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Chapter 22 : Proteins That Chaperone RNA Regulation

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Abstract:

Noncoding RNA sequences fold into useful structures that regulate gene expression as ribozymes, metabolite-binding sensors, or antisense RNAs ( ). These regulatory RNAs are chaperoned by diverse families of RNA-binding proteins, and the loss of RNA chaperone proteins can lead to impaired growth, reduced tolerance to stress, and reduced virulence ( ). RNA chaperones also facilitate conformational rearrangements during ribosome biogenesis ( ) and eukaryotic pre-mRNA splicing ( ).

Citation: Woodson S, Panja S, Santiago-Frangos A. 2019. Proteins That Chaperone RNA Regulation, p 385-397. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0026-2018
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Figure 1

Iterative annealing of RNA by chaperones. Typical kinetic mechanism for forming RNA secondary (2D) structure (left) and native tertiary structure (right). Assembly of the double helices (cylinders) into compact intermediates is followed by further reorganization of tertiary interactions to produce the native RNA. Because the RNA may adopt many secondary structures, some molecules fold directly to the native structure (top path) while others become trapped in nonnative structures. In the classic iterative annealing model, chaperones (gold, bottom) bind and partially unfold misfolded intermediates, then release the unfolded RNA to fold again. Adapted from reference with permission.

Citation: Woodson S, Panja S, Santiago-Frangos A. 2019. Proteins That Chaperone RNA Regulation, p 385-397. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0026-2018
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Image of Figure 2
Figure 2

Chaperone-assisted annealing of antisense RNA. Annealing of antisense or -acting sRNAs with a complementary RNA target typically begins with base-pairing between two hairpin loops (kissing complex) or a loop and a single strand (middle path). This is followed by extension of base-pairing, which often requires refolding of adjacent sequences. HIV nucleocapsid (NCp7) and Rom/Rop promote annealing by disrupting secondary structure in each RNA, lowering the energetic barriers for extending the antisense interactions (top path). NCp7 can also aggregate RNA strands to speed up initiation of base-pairing. Hfq facilitates sRNA-mRNA base-pairing by forming a ternary complex with both RNAs that increases the rate of helix nucleation (bottom path). Hfq can also favor antisense base-pairing by restructuring one or both RNAs.

Citation: Woodson S, Panja S, Santiago-Frangos A. 2019. Proteins That Chaperone RNA Regulation, p 385-397. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0026-2018
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References

/content/book/10.1128/9781683670247.chap22
1. Serganov A,, Patel DJ . 2007. Ribozymes, riboswitches and beyond: regulation of gene expression without proteins. Nat Rev Genet 8 : 776 790.[CrossRef][PubMed]
2. Grundy FJ,, Henkin TM . 2006. From ribosome to riboswitch: control of gene expression in bacteria by RNA structural rearrangements. Crit Rev Biochem Mol Biol 41 : 329 338.[CrossRef][PubMed]
3. Winkler WC,, Breaker RR . 2005. Regulation of bacterial gene expression by riboswitches. Annu Rev Microbiol 59 : 487 517.[CrossRef][PubMed]
4. Beisel CL,, Storz G . 2010. Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 34 : 866 882.[CrossRef][PubMed]
5. Wagner EG,, Romby P . 2015. Small RNAs in bacteria and archaea: who they are, what they do, and how they do it. Adv Genet 90 : 133 208.[CrossRef][PubMed]
6. Chao Y,, Vogel J . 2010. The role of Hfq in bacterial pathogens. Curr Opin Microbiol 13 : 24 33.[CrossRef][PubMed]
7. Gottesman S,, McCullen CA,, Guillier M,, Vanderpool CK,, Majdalani N,, Benhammou J,, Thompson KM,, FitzGerald PC,, Sowa NA,, FitzGerald DJ . 2006. Small RNA regulators and the bacterial response to stress. Cold Spring Harb Symp Quant Biol 71 : 1 11.[CrossRef][PubMed]
8. Romeo T,, Vakulskas CA,, Babitzke P . 2013. Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. Environ Microbiol 15 : 313 324.[CrossRef][PubMed]
9. Sobrero P,, Valverde C . 2012. The bacterial protein Hfq: much more than a mere RNA-binding factor. Crit Rev Microbiol 38 : 276 299.[CrossRef][PubMed]
10. Lucchetti-Miganeh C,, Burrowes E,, Baysse C,, Ermel G . 2008. The post-transcriptional regulator CsrA plays a central role in the adaptation of bacterial pathogens to different stages of infection in animal hosts. Microbiology 154 : 16 29.[CrossRef][PubMed]
11. Romby P,, Vandenesch F,, Wagner EG . 2006. The role of RNAs in the regulation of virulence-gene expression. Curr Opin Microbiol 9 : 229 236.[CrossRef][PubMed]
12. Redder P,, Hausmann S,, Khemici V,, Yasrebi H,, Linder P . 2015. Bacterial versatility requires DEAD-box RNA helicases. FEMS Microbiol Rev 39 : 392 412.[CrossRef][PubMed]
13. Staley JP,, Woolford JL Jr . 2009. Assembly of ribosomes and spliceosomes: complex ribonucleoprotein machines. Curr Opin Cell Biol 21 : 109 118.[CrossRef][PubMed]
14. Phadtare S,, Severinov K . 2010. RNA remodeling and gene regulation by cold shock proteins. RNA Biol 7 : 788 795.[CrossRef][PubMed]
15. Rudan M,, Schneider D,, Warnecke T,, Krisko A . 2015. RNA chaperones buffer deleterious mutations in E. coli. eLife 4 : e04745.[CrossRef][PubMed]
16. Herschlag D . 1995. RNA chaperones and the RNA folding problem. J Biol Chem 270 : 20871 20874.[CrossRef][PubMed]
17. Doetsch M,, Schroeder R,, Fürtig B . 2011. Transient RNA-protein interactions in RNA folding. FEBS J 278 : 1634 1642.[CrossRef][PubMed]
18. Jankowsky E,, Gross CH,, Shuman S,, Pyle AM . 2001. Active disruption of an RNA-protein interaction by a DExH/D RNA helicase. Science 291 : 121 125.[CrossRef][PubMed]
19. Bhaskaran H,, Russell R . 2007. Kinetic redistribution of native and misfolded RNAs by a DEAD-box chaperone. Nature 449 : 1014 1018.[CrossRef][PubMed]
20. Iost I,, Bizebard T,, Dreyfus M . 2013. Functions of DEAD-box proteins in bacteria: current knowledge and pending questions. Biochim Biophys Acta 1829 : 866 877.[CrossRef][PubMed]
21. Updegrove TB,, Zhang A,, Storz G . 2016. Hfq: the flexible RNA matchmaker. Curr Opin Microbiol 30 : 133 138.[CrossRef]
22. Olejniczak M,, Storz G . 2017. ProQ/FinO-domain proteins: another ubiquitous family of RNA matchmakers? Mol Microbiol 104 : 905 915.[CrossRef][PubMed]
23. Bear DG,, Ng R,, Van Derveer D,, Johnson NP,, Thomas G,, Schleich T,, Noller HF . 1976. Alteration of polynucleotide secondary structure by ribosomal protein S1. Proc Natl Acad Sci U S A 73 : 1824 1828.[CrossRef][PubMed]
24. Hajnsdorf E,, Boni IV . 2012. Multiple activities of RNA-binding proteins S1 and Hfq. Biochimie 94 : 1544 1553.[CrossRef][PubMed]
25. Kolb A,, Hermoso JM,, Thomas JO,, Szer W . 1977. Nucleic acid helix-unwinding properties of ribosomal protein S1 and the role of S1 in mRNA binding to ribosomes. Proc Natl Acad Sci U S A 74 : 2379 2383.[CrossRef][PubMed]
26. 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 1588.[CrossRef][PubMed]
27. Herschlag D,, Khosla M,, Tsuchihashi Z,, Karpel RL . 1994. An RNA chaperone activity of non-specific RNA binding proteins in hammerhead ribozyme catalysis. EMBO J 13 : 2913 2924.[PubMed]
28. Levin JG,, Guo J,, Rouzina I,, Musier-Forsyth K . 2005. Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog Nucleic Acid Res Mol Biol 80 : 217 286.[CrossRef]
29. Rein A,, Henderson LE,, Levin JG . 1998. Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem Sci 23 : 297 301.[CrossRef]
30. Bayfield MA,, Yang R,, Maraia RJ . 2010. Conserved and divergent features of the structure and function of La and La-related proteins (LARPs). Biochim Biophys Acta 1799 : 365 378.[CrossRef][PubMed]
31. Sim S,, Wolin SL . 2011. Emerging roles for the Ro 60-kDa autoantigen in noncoding RNA metabolism. Wiley Interdiscip Rev RNA 2 : 686 699.[CrossRef][PubMed]
32. Fürtig B,, Nozinovic S,, Reining A,, Schwalbe H . 2015. Multiple conformational states of riboswitches fine-tune gene regulation. Curr Opin Struct Biol 30 : 112 124.[CrossRef][PubMed]
33. Lau MW,, Ferré-D’Amaré AR . 2016. Many activities, one structure: functional plasticity of ribozyme folds. Molecules 21 : E1570.[CrossRef][PubMed]
34. Krajewski SS,, Narberhaus F . 2014. Temperature-driven differential gene expression by RNA thermosensors. Biochim Biophys Acta 1839 : 978 988.[CrossRef][PubMed]
35. Peer A,, Margalit H . 2014. Evolutionary patterns of Escherichia coli small RNAs and their regulatory interactions. RNA 20 : 994 1003.[CrossRef][PubMed]
36. Kang Z,, Zhang C,, Zhang J,, Jin P,, Zhang J,, Du G,, Chen J . 2014. Small RNA regulators in bacteria: powerful tools for metabolic engineering and synthetic biology. Appl Microbiol Biotechnol 98 : 3413 3424.[CrossRef][PubMed]
37. Trausch JJ,, Batey RT . 2015. Design of modular “plug-and-play” expression platforms derived from natural riboswitches for engineering novel genetically encodable RNA regulatory devices. Methods Enzymol 550 : 41 71.[CrossRef][PubMed]
38. Behrouzi R,, Roh JH,, Kilburn D,, Briber RM,, Woodson SA . 2012. Cooperative tertiary interaction network guides RNA folding. Cell 149 : 348 357.[CrossRef][PubMed]
39. Chauhan S,, Woodson SA . 2008. Tertiary interactions determine the accuracy of RNA folding. J Am Chem Soc 130 : 1296 1303.[CrossRef][PubMed]
40. Thirumalai D,, Hyeon C . 2005. RNA and protein folding: common themes and variations. Biochemistry 44 : 4957 4970.[CrossRef][PubMed]
41. Thirumalai D,, Woodson SA . 1996. Kinetics of folding of protein and RNA. Acc Chem Res 29 : 433 439.[CrossRef]
42. Crothers DM, . 2001. RNA conformational dynamics, p 61 70. In Söll D,, Nishimura S,, Moore P (ed), RNA. Elsevier, Oxford, United Kingdom.
43. Draper DE . 1996. Strategies for RNA folding. Trends Biochem Sci 21 : 145 149.[CrossRef]
44. Zarrinkar PP,, Williamson JR . 1994. Kinetic intermediates in RNA folding. Science 265 : 918 924.[CrossRef]
45. Pan T,, Sosnick TR . 1997. 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 4 : 931 938.[CrossRef][PubMed]
46. Sclavi B,, Sullivan M,, Chance MR,, Brenowitz M,, Woodson SA . 1998. RNA folding at millisecond intervals by synchrotron hydroxyl radical footprinting. Science 279 : 1940 1943.[CrossRef][PubMed]
47. Lai D,, Proctor JR,, Meyer IM . 2013. On the importance of cotranscriptional RNA structure formation. RNA 19 : 1461 1473.[CrossRef][PubMed]
48. Schroeder R,, Barta A,, Semrad K . 2004. Strategies for RNA folding and assembly. Nat Rev Mol Cell Biol 5 : 908 919.[CrossRef][PubMed]
49. Craig ME,, Crothers DM,, Doty P . 1971. Relaxation kinetics of dimer formation by self complementary oligonucleotides. J Mol Biol 62 : 383 401.[CrossRef]
50. Pörschke D . 1974. A direct measurement of the unzippering rate of a nucleic acid double helix. Biophys Chem 2 : 97 101.[CrossRef]
51. Nordström K,, Wagner EG . 1994. Kinetic aspects of control of plasmid replication by antisense RNA. Trends Biochem Sci 19 : 294 300.[CrossRef]
52. Tomizawa J . 1984. Control of ColE1 plasmid replication: the process of binding of RNA I to the primer transcript. Cell 38 : 861 870.[CrossRef]
53. Persson C,, Wagner EG,, Nordström K . 1990. Control of replication of plasmid R1: formation of an initial transient complex is rate-limiting for antisense RNA-target RNA pairing. EMBO J 9 : 3777 3785.[PubMed]
54. Tamm J,, Polisky B . 1985. Characterization of the ColE1 primer-RNA1 complex: analysis of a domain of ColE1 RNA1 necessary for its interaction with primer RNA. Proc Natl Acad Sci U S A 82 : 2257 2261.[CrossRef][PubMed]
55. Kolb FA,, Engdahl HM,, Slagter-Jäger JG,, Ehresmann B,, Ehresmann C,, Westhof E,, Wagner EG,, Romby P . 2000. Progression of a loop-loop complex to a four-way junction is crucial for the activity of a regulatory antisense RNA. EMBO J 19 : 5905 5915.[CrossRef][PubMed]
56. Tomizawa J . 1990. Control of ColE1 plasmid replication. Interaction of Rom protein with an unstable complex formed by RNA I and RNA II. J Mol Biol 212 : 695 708.[CrossRef]
57. Grossberger R,, Mayer O,, Waldsich C,, Semrad K,, Urschitz S,, Schroeder R . 2005. Influence of RNA structural stability on the RNA chaperone activity of the Escherichia coli protein StpA. Nucleic Acids Res 33 : 2280 2289.[CrossRef][PubMed]
58. Mayer O,, Rajkowitsch L,, Lorenz C,, Konrat R,, Schroeder R . 2007. RNA chaperone activity and RNA-binding properties of the E. coli protein StpA. Nucleic Acids Res 35 : 1257 1269.[CrossRef][PubMed]
59. Woodson SA . 2010. Taming free energy landscapes with RNA chaperones. RNA Biol 7 : 677 686.[CrossRef][PubMed]
60. Tijerina P,, Bhaskaran H,, Russell R . 2006. 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 U S A 103 : 16698 16703.[CrossRef][PubMed]
61. Todd MJ,, Lorimer GH,, Thirumalai D . 1996. Chaperonin-facilitated protein folding: optimization of rate and yield by an iterative annealing mechanism. Proc Natl Acad Sci U S A 93 : 4030 4035.[CrossRef][PubMed]
62. Hyeon C,, Thirumalai D . 2013. Generalized iterative annealing model for the action of RNA chaperones. J Chem Phys 139 : 121924.[CrossRef][PubMed]
63. Chakrabarti S,, Hyeon C,, Ye X,, Lorimer GH,, Thirumalai D . 2017. Molecular chaperones maximize the native state yield on biological times by driving substrates out of equilibrium. Proc Natl Acad Sci U S A 114 : E10919 E10927.[CrossRef][PubMed]
64. Storz G,, Opdyke JA,, Zhang A . 2004. Controlling mRNA stability and translation with small, noncoding RNAs. Curr Opin Microbiol 7 : 140 144.[CrossRef][PubMed]
65. Wagner EG . 2013. Cycling of RNAs on Hfq. RNA Biol 10 : 619 626.[CrossRef][PubMed]
66. Cruceanu M,, Gorelick RJ,, Musier-Forsyth K,, Rouzina I,, Williams MC . 2006. Rapid kinetics of protein-nucleic acid interaction is a major component of HIV-1 nucleocapsid protein’s nucleic acid chaperone function. J Mol Biol 363 : 867 877.[CrossRef][PubMed]
67. Cusick ME,, Belfort M . 1998. Domain structure and RNA annealing activity of the Escherichia coli regulatory protein StpA. Mol Microbiol 28 : 847 857.[CrossRef][PubMed]
68. Moll I,, Leitsch D,, Steinhauser T,, Bläsi U . 2003. RNA chaperone activity of the Sm-like Hfq protein. EMBO Rep 4 : 284 289.[CrossRef][PubMed]
69. Lease RA,, Woodson SA . 2004. Cycling of the Sm-like protein Hfq on the DsrA small regulatory RNA. J Mol Biol 344 : 1211 1223.[CrossRef][PubMed]
70. Rajkowitsch L,, Schroeder R . 2007. Dissecting RNA chaperone activity. RNA 13 : 2053 2060.[CrossRef][PubMed]
71. Hopkins JF,, Panja S,, Woodson SA . 2011. Rapid binding and release of Hfq from ternary complexes during RNA annealing. Nucleic Acids Res 39 : 5193 5202.[CrossRef][PubMed]
72. Adamson DN,, Lim HN . 2011. Essential requirements for robust signaling in Hfq dependent small RNA networks. PLoS Comput Biol 7 : e1002138.[CrossRef][PubMed]
73. Goldstein J,, Pollitt NS,, Inouye M . 1990. Major cold shock protein of Escherichia coli. Proc Natl Acad Sci U S A 87 : 283 287.[CrossRef][PubMed]
74. Jiang W,, Hou Y,, Inouye M . 1997. CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J Biol Chem 272 : 196 202.[CrossRef][PubMed]
75. Phadtare S,, Inouye M,, Severinov K . 2002. The nucleic acid melting activity of Escherichia coli CspE is critical for transcription antitermination and cold acclimation of cells. J Biol Chem 277 : 7239 7245.[CrossRef][PubMed]
76. Phadtare S,, Tadigotla V,, Shin WH,, Sengupta A,, Severinov K . 2006. Analysis of Escherichia coli global gene expression profiles in response to overexpression and deletion of CspC and CspE. J Bacteriol 188 : 2521 2527.[CrossRef][PubMed]
77. Newkirk K,, Feng W,, Jiang W,, Tejero R,, Emerson SD,, Inouye M,, Montelione GT . 1994. Solution NMR structure of the major cold shock protein (CspA) from Escherichia coli: identification of a binding epitope for DNA. Proc Natl Acad Sci U S A 91 : 5114 5118.[CrossRef][PubMed]
78. Schindelin H,, Jiang W,, Inouye M,, Heinemann U . 1994. Crystal structure of CspA, the major cold shock protein of Escherichia coli. Proc Natl Acad Sci U S A 91 : 5119 5123.[CrossRef][PubMed]
79. Phadtare S,, Tyagi S,, Inouye M,, Severinov K . 2002. Three amino acids in Escherichia coli CspE surface-exposed aromatic patch are critical for nucleic acid melting activity leading to transcription antitermination and cold acclimation of cells. J Biol Chem 277 : 46706 46711.[CrossRef][PubMed]
80. Phadtare S,, Inouye M,, Severinov K . 2004. The mechanism of nucleic acid melting by a CspA family protein. J Mol Biol 337 : 147 155.[CrossRef][PubMed]
81. Rennella E,, Sára T,, Juen M,, Wunderlich C,, Imbert L,, Solyom Z,, Favier A,, Ayala I,, Weinhäupl K,, Schanda P,, Konrat R,, Kreutz C,, Brutscher B . 2017. RNA binding and chaperone activity of the E. coli cold-shock protein CspA. Nucleic Acids Res 45 : 4255 4268.[PubMed]
82. Hall KB . 2017. RNA and proteins: mutual respect. F1000 Res 6 : 345.[CrossRef][PubMed]
83. Feng W,, Tejero R,, Zimmerman DE,, Inouye M,, Montelione GT . 1998. Solution NMR structure and backbone dynamics of the major cold-shock protein (CspA) from Escherichia coli: evidence for conformational dynamics in the single-stranded RNA-binding site. Biochemistry 37 : 10881 10896.[CrossRef][PubMed]
84. Tompa P,, Kovacs D . 2010. Intrinsically disordered chaperones in plants and animals. Biochem Cell Biol 88 : 167 174.[CrossRef][PubMed]
85. Darlix JL,, de Rocquigny H,, Mély Y . 2016. The multiple roles of the nucleocapsid in retroviral RNA conversion into proviral DNA by reverse transcriptase. Biochem Soc Trans 44 : 1427 1440.[CrossRef][PubMed]
86. Rein A,, Datta SA,, Jones CP,, Musier-Forsyth K . 2011. Diverse interactions of retroviral Gag proteins with RNAs. Trends Biochem Sci 36 : 373 380.
87. Guo J,, Wu T,, Kane BF,, Johnson DG,, Henderson LE,, Gorelick RJ,, Levin JG . 2002. Subtle alterations of the native zinc finger structures have dramatic effects on the nucleic acid chaperone activity of human immunodeficiency virus type 1 nucleocapsid protein. J Virol 76 : 4370 4378.[CrossRef][PubMed]
88. Heath MJ,, Derebail SS,, Gorelick RJ,, DeStefano JJ . 2003. Differing roles of the N- and C-terminal zinc fingers in human immunodeficiency virus nucleocapsid protein-enhanced nucleic acid annealing. J Biol Chem 278 : 30755 30763.[CrossRef][PubMed]
89. Williams MC,, Gorelick RJ,, Musier-Forsyth K . 2002. Specific zinc-finger architecture required for HIV-1 nucleocapsid protein’s nucleic acid chaperone function. Proc Natl Acad Sci U S A 99 : 8614 8619.[CrossRef][PubMed]
90. Williams MC,, Rouzina I,, Wenner JR,, Gorelick RJ,, Musier-Forsyth K,, Bloomfield VA . 2001. Mechanism for nucleic acid chaperone activity of HIV-1 nucleocapsid protein revealed by single molecule stretching. Proc Natl Acad Sci U S A 98 : 6121 6126.[CrossRef][PubMed]
91. Le Cam E,, Coulaud D,, Delain E,, Petitjean P,, Roques BP,, Gérard D,, Stoylova E,, Vuilleumier C,, Stoylov SP,, Mély Y . 1998. Properties and growth mechanism of the ordered aggregation of a model RNA by the HIV-1 nucleocapsid protein: an electron microscopy investigation. Biopolymers 45 : 217 229.[CrossRef]
92. Azoulay J,, Clamme JP,, Darlix JL,, Roques BP,, Mély Y . 2003. Destabilization of the HIV-1 complementary sequence of TAR by the nucleocapsid protein through activation of conformational fluctuations. J Mol Biol 326 : 691 700.[CrossRef]
93. Heilman-Miller SL,, Wu T,, Levin JG . 2004. Alteration of nucleic acid structure and stability modulates the efficiency of minus-strand transfer mediated by the HIV-1 nucleocapsid protein. J Biol Chem 279 : 44154 44165.[CrossRef][PubMed]
94. McCauley MJ,, Rouzina I,, Manthei KA,, Gorelick RJ,, Musier-Forsyth K,, Williams MC . 2015. Targeted binding of nucleocapsid protein transforms the folding landscape of HIV-1 TAR RNA. Proc Natl Acad Sci U S A 112 : 13555 13560.[CrossRef][PubMed]
95. You JC,, McHenry CS . 1994. Human immunodeficiency virus nucleocapsid protein accelerates strand transfer of the terminally redundant sequences involved in reverse transcription. J Biol Chem 269 : 31491 31495.[PubMed]
96. Godet J,, Ramalanjaona N,, Sharma KK,, Richert L,, de Rocquigny H,, Darlix JL,, Duportail G,, Mély Y . 2011. Specific implications of the HIV-1 nucleocapsid zinc fingers in the annealing of the primer binding site complementary sequences during the obligatory plus strand transfer. Nucleic Acids Res 39 : 6633 6645.[CrossRef][PubMed]
97. Grohman JK,, Gorelick RJ,, Lickwar CR,, Lieb JD,, Bower BD,, Znosko BM,, Weeks KM . 2013. A guanosine-centric mechanism for RNA chaperone function. Science 340 : 190 195.[CrossRef][PubMed]
98. Darlix JL,, Godet J,, Ivanyi-Nagy R,, Fossé P,, Mauffret O,, Mély Y . 2011. Flexible nature and specific functions of the HIV-1 nucleocapsid protein. J Mol Biol 410 : 565 581.[CrossRef][PubMed]
99. Wu H,, Mitra M,, Naufer MN,, McCauley MJ,, Gorelick RJ,, Rouzina I,, Musier-Forsyth K,, Williams MC . 2014. Differential contribution of basic residues to HIV-1 nucleocapsid protein’s nucleic acid chaperone function and retroviral replication. Nucleic Acids Res 42 : 2525 2537.[CrossRef][PubMed]
100. Duval M,, Korepanov A,, Fuchsbauer O,, Fechter P,, Haller A,, Fabbretti A,, Choulier L,, Micura R,, Klaholz BP,, Romby P,, Springer M,, Marzi S . 2013. Escherichia coli ribosomal protein S1 unfolds structured mRNAs onto the ribosome for active translation initiation. PLoS Biol 11 : e1001731.[CrossRef][PubMed]
101. Qu X,, Lancaster L,, Noller HF,, Bustamante C,, Tinoco I Jr . 2012. Ribosomal protein S1 unwinds double-stranded RNA in multiple steps. Proc Natl Acad Sci U S A 109 : 14458 14463.[CrossRef][PubMed]
102. Cléry A,, Blatter M,, Allain FH . 2008. RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol 18 : 290 298.[CrossRef][PubMed]
103. Raghunathan PL,, Guthrie C . 1998. A spliceosomal recycling factor that reanneals U4 and U6 small nuclear ribonucleoprotein particles. Science 279 : 857 860.[CrossRef]
104. Montemayor EJ,, Curran EC,, Liao HH,, Andrews KL,, Treba CN,, Butcher SE,, Brow DA . 2014. Core structure of the U6 small nuclear ribonucleoprotein at 1.7-Å resolution. Nat Struct Mol Biol 21 : 544 551.[CrossRef][PubMed]
105. Didychuk AL,, Montemayor EJ,, Brow DA,, Butcher SE . 2016. Structural requirements for protein-catalyzed annealing of U4 and U6 RNAs during di-snRNP assembly. Nucleic Acids Res 44 : 1398 1410.[CrossRef][PubMed]
106. Belair C,, Sim S,, Wolin SL . 2017. Noncoding RNA surveillance: the ends justify the means. Chem Rev 118 : 4422 4447.[CrossRef][PubMed]
107. Maraia RJ,, Lamichhane TN . 2011. 3′ processing of eukaryotic precursor tRNAs. Wiley Interdiscip Rev RNA 2 : 362 375.[CrossRef][PubMed]
108. Pannone BK,, Xue D,, Wolin SL . 1998. 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 17 : 7442 7453.[CrossRef][PubMed]
109. Blewett NH,, Maraia RJ . 2018. La involvement in tRNA and other RNA processing events including differences among yeast and other eukaryotes. Biochim Biophys Acta 1861 : 361 372.[CrossRef][PubMed]
110. Kotik-Kogan O,, Valentine ER,, Sanfelice D,, Conte MR,, Curry S . 2008. Structural analysis reveals conformational plasticity in the recognition of RNA 3′ ends by the human La protein. Structure 16 : 852 862.[CrossRef][PubMed]
111. Wilusz CJ,, Wilusz J . 2005. Eukaryotic Lsm proteins: lessons from bacteria. Nat Struct Mol Biol 12 : 1031 1036.[CrossRef][PubMed]
112. Babitzke P . 2004. Regulation of transcription attenuation and translation initiation by allosteric control of an RNA-binding protein: the Bacillus subtilis TRAP protein. Curr Opin Microbiol 7 : 132 139.[CrossRef][PubMed]
113. Waters LS,, Storz G . 2009. Regulatory RNAs in bacteria. Cell 136 : 615 628.[CrossRef][PubMed]
114. Zhang A,, Wassarman KM,, Ortega J,, Steven AC,, Storz G . 2002. The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 9 : 11 22.[CrossRef]
115. Vecerek B,, Moll I,, Afonyushkin T,, Kaberdin V,, Bläsi U . 2003. Interaction of the RNA chaperone Hfq with mRNAs: direct and indirect roles of Hfq in iron metabolism of Escherichia coli. Mol Microbiol 50 : 897 909.[CrossRef][PubMed]
116. Vecerek B,, Moll I,, Bläsi U . 2005. Translational autocontrol of the Escherichia coli hfq RNA chaperone gene. RNA 11 : 976 984.[CrossRef][PubMed]
117. Desnoyers G,, Massé E . 2012. Noncanonical repression of translation initiation through small RNA recruitment of the RNA chaperone Hfq. Genes Dev 26 : 726 739.[CrossRef][PubMed]
118. Chen J,, Gottesman S . 2017. Hfq links translation repression to stress-induced mutagenesis in E. coli. Genes Dev 31 : 1382 1395.[CrossRef][PubMed]
119. Ellis MJ,, Trussler RS,, Haniford DB . 2015. Hfq binds directly to the ribosome-binding site of IS 10 transposase mRNA to inhibit translation. Mol Microbiol 96 : 633 650.[CrossRef][PubMed]
120. Kavita K,, de Mets F,, Gottesman S . 2018. New aspects of RNA-based regulation by Hfq and its partner sRNAs. Curr Opin Microbiol 42 : 53 61.[CrossRef][PubMed]
121. Weichenrieder O . 2014. RNA binding by Hfq and ring-forming (L)Sm proteins: a trade-off between optimal sequence readout and RNA backbone conformation. RNA Biol 11 : 537 549.[CrossRef][PubMed]
122. Schumacher MA,, Pearson RF,, Møller T,, Valentin-Hansen P,, Brennan RG . 2002. Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. EMBO J 21 : 3546 3556.[CrossRef][PubMed]
123. Brescia CC,, Mikulecky PJ,, Feig AL,, Sledjeski DD . 2003. Identification of the Hfq-binding site on DsrA RNA: Hfq binds without altering DsrA secondary structure. RNA 9 : 33 43.[CrossRef][PubMed]
124. Otaka H,, Ishikawa H,, Morita T,, Aiba H . 2011. PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action. Proc Natl Acad Sci U S A 108 : 13059 13064.[CrossRef][PubMed]
125. Sauer E,, Weichenrieder O . 2011. Structural basis for RNA 3′-end recognition by Hfq. Proc Natl Acad Sci U S A 108 : 13065 13070.[CrossRef][PubMed]
126. Sledjeski DD,, Whitman C,, Zhang A . 2001. Hfq is necessary for regulation by the untranslated RNA DsrA. J Bacteriol 183 : 1997 2005.[CrossRef][PubMed]
127. Ishikawa H,, Otaka H,, Maki K,, Morita T,, Aiba H . 2012. The functional Hfq-binding module of bacterial sRNAs consists of a double or single hairpin preceded by a U-rich sequence and followed by a 3′ poly(U) tail. RNA 18 : 1062 1074.[CrossRef][PubMed]
128. Fei J,, Singh D,, Zhang Q,, Park S,, Balasubramanian D,, Golding I,, Vanderpool CK,, Ha T . 2015. RNA biochemistry. Determination of in vivo target search kinetics of regulatory noncoding RNA. Science 347 : 1371 1374.[CrossRef][PubMed]
129. Zhang A,, Schu DJ,, Tjaden BC,, Storz G,, Gottesman S . 2013. Mutations in interaction surfaces differentially impact E. coli Hfq association with small RNAs and their mRNA targets. J Mol Biol 425 : 3678 3697.[CrossRef][PubMed]
130. Mikulecky PJ,, Kaw MK,, Brescia CC,, Takach JC,, Sledjeski DD,, Feig AL . 2004. Escherichia coli Hfq has distinct interaction surfaces for DsrA, rpoS and poly(A) RNAs. Nat Struct Mol Biol 11 : 1206 1214.[CrossRef][PubMed]
131. Soper TJ,, Woodson SA . 2008. The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 14 : 1907 1917.[CrossRef][PubMed]
132. Link TM,, Valentin-Hansen P,, Brennan RG . 2009. Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc Natl Acad Sci U S A 106 : 19292 19297.[CrossRef][PubMed]
133. Soper T,, Mandin P,, Majdalani N,, Gottesman S,, Woodson SA . 2010. Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci U S A 107 : 9602 9607.[CrossRef][PubMed]
134. Updegrove T,, Wilf N,, Sun X,, Wartell RM . 2008. Effect of Hfq on RprA- rpoS mRNA pairing: Hfq-RNA binding and the influence of the 5′ rpoS mRNA leader region. Biochemistry 47 : 11184 11195.[CrossRef][PubMed]
135. Beisel CL,, Updegrove TB,, Janson BJ,, Storz G . 2012. Multiple factors dictate target selection by Hfq-binding small RNAs. EMBO J 31 : 1961 1974.[CrossRef][PubMed]
136. Møller T,, Franch T,, Højrup P,, Keene DR,, Bächinger HP,, Brennan RG,, Valentin-Hansen P . 2002. Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. Mol Cell 9 : 23 30.[CrossRef]
137. Sauer E,, Schmidt S,, Weichenrieder O . 2012. Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition. Proc Natl Acad Sci U S A 109 : 9396 9401.[CrossRef][PubMed]
138. Panja S,, Schu DJ,, Woodson SA . 2013. Conserved arginines on the rim of Hfq catalyze base pair formation and exchange. Nucleic Acids Res 41 : 7536 7546.[CrossRef][PubMed]
139. Papenfort K,, Said N,, Welsink T,, Lucchini S,, Hinton JCD,, Vogel J . 2009. Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 74 : 139 158.[CrossRef][PubMed]
140. Tree JJ,, Granneman S,, McAteer SP,, Tollervey D,, Gally DL . 2014. Identification of bacteriophage-encoded anti-sRNAs in pathogenic Escherichia coli. Mol Cell 55 : 199 213.[CrossRef][PubMed]
141. Peng Y,, Soper TJ,, Woodson SA . 2014. Positional effects of AAN motifs in rpoS regulation by sRNAs and Hfq. J Mol Biol 426 : 275 285.[CrossRef][PubMed]
142. Schu DJ,, Zhang A,, Gottesman S,, Storz G . 2015. Alternative Hfq-sRNA interaction modes dictate alternative mRNA recognition. EMBO J 34 : 2557 2573.[CrossRef][PubMed]
143. Hopkins JF,, Panja S,, McNeil SA,, Woodson SA . 2009. Effect of salt and RNA structure on annealing and strand displacement by Hfq. Nucleic Acids Res 37 : 6205 6213.[CrossRef][PubMed]
144. Arluison V,, Hohng S,, Roy R,, Pellegrini O,, Régnier P,, Ha T . 2007. Spectroscopic observation of RNA chaperone activities of Hfq in post-transcriptional regulation by a small non-coding RNA. Nucleic Acids Res 35 : 999 1006.[CrossRef][PubMed]
145. Zheng A,, Panja S,, Woodson SA . 2016. Arginine patch predicts the RNA annealing activity of Hfq from Gram negative and Gram positive bacteria. J Mol Biol 428 : 2259 2264.[CrossRef][PubMed]
146. Hwang W,, Arluison V,, Hohng S . 2011. Dynamic competition of DsrA and rpoS fragments for the proximal binding site of Hfq as a means for efficient annealing. Nucleic Acids Res 39 : 5131 5139.[CrossRef][PubMed]
147. Sukhodolets MV,, Garges S . 2003. Interaction of Escherichia coli RNA polymerase with the ribosomal protein S1 and the Sm-like ATPase Hfq. Biochemistry 42 : 8022 8034.[CrossRef][PubMed]
148. Wang W,, Wang L,, Zou Y,, Zhang J,, Gong Q,, Wu J,, Shi Y . 2011. Cooperation of Escherichia coli Hfq hexamers in DsrA binding. Genes Dev 25 : 2106 2117.[CrossRef][PubMed]
149. Ribeiro EA Jr,, Beich-Frandsen M,, Konarev PV,, Shang W,, Vecerek B,, Kontaxis G,, Hämmerle H,, Peterlik H,, Svergun DI,, Bläsi U,, Djinović-Carugo K . 2012. Structural flexibility of RNA as molecular basis for Hfq chaperone function. Nucleic Acids Res 40 : 8072 8084.[CrossRef][PubMed]
150. Panja S,, Paul R,, Greenberg MM,, Woodson SA . 2015. Light-triggered RNA annealing by an RNA chaperone. Angew Chem Int Ed Engl 54 : 7281 7284.[CrossRef][PubMed]
151. Updegrove TB,, Wartell RM . 2011. The influence of Escherichia coli Hfq mutations on RNA binding and sRNA•mRNA duplex formation in rpoS riboregulation. Biochim Biophys Acta 1809 : 532 540.[CrossRef][PubMed]
152. Peng Y,, Curtis JE,, Fang X,, Woodson SA . 2014. Structural model of an mRNA in complex with the bacterial chaperone Hfq. Proc Natl Acad Sci U S A 111 : 17134 17139.[CrossRef][PubMed]
153. Lease RA,, Belfort M . 2000. Riboregulation by DsrA RNA: trans-actions for global economy. Mol Microbiol 38 : 667 672.[CrossRef]
154. Bordeau V,, Felden B . 2014. Curli synthesis and biofilm formation in enteric bacteria are controlled by a dynamic small RNA module made up of a pseudoknot assisted by an RNA chaperone. Nucleic Acids Res 42 : 4682 4696.[CrossRef][PubMed]
155. Salim NN,, Feig AL . 2010. An upstream Hfq binding site in the fhlA mRNA leader region facilitates the OxyS- fhlA interaction. PLoS One 5 : e13028.[CrossRef][PubMed]
156. Gorski SA,, Vogel J,, Doudna JA . 2017. RNA-based recognition and targeting: sowing the seeds of specificity. Nat Rev Mol Cell Biol 18 : 215 228.[CrossRef][PubMed]
157. Hussein R,, Lim HN . 2011. Disruption of small RNA signaling caused by competition for Hfq. Proc Natl Acad Sci U S A 108 : 1110 1115.[CrossRef][PubMed]
158. Moon K,, Gottesman S . 2011. Competition among Hfq-binding small RNAs in Escherichia coli. Mol Microbiol 82 : 1545 1562.[CrossRef][PubMed]
159. Olejniczak M . 2011. Despite similar binding to the Hfq protein regulatory RNAs widely differ in their competition performance. Biochemistry 50 : 4427 4440.[CrossRef][PubMed]
160. Fender A,, Elf J,, Hampel K,, Zimmermann B,, Wagner EG . 2010. RNAs actively cycle on the Sm-like protein Hfq. Genes Dev 24 : 2621 2626.[CrossRef][PubMed]
161. Boehr DD,, Nussinov R,, Wright PE . 2009. The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol 5 : 789 796.[CrossRef][PubMed]
162. Uversky VN . 2015. The multifaceted roles of intrinsic disorder in protein complexes. FEBS Lett 589( 19 Pt A) : 2498 2506.[CrossRef][PubMed]
163. Vo MN,, Barany G,, Rouzina I,, Musier-Forsyth K . 2009. HIV-1 nucleocapsid protein switches the pathway of transactivation response element RNA/DNA annealing from loop-loop “kissing” to “zipper”. J Mol Biol 386 : 789 801.[CrossRef][PubMed]
164. Grohman JK,, Del Campo M,, Bhaskaran H,, Tijerina P,, Lambowitz AM,, Russell R . 2007. Probing the mechanisms of DEAD-box proteins as general RNA chaperones: the C-terminal domain of CYT-19 mediates general recognition of RNA. Biochemistry 46 : 3013 3022.[CrossRef][PubMed]
165. Mohr G,, Del Campo M,, Mohr S,, Yang Q,, Jia H,, Jankowsky E,, Lambowitz AM . 2008. Function of the C-terminal domain of the DEAD-box protein Mss116p analyzed in vivo and in vitro. J Mol Biol 375 : 1344 1364.[CrossRef][PubMed]
166. Busa VF,, Rector MJ,, Russell R . 2017. The DEAD-box protein CYT-19 uses arginine residues in its C-tail to tether RNA substrates. Biochemistry 56 : 3571 3578.[CrossRef][PubMed]
167. Russell R,, Jarmoskaite I,, Lambowitz AM . 2013. Toward a molecular understanding of RNA remodeling by DEAD-box proteins. RNA Biol 10 : 44 55.[CrossRef][PubMed]
168. Kucera NJ,, Hodsdon ME,, Wolin SL . 2011. An intrinsically disordered C terminus allows the La protein to assist the biogenesis of diverse noncoding RNA precursors. Proc Natl Acad Sci U S A 108 : 1308 1313.[CrossRef][PubMed]
169. Koculi E,, Lee NK,, Thirumalai D,, Woodson SA . 2004. Folding of the Tetrahymena ribozyme by polyamines: importance of counterion valence and size. J Mol Biol 341 : 27 36.[CrossRef][PubMed]
170. Koculi E,, Thirumalai D,, Woodson SA . 2006. Counterion charge density determines the position and plasticity of RNA folding transition states. J Mol Biol 359 : 446 454.[CrossRef][PubMed]
171. Hauk G,, McKnight JN,, Nodelman IM,, Bowman GD . 2010. The chromodomains of the Chd1 chromatin remodeler regulate DNA access to the ATPase motor. Mol Cell 39 : 711 723.[CrossRef][PubMed]
172. Kozlov AG,, Cox MM,, Lohman TM . 2010. Regulation of single-stranded DNA binding by the C termini of Escherichia coli single-stranded DNA-binding (SSB) protein. J Biol Chem 285 : 17246 17252.[CrossRef][PubMed]
173. Tretter EM,, Berger JM . 2012. Mechanisms for defining supercoiling set point of DNA gyrase orthologs: I. A nonconserved acidic C-terminal tail modulates Escherichia coli gyrase activity. J Biol Chem 287 : 18636 18644.[CrossRef][PubMed]
174. 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 1498.[CrossRef][PubMed]
175. Santiago-Frangos A,, Jeliazkov JR,, Gray JJ,, Woodson SA . 2017. Acidic C-terminal domains autoregulate the RNA chaperone Hfq. eLife 6 : e27049.[CrossRef][PubMed]
176. Santiago-Frangos A,, Kavita K,, Schu DJ,, Gottesman S,, Woodson SA . 2016. C-terminal domain of the RNA chaperone Hfq drives sRNA competition and release of target RNA. Proc Natl Acad Sci U S A 113 : E6089 E6096.[CrossRef][PubMed]
177. Beich-Frandsen M,, Vecerek B,, Konarev PV,, Sjöblom B,, Kloiber K,, Hämmerle H,, Rajkowitsch L,, Miles AJ,, Kontaxis G,, Wallace BA,, Svergun DI,, Konrat R,, Bläsi U,, Djinovic-Carugo K . 2011. Structural insights into the dynamics and function of the C-terminus of the E. coli RNA chaperone Hfq. Nucleic Acids Res 39 : 4900 4915.[CrossRef][PubMed]
178. Vincent HA,, Henderson CA,, Stone CM,, Cary PD,, Gowers DM,, Sobott F,, Taylor JE,, Callaghan AJ . 2012. The low-resolution solution structure of Vibrio cholerae Hfq in complex with Qrr1 sRNA. Nucleic Acids Res 40 : 8698 8710.[CrossRef][PubMed]
179. Qualley DF,, Stewart-Maynard KM,, Wang F,, Mitra M,, Gorelick RJ,, Rouzina I,, Williams MC,, Musier-Forsyth K . 2010. C-terminal domain modulates the nucleic acid chaperone activity of human T-cell leukemia virus type 1 nucleocapsid protein via an electrostatic mechanism. J Biol Chem 285 : 295 307.[CrossRef][PubMed]
180. Santiago-Frangos A,, Woodson SA . 2018. Hfq chaperone brings speed dating to bacterial sRNA. Wiley Interdiscip Rev RNA 9 : e1475.[CrossRef][PubMed]

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