Dynamic Encounters of Genes and Transcripts with the Nuclear Pore

Trends in Genetics

Volumn 32, Issue 7, 2016, Pages 419-431

  Ben Yishay, Rakefet ^a   Ashkenazy, Asaf J ^a   Shav Tal, Yaron ^a  

^a BAR ILAN UNIVERSITY   (Israel)

Author keywords

Chromatin; Gene tethering; MRNA dynamics; MRNA export; Nuclear pore complex

Indexed keywords

DNA DIRECTED RNA POLYMERASE III; LONG UNTRANSLATED RNA; MESSENGER RNA; NUCLEOPORIN; POLYADENYLATED RNA; SMALL NUCLEOLAR RNA; UBIQUITIN PROTEIN LIGASE E3; UNTRANSLATED RNA; WHEAT GERM AGGLUTININ; CHROMATIN; RIBONUCLEOPROTEIN;

CAENORHABDITIS ELEGANS; CELL NUCLEUS MEMBRANE; CHROMATIN STRUCTURE; CYTOPLASM; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE SILENCING; GENE TETHERING; GENETIC PROCEDURES; GENETIC TRANSCRIPTION; HETEROCHROMATIN; HUMAN; MAMMAL CELL; NONHUMAN; NUCLEAR PORE; NUCLEAR PORE COMPLEX; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RNA TRANSPORT; SACCHAROMYCES CEREVISIAE; YEAST CELL; CELL NUCLEUS; CHROMATIN; GENETICS;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEUS; CHROMATIN; CYTOPLASM; GENE EXPRESSION REGULATION; NUCLEAR PORE; RIBONUCLEOPROTEINS; RNA TRANSPORT; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 84966702471     PISSN: 01689525     EISSN: 13624555     Source Type: Journal    
DOI: 10.1016/j.tig.2016.04.003     Document Type: Review

References (139)

1. Shav-Tal Y., et al. Dynamics of single mRNPs in nuclei of living cells. Science 2004, 304:1797-1800.
2. Mor A., et al. Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Nat. Cell Biol. 2010, 12:543-552.
3. Politz J.C., et al. Movement of nuclear poly(A) RNA throughout the interchromatin space in living cells. Curr. Biol. 1999, 9:285-291.
4. Politz J.C., et al. Intranuclear diffusion and hybridization state of oligonucleotides measured by fluorescence correlation spectroscopy in living cells. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:6043-6048.
5. Grunwald D., Singer R.H. In vivo imaging of labelled endogenous beta-actin mRNA during nucleocytoplasmic transport. Nature 2010, 467:604-607.
6. Calapez A., et al. The intranuclear mobility of messenger RNA binding proteins is ATP dependent and temperature sensitive. J. Cell Biol. 2002, 159:795-805.
7. Vargas D.Y., et al. Mechanism of mRNA transport in the nucleus. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:17008-17013.
8. Siebrasse J.P., et al. Discontinuous movement of mRNP particles in nucleoplasmic regions devoid of chromatin. Proc. Natl. Acad. Sci. U S A 2008, 105:20291-20296.
9. Siebrasse J.P., et al. Nuclear export of single native mRNA molecules observed by light sheet fluorescence microscopy. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:9426-9431.
10. Molenaar C., et al. Poly(A)+ RNAs roam the cell nucleus and pass through speckle domains in transcriptionally active and inactive cells. J. Cell Biol. 2004, 165:191-202.
11. Daneholt B. A look at messenger RNP moving through the nuclear pore. Cell 1997, 88:585-588.
12. Mor A., Shav-Tal Y. Dynamics and kinetics of nucleo-cytoplasmic mRNA export. Wiley Interdiscip. Rev. RNA 2010, 1:388-401.
13. Spille J.H., Kubitscheck U. Labelling and imaging of single endogenous messenger RNA particles in vivo. J. Cell Sci. 2015, 128:3695-3706.
14. Bann D.V., Parent L.J. Application of live-cell RNA imaging techniques to the study of retroviral RNA trafficking. Viruses 2012, 4:963-979.
15. Blobel G. Gene gating: a hypothesis. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:8527-8529.
16. Casolari J.M., et al. Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 2004, 117:427-439.
17. Brickner J.H., Walter P. Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol. 2004, 2:e342.
18. Taddei A., et al. Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 2006, 441:774-778.
19. Texari L., et al. The nuclear pore regulates GAL1 gene transcription by controlling the localization of the SUMO protease Ulp1. Mol. Cell 2013, 51:807-818.
20. Rohner S., et al. Promoter- and RNA polymerase II-dependent hsp-16 gene association with nuclear pores in Caenorhabditis elegans. J. Cell Biol. 2013, 200:589-604.
21. Van de Vosse D.W., et al. A role for the nucleoporin Nup170p in chromatin structure and gene silencing. Cell 2013, 152:969-983.
22. Saroufim M.A., et al. The nuclear basket mediates perinuclear mRNA scanning in budding yeast. J. Cell Biol. 2015, 211:1131-1140.
23. Randise-Hinchliff C., et al. Strategies to regulate transcription factor-mediated gene positioning and interchromosomal clustering at the nuclear periphery. J. Cell Biol. 2016, 212:633-646.
24. Tan-Wong S.M., et al. Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex. Genes Dev. 2009, 23:2610-2624.
25. Green E.M., et al. A negative feedback loop at the nuclear periphery regulates GAL gene expression. Mol. Biol. Cell 2012, 23:1367-1375.
26. Brickner D.G., et al. H2A.Z-mediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol. 2007, 5:e81.
27. Ikegami K., Lieb J.D. Integral nuclear pore proteins bind to Pol III-transcribed genes and are required for Pol III transcript processing in C. elegans. Mol. Cell 2013, 51:840-849.
28. Ibarra A., Hetzer M.W. Nuclear pore proteins and the control of genome functions. Genes Dev. 2015, 29:337-349.
29. Krull S., et al. Protein Tpr is required for establishing nuclear pore-associated zones of heterochromatin exclusion. EMBO J. 2010, 29:1659-1673.
30. Bronshtein I., et al. Loss of lamin A function increases chromatin dynamics in the nuclear interior. Nat. Commun. 2015, 6:8044.
31. Khanna N., et al. HSP70 transgene directed motion to nuclear speckles facilitates heat shock activation. Curr. Biol. 2014, 24:1138-1144.
32. Chuang C.H., et al. Long-range directional movement of an interphase chromosome site. Curr. Biol. 2006, 16:825-831.
33. Breuer M., Ohkura H. A negative loop within the nuclear pore complex controls global chromatin organization. Genes Dev. 2015, 29:1789-1794.
34. Smith S., et al. Marker gene tethering by nucleoporins affects gene expression in plants. Nucleus 2015, 6:471-478.
35. Weiner A., et al. 3D nuclear architecture reveals coupled cell cycle dynamics of chromatin and nuclear pores in the malaria parasite Plasmodium falciparum. Cell Microbiol. 2011, 13:967-977.
36. Ralph S.A., et al. Antigenic variation in Plasmodium falciparum is associated with movement of var loci between subnuclear locations. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:5414-5419.
37. Dzikowski R., et al. Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites. EMBO Rep. 2007, 8:959-965.
38. Colon-Ramos D.A., et al. Asymmetric distribution of nuclear pore complexes and the cytoplasmic localization of beta2-tubulin mRNA in Chlamydomonas reinhardtii. Dev. Cell 2003, 4:941-952.
39. Ho H.C. Redistribution of nuclear pores during formation of the redundant nuclear envelope in mouse spermatids. J. Anat. 2010, 216:525-532.
40. Zachar Z., et al. Evidence for channeled diffusion of pre-mRNAs during nuclear RNA transport in metazoans. J. Cell Biol. 1993, 121:729-742.
41. Singh O.P., et al. The intranuclear movement of Balbiani ring premessenger ribonucleoprotein particles. Exp. Cell Res. 1999, 251:135-146.
42. Popken J., et al. Reprogramming of fibroblast nuclei in cloned bovine embryos involves major structural remodeling with both striking similarities and differences to nuclear phenotypes of in vitro fertilized embryos. Nucleus 2014, 5:555-589.
43. Ben-Ari Y., et al. The life of an mRNA in space and time. J. Cell Sci. 2010, 123:1761-1774.
44. Halstead J.M., et al. Translation. An RNA biosensor for imaging the first round of translation from single cells to living animals. Science 2015, 347:1367-1671.
45. Pederson T. The nuclear physique. Int. Rev. Cell Mol. Biol. 2014, 307:1-13.
46. Ma J., et al. High-resolution three-dimensional mapping of mRNA export through the nuclear pore. Nat. Commun. 2013, 4:2414.
47. Querido E., et al. Stochastic and reversible aggregation of mRNA with expanded CUG-triplet repeats. J. Cell. Sci. 2011, 124:1703-1714.
48. Thompson M.A., et al. Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17864-17871.
49. Veith R., et al. Balbiani ring mRNPs diffuse through and bind to clusters of large intranuclear molecular structures. Biophys J. 2010, 99:2676-2685.
50. Spille J.H., et al. Direct observation of mobility state transitions in RNA trajectories by sensitive single molecule feedback tracking. Nucleic Acids Res. 2015, 43:e14.
51. Kalo A., et al. Cellular levels of signaling factors are sensed by beta-actin alleles to modulate transcriptional pulse intensity. Cell Rep. 2015, 11:419-432.
52. Smith C., et al. In vivo single-particle imaging of nuclear mRNA export in budding yeast demonstrates an essential role for Mex67p. J. Cell Biol. 2015, 211:1121-1130.
53. Musser S.M., Grunwald D. Deciphering the structure and function of nuclear pores using single-molecule fluorescence approaches. J. Mol. Biol. 2016, Published online March 2, 2016. http://dx.doi.org/10.1016/j.jmb.2016.02.023.
54. Rajanala K., Nandicoori V.K. Localization of nucleoporin Tpr to the nuclear pore complex is essential for Tpr mediated regulation of the export of unspliced RNA. PLoS ONE 2012, 7:e29921.
55. Galy V., et al. Nuclear retention of unspliced mRNAs in yeast is mediated by perinuclear Mlp1. Cell 2004, 116:63-73.
56. Kohler A., Hurt E. Gene regulation by nucleoporins and links to cancer. Mol. Cell 2010, 38:6-15.
57. Knockenhauer K.E., Schwartz T.U. The nuclear pore complex as a flexible and dynamic gate. Cell 2016, 164:1162-1171.
58. Kosinski J., et al. Molecular architecture of the inner ring scaffold of the human nuclear pore complex. Science 2016, 352:363-365.
59. Lin D.H., et al. Architecture of the symmetric core of the nuclear pore. Science 2016, 352:aaf1015.
60. Dworetzky S.I., Feldherr C.M. Translocation of RNA-coated gold particles through the nuclear pores of oocytes. J. Cell Biol. 1988, 106:575-584.
61. Iborra F.J., et al. The path of RNA through nuclear pores: apparent entry from the sides into specialized pores. J. Cell Sci. 2000, 113 Pt2:291-302.
62. Huang S., et al. In vivo analysis of the stability and transport of nuclear poly(A)+ RNA. J. Cell Biol. 1994, 126:877-899.
63. Adams R.L., Wente S.R. Uncovering nuclear pore complexity with innovation. Cell 2013, 152:1218-1221.
64. Hodge C.A., et al. The Dbp5 cycle at the nuclear pore complex during mRNA export I: dbp5 mutants with defects in RNA binding and ATP hydrolysis define key steps for Nup159 and Gle1. Genes Dev. 2011, 25:1052-1064.
65. Kylberg K., et al. Exclusion of mRNPs and ribosomal particles from a thin zone beneath the nuclear envelope revealed upon inhibition of transport. Exp. Cell Res. 2010, 316:1028-1038.
66. Noble K.N., et al. The Dbp5 cycle at the nuclear pore complex during mRNA export II: nucleotide cycling and mRNP remodeling by Dbp5 are controlled by Nup159 and Gle1. Genes Dev. 2011, 25:1065-1077.
67. Folkmann A.W., et al. Dbp5, Gle1-IP6 and Nup159: a working model for mRNP export. Nucleus 2011, 2:540-548.
68. Natalizio B.J., Wente S.R. Postage for the messenger: designating routes for nuclear mRNA export. Trends Cell Biol. 2013, 23:365-373.
69. Le Hir H., et al. The exon junction complex as a node of post-transcriptional networks. Nat. Rev. Mol. Cell. Biol. 2016, 17:41-54.
70. Luo M.J., Reed R. Splicing is required for rapid and efficient mRNA export in metazoans. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:14937-14942.
71. Valencia P., et al. Splicing promotes rapid and efficient mRNA export in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:3386-3391.
72. Lei H., et al. Export and stability of naturally intronless mRNAs require specific coding region sequences and the TREX mRNA export complex. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:17985-17990.
73. Lei H., et al. Evidence that a consensus element found in naturally intronless mRNAs promotes mRNA export. Nucleic Acids Res. 2013, 41:2517-2525.
74. Bonnet A., et al. Nuclear pore components affect distinct stages of intron-containing gene expression. Nucleic Acids Res. 2015, 43:4249-4261.
75. Braunschweig U., et al. Widespread intron retention in mammals functionally tunes transcriptomes. Genome Res. 2014, 24:1774-1786.
76. Bosse J.B., et al. Remodeling nuclear architecture allows efficient transport of herpesvirus capsids by diffusion. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:E5725-E5733.
77. Hagen C., et al. Structural basis of vesicle formation at the inner nuclear membrane. Cell 2015, 163:1692-1701.
78. Speese S.D., et al. Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 2012, 149:832-846.
79. Jokhi V., et al. Torsin mediates primary envelopment of large ribonucleoprotein granules at the nuclear envelope. Cell Rep. 2013, 3:988-995.
80. Kurosaki T., Maquat L.E. Nonsense-mediated mRNA decay in humans at a glance. J. Cell Sci. 2016, 129:461-467.
81. Trcek T., et al. Temporal and spatial characterization of nonsense-mediated mRNA decay. Genes Dev. 2013, 27:541-551.
82. Aizer A., et al. The dynamics of mammalian P body transport, assembly, and disassembly in vivo. Mol. Biol. Cell. 2008, 19:4154-4166.
83. Aizer A., Shav-Tal Y. Intracellular trafficking and dynamics of P bodies. Prion 2008, 2:131-134.
84. Spector D.L., Lamond A.I. Nuclear speckles. Cold Spring Harb. Perspect Biol. 2011, 3:a000646.
85. Guttman M., et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009, 458:223-227.
86. Bhatt D.M., et al. Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions. Cell 2012, 150:279-290.
87. Shalgi R., et al. Widespread inhibition of posttranscriptional splicing shapes the cellular transcriptome following heat shock. Cell Rep. 2014, 7:1362-1370.
88. Prasanth K.V., et al. Regulating gene expression through RNA nuclear retention. Cell 2005, 123:249-263.
89. Chen L.L., Carmichael G.G. Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: functional role of a nuclear noncoding RNA. Mol. Cell 2009, 35:467-478.
90. Mao Y.S., et al. Direct visualization of the co-transcriptional assembly of a nuclear body by noncoding RNAs. Nat. Cell Biol. 2011, 13:95-101.
91. Shevtsov S.P., Dundr M. Nucleation of nuclear bodies by RNA. Nat. Cell Biol. 2011, 13:167-173.
92. Mao Y.S., et al. Biogenesis and function of nuclear bodies. Trends Genet. 2011, 27:295-306.
93. Hutchinson J.N., et al. A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains. BMC Genomics 2007, 8:39.
94. Tripathi V., et al. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol. Cell 2010, 39:925-938.
95. Wilusz J.E., et al. 3' end processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell 2008, 135:919-932.
96. Sunwoo H., et al. MEN epsilon/beta nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles. Genome Res. 2009, 19:347-359.
97. Clemson C.M., et al. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol. Cell 2009, 33:717-726.
98. Sasaki Y.T., et al. MENepsilon/beta noncoding RNAs are essential for structural integrity of nuclear paraspeckles. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2525-2530.
99. Borah S., et al. Tracking expression and subcellular localization of RNA and protein species using high-throughput single cell imaging flow cytometry. RNA 2012, 18:1573-1579.
100. Borah S., et al. A viral nuclear noncoding RNA binds re-localized poly(A) binding protein and is required for late KSHV gene expression. PLoS Pathog. 2011, 7:e1002300.
101. Bahar Halpern K., et al. Nuclear retention of mRNA in mammalian tissues. Cell Rep. 2015, 13:2653-2662.
102. Bahar Halpern K., et al. Bursty gene expression in the intact mammalian liver. Mol. Cell 2015, 58:147-156.
103. Battich N., et al. Control of transcript variability in single mammalian cells. Cell 2015, 163:1596-1610.
104. Larson D.R., et al. Real-time observation of transcription initiation and elongation on an endogenous yeast gene. Science 2011, 332:475-478.
105. Senecal A., et al. Transcription factors modulate c-Fos transcriptional bursts. Cell Rep. 2014, 8:75-83.
106. Yunger S., et al. Single-allele analysis of transcription kinetics in living mammalian cells. Nat. Methods 2010, 7:631-633.
107. Janes K.A. Cell-to-cell transcript variability: seeing signal in the noise. Cell 2015, 163:1566-1568.
108. Hocine S., et al. Single-molecule analysis of gene expression using two-color RNA labeling in live yeast. Nat. Methods 2013, 10:119-121.
109. Muller-McNicoll M., et al. SR proteins are NXF1 adaptors that link alternative RNA processing to mRNA export. Genes Dev. 2016, 30:553-566.
110. Zhang B., et al. A novel RNA motif mediates the strict nuclear localization of a long noncoding RNA. Mol. Cell Biol. 2014, 34:2318-2329.
111. Skoglund U., et al. Visualization of the formation and transport of a specific hnRNP particle. Cell 1983, 34:847-855.
112. Levsky J.M., Singer R.H. Fluorescence in situ hybridization: past, present and future. J. Cell Sci. 2003, 116:2833-2838.
113. Bertrand E., et al. Localization of ASH1 mRNA particles in living yeast. Mol. Cell 1998, 2:437-445.
114. Lionnet T., et al. A transgenic mouse for in vivo detection of endogenous labeled mRNA. Nat. Methods 2011, 8:165-170.
115. Chubb J.R., et al. Transcriptional pulsing of a developmental gene. Curr. Biol. 2006, 16:1018-1025.
116. Coulon A., et al. Kinetic competition during the transcription cycle results in stochastic RNA processing. eLife 2014, 3:03939.
117. Martin R.M., et al. Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity. Cell Rep. 2013, 4:1144-1155.
118. Papantonis A., Cook P.R. Transcription factories: genome organization and gene regulation. Chem. Rev. 2013, 113:8683-8705.
119. Ahmed S., et al. DNA zip codes control an ancient mechanism for gene targeting to the nuclear periphery. Nat. Cell Biol. 2010, 12:111-118.
120. Brickner D.G., et al. transcriptional memory leads to DNA zip code-dependent interchromosomal clustering. Microb. Cell 2015, 2:481-490.
121. Brickner D.G., et al. Transcription factor binding to a DNA zip code controls interchromosomal clustering at the nuclear periphery. Dev. Cell 2012, 22:1234-1246.
122. Robinett C.C., et al. In vivo localization of DNA sequences and visualization of large-scale chromatin organization using lac operator/repressor recognition. J. Cell Biol. 1996, 135:1685-1700.
123. Heun P., et al. Chromosome dynamics in the yeast interphase nucleus. Science 2001, 294:2181-2186.
124. Chubb J.R., et al. Chromatin motion is constrained by association with nuclear compartments in human cells. Curr. Biol. 2002, 12:439-445.
125. Tsukamoto T., et al. Visualization of gene activity in living cells. Nat. Cell Biol. 2000, 2:871-878.
126. Janicki S.M., et al. From silencing to gene expression; real-time analysis in single cells. Cell 2004, 116:683-698.
127. Newhart A., et al. Single-cell analysis of Daxx and ATRX-dependent transcriptional repression. J. Cell Sci. 2012, 125:5489-5501.
128. Newhart A., et al. Single cell analysis of RNA-mediated histone H3.3 recruitment to a cytomegalovirus promoter-regulated transcription site. J. Biol Chem. 2013, 288:19882-19899.
129. Tripathi V., et al. SRSF1 regulates the assembly of pre-mRNA processing factors in nuclear speckles. Mol. Biol. Cell 2012, 23:3694-3706.
130. Kaiser T.E., et al. De novo formation of a subnuclear body. Science 2008, 322:1713-1717.
131. Schwartz M., et al. Analysis of the initiation of nuclear pore assembly by ectopically targeting nucleoporins to chromatin. Nucleus 2015, 6:40-54.
132. Reddy K.L., et al. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 2008, 452:243-247.
133. Finlan L.E., et al. Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet. 2008, 4:e1000039.
134. Kumaran R.I., Spector D.L. A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J. Cell Biol. 2008, 180:51-65.
135. Freibaum B.D., et al. GGGGCC repeat expansion in C9orf72 compromises nucleocytoplasmic transport. Nature 2015, 525:129-133.
136. Zhang K., et al. The C9orf72 repeat expansion disrupts nucleocytoplasmic transport. Nature 2015, 525:56-61.
137. Woerner A.C., et al. Cytoplasmic protein aggregates interfere with nucleocytoplasmic transport of protein and RNA. Science 2016, 351:173-176.
138. Lund M.K., Guthrie C. The DEAD-box protein Dbp5p is required to dissociate Mex67p from exported mRNPs at the nuclear rim. Mol. Cell 2005, 20:645-651.
139. Weirich C.S., et al. Activation of the DExD/H-box protein Dbp5 by the nuclear-pore protein Gle1 and its coactivator InsP6 is required for mRNA export. Nat. Cell Biol. 2006, 8:668-676.