RecBCD Enzyme Switches Lead Motor Subunits in Response to χ Recognition

Cell

Volumn 131, Issue 4, 2007, Pages 694-705

  Spies, Maria ^a,b   Amitani, Ichiro ^a   Baskin, Ronald J ^a   Kowalczykowski, Stephen C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

DNA

Indexed keywords

EXODEOXYRIBONUCLEASE V; NUCLEASE; SINGLE STRANDED DNA;

ARTICLE; DNA REPAIR; ENZYME DEGRADATION; ENZYME THERAPY; GENE SWITCHING; GENE TRANSLOCATION; MOLECULAR RECOGNITION; MOTOR UNIT; MUTANT; PRIORITY JOURNAL; VELOCITY; WILD TYPE;

EID: 36049052525     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.09.023     Document Type: Article

References (37)

1. Amundsen S.K., Taylor A.F., Chaudhury A.M., and Smith G.R. recD: the gene for an essential third subunit of exonuclease V. Proc. Natl. Acad. Sci. USA 83 (1986) 5558-5562
2. Anderson D.G., and Kowalczykowski S.C. The recombination hot spot χ is a regulatory element that switches the polarity of DNA degradation by the RecBCD enzyme. Genes Dev. 11 (1997) 571-581
3. Anderson D.G., and Kowalczykowski S.C. The translocating RecBCD enzyme stimulates recombination by directing RecA protein onto ssDNA in a χ-regulated manner. Cell 90 (1997) 77-86
4. Anderson D.G., Churchill J.J., and Kowalczykowski S.C. Chi-activated RecBCD enzyme possesses 5′→3′ nucleolytic activity, but RecBC enzyme does not: evidence suggesting that the alteration induced by Chi is not simply ejection of the RecD subunit. Genes Cells 2 (1997) 117-128
5. Bianco P.R., and Kowalczykowski S.C. Translocation step size and mechanism of the RecBC DNA helicase. Nature 405 (2000) 368-372
6. Bianco P.R., Brewer L.R., Corzett M., Balhorn R., Yeh Y., Kowalczykowski S.C., and Baskin R.J. Processive translocation and DNA unwinding by individual RecBCD enzyme molecules. Nature 409 (2001) 374-378
7. Braedt G., and Smith G.R. Strand specificity of DNA unwinding by RecBCD enzyme. Proc. Natl. Acad. Sci. USA 86 (1989) 871-875
8. Chaudhury A.M., and Smith G.R. A new class of Escherichia coli recBC mutants: implications for the role of RecBC enzyme in homologous recombination. Proc. Natl. Acad. Sci. USA 81 (1984) 7850-7854
9. Chédin F., Handa N., Dillingham M.S., and Kowalczykowski S.C. The AddAB helicase/nuclease forms a stable complex with its cognate χ sequence during translocation. J. Biol. Chem. 281 (2006) 18610-18617
10. Churchill J.J., Anderson D.G., and Kowalczykowski S.C. The RecBC enzyme loads RecA protein onto ssDNA asymmetrically and independently of Chi, resulting in constitutive recombination activation. Genes Dev. 13 (1999) 901-911
11. Dillingham M.S., Spies M., and Kowalczykowski S.C. RecBCD enzyme is a bipolar DNA helicase. Nature 423 (2003) 893-897
12. Dillingham M.S., Webb M.R., and Kowalczykowski S.C. Bipolar DNA translocation contributes to highly processive DNA unwinding by RecBCD enzyme. J. Biol. Chem. 280 (2005) 37069-37077
13. Dixon D.A., and Kowalczykowski S.C. Homologous pairing in vitro stimulated by the recombination hotspot, Chi. Cell 66 (1991) 361-371
14. Dixon D.A., and Kowalczykowski S.C. The recombination hotspot χ is a regulatory sequence that acts by attenuating the nuclease activity of the E. coli RecBCD enzyme. Cell 73 (1993) 87-96
15. Dixon D.A., and Kowalczykowski S.C. Role of the Escherichia coli recombination hotspot, χ, in RecABCD-dependent homologous pairing. J. Biol. Chem. 270 (1995) 16360-16370
16. Galletto R., Amitani I., Baskin R.J., and Kowalczykowski S.C. Direct observation of individual RecA filaments assembling on single DNA molecules. Nature 443 (2006) 875-878
17. Handa N., Bianco P.R., Baskin R.J., and Kowalczykowski S.C. Direct visualization of RecBCD movement reveals cotranslocation of the RecD motor after χ recognition. Mol. Cell 17 (2005) 745-750
18. Korangy F., and Julin D.A. 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 (1992) 1727-1732
19. Kulkarni A., and Julin D.A. Specific inhibition of the E. coli RecBCD enzyme by Chi sequences in single-stranded oligodeoxyribonucleotides. Nucleic Acids Res. 32 (2004) 3672-3682
20. Lam S.T., Stahl M.M., McMilin K.D., and Stahl F.W. Rec-mediated recombinational hot spot activity in bacteriophage lambda. II. A mutation which causes hot spot activity. Genetics 77 (1974) 425-433
21. Muskavitch K.M., and Linn S. A unified mechanism for the nuclease and unwinding activities of the recBC enzyme of Escherichia coli. J. Biol. Chem. 257 (1982) 2641-2648
22. Myers R.S., Stahl M.M., and Stahl F.W. Chi recombination activity in phage lambda decays as a function of genetic distance. Genetics 141 (1995) 805-812
23. Ponticelli A.S., Schultz D.W., Taylor A.F., and Smith G.R. Chi-dependent DNA strand cleavage by RecBC enzyme. Cell 41 (1985) 145-151
24. Roman L.J., and Kowalczykowski S.C. Characterization of the helicase activity of the Escherichia coli RecBCD enzyme using a novel helicase assay. Biochemistry 28 (1989) 2863-2873
25. Roman L.J., Eggleston A.K., and Kowalczykowski S.C. Processivity of the DNA helicase activity of Escherichia coli recBCD enzyme. J. Biol. Chem. 267 (1992) 4207-4214
26. Romier C., Dominguez R., Lahm A., Dahl O., and Suck D. Recognition of single-stranded DNA by nuclease P1: high resolution crystal structures of complexes with substrate analogs. Proteins 32 (1998) 414-424
27. Singleton M.R., Dillingham M.S., Gaudier M., Kowalczykowski S.C., and Wigley D.B. Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks. Nature 432 (2004) 187-193
28. Spies M., and Kowalczykowski S.C. Homologous recombination by RecBCD and RecF pathways. In: Higgins N.P. (Ed). The Bacterial Chromosome (2005), ASM Press, Washington, D.C. 389-403
29. Spies M., and Kowalczykowski S.C. The RecA binding locus of RecBCD is a general domain for recruitment of DNA strand exchange proteins. Mol. Cell 21 (2006) 573-580
30. Spies M., Bianco P.R., Dillingham M.S., Handa N., Baskin R.J., and Kowalczykowski S.C. A molecular throttle: the recombination hotspot χ controls DNA translocation by the RecBCD helicase. Cell 114 (2003) 647-654
31. Spies M., Dillingham M.S., and Kowalczykowski S.C. Translocation by the RecB motor Is an absolute requirement for χ-recognition and RecA protein loading by RecBCD enzyme. J. Biol. Chem. 280 (2005) 37078-37087
32. Taylor A., and Smith G.R. Unwinding and rewinding of DNA by the RecBC enzyme. Cell 22 (1980) 447-457
33. Taylor A.F., and Smith G.R. Strand specificity of nicking of DNA at Chi sites by RecBCD enzyme: modulation by ATP and magnesium levels. J. Biol. Chem. 270 (1995) 24459-24467
34. Taylor A.F., and Smith G.R. Regulation of homologous recombination: Chi inactivates RecBCD enzyme by disassembly of the three subunits. Genes Dev. 13 (1999) 890-900
35. Taylor A.F., and Smith G.R. RecBCD enzyme is a DNA helicase with fast and slow motors of opposite polarity. Nature 423 (2003) 889-893
36. Taylor A.F., Schultz D.W., Ponticelli A.S., and Smith G.R. RecBC enzyme nicking at Chi sites during DNA unwinding: location and orientation-dependence of the cutting. Cell 41 (1985) 153-163
37. Yu M., Souaya J., and Julin D.A. 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. USA 95 (1998) 981-986