Histone chaperones link histone nuclear import and chromatin assembly

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1819, Issue 3-4, 2012, Pages 277-289

  Keck, Kristin M ^a   Pemberton, Lucy F ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Asf1; Histone acetylation; Histone chaperone; Importin; Nap1; NASP

Indexed keywords

CHAPERONE; DAXX PROTEIN; HISTONE H3; HISTONE H4; KARYOPHERIN; NUCLEOPHOSMIN; NUCLEOPLASMIN; NUCLEOSOME ASSEMBLY PROTEIN 1;

BIOGENESIS; CELL TRANSPORT; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOPLASM; HUMAN; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; YEAST CELL;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; CHROMATIN ASSEMBLY AND DISASSEMBLY; HISTONE CHAPERONES; HISTONES; HUMANS; NUCLEOSOME ASSEMBLY PROTEIN 1;

MAMMALIA;

EID: 84857109450     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2011.09.007     Document Type: Review

References (182)

1. Luger K., Mader A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8A resolution. Nature 1997, 389:251-260.
2. White C.L., Suto R.K., Luger K. Structure of the yeast nucleosome core particle reveals fundamental changes in internucleosome interactions. EMBO J. 2001, 20:5207-5218.
3. Nakagawa T., Bulger M., Muramatsu M., Ito T. Multistep chromatin assembly on supercoiled plasmid DNA by nucleosome assembly protein-1 and ATP-utilizing chromatin assembly and remodeling factor. J. Biol. Chem. 2001, 276:27384-27391.
4. Smith S., Stillman B. Stepwise assembly of chromatin during DNA replication in vitro. EMBO J. 1991, 10:971-980.
5. A.T. Annunziato, Assembling chromatin: the long and winding road, Biochim. Biophys. Acta, This issue (2011).
6. S.J. Elsasser, S. D'Arcy, Towards a mechanism for histone chaperones, Biochim. Biophys. Acta, This issue (2011).
7. Ito T., Bulger M., Kobayashi R., Kadonaga J.T. Drosophila NAP-1 is a core histone chaperone that functions in ATP-facilitated assembly of regularly spaced nucleosomal arrays. Mol. Cell. Biol. 1996, 16:3112-3124.
8. Bowman G.D. Mechanisms of ATP-dependent nucleosome sliding. Curr. Opin. Struct. Biol. 2010, 20:73-81.
9. Corpet A., Almouzni G. Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information. Trends Cell Biol. 2009, 19:29-41.
10. Das C., Tyler J.K., Churchill M.E. The histone shuffle: histone chaperones in an energetic dance. Trends Biochem. Sci. 2010, 35:476-489.
11. Hargreaves D.C., Crabtree G.R. ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res. 2011, 21:396-420.
12. Q. Li, R. Burgess, Z. Zhang, All roads lead to chromatin: multiple pathways for histone deposition, Biochim. Biophys. Acta, This issue (2011).
13. Eitoku M., Sato L., Senda T., Horikoshi M. Histone chaperones: 30years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell Mol. Life Sci. 2008, 65:414-444.
14. Rocha W., Verreault A. Clothing up DNA for all seasons: histone chaperones and nucleosome assembly pathways. FEBS Lett. 2008, 582:1938-1949.
15. McBryant S.J., Park Y.J., Abernathy S.M., Laybourn P.J., Nyborg J.K., Luger K. Preferential binding of the histone (H3-H4)2 tetramer by NAP1 is mediated by the amino-terminal histone tails. J. Biol. Chem. 2003, 278:44574-44583.
16. Ishimi Y., Kojima M., Yamada M., Hanaoka F. Binding mode of nucleosome-assembly protein (AP-I) and histones. Eur. J. Biochem. 1987, 162:19-24.
17. Bowman A., Ward R., Wiechens N., Singh V., El-Mkami H., Norman D.G., Owen-Hughes T. The histone chaperones Nap1 and Vps75 bind histones H3 and H4 in a tetrameric conformation. Mol. Cell 2011, 41:398-408.
18. Ransom M., Dennehey B.K., Tyler J.K. Chaperoning histones during DNA replication and repair. Cell 2010, 140:183-195.
19. Stuwe T., Hothorn M., Lejeune E., Rybin V., Bortfeld M., Scheffzek K., Ladurner A.G. The FACT Spt16 "peptidase" domain is a histone H3-H4 binding module. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:8884-8889.
20. Belotserkovskaya R., Oh S., Bondarenko V.A., Orphanides G., Studitsky V.M., Reinberg D. FACT facilitates transcription-dependent nucleosome alteration. Science 2003, 301:1090-1093.
21. VanDemark A.P., Xin H., McCullough L., Rawlins R., Bentley S., Heroux A., Stillman D.J., Hill C.P., Formosa T. Structural and functional analysis of the Spt16p N-terminal domain reveals overlapping roles of yFACT subunits. J. Biol. Chem. 2008, 283:5058-5068.
22. T. Formosa, The role of FACT in making and breaking nucleosomes, Biochim. Biophys. Acta, This issue (2011).
23. Laskey R.A., Honda B.M., Mills A.D., Finch J.T. Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 1978, 275:416-420.
24. Kleinschmidt J.A., Fortkamp E., Krohne G., Zentgraf H., Franke W.W. Co-existence of two different types of soluble histone complexes in nuclei of Xenopus laevis oocytes. J. Biol. Chem. 1985, 260:1166-1176.
25. Kleinschmidt J.A., Franke W.W. Soluble acidic complexes containing histones H3 and H4 in nuclei of Xenopus laevis oocytes. Cell 1982, 29:799-809.
26. Winkler D.D., Luger K. The histone chaperone FACT: structural insights and mechanisms for nucleosome reorganization. J. Biol. Chem. 2011, 286:18369-18374.
27. Luk E., Vu N.D., Patteson K., Mizuguchi G., Wu W.H., Ranjan A., Backus J., Sen S., Lewis M., Bai Y., Wu C. Chz1, a nuclear chaperone for histone H2AZ. Mol. Cell 2007, 25:357-368.
28. Straube K., Blackwell J.S., Pemberton L.F. Nap1 and Chz1 have separate Htz1 nuclear import and assembly functions. Traffic 2010, 11:185-197.
29. Mosammaparast N., Ewart C.S., Pemberton L.F. A role for nucleosome assembly protein 1 in the nuclear transport of histones H2A and H2B. EMBO J. 2002, 21:6527-6538.
30. Burgess R.J., Zhang Z. Histones, histone chaperones and nucleosome assembly. Protein Cell 2010, 1:607-612.
31. Avvakumov N., Nourani A., Cote J. Histone chaperones: modulators of chromatin marks. Mol. Cell 2011, 41:502-514.
32. Hansen J.C., Nyborg J.K., Luger K., Stargell L.A. Histone chaperones, histone acetylation, and the fluidity of the chromogenome. J. Cell. Physiol. 2010, 224:289-299.
33. Lee J.S., Smith E., Shilatifard A. The language of histone crosstalk. Cell 2010, 142:682-685.
34. Krebs J.E. Moving marks: dynamic histone modifications in yeast. Mol. Biosyst. 2007, 3:590-597.
35. Horn P.J., Peterson C.L. Heterochromatin assembly: a new twist on an old model. Chromosome Res. 2006, 14:83-94.
36. Suganuma T., Workman J.L. Signals and combinatorial functions of histone modifications. Annu. Rev. Biochem. 2011, 80:473-499.
37. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
38. Ruiz-Carrillo A., Wangh L.J., Allfrey V.G. Processing of newly synthesized histone molecules. Science 1975, 190:117-128.
39. Jackson V., Shires A., Tanphaichitr N., Chalkley R. Modifications to histones immediately after synthesis. J. Mol. Biol. 1976, 104:471-483.
40. Yuan J., Pu M., Zhang Z., Lou Z. Histone H3-K56 acetylation is important for genomic stability in mammals. Cell Cycle 2009, 8:1747-1753.
41. Xu F., Zhang K., Grunstein M. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 2005, 121:375-385.
42. Sobel R.E., Cook R.G., Perry C.A., Annunziato A.T., Allis C.D. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:1237-1241.
43. Li Q., Zhou H., Wurtele H., Davies B., Horazdovsky B., Verreault A., Zhang Z. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 2008, 134:244-255.
44. Jasencakova Z., Scharf A.N., Ask K., Corpet A., Imhof A., Almouzni G., Groth A. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol. Cell 2010, 37:736-743.
45. Kuo M.H., Brownell J.E., Sobel R.E., Ranalli T.A., Cook R.G., Edmondson D.G., Roth S.Y., Allis C.D. Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines. Nature 1996, 383:269-272.
46. Masumoto H., Hawke D., Kobayashi R., Verreault A. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 2005, 436:294-298.
47. Benson L.J., Gu Y., Yakovleva T., Tong K., Barrows C., Strack C.L., Cook R.G., Mizzen C.A., Annunziato A.T. Modifications of H3 and H4 during chromatin replication, nucleosome assembly, and histone exchange. J. Biol. Chem. 2006, 281:9287-9296.
48. Das C., Lucia M.S., Hansen K.C., Tyler J.K. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 2009, 459:113-117.
49. Tsubota T., Berndsen C.E., Erkmann J.A., Smith C.L., Yang L., Freitas M.A., Denu J.M., Kaufman P.D. Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol. Cell 2007, 25:703-712.
50. Han J., Zhou H., Horazdovsky B., Zhang K., Xu R.M., Zhang Z. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 2007, 315:653-655.
51. Driscoll R., Hudson A., Jackson S.P. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 2007, 315:649-652.
52. Loyola A., Tagami H., Bonaldi T., Roche D., Quivy J.P., Imhof A., Nakatani Y., Dent S.Y., Almouzni G. The HP1alpha-CAF1-SetDB1-containing complex provides H3K9me1 for Suv39-mediated K9me3 in pericentric heterochromatin. EMBO Rep. 2009, 10:769-775.
53. Alvarez F., Munoz F., Schilcher P., Imhof A., Almouzni G., Loyola A. Sequential establishment of marks on soluble histones H3 and H4. J. Biol. Chem. 2011, 286:17714-17721.
54. Poveda A., Pamblanco M., Tafrov S., Tordera V., Sternglanz R., Sendra R. Hif1 is a component of yeast histone acetyltransferase B, a complex mainly localized in the nucleus. J. Biol. Chem. 2004, 279:16033-16043.
55. Chook Y.M., Suel K.E. Nuclear import by karyopherin-betas: recognition and inhibition. Biochim. Biophys. Acta 2011, 1813:1593-1606.
56. Fiserova J., Goldberg M.W. Nucleocytoplasmic transport in yeast: a few roles for many actors. Biochem. Soc. Trans. 2010, 38:273-277.
57. Mingot J.M., Kostka S., Kraft R., Hartmann E., Gorlich D. Importin 13: a novel mediator of nuclear import and export. EMBO J. 2001, 20:3685-3694.
58. Yoshida K., Blobel G. The karyopherin Kap142p/Msn5p mediates nuclear import and nuclear export of different cargo proteins. J. Cell Biol. 2001, 152:729-740.
59. Cook A., Bono F., Jinek M., Conti E. Structural biology of nucleocytoplasmic transport. Annu. Rev. Biochem. 2007, 76:647-671.
60. Lange A., McLane L.M., Mills R.E., Devine S.E., Corbett A.H. Expanding the definition of the classical bipartite nuclear localization signal. Traffic 2010, 11:311-323.
61. Hodel M.R., Corbett A.H., Hodel A.E. Dissection of a nuclear localization signal. J. Biol. Chem. 2001, 276:1317-1325.
62. Lange A., Mills R.E., Lange C.J., Stewart M., Devine S.E., Corbett A.H. Classical nuclear localization signals: definition, function, and interaction with importin alpha. J. Biol. Chem. 2007, 282:5101-5105.
63. Lee D.C., Aitchison J.D. Kap104p-mediated nuclear import. Nuclear localization signals in mRNA-binding proteins and the role of Ran and Rna. J. Biol. Chem. 1999, 274:29031-29037.
64. Pemberton L.F., Rosenblum J.S., Blobel G. Nuclear import of the TATA-binding protein: mediation by the karyopherin Kap114p and a possible mechanism for intranuclear targeting. J. Cell Biol. 1999, 145:1407-1417.
65. Xu D., Farmer A., Chook Y.M. Recognition of nuclear targeting signals by Karyopherin-beta proteins. Curr. Opin. Struct. Biol. 2010, 20:782-790.
66. Stewart M. Molecular mechanism of the nuclear protein import cycle. Nat. Rev. Mol. Cell Biol. 2007, 8:195-208.
67. Loyola A., Almouzni G. Marking histone H3 variants: how, when and why?. Trends Biochem. Sci. 2007, 32:425-433.
68. Campos E.I., Fillingham J., Li G., Zheng H., Voigt P., Kuo W.H., Seepany H., Gao Z., Day L.A., Greenblatt J.F., Reinberg D. The program for processing newly synthesized histones H3.1 and H4. Nat. Struct. Mol. Biol. 2010, 17:1343-1351.
69. Blackwell J.S., Wilkinson S.T., Mosammaparast N., Pemberton L.F. Mutational analysis of H3 and H4 N termini reveals distinct roles in nuclear import. J. Biol. Chem. 2007, 282:20142-20150.
70. Mosammaparast N., Jackson K.R., Guo Y., Brame C.J., Shabanowitz J., Hunt D.F., Pemberton L.F. Nuclear import of histone H2A and H2B is mediated by a network of karyopherins. J. Cell Biol. 2001, 153:251-262.
71. Mosammaparast N., Guo Y., Shabanowitz J., Hunt D.F., Pemberton L.F. Pathways mediating the nuclear import of histones H3 and H4 in yeast. J. Biol. Chem. 2002, 277:862-868.
72. Ai X., Parthun M.R. The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. Mol. Cell 2004, 14:195-205.
73. Parthun M.R., Widom J., Gottschling D.E. The major cytoplasmic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism. Cell 1996, 87:85-94.
74. M.R. Parthun, Histone acetyltransferase 1: more than just an enzyme?, Biochim. Biophys. Acta, This issue (2011).
75. Fillingham J., Recht J., Silva A.C., Suter B., Emili A., Stagljar I., Krogan N.J., Allis C.D., Keogh M.C., Greenblatt J.F. Chaperone control of the activity and specificity of the histone H3 acetyltransferase Rtt109. Mol. Cell. Biol. 2008, 28:4342-4353.
76. Ejlassi-Lassallette A., Mocquard E., Arnaud M.C., Thiriet C. H4 replication-dependent diacetylation and Hat1 promote S-phase chromatin assembly in vivo. Mol. Biol. Cell 2011, 22:245-255.
77. Ruiz-Garcia A.B., Sendra R., Galiana M., Pamblanco M., Perez-Ortin J.E., Tordera V. HAT1 and HAT2 proteins are components of a yeast nuclear histone acetyltransferase enzyme specific for free histone H4. J. Biol. Chem. 1998, 273:12599-12605.
78. Verreault A., Kaufman P.D., Kobayashi R., Stillman B. Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase. Curr. Biol. 1998, 8:96-108.
79. Szenker E., Ray-Gallet D., Almouzni G. The double face of the histone variant H3.3. Cell Res. 2011, 21:421-434.
80. Goldberg A.D., Banaszynski L.A., Noh K.M., Lewis P.W., Elsaesser S.J., Stadler S., Dewell S., Law M., Guo X., Li X., Wen D., Chapgier A., DeKelver R.C., Miller J.C., Lee Y.L., Boydston E.A., Holmes M.C., Gregory P.D., Greally J.M., Rafii S., Yang C., Scambler P.J., Garrick D., Gibbons R.J., Higgs D.R., Cristea I.M., Urnov F.D., Zheng D., Allis C.D. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 2010, 140:678-691.
81. Tagami H., Ray-Gallet D., Almouzni G., Nakatani Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 2004, 116:51-61.
82. Parthun M.R. Hat1: the emerging cellular roles of a type B histone acetyltransferase. Oncogene 2007, 26:5319-5328.
83. Ge Z., Wang H., Parthun M.R. Nuclear Hat1p complex (NuB4) components participate in DNA repair-linked chromatin reassembly. J. Biol. Chem. 2011, 286:16790-16799.
84. Dunleavy E.M., Pidoux A.L., Monet M., Bonilla C., Richardson W., Hamilton G.L., Ekwall K., McLaughlin P.J., Allshire R.C. A NASP (N1/N2)-related protein, Sim3, binds CENP-A and is required for its deposition at fission yeast centromeres. Mol. Cell 2007, 28:1029-1044.
85. Richardson R.T., Batova I.N., Widgren E.E., Zheng L.X., Whitfield M., Marzluff W.F., O'Rand M.G. Characterization of the histone H1-binding protein, NASP, as a cell cycle-regulated somatic protein. J. Biol. Chem. 2000, 275:30378-30386.
86. Finn R.M., Browne K., Hodgson K.C., Ausio J. sNASP, a histone H1-specific eukaryotic chaperone dimer that facilitates chromatin assembly. Biophys. J. 2008, 95:1314-1325.
87. Wang H., Walsh S.T., Parthun M.R. Expanded binding specificity of the human histone chaperone NASP. Nucleic Acids Res. 2008, 36:5763-5772.
88. Richardson R.T., Alekseev O.M., Grossman G., Widgren E.E., Thresher R., Wagner E.J., Sullivan K.D., Marzluff W.F., O'Rand M.G. Nuclear autoantigenic sperm protein (NASP), a linker histone chaperone that is required for cell proliferation. J. Biol. Chem. 2006, 281:21526-21534.
89. Dimitrov S., Wolffe A.P. Remodeling somatic nuclei in Xenopus laevis egg extracts: molecular mechanisms for the selective release of histones H1 and H1(0) from chromatin and the acquisition of transcriptional competence. EMBO J. 1996, 15:5897-5906.
90. Saeki H., Ohsumi K., Aihara H., Ito T., Hirose S., Ura K., Kaneda Y. Linker histone variants control chromatin dynamics during early embryogenesis. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:5697-5702.
91. Shintomi K., Iwabuchi M., Saeki H., Ura K., Kishimoto T., Ohsumi K. Nucleosome assembly protein-1 is a linker histone chaperone in Xenopus eggs. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:8210-8215.
92. Alekseev O.M., Widgren E.E., Richardson R.T., O'Rand M.G. Association of NASP with HSP90 in mouse spermatogenic cells: stimulation of ATPase activity and transport of linker histones into nuclei. J. Biol. Chem. 2005, 280:2904-2911.
93. Groth A., Ray-Gallet D., Quivy J.P., Lukas J., Bartek J., Almouzni G. Human Asf1 regulates the flow of S phase histones during replicational stress. Mol. Cell 2005, 17:301-311.
94. Tang Y., Poustovoitov M.V., Zhao K., Garfinkel M., Canutescu A., Dunbrack R., Adams P.D., Marmorstein R. Structure of a human ASF1a-HIRA complex and insights into specificity of histone chaperone complex assembly. Nat. Struct. Mol. Biol. 2006, 13:921-929.
95. Green E.M., Antczak A.J., Bailey A.O., Franco A.A., Wu K.J., Yates J.R., Kaufman P.D. Replication-independent histone deposition by the HIR complex and Asf1. Curr. Biol. 2005, 15:2044-2049.
96. A.D. Amin, N. Vishnoi, P. Prochasson, A global requirement for the HIR complex in the assembly of chromatin, Biochim. Biophys. Acta, This issue (2011).
97. Loyola A., Bonaldi T., Roche D., Imhof A., Almouzni G. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol. Cell 2006, 24:309-316.
98. Natsume R., Eitoku M., Akai Y., Sano N., Horikoshi M., Senda T. Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature 2007, 446:338-341.
99. Tyler J.K., Adams C.R., Chen S.R., Kobayashi R., Kamakaka R.T., Kadonaga J.T. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 1999, 402:555-560.
100. Murzina N.V., Pei X.Y., Zhang W., Sparkes M., Vicente-Garcia J., Pratap J.V., McLaughlin S.H., Ben-Shahar T.R., Verreault A., Luisi B.F., Laue E.D. Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 2008, 16:1077-1085.
101. English C.M., Adkins M.W., Carson J.J., Churchill M.E., Tyler J.K. Structural basis for the histone chaperone activity of Asf1. Cell 2006, 127:495-508.
102. Shulga N., Roberts P., Gu Z., Spitz L., Tabb M.M., Nomura M., Goldfarb D.S. In vivo nuclear transport kinetics in Saccharomyces cerevisiae: a role for heat shock protein 70 during targeting and translocation. J. Cell Biol. 1996, 135:329-339.
103. Kose S., Furuta M., Koike M., Yoneda Y., Imamoto N. The 70-kD heat shock cognate protein (hsc70) facilitates the nuclear export of the import receptors. J. Cell Biol. 2005, 171:19-25.
104. Pratt W.B., Silverstein A.M., Galigniana M.D. A model for the cytoplasmic trafficking of signalling proteins involving the hsp90-binding immunophilins and p50cdc37. Cell. Signal. 1999, 11:839-851.
105. Wente S.R., Rout M.P. The nuclear pore complex and nuclear transport. Cold Spring Harb. Perspect. Biol. 2010, 2:a000562.
106. Glowczewski L., Waterborg J.H., Berman J.G. Yeast chromatin assembly complex 1 protein excludes nonacetylatable forms of histone H4 from chromatin and the nucleus. Mol. Cell. Biol. 2004, 24:10180-10192.
107. Greiner M., Caesar S., Schlenstedt G. The histones H2A/H2B and H3/H4 are imported into the yeast nucleus by different mechanisms. Eur. J. Cell Biol. 2004, 83:511-520.
108. Muhlhausser P., Muller E.C., Otto A., Kutay U. Multiple pathways contribute to nuclear import of core histones. EMBO Rep. 2001, 2:690-696.
109. Baake M., Bauerle M., Doenecke D., Albig W. Core histones and linker histones are imported into the nucleus by different pathways. Eur. J. Cell Biol. 2001, 80:669-677.
110. Morgan B.A., Mittman B.A., Smith M.M. The highly conserved N-terminal domains of histones H3 and H4 are required for normal cell cycle progression. Mol. Cell. Biol. 1991, 11:4111-4120.
111. Schuster T., Han M., Grunstein M. Yeast histone H2A and H2B amino termini have interchangeable functions. Cell 1986, 45:445-451.
112. Thiriet C., Hayes J.J. A novel labeling technique reveals a function for histone H2A/H2B dimer tail domains in chromatin assembly in vivo. Genes Dev. 2001, 15:2048-2053.
113. Rout M.P., Blobel G., Aitchison J.D. A distinct nuclear import pathway used by ribosomal proteins. Cell 1997, 89:715-725.
114. Johnson-Saliba M., Siddon N.A., Clarkson M.J., Tremethick D.J., Jans D.A. Distinct importin recognition properties of histones and chromatin assembly factors. FEBS Lett. 2000, 467:169-174.
115. Ma X.J., Lu Q., Grunstein M. A search for proteins that interact genetically with histone H3 and H4 amino termini uncovers novel regulators of the Swe1 kinase in Saccharomyces cerevisiae. Genes Dev. 1996, 10:1327-1340.
116. Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., Weissman J.S. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
117. Rodriguez P., Munroe D., Prawitt D., Chu L.L., Bric E., Kim J., Reid L.H., Davies C., Nakagama H., Loebbert R., Winterpacht A., Petruzzi M.J., Higgins M.J., Nowak N., Evans G., Shows T., Weissman B.E., Zabel B., Housman D.E., Pelletier J. Functional characterization of human nucleosome assembly protein-2 (NAP1L4) suggests a role as a histone chaperone. Genomics 1997, 44:253-265.
118. Krick R., Aschrafi A., Hasgun D., Arnemann J. CK2-dependent C-terminal phosphorylation at T300 directs the nuclear transport of TSPY protein. Biochem. Biophys. Res. Commun. 2006, 341:343-350.
119. Dong A., Liu Z., Zhu Y., Yu F., Li Z., Cao K., Shen W.H. Interacting proteins and differences in nuclear transport reveal specific functions for the NAP1 family proteins in plants. Plant Physiol. 2005, 138:1446-1456.
120. Rodriguez P., Pelletier J., Price G.B., Zannis-Hadjopoulos M. NAP-2: histone chaperone function and phosphorylation state through the cell cycle. J. Mol. Biol. 2000, 298:225-238.
121. Calvert M.E., Keck K.M., Ptak C., Shabanowitz J., Hunt D.F., Pemberton L.F. Phosphorylation by casein kinase 2 regulates Nap1 localization and function. Mol. Cell. Biol. 2008, 28:1313-1325.
122. Park Y.J., McBryant S.J., Luger K. A beta-hairpin comprising the nuclear localization sequence sustains the self-associated states of nucleosome assembly protein 1. J. Mol. Biol. 2008, 375:1076-1085.
123. Park Y.J., Luger K. The structure of nucleosome assembly protein 1. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:1248-1253.
124. Li M., Strand D., Krehan A., Pyerin W., Heid H., Neumann B., Mechler B.M. Casein kinase 2 binds and phosphorylates the nucleosome assembly protein-1 (NAP1) in Drosophila melanogaster. J. Mol. Biol. 1999, 293:1067-1084.
125. Zlatanova J., Thakar A. H2A.Z: view from the top. Structure 2008, 16:166-179.
126. Kobor M.S., Venkatasubrahmanyam S., Meneghini M.D., Gin J.W., Jennings J.L., Link A.J., Madhani H.D., Rine J. A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2004, 2:E131.
127. Mizuguchi G., Shen X., Landry J., Wu W.H., Sen S., Wu C. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 2004, 303:343-348.
128. Park Y.J., Chodaparambil J.V., Bao Y., McBryant S.J., Luger K. Nucleosome assembly protein 1 exchanges histone H2A-H2B dimers and assists nucleosome sliding. J. Biol. Chem. 2005, 280:1817-1825.
129. Zhou Z., Feng H., Hansen D.F., Kato H., Luk E., Freedberg D.I., Kay L.E., Wu C., Bai Y. NMR structure of chaperone Chz1 complexed with histones H2A.Z-H2B. Nat. Struct. Mol. Biol. 2008, 15:868-869.
130. Lorain S., Quivy J.P., Monier-Gavelle F., Scamps C., Lecluse Y., Almouzni G., Lipinski M. Core histones and HIRIP3, a novel histone-binding protein, directly interact with WD repeat protein HIRA. Mol. Cell. Biol. 1998, 18:5546-5556.
131. Park Y.J., Luger K. Structure and function of nucleosome assembly proteins. Biochem. Cell Biol. 2006, 84:549-558.
132. Kaplan T., Liu C.L., Erkmann J.A., Holik J., Grunstein M., Kaufman P.D., Friedman N., Rando O.J. Cell cycle- and chaperone-mediated regulation of H3K56ac incorporation in yeast. PLoS Genet. 2008, 4:e1000270.
133. Selth L.A., Lorch Y., Ocampo-Hafalla M.T., Mitter R., Shales M., Krogan N.J., Kornberg R.D., Svejstrup J.Q. An rtt109-independent role for vps75 in transcription-associated nucleosome dynamics. Mol. Cell. Biol. 2009, 29:4220-4234.
134. Schneider J., Bajwa P., Johnson F.C., Bhaumik S.R., Shilatifard A. Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J. Biol. Chem. 2006, 281:37270-37274.
135. Collins S.R., Miller K.M., Maas N.L., Roguev A., Fillingham J., Chu C.S., Schuldiner M., Gebbia M., Recht J., Shales M., Ding H., Xu H., Han J., Ingvarsdottir K., Cheng B., Andrews B., Boone C., Berger S.L., Hieter P., Zhang Z., Brown G.W., Ingles C.J., Emili A., Allis C.D., Toczyski D.P., Weissman J.S., Greenblatt J.F., Krogan N.J. Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 2007, 446:806-810.
136. Burgess R.J., Zhou H., Han J., Zhang Z. A role for Gcn5 in replication-coupled nucleosome assembly. Mol. Cell 2010, 37:469-480.
137. Grant P.A., Eberharter A., John S., Cook R.G., Turner B.M., Workman J.L. Expanded lysine acetylation specificity of Gcn5 in native complexes. J. Biol. Chem. 1999, 274:5895-5900.
138. Berndsen C.E., Tsubota T., Lindner S.E., Lee S., Holton J.M., Kaufman P.D., Keck J.L., Denu J.M. Molecular functions of the histone acetyltransferase chaperone complex Rtt109-Vps75. Nat. Struct. Mol. Biol. 2008, 15:948-956.
139. Pokholok D.K., Harbison C.T., Levine S., Cole M., Hannett N.M., Lee T.I., Bell G.W., Walker K., Rolfe P.A., Herbolsheimer E., Zeitlinger J., Lewitter F., Gifford D.K., Young R.A. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 2005, 122:517-527.
140. Tie F., Banerjee R., Stratton C.A., Prasad-Sinha J., Stepanik V., Zlobin A., Diaz M.O., Scacheri P.C., Harte P.J. CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 2009, 136:3131-3141.
141. Millar C.B., Grunstein M. Genome-wide patterns of histone modifications in yeast. Nat. Rev. Mol. Cell Biol. 2006, 7:657-666.
142. Keck K.M., Pemberton L.F. Interaction with the histone chaperone Vps75 promotes nuclear localization and HAT activity of Rtt109 in vivo. Traffic 2011, 12:826-839.
143. Lane A.A., Chabner B.A. Histone deacetylase inhibitors in cancer therapy. J. Clin. Oncol. 2009, 27:5459-5468.
144. Rangasamy D. Histone variant H2A.Z can serve as a new target for breast cancer therapy. Curr. Med. Chem. 2010, 17:3155-3161.
145. Polo S.E., Theocharis S.E., Grandin L., Gambotti L., Antoni G., Savignoni A., Asselain B., Patsouris E., Almouzni G. Clinical significance and prognostic value of chromatin assembly factor-1 overexpression in human solid tumours. Histopathology 2010, 57:716-724.
146. Corpet A., De Koning L., Toedling J., Savignoni A., Berger F., Lemaitre C., O'Sullivan R.J., Karlseder J., Barillot E., Asselain B., Sastre-Garau X., Almouzni G. Asf1b, the necessary Asf1 isoform for proliferation, is predictive of outcome in breast cancer. EMBO J. 2011, 30:480-493.
147. Lau Y.F. Gonadoblastoma, testicular and prostate cancers, and the TSPY gene. Am. J. Hum. Genet. 1999, 64:921-927.
148. Laskey R.A., Earnshaw W.C. Nucleosome assembly. Nature 1980, 286:763-767.
149. Frehlick L.J., Eirin-Lopez J.M., Ausio J. New insights into the nucleophosmin/nucleoplasmin family of nuclear chaperones. Bioessays 2007, 29:49-59.
150. Maggi L.B., Kuchenruether M., Dadey D.Y., Schwope R.M., Grisendi S., Townsend R.R., Pandolfi P.P., Weber J.D. Nucleophosmin serves as a rate-limiting nuclear export chaperone for the Mammalian ribosome. Mol. Cell. Biol. 2008, 28:7050-7065.
151. Okuwaki M. The structure and functions of NPM1/Nucleophsmin/B23, a multifunctional nucleolar acidic protein. J. Biochem. 2008, 143:441-448.
152. Prado A., Ramos I., Frehlick L.J., Muga A., Ausio J. Nucleoplasmin: a nuclear chaperone. Biochem. Cell Biol. 2004, 82:437-445.
153. Namboodiri V.M., Akey I.V., Schmidt-Zachmann M.S., Head J.F., Akey C.W. The structure and function of Xenopus NO38-core, a histone chaperone in the nucleolus. Structure 2004, 12:2149-2160.
154. Dutta S., Akey I.V., Dingwall C., Hartman K.L., Laue T., Nolte R.T., Head J.F., Akey C.W. The crystal structure of nucleoplasmin-core: implications for histone binding and nucleosome assembly. Mol. Cell 2001, 8:841-853.
155. Robbins J., Dilworth S.M., Laskey R.A., Dingwall C. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 1991, 64:615-623.
156. Vancurova I., Vancura A., Lou W., Paine P.L. A domain distinct from nucleoplasmin's nuclear localization sequence influences its transport. Biochem. Biophys. Res. Commun. 1997, 235:19-25.
157. Dingwall C., Dilworth S.M., Black S.J., Kearsey S.E., Cox L.S., Laskey R.A. Nucleoplasmin cDNA sequence reveals polyglutamic acid tracts and a cluster of sequences homologous to putative nuclear localization signals. EMBO J. 1987, 6:69-74.
158. Falces J., Arregi I., Konarev P.V., Urbaneja M.A., Svergun D.I., Taneva S.G., Banuelos S. Recognition of nucleoplasmin by its nuclear transport receptor importin alpha/beta: insights into a complete import complex. Biochemistry 2010, 49:9756-9769.
159. Dingwall C., Sharnick S.V., Laskey R.A. A polypeptide domain that specifies migration of nucleoplasmin into the nucleus. Cell 1982, 30:449-458.
160. Hingorani K., Szebeni A., Olson M.O. Mapping the functional domains of nucleolar protein B23. J. Biol. Chem. 2000, 275:24451-24457.
161. Falini B., Bolli N., Shan J., Martelli M.P., Liso A., Pucciarini A., Bigerna B., Pasqualucci L., Mannucci R., Rosati R., Gorello P., Diverio D., Roti G., Tiacci E., Cazzaniga G., Biondi A., Schnittger S., Haferlach T., Hiddemann W., Martelli M.F., Gu W., Mecucci C., Nicoletti I. Both carboxy-terminus NES motif and mutated tryptophan(s) are crucial for aberrant nuclear export of nucleophosmin leukemic mutants in NPMc+ AML. Blood 2006, 107:4514-4523.
162. Grisendi S., Mecucci C., Falini B., Pandolfi P.P. Nucleophosmin and cancer. Nat. Rev. Cancer 2006, 6:493-505.
163. Lindstrom M.S. NPM1/B23: a multifunctional chaperone in ribosome biogenesis and chromatin remodeling. Biochem. Res. Int. 2011, 2011:195209.
164. Bolli N., Nicoletti I., De Marco M.F., Bigerna B., Pucciarini A., Mannucci R., Martelli M.P., Liso A., Mecucci C., Fabbiano F., Martelli M.F., Henderson B.R., Falini B. Born to be exported: COOH-terminal nuclear export signals of different strength ensure cytoplasmic accumulation of nucleophosmin leukemic mutants. Cancer Res. 2007, 67:6230-6237.
165. Falini B., Mecucci C., Tiacci E., Alcalay M., Rosati R., Pasqualucci L., La Starza R., Diverio D., Colombo E., Santucci A., Bigerna B., Pacini R., Pucciarini A., Liso A., Vignetti M., Fazi P., Meani N., Pettirossi V., Saglio G., Mandelli F., Lo-Coco F., Pelicci P.G., Martelli M.F. Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype. N. Engl. J. Med. 2005, 352:254-266.
166. Falini B., Martelli M.P., Bolli N., Sportoletti P., Liso A., Tiacci E., Haferlach T. Acute myeloid leukemia with mutated nucleophosmin (NPM1): is it a distinct entity?. Blood 2011, 117:1109-1120.
167. Vancurova I., Paine T.M., Lou W., Paine P.L. Nucleoplasmin associates with and is phosphorylated by casein kinase II. J. Cell Sci. 1995, 108(Pt 2):779-787.
168. Shandilya J., Swaminathan V., Gadad S.S., Choudhari R., Kodaganur G.S., Kundu T.K. Acetylated NPM1 localizes in the nucleoplasm and regulates transcriptional activation of genes implicated in oral cancer manifestation. Mol. Cell. Biol. 2009, 29:5115-5127.
169. Angelov D., Bondarenko V.A., Almagro S., Menoni H., Mongelard F., Hans F., Mietton F., Studitsky V.M., Hamiche A., Dimitrov S., Bouvet P. Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes. EMBO J. 2006, 25:1669-1679.
170. Orrick L.R., Olson M.O., Busch H. Comparison of nucleolar proteins of normal rat liver and Novikoff hepatoma ascites cells by two-dimensional polyacrylamide gel electrophoresis. Proc. Natl. Acad. Sci. U. S. A. 1973, 70:1316-1320.
171. Drane P., Ouararhni K., Depaux A., Shuaib M., Hamiche A. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev. 2010, 24:1253-1265.
172. Campos E.I., Reinberg D. New chaps in the histone chaperone arena. Genes Dev. 2010, 24:1334-1338.
173. Xue Y., Gibbons R., Yan Z., Yang D., McDowell T.L., Sechi S., Qin J., Zhou S., Higgs D., Wang W. The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:10635-10640.
174. Jiao Y., Shi C., Edil B.H., de Wilde R.F., Klimstra D.S., Maitra A., Schulick R.D., Tang L.H., Wolfgang C.L., Choti M.A., Velculescu V.E., Diaz L.A., Vogelstein B., Kinzler K.W., Hruban R.H., Papadopoulos N. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 2011, 331:1199-1203.
175. Song J.J., Lee Y.J. Tryptophan 621 and serine 667 residues of Daxx regulate its nuclear export during glucose deprivation. J. Biol. Chem. 2004, 279:30573-30578.
176. Sawatsubashi S., Murata T., Lim J., Fujiki R., Ito S., Suzuki E., Tanabe M., Zhao Y., Kimura S., Fujiyama S., Ueda T., Umetsu D., Ito T., Takeyama K., Kato S. A histone chaperone, DEK, transcriptionally coactivates a nuclear receptor. Genes Dev. 2010, 24:159-170.
177. Elsasser S.J., Allis C.D., Lewis P.W. Cancer. New epigenetic drivers of cancers. Science 2011, 331:1145-1146.
178. von Lindern M., Fornerod M., van Baal S., Jaegle M., de Wit T., Buijs A., Grosveld G. The translocation (6;9), associated with a specific subtype of acute myeloid leukemia, results in the fusion of two genes, dek and can, and the expression of a chimeric, leukemia-specific dek-can mRNA. Mol. Cell. Biol. 1992, 12:1687-1697.
179. von Lindern M., van Baal S., Wiegant J., Raap A., Hagemeijer A., Grosveld G. Can, a putative oncogene associated with myeloid leukemogenesis, may be activated by fusion of its 3' half to different genes: characterization of the set gene. Mol. Cell. Biol. 1992, 12:3346-3355.
180. Fornerod M., Boer J., van Baal S., Morreau H., Grosveld G. Interaction of cellular proteins with the leukemia specific fusion proteins DEK-CAN and SET-CAN and their normal counterpart, the nucleoporin CAN. Oncogene 1996, 13:1801-1808.
181. Andrews A.J., Chen X., Zevin A., Stargell L.A., Luger K. The histone chaperone Nap1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol. Cell 2010, 37:834-842.
182. Jakel S., Mingot J.M., Schwarzmaier P., Hartmann E., Gorlich D. Importins fulfil a dual function as nuclear import receptors and cytoplasmic chaperones for exposed basic domains. EMBO J. 2002, 21:377-386.