Chromatin-Bound Nuclear Pore Components Regulate Gene Expression in Higher Eukaryotes

Cell

Volumn 140, Issue 3, 2010, Pages 372-383

  Capelson, Maya ^a   Liang, Yun ^a   Schulte, Roberta ^a   Mair, William ^a   Wagner, Ulrich ^b   Hetzer, Martin W ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (United States)

Author keywords

CELLBIO; DEVBIO; RNA

Indexed keywords

NUCLEOPORIN; NUCLEOPORIN 88; NUCLEOPORIN 98; NUCLEOPORIN SEC13; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS MEMBRANE; CHROMATIN; CONTROLLED STUDY; DROSOPHILA; EUKARYOTE; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOCATION; GENE LOCUS; GENE TARGETING; GENETIC REGULATION; GENETIC TRANSCRIPTION; HEAT SHOCK; METAZOON; NONHUMAN; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN BINDING; RNA INTERFERENCE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

EUKARYOTA; METAZOA;

EID: 75749103380     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2009.12.054     Document Type: Article

References (59)

1. Agudo D., Gomez-Esquer F., Martinez-Arribas F., Nunez-Villar M.J., Pollan M., and Schneider J. Nup88 mRNA overexpression is associated with high aggressiveness of breast cancer. Int. J. Cancer 109 (2004) 717-720
2. Akhtar A., and Gasser S.M. The nuclear envelope and transcriptional control. Nat. Rev. Genet. 8 (2007) 507-517
3. Alber F., Dokudovskaya S., Veenhoff L.M., Zhang W., Kipper J., Devos D., Suprapto A., Karni-Schmidt O., Williams R., Chait B.T., et al. Determining the architectures of macromolecular assemblies. Nature 450 (2007) 683-694
4. Alber F., Dokudovskaya S., Veenhoff L.M., Zhang W., Kipper J., Devos D., Suprapto A., Karni-Schmidt O., Williams R., Chait B.T., et al. The molecular architecture of the nuclear pore complex. Nature 450 (2007) 695-701
5. Andres A.J., and Thummel C.S. Methods for quantitative analysis of transcription in larvae and prepupae. Methods Cell Biol. 44 (1994) 565-573
6. Ashburner M. Patterns of puffing activity in the salivary gland chromosomes of Drosophila. I. Autosomal puffing patterns in a laboratory stock of Drosophila melanogaster. Chromosoma 21 (1967) 398-428
7. Ashburner M. Induction of puffs in polytene chromosomes of in vitro cultured salivary glands of Drosophila melanogaster by ecdysone and echysone analogues. Nat. New Biol. 230 (1971) 222-224
8. Beck M., Forster F., Ecke M., Plitzko J.M., Melchior F., Gerisch G., Baumeister W., and Medalia O. Nuclear pore complex structure and dynamics revealed by cryoelectron tomography. Science 306 (2004) 1387-1390
9. Belgareh N., Rabut G., Bai S.W., van Overbeek M., Beaudouin J., Daigle N., Zatsepina O.V., Pasteau F., Labas V., Fromont-Racine M., et al. An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. J. Cell Biol. 154 (2001) 1147-1160
10. Blobel G. Gene gating: a hypothesis. Proc. Natl. Acad. Sci. USA 82 (1985) 8527-8529
11. Brohawn S.G., Partridge J.R., Whittle J.R., and Schwartz T.U. The nuclear pore complex has entered the atomic age. Structure 17 (2009) 1156-1168
12. Brown C.R., Kennedy C.J., Delmar V.A., Forbes D.J., and Silver P.A. Global histone acetylation induces functional genomic reorganization at mammalian nuclear pore complexes. Genes Dev. 22 (2008) 627-639
13. Capelson M., and Hetzer M.W. The role of nuclear pores in gene regulation, development and disease. EMBO Rep. 10 (2009) 697-705
14. Casolari J.M., Brown C.R., Komili S., West J., Hieronymus H., and Silver P.A. Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117 (2004) 427-439
15. Casolari J.M., Brown C.R., Drubin D.A., Rando O.J., and Silver P.A. Developmentally induced changes in transcriptional program alter spatial organization across chromosomes. Genes Dev. 19 (2005) 1188-1198
16. Chao S.H., and Price D.H. Flavopiridol inactivates P-TEFb and blocks most RNA polymerase II transcription in vivo. J. Biol. Chem. 276 (2001) 31793-31799
17. Cherbas L., Hu X., Zhimulev I., Belyaeva E., and Cherbas P. EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development 130 (2003) 271-284
18. Cho E.J., Kobor M.S., Kim M., Greenblatt J., and Buratowski S. Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser 2 of the RNA polymerase II C-terminal domain. Genes Dev. 15 (2001) 3319-3329
19. D'Angelo M.A., Raices M., Panowski S.H., and Hetzer M.W. Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. Cell 136 (2009) 284-295
20. Davis L.I., and Blobel G. Nuclear pore complex contains a family of glycoproteins that includes p62: Glycosylation through a previously unidentified cellular pathway. Proc. Natl. Acad. Sci. USA 84 (1987) 7552-7556
21. Debler E.W., Ma Y., Seo H.S., Hsia K.C., Noriega T.R., Blobel G., and Hoelz A. A fence-like coat for the nuclear pore membrane. Mol. Cell 32 (2008) 815-826
22. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448 (2007) 151-156
23. Dilworth D.J., Tackett A.J., Rogers R.S., Yi E.C., Christmas R.H., Smith J.J., Siegel A.F., Chait B.T., Wozniak R.W., and Aitchison J.D. The mobile nucleoporin Nup2p and chromatin-bound Prp20p function in endogenous NPC-mediated transcriptional control. J. Cell Biol. 171 (2005) 955-965
24. Enninga J., Levay A., and Fontoura B.M. Sec13 shuttles between the nucleus and the cytoplasm and stably interacts with Nup96 at the nuclear pore complex. Mol. Cell. Biol. 23 (2003) 7271-7284
25. Gigliotti S., Callaini G., Andone S., Riparbelli M.G., Pernas-Alonso R., Hoffmann G., Graziani F., and Malva C. Nup154, a new Drosophila gene essential for male and female gametogenesis is related to the nup155 vertebrate nucleoporin gene. J. Cell Biol. 142 (1998) 1195-1207
26. Greber U.F., Senior A., and Gerace L. A major glycoprotein of the nuclear pore complex is a membrane-spanning polypeptide with a large lumenal domain and a small cytoplasmic tail. EMBO J. 9 (1990) 1495-1502
27. Griffis E.R., Altan N., Lippincott-Schwartz J., and Powers M.A. Nup98 is a mobile nucleoporin with transcription-dependent dynamics. Mol. Biol. Cell 13 (2002) 1282-1297
28. Griffis E.R., Craige B., Dimaano C., Ullman K.S., and Powers M.A. Distinct functional domains within nucleoporins Nup153 and Nup98 mediate transcription-dependent mobility. Mol. Biol. Cell 15 (2004) 1991-2002
29. Gruenbaum Y., Goldman R.D., Meyuhas R., Mills E., Margalit A., Fridkin A., Dayani Y., Prokocimer M., and Enosh A. The nuclear lamina and its functions in the nucleus. Int. Rev. Cytol. 226 (2003) 1-62
30. Guelen L., Pagie L., Brasset E., Meuleman W., Faza M.B., Talhout W., Eussen B.H., de Klein A., Wessels L., de Laat W., et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453 (2008) 948-951
31. Hamann S., and Stratling W.H. Specific binding of Drosophila nuclear protein PEP (protein on ecdysone puffs) to hsp70 DNA and RNA. Nucleic Acids Res. 26 (1998) 4108-4115
32. Hawryluk-Gara L.A., Shibuya E.K., and Wozniak R.W. 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
33. Hetzer M., Walther T.C., and Mattaj I.W. Pushing the envelope: Structure, function, and dynamics of the nuclear periphery. Annu. Rev. Cell Dev. Biol. 21 (2005) 347-380
34. Hochstrasser M., Mathog D., Gruenbaum Y., Saumweber H., and Sedat J.W. Spatial organization of chromosomes in the salivary gland nuclei of Drosophila melanogaster. J. Cell Biol. 102 (1986) 112-123
35. Huet F., Ruiz C., and Richards G. Puffs and PCR: the in vivo dynamics of early gene expression during ecdysone responses in Drosophila. Development 118 (1993) 613-627
36. Ishii K., Arib G., Lin C., Van Houwe G., and Laemmli U.K. Chromatin boundaries in budding yeast: the nuclear pore connection. Cell 109 (2002) 551-562
37. Kasper L.H., Brindle P.K., Schnabel C.A., Pritchard C.E., Cleary M.L., and van Deursen J.M. CREB binding protein interacts with nucleoporin-specific FG repeats that activate transcription and mediate NUP98-HOXA9 oncogenicity. Mol. Cell. Biol. 19 (1999) 764-776
38. Loiodice I., Alves A., Rabut G., Van Overbeek M., Ellenberg J., Sibarita J.B., and Doye V. The entire Nup107-160 complex, including three new members, is targeted as one entity to kinetochores in mitosis. Mol. Biol. Cell 15 (2004) 3333-3344
39. 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 21 (2006) 811-823
40. Menon B.B., Sarma N.J., Pasula S., Deminoff S.J., Willis K.A., Barbara K.E., Andrews B., and Santangelo G.M. Reverse recruitment: the Nup84 nuclear pore subcomplex mediates Rap1/Gcr1/Gcr2 transcriptional activation. Proc. Natl. Acad. Sci. USA 102 (2005) 5749-5754
41. Mirault M.E., Goldschmidt-Clermont M., Moran L., Arrigo A.P., and Tissieres A. The effect of heat shock on gene expression in Drosophila melanogaster. Cold Spring Harb. Symp. Quant. Biol. 42 (1978) 819-827
42. Ni Z., Schwartz B.E., Werner J., Suarez J.R., and Lis J.T. Coordination of transcription, RNA processing, and surveillance by P-TEFb kinase on heat shock genes. Mol. Cell 13 (2004) 55-65
43. Palancade B., and Bensaude O. Investigating RNA polymerase II carboxyl-terminal domain (CTD) phosphorylation. Eur. J. Biochem. 270 (2003) 3859-3870
44. Patturajan M., Schulte R.J., Sefton B.M., Berezney R., Vincent M., Bensaude O., Warren S.L., and Corden J.L. Growth-related changes in phosphorylation of yeast RNA polymerase II. J. Biol. Chem. 273 (1998) 4689-4694
45. Pickersgill H., Kalverda B., de Wit E., Talhout W., Fornerod M., and van Steensel B. Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat. Genet. 38 (2006) 1005-1014
46. Rabut G., Doye V., and Ellenberg J. Mapping the dynamic organization of the nuclear pore complex inside single living cells. Nat. Cell Biol. 6 (2004) 1114-1121
47. Roth P., Xylourgidis N., Sabri N., Uv A., Fornerod M., and Samakovlis C. The Drosophila nucleoporin DNup88 localizes DNup214 and CRM1 on the nuclear envelope and attenuates NES-mediated nuclear export. J. Cell Biol. 163 (2003) 701-706
48. Schmid M., Arib G., Laemmli C., Nishikawa J., Durussel T., and Laemmli U.K. Nup-PI: the nucleopore-promoter interaction of genes in yeast. Mol. Cell 21 (2006) 379-391
49. Shim E.Y., Walker A.K., Shi Y., and Blackwell T.K. CDK-9/cyclin T (P-TEFb) is required in two postinitiation pathways for transcription in the C. elegans embryo. Genes Dev. 16 (2002) 2135-2146
50. Siniossoglou S., Wimmer C., Rieger M., Doye V., Tekotte H., Weise C., Emig S., Segref A., and Hurt E.C. A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell 84 (1996) 265-275
51. Slape C., and Aplan P.D. The role of NUP98 gene fusions in hematologic malignancy. Leuk. Lymphoma 45 (2004) 1341-1350
52. Spradling A., Penman S., and Pardue M.L. Analysis of Drosophila mRNA by in situ hybridization: Sequences transcribed in normal and heat-shocked cultured cells. Cell 4 (1975) 395-404
53. Strasser K., Bassler J., and Hurt E. Binding of the Mex67p/Mtr2p heterodimer to FXFG, GLFG, and FG repeat nucleoporins is essential for nuclear mRNA export. J. Cell Biol. 150 (2000) 695-706
54. Taddei A., Van Houwe G., Hediger F., Kalck V., Cubizolles F., Schober H., and Gasser S.M. Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 441 (2006) 774-778
55. Thummel C.S. Puffs and gene regulation-molecular insights into the Drosophila ecdysone regulatory hierarchy. Bioessays 12 (1990) 561-568
56. Uv A.E., Roth P., Xylourgidis N., Wickberg A., Cantera R., and Samakovlis C. Members only encodes a Drosophila nucleoporin required for rel protein import and immune response activation. Genes Dev. 14 (2000) 1945-1957
57. Vasu S., Shah S., Orjalo A., Park M., Fischer W.H., and Forbes D.J. Novel vertebrate nucleoporins Nup133 and Nup160 play a role in mRNA export. J. Cell Biol. 155 (2001) 339-354
58. Weis K. Nucleocytoplasmic transport: cargo trafficking across the border. Curr. Opin. Cell Biol. 14 (2002) 328-335
59. Wente S.R. Gatekeepers of the nucleus. Science 288 (2000) 1374-1377