Emerging properties of nuclear RNP biogenesis and export

Current Opinion in Cell Biology

Volumn 34, Issue , 2015, Pages 46-53

  Oeffinger, Marlene ^a,b,c   Montpetit, Ben ^d  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEOPROTEIN; RNA; RNA BINDING PROTEIN;

BIOGENESIS; CELL FUNCTION; DNA MODIFICATION; GENE EXPRESSION; HUMAN; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN ANALYSIS; QUALITY CONTROL; REVIEW; TRANSPORT KINETICS; ANIMAL; GENETICS; METABOLISM; PROTEIN TRANSPORT;

ANIMALS; HUMANS; PROTEIN TRANSPORT; RIBONUCLEOPROTEINS; RNA; RNA-BINDING PROTEINS;

EID: 84928789961     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2015.04.007     Document Type: Review

References (86)

1. Woolford J.L., Baserga S.J. Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 2013, 195:643-681.
2. Niño C.A., Hérissant L., Babour A. Dargemont C: mRNA nuclear export in yeast. Chem Rev 2013, 113:8523-8545.
3. Fernández-Pevida A., Kressler D., de la Cruz J. Processing of preribosomal RNA in Saccharomyces cerevisiae. Wiley Interdiscip Rev RNA 2014, 10.1002/wrna.1267.
4. Müller-McNicoll M., Neugebauer K.M. How cells get the message: dynamic assembly and function of mRNA-protein complexes. Nat Rev Genet 2013, 14:275-287.
5. Rodríguez-Navarro S., Hurt E. Linking gene regulation to mRNA production and export. Curr Opin Cell Biol 2011, 23:302-309.
6. Mitchell S.F., Parker R. Principles and properties of eukaryotic mRNPs. Mol Cell 2014, 54:547-558.
7. Gamalinda M., Ohmayer U., Jakovljevic J., Kumcuoglu B., Woolford J., Mbom B., Lin L., Woolford J.L. A hierarchical model for assembly of eukaryotic 60S ribosomal subunit domains. Genes Dev 2014, 28:198-210.
8. Merz C., Urlaub H., Will C.L., Lührmann R. Protein composition of human mRNPs spliced in vitro and differential requirements for mRNP protein recruitment. RNA 2007, 13:116-128.
9. Oeffinger M., Wei K.E., Rogers R., Degrasse J.A., Chait B.T., Aitchison J.D., Rout M.P. Comprehensive analysis of diverse ribonucleoprotein complexes. Nat Methods 2007, 4:951-956.
10. Slobodin B., Gerst J.E. A novel mRNA affinity purification technique for the identification of interacting proteins and transcripts in ribonucleoprotein complexes. RNA 2010, 16:2277-2290.
11. Mitchell S.F., Jain S., She M., Parker R. Global analysis of yeast mRNPs. Nat Struct Mol Biol 2013, 20:127-133.
12. Castello A., Fischer B., Eichelbaum K., Horos R., Beckmann B.M., Strein C., Davey N.E., Humphreys D.T., Preiss T., Steinmetz L.M., et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 2012, 149:1393-1406.
13. Baltz A.G., Munschauer M., Schwanhäusser B., Vasile A., Murakawa Y., Schueler M., Youngs N., Penfold-Brown D., Drew K., Milek M., et al. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell 2012, 46:674-690.
14. Baejen C., Torkler P., Gressel S., Essig K., Söding J., Cramer P. Transcriptome maps of mRNP biogenesis factors define pre-mRNA recognition. Mol Cell 2014, 55:745-757.
15. Tuck A.C., Tollervey D. A transcriptome-wide atlas of RNP composition reveals diverse classes of mRNAs and lncRNAs. Cell 2013, 154:996-1009.
16. Granneman S., Petfalski E., Swiatkowska A., Tollervey D. Cracking pre-40S ribosomal subunit structure by systematic analyses of RNA-protein cross-linking. EMBO J 2010, 29:2026-2036.
17. Kudla G., Granneman S., Hahn D., Beggs J.D., Tollervey D. Cross-linking, ligation, and sequencing of hybrids reveals RNA-RNA interactions in yeast. Proc Natl Acad Sci U S A 2011, 108:10010-10015.
18. Trcek T., Larson D.R., Moldón A., Query C.C., Singer R.H. Single-molecule mRNA decay measurements reveal promoter-regulated mRNA stability in yeast. Cell 2011, 147:1484-1497.
19. Haimovich G., Choder M., Singer R.H., Trcek T. The fate of the messenger is pre-determined: a new model for regulation of gene expression. Biochim Biophys Acta 2013, 1829:643-653.
20. Trcek T., Sato H., Singer R.H., Maquat L.E. Temporal and spatial characterization of nonsense-mediated mRNA decay. Genes Dev 2013, 27:541-551.
21. Enssle J., Kugler W., Hentze M.W., Kulozik A.E. Determination of mRNA fate by different RNA polymerase II promoters. Proc Natl Acad Sci U S A 1993, 90:10091-10095.
22. Zid B.M., O'Shea E.K. Promoter sequences direct cytoplasmic localization and translation of mRNAs during starvation in yeast. Nature 2014, 514:117-121.
23. Hoyle N.P., Ish-Horowicz D. Transcript processing and export kinetics are rate-limiting steps in expressing vertebrate segmentation clock genes. Proc Natl Acad Sci U S A 2013, 110:E4316-E4324.
24. Wang L., Miao Y.-L., Zheng X., Lackford B., Zhou B., Han L., Yao C., Ward J.M., Burkholder A., Lipchina I., et al. The THO complex regulates pluripotency gene mRNA export and controls embryonic stem cell self-renewal and somatic cell reprogramming. Cell Stem Cell 2013, 13:676-690.
25. MacGregor D.R., Gould P., Foreman J., Griffiths J., Bird S., Page R., Stewart K., Steel G., Young J., Paszkiewicz K., et al. High expression of osmotically responsive genes is required for circadian periodicity through the promotion of nucleo-cytoplasmic mRNA export in Arabidopsis. Plant Cell 2013, 25:4391-4404.
26. Iglesias N., Tutucci E., Gwizdek C., Vinciguerra P., Von Dach E., Corbett A.H., Dargemont C., Stutz F. Ubiquitin-mediated mRNP dynamics and surveillance prior to budding yeast mRNA export. Genes Dev 2010, 24:1927-1938.
27. Gilbert W., Guthrie C. The Glc7p nuclear phosphatase promotes mRNA export by facilitating association of Mex67p with mRNA. Mol Cell 2004, 13:201-212.
28. Ma W.K., Cloutier S.C., Tran E.J. The DEAD-box protein Dbp2 functions with the RNA-binding protein Yra1 to promote mRNP assembly. J Mol Biol 2013, 425:3824-3838.
29. Stutz F., Bachi A., Doerks T., Braun I.C., Seraphin B., Wilm M., Bork P., Izaurralde E. REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA 2000, 6:638-650.
30. Strässer K., Hurt E. Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J 2000, 19:410-420.
31. Natalizio B.J., Wente S.R. Postage for the messenger: designating routes for nuclear mRNA export. Trends Cell Biol 2013, 23:365-373.
32. Wickramasinghe V.O., Savill J.M., Chavali S., Jonsdottir A.B., Rajendra E., Grüner T., Laskey R.A., Babu M.M., Venkitaraman A.R. Human inositol polyphosphate multikinase regulates transcript-selective nuclear mRNA export to preserve genome integrity. Mol Cell 2013, 51:737-750.
33. Jangi M., Sharp P.A. Building robust transcriptomes with master splicing factors. Cell 2014, 159:487-498.
34. Fu X.-D., Ares M. Context-dependent control of alternative splicing by RNA-binding proteins. Nat Rev Genet 2014, 15:689-701.
35. Singh G., Kucukural A., Cenik C., Leszyk J.D., Shaffer S.A., Weng Z., Moore M.J. The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell 2012, 151:750-764.
36. Schweingruber C., Rufener S.C., Zünd D., Yamashita A., Mühlemann O. Nonsense-mediated mRNA decay - mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim Biophys Acta 2013, 1829:612-623.
37. Hughes C., Krijgsveld J. Developments in quantitative mass spectrometry for the analysis of proteome dynamics. Trends Biotechnol 2012, 30:668-676.
38. Picotti P., Bodenmiller B., Aebersold R. Proteomics meets the scientific method. Nat Methods 2013, 10:24-27.
39. Machnicka M.A., Milanowska K., Osman Oglou O., Purta E., Kurkowska M., Olchowik A., Januszewski W., Kalinowski S., Dunin-Horkawicz S., Rother K.M., et al. MODOMICS: a database of RNA modification pathways - 2013 update. Nucleic Acids Res 2013, 41:D262-D267.
40. Jackman J.E., Alfonzo J.D. Transfer RNA modifications: nature's combinatorial chemistry playground. Wiley Interdiscip Rev RNA 2013, 4:35-48.
41. Meyer K.D., Saletore Y., Zumbo P., Elemento O., Mason C.E., Jaffrey S.R. Comprehensive analysis of mRNA methylation reveals enrichment in 3' UTRs and near stop codons. Cell 2012, 149:1635-1646.
42. Dominissini D., Moshitch-Moshkovitz S., Schwartz S., Salmon-Divon M., Ungar L., Osenberg S., Cesarkas K., Jacob-Hirsch J., Amariglio N., Kupiec M., et al. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 2012, 485:201-206.
43. Carlile T.M., Rojas-Duran M.F., Zinshteyn B., Shin H., Bartoli K.M., Gilbert W.V. Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature 2014, 515:143-146.
44. Schwartz S., Bernstein D.A., Mumbach M.R., Jovanovic M., Herbst R.H., León-Ricardo B.X., Engreitz J.M., Guttman M., Satija R., Lander E.S., et al. Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA. Cell 2014, 159:148-162.
45. Lovejoy A.F., Riordan D.P., Brown P.O. Transcriptome-wide mapping of pseudouridines: pseudouridine synthases modify specific mRNAs in S. cerevisiae. PLOS ONE 2014, 9:e110799.
46. Schwartz S., Agarwala S.D., Mumbach M.R., Jovanovic M., Mertins P., Shishkin A., Tabach Y., Mikkelsen T.S., Satija R., Ruvkun G., et al. High-resolution mapping reveals a conserved, widespread, dynamic mRNA methylation program in yeast meiosis. Cell 2013, 155:1409-1421.
47. Liu N., Dai Q., Zheng G., He C., Parisien M., Pan T. N6-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions. Nature 2015, 518:560-564.
48. Wang X., Lu Z., Gomez A., Hon G.C., Yue Y., Han D., Fu Y., Parisien M., Dai Q., Jia G., et al. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature 2014, 505:117-120.
49. Fernández I.S., Ng C.L., Kelley A.C., Wu G., Yu Y.-T., Ramakrishnan V. Unusual base pairing during the decoding of a stop codon by the ribosome. Nature 2013, 500:107-110.
50. Karijolich J., Yu Y.-T. Converting nonsense codons into sense codons by targeted pseudouridylation. Nature 2011, 474:395-398.
51. Hector R.D., Burlacu E., Aitken S., Le B.T., Tuijtel M., Zaplatina A., Cook A.G., Granneman S. Snapshots of pre-rRNA structural flexibility reveal eukaryotic 40S assembly dynamics at nucleotide resolution. Nucleic Acids Res 2014, 42:12138-12154.
52. Stelter P., Kunze R., Radwan M., Thomson E., Thierbach K., Thoms M., Hurt E. Monitoring spatiotemporal biogenesis of macromolecular assemblies by pulse-chase epitope labeling. Mol Cell 2012, 47:788-796.
53. Altvater M., Chang Y., Melnik A., Occhipinti L., Schütz S., Rothenbusch U., Picotti P., Panse V.G. Targeted proteomics reveals compositional dynamics of 60S pre-ribosomes after nuclear export. Mol Syst Biol 2012, 8.
54. Ohmayer U., Gamalinda M., Sauert M., Ossowski J., Pöll G., Linnemann J., Hierlmeier T., Perez-Fernandez J., Kumcuoglu B., Leger-Silvestre I., et al. Studies on the assembly characteristics of large subunit ribosomal proteins in S. cerevisae. PLOS ONE 2013, 8:e68412.
55. Bradatsch B., Leidig C., Granneman S., Gnädig M., Tollervey D., Böttcher B., Beckmann R., Hurt E. Structure of the pre-60S ribosomal subunit with nuclear export factor Arx1 bound at the exit tunnel. Nat Struct Mol Biol 2012, 19:1234-1241.
56. Baßler J., Paternoga H., Holdermann I., Thoms M., Granneman S., Barrio-Garcia C., Nyarko A., Stier G., Clark S.A., Schraivogel D., et al. A network of assembly factors is involved in remodeling rRNA elements during preribosome maturation. J Cell Biol 2014, 10.1083/jcb.201408111.
57. Matsuo Y., Granneman S., Thoms M., Manikas R.-G., Tollervey D., Hurt E. Coupled GTPase and remodelling ATPase activities form a checkpoint for ribosome export. Nature 2014, 505:112-116.
58. Gamalinda M., Jakovljevic J., Babiano R., Talkish J., de la Cruz J., Woolford J.L. Yeast polypeptide exit tunnel ribosomal proteins L17, L35 and L37 are necessary to recruit late-assembling factors required for 27SB pre-rRNA processing. Nucleic Acids Res 2013, 41:1965-1983.
59. Batisse J., Batisse C., Budd A., Böttcher B., Hurt E. Purification of nuclear poly(A)-binding protein Nab2 reveals association with the yeast transcriptome and a messenger ribonucleoprotein core structure. J Biol Chem 2009, 284:34911-34917.
60. Wan Y., Qu K., Zhang Q.C., Flynn R.A., Manor O., Ouyang Z., Zhang J., Spitale R.C., Snyder M.P., Segal E., et al. Landscape and variation of RNA secondary structure across the human transcriptome. Nature 2014, 505:706-709.
61. Rouskin S., Zubradt M., Washietl S., Kellis M., Weissman J.S. Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature 2014, 505:701-705.
62. Siegfried N.A., Busan S., Rice G.M., Nelson J.A.E., Weeks K.M. RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP). Nat Methods 2014, 11:959-965.
63. Schmid M., Jensen T.H. Transcription-associated quality control of mRNP. Biochim Biophys Acta 2012, 10.1016/j.bbagrm.2012.08.012.
64. Bonnet A., Palancade B. Regulation of mRNA trafficking by nuclear pore complexes. Genes (Basel) 2014, 5:767-791.
65. Porrua O., Libri D. RNA quality control in the nucleus: the Angels' share of RNA. Biochim Biophys Acta 2013, 1829:604-611.
66. Schneider C., Tollervey D. Threading the barrel of the RNA exosome. Trends Biochem Sci 2013, 38:485-493.
67. Gudipati R.K., Xu Z., Lebreton A., Séraphin B., Steinmetz L.M., Jacquier A., Libri D. Extensive degradation of RNA precursors by the exosome in wild-type cells. Mol Cell 2012, 48:409-421.
68. Schneider C., Kudla G., Wlotzka W., Tuck A., Tollervey D. Transcriptome-wide analysis of exosome targets. Mol Cell 2012, 48:422-433.
69. Ma J., Liu Z., Michelotti N., Pitchiaya S., Veerapaneni R., Androsavich J.R., Walter N.G., Yang W. High-resolution three-dimensional mapping of mRNA export through the nuclear pore. Nat Commun 2013, 4:2414.
70. Mor A., Suliman S., Ben-Yishay R., Yunger S., Brody Y., Shav-Tal Y. Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Nat Cell Biol 2010, 12:543-552.
71. Larson D.R., Zenklusen D., Wu B., Chao J.A., Singer R.H. Real-time observation of transcription initiation and elongation on an endogenous yeast gene. Science 2011, 332:475-478.
72. Hocine S., Raymond P., Zenklusen D., Chao J.A., Singer R.H. Single-molecule analysis of gene expression using two-color RNA labeling in live yeast. Nat Methods 2013, 10:119-121.
73. Siebrasse J.P., Kaminski T., Kubitscheck U. Nuclear export of single native mRNA molecules observed by light sheet fluorescence microscopy. Proc Natl Acad Sci U S A 2012, 109:9426-9431.
74. Grünwald D., Singer R.H. In vivo imaging of labelled endogenous β-actin mRNA during nucleocytoplasmic transport. Nature 2010, 467:604-607.
75. Fiserova J., Richards S.A., Wente S.R., Goldberg M.W. Facilitated transport and diffusion take distinct spatial routes through the nuclear pore complex. J Cell Sci 2010, 123:2773-2780.
76. Park H.Y., Lim H., Yoon Y.J., Follenzi A., Nwokafor C., Lopez-Jones M., Meng X., Singer R.H. Visualization of dynamics of single endogenous mRNA labeled in live mouse. Science 2014, 343:422-424.
77. Buxbaum A.R., Wu B., Singer R.H. Single β-actin mRNA detection in neurons reveals a mechanism for regulating its translatability. Science 2014, 343:419-422.
78. Kitano H. Systems biology: a brief overview. Science 2002, 295:1662-1664.
79. Ideker T., Galitski T., Hood L. A new approach to decoding life: systems biology. Annu Rev Genomics Hum Genet 2001, 2:343-372.
80. Ozsolak F., Milos P.M. RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 2011, 12:87-98.
81. Van Dijk E.L., Auger H., Jaszczyszyn Y., Thermes C. Ten years of next-generation sequencing technology. Trends Genet 2014, 30:418-426.
82. König J., Zarnack K., Luscombe N.M., Ule J. Protein-RNA interactions: new genomic technologies and perspectives. Nat Rev Genet 2011, 13:77-83.
83. Faoro C., Ataide S.F. Ribonomic approaches to study the RNA-binding proteome. FEBS Lett 2014, 588:3649-3664.
84. Rath A.K., Rentmeister A. Genetically encoded tools for RNA imaging in living cells. Curr Opin Biotechnol 2014, 31C:42-49.
85. Mortimer S.A., Kidwell M.A., Doudna J.A. Insights into RNA structure and function from genome-wide studies. Nat Rev Genet 2014, 15:469-479.
86. Pérez-Ortín J.E., Alepuz P., Chávez S., Choder M. Eukaryotic mRNA decay: methodologies, pathways, and links to other stages of gene expression. J Mol Biol 2013, 425:3750-3775.