Engineered proteins detect spontaneous DNA breakage in human and bacterial cells

eLife

Volumn 2013, Issue 2, 2013, Pages

  Shee, Chandan ^a   Cox, Ben D ^b   Gu, Franklin ^a   Luengas, Elizabeth M ^c   Joshi, Mohan C ^a   Chiu, Li Ya ^b   Magnan, David ^a   Halliday, Jennifer A ^a   Frisch, Ryan L ^a   Gibson, Janet L ^a   Nehring, Ralf Bernd ^a   Do, Huong G ^d   Hernandez, Marcos ^a   Li, Lei ^d   Herman, Christophe ^a   Hastings, P J ^a   Bates, David ^a   Harris, Reuben S ^c   Miller, Kyle M ^b   Rosenberg, Susan M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOBEC3A PROTEIN, HUMAN; BACTERIAL PROTEIN; CYTIDINE DEAMINASE; DNA; DNA BINDING PROTEIN; DNA HELICASE; GAM PROTEIN, COLIPHAGE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTEIN; PROTEIN GAM; SIGNAL PEPTIDE; TP53BP1 PROTEIN, HUMAN; UNCLASSIFIED DRUG; VIRUS PROTEIN; XRCC5 PROTEIN, HUMAN;

ANIMAL; ARTICLE; BACTERIAL CHROMOSOME; CELL DIVISION; CELL VIABILITY; CHEMISTRY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; DOUBLE STRANDED DNA BREAK; ENTEROBACTERIA PHAGE MU; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; GROWTH RATE; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; LASER MICROSCOPY; METABOLISM; MICROSCOPY; MOUSE; NONHUMAN; PHOTOGRAPHY; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PROCEDURES; PROTEIN ENGINEERING; REPORTER GENE; SYNTHETIC BIOLOGY; TIME LAPSE IMAGING; ULTRAVIOLET RADIATION; WESTERN BLOTTING;

ANIMALS; BACTERIOPHAGE MU; CHEMISTRY; CHROMOSOMES, BACTERIAL; CYTIDINE DEAMINASE; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA-BINDING PROTEINS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENES, REPORTER; GENETICS; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; METABOLISM; METHODS; MICE; PROTEIN ENGINEERING; PROTEINS; RECOMBINANT FUSION PROTEINS; SYNTHETIC BIOLOGY; VIRAL PROTEINS;

BACTERIA (MICROORGANISMS); ENTEROBACTERIA PHAGE MU; ESCHERICHIA COLI; MAMMALIA;

EID: 84887397458     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01222.001     Document Type: Article

References (89)

1. Abraham ZH, Symonds N. 1990. Purification of overexpressed gam gene protein from bacteriophage Mu by denaturation-renaturation techniques and a study of its DNA-binding properties. Biochem J 269:679-84.
2. Akroyd J, Symonds N. 1986. Localization of the gam gene of bacteriophage mu and characterisation of the gene product. Gene 49:273-82. doi: 10.1016/0378-1119(86)90288-X.
3. Akroyd JE, Clayson E, Higgins NP. 1986. Purification of the gam gene-product of bacteriophage Mu and determination of the nucleotide sequence of the gam gene. Nucleic Acids Res 14:6901-14. doi: 10.1093/nar/14.17.6901.
4. Al Mamun AA, Lombardo MJ, Shee C, Lisewski AM, Gonzalez C, Lin D, et al. 2012. Identity and function of a large gene network underlying mutagenic repair of DNA breaks. Science 338:1344-8. doi: 10.1126/science.1226683.
5. Bindra RS, Crosby ME, Glazer PM. 2007. Regulation of DNA repair in hypoxic cancer cells. Cancer Metastasis Rev 26:249-60. doi: 10.1007/s10555-007-9061-3.
6. Blier PR, Griffith AJ, Craft J, Hardin JA. 1993. Binding of Ku protein to DNA. Measurement of affinity for ends and demonstration of binding to nicks. J Biol Chem 268:7594-601.
7. Boles BR, Singh PK. 2008. Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc Natl Acad Sci USA 105:12503-8. doi: 10.1073/pnas.0801499105.
8. Bonura T, Smith KC. 1975. Enzymatic production of deoxyrobonucleic acid double-strand breaks and ultraviolet irradiation of Escherichia coli K12. J Bacteriol 122:511-7.
9. Bonura T, Smith KC. 1977. Sensitization of Escherichia coli C to gamma-radiation by 5-bromouracil incorporation. Int J Radiat Biol Relat Stud Phys Chem Med 32:457-64. doi: 10.1080/09553007714551211.
10. Bouquet F, Muller C, Salles B. 2006. The loss of gammaH2AX signal is a marker of DNA double strand breaks repair only at low levels of DNA damage. Cell Cycle 5:1116-22. doi: 10.4161/cc.5.10.2799.
11. Britton S, Coates J, Jackson SP. 2013. A new method for high-resolution imaging of Ku foci to decipher mechanisms of DNA double-strand break repair. J Cell Biol 202:579. doi: 10.1083/jcb.201303073.
12. Burns MB, Lackey L, Carpenter MA, Rathore A, Land AM, Leonard B, et al. 2013a. APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494:366-70. doi: 10.1038/nature11881.
13. Burns MB, Temiz NA, Harris RS. 2013b. Evidence for APOBEC3B mutagenesis in multiple human cancers. Nat Genet 45:977-83. doi: 10.1038/ng.2701.
14. Carpenter MA, Li M, Rathore A, Lackey L, Law EK, Land AM, et al. 2012. Methylcytosine and normal cytosine deamination by the foreign DNA restriction enzyme APOBEC3A. J Biol Chem 287:34801-8. doi: 10.1074/jbc.M112.385161.
15. Cirz RT, Chin JK, Andes DR, de Crecy-Lagard V, Craig WA, Romesberg FE. 2005. Inhibition of mutation and combating the evolution of antibiotic resistance. PLOS Biol 3:e176. doi: 10.1371/journal.pbio.0030176.
16. Conticello SG, Langlois MA, Yang Z, Neuberger MS. 2007. DNA deamination in immunity: AID in the context of its APOBEC relatives. Adv Immunol 94:37-73. doi: 10.1016/S0065-2776(06)94002-4.
17. Cox MM, Goodman MF, Kreuzer KN, Sherratt DJ, Sandler SJ, Marians KJ. 2000. The importance of repairing stalled replication forks. Nature 404:37-41. doi: 10.1038/35003501.
18. d'Adda di Fagagna F, Weller GR, Doherty AJ, Jackson SP. 2003. The Gam protein of bacteriophage Mu is an orthologue of eukaryotic Ku. EMBO Rep 4:47-52. doi: 10.1038/sj.embor.embor709.
19. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640-5. doi: 10.1073/pnas.120163297.
20. Dynan WS, Yoo S. 1998. Interaction of Ku protein and DNA-dependent protein kinase catalytic subunit with nucleic acids. Nucleic Acids Res 26:1551-9. doi: 10.1093/nar/26.7.1551.
21. Elowitz MB, Levine AJ, Siggia ED, Swain PS. 2002. Stochastic gene expression in a single cell. Science 297:1183-6. doi: 10.1126/science.1070919.
22. Fradet-Turcotte A, Canny MD, Escribano-Diaz C, Orthwein A, Leung CC, Huang H, et al. 2013. 53BP1 is a reader of the DNA damage-induced H2A Lys15 ubiquitin mark. Nature 499:50-4. doi: 10.1038/nature12318.
23. Gavrieli Y, Sherman Y, Ben-Sasson SA. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501. doi: 10.1083/jcb.119.3.493.
24. Ge J, Wood DK, Weingeist DM, Prasongtanakij S, Navasumrit P, Ruchirawat M, et al. 2013. Standard fluorescent imaging of live cells is highly genotoxic. Cytometry A 83:552-60. doi: 10.1002/cyto.a.22291.
25. Gravel S, Larrivee M, Labrecque P, Wellinger RJ. 1998. Yeast Ku as a regulator of chromosomal DNA end structure. Science 280:741-4. doi: 10.1126/science.280.5364.741.
26. Gumbiner-Russo LM, Lombardo M-J, Ponder RG, Rosenberg SM. 2001. The TGV transgenic vectors for single-copy gene expression from the Escherichia coli chromosome. Gene 273:97-104. doi: 10.1016/S0378-1119(01)00565-0.
27. Gupta MK, Guy CP, Yeeles JT, Atkinson J, Bell H, Lloyd RG, et al. 2013. Protein-DNA complexes are the primary sources of replication fork pausing in Escherichia coli. Proc Natl Acad Sci USA 110:7252-7. doi: 10.1073/pnas.1303890110.
28. Haaf T, Golub EI, Reddy G, Radding CM, Ward DC. 1995. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc Natl Acad Sci USA 92:2298-302. doi: 10.1073/pnas.92.6.2298.
29. Han J, Hendzel MJ, Allalunis-Turner J. 2006. Quantitative analysis reveals asynchronous and more than DSB-associated histone H2AX phosphorylation after exposure to ionizing radiation. Radiat Res 165:283-92. doi: 10.1667/RR3516.1.
30. Harrigan JA, Belotserkovskaya R, Coates J, Dimitrova DS, Polo SE, Bradshaw CR, et al. 2011. Replication stress induces 53BP1-containing OPT domains in G1 cells. J Cell Biol 193:97-108. doi: 10.1083/jcb.201011083.
31. Harris RS, Longerich S, Rosenberg SM. 1994. Recombination in adaptive mutation. Science 264:258-60. doi: 10.1126/science.8146657.
32. Hastings PJ, Ira G, Lupski JR. 2009. A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLOS Genet 5:e1000327. doi: 10.1371/journal.pgen.1000327.
33. Hecht SM. 2000. Bleomycin: new perspectives on the mechanism of action. J Nat Prod 63:158-68. doi: 10.1021/np990549f.
34. Jackson SP, Bartek J. 2009. The DNA-damage response in human biology and disease. Nature 461:1071-8. doi: 10.1038/nature08467.
35. Kidane D, Sanchez H, Alonso JC, Graumann PL. 2004. Visualization of DNA double-strand break repair in live bacteria reveals dynamic recruitment of Bacillus subtilis RecF, RecO and RecN proteins to distinct sites on the nucleoids. Mol Microbiol 52:1627-39. doi: 10.1111/j.1365-2958.2004.04102.x.
36. Kobayashi H, Simmons LA, Yuan DS, Broughton WJ, Walker GC. 2008. Multiple Ku orthologues mediate DNA non-homologous end-joining in the free-living form and during chronic infection of Sinorhizobium meliloti. Mol Microbiol 67:350-63. doi: 10.1111/j.1365-2958.2007.06036.x.
37. Koike M, Yutoku Y, Koike A. 2011. Accumulation of Ku70 at DNA double-strand breaks in living epithelial cells. Exp Cell Res 317:2429-37. doi: 10.1016/j.yexcr.2011.07.018.
38. Kongruttanachok N, Phuangphairoj C, Thongnak A, Ponyeam W, Rattanatanyong P, Pornthanakasem W, et al. 2010. Replication independent DNA double-strand break retention may prevent genomic instability. Mol cancer 9:70. doi: 10.1186/1476-4598-9-70.
39. Kuzminov A. 2001. Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc Natl Acad Sci USA 98:8241-6. doi: 10.1073/pnas.131009198.
40. Kuzminova EA, Kuzminov A. 2008. Patterns of chromosomal fragmentation due to uracil-DNA incorporation reveal a novel mechanism of replication-dependent double-strand breaks. Mol Microbiol 68:202-15. doi: 10.1111/j.1365-2958.2008.06149.x.
41. Lackey L, Demorest ZL, Land AM, Hultquist JF, Brown WL, Harris RS. 2012. APOBEC3B and AID have similar nuclear import mechanisms. J Mol Biol 419:301-14. doi: 10.1016/j.jmb.2012.03.011.
42. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-5. doi: 10.1038/227680a0.
43. Landry S, Narvaiza I, Linfesty DC, Weitzman MD. 2011. APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO Rep 12:444-50. doi: 10.1038/embor.2011.46.
44. Liu Y, Li M, Lee EY, Maizels N. 1999. Localization and dynamic relocalization of mammalian Rad52 during the cell cycle and in response to DNA damage. Curr Biol 9:975-8. doi: 10.1016/S0960-9822(99)80427-8.
45. Lukas C, Savic V, Bekker-Jensen S, Doil C, Neumann B, Pedersen RS, et al. 2011a. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat Cell Biol 13:243-53. doi: 10.1038/ncb2201.
46. Lukas J, Lukas C, Bartek J. 2011b. More than just a focus: the chromatin response to DNA damage and its role in genome integrity maintenance. Nat Cell Biol 13:1161-9. doi: 10.1038/ncb2344.
47. Maser RS, Monsen KJ, Nelms BE, Petrini JH. 1997. hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks. Mol Cell Biol 17:6087-96.
48. Merrikh H, Zhang Y, Grossman AD, Wang JD. 2012. Replication-transcription conflicts in bacteria. Nat Rev Microbiol 10:449-58. doi: 10.1038/nrmicro2800.
49. Michel B, Ehrlich SD, Uzest M. 1997. DNA double-strand breaks caused by replication arrest. EMBO J 16:430-8. doi: 10.1093/emboj/16.2.430.
50. Miller JH. 1992. A short course in bacterial genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
51. Miranda A, Kuzminov A. 2003. Chromosomal lesion suppression and removal in Escherichia coli via linear DNA degradation. Genetics 163:1255-71.
52. Negrini S, Gorgoulis VG, Halazonetis TD. 2010. Genomic instability-an evolving hallmark of cancer. Nat Rev Mol Cell Biol 11:220-8. doi: 10.1038/nrm2858.
53. Nik-Zainal S, Alexandrov LB, Wedge DC, Van Loo P, Greenman CD, Raine K, et al. 2012. Mutational processes molding the genomes of 21 breast cancers. Cell 149:979-93. doi: 10.1016/j.cell.2012.04.024.
54. Nishihara K, Kanemori M, Kitagawa M, Yanagi H, Yura T. 1998. Chaperone coexpression plasmids: differential and synergistic roles of DnaK-DnaJ-GrpE and GroEL-GroES in assisting folding of an allergen of Japanese cedar pollen, Cryj2, in Escherichia coli. Appl Environ Microbiol 64:1694-9.
55. O'Driscoll M, Jeggo PA. 2006. The role of double-strand break repair-insights from human genetics. Nat Rev Genet 7:45-54. doi: 10.1038/nrg1746.
56. Olive PL, Banath JP, Durand RE. 1990. Heterogeneity in radiation-induced DNA damage and repair in tumor and normal cells measured using the "comet" assay. Radiat Res 122:86-94. doi: 10.2307/3577587.
57. Paillard S, Strauss F. 1991. Analysis of the mechanism of interaction of simian Ku protein with DNA. Nucleic Acids Res 19:5619-24. doi: 10.1093/nar/19.20.5619.
58. Paques F, Haber JE. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63:349-404.
59. Pennington JM. 2006. On spontaneous DNA damage in single living cells. Ph.D. thesis, Baylor College of medicine, Houston.
60. Pennington JM, Rosenberg SM. 2007. Spontaneous DNA breakage in single living Escherichia coli cells. Nat Genet 39:797-802. doi: 10.1038/ng2051.
61. Ponder RG, Fonville NC, Rosenberg SM. 2005. A switch from high-fidelity to error-prone DNA double-strand break repair underlies stress-induced mutation. Mol Cell 19:791-804. doi: 10.1016/j.molcel.2005.07.025.
62. Porebski S, Bailey LG, Bernard RB. 1997. Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol reporter/ISPMB 15:8-15. doi: 10.1007/BF02772108.
63. Prieto AI, Ramos-Morales F, Casadesus J. 2006. Repair of DNA damage induced by bile salts in Salmonella enterica. Genetics 174:575-84. doi: 10.1534/genetics.106.060889.
64. Raderschall E, Golub EI, Haaf T. 1999. Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc Natl Acad Sci USA 96:1921-6. doi: 10.1073/pnas.96.5.1921.
65. Rappold I, Iwabuchi K, Date T, Chen J. 2001. Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J Cell Biol 153:613-20. doi: 10.1083/jcb.153.3.613.
66. Renzette N, Gumlaw N, Nordman JT, Krieger M, Yeh SP, Long E, et al. 2005. Localization of RecA in Escherichia coli K-12 using RecA-GFP. Mol Microbiol 57:1074-85. doi: 10.1111/j.1365-2958.2005.04755.x.
67. Robbiani DF, Nussenzweig MC. 2013. Chromosome translocation, B cell lymphoma, and activation-induced cytidine deaminase. Annu Rev Pathol 8:79-103. doi: 10.1146/annurev-pathol-020712-164004.
68. Roberts SA, Sterling J, Thompson C, Harris S, Mav D, Shah R, et al. 2012. Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol Cell 46:424-35. doi: 10.1016/j.molcel.2012.03.030.
69. Rogakou EP, Boon C, Redon C, Bonner WM. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146:905-16. doi: 10.1083/jcb.146.5.905.
70. Rosenberg SM, Longerich S, Gee P, Harris RS. 1994. Adaptive mutation by deletions in small mononucleotide repeats. Science 265:405-7. doi: 10.1126/science.8023163.
71. Rosenberg SM, Shee C, Frisch RL, Hastings PJ. 2012. Stress-induced mutation via DNA breaks in Escherichia coli: a molecular mechanism with implications for evolution and medicine. Bioessays 34:885-92. doi: 10.1002/bies.201200050.
72. Sambrook J, Russell DW. 2001. Molecular cloning-a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
73. Scully R, Chen J, Ochs RL, Keegan K, Hoekstra M, Feunteun J, et al. 1997. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90:425-35. doi: 10.1016/S0092-8674(00)80503-6.
74. Shee C, Gibson JL, Rosenberg SM. 2012. Two mechanisms produce mutation hotspots at DNA breaks in Escherichia coli. Cell Rep 2:714-21. doi: 10.1016/j.celrep.2012.08.033.
75. Shinohara M, Io K, Shindo K, Matsui M, Sakamoto T, Tada K, et al. 2012. APOBEC3B can impair genomic stability by inducing base substitutions in genomic DNA in human cells. Sci Rep 2:806. doi: 10.1038/srep00806.
76. Smith GR. 1983. General recombination. In: Hendrix R, Roberts J, Stahl F, Weisberg R, editors. InLambda II. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press. p. 175-209.
77. Strathern JN, Shafer BK, McGill CB. 1995. DNA synthesis errors associated with double-strand-break repair. Genetics 140:965-72.
78. Symington LS, Gautier J. 2011. Double-strand break end resection and repair pathway choice. Annu Rev Genet 45:247-71. doi: 10.1146/annurev-genet-110410-132435.
79. Taccioli GE, Gottlieb TM, Blunt T, Priestley A, Demengeot J, Mizuta R, et al. 1994. Ku80: product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science 265:1442-5. doi: 10.1126/science.8073286.
80. Taylor BJ, Nik-Zainal S, Wu YL, Stebbings LA, Raine K, Campbell PJ, et al. 2013. DNA deaminases induce break-associated mutation showers with implication of APOBEC3B and 3A in breast cancer kataegis. eLife 2:e00534. doi: 10.7554/eLife.00534.
81. Thaler DS, Stahl MM, Stahl FW. 1987. Evidence that the normal route of replication-allowed Red-mediated recombination involves double-chain ends. EMBO J 6:3171-6.
82. Torkelson J, Harris RS, Lombardo MJ, Nagendran J, Thulin C, Rosenberg SM. 1997. Genome-wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-dependent adaptive mutation. EMBO J 16:3303-11. doi: 10.1093/emboj/16.11.3303.
83. Traxler BA, Minkley EG Jnr. 1988. Evidence that DNA helicase I and oriT site-specific nicking are both functions of the F TraI protein. J Mol Biol 204:205-9. doi: 10.1016/0022-2836(88)90609-2.
84. Vilenchik MM, Knudson AG. 2003. Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc Natl Acad Sci USA 100:12871-6. doi: 10.1073/pnas.2135498100.
85. Wang X, Sherratt DJ. 2010. Independent segregation of the two arms of the Escherichia coli ori region requires neither RNA synthesis nor MreB dynamics. J Bacteriol 192:6143-53. doi: 10.1128/JB.00861-10.
86. Willetts NS, Clark AJ. 1969. Characteristics of some multiply recombination-deficient strains of Escherichia coli. J Bacteriol 100:231-9.
87. Williams JG, Radding CM. 1981. Partial purification and properties of an exonuclease inhibitor induced by bacteriophage Mu-1. J Virol 39:548-58.
88. Wimberly H, Shee C, Thornton PC, Sivaramakrishnan P, Rosenberg SM, Hastings PJ. 2013. R-loops and nicks initiate DNA breakage and genome instability in non-growing Escherichia coli. Nat Commun 4:2115. doi: 10.1038/ncomms3115.
89. Wojewodzka M, Buraczewska I, Kruszewski M. 2002. A modified neutral comet assay: elimination of lysis at high temperature and validation of the assay with anti-single-stranded DNA antibody. Mutat Res 518:9-20. doi: 10.1016/S1383-5718(02)00070-0.