Basic properties of epigenetic systems: Lessons from the centromere

Current Opinion in Genetics and Development

Volumn 23, Issue 2, 2013, Pages 219-227

  Gómez Rodríguez, Mariluz ^a   Jansen, Lars ET ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN A; CIS ACTING ELEMENT; HISTONE; HISTONE H3;

CELL CYCLE; CELL DIVISION; CENTROMERE; CHROMATIN; CHROMOSOME STRUCTURE; DNA METHYLATION; DNA SEQUENCE; EPIGENETICS; GENE EXPRESSION; HISTONE MODIFICATION; HUMAN; INHERITANCE; MITOSIS; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; REVIEW;

AUTOANTIGENS; CELL DIVISION; CENTROMERE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HISTONES; KINETOCHORES; NUCLEOSOMES;

EID: 84877804887     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2012.11.002     Document Type: Review

References (72)

1. Spalding K.L., Bhardwaj R.D., Buchholz B.A., Druid H., Frisén J. Retrospective birth dating of cells in humans. Cell 2005, 122:133-143.
2. Annunziato A.T. Split decision: what happens to nucleosomes during DNA replication?. J Biol Chem 2005, 280:12065-12068.
3. Ishimi Y., Sugasawa K., Hanaoka F., Kikuchi A. Replication of the simian virus 40 chromosome with purified proteins. J Biol Chem 1991, 266:16141-16148.
4. Jackson V. In vivo studies on the dynamics of histone-DNA interaction: evidence for nucleosome dissolution during replication and transcription and a low level of dissolution independent of both. Biochemistry 1990, 29:719-731.
5. Xu M., Long C., Chen X., Huang C., Chen S., Zhu B. Partitioning of histone H3-H4 tetramers during DNA replication-dependent chromatin assembly. Science 2010, 328:94-98.
6. Zee B.M., Levin R.S., DiMaggio P.A., Garcia B.A. Global turnover of histone post-translational modifications and variants in human cells. Epigenetics Chromatin 2010, 3:22.
7. Talbert P.B., Henikoff S. Histone variants-ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 2010, 11:264-275.
8. Gardner K.E., Allis C.D., Strahl B.D. OPERating ON chromatin, a colorful language where context matters. J Mol Biol 2011, 409:36-46.
9. Alabert C., Groth A. Chromatin replication and epigenome maintenance. Nat Rev Mol Cell Biol 2012, 13:153-167.
10. Luger K., Mäder A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8Å resolution. Nature 1997, 389:251-260.
11. Kimura H., Cook P.R. Kinetics of core histones in living human cells little exchange of H3 and H4 and some rapid exchange of H2b. J Cell Biol 2001, 153:1341-1354.
12. Ahmad K., Henikoff S. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 2002, 9:1191-1200.
13. 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., et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 2010, 140:678-691.
14. Ng R.K., Gurdon J.B. Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nat Cell Biol 2008, 10:102-109.
15. Radman-Livaja M., Verzijlbergen K.F., Weiner A., van Welsem T., Friedman N., Rando O.J., van Leeuwen F. Patterns and mechanisms of ancestral histone protein inheritance in budding yeast. PLoS Biol 2011, 9:e1001075.
16. Cleveland D.W., Mao Y., Sullivan K.F. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 2003, 112:407-421.
17. Allshire R.C., Karpen G.H. Epigenetic regulation of centromeric chromatin: old dogs, new tricks?. Nat Rev Genet 2008, 9:923-937.
18. Black B.E., Bassett E.A. The histone variant CENP-A and centromere specification. Curr Opin Cell Biol 2008, 20:91-100.
19. Valente L.P., Silva M.C.C., Jansen L.E.T. Temporal control of epigenetic centromere specification. Chromosome Res 2012, 20:481-492.
20. Keppler A., Gendreizig S., Gronemeyer T., Pick H., Vogel H., Johnsson K. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat Biotechnol 2003, 21:86-89.
21. Keppler A., Pick H., Arrivoli C., Vogel H., Johnsson K. Labeling of fusion proteins with synthetic fluorophores in live cells. Proc Natl Acad Sci USA 2004, 101:9955-9959.
22. Jansen L.E.T., Black B.E., Foltz D.R., Cleveland D.W. Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 2007, 176:795-805.
23. Hemmerich P., Weidtkamp-Peters S., Hoischen C., Schmiedeberg L., Erliandri I., Diekmann S. Dynamics of inner kinetochore assembly and maintenance in living cells. J Cell Biol 2008, 180:1101-1114.
24. Schuh M., Lehner C.F., Heidmann S. Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr Biol 2007, 17:237-243.
25. Barnhart M.C., Kuich P.H.J.L., Stellfox M.E., Ward J.A., Bassett E.A., Black B.E., Foltz D.R. HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J Cell Biol 2011, 194:229-243.
26. Guse A., Carroll C.W., Moree B., Fuller C.J., Straight A.F. In vitro centromere and kinetochore assembly on defined chromatin templates. Nature 2011, 477:354-358.
27. Mendiburo M.J., Padeken J., Fülöp S., Schepers A., Heun P. Drosophila CENH3 is sufficient for centromere formation. Science 2011, 334:686-690.
28. Dodd I.B., Micheelsen M.A., Sneppen K., Thon G. Theoretical analysis of epigenetic cell memory by nucleosome modification. Cell 2007, 129:813-822.
29. Deal R.B., Henikoff J.G., Henikoff S. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 2010, 328:1161-1164.
30. Wu S.C., Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 2010, 11:607-620.
31. Klose R.J., Bird A.P. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 2006, 31:89-97.
32. Bestor T.H., Ingram V.M. Two DNA methyltransferases from murine erythroleukemia cells: purification, sequence specificity, and mode of interaction with DNA. Proc Natl Acad Sci USA 1983, 80:5559-5563.
33. Hathaway N.A., Bell O., Hodges C., Miller E.L., Neel D.S., Crabtree G.R. Dynamics and memory of heterochromatin in living cells. Cell 2012, 149:1447-1460.
34. Honda B.M., Candido P.M., Dixon G.H. Histone methylation, its occurrence in different cell types and relation to histone H4 metabolism in developing trout testis. J Biol Chem 1975, 250:8686-8689.
35. Kouskouti A., Talianidis I. Histone modifications defining active genes persist after transcriptional and mitotic inactivation. EMBO J 2005, 24:347-357.
36. Petruk S., Sedkov Y., Johnston D.M., Hodgson J.W., Black K.L., Kovermann S.K., Beck S., Canaani E., Brock H.W., Mazo A. TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell 2012, 150:922-933.
37. Francis N.J., Follmer N.E., Simon M.D., Aghia G., Butler J.D. Polycomb proteins remain bound to chromatin and DNA during DNA replication in vitro. Cell 2009, 137:110-122.
38. Lo S.M., Follmer N.E., Lengsfeld B.M., Madamba E.V., Seong S., Grau D.J., Francis N.J. A bridging model for persistence of a Polycomb group protein complex through DNA replication in vitro. Mol Cell 2012, 46:784-796.
39. Buchenau P., Hodgson J., Strutt H., Arndt-Jovin D.J. The distribution of Polycomb-group proteins during cell division and development in Drosophila embryos: impact on models for silencing. J Cell Biol 1998, 141:469-481.
40. Miyagishima H., Isono K., Fujimura Y., Iyo M., Takihara Y., Masumoto H., Vidal M., Koseki H. Dissociation of mammalian Polycomb-group proteins, Ring1B and Rae28/Ph1, from the chromatin correlates with configuration changes of the chromatin in mitotic and meiotic prophase. Histochem Cell Biol 2003, 120:111-119.
41. Fonseca J.P., Steffen P.A., Müller S., Lu J., Sawicka A., Seiser C., Ringrose L. In vivo Polycomb kinetics and mitotic chromatin binding distinguish stem cells from differentiated cells. Genes Dev 2012, 26:857-871.
42. Ficz G., Heintzmann R., Arndt-Jovin D.J. Polycomb group protein complexes exchange rapidly in living Drosophila. Development 2005, 132:3963-3976.
43. Watson J.D., Crick F.H. Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 1953, 171:737-738.
44. Sonneborn T.M. The differentiation of cells. Proc Natl Acad Sci USA 1964, 51:915-929.
45. Prusiner S.B. Prions. Proc Natl Acad Sci USA 1998, 95:13363-13383.
46. Lachner M., O'Carroll D., Rea S., Mechtler K., Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 2001, 410:116-120.
47. Bannister A.J., Zegerman P., Partridge J.F., Miska E.A., Thomas J.O., Allshire R.C., Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 2001, 410:120-124.
48. Hansen K.H., Bracken A.P., Pasini D., Dietrich N., Gehani S.S., Monrad A., Rappsilber J., Lerdrup M., Helin K. A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol 2008, 10:1291-1300.
49. Margueron R., Justin N., Ohno K., Sharpe M.L., Son J., Iii W.J.D., Voigt P., Martin S.R., Taylor W.R., Marco V.D., et al. Role of the Polycomb protein EED in the propagation of repressive histone marks. Nature 2009, 461:762-767.
50. Carroll C.W., Silva M.C.C., Godek K.M., Jansen L.E.T., Straight A.F. Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat Cell Biol 2009, 11:896-902.
51. Carroll C.W., Milks K.J., Straight A.F. Dual recognition of CENP-A nucleosomes is required for centromere assembly. J Cell Biol 2010, 189:1143-1155.
52. Foltz D.R., Jansen L.E.T., Bailey A.O., Yates J.R., Bassett E.A., Wood S., Black B.E., Cleveland D.W. Centromere-specific assembly of CENP-A nucleosomes is mediated by HJURP. Cell 2009, 137:472-484.
53. Dunleavy E.M., Roche D., Tagami H., Lacoste N., Ray-Gallet D., Nakamura Y., Daigo Y., Nakatani Y., Almouzni-Pettinotti G. HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 2009, 137:485-497.
54. Fujita Y., Hayashi T., Kiyomitsu T., Toyoda Y., Kokubu A., Obuse C., Yanagida M. Priming of centromere for CENP-A recruitment by human hMis18α, hMis18β, and M18BP1. Dev Cell 2007, 12:17-30.
55. Maddox P.S., Hyndman F., Monen J., Oegema K., Desai A. Functional genomics identifies a Myb domain-containing protein family required for assembly of CENP-A chromatin. J Cell Biol 2007, 176:757-763.
56. Moree B., Meyer C.B., Fuller C.J., Straight A.F. CENP-C recruits M18BP1 to centromeres to promote CENP-A chromatin assembly. J Cell Biol 2011, 194:855-871.
57. Pidoux A.L., Choi E.S., Abbott J.K.R., Liu X., Kagansky A., Castillo A.G., Hamilton G.L., Richardson W., Rappsilber J., He X., et al. Fission yeast Scm3: a CENP-A receptor required for integrity of subkinetochore chromatin. Mol Cell 2009, 33:299-311.
58. Ohzeki J., Bergmann J.H., Kouprina N., Noskov V.N., Nakano M., Kimura H., Earnshaw W.C., Larionov V., Masumoto H. Breaking the HAC barrier: histone H3K9 acetyl/methyl balance regulates CENP-A assembly. EMBO J 2012, 31:2391-2402.
59. Bergmann J.H., Rodríguez M.G., Martins N.M.C., Kimura H., Kelly D.A., Masumoto H., Larionov V., Jansen L.E.T., Earnshaw W.C. Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J 2011, 30:328-340.
60. Blower M.D., Sullivan B.A., Karpen G.H. Conserved organization of centromeric chromatin in flies and humans. Dev Cell 2002, 2:319-330.
61. Dunleavy E.M., Almouzni G., Karpen G.H. H3.3 is deposited at centromeres in S phase as a placeholder for newly assembled CENP-A in G(1) phase. Nucleus 2011, 2:146-157.
62. Shibahara K., Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 1999, 96:575-585.
63. Iida T., Suetake I., Tajima S., Morioka H., Ohta S., Obuse C., Tsurimoto T. PCNA clamp facilitates action of DNA cytosine methyltransferase 1 on hemimethylated DNA. Genes Cells 2002, 7:997-1007.
64. Spada F., Haemmer A., Kuch D., Rothbauer U., Schermelleh L., Kremmer E., Carell T., Längst G., Leonhardt H. DNMT1 but not its interaction with the replication machinery is required for maintenance of DNA methylation in human cells. J Cell Biol 2007, 176:565-571.
65. Keller C., Krude T. Requirement of cyclin/Cdk2 and protein phosphatase 1 activity for chromatin assembly factor 1-dependent chromatin assembly during DNA synthesis. J Biol Chem 2000, 275:35512-35521.
66. Lavoie G., St-Pierre Y. Phosphorylation of human DNMT1: implication of cyclin-dependent kinases. Biochem Biophys Res Commun 2011, 409:187-192.
67. Régnier V., Vagnarelli P., Fukagawa T., Zerjal T., Burns E., Trouche D., Earnshaw W., Brown W. CENP-A is required for accurate chromosome segregation and sustained kinetochore association of BubR1. Mol Cell Biol 2005, 25:3967-3981.
68. Shelby R.D., Monier K., Sullivan K.F. Chromatin assembly at kinetochores is uncoupled from DNA replication. J Cell Biol 2000, 151:1113-1118.
69. Mellone B.G., Grive K.J., Shteyn V., Bowers S.R., Oderberg I., Karpen G.H. Assembly of Drosophila centromeric chromatin proteins during mitosis. PLoS Genet 2011, 7:e1002068.
70. Silva M.C.C., Bodor D.L., Stellfox M.E., Martins N.M.C., Hochegger H., Foltz D.R., Jansen L.E.T. Cdk activity couples epigenetic centromere inheritance to cell cycle progression. Dev Cell 2012, 22:52-63.
71. Bernad R., Sánchez P., Rivera T., Rodríguez-Corsino M., Boyarchuk E., Vassias I., Ray-Gallet D., Arnaoutov A., Dasso M., Almouzni G., et al. Xenopus HJURP and condensin II are required for CENP-A assembly. J Cell Biol 2011, 192:569-582.
72. Chen S., Bohrer L.R., Rai A.N., Pan Y., Gan L., Zhou X., Bagchi A., Simon J.A., Huang H. Cyclin-dependent kinases regulate epigenetic gene silencing through phosphorylation of EZH2. Nat Cell Biol 2010, 12:1108-1114.