Nup50 is required for cell differentiation and exhibits transcription-dependent dynamics

Molecular Biology of the Cell

Volumn 25, Issue 16, 2014, Pages 2472-2484

  Buchwalter, Abigail L ^a   Liang, Yun ^a   Hetzer, Martin W ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA INTERCALATOR; GREEN FLUORESCENT PROTEIN; INTERCALATING AGENT; KARYOPHERIN ALPHA; MYOSIN HEAVY CHAIN; NUCLEOPORIN; NUCLEOPORIN 153; NUCLEOPORIN 50; NUCLEOPORIN 98; RNA POLYMERASE II; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; CHROMATIN; NUP153 PROTEIN, MOUSE; NUP50 PROTEIN, MOUSE; RNA;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE LOCUS; HETEROCHROMATIN; MOLECULAR DYNAMICS; MOUSE; MYOBLAST; MYOTUBE; NONHUMAN; NUCLEAR PORE; NUCLEAR PORE COMPLEX; NUCLEOCYTOPLASMIC TRANSPORT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN IMMOBILIZATION; PROTEIN TRANSPORT; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; ANIMAL; CHROMATIN; CULTURE TECHNIQUE; CYTOPLASM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

ALPHA KARYOPHERINS; ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CHROMATIN; CYTOPLASM; GENE EXPRESSION REGULATION; MICE; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; RNA;

EID: 84905984203     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-04-0865     Document Type: Article

References (50)

1. Bensaude O (2011). Inhibiting eukaryotic transcription: which compound to choose? how to evaluate its activity? Transcription 2, 103-108.
2. Blevins MB, Smith AM, Phillips EM, Powers MA (2003). Complex formation among the RNA export proteins Nup98, Rae1/Gle2, and TAP. J Biol Chem 278, 20979-20988. (Pubitemid 36806407)
3. Blobel G (1985). Gene gating: a hypothesis. Proc Natl Acad Sci USA 82, 8527-8529.
4. Brickner DG, Ahmed S, Meldi L, Thompson A, Light W, Young M, Hickman TL, Chu F, Fabre E, Brickner JH (2012). Transcription factor binding to a DNA zip code controls interchromosomal clustering at the nuclear periphery. Dev Cell 22, 1234-1246.
5. Capelson M, Liang Y, Schulte R, Mair W, Wagner U, Hetzer MW (2010). Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 140, 372-383.
6. Casolari JM, Brown CR, Komili S, West J, Hieronymus H, Silver PA (2004). Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117, 427-439. (Pubitemid 38610229)
7. Catez F, Brown DT, Misteli T, Bustin M (2002). Competition between histone H1 and HMGN proteins for chromatin binding sites. EMBO Rep 3, 760-766. (Pubitemid 34966015)
8. Chen TA, Sterner R, Cozzolino A, Allfrey VG (1990). Reversible and irreversible changes in nucleosome structure along the c-fos and c-myc oncogenes following inhibition of transcription. J Mol Biol 212, 481-493.
9. Cheung TH, Rando TA (2013). Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol 14, 329-340.
10. Cheutin T, McNairn AJ, Jenuwein T, Gilbert DM, Singh PB, Misteli T (2003). Maintenance of stable heterochromatin domains by dynamic HP1 binding. Science 299, 721-725. (Pubitemid 36159490)
11. Cronshaw JM (2002). Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol 158, 915-927.
12. D'Angelo MA, Gomez-Cavazos JS, Mei A, Lackner DH, Hetzer MW (2012). A change in nuclear pore complex composition regulates cell differentiation. Dev Cell 22, 446-458.
13. Darzacq X, Shav-Tal Y, de Turris V, Brody Y, Shenoy SM, Phair RD, Singer RH (2007). In vivo dynamics of RNA polymerase II transcription. Nat Struct Mol Biol 14, 796-806. (Pubitemid 47373828)
14. Dilworth DJ (2005). The mobile nucleoporin Nup2p and chromatin-bound Prp20p function in endogenous NPC-mediated transcriptional control. J Cell Biol 171, 955-965.
15. Doucet CM, Talamas JA, Hetzer MW (2010). Cell cycle-dependent differences in nuclear pore complex assembly in Metazoa. Cell 141, 1030-1041.
16. Galbraith MD, Espinosa JM (2011). Lessons on transcriptional control from the serum response network. Curr Opin Genet Dev 21, 160-166.
17. Griffis ER, Altan N, Lippincott-Schwartz J, Powers MA (2002). Nup98 is a mobile nucleoporin with transcription-dependent dynamics. Mol Biol Cell 13, 1282-1297. (Pubitemid 34309623)
18. Griffis ER, Craige B, Dimaano C, Ullman KS, Powers MA (2004). Distinct functional domains within nucleoporins Nup153 and Nup98 mediate transcription-dependent mobility. Mol Biol Cell 15, 1991-2002. (Pubitemid 38401845)
19. Guan T, Kehlenbach RH, Schirmer EC, Kehlenbach A, Fan F, Clurman BE, Arnheim N, Gerace L (2000). Nup50, a nucleoplasmically oriented nucleoporin with a role in nuclear protein export. Mol Cell Biol 20, 5619-5630. (Pubitemid 30482896)
20. Hase ME, Cordes VC (2003). Direct interaction with nup153 mediates binding of Tpr to the periphery of the nuclear pore complex. Mol Biol Cell 14, 1923-1940. (Pubitemid 36583543)
21. Kalverda B, Pickersgill H, Shloma VV, Fornerod M (2010). Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell 140, 360-371.
22. Kimura H (2002). The transcription cycle of RNA polymerase II in living cells. J Cell Biol 159, 777-782.
23. Liang Y, Franks TM, Marchetto MC, Gage FH, Hetzer MW (2013). Dynamic association of NUP98 with the human genome. PLoS Genet 9, e1003308.
24. Light WH, Brickner DG, Brand VR, Brickner JH (2010). Interaction of a DNA zip code with the nuclear pore complex promotes H2A. Z incorporation and INO1 transcriptional memory. Mol Cell 40, 112-125.
25. Lindsay ME, Macara IG (2002). Npap60/Nup50 is a tri-stable switch that stimulates importin-alpha:beta-mediated nuclear protein import. Cell 110, 349-360.
26. Makise M, Mackay DR, Elgort S, Shankaran SS, Adam SA, Ullman KS (2012). The Nup153-Nup50 protein interface and its role in nuclear import. J Biol Chem 287, 38515-38522.
27. Mueller F, Karpova TS, Mazza D, McNally JG (2011). Monitoring dynamic binding of chromatin proteins in vivo by fluorescence recovery after photobleaching. Methods Mol Biol 833: 153-176.
28. Olsson M, Schéele S, Ekblom P (2004). Limited expression of nuclear pore membrane glycoprotein 210 in cell lines and tissues suggests cell-type specific nuclear pores in metazoans. Exp Cell Res 292, 359-370. (Pubitemid 38018851)
29. Pascual-Garcia P, Capelson M (2014). Nuclear pores as versatile platforms for gene regulation. Curr Opin Genet Dev 25C, 110-117.
30. Pumroy RA, Nardozzi JD, Hart DJ, Root MJ, Cingolani G (2012). Nucleoporin Nup50 stabilizes closed conformation of armadillo repeat 10 in importin α5. J Biol Chem 287, 2022-2031.
31. Rabut G, Doye V, Ellenberg J (2004a). Mapping the dynamic organization of the nuclear pore complex inside single living cells. Nat Cell Biol 6, 1114-1121. (Pubitemid 39468013)
32. Rabut G, Lénárt P, Ellenberg J (2004b). Dynamics of nuclear pore complex organization through the cell cycle. Curr Opin Cell Biol 16, 314-321. (Pubitemid 38610413)
33. Radu A, Moore MS, Blobel G (1995). The peptide repeat domain of nucleoporin Nup98 functions as a docking site in transport across the nuclear pore complex. Cell 81, 215-222.
34. Raices M, D'Angelo MA (2012). Nuclear pore complex composition: a new regulator of tissue-specific and developmental functions. Nat Rev Mol Cell Biol 13, 687-699.
35. Richard E, Causse S, Spriet C, Fourré N, Trinel D, Darzacq X, Vandenbunder B, Heliot L (2011). Short exposure to the DNA intercalator DRAQ5 dislocates the transcription machinery and induces cell death. Photochem Photobiol 87, 256-261.
36. Rodriguez-Bravo V, Maciejowski J, Corona J, Buch HK, Collin P, Kanemaki MT, Shah JV, Jallepalli PV (2014). Nuclear pores protect genome integrity by assembling a premitotic and mad1-dependent anaphase inhibitor. Cell 156, 1017-1031.
37. Rougemaille M et al. (2008). THO/Sub2p functions to coordinate 3′-end processing with gene-nuclear pore association. Cell 135, 308-321.
38. Singer S et al. (2012). Nuclear pore component Nup98 is a potential tumor suppressor and regulates posttranscriptional expression of select p53 target genes. Mol Cell 48, 799-810.
39. Smitherman M, Lee K, Swanger J, Kapur R, Clurman BE (2000). Characterization and targeted disruption of murine Nup50, a p27(Kip1)- interacting component of the nuclear pore complex. Mol Cell Biol 20, 5631-5642. (Pubitemid 30482897)
40. Stenoien DL, Patel K, Mancini MG, Dutertre M, Smith CL, O'Malley BW, Mancini MA (2001). FRAP reveals that mobility of oestrogen receptor-alpha is ligand- and proteasome-dependent. Nat Cell Biol 3, 15-23. (Pubitemid 32114827)
41. Taddei A, Van Houwe G, Hediger F, Kalck V, Cubizolles F, Schober H, Gasser SM (2006). Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 441, 774-778. (Pubitemid 43865226)
42. Tan-Wong SM, Wijayatilake HD, Proudfoot NJ (2009). Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex. Genes Dev 23, 2610-2624.
43. Umlauf D, Bonnet J, Waharte F, Fournier M, Stierle M, Fischer B, Brino L, Devys D, Tora L (2013). The human TREX-2 complex is stably associated with the nuclear pore basket. J Cell Sci 126, 2656-2667.
44. Van de Vosse DW, Wan Y, Lapetina DL, Chen W-M, Chiang J-H, Aitchison JD, Wozniak RW (2013). A role for the nucleoporin Nup170p in chromatin structure and gene silencing. Cell 152, 969-983.
45. Vargas JD, Hatch EM, Anderson DJ, Hetzer MW (2012). Transient nuclear envelope rupturing during interphase in human cancer cells. Nucleus 3, 88-100.
46. Vaquerizas JM, Suyama R, Kind J, Miura K, Luscombe NM, Akhtar A (2010). Nuclear pore proteins nup153 and megator define transcriptionally active regions in the Drosophila genome. PLoS Genet 6, e1000846.
47. Wente SR, Rout MP (2010). The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol 2, a000562.
48. White CM, Heidenreich O, Nordheim A, Beerman TA (2000). Evaluation of the effectiveness of DNA-binding drugs to inhibit transcription using the c-fos serum response element as a target. Biochemistry 39, 12262-12273.
49. Yu FL (1983). Actinomycin D-binding in vivo: active chromatin preferred. FEBS Lett 156, 83-87.
50. Zhang K, Sha J, Harter ML (2010). Activation of Cdc6 by MyoD is associated with the expansion of quiescent myogenic satellite cells. J Cell Biol 188, 39-48.