A role for the nucleoporin Nup170p in chromatin structure and gene silencing

Cell

Volumn 152, Issue 5, 2013, Pages 969-983

  Van De Vosse, David W ^a   Wan, Yakun ^b,c   Lapetina, Diego L ^a   Chen, Wei Ming ^b,d   Chiang, Jung Hsien ^d   Aitchison, John D ^b,e   Wozniak, Richard W ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^c SOUTHEAST UNIVERSITY   (China)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^e SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR PROTEIN; NUCLEOPORIN; NUCLEOPORIN NUP170P; PROTEIN INTERACTING WITH PROTEIN KINASE C; PROTEIN SIR4P; RIBOSOME PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS MEMBRANE; CHROMATIN; CHROMATIN STRUCTURE; CONTROLLED STUDY; GENE SILENCING; GENETIC ASSOCIATION; HETEROCHROMATIN; NONHUMAN; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; TELOMERE; TRANSCRIPTION REGULATION; YEAST;

EID: 84874773048     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.01.049     Document Type: Article

References (86)

1. J.D. Aitchison, and M.P. Rout The yeast nuclear pore complex and transport through it Genetics 190 2012 855 883
2. J.D. Aitchison, M.P. Rout, M. Marelli, G. Blobel, and R.W. Wozniak Two novel related yeast nucleoporins Nup170p and Nup157p: complementation with the vertebrate homologue Nup155p and functional interactions with the yeast nuclear pore-membrane protein Pom152p J. Cell Biol. 131 1995 1133 1148
3. F. Alber, S. Dokudovskaya, L.M. Veenhoff, W. Zhang, J. Kipper, D. Devos, A. Suprapto, O. Karni-Schmidt, R. Williams, and B.T. Chait The molecular architecture of the nuclear pore complex Nature 450 2007 695 701
4. S. Amlacher, P. Sarges, D. Flemming, V. van Noort, R. Kunze, D.P. Devos, M. Arumugam, P. Bork, and E. Hurt Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile Cell 146 2011 277 289
5. E.D. Andrulis, A.M. Neiman, D.C. Zappulla, and R. Sternglanz Perinuclear localization of chromatin facilitates transcriptional silencing Nature 394 1998 592 595
6. M.L. Angus-Hill, A. Schlichter, D. Roberts, H. Erdjument-Bromage, P. Tempst, and B.R. Cairns A Rsc3/Rsc30 zinc cluster dimer reveals novel roles for the chromatin remodeler RSC in gene expression and cell cycle control Mol. Cell 7 2001 741 751
7. S.H. Askree, T. Yehuda, S. Smolikov, R. Gurevich, J. Hawk, C. Coker, A. Krauskopf, M. Kupiec, and M.J. McEachern A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length Proc. Natl. Acad. Sci. USA 101 2004 8658 8663
8. G. Badis, E.T. Chan, H. van Bakel, L. Pena-Castillo, D. Tillo, K. Tsui, C.D. Carlson, A.J. Gossett, M.J. Hasinoff, and C.L. Warren A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters Mol. Cell 32 2008 878 887
9. M.C. Bosio, R. Negri, and G. Dieci Promoter architectures in the yeast ribosomal expression program Transcription 2 2011 71 77
10. S.W. Buck, and D. Shore Action of a RAP1 carboxy-terminal silencing domain reveals an underlying competition between HMR and telomeres in yeast Genes Dev. 9 1995 370 384
11. J.M. Casolari, C.R. Brown, S. Komili, J. West, H. Hieronymus, and P.A. Silver Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization Cell 117 2004 427 439
12. M. Cockell, F. Palladino, T. Laroche, G. Kyrion, C. Liu, A.J. Lustig, and S.M. Gasser The carboxy termini of Sir4 and Rap1 affect Sir3 localization: evidence for a multicomponent complex required for yeast telomeric silencing J. Cell Biol. 129 1995 909 924
13. M. Crisp, Q. Liu, K. Roux, J.B. Rattner, C. Shanahan, B. Burke, P.D. Stahl, and D. Hodzic Coupling of the nucleus and cytoplasm: role of the LINC complex J. Cell Biol. 172 2006 41 53
14. J.F. Diffley, and B. Stillman Transcriptional silencing and lamins Nature 342 1989 24
15. D.J. Dilworth, A.J. Tackett, R.S. Rogers, E.C. Yi, R.H. Christmas, J.J. Smith, A.F. Siegel, B.T. Chait, R.W. Wozniak, and J.D. Aitchison The mobile nucleoporin Nup2p and chromatin-bound Prp20p function in endogenous NPC-mediated transcriptional control J. Cell Biol. 171 2005 955 965
16. X. Ding, R. Xu, J. Yu, T. Xu, Y. Zhuang, and M. Han SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice Dev. Cell 12 2007 863 872
17. H. Ebrahimi, and A.D. Donaldson Release of yeast telomeres from the nuclear periphery is triggered by replication and maintained by suppression of Ku-mediated anchoring Genes Dev. 22 2008 3363 3374
18. S. Ehrentraut, J.M. Weber, J.N. Dybowski, D. Hoffmann, and A.E. Ehrenhofer-Murray Rpd3-dependent boundary formation at telomeres by removal of Sir2 substrate Proc. Natl. Acad. Sci. USA 107 2010 5522 5527
19. F. Feuerbach, V. Galy, E. Trelles-Sticken, M. Fromont-Racine, A. Jacquier, E. Gilson, J.C. Olivo-Marin, H. Scherthan, and U. Nehrbass Nuclear architecture and spatial positioning help establish transcriptional states of telomeres in yeast Nat. Cell Biol. 4 2002 214 221
20. V. Galy, J.C. Olivo-Marin, H. Scherthan, V. Doye, N. Rascalou, and U. Nehrbass Nuclear pore complexes in the organization of silent telomeric chromatin Nature 403 2000 108 112
21. S.M. Gasser, F. Hediger, A. Taddei, F.R. Neumann, and M.R. Gartenberg The function of telomere clustering in yeast: the circe effect Cold Spring Harb. Symp. Quant. Biol. 69 2004 327 337
22. M. Gotta, T. Laroche, A. Formenton, L. Maillet, H. Scherthan, and S.M. Gasser The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae J. Cell Biol. 134 1996 1349 1363
23. P.D. Hartley, and H.D. Madhani Mechanisms that specify promoter nucleosome location and identity Cell 137 2009 445 458
24. L.A. Hawryluk-ara, E.K. Shibuya, and R.W. Wozniak Vertebrate Nup53 interacts with the nuclear lamina and is required for the assembly of a Nup93-containing complex Mol. Biol. Cell 16 2005 2382 2394
25. F. Hediger, K. Dubrana, and S.M. Gasser Myosin-like proteins 1 and 2 are not required for silencing or telomere anchoring, but act in the Tel1 pathway of telomere length control J. Struct. Biol. 140 2002 79 91
26. F. Hediger, F.R. Neumann, G. Van Houwe, K. Dubrana, and S.M. Gasser Live imaging of telomeres: yKu and Sir proteins define redundant telomere-anchoring pathways in yeast Curr. Biol. 12 2002 2076 2089
27. S. Hiraga, E.D. Robertson, and A.D. Donaldson The Ctf18 RFC-like complex positions yeast telomeres but does not specify their replication time EMBO J. 25 2006 1505 1514
28. S. Hiraga, S. Botsios, and A.D. Donaldson Histone H3 lysine 56 acetylation by Rtt109 is crucial for chromosome positioning J. Cell Biol. 183 2008 641 651
29. K. Ishii, G. Arib, C. Lin, G. Van Houwe, and U.K. Laemmli Chromatin boundaries in budding yeast: the nuclear pore connection Cell 109 2002 551 562
30. S.L. Jaspersen, T.H. Giddings Jr.; and M. Winey Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p J. Cell Biol. 159 2002 945 956
31. I. Kehat, F. Accornero, B.J. Aronow, and J.D. Molkentin Modulation of chromatin position and gene expression by HDAC4 interaction with nucleoporins J. Cell Biol. 193 2011 21 29
32. O. Kerscher, P. Hieter, M. Winey, and M.A. Basrai Novel role for a Saccharomyces cerevisiae nucleoporin, Nup170p, in chromosome segregation Genetics 157 2001 1543 1553
33. T. Laroche, S.G. Martin, M. Tsai-Pflugfelder, and S.M. Gasser The dynamics of yeast telomeres and silencing proteins through the cell cycle J. Struct. Biol. 129 2000 159 174
34. Q. Liu, N. Pante, T. Misteli, M. Elsagga, M. Crisp, D. Hodzic, B. Burke, and K.J. Roux Functional association of Sun1 with nuclear pore complexes J. Cell Biol. 178 2007 785 798
35. C.P. Lusk, T. Makhnevych, M. Marelli, J.D. Aitchison, and R.W. Wozniak Karyopherins in nuclear pore biogenesis: a role for Kap121p in the assembly of Nup53p into nuclear pore complexes J. Cell Biol. 159 2002 267 278
36. T. Makio, L.H. Stanton, C.C. Lin, D.S. Goldfarb, K. Weis, and R.W. Wozniak The nucleoporins Nup170p and Nup157p are essential for nuclear pore complex assembly J. Cell Biol. 185 2009 459 473
37. S. Mendjan, M. Taipale, J. Kind, H. Holz, P. Gebhardt, M. Schelder, M. Vermeulen, A. Buscaino, K. Duncan, and J. Mueller Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila Mol. Cell 21 2006 811 823
38. J.M. Mitchell, J. Mansfeld, J. Capitanio, U. Kutay, and R.W. Wozniak Pom121 links two essential subcomplexes of the nuclear pore complex core to the membrane J. Cell Biol. 191 2010 505 521
39. G. Mizuguchi, X. Shen, J. Landry, W.H. Wu, S. Sen, and C. Wu ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex Science 303 2004 343 348
40. C. Ptak, A.M. Anderson, R.J. Scott, D. Van de Vosse, R.S. Rogers, Y. Sydorskyy, J.D. Aitchison, and R.W. Wozniak A role for the karyopherin Kap123p in microtubule stability Traffic 10 2009 1619 1634
41. M.P. Rout, J.D. Aitchison, A. Suprapto, K. Hjertaas, Y. Zhao, and B.T. Chait The yeast nuclear pore complex: composition, architecture, and transport mechanism J. Cell Biol. 148 2000 635 651
42. L.N. Rusche, A.L. Kirchmaier, and J. Rine The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae Annu. Rev. Biochem. 72 2003 481 516
43. E.Y. Shim, J.L. Ma, J.H. Oum, Y. Yanez, and S.E. Lee The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks Mol. Cell. Biol. 25 2005 3934 3944
44. N. Shulga, N. Mosammaparast, R. Wozniak, and D.S. Goldfarb Yeast nucleoporins involved in passive nuclear envelope permeability J. Cell Biol. 149 2000 1027 1038
45. C. Stark, B.J. Breitkreutz, T. Reguly, L. Boucher, A. Breitkreutz, and M. Tyers BioGRID: a general repository for interaction datasets Nucleic Acids Res. 34 Database issue 2006 D535 D539
46. Z.W. Sun, and C.D. Allis Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast Nature 418 2002 104 108
47. A. Taddei, F. Hediger, F.R. Neumann, C. Bauer, and S.M. Gasser Separation of silencing from perinuclear anchoring functions in yeast Ku80, Sir4 and Esc1 proteins EMBO J. 23 2004 1301 1312
48. A. Taddei, H. Schober, and S.M. Gasser The budding yeast nucleus Cold Spring Harb. Perspect. Biol. 2 2010 a000612
49. J.A. Talamas, and M.W. Hetzer POM121 and Sun1 play a role in early steps of interphase NPC assembly J. Cell Biol. 194 2011 27 37
50. P. Therizols, C. Fairhead, G.G. Cabal, A. Genovesio, J.C. Olivo-Marin, B. Dujon, and E. Fabre Telomere tethering at the nuclear periphery is essential for efficient DNA double strand break repair in subtelomeric region J. Cell Biol. 172 2006 189 199
51. L.C. Titus, T.R. Dawson, D.J. Rexer, K.J. Ryan, and S.R. Wente Members of the RSC chromatin-remodeling complex are required for maintaining proper nuclear envelope structure and pore complex localization Mol. Biol. Cell 21 2010 1072 1087
52. A.H. Tong, M. Evangelista, A.B. Parsons, H. Xu, G.D. Bader, N. Pagé, M. Robinson, S. Raghibizadeh, C.W. Hogue, and H. Bussey Systematic genetic analysis with ordered arrays of yeast deletion mutants Science 294 2001 2364 2368
53. D.W. Van de Vosse, Y. Wan, R.W. Wozniak, and J.D. Aitchison Role of the nuclear envelope in genome organization and gene expression Wiley Interdiscip. Rev. Syst. Biol. Med. 3 2011 147 166
54. Y. Wan, R.A. Saleem, A.V. Ratushny, O. Roda, J.J. Smith, C.H. Lin, J.H. Chiang, and J.D. Aitchison Role of the histone variant H2A.Z/Htz1p in TBP recruitment, chromatin dynamics, and regulated expression of oleate-responsive genes Mol. Cell. Biol. 29 2009 2346 2358
55. A. Weiner, A. Hughes, M. Yassour, O.J. Rando, and N. Friedman High-resolution nucleosome mapping reveals transcription-dependent promoter packaging Genome Res. 20 2010 90 100
56. T. Yoshida, K. Shimada, Y. Oma, V. Kalck, K. Akimura, A. Taddei, H. Iwahashi, K. Kugou, K. Ohta, S.M. Gasser, and M. Harata Actin-related protein Arp6 influences H2A.Z-dependent and -independent gene expression and links ribosomal protein genes to nuclear pores PLoS Genet. 6 2010 e1000910
57. T.J. Young, and A.L. Kirchmaier Cell cycle regulation of silent chromatin formation Biochim. Biophys. Acta 1819 2012 303 312
58. G.C. Yuan, Y.J. Liu, M.F. Dion, M.D. Slack, L.F. Wu, S.J. Altschuler, and O.J. Rando Genome-scale identification of nucleosome positions in S. cerevisiae Science 309 2005 626 630
59. F. Alber, S. Dokudovskaya, L.M. Veenhoff, W. Zhang, J. Kipper, D. Devos, A. Suprapto, O. Karni-Schmidt, R. Williams, and B.T. Chait Determining the architectures of macromolecular assemblies Nature 450 2007 683 694
60. J.D. Boeke, J. Trueheart, G. Natsoulis, and G.R. Fink 5-Fluoroorotic acid as a selective agent in yeast molecular genetics Methods Enzymol. 154 1987 164 175
61. C.B. Brachmann, A. Davies, G.J. Cost, E. Caputo, J. Li, P. Hieter, and J.D. Boeke Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications Yeast 14 1998 115 132
62. J.M. Bupp, A.E. Martin, E.S. Stensrud, and S.L. Jaspersen Telomere anchoring at the nuclear periphery requires the budding yeast Sad1-UNC-84 domain protein Mps3 J. Cell Biol. 179 2007 845 854
63. M. Costanzo, A. Baryshnikova, J. Bellay, Y. Kim, E.D. Spear, C.S. Sevier, H. Ding, J.L. Koh, K. Toufighi, and S. Mostafavi The genetic landscape of a cell Science 327 2010 425 431
64. D.J. Dilworth, A. Suprapto, J.C. Padovan, B.T. Chait, R.W. Wozniak, M.P. Rout, and J.D. Aitchison Nup2p dynamically associates with the distal regions of the yeast nuclear pore complex J. Cell Biol. 153 2001 1465 1478
65. R.D. Gietz, and R.A. Woods Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method Methods Enzymol. 350 2002 87 96
66. T. Ideker, V. Thorsson, A.F. Siegel, and L.E. Hood Testing for differentially-expressed genes by maximum-likelihood analysis of microarray data J. Comput. Biol. 7 2000 805 817
67. C. Janke, M.M. Magiera, N. Rathfelder, C. Taxis, S. Reber, H. Maekawa, A. Moreno-Borchart, G. Doenges, E. Schwob, E. Schiebel, and M. Knop A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes Yeast 21 2004 947 962
68. S. Jung, M. Marelli, R.A. Rachubinski, D.R. Goodlett, and J.D. Aitchison Dynamic changes in the subcellular distribution of Gpd1p in response to cell stress J. Biol. Chem. 285 2010 6739 6749
69. M. Krzywinski, J. Schein, I. Birol, J. Connors, R. Gascoyne, D. Horsman, S.J. Jones, and M.A. Marra Circos: an information aesthetic for comparative genomics Genome Res. 19 2009 1639 1645
70. M.S. Longtine, A. McKenzie 3rd, D.J. Demarini, N.G. Shah, A. Wach, A. Brachat, P. Philippsen, and J.R. Pringle Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae Yeast 14 1998 953 961
71. T. Makhnevych, C.P. Lusk, A.M. Anderson, J.D. Aitchison, and R.W. Wozniak Cell cycle regulated transport controlled by alterations in the nuclear pore complex Cell 115 2003 813 823
72. M. Marelli, J.D. Aitchison, and R.W. Wozniak Specific binding of the karyopherin Kap121p to a subunit of the nuclear pore complex containing Nup53p, Nup59p, and Nup170p J. Cell Biol. 143 1998 1813 1830
73. X. Pan, P. Ye, D.S. Yuan, X. Wang, J.S. Bader, and J.D. Boeke A DNA integrity network in the yeast Saccharomyces cerevisiae Cell 124 2006 1069 1081
74. S. Rohner, S.M. Gasser, and P. Meister Modules for cloning-free chromatin tagging in Saccharomyces cerevisae Yeast 25 2008 235 239
75. N.C. Shaner, R.E. Campbell, P.A. Steinbach, B.N. Giepmans, A.E. Palmer, and R.Y. Tsien Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein Nat. Biotechnol. 22 2004 1567 1572
76. P. Shannon, A. Markiel, O. Ozier, N.S. Baliga, J.T. Wang, D. Ramage, N. Amin, B. Schwikowski, and T. Ideker Cytoscape: a software environment for integrated models of biomolecular interaction networks Genome Res. 13 2003 2498 2504
77. S. Shivaswamy, A. Bhinge, Y. Zhao, S. Jones, M. Hirst, and V.R. Iyer Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation PLoS Biol. 6 2008 e65
78. R.S. Sikorski, and P. Hieter A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae Genetics 122 1989 19 27
79. M.S. Singer, and D.E. Gottschling TLC1: template RNA component of Saccharomyces cerevisiae telomerase Science 266 1994 404 409
80. J.J. Smith, M. Marelli, R.H. Christmas, F.J. Vizeacoumar, D.J. Dilworth, T. Ideker, T. Galitski, K. Dimitrov, R.A. Rachubinski, and J.D. Aitchison Transcriptome profiling to identify genes involved in peroxisome assembly and function J. Cell Biol. 158 2002 259 271
81. J.J. Smith, S.A. Ramsey, M. Marelli, B. Marzolf, D. Hwang, R.A. Saleem, R.A. Rachubinski, and J.D. Aitchison Transcriptional responses to fatty acid are coordinated by combinatorial control Mol. Syst. Biol. 3 2007 115
82. A.F. Straight, A.S. Belmont, C.C. Robinett, and A.W. Murray GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion Curr. Biol. 6 1996 1599 1608
83. A.H. Tong, G. Lesage, G.D. Bader, H. Ding, H. Xu, X. Xin, J. Young, G.F. Berriz, R.L. Brost, and M. Chang Global mapping of the yeast genetic interaction network Science 303 2004 808 813
84. Y. Wan, J.H. Chiang, C.H. Lin, C.E. Arens, R.A. Saleem, J.J. Smith, and J.D. Aitchison Histone chaperone Chz1p regulates H2B ubiquitination and subtelomeric anti-silencing Nucleic Acids Res. 38 2010 1431 1440
85. G.M. Wilmes, M. Bergkessel, S. Bandyopadhyay, M. Shales, H. Braberg, G. Cagney, S.R. Collins, G.B. Whitworth, T.L. Kress, and J.S. Weissman A genetic interaction map of RNA-processing factors reveals links between Sem1/Dss1-containing complexes and mRNA export and splicing Mol. Cell 32 2008 735 746
86. E.A. Winzeler, D.D. Shoemaker, A. Astromoff, H. Liang, K. Anderson, B. Andre, R. Bangham, R. Benito, J.D. Boeke, and H. Bussey Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis Science 285 1999 901 906