Purification and characterization of the RecA protein from Neisseria gonorrhoeae

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Stohl, Elizabeth A ^a   Gruenig, Marielle C ^b   Cox, Michael M ^b   Seifert, H Steven ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; LEXA PROTEIN; MAGNESIUM ION; PILIN; PROTEIN SSB; RECA PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; LEXA PROTEIN, BACTERIA; MAGNESIUM; RECOMBINANT PROTEIN; SERINE PROTEINASE;

ANTIGENIC VARIATION; ARTICLE; BIOCATALYSIS; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE OVEREXPRESSION; GENETIC IDENTIFICATION; IN VITRO STUDY; MOLECULAR CLONING; NEISSERIA GONORRHOEAE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; SEQUENCE HOMOLOGY; AMINO ACID SEQUENCE; BASE PAIRING; CHEMISTRY; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

NEISSERIA GONORRHOEAE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE PAIRING; BASE SEQUENCE; CLONING, MOLECULAR; DNA, SINGLE-STRANDED; HUMANS; MAGNESIUM; MOLECULAR SEQUENCE DATA; NEISSERIA GONORRHOEAE; REC A RECOMBINASES; RECOMBINANT PROTEINS; SERINE ENDOPEPTIDASES;

EID: 79951988786     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017101     Document Type: Article

References (76)

1. Lusetti SL, Cox MM, (2002) The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu Rev Biochem 71: 71-100.
2. Kowalczykowski SC, Dixon DA, Eggleston AK, Lauder SD, Rehrauer WM, (1994) Biochemistry of homologous recombination in Escherichia coli. [Review]. Microbiol Rev 94: 401-465.
3. Roca AI, Cox MM, (1997) RecA protein: structure, function, and role in recombinational DNA repair. Prog Nucleic Acid Res Mol Biol 56: 129-223.
4. Brenner SL, Mitchell RS, Morrical SW, Neuendorf SK, Schutte BC, et al. (1987) recA protein-promoted ATP hydrolysis occurs throughout recA nucleoprotein filaments. J Biol Chem 262: 4011-4016.
5. Shan Q, Cox MM, (1997) RecA filament dynamics during DNA strand exchange reactions. J Biol Chem 272: 11063-11073.
6. Arenson TA, Tsodikov OV, Cox MM, (1999) Quantitative analysis of the kinetics of end-dependent disassembly of RecA filaments from ssDNA. J Mol Biol 288: 391-401.
7. Bork JM, Cox MM, Inman RB, (2001) RecA protein filaments disassemble in the 5′ to 3′ direction on single-stranded DNA. J Biol Chem 276: 45740-45743.
8. Menetski JP, Bear DG, Kowalczykowski SC, (1990) Stable DNA heteroduplex formation catalyzed by the Escherichia coli RecA protein in the absence of ATP hydrolysis. Proc Natl Acad Sci U S A 87: 21-25.
9. 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. J Biol Chem 268: 1292-1297.
10. Kowalczykowski SC, Krupp RA, (1995) DNA-strand exchange promoted by RecA protein in the absence of ATP: implications for the mechanism of energy transduction in protein-promoted nucleic acid transactions. Proc Natl Acad Sci U S A 92: 3478-3482.
11. 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. J Biol Chem 269: 20653-20661.
12. Kim JI, Cox MM, Inman RB, (1992) On the role of ATP hydrolysis in RecA protein-mediated DNA strand exchange. I. Bypassing a short heterologous insert in one DNA substrate. J Biol Chem 267: 16438-16443.
13. Shan Q, Cox MM, Inman RB, (1996) DNA strand exchange promoted by RecA K72R. Two reaction phases with different Mg2+ requirements. J Biol Chem 271: 5712-5724.
14. Fernandez De Henestrosa AR, Ogi T, Aoyagi S, Chafin D, Hayes JJ, et al. (2000) Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol Microbiol 35: 1560-1572.
15. Pham P, Rangarajan S, Woodgate R, Goodman MF, (2001) Roles of DNA polymerases V and II in SOS-induced error-prone and error-free repair in Escherichia coli. Proc Natl Acad Sci U S A 98: 8350-8354.
16. Goodman MF, (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu Rev Biochem 71: 17-50.
17. Jiang Q, Karata K, Woodgate R, Cox MM, Goodman MF, (2009) The active form of DNA polymerase V is UmuD'2C-RecA-ATP. Nature 460: 359-363.
18. Lohman TM, Ferrari ME, (1994) Escherichia coli single-stranded DNA-binding protein: multiple DNA-binding modes and cooperativities. Annu Rev Biochem 63: 527-570.
19. Alani E, Thresher R, Griffith JD, Kolodner RD, (1992) Characterization of DNA-binding and strand-exchange stimulation properties of y-RPA, a yeast single-strand-DNA-binding protein. J Mol Biol 227: 54-71.
20. Steffen SE, Bryant FR, (2001) Purification and characterization of the single-stranded DNA binding protein from Streptococcus pneumoniae. Arch Biochem Biophys 388: 165-170.
21. Eggington JM, Haruta N, Wood EA, Cox MM, (2004) The single-stranded DNA-binding protein of Deinococcus radiodurans. BMC Microbiol 4: 2.
22. Steffen SE, Bryant FR, (2000) Purification and characterization of the RecA protein from Streptococcus pneumoniae. Arch Biochem Biophys 382: 303-309.
23. Kim JI, Cox MM, (2002) The RecA proteins of Deinococcus radiodurans and Escherichia coli promote DNA strand exchange via inverse pathways. Proc Natl Acad Sci U S A 99: 7917-7921.
24. Kowalczykowski SC, Krupp RA, (1987) Effects of Escherichia coli SSB protein on the single-stranded DNA-dependent ATPase activity of Escherichia coli RecA protein. Evidence that SSB protein facilitates the binding of RecA protein to regions of secondary structure within single-stranded DNA. J Mol Biol 193: 97-113.
25. Lavery PE, Kowalczykowski SC, (1992) A postsynaptic role for single-stranded DNA-binding protein in RecA protein-promoted DNA strand exchange. J Biol Chem 267: 9315-9320.
26. Beernink HT, Morrical SW, (1999) RMPs: recombination/replication mediator proteins. Trends Biochem Sci 24: 385-389.
27. Koomey M, Gotschlich EC, Robbins K, Bergstrom S, Swanson J, (1987) Effects of recA mutations on pilus antigenic variation and phase transitions in Neisseria gonorrhoeae. Genetics 117: 391-398.
28. Koomey JM, Falkow S, (1987) Cloning of the recA gene of Neisseria gonorrhoeae and construction of gonococcal recA mutants. J Bacteriol 169: 790-795.
29. Mehr IJ, Seifert HS, (1998) Differential roles of homologous recombination pathways in Neisseria gonorrhoeae pilin antigenic variation, DNA transformation, and DNA repair. Mol Microbiol 30: 697-710.
30. Stohl EA, Seifert HS, (2001) The recX gene potentiates homologous recombination in Neisseria gonorrhoeae. Mol Microbiol 40: 1301-1310.
31. Skaar EP, Lazio MP, Seifert HS, (2002) Roles of the recJ and recN genes in homologous recombination and DNA repair pathways of Neisseria gonorrhoeae. J Bacteriol 184: 919-927.
32. Kline KA, Sechman EV, Skaar EP, Seifert HS, (2003) Recombination, repair and replication in the pathogenic Neisseriae: the 3 R's of molecular genetics of two human-specific bacterial pathogens. Mol Microbiol 50: 3-13.
33. Biswas GD, Sox T, Blackman E, Sparling PF, (1977) Factors affecting genetic transformation of Neisseria gonorrhoeae. J Bacteriol 129: 983-992.
34. Elkins C, Thomas CE, Seifert HS, Sparling PF, (1991) Species-specific uptake of DNA by gonococci is mediated by a 10- base-pair sequence. J Bacteriol 173: 3911-3913.
35. Goodman SD, Scocca JJ, (1991) Factors influencing the specific interaction of Neisseria gonorrhoeae with transforming DNA. J Bacteriol 173: 5921-5923.
36. Hamilton HL, Dillard JP, (2006) Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol Microbiol 59: 376-385.
37. Kline KA, Seifert HS, (2005) Role of the Rep helicase gene in homologous recombination in Neisseria gonorrhoeae. J Bacteriol 187: 2903-2907.
38. Kline KA, Seifert HS, (2005) Mutation of the priA gene of Neisseria gonorrhoeae affects DNA transformation and DNA repair. J Bacteriol 187: 5347-5355.
39. Spratt BG, Zhang QY, Jones DM, Hutchison A, Brannigan JA, et al. (1989) Recruitment of a penicillin-binding protein gene from Neisseria flavescens during the emergence of penicillin resistance in Neisseria meningitidis. Proc Natl Acad Sci U S A 86: 8988-8992.
40. Seifert HS, Ajioka RS, Marchal C, Sparling PF, So M, (1988) DNA transformation leads to pilin antigenic variation in Neisseria gonorrhoeae. Nature 336: 392-395.
41. Howell-Adams B, Seifert HS, (2000) Molecular models accounting for the gene conversion reactions mediating gonococcal pilin antigenic variation. Mol Microbiol 37: 1146-1159.
42. Criss AK, Kline KA, Seifert HS, (2005) The frequency and rate of pilin antigenic variation in Neisseria gonorrhoeae. Mol Microbiol 58: 510-519.
43. Helm RA, Seifert HS, (2009) Pilin antigenic variation occurs independently of the RecBCD pathway in Neisseria gonorrhoeae. J Bacteriol 191: 5613-5621.
44. Sechman EV, Rohrer MS, Seifert HS, (2005) A genetic screen identifies genes and sites involved in pilin antigenic variation in Neisseria gonorrhoeae. Mol Microbiol 57: 468-483.
45. Mehr IJ, Long CD, Serkin CD, Seifert HS, (2000) A homologue of the recombination-dependent growth gene, rdgC, is involved in gonococcal pilin antigenic variation. Genetics 154: 523-532.
46. Campbell LA, Yasbin RE, (1984) Mutagenesis of Neisseria gonorrhoeae: absence of error-prone repair. J Bacteriol 160: 288-293.
47. Black CG, Fyfe JA, Davies JK, (1998) Absence of an SOS-like system in Neisseria gonorrhoeae. Gene 208: 61-66.
48. Stohl EA, Seifert HS, (2006) Neisseria gonorrhoeae DNA recombination and repair enzymes protect against oxidative damage caused by hydrogen peroxide. J Bacteriol 188: 7645-7651.
49. Kelley WL, (2006) Lex marks the spot: the virulent side of SOS and a closer look at the LexA regulon. Mol Microbiol 62: 1228-1238.
50. Schook POP, Stohl EA, Criss AK, Seifert HS, (2010) The DNA-binding activity of the Neisseria gonorrhoeae LexA orthologue NG1427 is modulated by oxidation. Mol Microbiol.
51. Fyfe JA, Davies JK, (1990) Nucleotide sequence and expression in Escherichia coli of the recA gene of Neisseria gonorrhoeae. Gene 93: 151-156.
52. Miller RV, Kokjohn TA, (1990) General microbiology of recA: Environmental and evolutionary significance. Ann Rev Microbiol 44: 365-394.
53. Shibata T, DasGupta C, Cunningham RP, Radding CM, (1979) Purified Escherichia coli RecA protein catalyzes homologous pairing of superhelical DNA and single-stranded fragments. Proc Natl Acad Sci U S A 76: 1638-1642.
54. Cox MM, Lehman IR, (1982) RecA protein-promoted DNA strand exchange. Stable complexes of RecA protein and single-stranded DNA formed in the presence of ATP and single-stranded DNA binding protein. J Biol Chem 257: 8523-8532.
55. Morrical SW, Lee J, Cox MM, (1986) Continuous association of Escherichia coli single-stranded DNA binding protein with stable complexes of RecA protein and single-stranded DNA. Biochemistry 25: 1482-1494.
56. Lindsley JE, Cox MM, (1990) Assembly and disassembly of RecA protein filaments occur at opposite filament ends. Relationship to DNA strand exchange. J Biol Chem 265: 9043-9054.
57. Cox MM, Lehman IR, (1981) RecA protein of Escherichia coli promotes branch migration, a kinetically distinct phase of DNA strand exchange. Proc Natl Acad Sci U S A 78: 3433-3437.
58. Kim JI, Sharma AK, Abbott SN, Wood EA, Dwyer DW, et al. (2002) RecA Protein from the extremely radioresistant bacterium Deinococcus radiodurans: expression, purification, and characterization. J Bacteriol 184: 1649-1660.
59. Haruta N, Yu X, Yang S, Egelman EH, Cox MM, (2003) A DNA pairing-enhanced conformation of bacterial RecA proteins. J Biol Chem 278: 52710-52723.
60. Britt RL, Haruta N, Lusetti SL, Chitteni-Pattu S, Inman RB, et al. Disassembly of Escherichia coli RecA E38K/DeltaC17 nucleoprotein filaments is required to complete DNA strand exchange. J Biol Chem 285: 3211-3226.
61. Seifert HS, Wright CJ, Jerse AE, Cohen MS, Cannon JG, (1994) Multiple gonococcal pilin antigenic variants are produced during experimental human infections. J Clin Invest 93: 2744-2749.
62. Pierre A, Paoletti C, (1983) Purification and characterization of RrecA protein from Salmonella typhimurium. J Biol Chem 258: 2870-2874.
63. Lovett CM Jr, Roberts JW, (1985) Purification of a RecA protein analogue from Bacillus subtilis. J Biol Chem 260: 3305-3313.
64. Kato R, Kuramitsu S, (1993) RecA protein from an extremely thermophilic bacterium, Thermus thermophilus HB8. J Biochem 114: 926-929.
65. Ganesh N, Muniyappa K, (2003) Characterization of DNA strand transfer promoted by Mycobacterium smegmatis RecA reveals functional diversity with Mycobacterium tuberculosis RecA. Biochemistry 42: 7216-7225.
66. Baitin DM, Zaitsev EN, Lanzov VA, (2003) Hyper-recombinogenic RecA protein from Pseudomonas aeruginosa with enhanced activity of its primary DNA binding site. J Mol Biol 328: 1-7.
67. Stohl EA, Blount L, Seifert HS, (2002) Differential cross-complementation patterns of Escherichia coli and Neisseria gonorrhoeae RecA proteins. Microbiology 148: 1821-1831.
68. Lusetti SL, Shaw JJ, Cox MM, (2003) Magnesium ion-dependent activation of the RecA protein involves the C terminus. J Biol Chem 278: 16381-16388.
69. McGrew DA, Knight KL, (2003) Molecular design and functional organization of the RecA protein. Crit Rev Biochem Mol Biol 38: 385-432.
70. Gruenig MC, Stohl EA, Chitteni-Pattu S, Seifert HS, Cox MM, Less is more: Neisseria gonorrhoeae RecX protein stimulates recombination by inhibiting RecA. J Biol Chem 285: 37188-37197.
71. Petrova V, Chitteni-Pattu S, Drees JC, Inman RB, Cox MM, (2009) An SOS inhibitor that binds to free RecA protein: the PsiB protein. Mol Cell 36: 121-130.
72. Gruenig MC, Renzette N, Long E, Chitteni-Pattu S, Inman RB, et al. (2008) RecA-mediated SOS induction requires an extended filament conformation but no ATP hydrolysis. Mol Microbiol 69: 1165-1179.
73. Kellogg DS Jr, Peacock WL Jr, Deacon WE, Brown L, Pirkle DI, (1963) Neisseria gonorrhoeae. I. Virulence Genetically Linked to Clonal Variation. J Bacteriol 85: 1274-1279.
74. Messing J, (1983) New M13 vectors for cloning. Methods Enzymol 101: 20-78.
75. Neuendorf SK, Cox MM, (1986) Exchange of RecA protein between adjacent RecA protein-single-stranded DNA complexes. J Biol Chem 261: 8276-8282.
76. Seifert HS, (1997) Insertionally inactivated and inducible recA alleles for use in Neisseria. Gene 188: 215-220.