Intersubunit signaling in RecBCD enzyme, a complex protein machine regulated by Chi hot spots

Genes and Development

Volumn 21, Issue 24, 2007, Pages 3296-3307

  Amundsen, Susan K ^a   Taylor, Andrew F ^a   Reddy, Manjula ^a,b   Smith, Gerald R ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

Chi sites; Complex protein machines; E. coli; Homologous recombination; RecBCD enzyme

Indexed keywords

DNA; ENZYME; EXODEOXYRIBONUCLEASE V; HELICASE; NUCLEASE; RECB ENZYME; RECD ENZYME; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME SUBUNIT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WILD TYPE;

DNA; DNA HELICASES; ESCHERICHIA COLI; MUTATION; SIGNAL TRANSDUCTION;

ESCHERICHIA COLI;

EID: 37249047064     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1605807     Document Type: Article

References (51)

1. Alberts, B. 1998. The cell as a collection of protein machines: Preparing the next generation of molecular biologists. Cell 92: 291-294.
2. Amundsen, S.K. and Smith, G.R. 2007. Chi hotspot activity in Escherichia coli without RecBCD exonuclease activity: Implications for the mechanism of recombination. Genetics 176: 41-54.
3. Amundsen, S.K., Taylor, A.F., Chaudhury, A.M., and Smith, G.R. 1986. recD: The gene for an essential third subunit of exonuclease V. Proc. Natl. Acad. Sci. 83: 5558-5562.
4. Amundsen, S.K., Neiman, A.M., Thibodeaux, S.M., and Smith, G.R. 1990. Genetic dissection of the biochemical activities of RecBCD enzyme. Genetics 126: 25-40.
5. Amundsen, S.K., Taylor, A.F., and Smith, G.R. 2000. The RecD subunit of the Escherichia coli RecBCD enzyme inhibits RecA loading, homologous recombination and DNA repair. Proc. Natl. Acad. Sci. 97: 7399-7404.
6. Amundsen, S.K., Taylor, A.F., and Smith, G.R. 2002. A domain of RecC required for assembly of the regulatory RecD subunit into the Escherichia coli RecBCD holoenzyme. Genetics 161: 483-492.
7. Anderson, D.G. and Kowalczykowski, S.C. 1997a. The recombination hot spot χ is a regulatory element that switches the polarity of DNA degradation by the RecBCD enzyme. Genes & Dev. 11: 571-581.
8. Anderson, D.G. and Kowalczykowski, S.C. 1997b. The translocating RecBCD enzyme stimulates recombination by directing RecA protein onto ssDNA in a χ regulated manner. Cell 90: 77-86.
9. D1080A, eliminates RecA protein loading but not Chi recognition by RecBCD enzyme. J. Biol. Chem. 274: 27139-27144.
10. Arnold, D.A., Handa, N., Kobayashi, I., and Kowalczykowski, S.C. 2000. A novel, 11 nucleotide variant of χ,χ*: One of a class of sequences defining the Escherichia coli recombination hotspot χ. J. Mol. Biol. 300: 469-479.
11. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K., eds. 2003. Current protocols in molecular biology. John Wiley & Sons, New York.
12. Bates, A.D. and Maxwell, A. 2007. Energy coupling in Type II topoisomerases: Why do they hydrolyze ATP? Biochemistry 46: 7929-7941.
13. Bianco, P.R. and Kowalczykowski, S.C. 1997. The recombination hotspot χ is recognized by the translocating RecBCD enzyme as the single strand of DNA containing the sequence 5′-GCTGGTGG-3′. Proc. Natl. Acad. Sci. 94: 6706-6711.
14. Cheng, K.C. and Smith, G.R. 1989. Distribution of Chi-stimulated recombinational exchanges and heteroduplex endpoints in phage λ. Genetics 123: 5-17.
15. Churchill, J.J., Anderson, D.G., and Kowalczykowski, S.C. 1999. The RecBC enzyme loads RecA protein onto ssDNA asymmetrically and independently of χ resulting in constitutive recombination activation. Genes & Dev. 13: 901-911.
16. Dixon, D.A. and Kowalczykowski, S.C. 1991. Homologous pairing in vitro stimulated by the recombination hotspot, Chi. Cell 66: 361-371.
17. Dixon, D.A. and Kowalczykowski, S.C. 1993. The recombination hotspot χ is a regulatory sequence that acts by attenuating the nuclease activity of the E. coli RecBCD enzyme. Cell 73: 87-96.
18. Dohoney, K.M. and Gelles, J. 2001. χ-sequence recognition and DNA translocation by single RecBCD helicase/nuclease molecules. Nature 409: 370-374.
19. Eichler, D.C. and Lehman, I.R. 1977. On the role of ATP in phosphodiester bond hydrolysis catalyzed by the RecBC deoxyribonuclease of Escherichia coli. J. Biol. Chem. 252: 499-503.
20. Farah, J.A. and Smith, G.R. 1997. The RecBCD enzyme initiation complex for DNA unwinding: Enzyme positioning and DNA opening. J. Mol. Biol. 272: 699-715.
21. Ganesan, S. and Smith, G.R. 1993. Strand-specific binding to duplex DNA ends by the subunits of Escherichia coli RecBCD enzyme. J. Mol. Biol. 229: 67-78.
22. Graves-Woodward, K.L., Gottlieb, J., Challberg, M.D., and Weller, S.K. 1997. Biochemical analyses of mutations in the HSV-1 helicase-primase that alter ATP hydrolysis, DNA unwinding, and coupling between hydrolysis and unwinding. J. Biol. Chem. 272: 4623-4630.
23. Hall, M.C., Ozsoy, A.Z., and Matson, S.W. 1998. Site-directed mutations in motif VI of Escherichia coli DNA helicase II result in multiple biochemical defects: Evidence for the involvement of motif VI in the coupling of ATPase and DNA binding activities via conformational changes. J. Mol. Biol. 277: 257-271.
24. Handa, N., Bianco, P.R., Baskin, R.J., and Kowalczykowski, S.C. 2005. Direct visualization of RecBCD movement reveals cotranslocation of the RecD motor after Chi recognition. Mol. Cell 17: 745-750.
25. Iyer, R.R., Pluciennik, A., Burdett, V., and Modrich, P.L. 2006. DNA mismatch repair: Functions and mechanisms. Chem. Rev. 106: 302-323.
26. Korangy, F. and Julin, D.A. 1992. Alteration by site-directed mutagenesis of the conserved lysine residue in the ATP-binding consensus sequence of the RecD subunit of the Escherichia coli RecBCD enzyme. J. Biol. Chem. 267: 1727-1732.
27. Lundblad, V., Taylor, A.F., Smith, G.R., and Kleckner, N. 1984. Unusual alleles of recB and recC stimulate excision of inverted repeat transposons Tn10 and Tn5. Proc. Natl. Acad. Sci. 81: 824-828.
28. Murray, N.E. 2000. Type I restriction systems: Sophisticated molecular machines (a legacy of Bertani and Weigle). Microbiol. Mol. Biol. Rev. 64: 412-434.
29. Oliver, D.B. and Goldberg, E.B. 1977. Protection of parental T4 DNA from a restriction exonuclease by the product of gene 2. J. Mol. Biol. 116: 877-881.
30. Schultz, D.W., Taylor, A.F., and Smith, G.R. 1983. Escherichia coli RecBC pseudorevertants lacking Chi recombinational hotspot activity. J. Bacteriol. 155: 664-680.
31. Singleton, M.R., Dillingham, M.S., Gaudier, M., Kowalczykowski, S.C., and Wigley, D.B. 2004. Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks. Nature 432: 187-193.
32. Smith, G.R. 1990. RecBCD enzyme. In Nucleic acids and molecular biology (eds. F. Eckstein, and D.M.J. Lilley), pp. 78-98. Springer-Verlag, Berlin.
33. Smith, G.R. 1991. Conjugational recombination in E. coli: Myths and mechanisms. Cell 64: 19-27.
34. Smith, G.R. 2001. Homologous recombination near and far from DNA breaks: Alternative roles and contrasting views. Annu. Rev. Genet. 35: 243-274.
35. Smith, G.R., Kunes, S.M., Schultz, D.W., Taylor, A., and Triman, K.L. 1981. Structure of Chi hotspots of generalized recombination. Cell 24: 429-436.
36. Spies, M. and Kowalczykowski, S.C. 2006. The RecA binding locus of RecBCD is a general domain for recruitment of DNA strand exchange proteins. Mol. Cell 21: 573-580.
37. Spies, M., Bianco, P.R., Dillingham, M.S., Handa, N., Baskin, R.J., and Kowalczykowski, S.C. 2003. A molecular throttle: The recombination hotspot Chi controls DNA translocation by the RecBCD helicase. Cell 114: 647-654.
38. Spies, M., Dillingham, M.S., and Kowalczykowski, S.C. 2005. Translocation by the RecB motor is an absolute requirement for χ-recognition and RecA protein loading by RecBCD enzyme. J. Biol. Chem. 280: 37078-37087.
39. Stahl, F.W. and Stahl, M.M. 1977. Recombination pathway specificity of Chi. Genetics 86: 715-725.
40. Taylor, A. and Smith, G.R. 1980. Unwinding and rewinding of DNA by the RecBC enzyme. Cell 22: 447-457.
41. Taylor, A.F. and Smith, G.R. 1992. RecBCD enzyme is altered upon cutting DNA at a Chi recombination hotspot. Proc. Natl. Acad. Sci. 89: 5226-5230.
42. Taylor, A.F. and Smith, G.R. 1995a. Monomeric RecBCD enzyme binds and unwinds DNA. J. Biol. Chem. 270: 24451-24458.
43. Taylor, A.F. and Smith, G.R. 1995b. Strand specificity of nicking of DNA at Chi sites by RecBCD enzyme: Modulation by ATP and magnesium levels. J. Biol. Chem. 270: 24459-24467.
44. Taylor, A.F. and Smith, G.R. 1999. Regulation of homologous recombination: Chi inactivates RecBCD enzyme by disassembly of the three subunits. Genes & Dev. 13: 890-900.
45. Taylor, A.F. and Smith, G.R. 2003. RecBCD enzyme is a DNA helicase with fast and slow motors of opposite polarity. Nature 423: 889-893.
46. Taylor, A.F., Schultz, D.W., Ponticelli, A.S., and Smith, G.R. 1985. RecBC enzyme nicking at Chi sites during DNA unwinding: Location and orientation dependence of the cutting. Cell 41: 153-163.
47. Thaler, D.S., Sampson, E., Siddiqi, I., Rosenberg, S.M., Stahl, F.W., and Stahl, M. 1988. A hypothesis: Chi-activation of RecBCD enzyme involves removal of the RecD subunit. In Mechanisms and Consequences of DNA Damage Processing, (eds. E. Friedberg, and P. Hanawalt), pp. 413-422. Alan R. Liss, New York.
48. Thomason, L., Court, D.L., Bubunenko, M., Costantino, N., Wilson, H., Datta, S., and Oppenheim, A. 2005. Recombineering: Genetic engineering in bacteria using homologous recombination. In Current Protocols in Molecular Biology (eds. F.M. Ausubel, et al.), unit 1.16. Wiley, New York.
49. Yu, M., Souaya, J., and Julin, D.A. 1998a. The 30-kDa C-terminal domain of the RecB protein is critical for the nuclease activity, but not the helicase activity, of the RecBCD enzyme from Escherichia coli. Proc. Natl. Acad. Sci. 95: 981-986.
50. Yu, M., Souaya, J., and Julin, D.A. 1998b. Identification of the nuclease active site in the multifunctional RecBCD enzyme by creation of a chimeric enzyme. J. Mol. Biol. 283: 797-808.
51. Zhang, X.J. and Julin, D.A. 1999. Isolation and characterization of the C-terminal nuclease domain from the RecB protein of Escherichia coli. Nucleic Acids Res. 27: 4200-4207.