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Review

Taming free energy landscapes with RNA chaperones

Pages 677-686 | Published online: 01 Nov 2010

References

  • Herschlag D. RNA chaperones and the RNA folding problem. J Biol Chem 1995; 270:77 - 79
  • Thirumalai D, Hyeon C. RNA and protein folding: common themes and variations. Biochemistry 2005; 44:4957 - 4970
  • Chen SJ. RNA folding: conformational statistics, folding kinetics and ion electrostatics. Annu Rev Biophys 2008; 37:197 - 214
  • Weeks KM. Protein-facilitated RNA folding. Curr Opin Struct Biol 1997; 7:336 - 342
  • Rajkowitsch L, Chen D, Stampfl S, Semrad K, Waldsich C, Mayer O, et al. RNA chaperones, RNA annealers and RNA helicases. RNA Biol 2007; 4:118 - 130
  • Wolin SL, Wurtmann EJ. Molecular chaperones and quality control in noncoding RNA biogenesis. Cold Spring Harbor Symp Quant Biol 2006; 71:505 - 511
  • Staley JP, Woolford JL Jr. Assembly of ribosomes and spliceosomes: complex ribonucleoprotein machines. Curr Opin Cell Biol 2009; 21:109 - 118
  • Zuniga S, Sola I, Cruz JL, Enjuanes L. Role of RNA chaperones in virus replication. Virus Res 2009; 139:253 - 266
  • Lafontaine DL. A ‘garbage can’ for ribosomes: how eukaryotes degrade their ribosomes. Trends Biochem Sci 2010; 35:267 - 277
  • Brion P, Westhof E. Hierarchy and dynamics of RNA folding. Annu Rev Biophys Biomol Struct 1997; 26:113 - 137
  • Tinoco IJ, Bustamante C. How RNA folds. J Mol Biol 1999; 293:271 - 281
  • Lescoute A, Leontis NB, Massire C, Westhof E. Recurrent structural RNA motifs, Isostericity Matrices and sequence alignments. Nucleic Acids Res 2005; 33:2395 - 2409
  • Shcherbakova I, Mitra S, Laederach A, Brenowitz M. Energy barriers, pathways and dynamics during folding of large, multidomain RNAs. Curr Opin Chem Biol 2008; 12:655 - 666
  • Sosnick TR. Kinetic barriers and the role of topology in protein and RNA folding. Protein Sci 2008; 17:1308 - 1318
  • Woodson SA. Compact intermediates in RNA folding. Annu Rev Biophys 2010; 39:61 - 77
  • Schultes EA, Spasic A, Mohanty U, Bartel DP. Compact and ordered collapse of randomly generated RNA sequences. Nat Struct Mol Biol 2005;
  • Buchmueller KL, Weeks KM. Near native structure in an RNA collapsed state. Biochemistry 2003; 42:13869 - 13878
  • Das R, Kwok LW, Millett IS, Bai Y, Mills TT, Jacob J, et al. The fastest global events in RNA folding: electrostatic relaxation and tertiary collapse of the Tetrahymena ribozyme. J Mol Biol 2003; 332:311 - 319
  • Takamoto K, Das R, He Q, Doniach S, Brenowitz M, Herschlag D, et al. Principles of RNA compaction: insights from the equilibrium folding pathway of the P4-P6 RNA domain in monovalent cations. J Mol Biol 2004; 343:1195 - 1206
  • Chauhan S, Caliskan G, Briber RM, Perez-Salas U, Rangan P, Thirumalai D, et al. RNA tertiary interactions mediate native collapse of a bacterial group I ribozyme. J Mol Biol 2005; 353:1199 - 1209
  • Chauhan S, Woodson SA. Tertiary interactions determine the accuracy of RNA folding. J Am Chem Soc 2008; 130:1296 - 1303
  • Lescoute A, Westhof E. The interaction networks of structured RNAs. Nucleic Acids Res 2006; 34:6587 - 6604
  • Rupert PB, Ferre-D'Amare AR. Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature 2001; 410:780 - 786
  • Pljevaljcic G, Klostermeier D, Millar DP. The tertiary structure of the hairpin ribozyme is formed through a slow conformational search. Biochemistry 2005; 44:4870 - 4876
  • Williamson JR. Induced fit in RNA-protein recognition. Nat Struct Biol 2000; 7:834 - 837
  • Wu M, Tinoco I Jr. RNA folding causes secondary structure rearrangement. Proc Natl Acad Sci USA 1998; 95:11555 - 11560
  • Andersen AA, Collins RA. Intramolecular secondary structure rearrangement by the kissing interaction of the Neurospora VS ribozyme. Proc Natl Acad Sci USA 2001; 98:7730 - 7735
  • Gluick TC, Gerstner RB, Draper DE. Effects of Mg2+, K+ and H+ on an equilibrium between alternative conformations of an RNA pseudoknot. J Mol Biol 1997; 270:451 - 463
  • Thirumalai D, Woodson SA. Kinetics of folding of protein and RNA. Acc Chem Res 1996; 29:433 - 439
  • Onuchic JN, Luthey-Schulten Z, Wolynes PG. Theory of protein folding: the energy landscape perspective. Annu Rev Phys Chem 1997; 48:545 - 600
  • Liphardt J, Onoa B, Smith SB, Tinoco IJ, Bustamante C. Reversible unfolding of single RNA molecules by mechanical force. Science 2001; 292:733 - 737
  • Woodside MT, Anthony PC, Behnke-Parks WM, Larizadeh K, Herschlag D, Block SM. Direct measurement of the full, sequence-dependent folding landscape of a nucleic acid. Science 2006; 314:1001 - 1004
  • Zhang W, Chen SJ. RNA hairpin-folding kinetics. Proc Natl Acad Sci USA 2002; 99:1931 - 1936
  • Ma H, Proctor DJ, Kierzek E, Kierzek R, Bevilacqua PC, Gruebele M. Exploring the energy landscape of a small RNA hairpin. J Am Chem Soc 2006; 128:1523 - 1530
  • Hyeon C, Dima RI, Thirumalai D. Size, shape and flexibility of RNA structures. J Chem Phys 2006; 125:194905
  • Go N. Theoretical studies of protein folding. Annu Rev Biophys Bioeng 1983; 12:183 - 210
  • Crothers DM, Cole PE, Hilbers CW, Shulman RG. The molecular mechanism of thermal unfolding of Escherichia coli formylmethionine transfer RNA. J Mol Biol 1974; 87:63 - 88
  • Kuznetsov SV, Ren CC, Woodson SA, Ansari A. Loop dependence of the stability and dynamics of nucleic acid hairpins. Nucleic Acids Res 2008; 36:1098 - 1112
  • Zarrinkar PP, Williamson JR. The kinetic folding pathway of the Tetrahymena ribozyme reveals possible similarities between RNA and protein folding. Nat Struct Biol 1996; 3:432 - 438
  • Sclavi B, Sullivan M, Chance MR, Brenowitz M, Woodson SA. RNA folding at millisecond intervals by synchrotron hydroxyl radical footprinting. Science 1998; 279:1940 - 1943
  • Treiber DK, Williamson JR. Exposing the kinetic traps in RNA folding. Curr Opin Struct Biol 1999; 9:339 - 345
  • Chen SJ, Dill KA. RNA folding energy landscapes. Proc Natl Acad Sci USA 2000; 97:646 - 651
  • Bokinsky G, Zhuang X. Single-molecule RNA folding. Acc Chem Res 2005; 38:566 - 573
  • Aleman EA, Lamichhane R, Rueda D. Exploring RNA folding one molecule at a time. Curr Opin Chem Biol 2008; 12:647 - 654
  • Fang XW, Pan T, Sosnick TR. Mg2+-dependent folding of a large ribozyme without kinetic traps. Nat Struct Biol 1999; 6:1091 - 1095
  • Hiley SL, Collins RA. Rapid formation of a solvent-inaccessible core in the Neurospora Varkud satellite ribozyme. EMBO J 2001; 20:5461 - 5469
  • Rangan P, Masquida B, Westhof E, Woodson SA. Assembly of core helices and rapid tertiary folding of a small bacterial group I ribozyme. Proc Natl Acad Sci USA 2003; 100:1574 - 1579
  • Woodson SA. Recent insights on RNA folding mechanisms from catalytic RNA. Cell Mol Life Sci 2000; 57:796 - 808
  • Pan J, Thirumalai D, Woodson SA. Folding of RNA involves parallel pathways. J Mol Biol 1997; 273:7 - 13
  • Pan J, Woodson SA. Folding intermediates of a self-splicing RNA: mispairing of the catalytic core. J Mol Biol 1998; 280:597 - 609
  • Pan J, Deras ML, Woodson SA. Fast folding of a ribozyme by stabilizing core interactions: evidence for multiple folding pathways in RNA. J Mol Biol 2000; 296:133 - 144
  • Zhuang X, Bartley LE, Babcock HP, Russell R, Ha T, Herschlag D, et al. A single-molecule study of RNA catalysis and folding. Science 2000; 288:2048 - 2051
  • Zarrinkar PP, Williamson JR. Kinetic intermediates in RNA folding. Science 1994; 265:918 - 924
  • Treiber DK, Rook MS, Zarrinkar PP, Williamson JR. Kinetic intermediates trapped by native interactions in RNA folding. Science 1998; 279:1943 - 1946
  • Treiber DK, Williamson JR. Concerted kinetic folding of a multidomain ribozyme with a disrupted loopreceptor interaction. J Mol Biol 2001; 305:11 - 21
  • Russell R, Zhuang X, Babcock HP, Millett IS, Doniach S, Chu S, et al. Exploring the folding landscape of a structured RNA. Proc Natl Acad Sci USA 2002; 99:155 - 160
  • Pan J, Woodson SA. The effect of long-range loop-loop interactions on folding of the Tetrahymena self-splicing RNA. J Mol Biol 1999; 294:955 - 965
  • Heilman-Miller SL, Woodson SA. Effect of transcription on folding of the Tetrahymena ribozyme. RNA 2003; 9:722 - 733
  • Lease RA, Adilakshmi T, Heilman-Miller S, Woodson SA. Communication between RNA folding domains revealed by folding of circularly permuted ribozymes. J Mol Biol 2007; 373:197 - 210
  • Thirumalai D, Woodson SA. Maximizing RNA folding rates: a balancing act. RNA 2000; 6:790 - 794
  • Russell R, Das R, Suh H, Travers KJ, Laederach A, Engelhardt MA, et al. The paradoxical behavior of a highly structured misfolded intermediate in RNA folding. J Mol Biol 2006; 363:531 - 544
  • Rook MS, Treiber DK, Williamson JR. Fast folding mutants of the Tetrahymena group I ribozyme reveal a rugged folding energy landscape. J Mol Biol 1998; 281:609 - 620
  • Mortimer SA, Weeks KM. C2′-endo nucleotides as molecular timers suggested by the folding of an RNA domain. Proc Natl Acad Sci USA 2009; 106:15622 - 15627
  • Ditzler MA, Rueda D, Mo J, Hakansson K, Walter NG. A rugged free energy landscape separates multiple functional RNA folds throughout denaturation. Nucleic Acids Res 2008; 36:7088 - 7099
  • Schroeder R, Barta A, Semrad K. Strategies for RNA folding and assembly. Nat Rev Mol Cell Biol 2004; 5:908 - 919
  • Russell R. RNA misfolding and the action of chaperones. Front Biosci 2008; 13:1 - 20
  • Karpel RL, Miller NS, Fresco JR. Mechanistic studies of ribonucleic acid renaturation by a helix-destabilizing protein. Biochemistry 1982; 21:2102 - 2108
  • Tsuchihashi Z, Brown PO. DNA strand exchange and selective DNA annealing promoted by the human immunodeficiency virus type 1 nucleocapsid protein. J Virol 1994; 68:5863 - 5870
  • Williams MC, Rouzina I, Wenner JR, Gorelick RJ, Musier-Forsyth K, Bloomfield VA. Mechanism for nucleic acid chaperone activity of HIV-1 nucleocapsid protein revealed by single molecule stretching. Proc Natl Acad Sci USA 2001; 98:6121 - 6126
  • Tijerina P, Bhaskaran H, Russell R. Nonspecific binding to structured RNA and preferential unwinding of an exposed helix by the CYT-19 protein, a DEAD-box RNA chaperone. Proc Natl Acad Sci USA 2006; 103:16698 - 16703
  • Pan T, Sosnick TR. Intermediates and kinetic traps in the folding of a large ribozyme revealed by circular dichroism and UV absorbance spectroscopies and catalytic activity. Nat Struct Biol 1997; 4:931 - 938
  • Karpel RL, Swistel DG, Miller NS, Geroch ME, Lu C, Fresco JR. Acceleration of RNA renaturation by nucleic acid unwinding proteins. Brookhaven Symp Biol 1975; 165 - 174
  • Thomas JA, Gorelick RJ. Nucleocapsid protein function in early infection processes. Virus Res 2008; 134:39 - 63
  • Levin JG, Guo J, Rouzina I, Musier-Forsyth K. Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog Nucleic Acid Res Mol Biol 2005; 80:217 - 286
  • Tsuchihashi Z, Khosla M, Herschlag D. Protein enhancement of hammerhead ribozyme catalysis. Science 1993; 262:99 - 102
  • Herschlag D, Khosla M, Tsuchihashi Z, Karpel RL. An RNA chaperone activity of non-specific RNA binding proteins in hammerhead ribozyme catalysis. EMBO J 1994; 13:2913 - 2924
  • Zhang A, Derbyshire V, Salvo JL, Belfort M. Escherichia coli protein StpA stimulates self-splicing by promoting RNA assembly in vitro. RNA 1995; 1:783 - 793
  • Clodi E, Semrad K, Schroeder R. Assaying RNA chaperone activity in vivo using a novel RNA folding trap. EMBO J 1999; 18:3776 - 3782
  • Waldsich C, Grossberger R, Schroeder R. RNA chaperone StpA loosens interactions of the tertiary structure in the td group I intron in vivo. Genes Dev 2002; 16:2300 - 2312
  • Coetzee T, Herschlag D, Belfort M. Escherichia coli proteins, including ribosomal protein S12, facilitate in vitro splicing of phage T4 introns by acting as RNA chaperones. Genes Dev 1994; 8:1575 - 1588
  • Rajkowitsch L, Schroeder R. Dissecting RNA chaperone activity. RNA 2007; 13:2053 - 2060
  • Pannone BK, Xue D, Wolin SL. A role for the yeast La protein in U6 snRNP assembly: evidence that the La protein is a molecular chaperone for RNA polymerase III transcripts. EMBO J 1998; 17:7442 - 7453
  • Stein AJ, Fuchs G, Fu C, Wolin SL, Reinisch KM. Structural insights into RNA quality control: the Ro autoantigen binds misfolded RNAs via its central cavity. Cell 2005; 121:529 - 539
  • Belisova A, Semrad K, Mayer O, Kocian G, Waigmann E, Schroeder R, et al. RNA chaperone activity of protein components of human Ro RNPs. RNA 2005; 11:1084 - 1094
  • Zhang A, Wassarman KM, Ortega J, Steven AC, Storz G. The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 2002; 9:11 - 22
  • Moller T, Franch T, Hojrup P, Keene DR, Bachinger HP, Brennan RG, et al. Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. Mol Cell 2002; 9:23 - 30
  • Moll I, Leitsch D, Steinhauser T, Blasi U. RNA chaperone activity of the Sm-like Hfq protein. EMBO Rep 2003; 4:284 - 289
  • Hopkins JF, Panja S, McNeil SA, Woodson SA. Effect of salt and RNA structure on annealing and strand displacement by Hfq. Nucleic Acids Res 2009; 37:6205 - 6213
  • Solem A, Zingler N, Pyle AM. A DEAD protein that activates intron self-splicing without unwinding RNA. Mol Cell 2006; 24:611 - 617
  • Mohr S, Stryker JM, Lambowitz AM. A DEAD-box protein functions as an ATP-dependent RNA chaperone in group I intron splicing. Cell 2002; 109:769 - 779
  • Bhaskaran H, Russell R. Kinetic redistribution of native and misfolded RNAs by a DEAD-box chaperone. Nature 2007; 449:1014 - 1018
  • Del Campo M, Tijerina P, Bhaskaran H, Mohr S, Yang Q, Jankowsky E, et al. Do DEAD-box proteins promote group II intron splicing without unwinding RNA?. Mol Cell 2007; 28:159 - 166
  • Fedorova O, Solem A, Pyle AM. Protein-facilitated folding of group II intron ribozymes. J Mol Biol 2010; 397:799 - 813
  • Mayer O, Rajkowitsch L, Lorenz C, Konrat R, Schroeder R. RNA chaperone activity and RNA-binding properties of the E. coli protein StpA. Nucleic Acids Res 2007; 35:1257 - 1269
  • Cruceanu M, Gorelick RJ, Musier-Forsyth K, Rouzina I, Williams MC. Rapid kinetics of protein-nucleic acid interaction is a major component of HIV-1 nucleocapsid protein's nucleic acid chaperone function. J Mol Biol 2006; 363:867 - 877
  • Grossberger R, Mayer O, Waldsich C, Semrad K, Urschitz S, Schroeder R. Influence of RNA structural stability on the RNA chaperone activity of the Escherichia coli protein StpA. Nucleic Acids Res 2005; 33:2280 - 2289
  • Pyle AM. Translocation and unwinding mechanisms of RNA and DNA helicases. Annu Rev Biophys 2008; 37:317 - 336
  • Hilbert M, Karow AR, Klostermeier D. The mechanism of ATP-dependent RNA unwinding by DEAD box proteins. Biol Chem 2009; 390:1237 - 1250
  • Diges CM, Uhlenbeck OC. Escherichia coli DbpA is an RNA helicase that requires hairpin 92 of 23S rRNA. EMBO J 2001; 20:5503 - 5512
  • Jankowsky E, Gross CH, Shuman S, Pyle AM. Active disruption of an RNA-protein interaction by a DExH/D RNA helicase. Science 2001; 291:121 - 125
  • Linder P. Dead-box proteins: a family affair—active and passive players in RNP-remodeling. Nucleic Acids Res 2006; 34:4168 - 4180
  • Jankowsky E, Bowers H. Remodeling of ribonucleoprotein complexes with DExH/D RNA helicases. Nucleic Acids Res 2006; 34:4181 - 4188
  • Yang Q, Jankowsky E. ATP- and ADP-dependent modulation of RNA unwinding and strand annealing activities by the DEAD-box protein DED1. Biochemistry 2005; 44:13591 - 13601
  • Kaczanowska M, Ryden-Aulin M. Ribosome biogenesis and the translation process in Escherichia coli. Microbiol Mol Biol Rev 2007; 71:477 - 494
  • Kressler D, Hurt E, Bassler J. Driving ribosome assembly. Biochim Biophys Acta 2010; 1803:673 - 683
  • Banroques J, Doere M, Dreyfus M, Linder P, Tanner NK. Motif III in superfamily 2 “helicases” helps convert the binding energy of ATP into a high-affinity RNA binding site in the yeast DEAD-box protein Ded1. J Mol Biol 2010; 396:949 - 966
  • Chen Y, Potratz JP, Tijerina P, Del Campo M, Lambowitz AM, Russell R. DEAD-box proteins can completely separate an RNA duplex using a single ATP. Proc Natl Acad Sci USA 2008; 105:20203 - 20208
  • Liu F, Putnam A, Jankowsky E. ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding. Proc Natl Acad Sci USA 2008; 105:20209 - 20214
  • Lorsch JR, Herschlag D. The DEAD box protein eIF4A. 1. A minimal kinetic and thermodynamic framework reveals coupled binding of RNA and nucleotide. Biochemistry 1998; 37:2180 - 2193
  • Sengoku T, Nureki O, Nakamura A, Kobayashi S, Yokoyama S. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 2006; 125:287 - 300
  • Del Campo M, Lambowitz AM. Structure of the Yeast DEAD box protein Mss116p reveals two wedges that crimp RNA. Mol Cell 2009; 35:598 - 609
  • Karow AR, Klostermeier D. A conformational change in the helicase core is necessary but not sufficient for RNA unwinding by the DEAD box helicase YxiN. Nucleic Acids Res 2009; 37:4464 - 4471
  • Li PT, Bustamante C, Tinoco I Jr. Unusual mechanical stability of a minimal RNA kissing complex. Proc Natl Acad Sci USA 2006; 103:15847 - 15852
  • Mohr G, Del Campo M, Mohr S, Yang Q, Jia H, Jankowsky E, et al. Function of the C-terminal domain of the DEAD-box protein Mss116p analyzed in vivo and in vitro. J Mol Biol 2008; 375:1344 - 1364
  • Woodson SA. Metal ions and RNA folding: a highly charged topic with a dynamic future. Curr Opin Chem Biol 2005; 9:104 - 109
  • Draper DE, Grilley D, Soto AM. Ions and RNA folding. Annu Rev Biophys Biomol Struct 2005; 34:221 - 243
  • Thomas TJ, Bloomfield VA. Ionic and structural effects on the thermal helix-coil transition of DNA complexed with natural and synthetic polyamines. Biopolymers 1984; 23:1295 - 1306
  • Rouzina I, Bloomfield VA. Influence of ligand spatial organization on competitive electrostatic binding to DNA. J Phys Chem 1996; 100:4305 - 4313
  • Koculi E, Hyeon C, Thirumalai D, Woodson SA. Charge density of divalent metal cations determines RNA stability. J Am Chem Soc 2007; 129:2676 - 2682
  • Moghaddam S, Caliskan G, Chauhan S, Hyeon C, Briber RM, Thirumalai D, et al. Metal ion dependence of cooperative collapse transitions in RNA. J Mol Biol 2009; 393:753 - 764
  • Heilman-Miller SL, Pan J, Thirumalai D, Woodson SA. Counterion condensation in folding of the Tetrahymena ribozyme. II. Counterion dependence of folding kinetics. J Mol Biol 2001; 309:57 - 68
  • Koculi E, Thirumalai D, Woodson SA. Counterion charge density determines the position and plasticity of RNA folding transition states. J Mol Biol 2006; 359:446 - 454
  • Fang XW, Thiyagarajan P, Sosnick TR, Pan T. The rate-limiting step in the folding of a large ribozyme without kinetic traps. Proc Natl Acad Sci USA 2002; 99:8518 - 8523
  • Brown TS, Chadalavada DM, Bevilacqua PC. Design of a highly reactive HDV ribozyme sequence uncovers facilitation of RNA folding by alternative pairings and physiological ionic strength. J Mol Biol 2004; 341:695 - 712
  • Record MT Jr, Anderson CF, Lohman TM. Thermodynamic analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids: the roles of ion association or release, screening and ion effects on water activity. Q Rev Biophys 1978; 11:103 - 178
  • Draper DE. Themes in RNA-protein recognition. J Mol Biol 1999; 293:255 - 270
  • Vo MN, Barany G, Rouzina I, Musier-Forsyth K. Effect of Mg(2+) and Na(+) on the nucleic acid chaperone activity of HIV-1 nucleocapsid protein: implications for reverse transcription. J Mol Biol 2009; 386:773 - 788
  • Tompa P, Kovacs D. Intrinsically disordered chaperones in plants and animals. Biochem Cell Biol 2010; 88:167 - 174
  • Thirumalai D, Lee N, Woodson SA, Klimov D. Early events in RNA folding. Annu Rev Phys Chem 2001; 52:751 - 762
  • Heilman-Miller SL, Thirumalai D, Woodson SA. Role of counterion condensation in folding of the Tetrahymena ribozyme. I. Equilibrium stabilization by cations. J Mol Biol 2001; 306:1157 - 1166
  • Webb AE, Weeks KM. A collapsed state functions to self-chaperone RNA folding into a native ribonucleoprotein complex. Nat Struct Biol 2001; 8:135 - 140
  • Su LJ, Brenowitz M, Pyle AM. An alternative route for the folding of large RNAs: apparent two-state folding by a group II intron ribozyme. J Mol Biol 2003; 334:639 - 652
  • Laederach A, Shcherbakova I, Jonikas MA, Altman RB, Brenowitz M. Distinct contribution of electrostatics, initial conformational ensemble and macromolecular stability in RNA folding. Proc Natl Acad Sci USA 2007; 104:7045 - 7050
  • Roh JH, Guo L, Kilburn JD, Briber RM, Irving T, Woodson SA. Multistage collapse of a bacterial ribozyme observed by time-resolved small-angle X-ray scattering. J Am Chem Soc 2010; 132:10148 - 10154
  • Woodside MT, Garcia-Garcia C, Block SM. Folding and unfolding single RNA molecules under tension. Curr Opin Chem Biol 2008; 12:640 - 646
  • Li PT, Vieregg J, Tinoco I Jr. How RNA unfolds and refolds. Annu Rev Biochem 2008; 77:77 - 100
  • Li PT, Collin D, Smith SB, Bustamante C, Tinoco I Jr. Probing the mechanical folding kinetics of TAR RNA by hopping, force-jump and force-ramp methods. Biophys J 2006; 90:250 - 260
  • Li PT, Bustamante C, Tinoco I Jr. Real-time control of the energy landscape by force directs the folding of RNA molecules. Proc Natl Acad Sci USA 2007; 104:7039 - 7044
  • Hyeon C, Thirumalai D. Mechanical unfolding of RNA: from hairpins to structures with internal multiloops. Biophys J 2007; 92:731 - 743
  • Bokinsky G, Nivon LG, Liu S, Chai G, Hong M, Weeks KM, et al. Two distinct binding modes of a protein cofactor with its target RNA. J Mol Biol 2006; 361:771 - 784
  • Adilakshmi T, Bellur DL, Woodson SA. Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly. Nature 2008; 455:1268 - 1272
  • Wagner EG, Altuvia S, Romby P. Antisense RNAs in bacteria and their genetic elements. Adv Genet 2002; 46:361 - 398
  • Geissmann TA, Touati D. Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J 2004; 23:396 - 405
  • Arluison V, Hohng S, Roy R, Pellegrini O, Regnier P, Ha T. Spectroscopic observation of RNA chaperone activities of Hfq in post-transcriptional regulation by a small non-coding RNA. Nucleic Acids Res 2007; 35:999 - 1006
  • Soper TJ, Woodson SA. The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 2008; 14:1907 - 1917
  • Vo MN, Barany G, Rouzina I, Musier-Forsyth K. Mechanistic studies of mini-TAR RNA/DNA annealing in the absence and presence of HIV-1 nucleocapsid protein. J Mol Biol 2006; 363:244 - 261
  • Zeng Y, Liu HW, Landes CF, Kim YJ, Ma X, Zhu Y, et al. Probing nucleation, reverse annealing and chaperone function along the reaction path of HIV-1 single-strand transfer. Proc Natl Acad Sci USA 2007; 104:12651 - 12656
  • Bae E, Reiter NJ, Bingman CA, Kwan SS, Lee D, Phillips GN Jr, et al. Structure and interactions of the first three RNA recognition motifs of splicing factor prp24. J Mol Biol 2007; 367:1447 - 1458
  • Mikulecky PJ, Kaw MK, Brescia CC, Takach JC, Sledjeski DD, Feig AL. Escherichia coli Hfq has distinct interaction surfaces for DsrA, rpoS and poly(A) RNAs. Nat Struct Mol Biol 2004; 11:1206 - 1214
  • Fuchs G, Stein AJ, Fu C, Reinisch KM, Wolin SL. Structural and biochemical basis for misfolded RNA recognition by the Ro autoantigen. Nat Struct Mol Biol 2006; 13:1002 - 1009
  • Storz G, Opdyke JA, Zhang A. Controlling mRNA stability and translation with small, noncoding RNAs. Curr Opin Microbiol 2004; 7:140 - 144
  • Heilman-Miller SL, Wu T, Levin JG. Alteration of nucleic acid structure and stability modulates the efficiency of minus-strand transfer mediated by the HIV-1 nucleocapsid protein. J Biol Chem 2004; 279:44154 - 44465
  • Nikolcheva T, Woodson SA. Facilitation of group I splicing in vivo: misfolding of the Tetrahymena IVS and the role of ribosomal RNA exons. J Mol Biol 1999; 292:557 - 567
  • Brion P, Schroede rR, Michel F, Westhof E. Influence of specific mutations on the thermal stability of the td group I intron in vitro and on its splicing efficiency in vivo: A comparative study. RNA 1999; 5:947 - 958
  • Mahen EM, Harger JW, Calderon EM, Fedor MJ. Kinetics and thermodynamics make different contributions to RNA folding in vitro and in yeast. Mol Cell 2005; 19:27 - 37
  • Koduvayur SP, Woodson SA. Intracellular folding of the Tetrahymena group I intron depends on exon sequence and promoter choice. RNA 2004; 10:1526 - 1532
  • Jackson SA, Koduvayur S, Woodson SA. Self-splicing of a group I intron reveals partitioning of native and misfolded RNA populations in yeast. RNA 2006; 12:2149 - 2159
  • Nikolcheva T, Woodson SA. Facilitation of group I splicing in vivo: misfolding of the Tetrahymena IVS and the role of ribosomal RNA exons. J Mol Biol 1999; 292:557 - 567
  • Mahen EM, Watson PY, Cottrell JW, Fedor MJ. mRNA secondary structures fold sequentially but exchange rapidly in vivo. PLoS Biol 2010; 8:1000307
  • Pan T, Artsimovitch I, Fang XW, Landick R, Sosnick TR. Folding of a large ribozyme during transcription and the effect of the elongation factor NusA. Proc Natl Acad Sci USA 1999; 96:9545 - 9550
  • Wong TN, Sosnick TR, Pan T. Folding of noncoding RNAs during transcription facilitated by pausing-induced nonnative structures. Proc Natl Acad Sci USA 2007; 104:17995 - 18000
  • Grundy FJ, Henkin TM. Regulation of gene expression by effectors that bind to RNA. Curr Opin Microbiol 2004; 7:126 - 131
  • Pan T, Sosnick T. RNA folding during transcription. Annu Rev Biophys Biomol Struct 2006; 35:161 - 175
  • Granneman S, Baserga SJ. Crosstalk in gene expression: coupling and co-regulation of rDNA transcription, pre-ribosome assembly and pre-rRNA processing. Curr Opin Cell Biol 2005; 17:281 - 286
  • Henras AK, Soudet J, Gerus M, Lebaron S, Caizergues-Ferrer M, Mougin A, et al. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci 2008; 65:2334 - 2359
  • Holmes KL, Culver GM. Mapping structural differences between 30S ribosomal subunit assembly intermediates. Nat Struct Mol Biol 2004; 11:179 - 186
  • Dammel CS, Noller HF. A cold-sensitive mutation in 16S rRNA provides evidence for helical switching in ribosome assembly. Genes Dev 1993; 7:660 - 670
  • Pardon B, Wagner R. The Escherichia coli ribosomal RNA leader nut region interacts specifically with mature 16S RNA. Nucleic Acids Res 1995; 23:932 - 941
  • Granneman S, Baserga SJ. Ribosome biogenesis: of knobs and RNA processing. Exp Cell Res 2004; 296:43 - 50
  • Beltrame M, Tollervey D. Base pairing between U3 and the pre-ribosomal RNA is required for 18S rRNA synthesis. EMBO J 1995; 14:4350 - 4356
  • Borovjagin AV, Gerbi SA. Xenopus U3 snoRNA docks on pre-rRNA through a novel base-pairing interaction. RNA 2004; 10:942 - 953
  • Granneman S, Tollervey D. Building ribosomes: even more expensive than expected?. Curr Biol 2007; 17:415 - 417
  • Karbstein K. The role of GTPases in ribosome assembly. Biopolymers 2007; 87:1 - 11

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