Dynamics in multi-domain protein recognition of RNA

Current Opinion in Structural Biology

Volumn 22, Issue 3, 2012, Pages 287-296

  Mackereth, Cameron D ^a   Sattler, Michael ^b,c  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RNA;

BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; REVIEW; RNA CONFORMATION; STRUCTURE ANALYSIS;

MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA; RNA-BINDING PROTEINS;

EUKARYOTA;

EID: 84862633452     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2012.03.013     Document Type: Review

References (75)

1. Moore M.J. From birth to death: the complex lives of eukaryotic mRNAs. Science 2005, 309:1514-1518.
2. Maniatis T., Reed R. An extensive network of coupling among gene expression machines. Nature 2002, 416:499-506.
3. Jinek M., Doudna J.A. A three-dimensional view of the molecular machinery of RNA interference. Nature 2009, 457:405-412.
4. Esteller M. Non-coding RNAs in human disease. Nat Rev Genet 2011, 12:861-874.
5. Lukong K.E., Chang K.W., Khandjian E.W., Richard S. RNA-binding proteins in human genetic disease. Trends Genet 2008, 24:416-425.
6. Kim M.Y., Hur J., Jeong S. Emerging roles of RNA and RNA-binding protein network in cancer cells. BMB Rep 2009, 42:125-130.
7. Cooper T.A., Wan L., Dreyfuss G. RNA and disease. Cell 2009, 136:777-793.
8. Petrov A., Kornberg G., O'Leary S., Tsai A., Uemura S., Puglisi J.D. Dynamics of the translational machinery. Curr Opin Struct Biol 2011, 21:137-145.
9. Cramer P., Armache K.J., Baumli S., Benkert S., Brueckner F., Buchen C., Damsma G.E., Dengl S., Geiger S.R., Jasiak A.J., et al. Structure of eukaryotic RNA polymerases. Annu Rev Biophys 2008, 37:337-352.
10. Wahl M.C., Will C.L., Luhrmann R. The spliceosome: design principles of a dynamic RNP machine. Cell 2009, 136:701-718.
11. Clery A., Blatter M., Allain F.H. RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol 2008, 18:290-298.
12. Valverde R., Edwards L., Regan L. Structure and function of KH domains. FEBS J 2008, 275:2712-2726.
13. Messias A.C., Sattler M. Structural basis of single-stranded RNA recognition. Acc Chem Res 2004, 37:279-287.
14. Font J., Mackay J.P. Beyond DNA: zinc finger domains as RNA-binding modules. Methods Mol Biol 2010, 649:479-491.
15. Sachs R., Max K.E., Heinemann U., Balbach J. RNA single strands bind to a conserved surface of the major cold shock protein in crystals and solution. RNA 2012, 18:65-76.
16. Lunde B.M., Moore C., Varani G. RNA-binding proteins: modular design for efficient function. Nat Rev Mol Cell Biol 2007, 8:479-490.
17. Mackay J.P., Font J., Segal D.J. The prospects for designer single-stranded RNA-binding proteins. Nat Struct Mol Biol 2011, 18:256-261.
18. Nam Y., Chen C., Gregory R.I., Chou J.J., Sliz P. Molecular basis for interaction of let-7 microRNAs with Lin28. Cell 2011, 147:1080-1091.
19. Thickman K.R., Sickmier E.A., Kielkopf C.L. Alternative conformations at the RNA-binding surface of the N-terminal U2AF(65) RNA recognition motif. J Mol Biol 2007, 366:703-710.
20. Boehr D.D., Nussinov R., Wright P.E. The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol 2009, 5:789-796.
21. Smock R.G., Gierasch L.M. Sending signals dynamically. Science 2009, 324:198-203.
22. Henzler-Wildman K., Kern D. Dynamic personalities of proteins. Nature 2007, 450:964-972.
23. Vogel J., Luisi B.F. Hfq and its constellation of RNA. Nat Rev Microbiol 2011, 9:578-589.
24. Rubinson E.H., Eichman B.F. Nucleic acid recognition by tandem helical repeats. Curr Opin Struct Biol 2012, 22:101-109.
25. Leeper T.C., Qu X., Lu C., Moore C., Varani G. Novel protein-protein contacts facilitate mRNA 3'-processing signal recognition by Rna15 and Hrp1. J Mol Biol 2010, 401:334-349.
26. Teplova M., Wohlbold L., Khin N.W., Izaurralde E., Patel D.J. Structure-function studies of nucleocytoplasmic transport of retroviral genomic RNA by mRNA export factor TAP. Nat Struct Mol Biol 2011, 18:990-998.
27. Stefl R., Oberstrass F.C., Hood J.L., Jourdan M., Zimmermann M., Skrisovska L., Maris C., Peng L., Hofr C., Emeson R.B., et al. The solution structure of the ADAR2 dsRBM-RNA complex reveals a sequence-specific readout of the minor groove. Cell 2010, 143:225-237.
28. Loughlin F.E., Gebert L.F., Towbin H., Brunschweiger A., Hall J., Allain F.H. Structural basis of pre-let-7 miRNA recognition by the zinc knuckles of pluripotency factor Lin28. Nat Struct Mol Biol 2011, 19:84-89.
29. Mackereth C.D., Madl T., Bonnal S., Simon B., Zanier K., Gasch A., Rybin V., Valcarcel J., Sattler M. Multi-domain conformational selection underlies pre-mRNA splicing regulation by U2AF. Nature 2011, 475:408-411.
30. Pancevac C., Goldstone D.C., Ramos A., Taylor I.A. Structure of the Rna15 RRM-RNA complex reveals the molecular basis of GU specificity in transcriptional 3'-end processing factors. Nucleic Acids Res 2010, 38:3119-3132.
31. Perez-Canadillas J.M. Grabbing the message: structural basis of mRNA 3'UTR recognition by Hrp1. EMBO J 2006, 25:3167-3178.
32. Moreno-Morcillo M., Minvielle-Sebastia L., Fribourg S., Mackereth C.D. Locked tether formation by cooperative folding of Rna14p monkeytail and Rna15p hinge domains in the yeast CF IA complex. Structure 2011, 19:534-545.
33. Liker E., Fernandez E., Izaurralde E., Conti E. The structure of the mRNA export factor TAP reveals a cis arrangement of a non-canonical RNP domain and an LRR domain. EMBO J 2000, 19:5587-5598.
34. Oberstrass F.C., Auweter S.D., Erat M., Hargous Y., Henning A., Wenter P., Reymond L., Amir-Ahmady B., Pitsch S., Black D.L., et al. Structure of PTB bound to RNA: specific binding and implications for splicing regulation. Science 2005, 309:2054-2057.
35. Lamichhane R., Daubner G.M., Thomas-Crusells J., Auweter S.D., Manatschal C., Austin K.S., Valniuk O., Allain F.H., Rueda D. RNA looping by PTB: evidence using FRET and NMR spectroscopy for a role in splicing repression. Proc Natl Acad Sci USA 2010, 107:4105-4110.
36. Chao J.A., Patskovsky Y., Patel V., Levy M., Almo S.C., Singer R.H. ZBP1 recognition of beta-actin zipcode induces RNA looping. Genes Dev 2010, 24:148-158.
37. Mackereth C.D., Simon B., Sattler M. Extending the size of protein-RNA complexes studied by nuclear magnetic resonance spectroscopy. Chembiochem 2005, 6:1578-1584.
38. Diaz-Moreno I., Hollingworth D., Kelly G., Martin S., Garcia-Mayoral M., Briata P., Gherzi R., Ramos A. Orientation of the central domains of KSRP and its implications for the interaction with the RNA targets. Nucleic Acids Res 2010, 38:5193-5205.
39. Teplova M., Malinina L., Darnell J.C., Song J., Lu M., Abagyan R., Musunuru K., Teplov A., Burley S.K., Darnell R.B., et al. Protein-RNA and protein-protein recognition by dual KH1/2 domains of the neuronal splicing factor Nova-1. Structure 2011, 19:930-944.
40. Edwards J., Malaurie E., Kondrashov A., Long J., de Moor C.H., Searle M.S., Emsley J. Sequence determinants for the tandem recognition of UGU and CUG rich RNA elements by the two N--terminal RRMs of CELF1. Nucleic Acids Res 2011, 39:8638-8650.
41. Teplova M., Song J., Gaw H.Y., Teplov A., Patel D.J. Structural insights into RNA recognition by the alternate-splicing regulator CUG-binding protein 1. Structure 2010, 18:1364-1377.
42. Teplova M., Patel D.J. Structural insights into RNA recognition by the alternative-splicing regulator muscleblind-like MBNL1. Nat Struct Mol Biol 2008, 15:1343-1351.
43. Liu Z., Luyten I., Bottomley M.J., Messias A.C., Houngninou-Molango S., Sprangers R., Zanier K., Kramer A., Sattler M. Structural basis for recognition of the intron branch site RNA by splicing factor 1. Science 2001, 294:1098-1102.
44. Ryder S.P., Frater L.A., Abramovitz D.L., Goodwin E.B., Williamson J.R. RNA target specificity of the STAR/GSG domain post-transcriptional regulatory protein GLD-1. Nat Struct Mol Biol 2004, 11:20-28.
45. Beuck C., Szymczyna B.R., Kerkow D.E., Carmel A.B., Columbus L., Stanfield R.L., Williamson J.R. Structure of the GLD-1 homodimerization domain: insights into STAR protein-mediated translational regulation. Structure 2010, 18:377-389.
46. Meyer N.H., Tripsianes K., Vincendeau M., Madl T., Kateb F., Brack-Werner R., Sattler M. Structural basis for homodimerization of the Src-associated during mitosis, 68-kDa protein (Sam68) Qua1 domain. J Biol Chem 2010, 285:28893-28901.
47. Varani L., Gunderson S.I., Mattaj I.W., Kay L.E., Neuhaus D., Varani G. The NMR structure of the 38 kDa U1A protein - PIE RNA complex reveals the basis of cooperativity in regulation of polyadenylation by human U1A protein. Nat Struct Biol 2000, 7:329-335.
48. Kelly R.C., Jensen D.E., von Hippel P.H. DNA "melting" proteins. IV. Fluorescence measurements of binding parameters for bacteriophage T4 gene 32-protein to mono-, oligo-, and polynucleotides. J Biol Chem 1976, 251:7240-7250.
49. Banerjee H., Rahn A., Davis W., Singh R. Sex lethal and U2 small nuclear ribonucleoprotein auxiliary factor (U2AF(65)) recognize polypyrimidine tracts using multiple modes of binding. RNA 2003, 9:88-99.
50. Iwahara J., Clore G.M. Detecting transient intermediates in macromolecular binding by paramagnetic NMR. Nature 2006, 440:1227-1230.
51. Kalodimos C.G., Boelens R., Kaptein R. Toward an integrated model of protein-DNA recognition as inferred from NMR studies on the Lac repressor system. Chem Rev 2004, 104:3567-3586.
52. 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.
53. Sickmier E.A., Frato K.E., Shen H., Paranawithana S.R., Green M.R., Kielkopf C.L. Structural basis for polypyrimidine tract recognition by the essential pre-mRNA splicing factor U2AF65. Mol Cell 2006, 23:49-59.
54. Shoemaker B.A., Portman J.J., Wolynes P.G. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc Natl Acad Sci USA 2000, 97:8868-8873.
55. Lee B.M., Xu J., Clarkson B.K., Martinez-Yamout M.A., Dyson H.J., Case D.A., Gottesfeld J.M., Wright P.E. Induced fit and "lock and key" recognition of 5S RNA by zinc fingers of transcription factor IIIA. J Mol Biol 2006, 357:275-291.
56. Ma B., Tsai C.J., Haliloglu T., Nussinov R. Dynamic allostery: linkers are not merely flexible. Structure 2011, 19:907-917.
57. Zhang Q., Stelzer A.C., Fisher C.K., Al-Hashimi H.M. Visualizing spatially correlated dynamics that directs RNA conformational transitions. Nature 2007, 450:1263-1267.
58. Hammes G.G., Chang Y.C., Oas T.G. Conformational selection or induced fit: a flux description of reaction mechanism. Proc Natl Acad Sci USA 2009, 106:13737-13741.
59. Tugarinov V., Kanelis V., Kay L.E. Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy. Nat Protoc 2006, 1:749-754.
60. Tugarinov V., Hwang P.M., Kay L.E. Nuclear magnetic resonance spectroscopy of high-molecular-weight proteins. Annu Rev Biochem 2004, 73:107-146.
61. Muona M., Aranko A.S., Raulinaitis V., Iwai H. Segmental isotopic labeling of multi-domain and fusion proteins by protein trans-splicing in vivo and in vitro. Nat Protoc 2010, 5:574-587.
62. Skrisovska L., Allain F.H. Improved segmental isotope labeling methods for the NMR study of multidomain or large proteins: application to the RRMs of Npl3p and hnRNP L. J Mol Biol 2008, 375:151-164.
63. Simon B., Madl T., Mackereth C.D., Nilges M., Sattler M. An efficient protocol for NMR-spectroscopy-based structure determination of protein complexes in solution. Angew Chem Int Ed Engl 2010, 49:1967-1970.
64. Blackledge M. Recent progress in the study of biomolecular structure and dynamics in solution from residual dipolar couplings. Prog NMR Spectrosc 2005, 46:23-61.
65. Clore G.M., Iwahara J. Theory, practice, and applications of paramagnetic relaxation enhancement for the characterization of transient low-population states of biological macromolecules and their complexes. Chem Rev 2009, 109:4108-4139.
66. Bernini A., Venditti V., Spiga O., Niccolai N. Probing protein surface accessibility with solvent and paramagnetic molecules. Prog NMR Spectrosc 2009, 54:278-289.
67. Madl T., Guttler T., Gorlich D., Sattler M. Structural analysis of large protein complexes using solvent paramagnetic relaxation enhancements. Angew Chem Int Ed Engl 2011, 50:3993-3997.
68. Madl T., Gabel F., Sattler M. NMR and small-angle scattering-based structural analysis of protein complexes in solution. J Struct Biol 2011, 173:472-482.
69. Güttler T., Madl T., Neumann P., Deichsel D., Corsini L., Monecke T., Ficner R., Sattler M., Görlich D. NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1. Nat Struct Mol Biol 2010, 17:1367-1376.
70. Mittermaier A., Kay L.E. New tools provide new insights in NMR studies of protein dynamics. Science 2006, 312:224-228.
71. Volkov A.N., Ubbink M., van Nuland N.A. Mapping the encounter state of a transient protein complex by PRE NMR spectroscopy. J Biomol NMR 2010, 48:225-236.
72. Petoukhov M.V., Svergun D.I. Analysis of X-ray and neutron scattering from biomacromolecular solutions. Curr Opin Struct Biol 2007, 17:562-571.
73. Putnam C.D., Hammel M., Hura G.L., Tainer J.A. X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution. Q Rev Biophys 2007, 40:191-285.
74. Wang Y.X., Zuo X., Wang J., Yu P., Butcher S.E. Rapid global structure determination of large RNA and RNA complexes using NMR and small-angle X-ray scattering. Methods 2010, 52:180-191.
75. Grishaev A., Wu J., Trewhella J., Bax A. Refinement of multidomain protein structures by combination of solution small-angle X-ray scattering and NMR data. J Am Chem Soc 2005, 127:16621-16628.