCC3 and XPD/ERCC2 single nucleotide polymorphisms and the risk of cancer: a HuGE review,” American Journal of Epidemiology, vol. 164, no. 4, pp. 297–302, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. X. D. Long, Y. Ma, D. Y. Qu et al., “The polymorphism of XRCC3 codon 241 and AFB1-related hepatocellular carcinoma in Guangxi population, China,” Annals of Epidemiology, vol. 18, no. 7, pp. 572–578, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. X. D. Long, Y. Ma, Y. F. Zhou et al., “XPD codon 312 and 751 polymorphisms, and AFB1 exposure, and hepatocellular carcinoma risk,” BMC Cancer, vol. 17, no. 9, article no. 400, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. R. D. Johnson and M. Jasin, “Double-strand-break-induced homologous recombination in mammalian cells,” Biochemical Society Transactions, vol. 29, no. 2, pp. 196–201, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. F. D. Araujo, A. J. Pierce, J. M. Stark, and M. Jasin, “Variant XRCC3 implicated in cancer is functional in homology-directed repair of double-strand breaks,” Oncogene, vol. 21, no. 26, pp. 4176–4180, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Sengstag, B. Weibel, and M. Fasullo, “Genotoxicity of aflatoxin B1: evidence for a recombination-mediated mechanism in Saccharomyces cerevisiae,” Cancer Research, vol. 56, no. 23, pp. 5457–5465, 1996. View at Google Scholar · View at Scopus
  27. M. U. Keller-Seitz, U. Certa, C. Sengstag, F. E. Würgler, M. Sun, and M. Fasullo, “Transcriptional response of yeast to aflatoxin B1: recombinational repair involving RAD51 and RAD1,” Molecular Biology of the Cell, vol. 15, no. 9, pp. 4321–4336, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Guo, L. L. Breeden, H. Zarbl, B. D. Preston, and D. L. Eaton, “Expression of a human cytochrome P450 in yeast permits analysis of pathways for response to and repair of aflatoxin-induced DNA damage,” Molecular and Cellular Biology, vol. 25, no. 14, pp. 5823–5833, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Fasullo, M. Sun, and P. Egner, “Stimulation of sister chromatid exchanges and mutation by aflatoxin B1-DNA adducts in Saccharomyces cerevisiae requires MEC1 (ATR), RAD53, and DUN1,” Molecular Carcinogenesis, vol. 47, no. 8, pp. 608–615, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Guo, L. L. Breeden, W. Fan, L. P. Zhao, D. L. Eaton, and H. Zarbl, “Analysis of cellular responses to aflatoxin B1 in yeast expressing human cytochrome P450 1A2 using cDNA microarrays,” Mutation Research, vol. 593, no. 1-2, pp. 121–142, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. D. Burke, D. Dawson, and T. Stearns, A Cold Spring Harbor Laboratory Course Manual, Methods in Yeast Genetics, Cold Spring Harbor Press, New York, NY, USA, 2000.
  32. M. T. Fasullo and R. W. Davis, “Recombinational substrates designed to study recombination between unique and repetitive sequences in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 17, pp. 6215–6219, 1987. View at Google Scholar · View at Scopus
  33. C. W. Fung, A. M. Mozlin, and L. S. Symington, “Suppression of the double-strand-break-repair defect of the Saccharomyces cerevisiae rad57 mutant,” Genetics, vol. 181, no. 4, pp. 1195–1206, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. Z. Dong and M. Fasullo, “Multiple recombination pathways for sister chromatid exchange in Saccharomyces cerevisiae: role of RAD1 and the RAD52 epistasis group genes,” Nucleic Acids Research, vol. 31, no. 10, pp. 2576–2585, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Lisby, U. H. Mortensen, and R. Rothstein, “Colocalization of multiple DNA double-strand breaks at a single Rad52 repair center,” Nature Cell Biology, vol. 5, no. 6, pp. 572–577, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. P. A. Egner, J. D. Groopman, J.-S. Wang, T. W. Kensler, and M. D. Friesen, “Quantification of aflatoxin-B1-N7-guanine in human urine by high-performance liquid chromatography and isotope dilution tandem mass spectrometry,” Chemical Research in Toxicology, vol. 19, no. 9, pp. 1191–1195, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. C. S. Hoffman and F. Winston, “A ten-minute DNA preparation from yeast efficiently releases automomous plasmids for transformation of Escherichia coli,” Gene, vol. 57, no. 2-3, pp. 267–272, 1987. View at Google Scholar · View at Scopus
  38. M. Foiani, F. Marini, D. Gamba, G. Lucchini, and P. Plevani, “The B subunit of the DNA polymerase α-primase complex in Saccharomyces cerevisiae executes an essential function at the initial stage of DNA replication,” Molecular and Cellular Biology, vol. 14, no. 2, pp. 923–933, 1994. View at Google Scholar · View at Scopus
  39. K. Herzberg, V. I. Bashkirov, M. Rolfsmeier et al., “Phosphorylation of Rad55 on serines 2, 8, and 14 is required for efficient homologous recombination in the recovery of stalled replication forks,” Molecular and Cellular Biology, vol. 26, no. 22, pp. 8396–8409, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Lisby, J. H. Barlow, R. C. Burgess, and R. Rothstein, “Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins,” Cell, vol. 118, no. 6, pp. 699–713, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Fasullo, Z. Dong, M. Sun, and L. Zeng, “Saccharomyces cerevisiae RAD53 (CHK2) but not CHK1 is required for double-strand break-initiated SCE and DNA damage-associated SCE after exposure to X rays and chemical agents,” DNA Repair, vol. 4, no. 11, pp. 1240–1251, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Toussaint and A. Conconi, “High-throughput and sensitive assay to measure yeast cell growth: a bench protocol for testing genotoxic agents,” Nature Protocols, vol. 1, no. 4, pp. 1922–1928, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Neecke, G. Lucchini, and M. P. Longhese, “Cell cycle progression in the presence of irreparable DNA damage is controlled by a Mec1- and Rad53-dependent checkpoint in budding yeast,” EMBO Journal, vol. 18, no. 16, pp. 4485–4497, 1999. View at Publisher · View at Google Scholar
  44. S. Sabbioneda, I. Bortolomai, M. Giannattasio, P. Plevani, and M. Muzi-Falconi, “Yeast Rev1 is cell cycle regulated, phosphorylated in response to DNA damage and its binding to chromosomes is dependent upon MEC1,” DNA Repair, vol. 6, no. 1, pp. 121–127, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. V. Pagès, S. R. Santa Maria, L. Prakash, and S. Prakash, “Role of DNA damage-induced replication checkpoint in promoting lesion bypass by translesion synthesis in yeast,” Genes and Development, vol. 23, no. 12, pp. 1438–1449, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. F. Conde, D. Ontoso, I. Acosta, A. Gallego-Sánchez,, A. Bueno, and P. A. San-Segundo, “Regulation of tolerance to DNA alkylating damage by Dot1 and Rad53 in Saccharomyces cerevisiae,” DNA Repair, vol. 9, no. 10, pp. 1038–1049, 2010. View at Google Scholar
  47. C. B. Bennett, A. L. Lewis, K. K. Baldwin, and M. A. Resnick, “Lethality induced by a single site-specific double-strand break in a dispensable yeast plasmid,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 12, pp. 5613–5617, 1993. View at Google Scholar · View at Scopus
  48. V. Gangavarapu, S. Prakash, and L. Prakash, “Requirement of RAD52 group genes for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae,” Molecular and Cellular Biology, vol. 27, no. 21, pp. 7758–7764, 2007. View at Publisher · View at Google Scholar · View at Scopus