Rad54 Functions as a Heteroduplex DNA Pump Modulated by Its DNA Substrates and Rad51 during D Loop Formation

Molecular Cell

Volumn 53, Issue 3, 2014, Pages 420-432

  Wright, William Douglass ^a   Heyer, Wolf Dietrich ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE MAGNESIUM; DOUBLE STRANDED DNA; HETERODUPLEX; PLASMID DNA; RAD51 PROTEIN; RAD54 PROTEIN; REPLICATION FACTOR A;

ARTICLE; CHROMOSOME ARM; DISSOCIATION; DNA BINDING; DNA STRAND; DNA STRUCTURE; DNA SUPERCOILING; DNA SYNTHESIS; ELECTROPHORETIC MOBILITY; HUMAN; IN VITRO STUDY; NONHUMAN; REACTION TIME; RESTRICTION SITE;

EUKARYOTA;

DNA HELICASES; DNA REPAIR ENZYMES; DNA, SINGLE-STRANDED; DNA, SUPERHELICAL; HOMOLOGOUS RECOMBINATION; MODELS, GENETIC; NUCLEIC ACID HETERODUPLEXES; RAD51 RECOMBINASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84893749175     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.12.027     Document Type: Article

References (41)

1. Alexeev A., Mazin A., Kowalczykowski S.C. Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51-ssDNA nucleoprotein filament. Nat. Struct. Biol. 2003, 10:182-186.
2. Alexiadis V., Lusser A., Kadonaga J.T. A conserved N-terminal motif in Rad54 is important for chromatin remodeling and homologous strand pairing. J.Biol. Chem. 2004, 279:27824-27829.
3. Amitani I., Baskin R.J., Kowalczykowski S.C. Visualization of Rad54, a chromatin remodeling protein, translocating on single DNA molecules. Mol. Cell 2006, 23:143-148.
4. Bianchi M., DasGupta C., Radding C.M. Synapsis and the formation of paranemic joints by E.coli RecA protein. Cell 1983, 34:931-939.
5. Bigot S., Saleh O.A., Lesterlin C., Pages C., El Karoui M., Dennis C., Grigoriev M., Allemand J.F., Barre F.X., Cornet F. KOPS: DNA motifs that control E.coli chromosome segregation by orienting the FtsK translocase. EMBO J. 2005, 24:3770-3780.
6. + activates human homologous recombination protein Rad51 by modulating its ATPase activity. Proc. Natl. Acad. Sci. USA 2004, 101:9988-9993.
7. Bugreev D.V., Hanaoka F., Mazin A.V. Rad54 dissociates homologous recombination intermediates by branch migration. Nat. Struct. Mol. Biol. 2007, 14:746-753.
8. Ceballos S.J., Heyer W.D. Functions of the Snf2/Swi2 family Rad54 motor protein in homologous recombination. Biochim. Biophys. Acta 2011, 1809:509-523.
9. Clever B., Schmuckli-Maurer J., Sigrist M., Glassner B.J., Heyer W.-D. Specific negative effects resulting from elevated levels of the recombinational repair protein Rad54p in Saccharomyces cerevisiae. Yeast 1999, 15:721-740.
10. Heyer W.D., Li X., Rolfsmeier M., Zhang X.P. Rad54: the Swiss Army knife of homologous recombination?. Nucleic Acids Res. 2006, 34:4115-4125.
11. Heyer W.D., Ehmsen K.T., Liu J. Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 2010, 44:113-139.
12. Hopfner K.P., Gerhold C.B., Lakomek K., Wollmann P. Swi2/Snf2 remodelers: hybrid views on hybrid molecular machines. Curr. Opin. Struct. Biol. 2012, 22:225-233.
13. Kiianitsa K., Solinger J.A., Heyer W.D. Rad54 protein exerts diverse modes of ATPase activity on duplex DNA partially and fully covered with Rad51 protein. J.Biol. Chem. 2002, 277:46205-46215.
14. Kiianitsa K., Solinger J.A., Heyer W.D. Terminal association of Rad54 protein with the Rad51-dsDNA filament. Proc. Natl. Acad. Sci. USA 2006, 103:9767-9772.
15. Li X., Heyer W.D. RAD54 controls access to the invading 3'-OH end after RAD51-mediated DNA strand invasion in homologous recombination in Saccharomyces cerevisiae. Nucleic Acids Res. 2009, 37:638-646.
16. Mazin A.V., Bornarth C.J., Solinger J.A., Heyer W.-D., Kowalczykowski S.C. Rad54 protein is targeted to pairing loci by the Rad51 nucleoprotein filament. Mol. Cell 2000, 6:583-592.
17. Mazin A.V., Alexeev A.A., Kowalczykowski S.C. A novel function of Rad54 protein. Stabilization of the Rad51 nucleoprotein filament. J.Biol. Chem. 2003, 278:14029-14036.
18. Mazin A.V., Mazina O.M., Bugreev D.V., Rossi M.J. Rad54, the motor of homologous recombination. DNA Repair (Amst.) 2010, 9:286-302.
19. +. J.Biol. Chem. 2004, 279:52042-52051.
20. Mazina O.M., Rossi M.J., Thomaä N.H., Mazin A.V. Interactions of human rad54 protein with branched DNA molecules. J.Biol. Chem. 2007, 282:21068-21080.
21. Oh S.D., Lao J.P., Hwang P.Y.H., Taylor A.F., Smith G.R., Hunter N. BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 2007, 130:259-272.
22. Petukhova G., Stratton S., Sung P. Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature 1998, 393:91-94.
23. Petukhova G., Van Komen S., Vergano S., Klein H., Sung P. Yeast Rad54 promotes Rad51-dependent homologous DNA pairing via ATP hydrolysis-driven change in DNA double helix conformation. J.Biol. Chem. 1999, 274:29453-29462.
24. Raschle M., Van Komen S., Chi P., Ellenberger T., Sung P. Multiple interactions with the Rad51 recombinase govern the homologous recombination function of Rad54. J.Biol. Chem. 2004, 279:51973-51980.
25. Ristic D., Wyman C., Paulusma C., Kanaar R. The architecture of the human Rad54-DNA complex provides evidence for protein translocation along DNA. Proc. Natl. Acad. Sci. USA 2001, 98:8454-8460.
26. Saleh O.A., Bigot S., Barre F.X., Allemand J.F. Analysis of DNA supercoil induction by FtsK indicates translocation without groove-tracking. Nat. Struct. Mol. Biol. 2005, 12:436-440.
27. Sanchez H., Kertokalio A., van Rossum-Fikkert S., Kanaar R., Wyman C. Combined optical and topographic imaging reveals different arrangements of human RAD54 with presynaptic and postsynaptic RAD51-DNA filaments. Proc. Natl. Acad. Sci. USA 2013, 110:11385-11390.
28. Shibata T., DasGupta C., Cunningham R.P., Radding C.M. Purified Escherichia coli recA protein catalyzes homologous pairing of superhelical DNA and single-stranded fragments. Proc. Natl. Acad. Sci. USA 1979, 76:1638-1642.
29. Shibata T., Ohtani T., Iwabuchi M., Ando T. D-loop cycle. Acircular reaction sequence which comprises formation and dissociation of D-loops and inactivation and reactivation of superhelical closed circular DNA promoted by recA protein of Escherichia coli. J.Biol. Chem. 1982, 257:13981-13986.
30. Sigurdsson S., Van Komen S., Petukhova G., Sung P. Homologous DNA pairing by human recombination factors Rad51 and Rad54. J.Biol. Chem. 2002, 277:42790-42794.
31. Solinger J.A., Kiianitsa K., Heyer W.-D. Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol. Cell 2002, 10:1175-1188.
32. Sung P. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 1994, 265:1241-1243.
33. Swagemakers S.M.A., Essers J., de Wit J., Hoeijmakers J.H.J., Kanaar R. The human RAD54 recombinational DNA repair protein is a double-stranded DNA-dependent ATPase. J.Biol. Chem. 1998, 273:28292-28297.
34. Tan T.L.R., Essers J., Citterio E., Swagemakers S.M.A., de Wit J., Benson F.E., Hoeijmakers J.H.J., Kanaar R. Mouse Rad54 affects DNA conformation and DNA-damage-induced Rad51 foci formation. Curr. Biol. 1999, 9:325-328.
35. Tan T.L.R., Kanaar R., Wyman C. Rad54, a Jack of all trades in homologous recombination. DNA Repair (Amst.) 2003, 2:787-794.
36. Tsuchiya H., Uchiyama M., Hara K., Nakatsu Y., Tsuzuki T., Inoue H., Harashima H., Kamiya H. Improved gene correction efficiency with a tailed duplex DNA fragment. Biochemistry 2008, 47:8754-8759.
37. Van Komen S., Petukhova G., Sigurdsson S., Stratton S., Sung P. Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54. Mol. Cell 2000, 6:563-572.
38. Van Komen S., Petukhova G., Sigurdsson S., Sung P. Functional cross-talk among Rad51, Rad54, and replication protein A in heteroduplex DNA joint formation. J.Biol. Chem. 2002, 277:43578-43587.
39. Wolner B., Peterson C.L. ATP-dependent and ATP-independent roles for the Rad54 chromatin remodeling enzyme during recombinational repair of a DNA double strand break. J.Biol. Chem. 2005, 280:10855-10860.
40. Wright W.D., Ehmsen K.T., Heyer W.D. Assays for structure-selective DNA endonucleases. Methods Mol. Biol. 2011, 745:345-362.
41. Zhu Z., Chung W.H., Shim E.Y., Lee S.E., Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 2008, 134:981-994.