92:731–743.
https://doi.org/10.1529/
biophysj.106.093062
48. Sattin BD, Zhao W, Travers K et al (2008)
Direct measurement of tertiary contact cooperativity in RNA folding. J Am Chem Soc
130:6085–6087. https://doi.org/10.1021/
ja800919q
49. Bisaria N, Greenfeld M, Limouse C et al
(2016) Kinetic and thermodynamic framework
for P4-P6 RNA reveals tertiary motif modularity and modulation of the folding preferred
pathway. Proc Natl Acad Sci 113:
E4956–E4965.
https://doi.org/10.1073/
pnas.1525082113
50. Solomatin SV, Greenfeld M, Herschlag D
(2010) Multiple native states reveal persistent
ruggedness of an RNA folding landscape.
Nature 463:681–684. https://doi.org/10.
1038/nature08717
51. Greenfeld M, Solomatin SV, Herschlag D
(2011) Removal of covalent heterogeneity
reveals simple folding behavior for P4-P6
RNA. J Biol Chem 286:19872–19879.
https://doi.org/10.1074/jbc.M111.235465
52. Murphy FL, Cech TR (1993) An independently folding domain of RNA tertiary structure within the Tetrahymena ribozyme.
Biochemistry 32:5291–5300. https://doi.
org/10.1021/bi00071a003
53. Murphy FL, Cech TR (1994) GAAA tetraloop
and conserved bulge stabilize tertiary structure
of a group I intron domain. J Mol Biol
236:49–63. https://doi.org/10.1006/jmbi.
1994.1117
54. Serganov A, Nudler E (2013) A decade of
riboswitches. Cell 152:17–24. https://doi.
org/10.1016/j.cell.2012.12.024
55. Dann CE, Wakeman CA, Sieling CL et al
(2007) Structure and mechanism of a metalsensing regulatory RNA. Cell 130:878–892.
https://doi.org/10.1016/j.cell.2007.06.051
56. Wakeman CA, Ramesh A, Winkler WC (2009)
Multiple metal-binding cores are required for
metalloregulation by M-box riboswitch RNAs.
J Mol Biol 392:723–735. https://doi.org/10.
1016/j.jmb.2009.07.033
57. Ramesh A, Wakeman CA, Winkler WC (2011)
Insights into metalloregulation by M-box
riboswitch RNAs via structural analysis of
manganese-bound complexes. J Mol Biol
407:556–570.
https://doi.org/10.1016/j.
jmb.2011.01.049
58. Trausch JJ, Ceres P, Reyes FE, Batey RT
(2011) The structure of a tetrahydrofolatesensing riboswitch reveals two ligand binding
sites in a single aptamer. Structure
19:1413–1423. https://doi.org/10.1016/j.
str.2011.06.019
59. Price IR, Gaballa A, Ding F et al (2015) Mn
2+
-
sensing mechanisms of yybP-ykoY orphan
riboswitches. Mol Cell 57:1110–1123.
https://doi.org/10.1016/j.molcel.2015.02.
016
60. Dambach M, Sandoval M, Updegrove TB et al
(2015) The ubiquitous yybP-ykoY riboswitch
is a manganese-responsive regulatory element.
Mol Cell 57:1099–1109. https://doi.org/10.
1016/j.molcel.2015.01.035
61. Gao A, Serganov A (2014) Structural insights
into recognition of c-di-AMP by the ydaO
riboswitch. Nat Chem Biol 10:787–792.
https://doi.org/10.1038/nchembio.1607
62. Jones CP, Ferre ´-D’Amare ´ AR (2014) Crystal
structure of a c-di-AMP riboswitch reveals an
internally pseudo-dimeric RNA. EMBO J
33:2692–2703. https://doi.org/10.15252/
embj.201489209
63. Ren A, Patel DJ (2014) c-di-AMP binds the
ydaO riboswitch in two pseudo-symmetryrelated pockets. Nat Chem Biol 10:780–786.
https://doi.org/10.1038/nchembio.1606
64. Held WA, Ballou B, Mizushima S, Nomura M
(1974) Assembly mapping of 30 S ribosomal
proteins from Escherichia coli. J Biol Chem
249:3103–3111
65. Nikulin A, Serganov A, Ennifar E et al (2000)
Crystal structure of the S15-rRNA complex.
Nat Struct Biol 7:273–277. https://doi.org/
10.1107/S0108767300022558
66. Agalarov SC, Sridhar Prasad G, Funke PM,
Stout CD, Williamson JR (2000) Structure of
the S15,S6,S18-rRNA complex: assembly of
the 30S ribosome central domain. Science
288:107–112. https://doi.org/10.1126/sci
ence.288.5463.107
67. Mulder AM, Yoshioka C, Beck AH et al (2010)
Visualizing ribosome biogenesis: parallel
assembly pathways for the 30S subunit. Science
330:673–677. https://doi.org/10.1126/sci
ence.1193220
68. Recht MI, Williamson JR (2001) Central
domain assembly: thermodynamics and kinetics of S6 and S18 binding to an S15-RNA
complex. J Mol Biol 313:35–48. https://doi.
org/10.1006/jmbi.2001.5018
RNA Cooperativity and Allostery
271
https://doi.org/10.1529/
biophysj.106.093062
48. Sattin BD, Zhao W, Travers K et al (2008)
Direct measurement of tertiary contact cooperativity in RNA folding. J Am Chem Soc
130:6085–6087. https://doi.org/10.1021/
ja800919q
49. Bisaria N, Greenfeld M, Limouse C et al
(2016) Kinetic and thermodynamic framework
for P4-P6 RNA reveals tertiary motif modularity and modulation of the folding preferred
pathway. Proc Natl Acad Sci 113:
E4956–E4965.
https://doi.org/10.1073/
pnas.1525082113
50. Solomatin SV, Greenfeld M, Herschlag D
(2010) Multiple native states reveal persistent
ruggedness of an RNA folding landscape.
Nature 463:681–684. https://doi.org/10.
1038/nature08717
51. Greenfeld M, Solomatin SV, Herschlag D
(2011) Removal of covalent heterogeneity
reveals simple folding behavior for P4-P6
RNA. J Biol Chem 286:19872–19879.
https://doi.org/10.1074/jbc.M111.235465
52. Murphy FL, Cech TR (1993) An independently folding domain of RNA tertiary structure within the Tetrahymena ribozyme.
Biochemistry 32:5291–5300. https://doi.
org/10.1021/bi00071a003
53. Murphy FL, Cech TR (1994) GAAA tetraloop
and conserved bulge stabilize tertiary structure
of a group I intron domain. J Mol Biol
236:49–63. https://doi.org/10.1006/jmbi.
1994.1117
54. Serganov A, Nudler E (2013) A decade of
riboswitches. Cell 152:17–24. https://doi.
org/10.1016/j.cell.2012.12.024
55. Dann CE, Wakeman CA, Sieling CL et al
(2007) Structure and mechanism of a metalsensing regulatory RNA. Cell 130:878–892.
https://doi.org/10.1016/j.cell.2007.06.051
56. Wakeman CA, Ramesh A, Winkler WC (2009)
Multiple metal-binding cores are required for
metalloregulation by M-box riboswitch RNAs.
J Mol Biol 392:723–735. https://doi.org/10.
1016/j.jmb.2009.07.033
57. Ramesh A, Wakeman CA, Winkler WC (2011)
Insights into metalloregulation by M-box
riboswitch RNAs via structural analysis of
manganese-bound complexes. J Mol Biol
407:556–570.
https://doi.org/10.1016/j.
jmb.2011.01.049
58. Trausch JJ, Ceres P, Reyes FE, Batey RT
(2011) The structure of a tetrahydrofolatesensing riboswitch reveals two ligand binding
sites in a single aptamer. Structure
19:1413–1423. https://doi.org/10.1016/j.
str.2011.06.019
59. Price IR, Gaballa A, Ding F et al (2015) Mn
2+
-
sensing mechanisms of yybP-ykoY orphan
riboswitches. Mol Cell 57:1110–1123.
https://doi.org/10.1016/j.molcel.2015.02.
016
60. Dambach M, Sandoval M, Updegrove TB et al
(2015) The ubiquitous yybP-ykoY riboswitch
is a manganese-responsive regulatory element.
Mol Cell 57:1099–1109. https://doi.org/10.
1016/j.molcel.2015.01.035
61. Gao A, Serganov A (2014) Structural insights
into recognition of c-di-AMP by the ydaO
riboswitch. Nat Chem Biol 10:787–792.
https://doi.org/10.1038/nchembio.1607
62. Jones CP, Ferre ´-D’Amare ´ AR (2014) Crystal
structure of a c-di-AMP riboswitch reveals an
internally pseudo-dimeric RNA. EMBO J
33:2692–2703. https://doi.org/10.15252/
embj.201489209
63. Ren A, Patel DJ (2014) c-di-AMP binds the
ydaO riboswitch in two pseudo-symmetryrelated pockets. Nat Chem Biol 10:780–786.
https://doi.org/10.1038/nchembio.1606
64. Held WA, Ballou B, Mizushima S, Nomura M
(1974) Assembly mapping of 30 S ribosomal
proteins from Escherichia coli. J Biol Chem
249:3103–3111
65. Nikulin A, Serganov A, Ennifar E et al (2000)
Crystal structure of the S15-rRNA complex.
Nat Struct Biol 7:273–277. https://doi.org/
10.1107/S0108767300022558
66. Agalarov SC, Sridhar Prasad G, Funke PM,
Stout CD, Williamson JR (2000) Structure of
the S15,S6,S18-rRNA complex: assembly of
the 30S ribosome central domain. Science
288:107–112. https://doi.org/10.1126/sci
ence.288.5463.107
67. Mulder AM, Yoshioka C, Beck AH et al (2010)
Visualizing ribosome biogenesis: parallel
assembly pathways for the 30S subunit. Science
330:673–677. https://doi.org/10.1126/sci
ence.1193220
68. Recht MI, Williamson JR (2001) Central
domain assembly: thermodynamics and kinetics of S6 and S18 binding to an S15-RNA
complex. J Mol Biol 313:35–48. https://doi.
org/10.1006/jmbi.2001.5018
RNA Cooperativity and Allostery
271