Nuclear pore proteins regulate chromatin structure and transcriptional memory by a conserved mechanism

Nucleus (United States)

Volumn 4, Issue 5, 2013, Pages 357-360

  Light, William H ^a,b   Brickner, Jason H ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Chromatin; Epigenetics; Nuclear pore complex; Nuclear porins; Transcriptional memory

Indexed keywords

GAMMA INTERFERON; HISTONE H3; HLA DR ANTIGEN; NUCLEOPORIN; NUCLEOPORIN 98; RNA POLYMERASE II; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR IIA; TRANSCRIPTION FACTOR IIB; TRANSCRIPTION FACTOR IID; TRANSCRIPTION FACTOR IIH; NUP98 PROTEIN, HUMAN;

ARTICLE; CHROMATIN STRUCTURE; DOWNSTREAM PROCESSING; EPIGENETICS; GENE DELETION; GENE EXPRESSION; GENE INTERACTION; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; INFLAMMATION; NONHUMAN; NUCLEOSOME; PROMOTER REGION; TRANSCRIPTION REGULATION; CHROMATIN; GENETICS; METABOLISM; NUCLEAR PORE; NUCLEAR PORE COMPLEX; NUCLEAR PORINS; REVIEW; TRANSCRIPTIONAL MEMORY;

CHROMATIN; EPIGENETICS; NUCLEAR PORE COMPLEX; NUCLEAR PORINS; TRANSCRIPTIONAL MEMORY;

CHROMATIN; HUMANS; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; RNA POLYMERASE II; TRANSCRIPTION, GENETIC;

EID: 84887433563     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.26209     Document Type: Article

References (34)

1. Light WH, Brickner DG, Brand VR, Brickner JH. Interaction of a DNA zip code with the nuclear pore complex promotes H2A.Z incorporation and INO1 transcriptional memory. Mol Cell 2010; 40:112-25. PMID:20932479; http://dx.doi.org/10.1016/j. molcel.2010.09.007.
2. Suntharalingam M, Wente SR. Peering through the pore: nuclear pore complex structure, assembly, and function. Dev Cell 2003; 4:775-89. PMID:12791264; http://dx.doi.org/10.1016/S1534-5807(03)00162-X
3. Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, et al. The molecular architecture of the nuclear pore complex. Nature 2007; 450:695-701. PMID:18046406; http://dx.doi.org/10.1038/nature06405.
4. Ishii K, Arib G, Lin C, Van Houwe G, Laemmli UK. Chromatin boundaries in budding yeast: the nuclear pore connection. Cell 2002; 109:551-62. PMID:12062099; http://dx.doi.org/10.1016/S0092-8674(02)00756-0.
5. Fischer T, Strässer K, Rácz A, Rodriguez-Navarro S, Oppizzi M, Ihrig P, Lechner J, Hurt E. The mRNA export machinery requires the novel Sac3p-Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores. EMBO J 2002; 21:5843-52. PMID:12411502; http://dx.doi.org/10.1093/emboj/cdf590.
6. Siniossoglou S, Wimmer C, Rieger M, Doye V, Tekotte H, Weise C, Emig S, Segref A, Hurt EC. A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell 1996; 84:265-75. PMID:8565072; http://dx.doi.org/10.1016/S0092-8674(00)80981-2.
7. Mendjan S, Taipale M, Kind J, Holz H, Gebhardt P, Schelder M, Vermeulen M, Buscaino A, Duncan K, Mueller J, et al. Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol Cell 2006; 21:811-23. PMID:16543150; http://dx.doi.org/10.1016/j.molcel.2006.02.007.
8. Menon BB, Sarma NJ, Pasula S, Deminoff SJ, Willis KA, Barbara KE, Andrews B, Santangelo GM. Reverse recruitment: the Nup84 nuclear pore subcomplex mediates Rap1/Gcr1/Gcr2 transcriptional activation. Proc Natl Acad Sci U S A 2005; 102:5749-54. PMID:15817685; http://dx.doi.org/10.1073/pnas.0501768102.
9. Lei EP, Krebber H, Silver PA. Messenger RNAs are recruited for nuclear export during transcription. Genes Dev 2001; 15:1771-82. PMID:11459827; http://dx.doi.org/10.1101/gad.892401
10. Dilworth DJ, Suprapto A, Padovan JC, Chait BT, Wozniak RW, Rout MP, Aitchison JD. Nup2p dynamically associates with the distal regions of the yeast nuclear pore complex. J Cell Biol 2001; 153:1465-78. PMID:11425876; http://dx.doi.org/10.1083/jcb.153.7.1465.
11. Dilworth DJ, Tackett AJ, Rogers RS, Yi EC, Christmas RH, Smith JJ, Siegel AF, Chait BT, Wozniak RW, Aitchison JD. The mobile nucleoporin Nup2p and chromatin-bound Prp20p function in endogenous NPC-mediated transcriptional control. J Cell Biol 2005; 171:955-65. PMID:16365162; http://dx.doi.org/10.1083/jcb.200509061.
12. Galy V, Olivo-Marin JC, Scherthan H, Doye V, Rascalou N, Nehrbass U. Nuclear pore complexes in the organization of silent telomeric chromatin. Nature 2000; 403:108-12. PMID:10638763; http://dx.doi.org/10.1038/47528.
13. Hediger F, Dubrana K, Gasser SM. 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 2002; 140:79-91. PMID:12490156; http://dx.doi.org/10.1016/S1047-8477(02)00533-6.
14. Hediger F, Neumann FR, Van Houwe G, Dubrana K, Gasser SM. Live imaging of telomeres: yKu and Sir proteins define redundant telomere-anchoring pathways in yeast. Curr Biol 2002; 12:2076-89. PMID:12498682; http://dx.doi.org/10.1016/S0960-9822(02)01338-6.
15. Casolari JM, Brown CR, Drubin DA, Rando OJ, Silver PA. Developmentally induced changes in transcriptional program alter spatial organization across chromosomes. Genes Dev 2005; 19:1188-98. PMID:15905407; http://dx.doi.org/10.1101/gad.1307205.
16. Casolari JM, Brown CR, Komili S, West J, Hieronymus H, Silver PA. Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 2004; 117:427-39. PMID:15137937; http://dx.doi.org/10.1016/S0092-8674(04)00448-9.
17. Brickner DG, Cajigas I, Fondufe-Mittendorf Y, Ahmed S, Lee PC, Widom J, Brickner JH. H2A.Zmediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol 2007; 5:e81. PMID:17373856; http://dx.doi.org/10.1371/journal.pbio.0050081.
18. Kundu S, Horn PJ, Peterson CL. SWI/SNF is required for transcriptional memory at the yeast GAL gene cluster. Genes Dev 2007; 21:997-1004. PMID:17438002; http://dx.doi.org/10.1101/gad.1506607.
19. Guan Q, Haroon S, Bravo DG, Will JL, Gasch AP. Cellular memory of acquired stress resistance in Saccharomyces cerevisiae. Genetics 2012; 192:495-505. PMID:22851651; http://dx.doi.org/10.1534/genetics.112.143016.
20. Faria AM, Levay A, Wang Y, Kamphorst AO, Rosa ML, Nussenzveig DR, Balkan W, Chook YM, Levy DE, Fontoura BM. The nucleoporin Nup96 is required for proper expression of interferon-regulated proteins and functions. Immunity 2006; 24:295-304. PMID:16546098; http://dx.doi.org/10.1016/j.immuni.2006.01.014.
21. Kalverda B, Pickersgill H, Shloma VV, Fornerod M. Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell 2010; 140:360-71. PMID:20144760; http://dx.doi.org/10.1016/j.cell.2010.01.011.
22. Brown CR, Kennedy CJ, Delmar VA, Forbes DJ, Silver PA. Global histone acetylation induces functional genomic reorganization at mammalian nuclear pore complexes. Genes Dev 2008; 22:627-39. PMID:18316479; http://dx.doi.org/10.1101/ gad.1632708.
23. Capelson M, Liang Y, Schulte R, Mair W, Wagner U, Hetzer MW. Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 2010; 140:372-83. PMID:20144761; http://dx.doi.org/10.1016/j.cell.2009.12.054.
24. Gialitakis M, Arampatzi P, Makatounakis T, Papamatheakis J. Gamma interferon-dependent transcriptional memory via relocalization of a gene locus to PML nuclear bodies. Mol Cell Biol 2010; 30:2046-56. PMID:20123968; http://dx.doi.org/10.1128/ MCB.00906-09.
25. Light WH, Freaney J, Sood V, Thompson A, D'Urso A, Horvath CM, Brickner JH. A conserved role for human Nup98 in altering chromatin structure and promoting epigenetic transcriptional memory. PLoS Biol 2013; 11:e1001524. PMID:23555195; http://dx.doi.org/10.1371/journal.pbio.1001524.
26. Fuda NJ, Ardehali MB, Lis JT. Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 2009; 461:186-92. PMID:19741698; http://dx.doi.org/10.1038/nature08449.
27. Peterlin BM, Price DH. Controlling the elongation phase of transcription with P-TEFb. Mol Cell 2006; 23:297-305. PMID:16885020; http://dx.doi.org/10.1016/j.molcel.2006.06.014.
28. Sims RJ 3rd, Belotserkovskaya R, Reinberg D. Elongation by RNA polymerase II: the short and long of it. Genes Dev 2004; 18:2437-68. PMID:15489290; http://dx.doi.org/10.1101/gad.1235904.
29. Radonjic M, Andrau JC, Lijnzaad P, Kemmeren P, Kockelkorn TT, van Leenen D, van Berkum NL, Holstege FC. Genome-wide analyses reveal RNA polymerase II located upstream of genes poised for rapid response upon S. cerevisiae stationary phase exit. Mol Cell 2005; 18:171-83. PMID:15837421; http://dx.doi.org/10.1016/j.molcel.2005.03.010.
30. Kouzine F, Wojtowicz D, Yamane A, Resch W, Kieffer-Kwon KR, Bandle R, Nelson S, Nakahashi H, Awasthi P, Feigenbaum L, et al. Global regulation of promoter melting in naive lymphocytes. Cell 2013; 153:988-99. PMID:23706737; http://dx.doi.org/10.1016/j.cell.2013.04.033.
31. Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 2004; 75:163-89. PMID:14525967; http://dx.doi.org/10.1189/jlb.0603252.
32. Boehm U, Klamp T, Groot M, Howard JC. Cellular responses to interferon-gamma. Annu Rev Immunol 1997; 15:749-95. PMID:9143706; http://dx.doi.org/10.1146/annurev.immunol.15.1.749.
33. Green EM, Jiang Y, Joyner R, Weis K. A negative feedback loop at the nuclear periphery regulates GAL gene expression. Mol Biol Cell 2012; 23:1367-75. PMID:22323286; http://dx.doi.org/10.1091/mbc.E11-06-0547.
34. Ahmed S, Brickner DG, Light WH, Cajigas I, McDonough M, Froyshteter AB, Volpe T, Brickner JH. DNA zip codes control an ancient mechanism for gene targeting to the nuclear periphery. Nat Cell Biol 2010; 12:111-8. PMID:20098417; http://dx.doi.org/10.1038/ncb2011