Emerging Roles of Disordered Sequences in RNA-Binding Proteins

Lukong, 2008, RNA-binding proteins in human genetic disease, Trends Genet., 24, 416, 10.1016/j.tig.2008.05.004 Cooper, 2009, RNA and disease, Cell, 136, 777, 10.1016/j.cell.2009.02.011 Castello, 2013, RNA-binding proteins in Mendelian disease, Trends Genet., 29, 318, 10.1016/j.tig.2013.01.004 Mittal, 2009, Dissecting the expression dynamics of RNA-binding proteins in posttranscriptional regulatory networks, Proc. Natl. Acad. Sci. U.S.A., 106, 20300, 10.1073/pnas.0906940106 Braunschweig, 2013, Dynamic integration of splicing within gene regulatory pathways, Cell, 152, 1252, 10.1016/j.cell.2013.02.034 Shi, 2015, The end of the message: multiple protein–RNA interactions define the mRNA polyadenylation site, Genes Dev., 29, 889, 10.1101/gad.261974.115 Ha, 2014, Regulation of microRNA biogenesis, Nat. Rev. Mol. Cell Biol., 15, 509, 10.1038/nrm3838 Rinn, 2014, lncRNAs: linking RNA to chromatin, Cold Spring Harb. Perspect. Biol., 6, a018614, 10.1101/cshperspect.a018614 Lasda, 2014, Circular RNAs: diversity of form and function, RNA, 20, 1829, 10.1261/rna.047126.114 St Laurent, 2015, The landscape of long noncoding RNA classification, Trends Genet., 31, 239, 10.1016/j.tig.2015.03.007 Pelletier, 1985, Photochemical cross-linking of cap binding proteins to eucaryotic mRNAs: effect of mRNA 5′ secondary structure, Mol. Cell. Biol., 5, 3222, 10.1128/MCB.5.11.3222 Krainer, 1985, Multiple factors including the small nuclear ribonucleoproteins U1 and U2 are necessary for pre-mRNA splicing in vitro, Cell, 42, 725, 10.1016/0092-8674(85)90269-7 Grabowski, 1986, Affinity chromatography of splicing complexes: U2, U5, and U4 + U6 small nuclear ribonucleoprotein particles in the spliceosome, Science, 233, 1294, 10.1126/science.3638792 Choi, 1986, Heterogeneous nuclear ribonucleoproteins: role in RNA splicing, Science, 231, 1534, 10.1126/science.3952495 Query, 1989, A common RNA recognition motif identified within a defined U1 RNA binding domain of the 70K U1 snRNP protein, Cell, 57, 89, 10.1016/0092-8674(89)90175-X Ramakrishnan, 1992, The structure of ribosomal protein S5 reveals sites of interaction with 16S rRNA, Nature, 358, 768, 10.1038/358768a0 Musco, 1996, Three-dimensional structure and stability of the KH domain: molecular insights into the fragile X syndrome, Cell, 85, 237, 10.1016/S0092-8674(00)81100-9 Shamoo, 1997, Crystal structure of the two RNA binding domains of human hnRNP A1 at 1.75 A resolution, Nat. Struct. Biol., 4, 215, 10.1038/nsb0397-215 Anantharaman, 2002, Comparative genomics and evolution of proteins involved in RNA metabolism, Nucleic Acids Res., 30, 1427, 10.1093/nar/30.7.1427 Hafner, 2010, PAR-CliP – a method to identify transcriptome-wide the binding sites of RNA binding proteins, J. Vis. Exp., 41, 2034 Huppertz, 2014, iCLIP: protein–RNA interactions at nucleotide resolution, Methods, 65, 274, 10.1016/j.ymeth.2013.10.011 Moore, 2014, Mapping Argonaute and conventional RNA-binding protein interactions with RNA at single-nucleotide resolution using HITS-CLIP and CIMS analysis, Nat. Protoc., 9, 263, 10.1038/nprot.2014.012 Nussbacher, 2015, RNA-binding proteins in neurodegeneration: Seq and you shall receive, Trends Neurosci., 38, 226, 10.1016/j.tins.2015.02.003 Ray, 2013, A compendium of RNA-binding motifs for decoding gene regulation, Nature, 499, 172, 10.1038/nature12311 Castello, 2012, Insights into RNA biology from an atlas of mammalian mRNA-binding proteins, Cell, 149, 1393, 10.1016/j.cell.2012.04.031 Baltz, 2012, The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts, Mol. Cell, 46, 674, 10.1016/j.molcel.2012.05.021 Kwon, 2013, The RNA-binding protein repertoire of embryonic stem cells, Nat. Struct. Mol. Biol., 20, 1122, 10.1038/nsmb.2638 Mitchell, 2013, Global analysis of yeast mRNPs, Nat. Struct. Mol. Biol., 20, 127, 10.1038/nsmb.2468 Gerstberger, 2014, A census of human RNA-binding proteins, Nat. Rev. Genet., 15, 829, 10.1038/nrg3813 Neelamraju, 2015, The human RBPome: from genes and proteins to human disease, J. Proteomics, 10.1016/j.jprot.2015.04.031 Thandapani, 2013, Defining the RGG/RG motif, Mol. Cell, 50, 613, 10.1016/j.molcel.2013.05.021 Wahl, 2015, SnapShot: spliceosome dynamics I, Cell, 161, 1474, 10.1016/j.cell.2015.05.050 Matsumoto, 1998, Nuclear history of a pre-mRNA determines the translational activity of cytoplasmic mRNA, EMBO J., 17, 2107, 10.1093/emboj/17.7.2107 Bono, 2011, Assembly, disassembly and recycling: the dynamics of exon junction complexes, RNA Biol., 8, 24, 10.4161/rna.8.1.13618 Rodnina, 2010, The ribosome goes Nobel, Trends Biochem. Sci., 35, 1, 10.1016/j.tibs.2009.11.003 Lunde, 2007, RNA-binding proteins: modular design for efficient function, Nat. Rev. Mol. Cell Biol., 8, 479, 10.1038/nrm2178 Cáceres, 1998, A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm, Genes Dev., 12, 55, 10.1101/gad.12.1.55 Xiao, 1997, Phosphorylation of the ASF/SF2 RS domain affects both protein–protein and protein–RNA interactions and is necessary for splicing, Genes Dev., 11, 334, 10.1101/gad.11.3.334 Bedford, 2000, Arginine methylation inhibits the binding of proline-rich ligands to Src homology 3, but not WW, domains, J. Biol. Chem., 275, 16030, 10.1074/jbc.M909368199 Cote, 2005, Tudor domains bind symmetrical dimethylated arginines, J. Biol. Chem., 280, 28476, 10.1074/jbc.M414328200 Tompa, 2012, Intrinsically disordered proteins: a 10-year recap, Trends Biochem. Sci., 37, 509, 10.1016/j.tibs.2012.08.004 Berlow, 2015, Functional advantages of dynamic protein disorder, FEBS Lett., 10.1016/j.febslet.2015.06.003 Uversky, 2015, The multifaceted roles of intrinsic disorder in protein complexes, FEBS Lett. Wright, 1999, Intrinsically unstructured proteins: re-assessing the protein structure–function paradigm, J. Mol. Biol., 293, 321, 10.1006/jmbi.1999.3110 Uversky, 2002, What does it mean to be natively unfolded?, Eur. J. Biochem., 269, 2, 10.1046/j.0014-2956.2001.02649.x Romero, 2001, Sequence complexity of disordered protein, Proteins, 42, 38, 10.1002/1097-0134(20010101)42:1<38::AID-PROT50>3.0.CO;2-3 Cumberworth, 2013, Promiscuity as a functional trait: intrinsically disordered regions as central players of interactomes, Biochem. J., 454, 361, 10.1042/BJ20130545 van der Lee, 2014, Classification of intrinsically disordered regions and proteins, Chem. Rev., 114, 6589, 10.1021/cr400525m Bah, 2015, Folding of an intrinsically disordered protein by phosphorylation as a regulatory switch, Nature, 519, 106, 10.1038/nature13999 Darnell, 2001, Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function, Cell, 107, 489, 10.1016/S0092-8674(01)00566-9 Hanakahi, 1999, High affinity interactions of nucleolin with G-G-paired rDNA, J. Biol. Chem., 274, 15908, 10.1074/jbc.274.22.15908 Phan, 2011, Structure–function studies of FMRP RGG peptide recognition of an RNA duplex-quadruplex junction, Nat. Struct. Mol. Biol., 18, 796, 10.1038/nsmb.2064 Thandapani, 2015, Aven recognition of RNA G-quadruplexes regulates translation of the mixed lineage leukemia protooncogenes, Elife, 4, 06234, 10.7554/eLife.06234 Kwon, 2013, Phosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low-complexity domains, Cell, 155, 1049, 10.1016/j.cell.2013.10.033 Meinhart, 2004, Recognition of RNA polymerase II carboxy-terminal domain by 3′-RNA-processing factors, Nature, 430, 223, 10.1038/nature02679 Fabrega, 2003, Structure of an mRNA capping enzyme bound to the phosphorylated carboxy-terminal domain of RNA polymerase II, Mol. Cell, 11, 1549, 10.1016/S1097-2765(03)00187-4 Zhou, 2013, Regulation of splicing by SR proteins and SR protein-specific kinases, Chromosoma, 122, 191, 10.1007/s00412-013-0407-z Friesen, 2001, SMN, the product of the spinal muscular atrophy gene, binds preferentially to dimethylarginine-containing protein targets, Mol. Cell, 7, 1111, 10.1016/S1097-2765(01)00244-1 Petrey, 2014, Structural bioinformatics of the interactome, Annu. Rev. Biophys., 43, 193, 10.1146/annurev-biophys-051013-022726 Haynes, 2006, Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes, PLoS Comput. Biol., 2, e100, 10.1371/journal.pcbi.0020100 Jonas, 2013, The role of disordered protein regions in the assembly of decapping complexes and RNP granules, Genes Dev., 27, 2628, 10.1101/gad.227843.113 Peng, 2014, A creature with a hundred waggly tails: intrinsically disordered proteins in the ribosome, Cell. Mol. Life Sci., 71, 1477, 10.1007/s00018-013-1446-6 Korneta, 2012, Intrinsic disorder in the human spliceosomal proteome, PLoS Comput. Biol., 8, e1002641, 10.1371/journal.pcbi.1002641 Wright, 2015, Intrinsically disordered proteins in cellular signalling and regulation, Nat. Rev. Mol. Cell Biol., 16, 18, 10.1038/nrm3920 Ngoc, 2014, Rapid proteasomal degradation of posttranscriptional regulators of the TIS11/tristetraprolin family is induced by an intrinsically unstructured region independently of ubiquitination, Mol. Cell. Biol., 34, 4315, 10.1128/MCB.00643-14 van der Lee, 2014, Intrinsically disordered segments affect protein half-life in the cell and during evolution, Cell Rep., 8, 1832, 10.1016/j.celrep.2014.07.055 Fishbain, 2015, Sequence composition of disordered regions fine-tunes protein half-life, Nat. Struct. Mol. Biol., 22, 214, 10.1038/nsmb.2958 Suskiewicz, 2011, Context-dependent resistance to proteolysis of intrinsically disordered proteins, Protein Sci., 20, 1285, 10.1002/pro.657 Tsvetkov, 2009, The nanny model for IDPs, Nat. Chem. Biol., 5, 778, 10.1038/nchembio.233 Gsponer, 2008, Tight regulation of unstructured proteins: from transcript synthesis to protein degradation, Science, 322, 1365, 10.1126/science.1163581 Gsponer, 2012, Cellular strategies for regulating functional and nonfunctional protein aggregation, Cell Rep., 2, 1425, 10.1016/j.celrep.2012.09.036 Hipp, 2012, Indirect inhibition of 26S proteasome activity in a cellular model of Huntington's disease, J. Cell Biol., 196, 573, 10.1083/jcb.201110093 Bence, 2001, Impairment of the ubiquitin–proteasome system by protein aggregation, Science, 292, 1552, 10.1126/science.292.5521.1552 Holmberg, 2004, Inefficient degradation of truncated polyglutamine proteins by the proteasome, EMBO J., 23, 4307, 10.1038/sj.emboj.7600426 Toretsky, 2014, Assemblages: functional units formed by cellular phase separation, J. Cell Biol., 206, 579, 10.1083/jcb.201404124 Kedersha, 2013, Stress granules and cell signaling: more than just a passing phase?, Trends Biochem. Sci., 38, 494, 10.1016/j.tibs.2013.07.004 Mazroui, 2006, Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2α phosphorylation, Mol. Biol. Cell, 17, 4212, 10.1091/mbc.e06-04-0318 Eulalio, 2007, P-body formation is a consequence, not the cause, of RNA-mediated gene silencing, Mol. Cell. Biol., 27, 3970, 10.1128/MCB.00128-07 Jain, 2013, The discovery and analysis of P bodies, Adv. Exp. Med. Biol., 768, 23, 10.1007/978-1-4614-5107-5_3 Jung, 2012, Axonal mRNA localization and local protein synthesis in nervous system assembly, maintenance and repair, Nat. Rev. Neurosci., 13, 308, 10.1038/nrn3210 Li, 2012, Phase transitions in the assembly of multivalent signalling proteins, Nature, 483, 336, 10.1038/nature10879 Han, 2012, Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies, Cell, 149, 768, 10.1016/j.cell.2012.04.016 Kato, 2012, Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels, Cell, 149, 753, 10.1016/j.cell.2012.04.017 Schwartz, 2013, RNA seeds higher-order assembly of FUS protein, Cell Rep., 5, 918, 10.1016/j.celrep.2013.11.017 Brangwynne, 2009, Germline P granules are liquid droplets that localize by controlled dissolution/condensation, Science, 324, 1729, 10.1126/science.1172046 Weber, 2012, Getting RNA and protein in phase, Cell, 149, 1188, 10.1016/j.cell.2012.05.022 Busch, 2015, Intrinsically disordered proteins drive membrane curvature, Nat. Commun., 24, 7875, 10.1038/ncomms8875 Elbaum-Garfinkle, 2015, The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics, Proc. Natl. Acad. Sci. U.S.A., 112, 7189, 10.1073/pnas.1504822112 Wang, 2014, Regulation of RNA granule dynamics by phosphorylation of serine-rich, intrinsically disordered proteins in C. elegans, Elife, 3, e04591, 10.7554/eLife.04591 Vacic, 2012, Disease-associated mutations disrupt functionally important regions of intrinsic protein disorder, PLoS Comput. Biol., 8, e1002709, 10.1371/journal.pcbi.1002709 Uversky, 2008, Intrinsically disordered proteins in human diseases: introducing the D2 concept, Annu. Rev. Biophys., 37, 215, 10.1146/annurev.biophys.37.032807.125924 Vance, 2009, Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6, Science, 323, 1208, 10.1126/science.1165942 Tradewell, 2012, Arginine methylation by PRMT1 regulates nuclear-cytoplasmic localization and toxicity of FUS/TLS harbouring ALS-linked mutations, Hum. Mol. Genet., 21, 136, 10.1093/hmg/ddr448 Knowles, 2014, The amyloid state and its association with protein misfolding diseases, Nat. Rev. Mol. Cell Biol., 15, 384, 10.1038/nrm3810 Droppelmann, 2014, RNA metabolism in ALS: when normal processes become pathological, Amyotroph. Lateral Scler. Frontotemporal Degener., 15, 321, 10.3109/21678421.2014.881377 Sreedharan, 2008, TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis, Science, 319, 1668, 10.1126/science.1154584 Neumann, 2006, Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis, Science, 314, 130, 10.1126/science.1134108 Kim, 2013, Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS, Nature, 495, 467, 10.1038/nature11922 Fan, 2001, Oligomerization of polyalanine expanded PABPN1 facilitates nuclear protein aggregation that is associated with cell death, Hum. Mol. Genet., 10, 2341, 10.1093/hmg/10.21.2341 Vacic, 2007, Characterization of molecular recognition features, MoRFs, and their binding partners, J. Proteome Res., 6, 2351, 10.1021/pr0701411 Weatheritt, 2012, The identification of short linear motif-mediated interfaces within the human interactome, Bioinformatics, 28, 976, 10.1093/bioinformatics/bts072 Ahmed, 2015, Hydrogel: preparation, characterization, and applications: a review, J. Adv. Res., 6, 105, 10.1016/j.jare.2013.07.006 Sipe, 2010, Amyloid fibril protein nomenclature: 2010 recommendations from the nomenclature committee of the International Society of Amyloidosis, Amyloid, 17, 101, 10.3109/13506129.2010.526812 King, 2012, The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease, Brain Res., 1462, 61, 10.1016/j.brainres.2012.01.016 Oates, 2013, D2P2: database of disordered protein predictions, Nucleic Acids Res., 41, D508, 10.1093/nar/gks1226