The 14-3-3 Protein Homologues from Saccharomyces cerevisiae, Bmh1p and Bmh2p, Have Cruciform DNA-binding Activity and Associate in Vivo with ARS307

We have previously shown that, in human cells, cruciform DNA-binding activity is due to 14-3-3 proteins (Todd, A., Cossons, N., Aitken, A., Price, G. B., and Zannis-Hadjopoulos, M. (1998) Biochemistry37, 14317-14325). Here, wild-type and single- and double-knockout nuclear extracts from the 14-3-3 Saccharomyces cerevisiaehomologues Bmh1p and Bmh2p were analyzed for similar cruciform-binding activities in relation to these proteins. The Bmh1p-Bmh2p heterodimer, present in the wild-type strain, bound efficiently to cruciform-containing DNA in a structure-specific manner because cruciform DNA efficiently competed with the formation of the complex, whereas linear DNA did not. In contrast, the band-shift ability of the Bmh1p-Bmh1p and Bmh2p-Bmh2p homodimers present in thebmh2 − and bmh1 −single-knockout cells, respectively, was reduced by ∼93 and 82%, respectively. The 14-3-3 plant homologue GF14 was also able to bind to cruciform DNA, suggesting that cruciform-binding activity is a common feature of the family of 14-3-3 proteins across species. Bmh1p and Bmh2p were found to associate in vivo with the yeast autonomous replication sequence ARS307, as assayed by formaldehyde cross-linking, followed by immunoprecipitation with anti-Bmh1p/Bmh2p antibody and conventional PCR. In agreement with the finding of an association of Bmh1p and Bmh2p with ARS307, another immunoprecipitation experiment using 2D3, an anti-cruciform DNA monoclonal antibody, revealed the presence of cruciform-containing DNA in ARS307. We have previously shown that, in human cells, cruciform DNA-binding activity is due to 14-3-3 proteins (Todd, A., Cossons, N., Aitken, A., Price, G. B., and Zannis-Hadjopoulos, M. (1998) Biochemistry37, 14317-14325). Here, wild-type and single- and double-knockout nuclear extracts from the 14-3-3 Saccharomyces cerevisiaehomologues Bmh1p and Bmh2p were analyzed for similar cruciform-binding activities in relation to these proteins. The Bmh1p-Bmh2p heterodimer, present in the wild-type strain, bound efficiently to cruciform-containing DNA in a structure-specific manner because cruciform DNA efficiently competed with the formation of the complex, whereas linear DNA did not. In contrast, the band-shift ability of the Bmh1p-Bmh1p and Bmh2p-Bmh2p homodimers present in thebmh2 − and bmh1 −single-knockout cells, respectively, was reduced by ∼93 and 82%, respectively. The 14-3-3 plant homologue GF14 was also able to bind to cruciform DNA, suggesting that cruciform-binding activity is a common feature of the family of 14-3-3 proteins across species. Bmh1p and Bmh2p were found to associate in vivo with the yeast autonomous replication sequence ARS307, as assayed by formaldehyde cross-linking, followed by immunoprecipitation with anti-Bmh1p/Bmh2p antibody and conventional PCR. In agreement with the finding of an association of Bmh1p and Bmh2p with ARS307, another immunoprecipitation experiment using 2D3, an anti-cruciform DNA monoclonal antibody, revealed the presence of cruciform-containing DNA in ARS307. cruciform DNA-binding protein whole cell extract monoclonal antibody autonomous replication sequence Although 14-3-3 protein was primarily isolated and characterized as an abundant brain protein (1Moore B.W. Perez V.J. Carlson F.D. Physiological and Biochemical Aspects of Nervous Integration. Prentice-Hall, Englewood Cliffs, NJ1967: 343-359Google Scholar), during the last decade, it has become evident that members of the 14-3-3 protein family are present in all types of eukaryotic cells. 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Nucleic Acids Res. 1987; 15: 8319-8331Crossref PubMed Scopus (38) Google Scholar, 21Noirot P. Bargonetti J. Novick R.P. Proc. Natl. Acad. Sci. U. S. A. 1990; 87: 8560-8564Crossref PubMed Scopus (82) Google Scholar, 22Jin R. Novick R.P. Plasmid. 2001; 46: 95-105Crossref PubMed Scopus (12) Google Scholar), eukaryotic viruses (23Pogue G.P. Hall T.C. J. Virol. 1992; 66: 674-684Crossref PubMed Google Scholar), and mammalian cells (24Zannis-Hadjopoulos M. Frappier L. Khoury M. Price G.B. EMBO J. 1988; 7: 1837-1844Crossref PubMed Scopus (60) Google Scholar), the cruciform-binding activity of 14-3-3 proteins represents a in the of these proteins. in we have found that 14-3-3 isoforms and associate in vivo with of DNA replication in a cell manner and are in DNA replication D. C.E. Price G.B. Zannis-Hadjopoulos M. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). In of the of the 14-3-3 proteins with to but also to in yeast have for the eukaryotic The of the and for S. cerevisiae of the of 14-3-3 proteins in cruciform binding and eukaryotic DNA the cruciform-binding activity of 14-3-3 found in mammalian cells is also present in we analyzed the cerevisiae Bmh1p and Bmh2p by or band-shift S. as a yeast because DNA replication is characterized in it by with the yeast S. Bmh1p and mammalian are in with a large number of proteins that are important in intracellular processes (for review, see van Heusden G.P.H. Steensma H.Y. 2001; PubMed Scopus Google Scholar). proteins are to the mammalian and for the Bmh1p kDa) and Bmh2p kDa) are and respectively, to with the homology in the of these proteins van Heusden G.P.H. Steensma H.Y. 2001; PubMed Scopus Google Scholar). of the a the of the cells, but the in for the yeast (6van Heusden G.P.H. Wenzel T.J. Lagendijk E.L. Steensma H.Y. van den Berg J.A. FEBS Lett. 1992; 302: 145-150Crossref PubMed Scopus (113) Google Scholar, 7van Heusden G.P.H. Griffiths D.J. Ford J.C. Chin-A-Woeng T.F. Schrader P.A. Carr A.M. Steensma H.Y. Eur. J. Biochem. 1995; 229: 45-53Crossref PubMed Scopus (139) Google Scholar). has been by at Arabidopsis isoforms Heusden G.P.H. van Ferl R.J. Steensma H.Y. FEBS Lett. PubMed Scopus Google Scholar). the of Bmh1p and Bmh2p with cruciform-containing DNA in and in vivo association with the S. cerevisiae autonomous replication sequence ARS307. association of these yeast of 14-3-3 is also to human the presence of cruciform at is revealed by anti-cruciform antibody immunoprecipitation and conventional PCR. The yeast in were of G. P. H. van Heusden of The S. cerevisiae and were as previously and with a of the for each cells were at S. cerevisiae wild-type cells were in at to the the cells were to for to the cells were in for to was by the cells from the for was by of from S. cerevisiae was by as previously DNA was and as previously (18Pearson C.E. Ruiz M.T. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1994; 33: 14185-14196Crossref PubMed Scopus (36) Google Scholar). of or nuclear extract as well as of human (15Todd A. Cossons N. Aitken A. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1998; 37: 14317-14325Crossref PubMed Scopus (48) Google Scholar, C.E. Ruiz M.T. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1994; 33: 14185-14196Crossref PubMed Scopus (36) Google Scholar) were as a and were with of cruciform DNA for in binding as previously (18Pearson C.E. Ruiz M.T. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1994; 33: 14185-14196Crossref PubMed Scopus (36) Google Scholar). The were to at for 2 The was and for The was followed with and 12 of or − S. cerevisiae nuclear of wild-type S. cerevisiae nuclear extract was with of cruciform DNA and and of cruciform DNA or linear DNA (18Pearson C.E. Ruiz M.T. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1994; 33: 14185-14196Crossref PubMed Scopus (36) Google Scholar), as a for in binding (18Pearson C.E. Ruiz M.T. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1994; 33: 14185-14196Crossref PubMed Scopus (36) Google Scholar). The were to at for 2 The was and for and GF14 were as previously (15Todd A. Cossons N. Aitken A. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1998; 37: 14317-14325Crossref PubMed Scopus (48) Google Scholar) with some In of cruciform DNA (18Pearson C.E. Ruiz M.T. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1994; 33: 14185-14196Crossref PubMed Scopus (36) Google Scholar) was for binding Bmh1p or Bmh2p from of wild-type S. cerevisiae nuclear extract or GF14 from the − in the presence of nuclear and were a and to at for was from the by as previously (15Todd A. Cossons N. Aitken A. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1998; 37: 14317-14325Crossref PubMed Scopus (48) Google Scholar). The were to using a of each and the nuclear extracts of were with and the were a was at for and the were to membrane at for at were with anti-Bmh1p/Bmh2p antibody Heusden G.P.H. Griffiths D.J. Ford J.C. Chin-A-Woeng T.F. Schrader P.A. Carr A.M. Steensma H.Y. Eur. J. Biochem. 1995; 229: 45-53Crossref PubMed Scopus (139) Google Scholar) or with monoclonal antibody by R. J. G. Ferl R. Proc. Natl. Acad. Sci. U. S. A. 1992; PubMed Scopus Google Scholar). In was as previously K. S. M. Sci. 2000; Scholar). In of in was to of formaldehyde was to the of and for at with The cell was in an for with were by at at for The was three with and from or cells were in of and of The of was to the cell and the was for and for another for of the cells were the the were and to to the DNA to and The were for each to the at for at the were to The protein of each was to by with of as the whole cell extract of the was with of protein a for at to the by of to protein The were at for 12 with of or anti-Bmh1p/Bmh2p antibody Heusden G.P.H. Griffiths D.J. Ford J.C. Chin-A-Woeng T.F. Schrader P.A. Carr A.M. Steensma H.Y. Eur. J. Biochem. 1995; 229: 45-53Crossref PubMed Scopus (139) Google Scholar). of protein was and the was for 2 The were for at with of each of the and and and the were in of of the was at to the followed by a at with of The was with the K. the were to the DNA by The and was as in conventional with and were to a DNA from the yeast autonomous replication sequence number for at was followed by of for at for at for at and a for at were with and with an apparatus of cruciform-containing DNA using 2D3, an anti-cruciform DNA monoclonal antibody L. Price G.B. Zannis-Hadjopoulos M. J. Mol. Biol. 1987; PubMed Scopus Google Scholar), was as previously D. M. Zannis-Hadjopoulos M. Price G.B. PubMed Scopus Google Scholar). of or cell was with and to with with DNA was by to the antibody of of yeast DNA using a DNA in a a of was and the was at of was the and the was a at DNA was from DNA using to The were by with and and with and in at 12 of was with the DNA for and The was of DNA three with of and by the at for the and the in the was three with of and The DNA was from the bound by the in of the were by the at for 2 The DNA was using the The was as for with and for the or and for the number shown in nuclear proteins from S. cells were able to the of a cruciform-containing DNA a human was which the band-shift (15Todd A. Cossons N. Aitken A. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1998; 37: 14317-14325Crossref PubMed Scopus (48) Google Scholar, C.E. Ruiz M.T. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1994; 33: 14185-14196Crossref PubMed Scopus (36) Google Scholar). extracts from − − cells to large of and and was extracts from the and were the was were also using nuclear extracts from the cells of S. cerevisiae strain, a of the Bmh1p and Bmh2p proteins Heusden G.P.H. Griffiths D.J. Ford J.C. Chin-A-Woeng T.F. Schrader P.A. Carr A.M. Steensma H.Y. Eur. J. Biochem. 1995; 229: 45-53Crossref PubMed Scopus (139) Google Scholar), was by the 14-3-3 Arabidopsis homologue GF14 Heusden G.P.H. Griffiths D.J. Ford J.C. Chin-A-Woeng T.F. Schrader P.A. Carr A.M. Steensma H.Y. Eur. J. Biochem. 1995; 229: 45-53Crossref PubMed Scopus (139) Google Scholar). The the GF14 protein is the of Heusden G.P.H. Griffiths D.J. Ford J.C. Chin-A-Woeng T.F. Schrader P.A. Carr A.M. Steensma H.Y. Eur. J. Biochem. 1995; 229: 45-53Crossref PubMed Scopus (139) Google Scholar). of GF14 in the presence of whereas in extracts from the cells in a in the of the cruciform DNA with that, in the was reduced and was of of GF14 in the presence of Although the S. cerevisiae double-knockout cells did with Heusden G.P.H. Griffiths D.J. Ford J.C. Chin-A-Woeng T.F. Schrader P.A. Carr A.M. Steensma H.Y. Eur. J. Biochem. 1995; 229: 45-53Crossref PubMed Scopus (139) Google Scholar), for at of was by of the cells which to the of the cruciform-binding activity these cells were was the of 14-3-3 proteins associate with partners as or as protein the cruciform-binding activity is found in 14-3-3 (15Todd A. Cossons N. Aitken A. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1998; 37: 14317-14325Crossref PubMed Scopus (48) Google Scholar). The in that the Bmh1p-Bmh2p nuclear extract from is in binding to cruciform DNA of the Bmh2p-Bmh2p nuclear extracts from and Bmh1p-Bmh1p nuclear extract from was in a of in which and 12 of nuclear extract from the three were of the for each of the nuclear extract that Bmh2p-Bmh2p was able to the of the cruciform DNA and at the its was and the with the wild-type nuclear extract and at the was nuclear extracts from were and at the that the Bmh1p-Bmh1p is able to bind to the cruciform DNA. has been shown to and to bind to cruciform DNA by sequence (18Pearson C.E. Ruiz M.T. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1994; 33: 14185-14196Crossref PubMed Scopus (36) Google Scholar). the binding of the cerevisiae Bmh1p and Bmh2p to cruciform DNA is or binding were as previously for human (18Pearson C.E. Ruiz M.T. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1994; 33: 14185-14196Crossref PubMed Scopus (36) Google Scholar). shown in 2 the cruciform at a of cruciform and was at a of cruciform as has also been for human (18Pearson C.E. Ruiz M.T. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1994; 33: 14185-14196Crossref PubMed Scopus (36) Google Scholar). of a of cruciform did in as also previously with human (18Pearson C.E. Ruiz M.T. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1994; 33: 14185-14196Crossref PubMed Scopus (36) Google Scholar). the was by as as a of linear 2 The protein of the with the wild-type nuclear extract was by using a antibody that S. Bmh1p and The nuclear extract from was as and as proteins were present in it Bmh1p and Bmh2p were also detected in the from the The presence of proteins in the was by the that isoforms were present in the cell extract from wild-type cells whereas Bmh2p or Bmh1p was present in the cell extract from bmh1 − or − cells, respectively. The analysis was with the with the nuclear extract from double-knockout cells in the presence of a monoclonal antibody GF14 a from the of R. J. the 14-3-3 plant protein was detected in the nuclear extract and the DNA replication have been well characterized in the yeast S. cerevisiae to the and of autonomous replication which were by ability to the autonomous replication of plasmids which were J. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar, K. S. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar). the presence of cruciform-containing DNA at S. cerevisiae replication anti-cruciform DNA antibody were using 2D3, which is for cruciform-containing DNA L. Price G.B. Zannis-Hadjopoulos M. J. Mol. Biol. 1987; PubMed Scopus Google Scholar, L. Price G.B. Zannis-Hadjopoulos M. J. Biol. Chem. Full Text PDF PubMed Google Scholar). The DNA was by conventional using for a of number H. Y. B. Mol. Cell. Biol. 1994; 14: PubMed Scopus Google Scholar, Mol. Cell. 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Cell. 2001; PubMed Scopus Google Scholar), followed by is an that efficiently and in vivo by of proteins bound to DNA or to each are to proteins to target DNA in from to see the was by at D. F.D. Price G.B. Zannis-Hadjopoulos M. Mol. Biol. Cell. 2001; PubMed Scopus Google Scholar), the was In contrast, the from cells or but cells did in 2 that formaldehyde is immunoprecipitation and that the is the is as previously D. F.D. Price G.B. Zannis-Hadjopoulos M. Mol. Biol. Cell. 2001; PubMed Scopus Google Scholar). using that was by the did the the of the whereas the of S. cerevisiae or DNA as the the of in cells was due to the was using anti-Bmh1p/Bmh2p Bmh1p and Bmh2p were detected with the from the or cells In contrast, these proteins were detected in the that was by the was to the of Bmh1p and Bmh2p associated with the cell S. cerevisiae wild-type cells were to and and the was by cell analysis cells at of the cell cycle were to in vivo formaldehyde and immunoprecipitation with anti-Bmh1p/Bmh2p antibody or The was by using the The association of the 14-3-3 yeast Bmh1p and Bmh2p was found to at the by with the and contrast, the that were by the were of for the binding of the cerevisiae to cruciform-containing DNA. The that similar to human (15Todd A. Cossons N. Aitken A. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1998; 37: 14317-14325Crossref PubMed Scopus (48) Google D. C.E. Price G.B. Zannis-Hadjopoulos M. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar), Bmh1p and Bmh2p have cruciform-binding activity in and in of the with the nuclear extracts from the and the function of these yeast isoforms as cruciform-binding proteins, which was in vivo by the immunoprecipitation The that was with the that the cerevisiae Bmh1p and Bmh2p are associated with or ARS307, an of DNA replication cerevisiae H. Y. B. Mol. Cell. Biol. 1994; 14: PubMed Scopus Google Scholar, Mol. Cell. Biol. 1994; 14: PubMed Scopus Google Scholar). the cell cycle studies that the association of Bmh1p and Bmh2p with is at the of to has been for some mammalian 14-3-3 isoforms and D. C.E. Price G.B. Zannis-Hadjopoulos M. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). of the cell association of the 14-3-3 yeast with a to in The 14-3-3 plant homologue GF14 was also able to a with cruciform DNA, the that 14-3-3 proteins from each The of in the presence of in the that cruciform-binding activity is a function of the 14-3-3 yeast to the cruciform-containing DNA as a (15Todd A. Cossons N. Aitken A. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1998; 37: 14317-14325Crossref PubMed Scopus (48) Google Scholar). The of the isoforms or group has that the mammalian isoforms have a DNA replication in D. C.E. Price G.B. Zannis-Hadjopoulos M. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). Here, we have shown by the cruciform DNA and using S. cerevisiae that the Bmh1p-Bmh2p was in binding to cruciform DNA of the Although of nuclear extract from were able to a of cruciform was with the nuclear extract from the cells, in which a Bmh1p-Bmh1p is the cruciform-binding activity of because proteins that from the with wild-type nuclear extracts did because the Bmh1p-Bmh2p was in binding to cruciform-containing DNA the Bmh2p-Bmh2p there some from is also that the association with Bmh2p cruciform-binding activity to the Bmh1p The association of Bmh1p and Bmh2p with cruciform-containing DNA was structure-specific because cruciform was able to the complex, a binding similar to the with human (18Pearson C.E. Ruiz M.T. Price G.B. Zannis-Hadjopoulos M. Biochemistry. 1994; 33: 14185-14196Crossref PubMed Scopus (36) Google Scholar). The of cruciform in the initiation of prokaryotic and eukaryotic DNA replication have been by (20Lin L.-S. Meyer R.J. Nucleic Acids Res. 1987; 15: 8319-8331Crossref PubMed Scopus (38) Google Scholar, 21Noirot P. Bargonetti J. Novick R.P. Proc. Natl. Acad. Sci. U. S. A. 1990; 87: 8560-8564Crossref PubMed Scopus (82) Google Scholar, 22Jin R. Novick R.P. Plasmid. 2001; 46: 95-105Crossref PubMed Scopus (12) Google Scholar, G.P. Hall T.C. J. Virol. 1992; 66: 674-684Crossref PubMed Google Scholar, M. Frappier L. Khoury M. Price G.B. EMBO J. 1988; 7: 1837-1844Crossref PubMed Scopus (60) Google Scholar, D. C.E. Price G.B. Zannis-Hadjopoulos M. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). In the of the presence of cruciform at yeast of DNA replication has been anti-cruciform DNA antibody immunoprecipitation and conventional we for the the presence of cruciform at the yeast of DNA replication ARS307. analysis of the sequence and its that of to and to at and respectively, did the of but that of to at did the a in Mol. Cell. Biol. 1990; PubMed Scopus Google Scholar). The for of the to the of cruciform The of cruciform and to at the of cruciform R.R. DNA and Scholar). The at and the at which are the of the to the and of a cruciform at that whereas the at which is at the of the In an at the with an to of the of the binding of anti-cruciform DNA monoclonal that these at the of the L. Price G.B. Zannis-Hadjopoulos M. J. Mol. Biol. 1987; PubMed Scopus Google Scholar, L. Price G.B. Zannis-Hadjopoulos M. J. Biol. Chem. Full Text PDF PubMed Google Scholar, K. Zannis-Hadjopoulos M. Price G.B. J. Mol. Biol. 1995; Scopus Google Scholar). the at the of the cruciform the at the binding of these monoclonal to the The finding of a cruciform to the sequence that DNA cruciform of initiation the of yeast revealed a novel of and the cruciform DNA CBP with the of the cruciform in an C.E. Zannis-Hadjopoulos M. Price G.B. Zorbas H. EMBO J. 1995; 14: 1571-1580Crossref PubMed Scopus (37) Google Scholar). the of in cruciform association to of and 14-3-3 isoforms sequence that are across all J. Mol. Evol. PubMed Scopus Google Scholar). The of mammalian 14-3-3 bound to peptides revealed that all in the of the K. J. Volinia S. Cantley L.C. Smerdon S.J. Gamblin S.J. M.B. Mol. Cell. 1999; Full Text Full Text PDF PubMed Scopus Google Scholar). We are some of the 14-3-3 yeast that the of We G. P. H. van Heusden for the S. cerevisiae and the antibody 14-3-3 yeast and R. J. Ferl for the monoclonal antibody the 14-3-3 We C. for sequence ARS307. We also for in analysis of yeast

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