Irreparable complex DNA double-strand breaks induce chromosome breakage in organotypic three-dimensional human lung epithelial cell culture

Nucleic Acids Research

Volumn 39, Issue 13, 2011, Pages 5474-5488

  Asaithamby, Aroumougame ^a   Hu, Burong ^b   Delgado, Oliver ^c   Ding, Liang Hao ^a   Story, Michael D ^a   Minna, John D ^d   Shay, Jerry W ^c   Chen, David J ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b INSTITUTE OF MODERN PHYSICS   (China)

^c Department of Cell Biology ^*  (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IRON;

ARTICLE; BRONCHUS MUCOSA; CELL CYCLE; CELL DIFFERENTIATION; CHROMOSOME ABERRATION; CHROMOSOME BREAKAGE; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; EPITHELIUM CELL; GAMMA RADIATION; HUMAN; HUMAN CELL; LINEAR ENERGY TRANSFER; MITOSIS; PRIORITY JOURNAL;

CELL DIFFERENTIATION; CELL LINE; CHROMOSOME ABERRATIONS; CHROMOSOME BREAKAGE; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DOWN-REGULATION; EPITHELIAL CELLS; HUMANS; IMAGING, THREE-DIMENSIONAL; IRON; KINETICS; LINEAR ENERGY TRANSFER; LUNG; ORGAN CULTURE TECHNIQUES;

EID: 80052254583     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr149     Document Type: Article

References (52)

1. Nikjoo, H., O'Neill, P., Wilson, W.E. and Goodhead, D.T. (2001) Computational approach for determining the spectrum of DNA damage induced by ionizing radiation. Radiat. Res., 156, 577-583. (Pubitemid 33027531)
2. Goodhead, D.T. (1994) Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int. J. Radiat. Biol., 65, 7-17. (Pubitemid 24063524)
3. Ward, J.F. (1988) DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and reparability. Prog. Nucleic Acid Res. Mol. Biol., 35, 95-125.
4. Brenner, D.J. and Ward, J.F. (1992) Constraints on energy deposition and target size of multiply damaged sites associated with DNA double-strand breaks. Int. J. Radiat. Biol., 61, 737-748.
5. Blaisdell, J.O., Harrison, L. and Wallace, S.S. (2001) Base excision repair processing of radiation-induced clustered DNA lesions. Radiat. Prot. Dosimetry, 97, 25-31. (Pubitemid 33094850)
6. Harrison, L., Hatahet, Z., Purmal, A.A. and Wallace, S.S. (1998) Multiply damaged sites in DNA: interactions with Escherichia coli endonucleases III and VIII. Nucleic Acids Res., 26, 932-941. (Pubitemid 28291644)
7. Sutherland, B.M., Bennett, P.V., Sidorkina, O. and Laval, J. (2000) Clustered DNA damages induced in isolated DNA and in human cells by low doses of ionizing radiation. Proc. Natl Acad. Sci. USA, 97, 103-108. (Pubitemid 30055791)
8. Kramer, M., Weyrather, W.K. and Scholz, M. (2003) The increased biological effectiveness of heavy charged particles: from radiobiology to treatment planning. Technol. Cancer Res. Treat., 2, 427-436. (Pubitemid 37362999)
9. Asaithamby, A. and Chen, D.J. (2010) Mechanism of cluster DNA damage repair in response to high-atomic number and energy particles radiation. Mutat. Res., doi:10.1016/j.mrfmmm.2010.11
10. .10. Weigelt, B. and Bissell, M.J. (2008) Unraveling the microenvironmental influences on the normal mammary gland and breast cancer. Semin. Cancer Biol., 18, 311-321.
11. Rhee, S. and Grinnell, F. (2007) Fibroblast mechanics in 3D collagen matrices. Adv. Drug Deliv. Rev., 59, 1299-1305. (Pubitemid 350088254)
12. Emerman, J.T. and Pitelka, D.R. (1977) Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes. In Vitro, 13, 316-328. (Pubitemid 8118093)
13. Nouspikel, T. (2007) DNA repair in differentiated cells: some new answers to old questions. Neuroscience, 145, 1213-1221. (Pubitemid 46602722)
14. Harper, J.V., Anderson, J.A. and O'Neill, P. (2010) Radiation induced DNA DSBs: Contribution from stalled replication forks? DNA Repair, 9, 907-913.
15. Lal, A., Pan, Y., Navarro, F., Dykxhoorn, D.M., Moreau, L., Meire, E., Bentwich, Z., Lieberman, J. and Chowdhury, D. (2009) miR-24-mediated downregulation of H2AX suppresses DNA repair in terminally differentiated blood cells. Nat. Struct. Mol. Biol., 16, 492-498.
16. Ramirez, R.D., Sheridan, S., Girard, L., Sato, M., Kim, Y., Pollack, J., Peyton, M., Zou, Y., Kurie, J.M., Dimaio, J.M. et al. (2004) Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res., 64, 9027-9034. (Pubitemid 39665513)
17. Asaithamby, A. and Chen, D.J. (2009) Cellular responses to DNA double-strand breaks after low-dose gamma-irradiation. Nucleic Acids Res., 37, 3912-3923.
18. Lee, G.Y., Kenny, P.A., Lee, E.H. and Bissell, M.J. (2007) Three-dimensional culture models of normal and malignant breast epithelial cells. Nat. Methods, 4, 359-365. (Pubitemid 46766981)
19. Chen, B.P., Chan, D.W., Kobayashi, J., Burma, S., Asaithamby, A., Morotomi-Yano, K., Botvinick, E., Qin, J. and Chen, D.J. (2005) Cell cycle dependence of DNA-dependent protein kinase phosphorylation in response to DNA double strand breaks. J. Biol. Chem., 280, 14709-14715. (Pubitemid 40562818)
20. Ding, L.H., Xie, Y., Park, S., Xiao, G. and Story, M.D. (2008) Enhanced identification and biological validation of differential gene expression via Illumina whole-genome expression arrays through the use of the model-based background correction methodology. Nucleic Acids Res., 36, e58.
21. DiBiase, S.J., Zeng, Z.C., Chen, R., Hyslop, T., Curran, W.J. Jr and Iliakis, G. (2000) DNA-dependent protein kinase stimulates an independently active, nonhomologous, end-joining apparatus. Cancer Res., 60, 1245-1253. (Pubitemid 30151991)
22. Asaithamby, A., Uematsu, N., Chatterjee, A., Story, M.D., Burma, S. and Chen, D.J. (2008) Repair of HZE-particle-induced DNA double-strand breaks in normal human fibroblasts. Radiat. Res., 169, 437-446. (Pubitemid 351620042)
23. Van Haute, L., De Block, G., Liebaers, I., Sermon, K. and De Rycke, M. (2009) Generation of lung epithelial-like tissue from human embryonic stem cells. Respir. Res., 10, 105.
24. Gerdes, J., Lemke, H., Baisch, H., Wacker, H.H., Schwab, U. and Stein, H. (1984) Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol., 133, 1710-1715. (Pubitemid 14035254)
25. Vaughan, M.B., Ramirez, R.D., Wright, W.E., Minna, J.D. and Shay, J.W. (2006) A three-dimensional model of differentiation of immortalized human bronchial epithelial cells. Differentiation, 74, 141-148.
26. Su, Y., Meador, J.A., Geard, C.R. and Balajee, A.S. (2010) Analysis of ionizing radiation-induced DNA damage and repair in three-dimensional human skin model system. Exp. Dermatol., 19, e16-22.
27. Schultz, L.B., Chehab, N.H., Malikzay, A. and Halazonetis, T.D. (2000) p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J. Cell Biol., 151, 1381-1390. (Pubitemid 32047588)
28. Ward, I.M., Wu, X. and Chen, J. (2001) Threonine 68 of Chk2 is phosphorylated at sites of DNA strand breaks. J. Biol. Chem., 276, 47755-47758.
29. Crosby, L.M. and Waters, C.M. (2010) Epithelial repair mechanisms in the lung. Am. J. Physiol. Lung Cell Mol. Physiol., 298, L715-731.
30. Fortini, P. and Dogliotti, E. (2010) Mechanisms of dealing with DNA damage in terminally differentiated cells. Mutat. Res., 685, 38-44.
31. Goodhead, D.T. (2006) Energy deposition stochastics and track structure: what about the target? Radiat. Prot. Dosimetry, 122, 3-15. (Pubitemid 47090415)
32. Gulston, M., de Lara, C., Jenner, T., Davis, E. and O'Neill, P. (2004) Processing of clustered DNA damage generates additional double-strand breaks in mammalian cells post-irradiation. Nucleic Acids Res., 32, 1602-1609. (Pubitemid 38854757)
33. Desai, N., Davis, E., O'Neill, P., Durante, M., Cucinotta, F.A. and Wu, H. (2005) Immunofluorescence detection of clustered gamma-H2AX foci induced by HZE-particle radiation. Radiat. Res., 164, 518-522. (Pubitemid 41368929)
34. Hada, M. and Georgakilas, A.G. (2008) Formation of clustered DNA damage after high-LET irradiation: a review. J. Radiat. Res., 49, 203-210. (Pubitemid 351744272)
35. David-Cordonnier, M.H., Cunniffe, S.M., Hickson, I.D. and O'Neill, P. (2002) Efficiency of incision of an AP site within clustered DNA damage by the major human AP endonuclease. Biochemistry, 41, 634-642. (Pubitemid 34062035)
36. Gulston, M., Fulford, J., Jenner, T., de Lara, C. and O'Neill, P. (2002) Clustered DNA damage induced by gamma radiation in human fibroblasts (HF19), hamster (V79-4) cells and plasmid DNA is revealed as Fpg and Nth sensitive sites. Nucleic Acids Res., 30, 3464-3472. (Pubitemid 34845943)
37. Budworth, H., Dianova, I.I., Podust, V.N. and Dianov, G.L. (2002) Repair of clustered DNA lesions. Sequence-specific inhibition of long-patch base excision repair be 8-oxoguanine. J. Biol. Chem., 277, 21300-21305. (Pubitemid 34952268)
38. Lomax, M.E., Cunniffe, S. and O'Neill, P. (2004) Efficiency of repair of an abasic site within DNA clustered damage sites by mammalian cell nuclear extracts. Biochemistry, 43, 11017-11026. (Pubitemid 39433690)
39. Eccles, L.J., Lomax, M.E. and O'Neill, P. (2010) Hierarchy of lesion processing governs the repair, double-strand break formation and mutability of three-lesion clustered DNA damage. Nucleic Acids Res., 38, 1123-1134.
40. Fujimoto, H., Pinak, M., Nemoto, T., O'Neill, P., Kume, E., Saito, K. and Maekawa, H. (2005) Molecular dynamics simulation of clustered DNA damage sites containing 8-oxoguanine and abasic site. J. Comput. Chem., 26, 788-798. (Pubitemid 40751572)
41. Harrison, L., Hatahet, Z. and Wallace, S.S. (1999) In vitro repair of synthetic ionizing radiation-induced multiply damaged DNA sites. J. Mol. Biol., 290, 667-684. (Pubitemid 29355700)
42. Malyarchuk, S., Castore, R. and Harrison, L. (2008) DNA repair of clustered lesions in mammalian cells: involvement of non-homologous end-joining. Nucleic Acids Res., 36, 4872-4882.
43. Bellon, S., Shikazono, N., Cunniffe, S., Lomax, M. and O'Neill, P. (2009) Processing of thymine glycol in a clustered DNA damage site: mutagenic or cytotoxic. Nucleic Acids Res., 37, 4430-4440.
44. Sedelnikova, O.A., Nakamura, A., Kovalchuk, O., Koturbash, I., Mitchell, S.A., Marino, S.A., Brenner, D.J. and Bonner, W.M. (2007) DNA double-strand breaks form in bystander cells after microbeam irradiation of three-dimensional human tissue models. Cancer Res., 67, 4295-4302. (Pubitemid 46815077)
45. Rothkamm, K., Kruger, I., Thompson, L.H. and Lobrich, M. (2003) Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol., 23, 5706-5715. (Pubitemid 36951334)
46. Lieber, M.R. (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem., 79, 181-211.
47. Wang, H., Zhang, X., Wang, P., Yu, X., Essers, J., Chen, D., Kanaar, R., Takeda, S. and Wang, Y. (2010) Characteristics of DNA-binding proteins determine the biological sensitivity to high-linear energy transfer radiation. Nucleic Acids Res., 38, 3245-3251.
48. Tabocchini, M.A., Rothkamm, K., Signoretti, C., Risse, J., Sapora, O. and Lobrich, M. (2000) Formation and repair of DNA double-strand breaks in gamma-irradiated K562 cells undergoing erythroid differentiation. Mutat. Res., 461, 71-82.
49. Moskwa, P., Buffa, F.M., Pan, Y., Panchakshari, R., Gottipati, P., Muschel, R.J., Beech, J., Kulshrestha, R., Abdelmohsen, K., Weinstock, D.M. et al. (2011) miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol. Cell, 41, 210-220.
50. Narciso, L., Fortini, P., Pajalunga, D., Franchitto, A., Liu, P., Degan, P., Frechet, M., Demple, B., Crescenzi, M. and Dogliotti, E. (2007) Terminally differentiated muscle cells are defective in base excision DNA repair and hypersensitive to oxygen injury. Proc. Natl Acad. Sci. USA, 104, 17010-17015. (Pubitemid 350210982)
51. Satoh, T., Hatanaka, M., Yamamoto, K., Kuro-o, M. and Sofuni, T. (2002) Application of mFISH for the analysis of chemically-induced chromosomal aberrations: a model for the formation of triradial chromosomes. Mutat. Res., 504, 57-65. (Pubitemid 34775099)
52. Holt, S.M., Scemama, J.L., Panayiotidis, M.I. and Georgakilas, A.G. (2009) Compromised repair of clustered DNA damage in the human acute lymphoblastic leukemia MSH2-deficient NALM-6 cells. Mutat. Res., 674, 123-130.