2016, Number 1
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Biotecnol Apl 2016; 33 (1)
A homologous DNA recombination pathway alternative to RecFOR and RecBCD induced by gamma irradiation in Salmonella typhimurium
Cuétara E, Sánchez-Lamar A, Montero-Montoya J, Espinosa-Aguirre J, Camacho-Carranza R
Language: English
References: 61
Page: 1201-1207
PDF size: 367.61 Kb.
ABSTRACT
Understanding how cells repair DNA damage is a key issue in molecular and cell biology. Ionizing radiation induces DNA damage mainly repaired by a universal mechanism, homologous recombination (HR). Since DNA is chemically the same in all organisms and repair machinery is highly conserved, bacterial models are suitable for assaying genotoxicity, due to their plasticity and low cost. Traditionally, the assays that measure HR use double-strand ends to initiate the recombination events, favoring the RecBCD pathway. The present work was aimed to evaluate gamma rays-induced HR in
Salmonella typhimurium, in terms of segregation rates by means of the duplication-segregation assay (seg-dup), which does not favor any particular DNA repair pathway. RecA-independent recombination events were detected at high doses of gamma radiation (150 Gy), which were partially dependent on RecB, SbcCD and RecQ. The seg-dup assay was efficient to elucidate the proteins involved in repairing radiation induced injury. Moreover, due to its simplicity, low costs and the versatility of
S. typhimurium strains available, it could be useful to assess the mechanism of action of novel drugs that exert their action by interacting with cell HR machinery.
REFERENCES
Syeda AH, Hawkins M, McGlynn P. Recombination and replication. Cold Spring Harb Perspect Biol. 2014;6(11):a016550.
Ansari MA, Didelot X. Inference of the properties of the recombination process from whole bacterial genomes. Genetics. 2014;196(1):253-65.
Cox MM. Historical overview: searching for replication help in all of the rec places. Proc Natl Acad Sci USA. 2001;98(15):8173-80.
Michel B, Grompone G, Flores MJ, Bidnenko V. Multiple pathways process stalled replication forks. Proc Natl Acad Sci USA. 2004;101(35):12783-8.
Costes A, Lambert SA. Homologous recombination as a replication fork escort: fork-protection and recovery. Biomolecules. 2012;3(1):39-71.
Dillingham MS, Kowalczykowski SC. RecBCD enzyme and the repair of doublestranded DNA breaks. Microbiol Mol Biol Rev. 2008;72(4):642-71.
Pennington JM, Rosenberg SM. Spontaneous DNA breakage in single living Escherichia coli cells. Nat Genet. 2007;39(6):797-802.
West SC. Molecular views of recombination proteins and their control. Nat Rev Mol Cell Biol. 2003;4(6):435-45.
Otsuji N, Horiuchi T, Nakata A, Kawamata J. Strains of Escherichia coli hypersensitive to representative carcinostatic and carcinogenic agents. J Antibiot (Tokyo). 1978;31(8):794-6.
Kuipers GK, Poldervaart HA, Slotman BJ, Lafleur MV. The influence of formamidopyrimidine- DNA glycosylase on the spontaneous and gamma-radiation-induced mutation spectrum of the lacZ alpha gene. Mutat Res. 1999;435(2):141-50.
Dianov GL, O’Neill P, Goodhead DT. Securing genome stability by orchestrating DNA repair: removal of radiation-induced clustered lesions in DNA. Bioessays. 2001;23(8):745-9.
Volkert MR, Elliott NA, Housman DE. Functional genomics reveals a family of eukaryotic oxidation protection genes. Proc Natl Acad Sci USA. 2000;97(26):14530-5.
Blackwood JK, Rzechorzek NJ, Bray SM, Maman JD, Pellegrini L, Robinson NP. Endresection at DNA double-strand breaks in the three domains of life. Biochem Soc Trans. 2013;41(1):314-20.
Wigley DB. Bacterial DNA repair: recent insights into the mechanism of RecBCD, AddAB and AdnAB. Nat Rev Microbiol. 2013;11(1):9-13.
Hiom K. Homologous recombination: how RecA finds the perfect partner. Curr Biol. 2012;22(8):R275-8.
Danilowicz C, Peacock-Villada A, Vlassakis J, Facon A, Feinstein E, Kleckner N, et al. The differential extension in ds- DNA bound to Rad51 filaments may play important roles in homology recognition and strand exchange. Nucleic Acids Res. 2014;42(1):526-33.
Ames BN, Durston WE, Yamasaki E, Lee FD. Carcinogens are mutagens: a simple test system combining liver homogenates for activation and bacteria for detection. Proc Natl Acad Sci USA. 1973;70(8):2281-5.
Zieg J, Kushner SR. Analysis of genetic recombination between two partially deleted lactose operons of Escherichia coli K-12. J Bacteriol. 1977;131(1):123-32.
Miesel L, Roth JR. Salmonella recD mutations increase recombination in a short sequence transduction assay. J Bacteriol. 1994;176(13):4092-103.
Fernandez-Lopez R, Machon C, Longshaw CM, Martin S, Molin S, Zechner EL, et al. Unsaturated fatty acids are inhibitors of bacterial conjugation. Microbiology. 2005;151(Pt 11):3517-26.
Galitski T, Roth JR. Pathways for homologous recombination between chromosomal direct repeats in Salmonella typhimurium. Genetics. 1997;146(3):751- 67.
Cuétara EB, Sánchez-Lamar A, Hernández- Guadarrama BE, Espinosa-Aguirre JJ, Camacho-Carranza R. Collection of Salmonella typhimurium strains for genotoxicologic and anti-genotoxicologic evaluation. Biotecnol Apl. 2014;31(4):278-84.
Luria SE, Delbruck M. Mutations of bacteria from virus sensitivity to virus resistance. Genetics. 1943;28(6):491-511.
Espinosa-Aguirre J, Barajas-Lemus C, Hernandez-Ojeda S, Govezensky T, Rubio J, Camacho-Carranza R. RecBCD and Rec- FOR dependent induction of chromosomal deletions by sodium selenite in Salmonella. Mutat Res. 2009;665(1-2):14-9.
Lea DE, Coulson CA. The distribution of the numbers of mutants in bacterial populations. J Genet. 1949;49(3):264-85.
Hishida T, Han YW, Shibata T, Kubota Y, Ishino Y, Iwasaki H, et al. Role of the Escherichia coli RecQ DNA helicase in SOS signaling and genome stabilization at stalled replication forks. Genes Dev. 2004;18(15):1886-97.
Kushner SR, Nagaishi H, Templin A, Clark AJ. Genetic recombination in Escherichia coli: the role of exonuclease I. Proc Natl Acad Sci USA. 1971;68(4):824-7.
Lloyd RG, Buckman C. Identification and genetic analysis of sbcC mutations in commonly used recBC sbcB strains of Escherichia coli K-12. J Bacteriol. 1985;164(2) :836-44.
Ivancic-Bace I, Vlasic I, Salaj-Smic E, Brcic-Kostic K. Genetic evidence for the requirement of RecA loading activity in SOS induction after UV irradiation in Escherichia coli. J Bacteriol. 2006;188(14):5024-32.
McCool JD, Long E, Petrosino JF, Sandler HA, Rosenberg SM, Sandler SJ. Measurement of SOS expression in individual Escherichia coli K-12 cells using fluorescence microscopy. Mol Microbiol. 2004;53(5) :1343-57.
Jockovich ME, Myers RS. Nuclease activity is essential for RecBCD recombination in Escherichia coli. Mol Microbiol. 2001;41(4):949-62.
Dutra BE, Sutera VA Jr., Lovett ST. RecAindependent recombination is efficient but limited by exonucleases. Proc Natl Acad Sci USA. 2007;104(1):216-21.
Garriss G, Poulin-Laprade D, Burrus V. DNA-damaging agents induce the RecAindependent homologous recombination functions of integrating conjugative elements of the SXT/R391 family. J Bacteriol. 2013;195(9):1991-2003.
Kim JS, Rose AM. The effect of gamma radiation on recombination frequency in Caenorhabditis elegans. Genome. 1987;29(3):457-62.
Sutherland BM, Bennett PV, Sidorkina O, Laval J. Clustered damages and total lesions induced in DNA by ionizing radiation: oxidized bases and strand breaks. Biochemistry. 2000;39(27):8026-31.
Trampuz A, Piper KE, Steckelberg JM, Patel R. Effect of gamma irradiation on viability and DNA of Staphylococcus epidermidis and Escherichia coli. J Med Microbiol. 2006;55(Pt 9):1271-5.
Otsuji N, Iyehara H, Hideshima Y. Isolation and characterization of an Escherichia coli ruv mutant which forms nonseptate filaments after low doses of ultraviolet light irradiation. J Bacteriol. 1974;117(2):337-44.
Otsuji N, Iyehara-Ogawa H. Thermoresistant revertants of an Escherichia coli strain carrying tif-1 and ruv mutations: non-suppressibility of ruv by sfi. J Bacteriol. 1979;138(1):1-6.
Lloyd RG, Benson FE, Shurvinton CE. Effect of ruv mutations on recombination and DNA repair in Escherichia coli K12. Mol Gen Genet. 1984;194(1-2):303-9.
Lloyd RG, Buckman C, Benson FE. Genetic analysis of conjugational recombination in Escherichia coli K12 strains deficient in RecBCD enzyme. J Gen Microbiol. 1987;133(9):2531-8.
Sargentini NJ, Smith KC. Involvement of RecB-mediated (but not RecF-mediated) repair of DNA double-strand breaks in the gamma-radiation production of long deletions in Escherichia coli. Mutat Res. 1992;265(1):83-101.
Sargentini NJ, Smith KC. Role of ruvAB genes in UV- and gamma-radiation and chemical mutagenesis in Escherichia coli. Mutat Res. 1989;215(1):115-29.
Shiba T, Iwasaki H, Nakata A, Shinagawa H. SOS-inducible DNA repair proteins, RuvA and RuvB, of Escherichia coli: functional interactions between RuvA and RuvB for ATP hydrolysis and renaturation of the cruciform structure in supercoiled DNA. Proc Natl Acad Sci USA. 1991;88(19):8445-9.
Donaldson JR, Courcelle CT, Courcelle J. RuvAB and RecG are not essential for the recovery of DNA synthesis following UVinduced DNA damage in Escherichia coli. Genetics. 2004;166(4):1631-40.
Harris DR, Pollock SV, Wood EA, Goiffon RJ, Klingele AJ, Cabot EL, et al. Directed evolution of ionizing radiation resistance in Escherichia coli. J Bacteriol. 2009;191(16):5240-52.
Chedin F, Kowalczykowski SC. A novel family of regulated helicases/nucleases from Gram-positive bacteria: insights into the initiation of DNA recombination. Mol Microbiol. 2002;43(4):823-34.
Bibikova M, Carroll D, Segal DJ, Trautman JK, Smith J, Kim YG, et al. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol Cell Biol. 2001;21(1):289-97.
Lehman IR, Nussbaum AL. The deoxyribonucleases of Escherichia coli. V. On the specificity of Exonuclease I (phosphodiesterase). J Biol Chem. 1964;239:2628-36.
Ivankovic S, Dermic D. DNA end resection controls the balance between homologous and illegitimate recombination in Escherichia coli. PLoS One. 2012;7(6):e39030.
Bennett RJ, Keck JL. Structure and function of RecQ DNA helicases. Crit Rev Biochem Mol Biol. 2004;39(2):79-97.
Buljubasic M, Repar J, Zahradka K, Dermic D, Zahradka D. RecF recombination pathway in Escherichia coli cells lacking RecQ, UvrD and HelD helicases. DNA Repair (Amst). 2012;11(4):419-30.
Hishida T, Han YW, Shibata T, Kubota Y, Ishino Y, Iwasaki H, et al. Role of the Escherichia coli RecQ DNA helicase in SOS signaling and genome stabilization at stalled replication forks. Genes Dev. 2004;18(15) :1886-97.
Khan SR, Kuzminov A. Replication forks stalled at ultraviolet lesions are rescued via RecA and RuvABC protein-catalyzed disintegration in Escherichia coli. J Biol Chem. 2012;287(9):6250-65.
Zahradka D, Zahradka K, Petranovic M, Dermic D, Brcic-Kostic K. The RuvABC resolvase is indispensable for recombinational repair in sbcB15 mutants of Escherichia coli. J Bacteriol. 2002;184(15):4141-7.
Swingle B, Markel E, Costantino N, Bubunenko MG, Cartinhour S, Court DL. Oligonucleotide recombination in Gram-negative bacteria. Mol Microbiol. 2010;75(1):138-48.
Bierne H, Vilette D, Ehrlich SD, Michel B. Isolation of a dnaE mutation which enhances RecA-independent homologous recombination in the Escherichia coli chromosome. Mol Microbiol. 1997;24(6):1225-34.
Koskiniemi S, Andersson DI. Translesion DNA polymerases are required for spontaneous deletion formation in Salmonella typhimurium. Proc Natl Acad Sci USA. 2009;106(25):10248-53.
Sutherland JC. Repair-dependent cell radiation survival and transformation: an integrated theory. Phys Med Biol. 2014; 59(17):5073-90.
Ikeda H, Shiraishi K, Ogata Y. Illegitimate recombination mediated by double-strand break and end-joining in Escherichia coli. Adv Biophys. 2004;38:3-20.
Bowater R, Doherty AJ. Making ends meet: repairing breaks in bacterial DNA by non-homologous end-joining. PLoS Genet. 2006;2(2):e8.
Brena-Valle M, Serment-Guerrero J. SOS induction by gamma-radiation in Escherichia coli strains defective in repair and/or recombination mechanisms. Mutagenesis. 1998;13(6):637-41.