Table of Contents Author Guidelines Submit a Manuscript
Journal of Nucleic Acids
Volume 2010, Article ID 356917, 6 pages
http://dx.doi.org/10.4061/2010/356917
Research Article

Mouse WRN Helicase Domain Is Not Required for Spontaneous Homologous Recombination-Mediated DNA Deletion

1Greehey Children's Cancer Research Institute, The University of Texas Health Science Center at San Antonio, San Antonio, TX 78229, USA
2Department of Cellular and Structural Biology, The University of Texas Health Science Center at San Antonio, San Antonio, TX 78229, USA

Received 16 May 2010; Accepted 7 July 2010

Academic Editor: Ashis Basu

Copyright © 2010 Adam D. Brown 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. B. A. Kudlow, B. K. Kennedy, and R. J. Monnat Jr., “Werner and Hutchinson-Gilford progeria syndromes: mechanistic basis of human progeroid diseases,” Nature Reviews Molecular Cell Biology, vol. 8, no. 5, pp. 394–404, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Muftuoglu, J. Oshima, C. von Kobbe, W.-H. Cheng, D. F. Leistritz, and V. A. Bohr, “The clinical characteristics of Werner syndrome: molecular and biochemical diagnosis,” Human Genetics, vol. 124, no. 4, pp. 369–377, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. F. Takeuchi, F. Hanaoka, M. Goto, M. Yamada, and T. Miyamoto, “Prolongation of S phase and whole cell cycle in Werner's syndrome fibroblasts,” Experimental Gerontology, vol. 17, no. 6, pp. 473–480, 1982. View at Google Scholar · View at Scopus
  4. R. G. A. Faragher, I. R. Kill, J. A. A. Hunter, F. M. Pope, C. Tannock, and S. Shall, “The gene responsible for Werner syndrome may be a cell division “counting” gene,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 24, pp. 12030–12034, 1993. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Lebel and P. Leder, “A deletion within the murine Werner syndrome helicase induces sensitivity to inhibitors of topoisomerase and loss of cellular proliferative capacity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 22, pp. 13097–13102, 1998. View at Publisher · View at Google Scholar · View at Scopus
  6. A. J. R. Bishop, M. C. Hollander, B. Kosaras, R. L. Sidman, A. J. Fornace Jr., and R. H. Schiestl, “Atm-, p53-, and Gadd45a-deficient mice show an increased frequency of homologous recombination at different stages during development,” Cancer Research, vol. 63, no. 17, pp. 5335–5343, 2003. View at Google Scholar · View at Scopus
  7. A. J. R. Bishop, B. Kosaras, N. Carls, R. L. Sidman, and R. H. Schiestl, “Susceptibility of proliferating cells to benzo[a]pyrene-induced homologous recombination in mice,” Carcinogenesis, vol. 22, no. 4, pp. 641–649, 2001. View at Google Scholar · View at Scopus
  8. A. J. R. Bishop, B. Kosaras, R. L. Sidman, and R. H. Schiestl, “Benzo(a)pyrene and X-rays induce reversions of the pink-eyed unstable mutation in the retinal pigment epithelium of mice,” Mutation Research, vol. 457, no. 1-2, pp. 31–40, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. C.-E. Yu, J. Oshima, Y.-H. Fu et al., “Positional cloning of the Werner's syndrome gene,” Science, vol. 272, no. 5259, pp. 258–262, 1996. View at Google Scholar · View at Scopus
  10. C.-E. Yu, J. Oshima, E. M. Wijsman et al., “Mutations in the consensus helicase domains of the Werner syndrome gene. Werner's Syndrome Collaborative Group,” American Journal of Human Genetics, vol. 60, no. 2, pp. 330–341, 1997. View at Google Scholar
  11. Y. Gondo, J. M. Gardner, Y. Nakatsu et al., “High-frequency genetic reversion mediated by a DNA duplication: the mouse pink-eyed unstable mutation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 1, pp. 297–301, 1993. View at Publisher · View at Google Scholar · View at Scopus
  12. R. H. Schiestl, F. Khogali, and N. Carls, “Reversion of the mouse pink-eyed unstable mutation induced by low doses of X-rays,” Science, vol. 266, no. 5190, pp. 1573–1576, 1994. View at Google Scholar · View at Scopus
  13. A. Galli and R. H. Schiestl, “On the mechanism of UV and γ-ray induced intrachromosomal recomhination in yeast cells synchronized in different stages of the cell cycle,” Molecular and General Genetics, vol. 248, no. 3, pp. 301–310, 1995. View at Publisher · View at Google Scholar · View at Scopus
  14. F. Pâques and J. E. Haber, “Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae,” Microbiology and Molecular Biology Reviews, vol. 63, no. 2, pp. 349–404, 1999. View at Google Scholar · View at Scopus
  15. C. Arnaudeau, C. Lundin, and T. Helleday, “DNA double-strand breaks associated with replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells,” Journal of Molecular Biology, vol. 307, no. 5, pp. 1235–1245, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. A. B. Claybon, B. Karia, C. Bruce, and A. J. R. Bishop, “PARP1 suppresses homologous recombination events in mice in vivo,” Nucleic Acids Research, pp. 1–8, 2010. View at Publisher · View at Google Scholar
  17. M. Lebel, “Increased frequency of DNA deletions in pink-eyed unstable mice carrying a mutation in the Werner syndrome gene homologue,” Carcinogenesis, vol. 23, no. 1, pp. 213–216, 2002. View at Google Scholar · View at Scopus
  18. A. J. R. Bishop, B. Kosaras, M. C. Hollander, A. Fornace Jr., R. L. Sidman, and R. H. Schiestl, “p21 controls patterning but not homologous recombination in RPE development,” DNA Repair, vol. 5, no. 1, pp. 111–120, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Bodenstein and R. L. Sidman, “Growth and development of the mouse retinal pigment epithelium. I. Cell and tissue morphometrics and topography of mitotic activity,” Developmental Biology, vol. 121, no. 1, pp. 192–204, 1987. View at Google Scholar · View at Scopus
  20. A. V. Ershov and O. G. Stroeva, “Post-natal pattern of cell proliferation in retinal pigment epithelium of mice studied with tritiated thymidine autoradiography,” Cell Differentiation and Development, vol. 28, no. 3, pp. 173–177, 1989. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Nakayama, M.-T. T. Nguyen, C. C. Chen, K. Opdecamp, C. A. Hodgkinson, and H. Arnheiter, “Mutations in microphthalmia, the mouse homolog of the human deafness gene MITF, affect neuroepithelial and neural crest-derived melanocytes differently,” Mechanisms of Development, vol. 70, no. 1-2, pp. 155–166, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. M. L. Yamamoto, R. Reliene, J. Oshima, and R. H. Schiestl, “Effects of human Werner helicase on intrachromosomal homologous recombination mediated DNA deletions in mice,” Mutation Research, vol. 644, no. 1-2, pp. 11–16, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. D. Salk, K. Au, H. Hoehn, and G. M. Martin, “Cytogenetics of Werner's syndrome cultured skin fibroblasts: variegated translocation mosaicism,” Cytogenetics and Cell Genetics, vol. 30, no. 2, pp. 92–107, 1981. View at Google Scholar · View at Scopus
  24. R. Z. Cheng, S. Murano, B. Kurz, and R. J. Shmookler Reis, “Homologous recombination is elevated in some Werner-like syndromes but not during normal in vitro or in vivo senescence of mammalian cells,” Mutation Research, vol. 237, no. 5-6, pp. 259–269, 1990. View at Google Scholar · View at Scopus
  25. P. Pichierri, A. Franchitto, P. Mosesso, and F. Palitti, “Werner's syndrome protein is required for correct recovery after replication arrest and DNA damage induced in S-phase of cell cycle,” Molecular Biology of the Cell, vol. 12, no. 8, pp. 2412–2421, 2001. View at Google Scholar · View at Scopus
  26. R. Elli, L. Chessa, A. Antonelli, P. Petrinelli, R. Ambra, and L. Marcucci, “Effects of topoisomerase II inhibition in lymphoblasts from patients with progeroid and "chromosome instability" syndromes,” Cancer Genetics and Cytogenetics, vol. 87, no. 2, pp. 112–116, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Okada, M. Goto, Y. Furuichi, and M. Sugimoto, “Differential effects of cytotoxic drugs on mortal and immortalized B-lymphoblastoid cell lines from normal and Werner's syndrome patients,” Biological & Pharmaceutical Bulletin, vol. 21, pp. 235–239, 1998. View at Google Scholar
  28. M. Poot, K. A. Gollahon, and P. S. Rabinovitch, “Werner syndrome lymphoblastoid cells are sensitive to camptothecin-induced apoptosis in S-phase,” Human Genetics, vol. 104, no. 1, pp. 10–14, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. J.-C. Shen, M. D. Gray, J. Oshima, and L. A. Loeb, “Characterization of Werner syndrome protein DNA helicase activity: directionality, substrate dependence and stimulation by replication protein A,” Nucleic Acids Research, vol. 26, no. 12, pp. 2879–2885, 1998. View at Publisher · View at Google Scholar · View at Scopus
  30. R. M. Brosh Jr., D. K. Orren, J. O. Nehlin et al., “Functional and physical interaction between WRN helicase and human replication protein A,” Journal of Biological Chemistry, vol. 274, no. 26, pp. 18341–18350, 1999. View at Publisher · View at Google Scholar · View at Scopus
  31. K. M. Doherty, J. A. Sommers, M. D. Gray et al., “Physical and functional mapping of the replication protein A interaction domain of the Werner and Bloom syndrome helicases,” Journal of Biological Chemistry, vol. 280, no. 33, pp. 29494–29505, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. J.-C. Shen, Y. Lao, A. Kamath-Loeb, M. S. Wold, and L. A. Loeb, “The N-terminal domain of the large subunit of human replication protein A binds to Werner syndrome protein and stimulates helicase activity,” Mechanisms of Ageing and Development, vol. 124, no. 8-9, pp. 921–930, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Lebel, E. A. Spillare, C. C. Harris, and P. Leder, “The Werner syndrome gene product co-purifies with the DNA replication complex and interacts with PCNA and topoisomerase I,” Journal of Biological Chemistry, vol. 274, no. 53, pp. 37795–37799, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Huang, S. Beresten, B. Li, J. Oshima, N. A. Ellis, and J. Campisi, “Characterization of the human and mouse WRN 35 exonuclease,” Nucleic Acids Research, vol. 28, no. 12, pp. 2396–2405, 2000. View at Google Scholar · View at Scopus
  35. A. M. Rodríguez-López, D. A. Jackson, J. O. Nehlin, F. Iborra, A. V. Warren, and L. S. Cox, “Characterisation of the interaction between WRN, the helicase/exonuclease defective in progeroid Werner's syndrome, and an essential replication factor, PCNA,” Mechanisms of Ageing and Development, vol. 124, no. 2, pp. 167–174, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. A. S. Kamath-Loeb, E. Johansson, P. M. J. Burgers, and L. A. Loeb, “Functional interaction between the Werner syndrome protein and DNA polymerase δ,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 9, pp. 4603–4608, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. A. S. Kamath-Loeb, L. A. Loeb, E. Johansson, P. M. J. Burgers, and M. Fry, “Interactions between the Werner syndrome helicase and DNA polymerase δ specifically facilitate copying of tetraplex and hairpin structures of the d(CGG)n trinucleotide repeat sequence,” Journal of Biological Chemistry, vol. 276, no. 19, pp. 16439–16446, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Baynton, M. Otterlei, M. Bjørås, C. Von Kobbe, V. A. Bohr, and E. Seeberg, “WRN interacts physically and functionally with the recombination mediator protein RAD52,” Journal of Biological Chemistry, vol. 278, no. 38, pp. 36476–36486, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. M. I. Melaragno, D. Pagni, and M. D. A. C. Smith, “Cytogenetic aspects of Werner's syndrome lymphocyte cultures,” Mechanisms of Ageing and Development, vol. 78, no. 2, pp. 117–122, 1995. View at Publisher · View at Google Scholar · View at Scopus
  40. E. P. Mimitou and L. S. Symington, “Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing,” Nature, vol. 455, no. 7214, pp. 770–774, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. Z. Zhu, W.-H. Chung, E. Y. Shim, S. E. Lee, and G. Ira, “Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends,” Cell, vol. 134, no. 6, pp. 981–994, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Gravel, J. R. Chapman, C. Magill, and S. P. Jackson, “DNA helicases Sgs1 and BLM promote DNA double-strand break resection,” Genes and Development, vol. 22, no. 20, pp. 2767–2772, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Zecevic, H. Menard, V. Gurel, E. Hagan, R. DeCaro, and A. Zhitkovich, “WRN helicase promotes repair of DNA double-strand breaks caused by aberrant mismatch repair of chromium-DNA adducts,” Cell Cycle, vol. 8, no. 17, pp. 2769–2778, 2009. View at Google Scholar · View at Scopus