90
Views
37
CrossRef citations to date
0
Altmetric
Minireview

From Hypothesis to Mechanism: Uncovering Nuclear Pore Complex Links to Gene Expression

&
Pages 2114-2120 | Published online: 20 Mar 2023

REFERENCES

  • Blobel G. 1985. Gene gating: a hypothesis. Proc. Natl. Acad. Sci. U. S. A. 82:8527–8529. http://dx.doi.org/10.1073/pnas.82.24.8527.
  • Zirbel RM, Mathieu UR, Kurz A, Cremer T, Lichter P. 1993. Evidence for a nuclear compartment of transcription and splicing located at chromosome domain boundaries. Chromosome Res. 1:93–106. http://dx.doi.org/10.1007/BF00710032.
  • Cremer T, Kurz A, Zirbel R, Dietzel S, Rinke B, Schrock E, Speicher MR, Mathieu U, Jauch A, Emmerich P, Scherthan H, Ried T, Cremer C, Lichter P. 1993. Role of chromosome territories in the functional compartmentalization of the cell nucleus. Cold Spring Harbor Symp. Quant. Biol. 58:777–792. http://dx.doi.org/10.1101/SQB.1993.058.01.085.
  • Aitchison JD, Rout MP. 2012. The yeast nuclear pore complex and transport through it. Genetics 190:855–883. http://dx.doi.org/10.1534/genetics.111.127803.
  • Goldberg MW, Allen TD. 1992. High resolution scanning electron microscopy of the nuclear envelope: demonstration of a new, regular, fibrous lattice attached to the baskets of the nucleoplasmic face of the nuclear pores. J. Cell Biol. 119:1429–1440. http://dx.doi.org/10.1083/jcb.119.6.1429.
  • Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, Chait BT. 2000. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 148:635–651. http://dx.doi.org/10.1083/jcb.148.4.635.
  • Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, Sali A, Rout MP. 2007. The molecular architecture of the nuclear pore complex. Nature 450:695–701. http://dx.doi.org/10.1038/nature06405.
  • Bilokapic S, Schwartz TU. 2012. 3D ultrastructure of the nuclear pore complex. Curr. Opin. Cell Biol. 24:86–91. http://dx.doi.org/10.1016/j.ceb.2011.12.011.
  • Fernandez-Martinez J, Rout MP. 2012. A jumbo problem: mapping the structure and functions of the nuclear pore complex. Curr. Opin. Cell Biol. 24:92–99. http://dx.doi.org/10.1016/j.ceb.2011.12.013.
  • Rothballer A, Kutay U. 2012. SnapShot: the nuclear envelope II. Cell 150:1084–1084.e1081. http://dx.doi.org/10.1016/j.cell.2012.08.003.
  • Rabut G, Doye V, Ellenberg J. 2004. Mapping the dynamic organization of the nuclear pore complex inside single living cells. Nat. Cell Biol. 6:1114–1121. http://dx.doi.org/10.1038/ncb1184.
  • Dilworth DJ, Suprapto A, Padovan JC, Chait BT, Wozniak RW, Rout MP, Aitchison JD. 2001. Nup2p dynamically associates with the distal regions of the yeast nuclear pore complex. J. Cell Biol. 153:1465–1478. http://dx.doi.org/10.1083/jcb.153.7.1465.
  • Kohler A, Hurt E. 2007. Exporting RNA from the nucleus to the cytoplasm. Nat. Rev. Mol. Cell Biol. 8:761–773. http://dx.doi.org/10.1038/nrm2255.
  • Natalizio BJ, Wente SR. 2013. Postage for the messenger: designating routes for nuclear mRNA export. Trends Cell Biol. 23:365–373. http://dx.doi.org/10.1016/j.tcb.2013.03.006.
  • Rodriguez-Navarro S, Hurt E. 2011. Linking gene regulation to mRNA production and export. Curr. Opin. Cell Biol. 23:302–309. http://dx.doi.org/10.1016/j.ceb.2010.12.002.
  • Babour A, Dargemont C, Stutz F. 2012. Ubiquitin and assembly of export competent mRNP. Biochim. Biophys. Acta 1819:521–530. http://dx.doi.org/10.1016/j.bbagrm.2011.12.006.
  • Muller-McNicoll M, Neugebauer KM. 2013. How cells get the message: dynamic assembly and function of mRNA-protein complexes. Nat. Rev. Genet. 14:275–287. http://dx.doi.org/10.1038/nrg3434.
  • Tutucci E, Stutz F. 2011. Keeping mRNPs in check during assembly and nuclear export. Nat. Rev. Mol. Cell Biol. 12:377–384. http://dx.doi.org/10.1038/nrm3119.
  • Schmid M, Jensen TH. 2013. Transcription-associated quality control of mRNP. Biochim. Biophys. Acta 1829:158–168. http://dx.doi.org/10.1016/j.bbagrm.2012.08.012.
  • Folkmann AW, Noble KN, Cole CN, Wente SR. 2011. Dbp5, Gle1-IP6 and Nup159: a working model for mRNP export. Nucleus 2:540–548. http://dx.doi.org/10.4161/nucl.2.6.17881.
  • Valkov E, Dean JC, Jani D, Kuhlmann SI, Stewart M. 2012. Structural basis for the assembly and disassembly of mRNA nuclear export complexes. Biochim. Biophys. Acta 1819:578–592. http://dx.doi.org/10.1016/j.bbagrm.2012.02.017.
  • Nino CA, Herissant L, Babour A, Dargemont C. 2013. mRNA nuclear export in yeast. Chem. Rev. 113:8523–8545. http://dx.doi.org/10.1021/cr400002g.
  • Dilworth DJ, Tackett AJ, Rogers RS, Yi EC, Christmas RH, Smith JJ, Siegel AF, Chait BT, Wozniak RW, Aitchison JD. 2005. The mobile nucleoporin Nup2p and chromatin-bound Prp20p function in endogenous NPC-mediated transcriptional control. J. Cell Biol. 171:955–965. http://dx.doi.org/10.1083/jcb.200509061.
  • Ishii K, Arib G, Lin C, Van Houwe G, Laemmli UK. 2002. Chromatin boundaries in budding yeast: the nuclear pore connection. Cell 109:551–562. http://dx.doi.org/10.1016/S0092-8674(02)00756-0.
  • Brickner DG, Cajigas I, Fondufe-Mittendorf Y, Ahmed S, Lee PC, Widom J, Brickner JH. 2007. H2A.Z-mediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol. 5:e81. http://dx.doi.org/10.1371/journal.pbio.0050081.
  • 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. http://dx.doi.org/10.1038/nature04845.
  • Brickner JH, Walter P. 2004. Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol. 2:e342. http://dx.doi.org/10.1371/journal.pbio.0020342.
  • Cabal GG, Genovesio A, Rodriguez-Navarro S, Zimmer C, Gadal O, Lesne A, Buc H, Feuerbach-Fournier F, Olivo-Marin JC, Hurt EC, Nehrbass U. 2006. SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441:770–773. http://dx.doi.org/10.1038/nature04752.
  • Dieppois G, Iglesias N, Stutz F. 2006. Cotranscriptional recruitment to the mRNA export receptor Mex67p contributes to nuclear pore anchoring of activated genes. Mol. Cell. Biol. 26:7858–7870. http://dx.doi.org/10.1128/MCB.00870-06.
  • 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. http://dx.doi.org/10.1016/S0092-8674(04)00448-9.
  • Schmid M, Arib G, Laemmli C, Nishikawa J, Durussel T, Laemmli UK. 2006. Nup-PI: the nucleopore-promoter interaction of genes in yeast. Mol. Cell 21:379–391. http://dx.doi.org/10.1016/j.molcel.2005.12.012.
  • Luthra R, Kerr SC, Harreman MT, Apponi LH, Fasken MB, Ramineni S, Chaurasia S, Valentini SR, Corbett AH. 2007. Actively transcribed GAL genes can be physically linked to the nuclear pore by the SAGA chromatin modifying complex. J. Biol. Chem. 282:3042–3049. http://dx.doi.org/10.1074/jbc.M608741200.
  • Abruzzi KC, Belostotsky DA, Chekanova JA, Dower K, Rosbash M. 2006. 3′-end formation signals modulate the association of genes with the nuclear periphery as well as mRNP dot formation. EMBO J. 25:4253–4262. http://dx.doi.org/10.1038/sj.emboj.7601305.
  • Sarma NJ, Haley TM, Barbara KE, Buford TD, Willis KA, Santangelo GM. 2007. Glucose-responsive regulators of gene expression in Saccharomyces cerevisiae function at the nuclear periphery via a reverse recruitment mechanism. Genetics 175:1127–1135.
  • Ahmed S, Brickner DG, Light WH, Cajigas I, McDonough M, Froyshteter AB, Volpe T, Brickner JH. 2010. DNA zip codes control an ancient mechanism for gene targeting to the nuclear periphery. Nat. Cell Biol. 12:111–118. http://dx.doi.org/10.1038/ncb2011.
  • 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. http://dx.doi.org/10.1016/j.devcel.2012.03.012.
  • Burns LT, Wente SR. 2012. Nuclear GPS for interchromosomal clustering. Dev. Cell 22:1119–1120. http://dx.doi.org/10.1016/j.devcel.2012.05.019.
  • Seo HS, Blus BJ, Jankovic NZ, Blobel G. 2013. Structure and nucleic acid binding activity of the nucleoporin Nup157. Proc. Natl. Acad. Sci. U. S. A. 110:16450–16455. http://dx.doi.org/10.1073/pnas.1316607110.
  • Ball JR, Dimaano C, Bilak A, Kurchan E, Zundel MT, Ullman KS. 2007. Sequence preference in RNA recognition by the nucleoporin Nup153. J. Biol. Chem. 282:8734–8740. http://dx.doi.org/10.1074/jbc.M608477200.
  • 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. http://dx.doi.org/10.1016/j.molcel.2010.09.007.
  • Brickner DG, Brickner JH. 2010. Cdk phosphorylation of a nucleoporin controls localization of active genes through the cell cycle. Mol. Biol. Cell 21:3421–3432. http://dx.doi.org/10.1091/mbc.E10-01-0065.
  • Hakim O, Misteli T. 2012. SnapShot: chromosome confirmation capture. Cell 148:1068.e1-2. http://dx.doi.org/10.1016/j.cell.2012.02.019.
  • Van de Vosse DW, Wan Y, Lapetina DL, Chen WM, Chiang JH, Aitchison JD, Wozniak RW. 2013. A role for the nucleoporin Nup170p in chromatin structure and gene silencing. Cell 152:969–983. http://dx.doi.org/10.1016/j.cell.2013.01.049.
  • Dubarry M, Loiodice I, Chen CL, Thermes C, Taddei A. 2011. Tight protein-DNA interactions favor gene silencing. Genes Dev. 25:1365–1370. http://dx.doi.org/10.1101/gad.611011.
  • Meister P, Towbin BD, Pike BL, Ponti A, Gasser SM. 2010. The spatial dynamics of tissue-specific promoters during C. elegans development. Genes Dev. 24:766–782. http://dx.doi.org/10.1101/gad.559610.
  • Mattout A, Pike BL, Towbin BD, Bank EM, Gonzalez-Sandoval A, Stadler MB, Meister P, Gruenbaum Y, Gasser SM. 2011. An EDMD mutation in C. elegans lamin blocks muscle-specific gene relocation and compromises muscle integrity. Curr. Biol. 21:1603–1614. http://dx.doi.org/10.1016/j.cub.2011.08.030.
  • Towbin BD, Gonzalez-Aguilera C, Sack R, Gaidatzis D, Kalck V, Meister P, Askjaer P, Gasser SM. 2012. Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150:934–947. http://dx.doi.org/10.1016/j.cell.2012.06.051.
  • Rohner S, Kalck V, Wang X, Ikegami K, Lieb JD, Gasser SM, Meister P. 2013. Promoter- and RNA polymerase II-dependent hsp-16 gene association with nuclear pores in Caenorhabditis elegans. J. Cell Biol. 200:589–604. http://dx.doi.org/10.1083/jcb.201207024.
  • 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. http://dx.doi.org/10.1371/journal.pgen.1000846.
  • 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. http://dx.doi.org/10.1016/j.cell.2010.01.011.
  • 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. http://dx.doi.org/10.1016/j.cell.2009.12.054.
  • Lawrence JB, Singer RH, Marselle LM. 1989. Highly localized tracks of specific transcripts within interphase nuclei visualized by in situ hybridization. Cell 57:493–502. http://dx.doi.org/10.1016/0092-8674(89)90924-0.
  • Huang S, Spector DL. 1991. Nascent pre-mRNA transcripts are associated with nuclear regions enriched in splicing factors. Genes Dev. 5:2288–2302. http://dx.doi.org/10.1101/gad.5.12a.2288.
  • Vargas DY, Raj A, Marras SA, Kramer FR, Tyagi S. 2005. Mechanism of mRNA transport in the nucleus. Proc. Natl. Acad. Sci. U. S. A. 102:17008–17013. http://dx.doi.org/10.1073/pnas.0505580102.
  • Mor A, Suliman S, Ben-Yishay R, Yunger S, Brody Y, Shav-Tal Y. 2010. Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Nat. Cell Biol. 12:543–552. http://dx.doi.org/10.1038/ncb2056.
  • 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. http://dx.doi.org/10.1016/j.devcel.2011.11.021.
  • Williams RR, Azuara V, Perry P, Sauer S, Dvorkina M, Jorgensen H, Roix J, McQueen P, Misteli T, Merkenschlager M, Fisher AG. 2006. Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J. Cell Sci. 119:132–140. http://dx.doi.org/10.1242/jcs.02727.
  • Ragoczy T, Bender MA, Telling A, Byron R, Groudine M. 2006. The locus control region is required for association of the murine beta-globin locus with engaged transcription factories during erythroid maturation. Genes Dev. 20:1447–1457. http://dx.doi.org/10.1101/gad.1419506.
  • Takizawa T, Gudla PR, Guo L, Lockett S, Misteli T. 2008. Allele-specific nuclear positioning of the monoallelically expressed astrocyte marker GFAP. Genes Dev. 22:489–498. http://dx.doi.org/10.1101/gad.1634608.
  • Yao J, Fetter RD, Hu P, Betzig E, Tjian R. 2011. Subnuclear segregation of genes and core promoter factors in myogenesis. Genes Dev. 25:569–580. http://dx.doi.org/10.1101/gad.2021411.
  • Liang Y, Franks TM, Marchetto MC, Gage FH, Hetzer MW. 2013. Dynamic association of NUP98 with the human genome. PLoS Genet. 9:e1003308. http://dx.doi.org/10.1371/journal.pgen.1003308.
  • Chatel G, Desai SH, Mattheyses AL, Powers MA, Fahrenkrog B. 2012. Domain topology of nucleoporin Nup98 within the nuclear pore complex. J. Struct. Biol. 177:81–89. http://dx.doi.org/10.1016/j.jsb.2011.11.004.
  • Singer S, Zhao R, Barsotti AM, Ouwehand A, Fazollahi M, Coutavas E, Breuhahn K, Neumann O, Longerich T, Pusterla T, Powers MA, Giles KM, Leedman PJ, Hess J, Grunwald D, Bussemaker HJ, Singer RH, Schirmacher P, Prives C. 2012. Nuclear pore component Nup98 is a potential tumor suppressor and regulates posttranscriptional expression of select p53 target genes. Mol. Cell 48:799–810. http://dx.doi.org/10.1016/j.molcel.2012.09.020.
  • 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. http://dx.doi.org/10.1091/mbc.01-11-0538.
  • Light WH, Freaney J, Sood V, Thompson A, D'Urso A, Horvath CM, Brickner JH. 2013. A conserved role for human Nup98 in altering chromatin structure and promoting epigenetic transcriptional memory. PLoS Biol. 11:e1001524. http://dx.doi.org/10.1371/journal.pbio.1001524.
  • Krull S, Dorries J, Boysen B, Reidenbach S, Magnius L, Norder H, Thyberg J, Cordes VC. 2010. Protein Tpr is required for establishing nuclear pore-associated zones of heterochromatin exclusion. EMBO J. 29:1659–1673. http://dx.doi.org/10.1038/emboj.2010.54.
  • Miyanari Y, Ziegler-Birling C, Torres-Padilla ME. 2013. Live visualization of chromatin dynamics with fluorescent TALEs. Nat. Struct. Mol. Biol. 20:1321–1324. http://dx.doi.org/10.1038/nsmb.2680.
  • Bickmore WA, van Steensel B. 2013. Genome architecture: domain organization of interphase chromosomes. Cell 152:1270–1284. http://dx.doi.org/10.1016/j.cell.2013.02.001.
  • Chen B, Gilbert LA, Cimini BA, Schnitzbauer J, Zhang W, Li GW, Park J, Blackburn EH, Weissman JS, Qi LS, Huang B. 2013. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155:1479–1491. http://dx.doi.org/10.1016/j.cell.2013.12.001.
  • Hopper AK. 2013. Transfer RNA post-transcriptional processing, turnover, and subcellular dynamics in the yeast Saccharomyces cerevisiae. Genetics 194:43–67. http://dx.doi.org/10.1534/genetics.112.147470.
  • Zhao X, Wu CY, Blobel G. 2004. Mlp-dependent anchorage and stabilization of a desumoylating enzyme is required to prevent clonal lethality. J. Cell Biol. 167:605–611. http://dx.doi.org/10.1083/jcb.200405168.
  • Vinciguerra P, Iglesias N, Camblong J, Zenklusen D, Stutz F. 2005. Perinuclear Mlp proteins downregulate gene expression in response to a defect in mRNA export. EMBO J. 24:813–823. http://dx.doi.org/10.1038/sj.emboj.7600527.
  • Colon-Ramos DA, Salisbury JL, Sanders MA, Shenoy SM, Singer RH, Garcia-Blanco MA. 2003. Asymmetric distribution of nuclear pore complexes and the cytoplasmic localization of beta2-tubulin mRNA in Chlamydomonas reinhardtii. Dev. Cell 4:941–952. http://dx.doi.org/10.1016/S1534-5807(03)00163-1.
  • Powrie EA, Zenklusen D, Singer RH. 2011. A nucleoporin, Nup60p, affects the nuclear and cytoplasmic localization of ASH1 mRNA in S. cerevisiae. RNA 17:134–144. http://dx.doi.org/10.1261/rna.1210411.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.