A unique binding mode enables MCM2 to chaperone histones H3-H4 at replication forks

Nature Structural and Molecular Biology

Volumn 22, Issue 8, 2015, Pages 618-626

  Huang, Hongda ^a   Strømme, Caroline B ^b   Saredi, Giulia ^b   Hödl, Martina ^b   Strandsby, Anne ^b   González Aguilera, Cristina ^b   Chen, Shoudeng ^a   Groth, Anja ^b   Patel, Dinshaw J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ASF1 PROTEIN; CENTROMERE PROTEIN A; CHAPERONE; DIMER; HISTONE H3; HISTONE H4; MINICHROMOSOME MAINTENANCE PROTEIN 2; TETRAMER; UNCLASSIFIED DRUG; CHROMATIN; DNA; HISTONE; MCM2 PROTEIN, HUMAN; PROTEIN BINDING;

ARTICLE; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA HISTONE INTERACTION; DNA REPLICATION; GENOME; MUTATIONAL ANALYSIS; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; CHROMATIN; CONFORMATION; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE; SEQUENCE HOMOLOGY; TUMOR CELL LINE; WESTERN BLOTTING;

AMINO ACID SEQUENCE; BLOTTING, WESTERN; CELL LINE, TUMOR; CHROMATIN; DNA; DNA REPLICATION; HELA CELLS; HISTONES; HUMANS; MINICHROMOSOME MAINTENANCE COMPLEX COMPONENT 2; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RNA INTERFERENCE; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84938692151     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3055     Document Type: Article

References (57)

1. Alabert, C. & Groth, A. Chromatin replication and epigenome maintenance. Nat. Rev. Mol. Cell Biol. 13, 153-167 (2012).
2. Hake, S. B. & Allis, C. D. Histone H3 variants and their potential role in indexing mammalian genomes: the "H3 barcode hypothesis". Proc. Natl. Acad. Sci. USA 103, 6428-6435 (2006).
3. Margueron, R. & Reinberg, D. Chromatin structure and the inheritance of epigenetic information. Nat. Rev. Genet. 11, 285-296 (2010).
4. Probst, A. V., Dunleavy, E. & Almouzni, G. Epigenetic inheritance during the cell cycle. Nat. Rev. Mol. Cell Biol. 10, 192-206 (2009).
5. Shibahara, K. & Stillman, B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96, 575-585 (1999).
6. Zhang, Z., Shibahara, K. & Stillman, B. PCNA connects DNA replication to epigenetic inheritance in yeast. Nature 408, 221-225 (2000).
7. Groth, A. et al. Regulation of replication fork progression through histone supply and demand. Science 318, 1928-1931 (2007).
8. Ishimi, Y., Komamura-Kohno, Y., Arai, K. & Masai, H. Biochemical activities associated with mouse Mcm2 protein. J. Biol. Chem. 276, 42744-42752 (2001).
9. Jasencakova, Z. et al. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol. Cell 37, 736-743 (2010).
10. Bochman, M. L. & Schwacha, A. The Mcm complex: unwinding the mechanism of a replicative helicase. Microbiol. Mol. Biol. Rev. 73, 652-683 (2009).
11. Boos, D., Frigola, J. & Diffley, J. F. Activation of the replicative DNA helicase: breaking up is hard to do. Curr. Opin. Cell Biol. 24, 423-430 (2012).
12. McKnight, S. L. & Miller, O. L. Jr. Electron microscopic analysis of chromatin replication in the cellular blastoderm Drosophila melanogaster embryo. Cell 12, 795-804 (1977).
13. Sogo, J. M., Stahl, H., Koller, T. & Knippers, R. Structure of replicating simian virus 40 minichromosomes: the replication fork, core histone segregation and terminal structures. J. Mol. Biol. 189, 189-204 (1986).
14. Annunziato, A. T. Split decision: what happens to nucleosomes during DNA replication? J. Biol. Chem. 280, 12065-12068 (2005).
15. Jackson, V. & Chalkley, R. A new method for the isolation of replicative chromatin: selective deposition of histone on both new and old DNA. Cell 23, 121-134 (1981).
16. Annunziato, A. T. Assembling chromatin: the long and winding road. Biochim. Biophys. Acta 1819, 196-210 (2013).
17. Smith, S. & Stillman, B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58, 15-25 (1989).
18. 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 116, 51-61 (2004).
19. Tyler, J. K. et al. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402, 555-560 (1999).
20. Burgess, R. J. & Zhang, Z. Histone chaperones in nucleosome assembly and human disease. Nat. Struct. Mol. Biol. 20, 14-22 (2013).
21. Ransom, M., Dennehey, B. K. & Tyler, J. K. Chaperoning histones during DNA replication and repair. Cell 140, 183-195 (2010).
22. Foltman, M. et al. Eukaryotic replisome components cooperate to process histones during chromosome replication. Cell Reports 3, 892-904 (2013).
23. Ishimi, Y., Komamura, Y., You, Z. & Kimura, H. Biochemical function of mouse minichromosome maintenance 2 protein. J. Biol. Chem. 273, 8369-8375 (1998).
24. Richet, N. et al. Structural insight into how the human helicase subunit MCM2 may act as a histone chaperone together with ASF1 at the replication fork. Nucleic Acids Res. 43, 1905-1917 (2015).
25. 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 127, 495-508 (2006).
26. Natsume, R. et al. Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature 446, 338-341 (2007).
27. Loyola, A., Bonaldi, T., Roche, D., Imhof, A. & Almouzni, G. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol. Cell 24, 309-316 (2006).
28. Mello, J. A. & Almouzni, G. The ins and outs of nucleosome assembly. Curr. Opin. Genet. Dev. 11, 136-141 (2001).
29. Groth, A. et al. Human Asf1 regulates the flow of S phase histones during replicational stress. Mol. Cell 17, 301-311 (2005).
30. Forsburg, S. L. Eukaryotic MCM proteins: beyond replication initiation. Microbiol. Mol. Biol. Rev. 68, 109-131 (2004).
31. Dimitrova, D. S., Todorov, I. T., Melendy, T. & Gilbert, D. M. Mcm2, but not RPA, is a component of the mammalian early G1-phase prereplication complex. J. Cell Biol. 146, 709-722 (1999).
32. Montagnoli, A. et al. Identification of Mcm2 phosphorylation sites by S-phase-regulating kinases. J. Biol. Chem. 281, 10281-10290 (2006).
33. Ge, X. Q., Jackson, D. A. & Blow, J. J. Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev. 21, 3331-3341 (2007).
34. Gillespie, P. J. & Blow, J. J. Clusters, factories and domains: the complex structure of S-phase comes into focus. Cell Cycle 9, 3218-3226 (2010).
35. Alabert, C. et al. Two distinct modes for propagation of histone PTMs across the cell cycle. Genes Dev. 29, 585-590 (2015).
36. Bodor, D. L., Valente, L. P., Mata, J. F., Black, B. E. & Jansen, L. E. Assembly in G1 phase and long-term stability are unique intrinsic features of CENP-A nucleosomes. Mol. Biol. Cell 24, 923-932 (2013).
37. Latreille, D., Bluy, L., Benkirane, M. & Kiernan, R. E. Identification of histone 3 variant 2 interacting factors. Nucleic Acids Res. 42, 3542-3550 (2014).
38. Tachiwana, H. et al. Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 476, 232-235 (2011).
39. Dunleavy, E. M. et al. HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137, 485-497 (2009).
40. Foltz, D. R. et al. Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137, 472-484 (2009).
41. Kaufman, P. D., Kobayashi, R. & Stillman, B. Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor-I. Genes Dev. 11, 345-357 (1997).
42. Hoek, M. & Stillman, B. Chromatin assembly factor 1 is essential and couples chromatin assembly to DNA replication in vivo. Proc. Natl. Acad. Sci. USA 100, 12183-12188 (2003).
43. Klapholz, B. et al. CAF-1 is required for efficient replication of euchromatic DNA in Drosophila larval endocycling cells. Chromosoma 118, 235-248 (2009).
44. Mejlvang, J. et al. New histone supply regulates replication fork speed and PCNA unloading. J. Cell Biol. 204, 29-43 (2014).
45. Houlard, M. et al. CAF-1 is essential for heterochromatin organization in pluripotent embryonic cells. PLoS Genet. 2, e181 (2006).
46. Song, Y. et al. CAF-1 is essential for Drosophila development and involved in the maintenance of epigenetic memory. Dev. Biol. 311, 213-222 (2007).
47. Groth, A. Replicating chromatin: a tale of histones. Biochem. Cell Biol. 87, 51-63 (2009).
48. Xu, M. et al. Partitioning of histone H3-H4 tetramers during DNA replication-dependent chromatin assembly. Science 328, 94-98 (2010).
49. Huang, C. et al. H3. 3-H4 tetramer splitting events feature cell-type specific enhancers. PLoS Genet. 9, e1003558 (2013).
50. Hu, H. et al. Structure of a CENP-A-histone H4 heterodimer in complex with chaperone HJURP. Genes Dev. 25, 901-906 (2011).
51. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. Crystal structure of the nucleosome core particle at 2. 8 A resolution. Nature 389, 251-260 (1997).
52. Amaro, A. C. et al. Molecular control of kinetochore-microtubule dynamics and chromosome oscillations. Nat. Cell Biol. 12, 319-329 (2010).
53. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
54. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
55. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954 (2002).
56. Fujita, M., Kiyono, T., Hayashi, Y. & Ishibashi, M. In vivo interaction of human MCM heterohexameric complexes with chromatin: possible involvement of ATP. J. Biol. Chem. 272, 10928-10935 (1997).
57. Jansen, L. E., Black, B. E., Foltz, D. R. & Cleveland, D. W. Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176, 795-805 (2007).