DNA helicase activity of PcrA is not required for the displacement of RecA protein from DNA or inhibition of RecA-mediated strand exchange

Journal of Bacteriology

Volumn 189, Issue 12, 2007, Pages 4502-4509

  Anand, Syam P ^a   Zheng, Haocheng ^b   Bianco, Piero R ^c   Leuba, Sanford H ^b   Khan, Saleem A ^a,d  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

^d East 1240 Biomedical Science Tower ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DOUBLE STRANDED DNA; HELICASE; PCRA PROTEIN; PHOSPHORUS 32; RECA PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; DNA BINDING; ENZYME ACTIVITY; ENZYME ASSAY; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; GRAM POSITIVE BACTERIUM; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PURIFICATION; SITE DIRECTED MUTAGENESIS; STAPHYLOCOCCUS AUREUS;

BACTERIAL PROTEINS; DNA HELICASES; DNA, BACTERIAL; DNA, SINGLE-STRANDED; FLUORESCENCE RESONANCE ENERGY TRANSFER; GRAM-POSITIVE BACTERIA; MUTATION; REC A RECOMBINASES; RECOMBINATION, GENETIC;

POSIBACTERIA;

EID: 34250305132     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00376-07     Document Type: Article

References (50)

1. Aguilera, A. 2001. Double-strand break repair: are Rad51/RecA-DNA joints barriers to DNA replication? Trends Genet. 17:318-321.
2. Anand, S. P., A. Chattopadhyay, and S. A. Khan. 2005. The PcrA3 mutant binds DNA and interacts with the RepC initiator protein of plasmid pT181 but is defective in its DNA helicase and unwinding activities. Plasmid 54:104-113.
3. Anand, S. P., and S. A. Khan. 2004. Structure-specific DNA binding and bipolar helicase activities of PcrA. Nucleic Acids Res. 32:3190-3197.
4. Anand, S. P., P. Mitra, A. Naqvi, and S. A. Khan. 2004. Bacillus anthracis and Bacillus cereus PcrA helicases can support DNA unwinding and in vitro rolling-circle replication of plasmid pT181 of Staphylococcus aureus. J. Bacteriol. 186:2195-2199.
5. Bianco, P. R., and G. M. Weinstock. 1996. Interaction of the RecA protein of Escherichia coli with single-stranded oligodeoxyribonucleotides. Nucleic Acids Res. 24:4933-4939.
6. Bork, J. M., M. M. Cox, and R. B. Inman. 2001. The RecOR proteins modulate RecA protein function at 5′ ends of single-stranded DNA. EMBO J. 20:7313-7322.
7. Chang, T. L., A. Naqvi, S. P. Anand, M. G. Kramer, R. Munshi, and S. A. Khan. 2002. Biochemical characterization of the Staphylococcus aureus PcrA helicase and its role in plasmid rolling circle replication. J. Biol. Chem. 277:45880-45886.
8. Colasanti, J., and D. T. Denhardt. 1987. The Escherichia coli rep mutation. X. Consequences of increased and decreased Rep protein levels. Mol. Gen. Genet. 209:382-390.
9. Cox, J. M., O. V. Tsodikov, and M. M. Cox. 2005. Organized unidirectional waves of ATP hydrolysis within a RecA filament. PLoS Biol. 3:231-243.
10. Cox, M. M. 2003. The bacterial RecA protein as a motor protein. Annu. Rev. Microbiol. 57:551-577.
11. Cox, M. M., and I. R. Lehman. 1981. recA protein of Escherichia coli promotes branch migration, a kinetically distinct phase of DNA strand exchange. Proc. Natl. Acad. Sci. USA 78:3433-3437.
12. Datta, S., N. Ganesh, N. R. Chandra, K. Muniyappa, and M. Vijayan. 2003. Structural studies on MtRecA-nucleotide complexes: insights into DNA and nucleotide binding and the structural signature of NTP recognition. Proteins 50:474-485.
13. de Vos, W. M., S. C. de Vries, and G. Venema. 1983. Cloning and expression of the Escherichia coli recA gene in Bacillus subtilis. Gene 25:301-308.
14. Dillingham, M. S., P. Soultanas, and D. B. Wigley. 1999. Site-directed mutagenesis of motif III in PcrA helicase reveals a role in coupling ATP hydrolysis to strand separation. Nucleic Acids Res. 27:3310-3317.
15. Drees, J. C., S. Chitteni-Pattu, D. R. McCaslin, R. B. Inman, and M. M. Cox. 2006. Inhibition of RecA protein function by the RdgC protein from Escherichia coli. J. Biol. Chem. 281:4708-4717.
16. Drees, J. C., S. L. Lusetti, S. Chitteni-Pattu, R. B. Inman, and M. M. Cox. 2004. A RecA filament capping mechanism for RecX protein. Mol. Cell 15:789-798.
17. Egelman, E. H. 1998. Bacterial helicases. J. Struct. Biol. 124:123-128.
18. Hall, M. C., and S. W. Matson. 1999. Helicase motifs: the engine that powers DNA unwinding. Mol. Microbiol. 34:867-877.
19. Holmberg, A., A. Blomstergren, O. Nord, M. Lukacs, J. Lundeberg, and M. Uhlen. 2005. The biotin-streptavidin interaction can be reversibly broken using water at elevated temperatures. Electrophoresis 26:501-510.
20. Iordanescu, S. 1993. Characterization of the Staphylococcus aureus chromosomal gene pcrA, identified by mutations affecting plasmid pT181 replication. Mol. Gen. Genet. 241:185-192.
21. Ji, Y., B. Zhang, S. F. Van Horn, P. Warren, G. Woodnutt, M. K. R. Burnham, and M. Rosenberg. 2001. Identification of critical staphylococcal genes using conditional phenotypes generated by antisense RNA. Science 293:2266-2269.
22. Kelley De Zutter, J., A. L. Forget, K. M. Logan, and K. L. Knight. 2001. Phe217 regulates the transfer of allosteric information across the subunit interface of the RecA protein filament. Structure 9:47-55.
23. Kelley, J. A., and K. L. Knight. 1997. Allosteric regulation of RecA protein function is mediated by Gln194. J. Biol. Chem. 272:25778- 25782.
24. Kornberg, A., and T. Baker. 1992. DNA replication, 2nd ed. W. H. Freeman & Co., New York, NY.
25. Kowalczykowski, S. C. 1991. Biochemistry of genetic recombination: energetics and mechanism of DNA strand exchange. Annu. Rev. Biophys. Biophys. Chem. 20:539-575.
26. Krejci, L., M. Macris, Y. Li, S. Van Komen, J. Villemain, T. Ellenberger, H. Klein, and P. Sung. 2004. Role of ATP hydrolysis in the antirecombinase function of Saccharomyces cerevisiae Srs2 protein. J. Biol. Chem. 279:23193-23199.
27. Krejci, L., S. Van Komen, Y. Li, J. Villemain, M. S. Reddy, H. Klein, T. Ellenberger, and P. Sung. 2003. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423:305-309.
28. Lindsley, J. E., and M. M. Cox. 1990. Assembly and disassembly of RecA protein filaments occur at opposite filament ends. Relationship to DNA strand exchange. J. Biol. Chem. 265:9043-9054.
29. Lo, Y. C., K. S. Paffett, O. Amit, J. A. Clikeman, R. Sterk, M. A. Brenneman, and J. A. Nickoloff. 2006. Sgs1 regulates gene conversion tract lengths and crossovers independently of its helicase activity. Mol. Cell. Biol. 26:4086-4094.
30. Lohmann, T. M., and M. E. Ferrari. 1994. Escherichia coli single-stranded DNA binding protein: multiple DNA-binding modes and cooperativities. Annu. Rev. Biochem. 63:527-570.
31. McGrew, D. A., and K. L. Knight. 2003. Molecular design and functional organization of the RecA protein. Crit. Rev. Biochem. Mol. Biol. 38:385-432.
32. Menetski, J. P., and S. C. Kowalczykowski. 1989. Enhancement of Escherichia coli RecA protein enzymatic function by dATP. Biochemistry 28:5871-5881.
33. Morimatsu, K., and S. C. Kowalczykowski. 2003. RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol. Cell 11:1337-1347.
34. Myong, S., I. Rasnik, C. Joo, T. M. Lohman, and T. Ha. 2005. Repetitive shuttling of a motor protein on DNA. Nature 437:1321-1325.
35. Naqvi, A., E. Tinsley, and S. A. Khan. 2003. Purification and characterization of the PcrA helicase of Bacillus anthracis. J. Bacteriol. 185:6633-6639.
36. Petit, M. A., E. Dervyn, M. Rose, K. D. Entian, S. McGovern, S. D. Ehrlich, and C. Bruand. 1998. PcrA is an essential DNA helicase of Bacillus subtilis fulfilling functions both in repair and rolling-circle replication. Mol. Microbiol. 29:261-273.
37. Petit, M. A., and D. Ehrlich. 2002. Essential bacterial helicases that counteract the toxicity of recombination proteins. EMBO J. 21:3137-3147.
38. Radding, C. M. 1989. Helical RecA nucleoprotein filaments mediate homologous pairing and strand exchange. Biochim. Biophys. Acta 1008:131-145.
39. Roca, A. I., and M. M. Cox. 1990. The RecA protein: structure and function. Crit. Rev. Biochem. Mol. Biol. 25:415-456.
40. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Shan, Q., J. M. Bork, B. L. Webb, R. B. Inman, and M. M. Cox. 1997. RecA protein filaments: end-dependent dissociation from ssDNA and stabilization by RecO and RecR proteins. J. Mol. Biol. 265:519-540.
42. Soultanas, P., M. S. Dillingham, F. Papadopoulos, S. E. Phillips, C. D. Thomas, and D. B. Wigley. 1999. Plasmid replication initiator protein RepD increases the processivity of PcrA DNA helicase. Nucleic Acids Res. 27:1421-1428.
43. Stasiak, A., E. Di Capua, and T. Koller. 1981. Elongation of duplex DNA by recA protein. J. Mol. Biol. 151:557-564.
44. Tomschik, M., H. Zheng, K. van Holde, J. Zlatanova, and S. H. Leuba. 2005. Fast, long-range, reversible conformational fluctuations in nucleosomes revealed by single-pair fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. USA 102:3278-3283.
45. Tuteja, N., and R. Tuteja. 2004. Prokaryotic and eukaryotic DNA helicases. Essential molecular motor proteins for cellular machinery. Eur. J. Biochem. 271:1835-1848.
46. Veaute, X., S. Delmas, M. Selva, J. Jeusset, E. Le Cam, I. Matic, F. Fabre, and M. A. Petit. 2005. UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli. EMBO J. 24:180-189.
47. Veaute, X., J. Jeusset, C. Soustelle, S. C. Kowalczykowski, E. Le Cam, and F. Fabre. 2003. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309-312.
48. Velankar, S. S., P. Soultanas, M. S. Dillingham, H. S. Subramanya, and D. B. Wigley. 1999. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 97:75-84.
49. Venkatesh, R., N. Ganesh, N. Guhan, M. S. Reddy, T. Chandrasekhar, and K. Muniyappa. 2002. RecX protein abrogates ATP hydrolysis and strand exchange promoted by RecA: insights into negative regulation of homologous recombination. Proc. Natl. Acad. Sci. USA 99:12091-12096.
50. Zheng, H., M. Tomschik, J. Zlatanova, and S. H. Leuba. 2005. Evanescent field fluorescence microscopy for analysis of protein/DNA interactions at the single-molecule level, p. 429-444. In E. Golemis and P. Adams (ed.), Protein-protein interactions, a molecular cloning manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.