Cellular and Molecular Life Sciences

, Volume 73, Issue 21, pp 4075–4084 | Cite as

A structural perspective of RNA recognition by intrinsically disordered proteins

Review

Abstract

Protein-RNA recognition is essential for gene expression and its regulation, which is indispensable for the survival of the living organism at one hand, on the other hand, misregulation of this recognition may lead to their extinction. Polymorphic conformation of both the interacting partners is a characteristic feature of such molecular recognition that promotes the assembly. Many RNA binding proteins (RBP) or regions in them are found to be intrinsically disordered, and this property helps them to play a central role in the regulatory processes. Sequence composition and the length of the flexible linkers between RNA binding domains in RBPs are crucial in making significant contacts with its partner RNA. Polymorphic conformations of RBPs can provide thermodynamic advantage to its binding partner while acting as a chaperone. Prolonged extensions of the disordered regions in RBPs also contribute to the stability of the large cellular machines including ribosome and viral assemblies. The involvement of these disordered regions in most of the significant cellular processes makes RBPs highly associated with various human diseases that arise due to their misregulation.

Keywords

RNA binding proteins Protein-RNA recognition Structural flexibility Induced folding Polymorphic conformation 

References

  1. 1.
    Gerstberger S, Hafner M, Tuschl T (2014) A census of human RNA-binding proteins. Nat Rev Genet 15:829–845PubMedCrossRefGoogle Scholar
  2. 2.
    Ban T, Zhu JK, Melcher K, Xu HE (2015) Structural mechanisms of RNA recognition: sequence-specific and non-specific RNA-binding proteins and the Cas9-RNA-DNA complex. Cell Mol Life Sci 72:1045–1058PubMedCrossRefGoogle Scholar
  3. 3.
    Leeper TC, Qu X, Lu C, Moore C, Varani G (2010) Novel protein–protein contacts facilitate mRNA 3′-processing signal recognition by Rna15 and Hrp1. J Mol Biol 401:334–349PubMedCrossRefGoogle Scholar
  4. 4.
    Stefl R, Oberstrass FC, Hood JL, Jourdan M, Zimmermann M, Skrisovska L, Maris C, Peng L, Hofr C, Emeson RB, Allain FH (2010) The solution structure of the ADAR2 dsRBM-RNA complex reveals a sequence-specific readout of the minor groove. Cell 143:225–237PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Thickman KR, Sickmier EA, Kielkopf CL (2007) Alternative conformations at the RNA-binding surface of the N-terminal U2AF65 RNA recognition motif. J Mol Biol 366:703–710PubMedCrossRefGoogle Scholar
  6. 6.
    Mackereth CD, Sattler M (2012) Dynamics in multi-domain protein recognition of RNA. Curr Opin Struct Biol 22:287–296PubMedCrossRefGoogle Scholar
  7. 7.
    Järvelin AI, Noerenberg M, Davis I, Castello A (2016) The new (dis)order in RNA regulation. Cell Commun Signal 14:1–22CrossRefGoogle Scholar
  8. 8.
    Williamson JR (2000) Induced fit in RNA-protein recognition. Nat Struct Biol 7:834–837PubMedCrossRefGoogle Scholar
  9. 9.
    Varadi M, Zsolyomi F, Guharoy M, Tompa P (2015) Functional advantages of conserved intrinsic disorder in RNA-binding proteins. PLoS One 10:e0139731PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Skupien-Rabian B, Jankowska U, Swiderska B, Lukasiewicz S, Ryszawy D, Dziedzicka-Wasylewska M, Kedracka-Krok S (2016) Proteomic and bioinformatic analysis of a nuclear intrinsically disordered proteome. J Proteomics 130:76–84PubMedCrossRefGoogle Scholar
  11. 11.
    Wright PE, Dyson HJ (1999) Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol 293:321–331PubMedCrossRefGoogle Scholar
  12. 12.
    Dunker AK (2001) Intrinsically disordered protein. J Mol Graph Model 19:26–59PubMedCrossRefGoogle Scholar
  13. 13.
    Bairoch A, Apweiler R (1996) The SWISS-PROT Protein sequence data bank and its new supplement TREMBL. Nucleic Acids Res 24:21–25PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Xie H, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN (2007) Functional anthology of intrinsic disorder. 3. Ligands, post-translational modifications, and diseases associated with intrinsically disordered proteins. J Proteome Res 6:1917–1932PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27:527–533PubMedCrossRefGoogle Scholar
  16. 16.
    Van der Lee R, Buljan M, Lang B, Weatheritt RJ, Daughdrill GW, Dunker AK, Fuxreiter M, Gough J, Gsponer J, Jones DT, Kim PM, Kriwacki RW, Oldfield CJ, Pappu RV, Tompa P, Uversky VN, Wright PE, Babu MM (2014) Classification of intrinsically disordered regions and proteins. Chem Rev 114:6589–6631PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Davey NE, Van Roey K, Weatheritt RJ, Toedt G, Uyar B, Altenberg B, Budd A, Diella F, Dinkel H, Gibson TJ (2012) Attributes of short linear motifs. Mol BioSyst 8:268–281PubMedCrossRefGoogle Scholar
  18. 18.
    Diella F, Haslam N, Chica C, Budd A, Michael S, Brown NP, Trave G, Gibson TJ (2008) Understanding eukaryotic linear motifs and their role in cell signaling and regulation. Front Biosci 13:6580–6603PubMedCrossRefGoogle Scholar
  19. 19.
    Ren S, Uversky VN, Chen Z, Dunker AK, Obradovic Z (2008) Short linear motifs recognized by SH2, SH3 and Ser/Thr kinase domains are conserved in disordered protein regions. BMC Genom 9(Suppl 2):S26CrossRefGoogle Scholar
  20. 20.
    Mohan A, Oldfield CJ, Radivojac P, Vacic V, Cortese MS, Dunker AK, Uversky VN (2006) Analysis of molecular recognition features (MoRFs). J Mol Biol 362:1043–1059PubMedCrossRefGoogle Scholar
  21. 21.
    Vacic V, Oldfield CJ, Mohan A, Radivojac P, Cortese MS, Uversky VN, Dunker AK (2007) Characterization of molecular recognition features, MoRFs, and their binding partners. J Proteome Res 6:2351–2366PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Romero P (2001) Sequence complexity of disordered protein. Proteins 42:38–48PubMedCrossRefGoogle Scholar
  23. 23.
    Fuxreiter M, Simon I, Friedrich P, Tompa P (2004) Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J Mol Biol 338:1015–1026PubMedCrossRefGoogle Scholar
  24. 24.
    Mészáros B, Tompa P, Simon I, Dosztányi Z (2007) Molecular principles of the interactions of disordered proteins. J Mol Biol 372:549–561PubMedCrossRefGoogle Scholar
  25. 25.
    Dyson HJ, Wright PE (2001) Nuclear magnetic resonance methods for elucidation of structure and dynamics in disordered states. Methods Enzymol 339:258–270PubMedCrossRefGoogle Scholar
  26. 26.
    Syme CD, Blanch EW, Holt C, Jakes R, Goedert M, Hecht L, Barron LD (2002) A Raman optical activity study of rheomorphism in caseins, synucleins and tau. New insight into the structure and behaviour of natively unfolded proteins. FEBS J 269:148–156CrossRefGoogle Scholar
  27. 27.
    Lobanov MY, Furletova EI, Bogatyreva NS, Roytberg MA, Galzitskaya OV (2010) Library of disordered patterns in 3D protein structures. PLoS Comput Biol 6:e1000958PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Lee JT (2012) Epigenetic regulation by long noncoding RNAs. Science 338:1435–1439PubMedCrossRefGoogle Scholar
  29. 29.
    Stefl R, Skrisovska L, Allain FH (2005) RNA sequence-and shape-dependent recognition by proteins in the ribonucleoprotein particle. EMBO Rep 6:33–38PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Frankel AD, Smith CA (1998) Induced folding in RNA-protein recognition: more than a simple molecular handshake. Cell 92:149–151PubMedCrossRefGoogle Scholar
  31. 31.
    Dyson HJ (2012) Roles of intrinsic disorder in protein-nucleic acid interactions. Mol BioSyst 8:97–104PubMedCrossRefGoogle Scholar
  32. 32.
    Pan H, Agarwalla S, Moustakas DT, Finer-Moore J, Stroud RM (2003) Structure of tRNA pseudouridine synthase TruB and its RNA complex: RNA recognition through a combination of rigid docking and induced fit. Proc Natl Acad Sci USA 100:12648–12653PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Font J, Mackay JP (2010) Beyond DNA: zinc finger domains as RNA-binding modules. Methods Mol Biol 649:479–491PubMedCrossRefGoogle Scholar
  34. 34.
    Clery A, Blatter M, Allain FH (2008) RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol 18:290–298PubMedCrossRefGoogle Scholar
  35. 35.
    Valverde R, Edwards L, Regan L (2008) Structure and function of KH domains. FEBS J 275:2712–2726PubMedCrossRefGoogle Scholar
  36. 36.
    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 149:1393–1406PubMedCrossRefGoogle Scholar
  37. 37.
    Phan AT, Kuryavyi V, Darnell JC, Serganov A, Majumdar A, Ilin S, Raslin T, Polonskaia A, Chen C, Clain D, Darnell RB, Patel DJ (2011) Structure-function studies of FMRP RGG peptide recognition of an RNA duplex-quadruplex junction. Nature Struct Mol Biol 18:796–804CrossRefGoogle Scholar
  38. 38.
    Wang C, Uversky VN, Kurgan L (2016) Disordered nucleiome: abundance of intrinsic disorder in the DNA and RNA binding proteins in 1121 species from eukaryota, bacteria and archaea. Proteomics 16:1486–1498PubMedCrossRefGoogle Scholar
  39. 39.
    Calabretta S, Richard S (2015) Emerging roles of disordered sequences in RNA-binding proteins. Trends Biochem Sci 40:662–672PubMedCrossRefGoogle Scholar
  40. 40.
    Dan A, Ofran Y, Kliger Y (2010) Large-scale analysis of secondary structure changes in proteins suggests a role for disorder-to-order transitions in nucleotide binding proteins. Proteins 78:236–248PubMedCrossRefGoogle Scholar
  41. 41.
    Tompa P, Csermely P (2004) The role of structural disorder in the function of RNA and protein chaperones. FASEB J 18:1169–1175PubMedCrossRefGoogle Scholar
  42. 42.
    DiNitto JP, Huber PW (2003) Mutual induced fit binding of Xenopus ribosomal protein L5 to 5S rRNA. J Mol Biol 330:979–992PubMedCrossRefGoogle Scholar
  43. 43.
    Coetzee T, Herschlag D, Belfort M (1994) Escherichia coli proteins, including ribosomal protein S12, facilitate in vitro splicing of phage T4 introns by acting as RNA chaperones. Genes Dev 8:1575–1588PubMedCrossRefGoogle Scholar
  44. 44.
    Gabus C, Derrington E, Leblanc P, Chnaiderman J, Dormont D, Swietnicki W, Morillas M, Surewicz WK, Marc D, Nandi P, Darlix JL (2001) The prion protein has RNA binding and chaperoning properties characteristic of nucleocapsid protein NCP7 of HIV-1. J Biol Chem 276:19301–19309PubMedCrossRefGoogle Scholar
  45. 45.
    Cumberworth A, Lamour G, Babu MM, Gsponer J (2013) Promiscuity as a functional trait: intrinsically disordered regions as central players of interactomes. Biochem J 454:361–369PubMedCrossRefGoogle Scholar
  46. 46.
    Peng Z, Oldfield CJ, Xue B, Mizianty MJ, Dunker AK, Kurgan L, Uversky VN (2014) A creature with a hundred waggly tails: intrinsically disordered proteins in the ribosome. Cell Mol Life Sci 71:1477–1504PubMedCrossRefGoogle Scholar
  47. 47.
    Timsit Y, Acosta Z, Allemand F, Chiaruttini C, Springer M (2009) The role of disordered ribosomal protein extensions in the early steps of eubacterial 50S ribosomal subunit assembly. Int J Mol Sci 10:817–834PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Ogle JM, Murphy FV, Tarry MJ, Ramakrishnan V (2002) Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111:721–732PubMedCrossRefGoogle Scholar
  49. 49.
    Wilson DN, Nierhaus KH (2005) Ribosomal proteins in the spotlight. Crit Rev Biochem Mol Biol 40:243–267PubMedCrossRefGoogle Scholar
  50. 50.
    Gunasekaran K, Tsai CJ, Nussinov R (2004) Analysis of ordered and disordered protein complexes reveals structural features discriminating between stable and unstable monomers. J Mol Biol 341:1327–1341PubMedCrossRefGoogle Scholar
  51. 51.
    Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M (2011) The structure of the eukaryotic ribosome at 3.0 Å resolution. Science 334:1524–1529PubMedCrossRefGoogle Scholar
  52. 52.
    Uversky VN (2011) Multitude of binding modes attainable by intrinsically disordered proteins: a portrait gallery of disorder-based complexes. Chem Soc Rev 40:1623–1634PubMedCrossRefGoogle Scholar
  53. 53.
    Singh D, Chang SJ, Lin PH, Averina OV, Kaberdin VR, Lin-Chao S (2009) Regulation of ribonuclease E activity by the L4 ribosomal protein of Escherichia coli. Proc Natl Acad Sci USA 106:864–869PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Hennig J, Sattler M (2015) Deciphering the protein-RNA recognition code: combining large-scale quantitative methods with structural biology. BioEssays 37:899–908PubMedCrossRefGoogle Scholar
  55. 55.
    Hudson BP, Martinez-Yamout MA, Dyson HJ, Wright PE (2004) Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d. Nat Struct Mol Biol 11:257–264PubMedCrossRefGoogle Scholar
  56. 56.
    Barik A, Pilla SP, Bahadur RP (2015) Molecular architecture of protein-RNA recognition sites. J Biomol Struct Dyn 33:2738–2751PubMedCrossRefGoogle Scholar
  57. 57.
    Nahalka J (2014) Protein–RNA recognition: cracking the code. J Theor Biol 343:9–15PubMedCrossRefGoogle Scholar
  58. 58.
    Shoemaker BA, Portman JJ, Wolynes PG (2000) Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc Natl Acad Sci USA 97:8868–8873PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Chen W, Moore MJ (2014) The spliceosome: disorder and dynamics defined. Curr Opin Struct Biol 24:141–149PubMedCrossRefGoogle Scholar
  60. 60.
    Radivojac P, Iakoucheva LM, Oldfield CJ, Obradovic Z, Uversky VN, Dunker AK (2007) Intrinsic disorder and functional proteomics. Biophys J 92:1439–1456PubMedCrossRefGoogle Scholar
  61. 61.
    Korneta I, Bujnicki JM (2012) Intrinsic disorder in the human spliceosomal proteome. PLoS Comput Biol 8:e1002641PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Shepard PJ, Hertel KJ (2009) The SR protein family. Genome Biol 10:242PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Haynes C, Iakoucheva LM (2006) Serine/arginine-rich splicing factors belong to a class of intrinsically disordered proteins. Nucleic Acids Res 34:305–312PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Perez-Canadillas JM, Varani G (2001) Recent advances in RNA-protein recognition. Curr Opin Struct Biol 11:53–58PubMedCrossRefGoogle Scholar
  65. 65.
    Wu JY, Maniatis T (1993) Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75:1061–1070PubMedCrossRefGoogle Scholar
  66. 66.
    Shen H, Kan JL, Green MR (2004) Arginine-serine-rich domains bound at splicing enhancers contact the branchpoint to promote prespliceosome assembly. Mol Cell 13:367–376PubMedCrossRefGoogle Scholar
  67. 67.
    Labourier E, Rossi F, Gallouzi IE, Allemand E, Divita G, Tazi J (1998) Interaction between the N-terminal domain of human DNA topoisomerase I and the arginine-serine domain of its substrate determines phosphorylation of SF2/ASF splicing factor. Nucleic Acids Res 26:2955–2962PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Jurica MS, Moore MJ (2003) Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 12:5–14PubMedCrossRefGoogle Scholar
  69. 69.
    Boulant S, Vanbelle C, Ebel C, Penin F, Lavergne JP (2005) Hepatitis C virus core protein is a dimeric alpha-helical protein exhibiting membrane protein features. J Virol 79:11353–11365PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Barba G, Harper F, Harada T, Kohara M, Goulinet S, Matsuura Y, Eder G, Schaff Z, Chapman M, Miyamura T, Bréchot C (1997) Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci USA 94:1200–1205PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Duvignaud JB, Savard C, Fromentin R, Majeau N, Leclerc D, Gagne SM (2009) Structure and dynamics of the N-terminal half of hepatitis C virus core protein: an intrinsically unstructured protein. Biochem Biophys Res Commun 378:27–31PubMedCrossRefGoogle Scholar
  72. 72.
    Ivanyi-Nagy R, Lavergne J-P, Gabus C, Ficheux D, Darlix J-L (2008) RNA chaperoning and intrinsic disorder in the core proteins of Flaviviridae. Nucleic Acids Res 36:712–725PubMedCrossRefGoogle Scholar
  73. 73.
    Chang CK, Hsu YL, Chang YH, Chao FA, Wu MC, Huang YS, Hu CK, Huang TH (2009) Multiple nucleic acid binding sites and intrinsic disorder of severe acute respiratory syndrome coronavirus nucleocapsid protein: implications for ribonucleocapsid protein packaging. J Virol 83:2255–2264PubMedCrossRefGoogle Scholar
  74. 74.
    Campbell GR, Loret EP (2009) What does the structure-function relationship of the HIV-1 Tat protein teach us about developing an AIDS vaccine? Retrovirology 6:50PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Vendel AC, Lumb KJ (2004) NMR mapping of the HIV-1 Tat interaction surface of the KIX domain of the human coactivator CBP. Biochemistry 43:904–908PubMedCrossRefGoogle Scholar
  76. 76.
    Cai Z, Gorin A, Frederick R, Ye X, Hu W, Majumdar A, Kettani A, Patel DJ (1998) Solution structure of P22 transcriptional antitermination N peptide-boxB RNA complex. Nat Struct Biol 5(3):203–212PubMedCrossRefGoogle Scholar
  77. 77.
    Mogridge J, Legault P, Li J, Van Oene MD, Kay LE, Greenblatt J (1998) Independent ligand-induced folding of the RNA-binding domain and two functionally distinct antitermination regions in the phage lambda N protein. Mol Cell 1:265–275PubMedCrossRefGoogle Scholar
  78. 78.
    Van Gilst MR, Rees WA, Das A, von Hippel PH (1997) Complexes of N antitermination protein of phage λ with specific and nonspecific RNA target sites on the nascent transcript. Biochemistry 36:1514–1524PubMedCrossRefGoogle Scholar
  79. 79.
    Bahadur RP, Kannan S, Zacharias M (2009) Binding of the bacteriophage P22 N-peptide to the boxB RNA motif studied by molecular dynamics simulations. Biophys J 97:3139–3149PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Cooper TA, Wan L, Dreyfuss G (2009) RNA and disease. Cell 136:777–793PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Uversky VN, Oldfield CJ, Dunker AK (2008) Intrinsically disordered proteins in human diseases: introducing the D2 concept. Annu Rev Bio 37:215–246CrossRefGoogle Scholar
  82. 82.
    Kai M (2016) Roles of RNA-binding proteins in DNA damage response. Int J Mol Sci 17Google Scholar
  83. 83.
    Vacic V, Markwick PR, Oldfield CJ, Zhao X, Haynes C, Uversky VN, Iakoucheva LM (2012) Disease-associated mutations disrupt functionally important regions of intrinsic protein disorder. PLoS Comput Biol 8:e1002709PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Vance C, Rogelj B, Hortobagyi T, De Vos KJ, Nishimura AL, Sreedharan J, Hu X, Smith B, Ruddy D, Wright P, Ganesalingam J, Williams KL, Tripathi V, Al-Saraj S, Al-Chalabi A, Leigh PN, Blair IP, Nicholson G, de Belleroche J, Gallo JM, Miller CC, Shaw CE (2009) Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323:1208–1211PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Sprangers R, Groves MR, Sinning I, Sattler M (2003) High-resolution X-ray and NMR structures of the SMN tudor domain: conformational variation in the binding site for symmetrically dimethylated arginine residues. J Mol Biol 327:507–520PubMedCrossRefGoogle Scholar
  86. 86.
    Fischer U, Liu Q, Dreyfuss G (1997) The SMN-SIP1 complex has an essential role in spliceosomal snRNP biogenesis. Cell 90:1023–1029PubMedCrossRefGoogle Scholar
  87. 87.
    Selenko P, Sprangers R, Stier G, Buhler D, Fischer U, Sattler M (2001) SMN tudor domain structure and its interaction with the Sm proteins. Nat Struct Biol 8:27–31PubMedCrossRefGoogle Scholar
  88. 88.
    Gabus C, Mazroui R, Tremblay S, Khandjian EW, Darlix J-L (2004) The fragile X mental retardation protein has nucleic acid chaperone properties. Nucleic Acids Res 32:2129–2137PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Adinolfi S, Bagni C, Musco G, Gibson T, Mazzarella L, Pastore A (1999) Dissecting FMR1, the protein responsible for fragile X syndrome, in its structural and functional domains. RNA 5:1248–1258PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Sung YJ, Conti J, Currie JR, Brown WT, Denman RB (2000) RNAs that interact with the fragile X syndrome RNA binding protein FMRP. Biochem Biophys Res Commun 275:973–980PubMedCrossRefGoogle Scholar
  91. 91.
    Chen L, Yun SW, Seto J, Liu W, Toth M (2003) The fragile X mental retardation protein binds and regulates a novel class of mRNAs containing U rich target sequences. Neuroscience 120:1005–1017PubMedCrossRefGoogle Scholar
  92. 92.
    Brown V, Jin P, Ceman S, Darnell JC, O’Donnell WT, Tenenbaum SA, Jin X, Feng Y, Wilkinson KD, Keene JD, Darnell RB, Warren ST (2001) Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107:477–487PubMedCrossRefGoogle Scholar
  93. 93.
    Jin P, Alisch RS, Warren ST (2004) RNA and microRNAs in fragile X mental retardation. Nature Cell Biol 6:1048–1053PubMedCrossRefGoogle Scholar
  94. 94.
    Summers MF, Henderson LE, Chance MR, Bess JW Jr, South TL, Blake PR, Sagi I, Perez-Alvarado G, Sowder RC 3rd, Hare DR, Arthur LO (1992) Nucleocapsid zinc fingers detected in retroviruses: EXAFS studies of intact viruses and the solution-state structure of the nucleocapsid protein from HIV-1. Protein Sci 1:563–574PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Ivanyi-Nagy R, Davidovic L, Khandjian EW, Darlix JL (2005) Disordered RNA chaperone proteins: from functions to disease. Cell Mol Life Sci 62:1409–1417PubMedCrossRefGoogle Scholar
  96. 96.
    Janin J, Sternberg MJ (2013) Protein flexibility, not disorder, is intrinsic to molecular recognition. F1000 Biol Rep 5:2Google Scholar
  97. 97.
    Barik A, C N, P M, Bahadur RP (2012) A protein-RNA docking benchmark (I): nonredundant cases. Proteins 80:1866–1871PubMedGoogle Scholar

Copyright information

© Springer International Publishing 2016

Authors and Affiliations

  1. 1.Computational Structural Biology Lab, Department of BiotechnologyIndian Institute of Technology KharagpurKharagpurIndia

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