Journey from the Center of the Cell - the intra- and intercellular transport of mRNA

• Authors: Anna Kasprowicz-Maluśki , Wojciech Kwiatkowski , Alicja Starosta , Przemysław Wojtaszek
• Languages of publication: EN

Abstracts

EN

Transport and localized translation of mRNA is crucial for the proper spatiotemporal organization of proteins within cells. Distribution of RNAs to subcellular domains has recently emerged as a major mechanism for establishing functionally distinct compartments and structures in the cells. There is an emerging evidence that active transport of mRNA involves cytoskeleton and membrane trafficking pathways in fungi, plants and animals, suggesting that it is a common phenomenon among eukaryotes. The important highlights are that the RNA-binding proteins recognize the cargo mRNA and that RNPs are actively transported on the cytoskeletal tracks or co-transported with membranous compartments, such as the endoplasmic reticulum and endosomes. The interest of scientists has expanded over the past years in response to the discoveries that RNA can be exported from cells to play a role in the intercellular communication. In this review, we will focus on characterization of the RNA transport both, within a cell and between cells, and on the currently proposed mechanisms for RNA targeting.

Keywords

EN

RNP; extracellular RNA; localized RNA; cytoskeleton; extracellular vesicle (EV); multivesicular body (MVB)

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2016
• Volume: 63
• Issue: 4
• Pages: 693-699

Dates

published

2016

received

2016-06-06

revised

2016-07-13

accepted

2016-07-19

(unknown)

2016-12-06

Contributors

author

Anna Kasprowicz-Maluśki

• Department of Molecular and Cellular Biology, Adam Mickiewicz University, Poznań, Poland

author

Wojciech Kwiatkowski

• Department of Molecular and Cellular Biology, Adam Mickiewicz University, Poznań, Poland

author

Alicja Starosta

• Department of Molecular and Cellular Biology, Adam Mickiewicz University, Poznań, Poland

author

Przemysław Wojtaszek

• Department of Molecular and Cellular Biology, Adam Mickiewicz University, Poznań, Poland

References

• Aliotta JM, Pereira M, Johnson KW, de Paz N, Dooner MS, Puente N, Ayala C, Brilliant K, Berz D, Lee D, Ramratnam B, McMillan PN, Hixson DC, Josic D, Quesenberry PJ (2010) Microvesicle entry into marrow cells mediates tissue-specific changes in mRNA by direct delivery of mRNA and induction of transcription. Exp Hematol 38: 233-245. https://doi.org/10.1016/j.exphem.2010.01.002.
• Anderson P, Kedersha N (2006) RNA granules. J Cell Biol 172: 803-808. https://doi.org/10.1083/jcb.200512082.
• Baj G, Leone E, Chao M V, Tongiorgi E (2011) Spatial segregation of BDNF transcripts enables BDNF to differentially shape distinct dendritic compartments. Proc Natl Acad Sci U S A 108: 16813-16818. https://doi.org/10.1073/pnas.1014168108.
• Batagov AO, Kuznetsov VA, Kurochkin I V (2011) Identification of nucleotide patterns enriched in secreted RNAs as putative cis-acting elements targeting them to exosome nano-vesicles. BMC Genomics 12 (Suppl 3): S18. https://doi.org/10.1186/1471-2164-12-S3-S18.
• Batisse J, Batisse C, Budd A, Böttcher B, Hurt E (2009) Purification of nuclear poly(A)-binding protein Nab2 reveals association with the yeast transcriptome and a messenger ribonucleoprotein core structure. J Biol Chem 284: 34911-34917. https://doi.org/10.1074/jbc.M109.062034.
• Baumann S, Pohlmann T, Jungbluth M, Brachmann A, Feldbrügge M (2012) Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes. J Cell Sci 125: 2740-2752. https://doi.org/10.1242/jcs.101212.
• Bellingham SA, Coleman BM, Hill AF (2012) Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res 40: 10937-10949. https://doi.org/10.1093/nar/gks832.
• Besse F, Ephrussi A (2008) Translational control of localized mRNAs: restricting protein synthesis in space and time. Nat Rev Mol Cell Biol 9: 971-980. https://doi.org/10.1038/nrm2548.
• Bianco P, Cao X, Frenette PS, Mao JJ, Robey PG, Simmons PJ, Wang CY (2013) The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat Med 19: 35-42. https://doi.org/10.1038/nm.3028.
• Böhl F, Kruse C, Frank A, Ferring D, Jansen RP (2000) She2p, a novel RNA-binding protein tethers ASH1 mRNA to the Myo4p myosin motor via She3p. EMBO J 19: 5514-5524. https://doi.org/10.1093/emboj/19.20.5514.
• Brennan CM, Gallouzi IE, Steitz JA (2000) Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J Cell Biol 151: 1-13. https://doi.org/10.1083/jcb.151.1.1.
• Bullock SL, Nicol A, Gross SP, Zicha D (2006a) Guidance of bidirectional motor complexes by mRNA cargoes through control of dynein number and activity. Curr Biol 16: 1447-1452. https://doi.org/10.1016/j.cub.2006.05.055.
• Bullock SL, Nicol A, Gross SP, Zicha D (2006b) Guidance of bidirectional motor complexes by mRNA cargoes through control of dynein number and activity. Curr Biol 16: 1447-1452. https://doi.org/10.1016/j.cub.2006.05.055.
• Carlile TM, Rojas-Duran MF, Zinshteyn B, Shin H, Bartoli KM, Gilbert W V (2014) Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature 515: 143-146. https://doi.org/10.1038/nature13802.
• Carmody SR, Wente SR (2009) mRNA nuclear export at a glance. J Cell Sci 122: 1933-1937. https://doi.org/10.1242/jcs.041236.
• Castello A, Fischer B, Eichelbaum K, Horos R, Beckmann BM, Strein C, Davey NE, Humphreys DT, Preiss T, Steinmetz LM, Krijgsveld J, Hentze MW (2012) Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149: 1393-1406. https://doi.org/10.1016/j.cell.2012.04.031.
• Castello A, Hentze MW, Preiss T (2015) Metabolic enzymes enjoying new partnerships as RNA-binding proteins. Trends Endocrinol Metab 26: 746-757. https://doi.org/10.1016/j.tem.2015.09.012.
• Chang P, Torres J, Lewis RA, Mowry KL, Houliston E, King ML (2004) Localization of RNAs to the mitochondrial cloud in Xenopus oocytes through entrapment and association with endoplasmic reticulum. Mol Biol Cell 15: 4669-4681. https://doi.org/10.1091/mbc.E04-03-0265.
• Cheng H, Dufu K, Lee CS, Hsu JL, Dias A, Reed R (2006) Human mRNA export machinery recruited to the 5' end of mRNA. Cell 127: 1389-400. https://doi.org/10.1016/j.cell.2006.10.044.
• Chung S, Takizawa PA (2010) Multiple Myo4 motors enhance ASH1 mRNA transport in Saccharomyces cerevisiae. J Cell Biol 189: 755-767. https://doi.org/10.1083/jcb.200912011.
• Cocucci E, Racchetti G, Meldolesi J (2009) Shedding microvesicles: artefacts no more. Trends Cell Biol 19: 43-51. https://doi.org/10.1016/j.tcb.2008.11.003.
• Cohen RS (2005) The role of membranes and membrane trafficking in RNA localization. Biol Cell 97: 5-18. https://doi.org/10.1042/BC20040056.
• Crofts AJ, Washida H, Okita TW, Satoh M, Ogawa M, Kumamaru T, Satoh H (2005) The role of mRNA and protein sorting in seed storage protein synthesis, transport, and deposition. Biochem Cell Biol 83: 728-737. https://doi.org/10.1139/o05-156.
• Daneholt B (2001) Packing and delivery of a genetic message. Chromosoma 110: 173-85.
• Delanoue R, Davis I (2005) Dynein anchors its mRNA cargo after apical transport in the Drosophila blastoderm embryo. Cell 122: 97-106. https://doi.org/10.1016/j.cell.2005.04.033.
• Dictenberg JB, Swanger SA, Antar LN, Singer RH, Bassell GJ (2008) A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome. Dev Cell 14: 926-939. https://doi.org/10.1016/j.devcel.2008.04.003.
• Ding D, Parkhurst SM, Halsell SR, Lipshitz HD (1993) Dynamic Hsp83 RNA localization during Drosophila oogenesis and embryogenesis. Mol Cell Biol 13: 3773-3781.
• Domínguez-Sánchez MS, Barroso S, Gómez-González B, Luna R, Aguilera A (2011) Genome instability and transcription elongation impairment in human cells depleted of THO/TREX. PLoS Genet 7: e1002386. https://doi.org/10.1371/journal.pgen.1002386.
• Doyle M, Kiebler MA (2011) Mechanisms of dendritic mRNA transport and its role in synaptic tagging. EMBO J 30: 3540-3552. https://doi.org/10.1038/emboj.2011.278.
• Forrest KM, Gavis ER (2003) Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila. Curr Biol 13: 1159-1168.
• Fritzsche R, Karra D, Bennett KL, Ang FY, Heraud-Farlow JE, Tolino M, Doyle M, Bauer KE, Thomas S, Planyavsky M, Arn E, Bakosova A, Jungwirth K, Hörmann A, Palfi Z, Sandholzer J, Schwarz M, Macchi P, Colinge J, Superti-Furga G, Kiebler MA (2013) Interactome of two diverse RNA granules links mRNA localization to translational repression in neurons. Cell Rep 5: 1749-1762. https://doi.org/10.1016/j.celrep.2013.11.023.
• Fundakowski J, Hermesh O, Jansen RP (2012) Localization of a subset of yeast mRNAs depends on inheritance of endoplasmic reticulum. Traffic 13: 1642-1652. https://doi.org/10.1111/tra.12011.
• Fusco D, Accornero N, Lavoie B, Shenoy SM, Blanchard JM, Singer RH, Bertrand E (2003) Single mRNA molecules demonstrate probabilistic movement in living mammalian cells. Curr Biol 13: 161-167.
• Gagnon JA, Mowry KL (2011) Molecular motors: directing traffic during RNA localization. Crit Rev Biochem Mol Biol 46: 229-239. https://doi.org/10.3109/10409238.2011.572861.
• Gangoda L, Boukouris S, Liem M, Kalra H, Mathivanan S (2015) Extracellular vesicles including exosomes are mediators of signal transduction: are they protective or pathogenic? Proteomics 15: 260-271. https://doi.org/10.1002/pmic.201400234.
• Gebhardt A, Habjan M, Benda C, Meiler A, Haas DA, Hein MY, Mann A, Mann M, Habermann B, Pichlmair A (2015) mRNA export through an additional cap-binding complex consisting of NCBP1 and NCBP3. Nat Commun 6: 8192. https://doi.org/10.1038/ncomms9192.
• Gehring NH, Lamprinaki S, Kulozik AE, Hentze MW (2009) Disassembly of exon junction complexes by PYM. Cell 137: 536-548. https://doi.org/10.1016/j.cell.2009.02.042.
• Genz C, Fundakowski J, Hermesh O, Schmid M, Jansen RP (2013) Association of the yeast RNA-binding protein She2p with the tubular endoplasmic reticulum depends on membrane curvature. J Biol Chem 288: 32384-32393. https://doi.org/10.1074/jbc.M113.486431.
• Ghoujal B, Milev MP, Ajamian L, Abel K, Mouland AJ (2012) ESCRT-II's involvement in HIV-1 genomic RNA trafficking and assembly. Biol Cell 104: 706-721. https://doi.org/10.1111/boc.201200021.
• Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O (2009) Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11: 1143-1149. https://doi.org/10.1038/ncb1929.
• Hentze MW, Preiss T (2010) The REM phase of gene regulation. Trends Biochem Sci 35: 423-426. https://doi.org/10.1016/j.tibs.2010.05.009.
• Hermesh O, Jansen RP (2013) Take the (RN)A-train: localization of mRNA to the endoplasmic reticulum. Biochim Biophys Acta 1833: 2519-2525. https://doi.org/10.1016/j.bbamcr.2013.01.013.
• Heym RG, Niessing D (2012) Principles of mRNA transport in yeast. Cell Mol Life Sci 69: 1843-1853. https://doi.org/10.1007/s00018-011-0902-4.
• Huang Y, Yario TA, Steitz JA (2004) A molecular link between SR protein dephosphorylation and mRNA export. Proc Natl Acad Sci U S A 101: 9666-96670. https://doi.org/10.1073/pnas.0403533101.
• Jansen RP, Niessing D, Baumann S, Feldbrügge M (2014) mRNA transport meets membrane traffic. Trends Genet 30: 408-417. https://doi.org/10.1016/j.tig.2014.07.002.
• Ji Z, Song R, Huang H, Regev A, Struhl K (2016) Transcriptome-scale RNase-footprinting of RNA-protein complexes. Nat Biotechnol 34: 410-413. https://doi.org/10.1038/nbt.3441.
• Keene JD (2007) RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 8: 533-543. https://doi.org/10.1038/nrg2111.
• Keerthikumar S, Gangoda L, Liem M, Fonseka P, Atukorala I, Ozcitti C, Mechler A, Adda CG, Ang CS, Mathivanan S (2015) Proteogenomic analysis reveals exosomes are more oncogenic than ectosomes. Oncotarget 6: 15375-15396. https://doi.org/10.18632/oncotarget.3801.
• Keiler KC (2011) RNA localization in bacteria. Curr Opin Microbiol 14: 155-159. https://doi.org/10.1016/j.mib.2011.01.009.
• Kim VN, Dreyfuss G (2001) Nuclear mRNA binding proteins couple pre-mRNA splicing and post-splicing events. Mol Cells 12: 1-10.
• Kim YJ, Maizel A, Chen X (2014) Traffic into silence: endomembranes and post-transcriptional RNA silencing. EMBO J 33: 968-980. https://doi.org/10.1002/embj.201387262.
• Koepke J, Kaffarnik F, Haag C, Zarnack K, Luscombe NM, König J, Ule J, Kellner R, Begerow D, Feldbrügge M (2011) The RNA-binding protein Rrm4 is essential for efficient secretion of endochitinase Cts1. Mol Cell Proteomics 10: M111.011213. https://doi.org/10.1074/mcp.M111.011213.
• Krichevsky AM, Kosik KS (2001) Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32: 683-696. https://doi.org/10.1016/S0896-6273(01)00508-6.
• Kurosaki T, Maquat LE (2016) Nonsense-mediated mRNA decay in humans at a glance. J Cell Sci 129: 461-467. https://doi.org/10.1242/jcs.181008.
• Li S, Liu L, Zhuang X, Yu Y, Liu X, Cui X, Ji L, Pan Z, Cao X, Mo B, Zhang F, Raikhel N, Jiang L, Chen X (2013) MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153: 562-574. https://doi.org/10.1016/j.cell.2013.04.005.
• Li X, Niu T, Manley JL (2007) The RNA binding protein RNPS1 alleviates ASF/SF2 depletion-induced genomic instability. RNA 13: 2108-2115. https://doi.org/10.1261/rna.734407.
• Lötvall J, Hill AF, Hochberg F, Buzás EI, Vizio D Di, Gardiner C, Gho YS, Kurochkin IV, Mathivanan S, Quesenberry P, Sahoo S, Tahara H, Wauben MH, Witwer KW, Théry C (2014) Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J Extracell Vesicles 3: 26913.
• MacDougall N, Clark A, MacDougall E, Davis I (2003) Drosophila gurken (TGFα) mRNA Localizes as particles that move within the oocyte in two dynein-dependent steps. Dev Cell 4: 307-319. https://doi.org/10.1016/S1534-5807(03)00058-3.
• Maquat LE, Hwang J, Sato H, Tang Y (2010) CBP80-promoted mRNP rearrangements during the pioneer round of translation, nonsense-mediated mRNA decay, and thereafter. Cold Spring Harb Symp Quant Biol 75: 127-134. https://doi.org/10.1101/sqb.2010.75.028.
• Marchand V, Gaspar I, Ephrussi A (2012) An intracellular transmission control protocol: assembly and transport of ribonucleoprotein complexes. Curr Opin Cell Biol 24: 202-210. https://doi.org/10.1016/j.ceb.2011.12.014.
• Martin KC, Ephrussi A (2009) mRNA localization: gene expression in the spatial dimension. Cell 136: 719-730. https://doi.org/10.1016/j.cell.2009.01.044.
• Medioni C, Mowry K, Besse F (2012) Principles and roles of mRNA localization in animal development. Development 139: 3263-3276. https://doi.org/10.1242/dev.078626.
• Merz C, Urlaub H, Will CL, Lührmann R (2007) Protein composition of human mRNPs spliced in vitro and differential requirements for mRNP protein recruitment. RNA 13: 116-128. https://doi.org/10.1261/rna.336807.
• Meyer D, Pajonk S, Micali C, O'Connell R, Schulze-Lefert P (2009) Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J 57: 986-999. https://doi.org/10.1111/j.1365-313X.2008.03743.x.
• Mili S, Moissoglu K, Macara IG (2008) Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions. Nature 453: 115-119. https://doi.org/10.1038/nature06888.
• Mingle LA, Okuhama NN, Shi J, Singer RH, Condeelis J, Liu G (2005) Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts. J Cell Sci 118: 2425-2433. https://doi.org/10.1242/jcs.02371.
• Molle D, Segura-Morales C, Camus G, Berlioz-Torrent C, Kjems J, Basyuk E, Bertrand E (2009) Endosomal trafficking of HIV-1 gag and genomic RNAs regulates viral egress. J Biol Chem 284: 19727-19743. https://doi.org/10.1074/jbc.M109.019844.
• Moore MJ, Proudfoot NJ (2009) Pre-mRNA Processing reaches back totranscription and ahead to translation. Cell 136: 688-700. https://doi.org/10.1016/j.cell.2009.02.001.
• Nolte-'t Hoen EN, Buermans HP, Waasdorp M, Stoorvogel W, Wauben MH, 't Hoen PA (2012) Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Res 40: 9272-9285. https://doi.org/10.1093/nar/gks658.
• Oeffinger M, Zenklusen D (2012) To the pore and through the pore: A story of mRNA export kinetics. Biochim Biophys Acta 1819: 494-506. https://doi.org/10.1016/j.bbagrm.2012.02.011.
• Paix A, Le Nguyen PN, Sardet C (2011) Bi-polarized translation of ascidian maternal mRNA determinant pem-1 associated with regulators of the translation machinery on cortical Endoplasmic Reticulum (cER). Dev Biol 357: 211-226. https://doi.org/10.1016/j.ydbio.2011.06.019.
• Park HY, Lim H, Yoon YJ, Follenzi A, Nwokafor C, Lopez-Jones M, Meng X, Singer RH (2014) Visualization of dynamics of single endogenous mRNA labeled in live mouse. Science 343: 422-424. https://doi.org/10.1126/science.1239200.
• Patzelt E, Blaas D, Kuechler E (1983) CAP binding proteins associated with the nucleus. Nucleic Acids Res 11: 5821-5835.
• Paulsen RD, Soni D V, Wollman R, Hahn AT, Yee M, Guan A, Hesley JA, Miller SC, Cromwell EF, Solow-Cordero DE, Meyer T, Cimprich KA (2009) A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol Cell 35: 228-239. https://doi.org/10.1016/j.molcel.2009.06.021.
• Percipalle P, Raju CS, Fukuda N (2009) Actin-associated hnRNP proteins as transacting factors in the control of mRNA transport and localization. RNA Biol 6: 171-174. https://doi.org/10.4161/rna.6.2.8195.
• Raposo G, Stoorvogel W (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200: 373-383. https://doi.org/10.1083/jcb.201211138.
• Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, Ratajczak MZ (2006) Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20: 847-856. https://doi.org/10.1038/sj.leu.2404132.
• Riquelme M (2013) Tip growth in filamentous fungi: a road trip to the apex. Annu Rev Microbiol 67: 587-609. https://doi.org/10.1146/annurev-micro-092412-155652.
• Roberts CT, Kurre P (2013) Vesicle trafficking and RNA transfer add complexity and connectivity to cell-cell communication. Cancer Res 73: 3200-3205. https://doi.org/10.1158/0008-5472.CAN-13-0265.
• Rodrigues ML, Nimrichter L, Oliveira DL, Nosanchuk JD, Casadevall A (2008) Vesicular trans-cell wall transport in fungi: a mechanism for the delivery of virulence-associated macromolecules? Lipid Insights 2: 27-40.
• Samuel M, Bleackley M, Anderson M, Mathivanan S (2015) Extracellular vesicles including exosomes in cross kingdom regulation: a viewpoint from plant-fungal interactions. Front Plant Sci 6: 766. https://doi.org/10.3389/fpls.2015.00766.
• Schmid M, Jaedicke A, Du TG, Jansen RP (2006) Coordination of endoplasmic reticulum and mRNA localization to the yeast bud. Curr Biol 16: 1538-1543. https://doi.org/10.1016/j.cub.2006.06.025.
• Schoenberg DR, Maquat LE (2012) Regulation of cytoplasmic mRNA decay. Nat Rev Genet 13: 246-259. https://doi.org/10.1038/nrg3160.
• Siebrasse JP, Kaminski T, Kubitscheck U (2012) Nuclear export of single native mRNA molecules observed by light sheet fluorescence microscopy. Proc Natl Acad Sci U S A 109: 9426-9431. https://doi.org/10.1073/pnas.1201781109.
• Silverman IM, Li F, Alexander A, Goff L, Trapnell C, Rinn JL, Gregory BD (2014) RNase-mediated protein footprint sequencing reveals protein-binding sites throughout the human transcriptome. Genome Biol 15: R3. https://doi.org/10.1186/gb-2014-15-1-r3.
• Simons M, Raposo G (2009) Exosomes - vesicular carriers for intercellular communication. Curr Opin Cell Biol 21: 575-581. https://doi.org/10.1016/j.ceb.2009.03.007.
• Singh G, Pratt G, Yeo GW, Moore MJ (2015) The Clothes Make the mRNA: Past and Present Trends in mRNP Fashion. Annu Rev Biochem 84: 325-354. https://doi.org/10.1146/annurev-biochem-080111-092106.
• Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT, Carter BS, Krichevsky AM, Breakefield XO (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10: 1470-1476. https://doi.org/10.1038/ncb1800.
• Skoglund U, Andersson K, Björkroth B, Lamb MM, Daneholt B (1983) Visualization of the formation and transport of a specific hnRNP particle. Cell 34: 847-855.
• Sonenberg N, Rupprecht KM, Hecht SM, Shatkin AJ (1979) Eukaryotic mRNA cap binding protein: purification by affinity chromatography on sepharose-coupled m7GDP. Proc Natl Acad Sci U S A 76: 4345-4349. https://doi.org/10.1073/pnas.76.9.4345.
• Speese SD, Ashley J, Jokhi V, Nunnari J, Barria R, Li Y, Ataman B, Koon A, Chang YT, Li Q, Moore MJ, Budnik V (2012) Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 149: 832-846. https://doi.org/10.1016/j.cell.2012.03.032.
• Squires JE, Patel HR, Nousch M, Sibbritt T, Humphreys DT, Parker BJ, Suter CM, Preiss T (2012) Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic Acids Res 40: 5023-5033. https://doi.org/10.1093/nar/gks144.
• St Johnston D (2005) Moving messages: the intracellular localization of mRNAs. Nat Rev Mol Cell Biol 6: 363-375. https://doi.org/10.1038/nrm1643.
• Stalder L, Heusermann W, Sokol L, Trojer D, Wirz J, Hean J, Fritzsche A, Aeschimann F, Pfanzagl V, Basselet P, Weiler J, Hintersteiner M, Morrissey D V, Meisner-Kober NC (2013) The rough endoplasmatic reticulum is a central nucleation site of siRNA-mediated RNA silencing. EMBO J 32: 1115-1127. https://doi.org/10.1038/emboj.2013.52.
• Takizawa PA, Sil A, Swedlow JR, Herskowitz I, Vale RD (1997) Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 389: 90-93. https://doi.org/10.1038/38015.
• Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659. https://doi.org/10.1038/ncb1596.
• Valencia P, Dias AP, Reed R (2008) Splicing promotes rapid and efficient mRNA export in mammalian cells. Proc Natl Acad Sci U S A 105: 3386-3391. https://doi.org/10.1073/pnas.0800250105.
• 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. https://doi.org/10.1016/j.bbagrm.2012.02.017.
• Veith R, Sorkalla T, Baumgart E, Anzt J, Häberlein H, Tyagi S, Siebrasse JP, Kubitscheck U (2010) Balbiani ring mRNPs diffuse through and bind to clusters of large intranuclear molecular structures. Biophys J 99: 2676-2685. https://doi.org/10.1016/j.bpj.2010.08.004.
• Visa N, Alzhanova-Ericsson AT, Sun X, Kiseleva E, Björkroth B, Wurtz T, Daneholt B (1996) A Pre-mRNA-binding protein accompanies the RNA from the gene through the nuclear pores and into polysomes. Cell 84: 253-264. https://doi.org/10.1016/S0092-8674(00)80980-0.
• Voronina E, Seydoux G, Sassone-Corsi P, Nagamori I (2011) RNA Granules in Germ Cells. Cold Spring Harb Perspect Biol 3: a002774-a002774. https://doi.org/10.1101/cshperspect.a002774.
• Wachsmuth M, Caudron-Herger M, Rippe K (2008) Genome organization: Balancing stability and plasticity. Biochim Biophys Acta 1783: 2061-2079. https://doi.org/10.1016/j.bbamcr.2008.07.022.
• Wang X, He C (2014) Reading RNA methylation codes through methyl-specific binding proteins. RNA Biol 11: 669-672. https://doi.org/dx.doi.org/10.4161/rna.28829.
• Weil TT, Forrest KM, Gavis ER (2006) Localization of bicoid mRNA in late oocytes is maintained by continual active transport. Dev Cell 11: 251-262. https://doi.org/10.1016/j.devcel.2006.06.006.
• Wilkie GS, Davis I (2001) Drosophila wingless and Pair-Rule Transcripts Localize Apically by Dynein-Mediated Transport of RNA Particles. Cell 105: 209-219. https://doi.org/10.1016/S0092-8674(01)00312-9.
• Zarnack K, Feldbrügge M (2010) Microtubule-dependent mRNA transport in fungi. Eukaryot Cell 9: 982-990. https://doi.org/10.1128/EC.00030-10.
• Zimyanin VL, Belaya K, Pecreaux J, Gilchrist MJ, Clark A, Davis I, St Johnston D (2008) In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134: 843-853. https://doi.org/10.1016/j.cell.2008.06.053.

Identifiers

DOI

10.18388/abp.2016_1359