Recombinational branch migration by the RadA/Sms paralog of RecA in Escherichia coli

eLife

Volumn 5, Issue FEBRUARY2016, 2016, Pages

  Cooper, Deani L ^a   Lovett, Susan T ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA BINDING PROTEIN; DNA POLYMERASE; HETERODUPLEX; RAD A PROTEIN; RECA PROTEIN; SINGLE STRANDED DNA BINDING PROTEIN; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; MUTANT PROTEIN; RADA PROTEIN, E COLI;

ARTICLE; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; ENZYME ACTIVITY; ESCHERICHIA COLI; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; MOLECULAR CLONING; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN PURIFICATION; SITE DIRECTED MUTAGENESIS; DNA MUTATIONAL ANALYSIS; ENZYMOLOGY; GENETIC RECOMBINATION; GENETICS; METABOLISM;

DNA MUTATIONAL ANALYSIS; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MUTANT PROTEINS; RECOMBINATION, GENETIC;

EID: 84961275699     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.10807     Document Type: Article

References (76)

1. Abd Wahab S, Choi M, Bianco PR. 2013. Characterization of the ATPase activity of RecG and RuvAB proteins on model fork structures reveals insight into stalled DNA replication fork repair. The Journal of Biological Chemistry 288:26397-26409. doi: 10.1074/jbc.M113.500223
2. Adelman CA, Boulton SJ. 2010. Metabolism of postsynaptic recombination intermediates. FEBS Letters 584: 3709-3716. doi: 10.1016/j.febslet.2010.05.023
3. Anand RP, Lovett ST, Haber JE. 2013. Break-induced DNA replication. Cold Spring Harbor Perspectives in Biology 5:a010397. doi: 10.1101/cshperspect.a010397
4. Beam CE, Saveson CJ, Lovett ST. 2002. Role for radA/sms in recombination intermediate processing in escherichia coli. Journal of Bacteriology 184:6836-6844. doi: 10.1128/JB.184.24.6836-6844.2002
5. Bell JC, Plank JL, Dombrowski CC, Kowalczykowski SC. 2012. Direct imaging of RecA nucleation and growth on single molecules of SSB-coated ssDNA. Nature 491:274-278. doi: 10.1038/nature11598
6. Bernstein KA, Juanchich A, Sunjevaric I, Rothstein R. 2013. The shu complex regulates Rad52 localization during rDNA repair. DNA Repair 12:786-790. doi: 10.1016/j.dnarep.2013.05.003
7. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248-254. doi: 10.1016/0003-2697(76) 90527-3
8. Bugreeva IP, Bugreev DV, Nevinsky GA. 2005. Formation of nucleoprotein RecA filament on single-stranded DNA. analysis by stepwise increase in ligand complexity. The FEBS Journal 272:2734-2745. doi: 10.1111/j.1742-4658.2005.04693.x
9. Burghout P, Bootsma HJ, Kloosterman TG, Bijlsma JJ, de Jongh CE, Kuipers OP, Hermans PW. 2007. Search for genes essential for pneumococcal transformation: the RADA DNA repair protein plays a role in genomic recombination of donor DNA. Journal of Bacteriology 189:6540-6550. doi: 10.1128/JB.00573-07
10. Carrasco B, Cozar MC, Lurz R, Alonso JC, Ayora S. 2004. Genetic recombination in bacillus subtilis 168: contribution of holliday junction processing functions in chromosome segregation. Journal of Bacteriology 186: 5557-5566. doi: 10.1128/JB.186.17.5557-5566.2004
11. Castellanos M, Romero D. 2009. The extent of migration of the holliday junction is a crucial factor for gene conversion in rhizobium etli. Journal of Bacteriology 191:4987-4995. doi: 10.1128/JB.00111-09
12. Chen Z, Yang H, Pavletich NP. 2008. Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453:489-484. doi: 10.1038/nature06971
13. Chung CH, Goldberg AL. 1981. The product of the lon (capR) gene in escherichia coli is the ATP-dependent protease, protease la. Proceedings of the National Academy of Sciences of the United States of America 78: 4931-4935. doi: 10.1073/pnas.78.8.4931
14. Cooper DL, Boyle DC, Lovett ST. 2015. Genetic analysis of escherichia coli RadA: functional motifs and genetic interactions. Molecular Microbiology 95:769-779. doi: 10.1111/mmi.12899
15. Cox MM. 2007. Regulation of bacterial RecA protein function. Critical Reviews in Biochemistry and Molecular Biology 42:41-63. doi: 10.1080/10409230701260258
16. Diver WP, Sargentini NJ, Smith KC. 1982. A mutation (radA100) in escherichia coli that selectively sensitizes cells grown in rich medium to x- or U.V.-radiation, or methyl methanesulphonate. International Journal of Radiation Biology 42:339-346. doi: 10.1080/09553008214551251
17. Eggleston AK, Mitchell AH, West SC. 1997. In vitro reconstitution of the late steps of genetic recombination in e. coli. Cell 89:607-617. doi: 10.1016/S0092-8674(00)80242-1
18. Fagerburg MV, Schauer GD, Thickman KR, Bianco PR, Khan SA, Leuba SH, Anand SP. 2012. PcrA-mediated disruption of RecA nucleoprotein filaments-essential role of the ATPase activity of RecA. Nucleic Acids Research 40:8416-8424. doi: 10.1093/nar/gks641
19. Galletto R, Amitani I, Baskin RJ, Kowalczykowski SC. 2006. Direct observation of individual RecA filaments assembling on single DNA molecules. Nature 443:875-878. doi: 10.1038/nature05197
20. Gasior SL, Olivares H, Ear U, Hari DM, Weichselbaum R, Bishop DK. 2001. Assembly of RecA-like recombinases: distinct roles for mediator proteins in mitosis and meiosis. Proceedings of the National Academy of Sciences of the United States of America 98:8411-8418. doi: 10.1073/pnas.121046198
21. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins M, Appel R, Bairoch A. 2005. Protein identification and analysis tools on the ExPASy server. In: JM Walker (Ed). The Proteomics Protocols Handbook. New York, NY: Humana Press 571-607.
22. Giri N, Bhowmik P, Bhattacharya B, Mitra M, Das Gupta SK. 2009. The mycobacteriophage D29 gene 65 encodes an early-expressed protein that functions as a structure-specific nuclease. Journal of Bacteriology 191:959-967. doi: 10.1128/JB.00960-08
23. Haber JE, Ira G, Malkova A, Sugawara N. 2004. Repairing a double-strand chromosome break by homologous recombination: revisiting robin holliday’s model. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359:79-86. doi: 10.1098/rstb.2003.1367
24. Jain SK, Cox MM, Inman RB. 1994. On the role of ATP hydrolysis in RecA protein-mediated DNA strand exchange. III. unidirectional branch migration and extensive hybrid DNA formation. The Journal of Biological Chemistry 269:20653-20661.
25. Johnson RD, Symington LS. 1995. Functional differences and interactions among the putative RecA homologs Rad51, Rad55, and Rad57. Molecular and Cellular Biology 15:4843-4850. doi: 10.1128/MCB.15.9.4843
26. Kahn R, Radding CM. 1984. Separation of the presynaptic and synaptic phases of homologous pairing promoted by recA protein. The Journal of Biological Chemistry 259:7495-7503.
27. Kiianitsa K, Solinger JA, Heyer W-D. 2003. NADH-coupled microplate photometric assay for kinetic studies of ATP-hydrolyzing enzymes with low and high specific activities. Analytical Biochemistry 321:266-271. doi: 10.1016/S0003-2697(03)00461-5
28. Kornberg A, Scott JF, Bertsch LL. 1978. ATP utilization by rep protein in the catalytic separation of DNA strands at a replicating fork. The Journal of Biological Chemistry 253:3298-3304.
29. Kruger E, Msadek T, Ohlmeier S, Hecker M. 1997. The bacillus subtilis clpC operon encodes DNA repair and competence proteins. Microbiology 143:1309-1316. doi: 10.1099/00221287-143-4-1309
30. Lee JW, Cox MM. 1990a. Inhibition of RecA protein promoted ATP hydrolysis. 1. ATP.gamma.S and ADP are antagonistic inhibitors. Biochemistry 29:7666-7676. doi: 10.1021/bi00485a016
31. Lee JW, Cox MM. 1990b. Inhibition of RecA protein promoted ATP hydrolysis. 2. longitudinal assembly and disassembly of RecA protein filaments mediated by ATP and ADP. Biochemistry 29:7677-7683. doi: 10.1021/bi00485a017
32. Liu J, Renault L, Veaute X, Fabre F, Stahlberg H, Heyer WD. 2011. Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation. Nature 479:245-248. doi: 10.1038/nature10522
33. Liu Y, Masson JY, Shah R, O’Regan P, West SC. 2004. RAD51C is required for holliday junction processing in mammalian cells. Science 303:243-246. doi: 10.1126/science.1093037
34. Liu Y, Tarsounas M, O’regan P, West SC. 2007. Role of RAD51C and XRCC3 in genetic recombination and DNA repair. The Journal of Biological Chemistry 282:1973-1979. doi: 10.1074/jbc.M609066200
35. Lovett ST. 2006. Replication arrest-stimulated recombination: dependence on the RecA paralog, RadA/Sms and translesion polymerase, DinB. DNA Repair 5:1421-1427. doi: 10.1016/j.dnarep.2006.06.008
36. Marino-Ramirez L, Minor JL, Reading N, Hu JC. 2004. Identification and mapping of self-assembling protein domains encoded by the escherichia coli k-12 genome by use of repressor fusions. Journal of Bacteriology 186: 1311-1319. doi: 10.1128/JB.186.5.1311-1319.2004
37. Massoni SC, Leeson MC, Long JE, Gemme K, Mui A, Sandler SJ. 2012. Factors limiting SOS expression in log- phase cells of escherichia coli. Journal of Bacteriology 194:5325-5333. doi: 10.1128/JB.00674-12
38. Mazin AV, Kowalczykowski SC. 1996. The specificity of the secondary DNA binding site of RecA protein defines its role in DNA strand exchange. Proceedings of the National Academy of Sciences of the United States of America 93:10673-10678. doi: 10.1073/pnas.93.20.10673
39. Mazin AV, Kowalczykowski SC. 1998. The function of the secondary DNA-binding site of RecA protein during DNA strand exchange. The EMBO Journal 17:1161-1168. doi: 10.1093/emboj/17.4.1161
40. McEntee K, Weinstock GM, Lehman IR. 1981. Binding of the recA protein of escherichia coli to single- and double-stranded DNA. The Journal of Biological Chemistry 256:8835-8844.
41. Mills JB, Vacano E, Hagerman PJ. 1999. Flexibility of single-stranded DNA: use of gapped duplex helices to determine the persistence lengths of poly(dT) and poly(dA). Journal of Molecular Biology 285:245-257. doi: 10.1006/jmbi.1998.2287
42. Nassif N, Penney J, Pal S, Engels WR, Gloor GB. 1994. Efficient copying of nonhomologous sequences from ectopic sites via p-element-induced gap repair. Molecular and Cellular Biology 14:1613-1625. doi: 10.1128/MCB.14.3.1613
43. Park J, Myong S, Niedziela-Majka A, Lee KS, Yu J, Lohman TM, Ha T. 2010. PcrA helicase dismantles RecA filaments by reeling in DNA in uniform steps. Cell 142:544-555. doi: 10.1016/j.cell.2010.07.016
44. Parsons CA, Stasiak A, Bennett RJ, West SC. 1995. Structure of a multisubunit complex that promotes DNA branch migration. Nature 374:375-378. doi: 10.1038/374375a0
45. Parsons CA, West SC. 1993. Formation of a RuvAB-holliday junction complex in vitro. Journal of Molecular Biology 232:397-405. doi: 10.1006/jmbi.1993.1399
46. Patel M, Jiang Q, Woodgate R, Cox MM, Goodman MF. 2010. A new model for SOS-induced mutagenesis: how RecA protein activates DNA polymerase v. Critical Reviews in Biochemistry and Molecular Biology 45:171-184. doi: 10.3109/10409238.2010.480968
47. Perrotti N, Accili D, Marcus-Samuels B, Rees-Jones RW, Taylor SI. 1987. Insulin stimulates phosphorylation of a 120-kDa glycoprotein substrate (pp120) for the receptor-associated protein kinase in intact h-35 hepatoma cells. Proceedings of the National Academy of Sciences of the United States of America 84:3137-3140. doi: 10.1073/pnas.84.10.3137
48. Persky NS, Lovett ST. 2008. Mechanisms of recombination: lessons from e. coli. Critical Reviews in Biochemistry and Molecular Biology 43:347-370. doi: 10.1080/10409230802485358
49. Petrova V, Chen SH, Molzberger ET, Tomko E, Chitteni-Pattu S, Jia H, Ordabayev Y, Lohman TM, Cox MM. 2015. Active displacement of RecA filaments by UvrD translocase activity. Nucleic Acids Research 43:4133- 4149. doi: 10.1093/nar/gkv186
50. Piechura JR, Tseng TL, Hsu HF, Byrne RT, Windgassen TA, Chitteni-Pattu S, Battista JR, Li HW, Cox MM. 2015. Biochemical characterization of RecA variants that contribute to extreme resistance to ionizing radiation. DNA Repair 26:30-43. doi: 10.1016/j.dnarep.2014.12.001
51. Prentiss M, Prévost C, Danilowicz C. 2015. Structure/function relationships in RecA protein-mediated homology recognition and strand exchange. Critical Reviews in Biochemistry and Molecular Biology 50:453-476. doi: 10.3109/10409238.2015.1092943
52. Qing Y, Yamazoe M, Hirota K, Dejsuphong D, Sakai W, Yamamoto KN, Bishop DK, Wu X, Takeda S. 2011. The epistatic relationship between BRCA2 and the other RAD51 mediators in homologous recombination. PLoS Genetics 7:e1002148. doi: 10.1371/journal.pgen.1002148
53. Radding CM, Flory J, Wu A, Kahn R, DasGupta C, Gonda D, Bianchi M, Tsang SS. 1983. Three phases in homologous pairing: polymerization of recA protein on single-stranded DNA, synapsis, and polar strand exchange. Cold Spring Harbor Symposia on Quantitative Biology 47:821-828. doi: 10.1101/SQB.1983.047.01.094
54. Rehrauer WM, Kowalczykowski SC. 1993. Alteration of the nucleoside triphosphate (nTP) catalytic domain within escherichia coli recA protein attenuates NTP hydrolysis but not joint molecule formation. The Journal of Biological Chemistry 268:1292-1297.
55. Seitz EM, Brockman JP, Sandler SJ, Clark AJ, Kowalczykowski SC. 1998. RadA protein is an archaeal RecA protein homolog that catalyzes DNA strand exchange. Genes & Development 12:1248-1253. doi: 10.1101/gad.12.9.1248
56. Shah R, Bennett RJ, West SC. 1994. Genetic recombination in e. coli: RuvC protein cleaves holliday junctions at resolution hotspots in vitro. Cell 79:853-864. doi: 10.1016/0092-8674(94)90074-4
57. Shan Q, Cox MM, Inman RB. 1996. DNA strand exchange promoted by RecA K72R: TWO REACTION PHASES with DIFFERENT mg REQUIREMENTS. Journal of Biological Chemistry 271:5712-5724. doi: 10.1074/jbc.271.10.5712
58. Sheng D, Zhu S, Wei T, Ni J, Shen Y. 2008. The in vitro activity of a Rad55 homologue from sulfolobus tokodaii, a candidate mediator in RadA-catalyzed homologous recombination. Extremophiles 12:147-157. doi: 10.1007/s00792-007-0113-y
59. Shida T, Iwasaki H, Shinagawa H, Kyogoku Y. 1995. Structural requirement of four-way junction DNA for binding to and cleavage by RuvC. Nucleic Acids Symposium Series:5-6.
60. Simmons LA, Foti JJ, Cohen SE, Walker GC. 2008. The SOS regulatory network. EcoSal Plus
61. Slade D, Lindner AB, Paul G, Radman M. 2009. Recombination and replication in DNA repair of heavily irradiated deinococcus radiodurans. Cell 136:1044-1055. doi: 10.1016/j.cell.2009.01.018
62. Song Y, Sargentini NJ. 1996. Escherichia coli DNA repair genes radA and sms are the same gene. Journal of Bacteriology 178:5045-5048.
63. Sung P. 1997. Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein a to promote DNA strand exchange by Rad51 recombinase. Genes & Development 11:1111-1121. doi: 10.1101/gad.11.9.1111
64. Suwaki N, Klare K, Tarsounas M. 2011. RAD51 paralogs: roles in DNA damage signalling, recombinational repair and tumorigenesis. Seminars in Cell & Developmental Biology 22:898-905. doi: 10.1016/j.semcdb.2011.07.019
65. Taylor MR, pírek M, Chaurasiya KR, Ward JD, Carzaniga R, Yu X, Egelman EH, Collinson LM, Rueda D, Krejci L, Boulton SJ. 2015. Rad51 paralogs remodel pre-synaptic Rad51 filaments to stimulate homologous recombination. Cell 162:271-286. doi: 10.1016/j.cell.2015.06.015
66. Tsaneva IR, Muller B, West SC. 1993. RuvA and RuvB proteins of escherichia coli exhibit DNA helicase activity in vitro. Proceedings of the National Academy of Sciences of the United States of America 90:1315-1319. doi: 10.1073/pnas.90.4.1315
67. Uranga LA, Balise VD, Benally CV, Grey A, Lusetti SL. 2011. The escherichia coli DinD protein modulates RecA activity by inhibiting postsynaptic RecA filaments. The Journal of Biological Chemistry 286:29480-29491. doi: 10.1074/jbc.M111.245373
68. Weinstock GM, McEntee K, Lehman IR. 1981. Hydrolysis of nucleoside triphosphates catalyzed by the recA protein of escherichia coli. steady state kinetic analysis of ATP hydrolysis. The Journal of Biological Chemistry 256:8845-8849.
69. West SC. 1997. Processing of recombination intermediates by the RuvABC proteins. Annual Review of Genetics 31:213-244. doi: 10.1146/annurev.genet.31.1.213
70. Whitby MC, Lloyd RG. 1998. Targeting holliday junctions by the RecG branch migration protein of escherichia coli. The Journal of Biological Chemistry 273:19729-19739.
71. Whitby MC, Ryder L, Lloyd RG. 1993. Reverse branch migration of holliday junctions by RecG protein: a new mechanism for resolution of intermediates in recombination and DNA repair. Cell 75:341-350. doi: 10.1016/0092-8674(93)80075-P
72. Wu AM, Kahn R, DasGupta C, Radding CM. 1982. Formation of nascent heteroduplex structures by RecA protein and DNA. Cell 30:37-44. doi: 10.1016/0092-8674(82)90009-5
73. Wu Y, He Y, Moya IA, Qian X, Luo Y. 2004. Crystal structure of archaeal recombinase RADA: a snapshot of its extended conformation. Molecular Cell 15:423-435. doi: 10.1016/j.molcel.2004.07.014
74. Yamada K, Miyata T, Tsuchiya D, Oyama T, Fujiwara Y, Ohnishi T, Iwasaki H, Shinagawa H, Ariyoshi M, Mayanagi K, Morikawa K. 2002. Crystal structure of the RuvA-RuvB complex. Molecular Cell 10:671-681. doi: 10.1016/S1097-2765(02)00641-X
75. Yang S, Yu X, Seitz EM, Kowalczykowski SC, Egelman EH. 2001. Archaeal RadA protein binds DNA as both helical filaments and octameric rings. Journal of Molecular Biology 314:1077-1085. doi: 10.1006/jmbi.2000.5213
76. Zahradka K, Slade D, Bailone A, Sommer S, Averbeck D, Petranovic M, Lindner AB, Radman M. 2006. Reassembly of shattered chromosomes in deinococcus radiodurans. Nature 443:569-573. doi: 10.1038/nature05160