Nucleosome Assembly Protein 1 Exchanges Histone H2A-H2B Dimers and Assists Nucleosome Sliding

Eukaryotic chromatin is highly dynamic and turns over rapidly even in the absence of DNA replication. Here we show that the acidic histone chaperone nucleosome assembly protein 1 (NAP-1) from yeast reversibly removes and replaces histone protein dimer H2A-H2B or histone variant dimers from assembled nucleosomes, resulting in active histone exchange. Transient removal of H2A-H2B dimers facilitates nucleosome sliding along the DNA to a thermodynamically favorable position. Histone exchange as well as nucleosome sliding is independent of ATP and relies on the presence of the C-terminal acidic domain of yeast NAP-1, even though this region is not required for histone binding and chromatin assembly. Our results suggest a novel role for NAP-1 (and perhaps other acidic histone chaperones) in mediating chromatin fluidity by incorporating histone variants and assisting nucleosome sliding. NAP-1 may function either untargeted (if acting alone) or may be targeted to specific regions within the genome through interactions with additional factors. Eukaryotic chromatin is highly dynamic and turns over rapidly even in the absence of DNA replication. Here we show that the acidic histone chaperone nucleosome assembly protein 1 (NAP-1) from yeast reversibly removes and replaces histone protein dimer H2A-H2B or histone variant dimers from assembled nucleosomes, resulting in active histone exchange. Transient removal of H2A-H2B dimers facilitates nucleosome sliding along the DNA to a thermodynamically favorable position. Histone exchange as well as nucleosome sliding is independent of ATP and relies on the presence of the C-terminal acidic domain of yeast NAP-1, even though this region is not required for histone binding and chromatin assembly. Our results suggest a novel role for NAP-1 (and perhaps other acidic histone chaperones) in mediating chromatin fluidity by incorporating histone variants and assisting nucleosome sliding. NAP-1 may function either untargeted (if acting alone) or may be targeted to specific regions within the genome through interactions with additional factors. The organization of DNA into chromatin has profound consequences for all processes that involve the DNA template, and the biochemical makeup of the nucleosome has important regulatory functions. The nucleosome consists of an octamer of two copies each of the four histone proteins H2A, H2B, H3, and H4, around which 147 bp of DNA are wrapped in 1.65 superhelical turns (1Luger K. Maeder A.W. Richmond R.K. Sargent D.F. Richmond T.J. Nature. 1997; 389: 251-259Crossref PubMed Scopus (7141) Google Scholar). A (H3-H4)2 tetramer organizes the central ∼70 bp of DNA and is flanked on either side by one H2A-H2B dimer that each organizes about 40 bp of DNA. Structural and functional variability is introduced by highly regulated reversible post-translational modifications of individual histones and by the introduction of histone variants, in particular H2A and H3 variants, at specific regions in the genome (for review, see Refs. 2Khorasanizadeh S. Cell. 2004; 116: 259-272Abstract Full Text Full Text PDF PubMed Scopus (532) Google Scholar and 3Malik H.S. Henikoff S. Nat. Struct. Biol. 2003; 10: 882-891Crossref PubMed Scopus (431) Google Scholar). Despite the high degree of DNA compaction, chromatin is surprisingly dynamic and fluidic, and its histone components are exchanged at a high rate in the absence of transcription and replication. Histone H2A-H2B dimers (and, to a certain extent, also (H3-H4)2 tetramers) appear to be in rapid exchange in most regions of compacted chromatin (4Jackson V. Biochemistry. 1990; 29: 719-731Crossref PubMed Scopus (221) Google Scholar, 5Kimura H. Cook P.R. J. Cell Biol. 2001; 153: 1341-1353Crossref PubMed Scopus (556) Google Scholar), and histone variants are incorporated in replication-independent assembly pathways (e.g. Ref. 6Ahmad K. Henikoff S. Mol. Cell. 2002; 9: 1191-1200Abstract Full Text Full Text PDF PubMed Scopus (903) Google Scholar). ATP-dependent chromatin remodeling factors, in collaboration with histone modifying activities, further enhance chromatin fluidity (7Flaus A. Owen-Hughes T. Curr. Opin. Genet. Dev. 2001; 11: 148-154Crossref PubMed Scopus (161) Google Scholar, 8Becker P.B. Horz W. Annu. Rev. Biochem. 2002; 71: 247-273Crossref PubMed Scopus (633) Google Scholar, 9Geiman T.M. Robertson K.D. J. Cell. Biochem. 2002; 87: 117-125Crossref PubMed Scopus (257) Google Scholar), with pronounced effects on gene expression patterns. The transient removal of one or both H2A-H2B dimers from a nucleosome is involved in many vital cellular processes. For example, it has been known for more than 20 years that transcriptionally active chromatin is depleted in H2A and H2B (10Baer B.W. Rhodes D. Nature. 1983; 301: 482-488Crossref PubMed Scopus (180) Google Scholar). The FACT complex is likely to be at least in part responsible (11Belotserkovskaya R. Oh S. Bondarenko V.A. Orphanides G. Studitsky V.M. Reinberg D. Science. 2003; 301: 1090-1093Crossref PubMed Scopus (666) Google Scholar), but a possible role for the histone chaperone NAP-1 1The abbreviations used are: NAP-1, nucleosome assembly protein 1; GST, glutathione S-transferase; CPM, 7-diethylamino-3-(4′-maleimidylphenyl)-4-methylcoumarin; yNAP-1, yeast NAP-1; NCP, nucleosome core particle; MNase, micrococcal nuclease. has also been described recently (12Levchenko V. Jackson V. Biochemistry. 2004; 43: 2359-2372Crossref PubMed Scopus (56) Google Scholar). RNA polymerase II alone is also able to displace H2A-H2B dimers during elongation in vitro (13Kireeva M.L. Walter W. Tchernajenko V. Bondarenko V. Kashlev M. Studitsky V.M. Mol. Cell. 2002; 9: 541-552Abstract Full Text Full Text PDF PubMed Scopus (360) Google Scholar). H2A-H2B destabilization occurs as a consequence of nucleosome sliding catalyzed by several chromatin remodeling complexes (14Bruno M. Flaus A. Stockdale C. Rencurel C. Ferreira H. Owen-Hughes T. Mol. Cell. 2003; 12: 1599-1606Abstract Full Text Full Text PDF PubMed Scopus (162) Google Scholar). Finally, it was recently found that a specific ATP-dependent chromatin remodeling factor, Swr1, is responsible for the replication-independent incorporation of the histone variant H2A.Z into yeast chromatin (for review, see Ref. 15Korber P. Horz W. Cell. 2004; 117: 5-7Abstract Full Text Full Text PDF PubMed Scopus (52) Google Scholar). Histones are highly basic and are usually found in complex with histone chaperones when not bound to DNA (for review, see Ref. 16Loyola A. Almouzni G. Biochim. Biophys. Acta. 2004; 1677: 3-11Crossref PubMed Scopus (279) Google Scholar). These acidic proteins (several nonrelated families exist) are quite abundant in most eukaryotic cells, but their role in nucleosome turnover has not been investigated thoroughly (for review, see Refs. 17Tyler J.K. Eur. J. Biochem. 2002; 269: 2268-2274Crossref PubMed Scopus (124) Google Scholar and 18Akey C.W. Luger K. Curr. Opin. Struct. Biol. 2003; 13: 6-14Crossref PubMed Scopus (166) Google Scholar). A renewal of interest has come with the recent discovery in yeast that the acidic histone chaperone NAP-1 is found in association with an H2A.Z-H2B dimer in vivo. This NAP·Z complex is thought to supply H2A.Z-H2B dimers to the Swr1 complex (19Krogan N.J. Keogh M.C. Datta N. Sawa C. Ryan O.W. Ding H. Haw R.A. Pootoolal J. Tong A. Canadien V. Richards D.P. Wu X. Emili A. Hughes T.R. Buratowski S. Greenblatt J.F. Mol. Cell. 2003; 12: 1565-1576Abstract Full Text Full Text PDF PubMed Scopus (478) Google Scholar, 20Mizuguchi G. Shen X. Landry J. Wu W.H. Sen S. Wu C. Science. 2004; 303: 343-348Crossref PubMed Scopus (1015) Google Scholar, 21Kobor M.S. Venkatasubrahmanyam S. Meneghini M.D. Gin J.W. Jennings J.L. Link A.J. Madhani H.D. Rine J. PloS. Biol. 2004; 2: E131Crossref PubMed Scopus (474) Google Scholar) to promote assembly of H2A.Z-containing NAP-1 is an acidic protein of with a of and a of of all are either or in several acidic The of NAP-1 is T. M. R. Mol. Cell. Biol. PubMed Scopus Google Scholar), but their is most of its its in histone and nucleosome assembly are NAP-1 to in vivo. NAP-1 is a part of the chromatin assembly that the assembly of T. M. R. Mol. Cell. Biol. PubMed Scopus Google Scholar, T. J.K. M. R. J. Biol. Full Text Full Text PDF PubMed Scopus Google Scholar). NAP-1 and other acidic histone chaperones also to with complexes in chromatin remodeling and to transcription binding to DNA in vitro H. J.L. J. 13: PubMed Scopus Google Scholar, J. J. J.L. Science. PubMed Scopus Google Scholar, Owen-Hughes J. J.L. Mol. Cell. Biol. PubMed Scopus Google Scholar). functional and interactions and NAP-1 H. S. T. T. T. T. M. Mol. Cell. Biol. 2002; PubMed Scopus Google Scholar, N. M. C.W. W. Mol. Cell. Biol. PubMed Scopus Google Scholar, M. G. Mol. Cell. Biol. 2004; PubMed Scopus (56) Google Scholar). of the NAP-1 gene in yeast pronounced on yeast G. Ding H. H. X. J. M. X. G. H. J. C. G. S. N. H. P. C. Ryan R. T. J. H. S. C. Rine J. Greenblatt J. M. A. G. H. C. Science. 2004; 303: PubMed Scopus Google Scholar), in its expression of NAP-1 in yeast has that the transcription of of all yeast by at least K. K. A. Biochem. Biophys. 2003; PubMed Scopus Google Scholar). of the NAP-1 gene in is S. T. J. 2003; PubMed Google Scholar). has that yeast NAP-1 as an dimer in Biochemistry. 2004; 43: PubMed Scopus Google Scholar). of NAP-1 in vitro is on its to into DNA in the presence of core histones T. A. A. J. Biol. Full Text PDF PubMed Google Scholar) and to on chromatin J. Biol. Full Text Full Text PDF PubMed Scopus Google Scholar) a that has been for in vitro nucleosome assembly 2003; PubMed Scopus Google Scholar). it was also that of and for histone binding and in vitro assembly and that a at the was for its assembly in vitro T. A. A. J. Biol. Full Text PDF PubMed Google Scholar, J.K. Luger K. J. Biol. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar). The described be to the well of NAP-1 to and histone complexes J.K. Luger K. J. Biol. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar and a the interactions of NAP-1 or other chaperone with and chromatin or its on chromatin and (12Levchenko V. Jackson V. Biochemistry. 2004; 43: 2359-2372Crossref PubMed Scopus (56) Google Scholar, Owen-Hughes J. J.L. Mol. Cell. Biol. PubMed Scopus Google Scholar, T. T. T. M. Dev. PubMed Google Scholar, M. Flaus A. Owen-Hughes T. 2004; PubMed Scopus Google Scholar). Here we as a to and histone chaperones to dynamic histone a that is as an of eukaryotic histones and we that the absence of ATP or other protein is of H2A-H2B dimers from and histone dimers an H2A variant into assembled the of to nucleosome sliding on DNA and show that this the transient of H2A-H2B dimers from nucleosome core of yNAP-1, and DNA from a gene S. A. 1983; PubMed Scopus Google Scholar) was as described S. Luger K. 2004; PubMed Scopus Google Scholar). of the DNA with Luger K. J. Biol. 2004; Full Text Full Text PDF PubMed Scopus Google Scholar). the and used Luger K. J. Biol. 2004; Full Text Full Text PDF PubMed Scopus Google Scholar). histones and histone H2A variants histone and H2A to histone dimer or by as described S. Luger K. 2004; PubMed Scopus Google Scholar) and by on in yNAP-1, and and and as described J.K. Luger K. J. Biol. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar). The C-terminal domain of was over a The was with by over a of H2A-H2B from the histones or DNA as described was with of at for in A 1 H2A-H2B dimer was by as described and from into and by was with a of from the Histone was with dimer H2A-H2B dimer and at for in A. dimer as a The exchange of H2A-H2B dimer or dimer was by as described was by to at by with as (H3-H4)2 tetramer assembled on a DNA from the gene S. A. 1983; PubMed Scopus Google Scholar, S. A. 1990; 87: PubMed Scopus Google Scholar). at the or of the DNA by with Cell described for S. Luger K. 2004; PubMed Scopus Google Scholar). in the presence or absence of was at for in A. was with the of by of and of with of micrococcal at K. S. D. Luger K. J. 2004; PubMed Scopus Google Scholar). histone on a in and the nucleosome into for at and The was and by and used to for was with of for at with at a of The DNA on a and by with H2A-H2B from the the in resulting from we used a highly for nucleosome S. Luger K. 2004; PubMed Scopus Google Scholar), in with Luger K. J. Biol. 2004; Full Text Full Text PDF PubMed Scopus Google Scholar). that binding was not least by the of the to H2B and that a dimer complex was in was in all in which H2A-H2B or H2A.Z-H2B dimers The of the dimer complex has been to be one dimer J.K. Luger K. J. Biol. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar). this into the of Biochemistry. 2004; 43: PubMed Scopus Google Scholar). of with H2B with of yNAP-1, two by and one additional that is also in the in two of with and that additional at is with and at the of dimer over of DNA are The was and the of the and the of to This that is in at a dimer to of and that at the of was to be further the of each we the and in which H2B, H4, or the DNA was as described Luger K. J. Biol. 2004; Full Text Full Text PDF PubMed Scopus Google Scholar). The with a of dimer over to in and the by The to we not tetramer complexes and at a for and a of over NCP, of the (H3-H4)2 tetramer from the DNA was show that and (H3-H4)2 and H2A-H2B dimers both of with DNA and H2B are with the that we this particular DNA and is as a with an of the DNA with to the histone octamer A. Luger K. S. Richmond T.J. S. A. PubMed Scopus Google Scholar, R.K. S. Luger K. 2003; PubMed Scopus Google Scholar). (H3-H4)2 tetramer and but H2A-H2B dimer and and is as a (H3-H4)2 H2A-H2B dimer but DNA or (H3-H4)2 tetramer and with a dimer complex of novel from DNA that been with at the at or at Luger K. J. Biol. 2004; Full Text Full Text PDF PubMed Scopus Google Scholar). in the presence or absence of a of and as in and in the absence and presence of and in the absence and presence of and in the absence and presence of H2A-H2B dimer with of complex was by 1 and with and or with and dimer complex is of the protein of nucleosome by and from in protein and the is specific for H2A-H2B dimer or DNA was with a of or a of at for dimer with and or and and and was with or as that yNAP-1, we a with and its by is as in to and but is with the of to we an additional on with Our show of a complex the of and and from a and the protein of by with of the results we found that and of the four histone H3 and H4, that at removes both H2A-H2B dimers from a results a of we also that H2A, H2B, and is highly it is possible that the removal of H2A-H2B dimers from the is a of and DNA and for the the of in H2A-H2B dimer we the of and to the is a protein of and acidic yNAP-1, a of on the with and with H2A-H2B dimer or of the was of an to of not The of for the of the H2A-H2B from the NCP, for Histone and that the domain and the acidic of are not required for histone binding and nucleosome assembly T. A. A. J. Biol. Full Text PDF PubMed Google Scholar, J.K. Luger K. J. Biol. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar). regions of are required for the interactions with the we the of from the or the and C-terminal to H2A-H2B dimers from the the to H2A-H2B dimers from the has the to the This was of two and the alone has on the as has been for is possible that the in the absence of the and this to be yNAP-1, and are all of a complex with the H2A-H2B dimer and with of J.K. Luger K. J. Biol. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar). the core domain of is to the H2A-H2B dimer in as well as to chromatin from DNA and histone this core domain is not to H2A-H2B dimers are assembled into a functional but the acidic H2A-H2B in and of by that is of H2A-H2B dimers from a NCP, we to is of one H2A-H2B dimer with the exchanged and and to the that with the in we of histone A of H2A-H2B dimer was with to complex not The by and by in about of the nucleosome four independent was as in the of a when with a dimer but not with dimer or alone A to the dimer complex is also in 1 and of DNA are in this as is in the with tetramer complex incorporation of (H3-H4)2 tetramer into was not a dimer complex was with complex or complex was not also see Ref. T. M. M. T. J. Biol. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar). results that H2A-H2B dimer exchange not by of the and that the exchange is to the histone H2A-H2B the of to the (H3-H4)2 tetramer in with or J.K. Luger K. J. Biol. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar). is of H2A-H2B dimer with a dimer an H2A not a to the with several histone variant complexes of with a was These show that exchange of histone H2A-H2B dimers into Our that histone variants are bound by and are in this exchange to that not H2A.Z but other H2A histone variants in complex with H2B may be exchanged into assembled of with on a DNA at we a in and which a of histone proteins and DNA and with a well that is on this particular DNA This an in which the histone octamer is on the it is over at but be into a thermodynamically more favorable in which the DNA is around the histone octamer by at (e.g. and that the that of the histone octamer along the DNA is by the transient removal of the H2A-H2B further the that facilitates nucleosome we on a DNA from the gene S. A. 1983; PubMed Scopus Google Scholar). two nucleosome and are These been described as with S. A. 1990; 87: PubMed Scopus Google Scholar). The two from each other by and that and an and of histones 1 and with of the that both bp of DNA and with was into in the presence of of dimer and The was at as as that on the of in the absence of at and on the of either or the histone of both and the of DNA that is with micrococcal of with results in nucleosome it was to the of the histone octamer with to the DNA in and and in with micrococcal for and in the DNA are in the absence of yNAP-1, is to about with and and an with this the two of and bp in be this that the regions of the DNA not by are of bound with the that bp are from with this is with for at either of the DNA is to with but is from with and This bp and which to the on this particular DNA Cell. Full Text PDF PubMed Scopus Google Scholar). with not the of in and with the that has on the of in and and and a of all four histones that nucleosome sliding. investigated the of to exchange histone H2A-H2B dimers is required to nucleosome sliding. this we that a of was of histone dimers from nucleosomes, this was of chromatin and binding histone and used as was with a of the as and by in and able to the of to with the of a complex and was in the presence of and dimer was This that transient H2A-H2B dimer from the facilitates nucleosome sliding in the presence of of DNA are and (H3-H4)2 tetramer is not that nucleosome sliding occurs nucleosome was the with nucleosome core on DNA that to in all by in is an acidic histone chaperone that has been to be involved in histone and chromatin assembly. Here we that is also of H2A-H2B dimers from a This results in the active exchange of H2A-H2B or histone variant dimers into in an DNA replication-independent but also facilitates sliding of the nucleosome along the DNA to it a thermodynamically more favorable position. These for are likely to be of and may be a of acidic histone facilitates the removal of one or both H2A-H2B dimers from a nucleosome at of the (H3-H4)2 tetramer is at This is with results T. T. T. M. Dev. PubMed Google Scholar) and with the rapid exchange of H2A-H2B dimers in (4Jackson V. Biochemistry. 1990; 29: 719-731Crossref PubMed Scopus (221) Google Scholar, 5Kimura H. Cook P.R. J. Cell Biol. 2001; 153: 1341-1353Crossref PubMed Scopus (556) Google Scholar) and is one the central of the (H3-H4)2 tetramer on the DNA (1Luger K. Maeder A.W. Richmond R.K. Sargent D.F. Richmond T.J. Nature. 1997; 389: 251-259Crossref PubMed Scopus (7141) Google Scholar). The removal of H2A-H2B dimers is likely to transcription (12Levchenko V. Jackson V. Biochemistry. 2004; 43: 2359-2372Crossref PubMed Scopus (56) Google Scholar, T. T. T. M. Dev. PubMed Google Scholar). This has also been recently to the FACT complex (11Belotserkovskaya R. Oh S. Bondarenko V.A. Orphanides G. Studitsky V.M. Reinberg D. Science. 2003; 301: 1090-1093Crossref PubMed Scopus (666) Google see also Ref. S. T. Mol. Cell. Biol. 2004; PubMed Scopus Google Scholar). of transcription to DNA in the presence of acidic histone chaperone with a and to and has also been to their to of H2A-H2B dimers H. J.L. J. 13: PubMed Scopus Google Scholar, Owen-Hughes J. J.L. Mol. Cell. Biol. PubMed Scopus Google Scholar). nucleosome and has as an important of the H. Horz W. Mol. Cell. 2003; 11: Full Text Full Text PDF PubMed Scopus Google Scholar, H. J. Mol. Cell. 2004; Full Text Full Text PDF PubMed Scopus Google Scholar). The recent that the histone chaperone nucleosome from the in J.K. Mol. Cell. 2004; Full Text Full Text PDF PubMed Scopus (257) Google Scholar) that histone chaperones in may a more role than in nucleosome during Here we that the of to a H2A-H2B dimer from a nucleosome on the acidic of yNAP-1, which is for histone binding and nucleosome assembly J.K. Luger K. J. Biol. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar and histone removal from a nucleosome is not a of the involved in histone during nucleosome assembly. The acidic of the in the of a of in the are of all acidic in the may be required to with the DNA for the histone or it may to histone removal a more complex that to be the acidic of the FACT is required for with the in of yNAP-1, it to be required also for histone DNA (11Belotserkovskaya R. Oh S. Bondarenko V.A. Orphanides G. Studitsky V.M. Reinberg D. Science. 2003; 301: 1090-1093Crossref PubMed Scopus (666) Google Scholar). The removal of one or both H2A-H2B dimers from a is reversible and to an exchange with histone dimers variants of histone H2A, as H2A.Z and and also the in which a histone nucleosome is into a nucleosome not the of that has for H2A-H2B both in and when bound to a histone exchange is independent of not and not in the of a of DNA or exchange of (H3-H4)2 This that nucleosome and are not alone is to histone variants to specific regions within it is possible that and other assembly proteins to the incorporation of histone variants at specific regions within chromatin association with histone chromatin assembly factors, as the Swr1 complex that in with a dimer complex (19Krogan N.J. Keogh M.C. Datta N. Sawa C. Ryan O.W. Ding H. Haw R.A. Pootoolal J. Tong A. Canadien V. Richards D.P. Wu X. Emili A. Hughes T.R. Buratowski S. Greenblatt J.F. Mol. Cell. 2003; 12: 1565-1576Abstract Full Text Full Text PDF PubMed Scopus (478) Google Scholar, 20Mizuguchi G. Shen X. Landry J. Wu W.H. Sen S. Wu C. Science. 2004; 303: 343-348Crossref PubMed Scopus (1015) Google Scholar, 21Kobor M.S. Venkatasubrahmanyam S. Meneghini M.D. Gin J.W. Jennings J.L. Link A.J. Madhani H.D. Rine J. PloS. Biol. 2004; 2: E131Crossref PubMed Scopus (474) Google The Swr1 complex the exchange of an H2A-H2B dimer for an H2A.Z-H2B dimer in yeast in an ATP-dependent in both and in Despite the presence of the see exchange in the absence of ATP in to the of exchange of Finally, we that the of to one or both H2A-H2B dimers from a nucleosome facilitates nucleosome sliding from a to an more favorable position. Our that in a independent of A of the acidic which is of binding histones and chromatin but has its to a H2A-H2B dimer from the NCP, is of this sliding we not the that the C-terminal and functions. is in that nucleosome from the to the central is the ATP-dependent remodeling and its which also to an but is to from the to the of the DNA G. P.B. J. Cell 2001; PubMed Google Scholar). it has been found that and the of binding to by the that histone chaperones and remodeling may J. J. J.L. Science. PubMed Scopus Google Scholar). the of and as is the by which is likely to be nucleosome sliding on its to and one or both H2A-H2B in the presence of ATP-dependent dimer exchange occurs to the of from their with and to the of at at and DNA that destabilization is not an in nucleosome (14Bruno M. Flaus A. Stockdale C. Rencurel C. Ferreira H. Owen-Hughes T. Mol. Cell. 2003; 12: 1599-1606Abstract Full Text Full Text PDF PubMed Scopus (162) Google Scholar). not from ATP to the histone dimer or to the is not a and not along the but to the that nucleosome sliding to favorable of the of acidic histone chaperones which is one are abundant in the their in role may well be For example, histone chaperones may a role in H2A variants into chromatin in a replication-independent and in nucleosome along the DNA by the that for nucleosome sliding. NAP-1 may also to the and of during transcription and as The role of NAP-1 (and that of other acidic histone chaperones) is from as a histone that histone into the its over to chromatin assembly and remodeling factors, to a more role in chromatin and nucleosome fluidity and has been as an that an (and an RNA displace Cell. Full Text PDF PubMed Scopus Google Scholar). is as a highly dynamic and assembly that is of with the cellular to be on this is and many that are involved in this important of chromatin to be with

Fetched live from OpenAlex and de-inverted. Abstracts are not stored in this database: the inverted indexes are 8.6 GB of the frame’s 9.3 GB of text, and the host has 13 GB free.