Strategies for the evaluation of DNA damage and repair mechanisms in cancer (Review)
- Authors:
- Gabriela Figueroa‑González
- Carlos Pérez‑Plasencia
-
Affiliations: Genomics Laboratory, National Cancer Institute of Mexico, Mexico City 14080, Mexico - Published online on: April 6, 2017 https://doi.org/10.3892/ol.2017.6002
- Pages: 3982-3988
-
Copyright: © Figueroa‑González et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
 |
|
Cadet J and Wagner JR: DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation. Cold Spring Harb Perspect Biol. 5:a0125592013. View Article : Google Scholar : PubMed/NCBI | |
|
Li Z, Pearlman AH and Hsieh P: DNA mismatch repair and the DNA damage response. DNA Repair (Amst). 38:94–101. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Altaf M, Saksouk N and Côté J: Histone modifications in response to DNA damage. Mutat Res. 618:81–90. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Lord CJ and Ashworth A: The DNA damage response and cancer therapy. Nature. 481:287–294. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Cao LL, Shen C and Zhu WG: Histone modifications in DNA damage response. Sci China Life Sci. 59:257–270. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Schipler A and Iliakis G: DNA double-strand-break complexity levels and their possible contributions to the probability for error-prone processing and repair pathway choice. Nucleic Acids Res. 41:7589–7605. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Grimaldi KA, McGurk CJ, McHugh PJ and Hartley JA: PCR-based methods for detecting DNA damage and its repair at the sub-gene and single nucleotide levels in cells. Mol Biotechnol. 20:181–196. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Osborne DJ: Technologies for detection of DNA damage and mutations. Endeavour. 21:178–179. 1997. View Article : Google Scholar | |
|
Furda A, Santos JH, Meyer JN and van Houten B: Quantitative PCR-based measurement of nuclear and mitochondrial DNA damage and repair in mammalian cellsMolecular Toxicology Protocols. Keohavong P and Grant GS: Humana Press; Totowa, NJ: pp. 419–437. 2014, View Article : Google Scholar | |
|
Senoo T, Yamanaka M, Nakamura A, Terashita T, Kawano S and Ikeda S: Quantitative PCR for detection of DNA damage in mitochondrial DNA of the fission yeast Schizosaccharomyces pombe. J Microbiol Methods. 127:77–81. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
De Boer JG and Glickman BW: Mutations recovered in the Chinese hamster aprt gene after exposure to carboplatin: A comparison with cisplatin. Carcinogenesis. 13:15–17. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Van Houten B, Cheng S and Chen Y: Measuring gene-specific nucleotide excision repair in human cells using quantitative amplification of long targets from nanogram quantities of DNA. Mutat Res. 460:81–94. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Strauss EC and Orkin SH: Guanine-adenine ligation-mediated PCR in vivo footprinting. Methods. 11:164–170. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Pfeifer GP and Tornaletti S: Footprinting with UV irradiation and LMPCR. Methods. 11:189–196. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Pfeifer GP, Chen HH, Komura J and Riggs AD: Chromatin structure analysis by ligation-mediated and terminal transferase-mediated polymerase chain reaction. Methods Enzymol. 304:548–571. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Chang L, Li J and Wang L: Immuno-PCR: An ultrasensitive immunoassay for biomolecular detection. Anal Chim Acta. 910:12–24. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Karakoula A, Evans MD, Podmore ID, Hutchinson PE, Lunec J and Cooke MS: Quantification of UVR-induced DNA damage: Global-versus gene-specific levels of thymine dimers. J Immunol Methods. 277:27–37. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Wang G, Hallberg LM and Englander EW: Rapid SINE-mediated detection of cisplatin: DNA adduct formation in vitro and in vivo in blood. Mutat Res. 434:67–74. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Wang G, Hallberg LM, Saphier E and Englander EW: Short interspersed DNA element-mediated detection of UVB-induced DNA damage and repair in the mouse genome, in vitro, and in vivo in skin. Mutat Res. 433:147–157. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Featherstone C and Jackson SP: Ku, a DNA repair protein with multiple cellular functions? Mutat Res. 434:3–15. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Jones JM, Gellert M and Yang W: A Ku bridge over broken DNA. Structure. 9:881–884. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Gullo C, Au M, Feng G and Teoh G: The biology of Ku and its potential oncogenic role in cancer. Biochim Biophys Acta. 1765:223–234. 2006.PubMed/NCBI | |
|
Doherty AJ and Jackson SP: DNA repair: How Ku makes ends meet. Curr Biol. 11:R920–R924. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Walker JR, Corpina RA and Goldberg J: Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature. 412:607–614. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M and Bonner WM: A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol. 10:886–895. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Rogakou EP, Boon C, Redon C and Bonner WM: Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol. 146:905–916. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Henderson DS: DNA repair protocolsMethods in Molecular Biology. 2nd. Humana Press; New Jersey, NJ: pp. 4982006 | |
|
Levy N, Martz A, Bresson A, Spenlehauer C, De Murcia G and Ménissier-De Murcia J: Xrcc1 is phosphorylated by DNA-dependent protein kinase in response to DNA damage. Nucleic Acids Res. 34:32–41. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Caldecott KW: Protein-protein interactions during mammalian DNA single-strand break repair. Biochem Soc Trans. 31:247–251. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Brem R and Hall J: XRCC1 is required for DNA single-strand break repair in human cells. Nucleic Acids Res. 33:2512–2520. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Goode EL, Ulrich CM and Potter JD: Polymorphisms in DNA repair genes and associations with cancer risk. Cancer Epidemiol Biomarkers Prev. 11:1513–1530. 2002.PubMed/NCBI | |
|
Strom CE, Mortusewicz O, Finch D, Parsons JL, Lagerqvist A, Johansson F, Schultz N, Erixon K, Dianov GL and Helleday T: CK2 phosphorylation of XRCC1 facilitates dissociation from DNA and single-strand break formation during base excision repair. DNA Repair (Amst). 10:961–969. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Caldecott KW: XRCC1 and DNA strand break repair. DNA Repair (Amst). 2:955–969. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Collins AR: The comet assay for DNA damage and repair: Principles, applications, and limitations. Mol Biotechnol. 26:249–261. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Collins AR: Measuring oxidative damage to DNA and its repair with the comet assay. Biochim Biophys Acta. 1840:794–800. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Collins AR and Azqueta A: DNA repair as a biomarker in human biomonitoring studies; further applications of the comet assay. Mutat Res. 736:122–129. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Kent CR, Eady JJ, Ross GM and Steel GG: The comet moment as a measure of DNA damage in the comet assay. Int J Radiat Biol. 67:655–660. 1995. View Article : Google Scholar : PubMed/NCBI | |
|
Jyoti S, Khan S, Naz F, Ali Rahul F and Siddique YH: Assessment of DNA damage by panmasala, gutkha chewing and smoking in buccal epithelial cells using alkaline single cell gel electrophoresis (SCGE). Egyptian J Med Human Gen. 14:391–394. 2013. View Article : Google Scholar | |
|
Ostling O and Johanson KJ: Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells. Biochem Biophys Res Commun. 123:291–298. 1984. View Article : Google Scholar : PubMed/NCBI | |
|
Glei M, Hovhannisyan G and Pool-Zobel BL: Use of comet-FISH in the study of DNA damage and repair: Review. Mutat Res. 681:33–43. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Collins AR, Dobson VL, Dušinská M, Kennedy G and Štětina R: The comet assay: What can it really tell us? Mutat Res. 375:183–193. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Rojas E, Lopez MC and Valverde M: Single cell gel electrophoresis assay: Methodology and applications. J Chromatogr B Biomed Sci Appl. 722:225–254. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Angelis KJ, Dusinská M and Collins AR: Single cell gel electrophoresis: Detection of DNA damage at different levels of sensitivity. Electrophoresis. 20:2133–2138. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Collins AR and Azqueta A: Chapter 4-single-cell gel electrophoresis combined with lesion-specific enzymes to measure oxidative damage to DNAMethods in Cell Biology. Conn PM: Academic Press; Burlington, MA: pp. 69–92. 2012, View Article : Google Scholar | |
|
Kumari S, Rastogi R, Singh K, Singh S and Sinha R: DNA damage: Detection strategies. EXCLI J. 7:44–62. 2008. | |
|
Roti Roti JL and Wright WD: Visualization of DNA loops in nucleoids from HeLa cells: Assays for DNA damage and repair. Cytometry. 8:461–467. 1987. View Article : Google Scholar : PubMed/NCBI | |
|
Gavrieli Y, Sherman Y and Ben-Sasson SA: Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol. 119:493–501. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Walker PR, Carson C, Leblanc J and Sikorska M: Labeling DNA damage with terminal transferase, in in situ detection of DNA damageMethods and Protocols. Didenko VV: Humana Press; Totowa, NJ: pp. 3–19. 2002 | |
|
Loo DT: TUNEL assay. An overview of techniques. Methods Mol Biol. 203:21–30. 2002.PubMed/NCBI | |
|
Kanoh M, Takemura G, Misao J, Hayakawa Y, Aoyama T, Nishigaki K, Noda T, Fujiwara T, Fukuda K, Minatoguchi S and Fujiwara H: Significance of myocytes with positive DNA in situ nick end-labeling (TUNEL) in hearts with dilated cardiomyopathy: Not apoptosis but DNA repair. Circulation. 99:2757–2764. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Otsuki Y and Ito Y: Quantitative differentiation of both free 3′ oh and 5′ oh DNA ends using terminal transferase-based labeling combined with transmission electron microscopy, in in situ detection of DNA damageMethods and Protocols. Didenko VV: Humana Press; Totowa, NJ: pp. 41–54. 2002 | |
|
Didenko VV and Hornsby PJ: Presence of double-strand breaks with single-base 3′ overhangs in cells undergoing apoptosis but not necrosis. J Cell Biol. 135:1369–1376. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Didenko VV: Detection of specific double-strand DNA breaks and apoptosis in situ using T4 DNA ligase. Methods Mol Biol. 203:143–151. 2002.PubMed/NCBI | |
|
Levsky JM and Singer RH: Fluorescence in situ hybridization: Past, present and future. J Cell Sci. 116:2833–2838. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Gall JG and Pardue ML: Formation and detection of RNA-DNA hybrid molecules in cytological preparations. Proc Natl Acad Sci USA. 63:378–383. 1969. View Article : Google Scholar : PubMed/NCBI | |
|
Halling KC and Kipp BR: Fluorescence in situ hybridization in diagnostic cytology. Hum Pathol. 38:1137–1144. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Cortés-Gutiérrez EI, Fernández JL, Dávila-Rodríguez MI, López-Fernández C and Gosálvez J: Use of DBD-FISH for the study of cervical cancer progression, in cervical cancerMethods and Protocols. Keppler D and Lin WA: Springer; New York, NY: pp. 291–301. 2015 | |
|
Fernández JL, Vázquez-Gundín F, Rivero MT, Genescá A, Gosálvez J and Goyanes V: DBD-fish on neutral comets: Simultaneous analysis of DNA single- and double-strand breaks in individual cells. Exp Cell Res. 270:102–109. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Fink SL and Cookson BT: Apoptosis, pyroptosis, and necrosis: Mechanistic description of dead and dying eukaryotic cells. Infect Immun. 73:1907–1916. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Basiji D and O'Gorman MR: Imaging flow cytometry. J Immunol Methods. 423:1–2. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Muehlbauer PA and Schuler MJ: Detection of numerical chromosomal aberrations by flow cytometry: A novel process for identifying aneugenic agents. Mutat Res. 585:156–169. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Henry CM, Hollville E and Martin SJ: Measuring apoptosis by microscopy and flow cytometry. Methods. 61:90–97. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Huerta S, Goulet EJ, Huerta-Yepez S and Livingston EH: Screening and detection of apoptosis. J Surg Res. 139:143–156. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Vermes I, Haanen C, Steffens-Nakken H and Reutelingsperger C: A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods. 184:39–51. 1995. View Article : Google Scholar : PubMed/NCBI | |
|
Pietkiewicz S, Schmidt JH and Lavrik IN: Quantification of apoptosis and necroptosis at the single cell level by a combination of imaging flow cytometry with classical Annexin V/propidium iodide staining. J Immunol Methods. 423:99–103. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Berton TR and Mitchell DL: Quantification of DNA photoproducts in mammalian cell DNA using radioimmunoassay. Methods Mol Biol. 920:177–187. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Santella RM: Immunological methods for detection of carcinogen-DNA damage in humans. Cancer Epidemiol Biomarkers Prev. 8:733–739. 1999.PubMed/NCBI | |
|
Yatabe Y: ALK FISH and IHC: You cannot have one without the other. J Thorac Oncol. 10:548–550. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Kriste AG, Martincigh BS and Salter LF: A sensitive immunoassay technique for thymine dimer quantitation in UV-irradiated DNA. J Photochem Photobiol A: Chemistry. 93:185–192. 1996. View Article : Google Scholar | |
|
El-Yazbi AF and Loppnow GR: Detecting UV-induced nucleic-acid damage. TrAC Trends Analytical Chemistry. 61:83–91. 2014. View Article : Google Scholar | |
|
Toyokuni S: Oxidative stress as an iceberg in carcinogenesis and cancer biology. Arch Biochem Biophys. 595:46–49. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Rindgen D, Turesky RJ and Vouros P: Determination of in vitro formed DNA adducts of 2-amino-1-methyl-6-phenylimidazo [4,5-b]pyridine using capillary liquid chromatography/electrospray ionization/tandem mass spectrometry. Chem Res Toxicol. 8:1005–1013. 1995. View Article : Google Scholar : PubMed/NCBI | |
|
Mullins EA, Rubinson EH, Pereira KN, Calcutt MW, Christov PP and Eichman BF: An HPLC-tandem mass spectrometry method for simultaneous detection of alkylated base excision repair products. Methods. 64:59–66. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Caldecott KW: DNA single-strand break repair. Exp Cell Res. 329:2–8. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Cadet J, Douki T, Frelon S, Sauvaigo S, Pouget JP and Ravanat JL: Assessment of oxidative base damage to isolated and cellular DNA by HPLC-MS/MS measurement. Free Radic Biol Med. 33:441–449. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Pouget JP, Douki T, Richard MJ and Cadet J: DNA damage induced in cells by gamma and UVA radiation as measured by HPLC/GC-MS and HPLC-EC and comet assay. Chem Res Toxicol. 13:541–549. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Gowda GA and Djukovic D: Overview of mass spectrometry-based metabolomics: Opportunities and challenges. Methods Mol Biol. 1198:3–12. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Dizdaroglu M, Coskun E and Jaruga P: Measurement of oxidatively induced DNA damage and its repair, by mass spectrometric techniques. Free Radic Res. 49:525–548. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Sato K and Greenberg MM: Selective detection of 2-deoxyribonolactone in DNA. J Am Chem Soc. 127:2806–2807. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Dizdaroglu M: Substrate specificities and excision kinetics of DNA glycosylases involved in base-excision repair of oxidative DNA damage. Mutat Res. 531:109–126. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Reddy PT, Jaruga P, Nelson BC, Lowenthal M and Dizdaroglu M: Stable isotope-labeling of DNA repair proteins and their purification, and characterization. Protein Expr Purif. 78:94–101. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Gajewski E and Dizdaroglu M: Hydroxyl radical induced cross-linking of cytosine and tyrosine in nucleohistone. Biochemistry. 29:977–980. 1990. View Article : Google Scholar : PubMed/NCBI | |
|
Koivisto P and Peltonen K: Analytical methods in DNA and protein adduct analysis. Anal Bioanal Chem. 398:2563–2572. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Dizdaroglu M and Gajewski E: Structure and mechanism of hydroxyl radical-induced formation of a DNA-protein cross-link involving thymine and lysine in nucleohistone. Cancer Res. 49:3463–3467. 1989.PubMed/NCBI | |
|
Fojta M, Daňhel A, Havran L and Vyskočil V: Recent progress in electrochemical sensors and assays for DNA damage and repair. TrAC Trends Analytical Chemistry. 79:160–167. 2016. View Article : Google Scholar | |
|
Boal AK and Barton JK: Electrochemical detection of lesions in DNA. Bioconjug Chem. 16:312–321. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Boon EM, Ceres DM, Drummond TG, Hill MG and Barton JK: Mutation detection by electrocatalysis at DNA-modified electrodes. Nat Biotechnol. 18:1096–1100. 2000. View Article : Google Scholar : PubMed/NCBI |
