Small-angle X-ray scattering: A bridge between RNA secondary structures and three-dimensional topological structures

Current Opinion in Structural Biology

Volumn 30, Issue , 2015, Pages 147-160

  Fang, Xianyang ^a   Stagno, Jason R ^a   Bhandari, Yuba R ^a   Zuo, Xiaobing ^b   Wang, Yun Xing ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SUGAR PHOSPHATE; RNA;

DENSITY; ELECTRON; EXPERIMENT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; REVIEW; RNA SECONDARY STRUCTURE; RNA STRUCTURE; RNA TOPOLOGICAL STRUCTURE; SAMPLE; SENSITIVITY AND SPECIFICITY; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY; BASE PAIRING; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER PROGRAM; CONFORMATION; GENETICS; PROCEDURES; SMALL ANGLE SCATTERING; STRUCTURE ACTIVITY RELATION; X RAY DIFFRACTION;

BASE PAIRING; COMPUTATIONAL BIOLOGY; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; RNA; SCATTERING, SMALL ANGLE; SOFTWARE; STRUCTURE-ACTIVITY RELATIONSHIP; X-RAY DIFFRACTION;

EID: 84924290425     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2015.02.010     Document Type: Review

References (95)

1. Feigin L.A., Svergun D.I. Structure Analysis by Small Angle X-ray and Neutron Scattering 1987, Plenum Press, New York.
2. Glatter O., Kratky O. Small Angle X-ray Scattering 1982, Academic Press, New York.
3. Svergun D.I., Volkov V.V., Kozin M.B., Stuhrmann H.B. New developments in direct shape determination from small-angle scattering. 2. Uniqueness. Acta Crystallogr A 1996, 52:419-426.
4. Svergun D.I., Volkov V.V., Kozin M.B., Stuhrmann H.B., Barberato C., Koch M.H.J. Shape determination from solution scattering of biopolymers. J ApplCrystallogr 1997, 30:798-802.
5. Svergun D.I., Petoukhov M.V., Koch M.H. Determination of domain structure of proteins from X-ray solution scattering. Biophys J 2001, 80:2946-2953.
6. Svergun D.I. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys J 1999, 77:2879-2886.
7. Svergun D.I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J ApplCrystallogr 1992, 25:495-503.
8. Franke D., Svergun D.I. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J Appl Crystallogr 2009, 42:342-346.
9. Chacon P., Moran F., Diaz J.F., Pantos E., Andreu J.M. Low-resolution structures of proteins in solution retrieved from X-ray scattering with a genetic algorithm. Biophys J 1998, 74:2760-2775.
10. Walther D., Cohen F.E., Doniach S. Reconstruction of low-resolution three-dimensional density maps from one-dimensional small-angle X-ray solution scattering data for biomolecules. J ApplCrystallogr 2000, 33:350-363.
11. Lake J.A. Yeast transfer RNA: a small-angle X-ray study. Science 1967, 156:1371-1373.
12. Rambo R.P., Tainer J.A. Characterizing flexible and intrinsically unstructured biological macromolecules by SAS using the Porod-Debye law. Biopolymers 2011, 95:559-571.
13. Russell R., Millett I.S., Tate M.W., Kwok L.W., Nakatani B., Gruner S.M., Mochrie S.G., Pande V., Doniach S., Herschlag D., et al. Rapid compaction during RNA folding. Proc Natl Acad Sci U S A 2002, 99:4266-4271.
14. Russell R., Millett I.S., Doniach S., Herschlag D. Small angle X-ray scattering reveals a compact intermediate in RNA folding. Nat Struct Biol 2000, 7:367-370.
15. Feigin L.A., Svergun D.I. Structure Analysis by Small-angle X-ray Scattering and Neutron Scattering 1987, Plenum Press, New York. L.A. Fiegin, D.I. Svergun (Eds.).
16. Hura G.L., Budworth H., Dyer K.N., Rambo R.P., Hammel M., McMurray C.T., Tainer J.A. Comprehensive macromolecular conformations mapped by quantitative SAXS analyses. Nat Methods 2013, 10:453-454.
17. Lipfert J., Doniach S. Small-angle X-ray scattering from RNA, proteins, and protein complexes. Annu Rev Biophys Biomol Struct 2007, 36:307-327.
18. Lipfert J., Herschlag D., Doniach S. Riboswitch conformations revealed by small-angle X-ray scattering. Methods Mol Biol 2009, 540:141-159.
19. Burke J.E., Butcher S.E. Nucleic acid structure characterization by small angle X-ray scattering (SAXS). Curr Protoc Nucleic Acid Chem 2012, 18. Chapter 7:Unit7.
20. Zhang J., Lau M.W., Ferre-D'Amare A.R. Ribozymes and riboswitches: modulation of RNA function by small molecules. Biochemistry 2010, 49:9123-9131.
21. Mathews D.H., Turner D.H., Zuker M. RNA secondary structure prediction. Curr Protoc Nucleic Acid Chem 2007, 12. Chapter 11:Unit 11.
22. Hofacker I.L., Fontana W., Stadler P.F., Bonhoeffer S., Tacker M., Schuster P. Fast folding and comparison of RNA secondary structures. Monatsh Chem 1994, 125:167-188.
23. Merino E.J., Wilkinson K.A., Coughlan J.L., Weeks K.M. RNA structure analysis at single nucleotide resolution by selective 2'-hydroxyl acylation and primer extension (SHAPE). J Am Chem Soc 2005, 127:4223-4231.
24. Holbrook S.R. Structural principles from large RNAs. Annu Rev Biophys 2008, 37:445-464.
25. Zhang J., Jones C.P., Ferre-D'Amare A.R. Global analysis of riboswitches by small-angle X-ray scattering and calorimetry. Biochim Biophys Acta 2014, 1839:1020-1029.
26. Laing C., Wen D., Wang J.T., Schlick T. Predicting coaxial helical stacking in RNA junctions. Nucleic Acids Res 2012, 40:487-498.
27. de la Pena M., Dufour D., Gallego J. Three-way RNA junctions with remote tertiary contacts: a recurrent and highly versatile fold. RNA 2009, 15:1949-1964.
28. Lescoute A., Westhof E. Topology of three-way junctions in folded RNAs. RNA 2006, 12:83-93.
29. Lipfert J., Ouellet J., Norman D.G., Doniach S., Lilley D.M. The complete VS ribozyme in solution studied by small-angle X-ray scattering. Structure 2008, 16:1357-1367.
30. Bailor M.H., Mustoe A.M., Brooks C.L., Al-Hashimi H.M. Topological constraints: using RNA secondary structure to model 3D conformation, folding pathways, and dynamic adaptation. Curr Opin Struct Biol 2011, 21:296-305.
31. Bailor M.H., Sun X., Al-Hashimi H.M. Topology links RNA secondary structure with global conformation, dynamics, and adaptation. Science 2011, 327:202-206.
32. Witz J. 1964: the first model for the shape of a transfer RNA molecule. An account of an unpublished small-angle X-ray scattering study. Biochimie 2003, 85:1265-1268.
33. Robertus J.D., Ladner J.E., Finch J.T., Rhodes D., Brown R.S., Clark B.F., Klug A. Structure of yeast phenylalanine tRNA at 3A resolution. Nature 1974, 250:546-551.
34. Funari S.S., Rapp G., Perbandt M., Dierks K., Vallazza M., Betzel C., Erdmann V.A., Svergun D.I. Structure of free Thermus flavus 5S rRNA at 1.3nm resolution from synchrotron X-ray solution scattering. J Biol Chem 2000, 275:31283-31288.
35. Lipfert J., Chu V.B., Bai Y., Herschlag D., Doniach S. Low-resolution models for nucleic acids from small-angle X-ray scattering with applications to electrostatic modeling. J ApplCrystallogr 2007, 40:S229-S234.
36. Jones C.P., Cantara W.A., Olson E.D., Musier-Forsyth K. Small-angle X-ray scattering-derived structure of the HIV-1 5' UTR reveals 3D tRNA mimicry. Proc Natl Acad Sci U S A 2014, 111:3395-3400.
37. Burke J.E., Sashital D.G., Zuo X., Wang Y.X., Butcher S.E. Structure of the yeast U2/U6 snRNA complex. RNA 2012, 18:673-683.
38. Bai Y., Tambe A., Zhou K., Doudna J.A. RNA-guided assembly of Rev-RRE nuclear export complexes. Elife 2014, 3:e03656.
39. Hammond J.A., Rambo R.P., Filbin M.E., Kieft J.S. Comparison and functional implications of the 3D architectures of viral tRNA-like structures. RNA 2009, 15:294-307.
40. Rambo R.P., Tainer J.A. Improving small-angle X-ray scattering data for structural analyses of the RNA world. RNA 2010, 16:638-646.
41. Zuo X.B., Wang J.B., Yu P., Eyler D., Xu H., Starich M.R., Tiede D.M., Simon A.E., Kasprzak W., Schwieters C.D., et al. Solution structure of the cap-independent translational enhancer and ribosome-binding element in the 3' UTR of turnip crinkle virus. Proc Natl Acad Sci U S A 2010, 107:1385-1390.
42. Hiley S.L., Collins R.A. Rapid formation of a solvent-inaccessible core in the Neurospora Varkud satellite ribozyme. EMBO J 2001, 20:5461-5469.
43. Wilson T.J., Lilley D.M. Do the hairpin and VS ribozymes share a common catalytic mechanism based on general acid-base catalysis? A critical assessment of available experimental data. RNA 2011, 17:213-221.
44. Baird N.J., Kulshina N., Ferre-D'Amare A.R. Riboswitch function: flipping the switch or tuning the dimmer?. RNA Biol 2010, 7:328-332.
45. Haller A., Souliere M.F., Micura R. The dynamic nature of RNA as key to understanding riboswitch mechanisms. Acc Chem Res 2011, 44:1339-1348.
46. Mann D.A., Mikaelian I., Zemmel R.W., Green S.M., Lowe A.D., Kimura T., Singh M., Butler P.J., Gait M.J., Karn J. A molecular rheostat. Co-operative rev binding to stem I of the rev-response element modulates human immunodeficiency virus type-1 late gene expression. J Mol Biol 1994, 241:193-207.
47. Heaphy S., Finch J.T., Gait M.J., Karn J., Singh M. Human immunodeficiency virus type 1 regulator of virion expression, rev, forms nucleoprotein filaments after binding to a purine-rich "bubble" located within the rev-responsive region of viral mRNAs. Proc Natl Acad Sci U S A 1991, 88:7366-7370.
48. Dayton E.T., Powell D.M., Dayton A.I. Functional analysis of CAR, the target sequence for the Rev protein of HIV-1. Science 1989, 246:1625-1629.
49. Kjems J., Brown M., Chang D.D., Sharp P.A. Structural analysis of the interaction between the human immunodeficiency virus Rev protein and the Rev response element. Proc Natl Acad Sci U S A 1991, 88:683-687.
50. Battiste J.L., Mao H., Rao N.S., Tan R., Muhandiram D.R., Kay L.E., Frankel A.D., Williamson J.R. Alpha helix-RNA major groove recognition in an HIV-1 rev peptide-RRE RNA complex. Science 1996, 273:1547-1551.
51. Daugherty M.D., D'Orso I., Frankel A.D. A solution to limited genomic capacity: using adaptable binding surfaces to assemble the functional HIV Rev oligomer on RNA. Mol Cell 2008, 31:824-834.
52. Fang X., Wang J., O'Carroll I.P., Mitchell M., Zuo X., Wang Y., Yu P., Liu Y., Rausch J.W., Dyba M.A., et al. An unusual topological structure of the HIV-1 Rev response element. Cell 2013, 155:594-605.
53. DiMattia M.A., Watts N.R., Stahl S.J., Rader C., Wingfield P.T., Stuart D.I., Steven A.C., Grimes J.M. Implications of the HIV-1 Rev dimer structure at 3.2A resolution for multimeric binding to the Rev response element. Proc Natl Acad Sci U S A 2010, 107:5810-5814.
54. Daugherty M.D., Liu B., Frankel A.D. Structural basis for cooperative RNA binding and export complex assembly by HIV Rev. Nat Struct Mol Biol 2010, 17:1337-1342.
55. Cruz J.A., Westhof E. The dynamic landscapes of RNA architecture. Cell 2009, 136:604-609.
56. Zuo X.B., Wang J.B., Foster T.R., Schwieters C.D., Tiede D.M., Butcher S.E., Wang Y.X. Global molecular structure and interfaces: refining an RNA: RNA complex structure using solution X-ray scattering data. J Am Chem Soc 2008, 130:3292-3294.
57. Grishaev A., Ying J., Canny M.D., Pardi A., Bax A. Solution structure of tRNAVal from refinement of homology model against residual dipolar coupling and SAXS data. J Biomol NMR 2008, 42:99-109.
58. Wang J., Zuo X., Yu P., Xu H., Starich M.R., Tiede D.M., Shapiro B.A., Schwieters C.D., Wang Y.X. A method for helical RNA global structure determination in solution using small-angle X-ray scattering and NMR measurements. J Mol Biol 2009.
59. Chen B., Zuo X., Wang Y.X., Dayie T.K. Multiple conformations of SAM-II riboswitch detected with SAXS and NMR spectroscopy. Nucleic Acids Res 2012, 40:3117-3130.
60. Wang X., Wang J., Zuo X. A top-down approach to determining global structures of RNAs in solution using NMR and small-angle X-ray scattering measurements. Nucleic Acids and Molecular Biology 2012, vol 27. Springer. N. Leontis, E. Westhof (Eds.).
61. Wang Y.X., Zuo X.B., Wang J.B., 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.
62. Zuo X., Wang J., Wang X. NMR and SAXS: a perfect marriage and new approach for RNA structure determination. Advances in Biomedical Spectroscopy 2011, vol 3. IOS Press. A.J. Dingley, S.M. Pascal (Eds.).
63. Dethoff E.A., Chugh J., Mustoe A.M., Al-Hashimi H.M. Functional complexity and regulation through RNA dynamics. Nature 2012, 482:322-330.
64. Al-Hashimi H.M., Walter N.G. RNA dynamics: it is about time. Curr Opin Struct Biol 2008, 18:321-329.
65. Sharp P.A. The centrality of RNA. Cell 2009, 136:577-580.
66. Stelzer A.C., Kratz J.D., Zhang Q., Al-Hashimi H.M. RNA dynamics by design: biasing ensembles towards the ligand-bound state. Angew Chem Int Ed Engl 2012, 49:5731-5733.
67. Bailor M.H., Sun X., Al-Hashimi H.M. Topology links RNA secondary structure with global conformation, dynamics, and adaptation. Science 2010, 327:202-206.
68. 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.
69. Zhang Q., Sun X., Watt E.D., Al-Hashimi H.M. Resolving the motional modes that code for RNA adaptation. Science 2006, 311:653-656.
70. Debye P. Zerstreuung von Roentgenstrahlen. Annalen der Physik 1915, 46:809-823.
71. Schwieters C.D., Clore G.M. A physical picture of atomic motions within the Dickerson DNA dodecamer in solution derived from joint ensemble refinement against NMR and large-angle X-ray scattering data. Biochemistry 2007, 46:1152-1166.
72. Bernado P., Mylonas E., Petoukhov M.V., Blackledge M., Svergun D.I. Structural characterization of flexible proteins using small-angle X-ray scattering. J Am Chem Soc 2007, 129:5656-5664.
73. Pelikan M., Hura G.L., Hammel M. Structure and flexibility within proteins as identified through small angle X-ray scattering. Gen Physiol Biophys 2009, 28:174-189.
74. Gopal A., Zhou Z.H., Knobler C.M., Gelbart W.M. Visualizing large RNA molecules in solution. RNA 2012, 18:284-299.
75. Kazantsev A.V., Rambo R.P., Karimpour S., SantaLucia J., Tainer J.A., Pace N.R. Solution structure of RNase P RNA. RNA 2011, 17:1159-1171.
76. Perard J., Leyrat C., Baudin F., Drouet E., Jamin M. Structure of the full-length HCV IRES in solution. Nat Commun 2013, 4:1612.
77. Ribeiro Ede A., Beich-Frandsen M., Konarev P.V., Shang W., Vecerek B., Kontaxis G., Hammerle H., Peterlik H., Svergun D.I., Blasi U., et al. Structural flexibility of RNA as molecular basis for Hfq chaperone function. Nucleic Acids Res 2012, 40:8072-8084.
78. Pollack L. SAXS studies of ion-nucleic acid interactions. Annu Rev Biophys 2011, 40:225-242.
79. Ducruix A., Guilloteau J.P., Riès-Kautt M., Tardieu A. Protein interactions as seen by solution X-ray scattering prior to crystallogenesis. J Cryst Growth 1996, 168:28-39.
80. Putnam C.D., Hammel M., Hura G.L., Tainer J.A. SAXS combined with crystallography and computation: defining accurate macromolecular structures conformations and assemblies in solution. Q Rev Biophys 2007, 40:191-285.
81. Konarev P.V., Volkov V.V., Sokolova A.V., Koch M.H.J., Svergun D.I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J ApplCrystallogr 2003, 36:1277-1282.
82. Petoukhov M.V., Franke D., Shkumatov A.V., Tria G., Kikhney A.G., Gajda M., Gorba C., Mertens H.D.T., Konarev P.V., Svergun D.I. New developments in the ATSAS program package for small-angle scattering data analysis. J ApplCrystallogr 2012, 45:342-350.
83. Schwieters C.D., Kuszewski J.J., Clore G.M. Using Xplor-NIH for NMR molecular structure determination. Prog Nucl Magn Reson Spectrosc 2006, 48:47-62.
84. Svergun D., Barberato C., Koch M.H.J. CRYSOL-a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J ApplCrystallogr 1995, 28:768-773.
85. Schneidman-Duhovny D., Hammel M., Sali A. FoXS: a web server for rapid computation and fitting of SAXS profiles. Nucleic Acids Res 2010, 38:W540-W544.
86. Pollack L., Doniach S. Time-resolved X-ray scattering and RNA folding. Methods Enzymol 2009, 469:253-268.
87. Pollack L. Time resolved SAXS and RNA folding. Biopolymers 2011, 95:543-549.
88. Kwok L.W., Shcherbakova I., Lamb J.S., Park H.Y., Andresen K., Smith H., Brenowitz M., Pollack L. Concordant exploration of the kinetics of RNA folding from global and local perspectives. J Mol Biol 2006, 355:282-293.
89. Graceffa R., Nobrega R.P., Barrea R.A., Kathuria S.V., Chakravarthy S., Bilsel O., Irving T.C. Sub-millisecond time-resolved SAXS using a continuous-flow mixer and X-ray microbeam. J Synchrotron Radiat 2013, 20:820-825.
90. 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.
91. Hennig J., Wang I., Sonntag M., Gabel F., Sattler M. Combining NMR and small angle X-ray and neutron scattering in the structural analysis of a ternary protein-RNA complex. J Biomol NMR 2013, 56:17-30.
92. Gupta K., Contreras L.M., Smith D., Qu G., Huang T., Spruce L.A., Seeholzer S.H., Belfort M., Van Duyne G.D. Quaternary arrangement of an active, native group II intron ribonucleoprotein complex revealed by small-angle X-ray scattering. Nucleic Acids Res 2014, 42:5347-5360.
93. Chapman H.N. X-ray imaging beyond the limits. Nat Mater 2009, 8:299-301.
94. Arnlund D., Johansson L.C., Wickstrand C., Barty A., Williams G.J., Malmerberg E., Davidsson J., Milathianaki D., DePonte D.P., Shoeman R.L., et al. Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser. Nat Methods 2014, 11:923-926.
95. Jonikas M.A., Radmer R.J., Laederach A., Das R., Pearlman S., Herschlag D., Altman R.B. Coarse-grained modeling of large RNA molecules with knowledge-based potentials and structural filters. RNA 2009, 15:189-199.