Determinants of affinity and specificity in RNA-binding proteins

Current Opinion in Structural Biology

Volumn 38, Issue , 2016, Pages 83-91

  Helder, Stephanie ^a   Blythe, Amanda J ^b   Bond, Charles S ^b   Mackay, Joel P ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; FLAVINE ADENINE NUCLEOTIDE; LONG UNTRANSLATED RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; RNA RECOGNITION MOTIF PROTEIN; TRANSCRIPTION FACTOR YY1; ZINC FINGER PROTEIN; PROTEIN BINDING;

BINDING AFFINITY; CELL STRUCTURE; DNA BINDING; GENE CONTROL; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN RNA BINDING; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; RNA STRUCTURE; SEQUENCE ANALYSIS; TRANSCRIPTION REGULATION; CHEMISTRY; ENZYME SPECIFICITY; METABOLISM; PROTEIN DOMAIN;

HUMANS; PROTEIN BINDING; PROTEIN DOMAINS; RNA, LONG NONCODING; RNA-BINDING PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84973861043     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2016.05.005     Document Type: Review

References (65)

1. Gerstberger S., Hafner M., Tuschl T. A census of human RNA-binding proteins. Nat Rev Genet 2014, 15:829-845.
2. Daubner G.M., Clery A., Allain F.H. RRM-RNA recognition: NMR or crystallography... and new findings. Curr Opin Struct Biol 2013, 23:100-108.
3. Murn J., Teplova M., Zarnack K., Shi Y., Patel D.J. Recognition of distinct RNA motifs by the clustered CCCH zinc fingers of neuronal protein Unkempt. Nat Struct Mol Biol 2016, 23:16-23.
4. Hudson B.P., Martinez-Yamout M.A., Dyson H.J., Wright P.E. Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d. Nat Struct Mol Biol 2004, 11:257-264.
5. Koh Y.Y., Opperman L., Stumpf C., Mandan A., Keles S., Wickens M. A single C. elegans PUF protein binds RNA in multiple modes. RNA 2009, 15:1090-1099.
6. Ray D., Kazan H., Cook K.B., Weirauch M.T., Najafabadi H.S., Li X., Gueroussov S., Albu M., Zheng H., Yang A., et al. A compendium of RNA-binding motifs for decoding gene regulation. Nature 2013, 499:172-177.
7. van Gelder C.W., Gunderson S.I., Jansen E.J., Boelens W.C., Polycarpou-Schwarz M., Mattaj I.W., van Venrooij W.J. A complex secondary structure in U1A pre-mRNA that binds two molecules of U1A protein is required for regulation of polyadenylation. EMBO J 1993, 12:5191-5200.
8. Wang I., Hennig J., Jagtap P.K., Sonntag M., Valcarcel J., Sattler M. Structure, dynamics and RNA binding of the multi-domain splicing factor TIA-1. Nucleic Acids Res 2014, 42:5949-5966.
9. Sabogal A., Lyubimov A.Y., Corn J.E., Berger J.M., Rio D.C. THAP proteins target specific DNA sites through bipartite recognition of adjacent major and minor grooves. Nat Struct Mol Biol 2010, 17:117-123.
10. Guenther U.P., Yandek L.E., Niland C.N., Campbell F.E., Anderson D., Anderson V.E., Harris M.E., Jankowsky E. Hidden specificity in an apparently nonspecific RNA-binding protein. Nature 2013, 502:385-388.
11. Herzog V.A., Lempradl A., Trupke J., Okulski H., Altmutter C., Ruge F., Boidol B., Kubicek S., Schmauss G., Aumayr K., et al. A strand-specific switch in noncoding transcription switches the function of a Polycomb/Trithorax response element. Nat Genet 2014, 46:973-981.
12. Duss O., Michel E., Diarra dit Konte N., Schubert M., Allain F.H. Molecular basis for the wide range of affinity found in Csr/Rsm protein-RNA recognition. Nucleic Acids Res 2014, 42:5332-5346.
13. Kindgren P., Yap A., Bond C.S., Small I. Predictable alteration of sequence recognition by RNA editing factors from Arabidopsis. Plant Cell 2015, 27:403-416.
14. Vasilyev N., Polonskaia A., Darnell J.C., Darnell R.B., Patel D.J., Serganov A. Crystal structure reveals specific recognition of a G-quadruplex RNA by a beta-turn in the RGG motif of FMRP. Proc Natl Acad Sci U S A 2015, 112:E5391-E5400.
15. Haeusler A.R., Donnelly C.J., Periz G., Simko E.A., Shaw P.G., Kim M.S., Maragakis N.J., Troncoso J.C., Pandey A., Sattler R., et al. C9orf72 nucleotide repeat structures initiate molecular cascades of disease. Nature 2014, 507:195-200.
16. Shamoo Y., Abdul-Manan N., Williams K.R. Multiple RNA binding domains (RBDs) just don't add up. Nucleic Acids Res 1995, 23:725-728.
17. Kelly R.C., von Hippel P.H. DNA "melting" proteins. III. Fluorescence "mapping" of the nucleic acid binding site of bacteriophage T4 gene 32-protein. J Biol Chem 1976, 251:7229-7239.
18. Mackereth C.D., Sattler M. Dynamics in multi-domain protein recognition of RNA. Curr Opin Struct Biol 2012, 22:287-296.
19. Kuwasako K., Takahashi M., Unzai S., Tsuda K., Yoshikawa S., He F., Kobayashi N., Guntert P., Shirouzu M., Ito T., et al. RBFOX and SUP-12 sandwich a G base to cooperatively regulate tissue-specific splicing. Nat Struct Mol Biol 2014, 21:778-786.
20. Hennig J., Militti C., Popowicz G.M., Wang I., Sonntag M., Geerlof A., Gabel F., Gebauer F., Sattler M. Structural basis for the assembly of the Sxl-Unr translation regulatory complex. Nature 2014, 515:287-290.
21. Tan D., Marzluff W.F., Dominski Z., Tong L. Structure of histone mRNA stem-loop, human stem-loop binding protein, and 3'hExo ternary complex. Science 2013, 339:318-321.
22. Beckmann B.M., Horos R., Fischer B., Castello A., Eichelbaum K., Alleaume A.M., Schwarzl T., Curk T., Foehr S., Huber W., et al. The RNA-binding proteomes from yeast to man harbour conserved enigmRBPs. Nat Commun 2015, 6:10127.
23. Lu D., Searles M.A., Klug A. Crystal structure of a zinc-finger-RNA complex reveals two modes of molecular recognition. Nature 2003, 426:96-100.
24. Burdach J., O'Connell M.R., Mackay J.P., Crossley M. Two-timing zinc finger transcription factors liaising with RNA. Trends Biochem Sci 2012, 37:199-205.
25. Walden W.E., Selezneva A.I., Dupuy J., Volbeda A., Fontecilla-Camps J.C., Theil E.C., Volz K. Structure of dual function iron regulatory protein 1 complexed with ferritin IRE-RNA. Science 2006, 314:1903-1908.
26. Baltz A.G., Munschauer M., Schwanhausser 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.
27. 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.
28. Kwon S.C., Yi H., Eichelbaum K., Fohr S., Fischer B., You K.T., Castello A., Krijgsveld J., Hentze M.W., Kim V.N. The RNA-binding protein repertoire of embryonic stem cells. Nat Struct Mol Biol 2013, 20:1122-1130.
29. Jeon Y., Lee J.T. YY1 tethers Xist RNA to the inactive X nucleation center. Cell 2011, 146:119-133.
30. Sigova A.A., Abraham B.J., Ji X., Molinie B., Hannett N.M., Guo Y.E., Jangi M., Giallourakis C.C., Sharp P.A., Young R.A. Transcription factor trapping by RNA in gene regulatory elements. Science 2015, 350:978-981.
31. Hentze M.W., Preiss T. The REM phase of gene regulation. Trends Biochem Sci 2010, 35:423-426.
32. Popow J., Alleaume A.M., Curk T., Schwarzl T., Sauer S., Hentze M.W. FASTKD2 is an RNA-binding protein required for mitochondrial RNA processing and translation. RNA 2015, 21:1873-1884.
33. Preitner N., Quan J., Nowakowski D.W., Hancock M.L., Shi J., Tcherkezian J., Young-Pearse T.L., Flanagan J.G. APC is an RNA-binding protein, and its interactome provides a link to neural development and microtubule assembly. Cell 2014, 158:368-382.
34. Yang N., Yu Z., Hu M., Wang M., Lehmann R., Xu R.M. Structure of Drosophila Oskar reveals a novel RNA binding protein. Proc Natl Acad Sci U S A 2015, 112:11541-11546.
35. Smith A.M., Fuchs R.T., Grundy F.J., Henkin T.M. Riboswitch RNAs: regulation of gene expression by direct monitoring of a physiological signal. RNA Biol 2010, 7:104-110.
36. Woo C.J., Kingston R.E. HOTAIR lifts noncoding RNAs to new levels. Cell 2007, 129:1257-1259.
37. Yang Y., Wen L., Zhu H. Unveiling the hidden function of long non-coding RNA by identifying its major partner-protein. Cell Biosci 2015, 5:1-10.
38. Davidovich C., Cech T.R. The recruitment of chromatin modifiers by long noncoding RNAs: lessons from PRC2. RNA 2015, 21:2007-2022.
39. Blythe A.J., Fox A.H., Bond C.S. The ins and outs of lncRNA structure: how, why and what comes next?. Biochim Biophys Acta 2016, 1859:46-58.
40. Somarowthu S., Legiewicz M., Chillon I., Marcia M., Liu F., Pyle A.M. HOTAIR forms an intricate and modular secondary structure. Mol Cell 2015, 58:353-361.
41. Hyman A.A., Weber C.A., Julicher F. Liquid-liquid phase separation in biology. Annu Rev Cell Dev Biol 2014, 30:39-58.
42. Brangwynne C.P., Tompa P., Pappu R.V. Polymer physics of intracellular phase transitions. Nat Phys 2015, 11:899-904.
43. Coletta A., Pinney J.W., Solís D.Y.W., Marsh J., Pettifer S.R., Attwood T.K. Low-complexity regions within protein sequences have position-dependent roles. BMC Syst Biol 2010, 4:1-13.
44. Zhang H., Elbaum-Garfinkle S., Langdon E.M., Taylor N., Occhipinti P., Bridges A.A., Brangwynne C.P., Gladfelter A.S. RNA controls PolyQ protein phase transitions. Mol Cell 2015, 60:220-230.
45. Reijns M.A., Alexander R.D., Spiller M.P., Beggs J.D. A role for Q/N-rich aggregation-prone regions in P-body localization. J Cell Sci 2008, 121:2463-2472.
46. Kato M., Han T.W., Xie S., Shi K., Du X., Wu L.C., Mirzaei H., Goldsmith E.J., Longgood J., Pei J., et al. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 2012, 149:753-767.
47. Gilks N., Kedersha N., Ayodele M., Shen L., Stoecklin G., Dember L.M., Anderson P. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 2004, 15:5383-5398.
48. Hennig S., Kong G., Mannen T., Sadowska A., Kobelke S., Blythe A., Knott G.J., Iyer K.S., Ho D., Newcombe E.A., et al. Prion-like domains in RNA binding proteins are essential for building subnuclear paraspeckles. J Cell Biol 2015, 210:529-539.
49. Huntley M., Golding G. Simple sequences are rare in the Protein Data Bank. Proteins 2002, 48.
50. Uversky V.N. Natively unfolded proteins: a point where biology waits for physics. Protein Sci 2002, 11:739-756.
51. Han T.W., Kato M., Xie S., Wu L.C., Mirzaei H., Pei J., Chen M., Xie Y., Allen J., Xiao G., et al. Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell 2012, 149:768-779.
52. Patel A., Lee H.O., Jawerth L., Maharana S., Jahnel M., Hein M.Y., Stoynov S., Mahamid J., Saha S., Franzmann T.M., et al. A liquid-to-solid phase transition of the ALS protein FUS accelerated by disease mutation. Cell 2015, 162:1066-1077.
53. Kwon I., Kato M., Xiang S., Wu L., Theodoropoulos P., Mirzaei H., Han T., Xie S., Corden J.L., McKnight S.L. Phosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low-complexity domains. Cell 2013, 155:1049-1060.
54. Lee M., Sadowska A., Bekere I., Ho D., Gully B.S., Lu Y., Iyer K.S., Trewhella J., Fox A.H., Bond C.S. The structure of human SFPQ reveals a coiled-coil mediated polymer essential for functional aggregation in gene regulation. Nucleic Acids Res 2015, 43:3826-3840.
55. Elbaum-Garfinkle S., Kim Y., Szczepaniak K., Chen C.C., Eckmann C.R., Myong S., Brangwynne C.P. The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics. Proc Natl Acad Sci U S A 2015, 112:7189-7194.
56. Molliex A., Temirov J., Lee J., Coughlin M., Kanagaraj A.P., Kim H.J., Mittag T., Taylor J.P. Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell 2015, 163:123-133.
57. Altmeyer M., Neelsen K.J., Teloni F., Pozdnyakova I., Pellegrino S., Grofte M., Rask M.B., Streicher W., Jungmichel S., Nielsen M.L., et al. Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose). Nat Commun 2015, 6:8088.
58. Leung A.K. Poly(ADP-ribose): an organizer of cellular architecture. J Cell Biol 2014, 205:613-619.
59. Xiang S., Kato M., Wu L.C., Lin Y., Ding M., Zhang Y., Yu Y., McKnight S.L. The LC domain of hnRNPA2 adopts similar conformations in hydrogel polymers, liquid-like droplets, and nuclei. Cell 2015, 163:829-839.
60. Nott T.J., Petsalaki E., Farber P., Jervis D., Fussner E., Plochowietz A., Craggs T.D., Bazett-Jones D.P., Pawson T., Forman-Kay J.D., et al. Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Mol Cell 2015, 57:936-947.
61. Murakami T., Qamar S., Lin J.Q., Schierle G.S., Rees E., Miyashita A., Costa A.R., Dodd R.B., Chan F.T., Michel C.H., et al. ALS/FTD mutation-induced phase transition of FUS liquid droplets and reversible hydrogels into irreversible hydrogels impairs RNP granule function. Neuron 2015, 88:678-690.
62. Lin Y., Protter D.S., Rosen M.K., Parker R. Formation and maturation of phase-separated liquid droplets by RNA-binding proteins. Mol Cell 2015, 60:208-219.
63. Schmidt H.B., Gorlich D. Transport selectivity of nuclear pores, phase separation, and membraneless organelles. Trends Biochem Sci 2016, 41:46-61.
64. Shen W., Liang X.H., Crooke S.T. Phosphorothioate oligonucleotides can displace NEAT1 RNA and form nuclear paraspeckle-like structures. Nucleic Acids Res 2014, 42:8648-8662.
65. Liang X.H., Shen W., Sun H., Prakash T.P., Crooke S.T. TCP1 complex proteins interact with phosphorothioate oligonucleotides and can co-localize in oligonucleotide-induced nuclear bodies in mammalian cells. Nucleic Acids Res 2014, 42:7819-7832.