Molecular dynamics of de novo telomere heterochromatin formation in budding yeast

a.
The State Key Laboratory of Molecular Biology, Shanghai Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, University of Chinese Academy of Sciences, 320 Yue Yang Road, Shanghai 200031, China
b.
School of Life Science and Technology, Shanghai Tech University, 100 Haike Road, Shanghai 200031, China

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Corresponding author: E-mail address: jqzhou@sibcb.ac.cn (Jin-Qiu Zhou)

摘要

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Abstract: In the budding yeast Saccharomyces cerevisiae, heterochromatin structure is found at three chromosome regions, which are homothallic mating-type loci, rDNA regions and telomeres. To address how telomere heterochromatin is assembled under physiological conditions, we employed a de novo telomere addition system, and analyzed the dynamic chromatin changes of the TRP1 reporter gene during telomere elongation. We found that integrating a 255-bp, but not an 81-bp telomeric sequence near theTRP1 promoter could trigger Sir2 recruitment, active chromatin mark(s)' removal, chromatin compaction and TRP1 gene silencing, indicating that the length of the telomeric sequence inserted in the internal region of a chromosome is critical for determining the chromatin state at the proximal region. Interestingly, Rif1 but not Rif2 or yKu is indispensable for the formation of intra-chromosomal silent chromatin initiated by telomeric sequence. When an internal short telomeric sequence (e.g., 81 bp) gets exposed to become a de novo telomere, the herterochromatin features, such as Sir recruitment, active chromatin mark(s)' removal and chromatin compaction, are detected within a few hours before the de novo telomere reaches a stable length. Our results recapitulate the molecular dynamics and reveal a coherent picture of telomere heterochromatin formation.
- Telomere /
- Heterochromatin /
- Nucleosome positioning /
- Sir /
- yKu

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参考文献(67)

[1]	Altaf, M., Utley, R.T., Lacoste, N. et al. Interplay of chromatin modifiers on a short basic patch of histone H4 tail defines the boundary of telomeric heterochromatin Mol. Cell, 28 (2007),pp. 1002-1014
[2]	Arneric, M., Lingner, J. Tel1 kinase and subtelomere-bound Tbf1 mediate preferential elongation of short telomeres by telomerase in yeast EMBO Rep., 8 (2007),pp. 1080-1085
[3]	Bianchi, A., Shore, D. Early replication of short telomeres in budding yeast Cell, 128 (2007),pp. 1051-1062
[4]	Brand, A.H., Micklem, G., Nasmyth, K. A yeast silencer contains sequences that can promote autonomous plasmid replication and transcriptional activation Cell, 51 (1987),pp. 709-719
[5]	Buchman, A.R., Kimmerly, W.J., Rine, J. et al. Mol. Cell. Biol., 8 (1988),pp. 210-225
[6]	Buck, S.W., Shore, D. Action of a RAP1 carboxy-terminal silencing domain reveals an underlying competition between HMR and telomeres in yeast Genes Dev., 9 (1995),pp. 370-384
[7]	Davey, C.A., Sargent, D.F., Luger, K. et al. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution J. Mol. Biol., 319 (2002),pp. 1097-1113
[8]	Diede, S.J., Gottschling, D.E. Cell, 99 (1999),pp. 723-733
[9]	Evans, S.K., Sistrunk, M.L., Nugent, C.I. et al. Chromosoma, 107 (1998),pp. 352-358
[10]	Feeser, E.A., Wolberger, C. Structural and functional studies of the Rap1 C-terminus reveal novel separation-of-function mutants J. Mol. Biol., 380 (2008),pp. 520-531
[11]	Ganapathi, M., Palumbo, M.J., Ansari, S.A. et al. Extensive role of the general regulatory factors, Abf1 and Rap1, in determining genome-wide chromatin structure in budding yeast Nucleic Acids Res., 39 (2010),pp. 2032-2044
[12]	Gottschling, D.E., Aparicio, O.M., Billington, B.L. et al. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription Cell, 63 (1990),pp. 751-762
[13]	Grewal, S.I., Moazed, D. Heterochromatin and epigenetic control of gene expression Science, 301 (2003),pp. 798-802
[14]	Grunstein, M. Molecular model for telomeric heterochromatin in yeast Curr. Opin. Cell Biol., 9 (1997),pp. 383-387
[15]	Hecht, A., Laroche, T., Strahl-Bolsinger, S. et al. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast Cell, 80 (1995),pp. 583-592
[16]	Hecht, A., Strahl-Bolsinger, S., Grunstein, M. Spreading of transcriptional repressor SIR3 from telomeric heterochromatin Nature, 383 (1996),pp. 92-96
[17]	Hector, R.E., Shtofman, R.L., Ray, A. et al. Tel1p preferentially associates with short telomeres to stimulate their elongation Mol. Cell, 27 (2007),pp. 851-858
[18]	Hoppe, G.J., Tanny, J.C., Rudner, A.D. et al. Steps in assembly of silent chromatin in yeast: Sir3-independent binding of a Sir2/Sir4 complex to silencers and role for Sir2-dependent deacetylation Mol. Cell. Biol., 22 (2002),pp. 4167-4180
[19]	Imai, S., Armstrong, C.M., Kaeberlein, M. et al. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase Nature, 403 (2000),pp. 795-800
[20]	Johnson, L.M., Kayne, P.S., Kahn, E.S. et al. Proc. Natl. Acad. Sci. U. S. A., 87 (1990),pp. 6286-6290
[21]	Katan-Khaykovich, Y., Struhl, K. Heterochromatin formation involves changes in histone modifications over multiple cell generations EMBO J., 24 (2005),pp. 2138-2149
[22]	Kirchmaier, A.L., Rine, J. Mol. Cell. Biol., 26 (2006),pp. 852-862
[23]	Kitada, T., Kuryan, B.G., Tran, N.N. et al. Mechanism for epigenetic variegation of gene expression at yeast telomeric heterochromatin Genes Dev., 26 (2012),pp. 2443-2455
[24]	Konig, P., Giraldo, R., Chapman, L. et al. The crystal structure of the DNA-binding domain of yeast RAP1 in complex with telomeric DNA Cell, 85 (1996),pp. 125-136
[25]	Kueng, S., Oppikofer, M., Gasser, S.M. SIR proteins and the assembly of silent chromatin in budding yeast Annu. Rev. Genet., 47 (2013),pp. 275-306
[26]	Landry, J., Slama, J.T., Sternglanz, R. Role of NAD(+) in the deacetylase activity of the SIR2-like proteins Biochem. Biophys. Res. Commun., 278 (2000),pp. 685-690
[27]	Landry, J., Sutton, A., Tafrov, S.T. et al. The silencing protein SIR2 and its homologs are NAD-dependent protein deacetylases Proc. Natl. Acad. Sci. U. S. A., 97 (2000),pp. 5807-5811
[28]	Lau, A., Blitzblau, H., Bell, S.P. Genes Dev., 16 (2002),pp. 2935-2945
[29]	Levy, D.L., Blackburn, E.H. Mol. Cell. Biol., 24 (2004),pp. 10857-10867
[30]	Lieb, J.D., Liu, X., Botstein, D. et al. Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association Nat. Genet., 28 (2001),pp. 327-334
[31]	Liou, G.G., Tanny, J.C., Kruger, R.G. et al. Assembly of the SIR complex and its regulation by O-acetyl-ADP-ribose, a product of NAD-dependent histone deacetylation Cell, 121 (2005),pp. 515-527
[32]	Loney, E.R., Inglis, P.W., Sharp, S. et al. Epigenetics Chromatin, 2 (2009),p. 18
[33]	Longtine, M.S., Wilson, N.M., Petracek, M.E. et al. A yeast telomere binding activity binds to two related telomere sequence motifs and is indistinguishable from RAP1 Curr. Genet., 16 (1989),pp. 225-239
[34]	Luger, K., Mader, A.W., Richmond, R.K. et al. Crystal structure of the nucleosome core particle at 2.8 A resolution Nature, 389 (1997),pp. 251-260
[35]	Luo, K., Vega-Palas, M.A., Grunstein, M. Rap1-Sir4 binding independent of other Sir, yKu, or histone interactions initiates the assembly of telomeric heterochromatin in yeast Genes Dev., 16 (2002),pp. 1528-1539
[36]	Maltby, V.E., Martin, B.J., Brind'Amour, J. et al. Proc. Natl. Acad. Sci. U. S. A., 109 (2012),pp. 18505-18510
[37]	Martins-Taylor, K., Dula, M.L., Holmes, S.G. Heterochromatin spreading at yeast telomeres occurs in M phase Genetics, 168 (2004),pp. 65-75
[38]	Meng, F.L., Hu, Y., Shen, N. et al. Sua5p a single-stranded telomeric DNA-binding protein facilitates telomere replication EMBO J., 28 (2009),pp. 1466-1478
[39]	Mishra, K., Shore, D. Yeast Ku protein plays a direct role in telomeric silencing and counteracts inhibition by rif proteins Curr. Biol., 9 (1999),pp. 1123-1126
[40]	Moazed, D., Kistler, A., Axelrod, A. et al. Proc. Natl. Acad. Sci. U. S. A., 94 (1997),pp. 2186-2191
[41]	Moretti, P., Freeman, K., Coodly, L. et al. Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1 Genes Dev., 8 (1994),pp. 2257-2269
[42]	Ng, H.H., Ciccone, D.N., Morshead, K.B. et al. Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells: a potential mechanism for position-effect variegation Proc. Natl. Acad. Sci. U. S. A., 100 (2003),pp. 1820-1825
[43]	Osborne, E.A., Dudoit, S., Rine, J. The establishment of gene silencing at single-cell resolution Nat. Genet., 41 (2009),pp. 800-806
[44]	Peng, J., Zhou, J.Q. The tail-module of yeast Mediator complex is required for telomere heterochromatin maintenance Nucleic Acids Res., 40 (2011),pp. 581-593
[45]	Pina, B., Fernandez-Larrea, J., Garcia-Reyero, N. et al. The different (sur)faces of Rap1p Mol. Genet. Genomics, 268 (2003),pp. 791-798
[46]	Poschke, H., Dees, M., Chang, M. et al. Rif2 promotes a telomere fold-back structure through Rpd3L recruitment in budding yeast PLoS Genet., 8 (2012),p. e1002960
[47]	Radman-Livaja, M., Ruben, G., Weiner, A. et al. Dynamics of Sir3 spreading in budding yeast: secondary recruitment sites and euchromatic localization EMBO J., 30 (2011),pp. 1012-1026
[48]	Rossetti, L., Cacchione, S., De Menna, A. et al. Specific interactions of the telomeric protein Rap1p with nucleosomal binding sites J. Mol. Biol., 306 (2001),pp. 903-913
[49]	Roy, R., Meier, B., McAinsh, A.D. et al. Separation-of-function mutants of yeast Ku80 reveal a Yku80p-Sir4p interaction involved in telomeric silencing J. Biol. Chem., 279 (2004),pp. 86-94
[50]	Rusche, L.N., Kirchmaier, A.L., Rine, J. Annu. Rev. Biochem., 72 (2003),pp. 481-516
[51]	Sabourin, M., Tuzon, C.T., Zakian, V.A. Mol. Cell, 27 (2007),pp. 550-561
[52]	Shi, T., Bunker, R.D., Mattarocci, S. et al. Rif1 and Rif2 shape telomere function and architecture through multivalent Rap1 interactions Cell, 153 (2013),pp. 1340-1353
[53]	Shogren-Knaak, M., Ishii, H., Sun, J.M. et al. Histone H4-K16 acetylation controls chromatin structure and protein interactions Science, 311 (2006),pp. 844-847
[54]	Shore, D., Nasmyth, K. Purification and cloning of a DNA binding protein from yeast that binds to both silencer and activator elements Cell, 51 (1987),pp. 721-732
[55]	Shore, D., Stillman, D.J., Brand, A.H. et al. Identification of silencer binding proteins from yeast: possible roles in SIR control and DNA replication EMBO J., 6 (1987),pp. 461-467
[56]	Stavenhagen, J.B., Zakian, V.A. Genes Dev., 8 (1994),pp. 1411-1422
[57]	Strahl-Bolsinger, S., Hecht, A., Luo, K. et al. SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast Genes Dev., 11 (1997),pp. 83-93
[58]	Strahl, B.D., Allis, C.D. The language of covalent histone modifications Nature, 403 (2000),pp. 41-45
[59]	Suka, N., Luo, K., Grunstein, M. Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin Nat. Genet., 32 (2002),pp. 378-383
[60]	Tanny, J.C., Dowd, G.J., Huang, J. et al. An enzymatic activity in the yeast Sir2 protein that is essential for gene silencing Cell, 99 (1999),pp. 735-745
[61]	Tsukamoto, Y., Kato, J., Ikeda, H. Nature, 388 (1997),pp. 900-903
[62]	Vandre, C.L., Kamakaka, R.T., Rivier, D.H. Genetics, 180 (2008),pp. 1407-1418
[63]	Wellinger, R.J., Zakian, V.A. Genetics, 191 (2012),pp. 1073-1105
[64]	Wotton, D., Shore, D. Genes Dev., 11 (1997),pp. 748-760
[65]	Wright, J.H., Zakian, V.A. Nucleic Acids Res., 23 (1995),pp. 1454-1460
[66]	Yarragudi, A., Miyake, T., Li, R. et al. Mol. Cell. Biol., 24 (2004),pp. 9152-9164
[67]	Zhang, Z., Reese, J.C. Isolation of yeast nuclei and micrococcal nuclease mapping of nucleosome positioning Methods Mol. Biol., 313 (2006),pp. 245-255