468:409–422.
https://doi.org/10.1016/
S0076-6879(09)68019-8
24. Kobitski AY, Nierth A, Helm M et al (2007)
Mg
2+ -dependent folding of a Diels-Alderase
ribozyme probed by single-molecule FRET
analysis. Nucleic Acids Res 35:2047–2059.
https://doi.org/10.1093/nar/gkm072
25. Shaw E, St-Pierre P, McCluskey K et al (2014)
Using sm-FRET and denaturants to reveal
folding landscapes. Methods Enzymol
549:313–341.
https://doi.org/10.1016/
B978-0-12-801122-5.00014-3
26. Hill AV (1910) The possible effects of the
aggregation of the molecules of hæmoglobin
on its dissociation curves. J Physiol 40:iv–vii.
https://doi.org/10.1113/jphysiol.1910.
sp001386
27. Sherman EM, Esquiaqui J, Elsayed G, Ye J-D
(2012) An energetically beneficial leader-linker
interaction abolishes ligand-binding cooperativity
in
glycine
riboswitches.
RNA
18:496–507. https://doi.org/10.1261/rna.
031286.111
28. Kladwang W, Chou FC, Das R (2012) Automated RNA structure prediction uncovers a
kink-turn linker in double glycine riboswitches.
J Am Chem Soc 134:1404–1407. https://doi.
org/10.1021/ja2093508
29. Mandal M, Lee M, Barrick JE, Weinberg Z,
Emilsson GM, Ruzzo WL, Breaker RR
(2004) A glycine-dependent riboswitch that
uses cooperative binding to control gene
expression. Science 306:275–279. https://
doi.org/10.1126/science.1100829
30. Lipfert J, Das R, Chu VB et al (2007) Structural transitions and thermodynamics of a
glycine-dependent riboswitch from Vibrio cholerae. J Mol Biol 365:1393–1406. https://doi.
org/10.1016/j.jmb.2006.10.022
31. Cheng CY, Chou FC, Kladwang W et al (2015)
Consistent global structures of complex RNA
states through multidimensional chemical
mapping. elife 4:e07600. https://doi.org/10.
7554/eLife.07600
32. Regulski EE, Breaker RR (2008) In-line probing analysis of riboswitches. Methods Mol Biol
419:53–67. https://doi.org/10.1007/978-159745-033-1_4
33. Misra VK, Draper DE (2002) The linkage
between magnesium binding and RNA folding. J Mol Biol 317:507–521. https://doi.
org/10.1006/jmbi.2002.5422
34. Tinoco I, Bustamante C (1999) How RNA
folds. J Mol Biol 293:271–281. https://doi.
org/10.1006/jmbi.1999.3001
35. Heilman-Miller SL, Woodson SA (2003)
Effect of transcription on folding of the
Tetrahymena ribozyme. RNA 9:722–733.
https://doi.org/10.1261/rna.5200903
36. Varani G (1995) Exceptionally stable nucleic
acid hairpins. Annu Rev Biophys Biomol Struct
24:379–404.
https://doi.org/10.1146/
annurev.bb.24.060195.002115
37. Gutell RR (1994) Collection of small subunit
(16S- and 16S-like) ribosomal RNA structures:
1994. Nucleic Acids Res 22:3502–3507.
https://doi.org/10.1093/nar/22.17.3502
38. Ma H, Proctor DJ, Kierzek E et al (2006)
Exploring the energy landscape of a small
RNA
hairpin.
J
Am
Chem
Soc
128:1523–1530. https://doi.org/10.1021/
ja0553856
39. Proctor DJ, Ma H, Kierzek E et al (2004)
Folding thermodynamics and kinetics of
YNMG RNA hairpins: specific incorporation
of 8-bromoguanosine leads to stabilization by
enhancement of the folding rate. Biochemistry
43:14004–14014. https://doi.org/10.1021/
bi048213e
40. Fiore JL, Nesbitt DJ (2013) An RNA folding
motif: GNRA tetraloop–receptor interactions.
Q Rev Biophys 46:223–264. https://doi.org/
10.1017/S0033583513000048
41. Cate JH, Gooding AR, Podell E et al (1996)
Crystal structure of a group I ribozyme
domain: principles of RNA packing. Science
273:1678–1685. https://doi.org/10.1126/
science.273.5282.1678
42. Cheong C, Varani G, Tinoco I Jr (1990) Solution structure of an unusually stable RNA hairpin, 5
0
GGAC(UUCG)GUCC. Nature
346:680–682.
https://doi.org/10.1038/
346680a0
43. Ennifar E, Nikulin A, Tishchenko S et al
(2000) The crystal structure of UUCG tetraloop. J Mol Biol 304:35–42. https://doi.org/
10.1006/jmbi.2000.4204
44. Moody EM, Feerrar JC, Bevilacqua PC (2004)
Evidence that folding of an RNA tetraloop
hairpin is less cooperative than its DNA counterpart. Biochemistry 43:7992–7998. https://
doi.org/10.1021/bi049350e
45. Liphardt J, Onoa B, Smith SB et al (2001)
Reversible unfolding of single RNA molecules
by mechanical force. Science 292:733–737.
https://doi.org/10.1126/science.1058498
46. Hyeon C, Thirumalai D (2005) Mechanical
unfolding of RNA hairpins. Proc Natl Acad
Sci U S A 102:6789–6794. https://doi.org/
10.1073/pnas.0408314102
47. Hyeon C, Thirumalai D (2007) Mechanical
unfolding of RNA: from hairpins to structures
with
internal
multiloops.
Biophys
J
270
Alla Peselis and Alexander Serganov
https://doi.org/10.1016/
S0076-6879(09)68019-8
24. Kobitski AY, Nierth A, Helm M et al (2007)
Mg
2+ -dependent folding of a Diels-Alderase
ribozyme probed by single-molecule FRET
analysis. Nucleic Acids Res 35:2047–2059.
https://doi.org/10.1093/nar/gkm072
25. Shaw E, St-Pierre P, McCluskey K et al (2014)
Using sm-FRET and denaturants to reveal
folding landscapes. Methods Enzymol
549:313–341.
https://doi.org/10.1016/
B978-0-12-801122-5.00014-3
26. Hill AV (1910) The possible effects of the
aggregation of the molecules of hæmoglobin
on its dissociation curves. J Physiol 40:iv–vii.
https://doi.org/10.1113/jphysiol.1910.
sp001386
27. Sherman EM, Esquiaqui J, Elsayed G, Ye J-D
(2012) An energetically beneficial leader-linker
interaction abolishes ligand-binding cooperativity
in
glycine
riboswitches.
RNA
18:496–507. https://doi.org/10.1261/rna.
031286.111
28. Kladwang W, Chou FC, Das R (2012) Automated RNA structure prediction uncovers a
kink-turn linker in double glycine riboswitches.
J Am Chem Soc 134:1404–1407. https://doi.
org/10.1021/ja2093508
29. Mandal M, Lee M, Barrick JE, Weinberg Z,
Emilsson GM, Ruzzo WL, Breaker RR
(2004) A glycine-dependent riboswitch that
uses cooperative binding to control gene
expression. Science 306:275–279. https://
doi.org/10.1126/science.1100829
30. Lipfert J, Das R, Chu VB et al (2007) Structural transitions and thermodynamics of a
glycine-dependent riboswitch from Vibrio cholerae. J Mol Biol 365:1393–1406. https://doi.
org/10.1016/j.jmb.2006.10.022
31. Cheng CY, Chou FC, Kladwang W et al (2015)
Consistent global structures of complex RNA
states through multidimensional chemical
mapping. elife 4:e07600. https://doi.org/10.
7554/eLife.07600
32. Regulski EE, Breaker RR (2008) In-line probing analysis of riboswitches. Methods Mol Biol
419:53–67. https://doi.org/10.1007/978-159745-033-1_4
33. Misra VK, Draper DE (2002) The linkage
between magnesium binding and RNA folding. J Mol Biol 317:507–521. https://doi.
org/10.1006/jmbi.2002.5422
34. Tinoco I, Bustamante C (1999) How RNA
folds. J Mol Biol 293:271–281. https://doi.
org/10.1006/jmbi.1999.3001
35. Heilman-Miller SL, Woodson SA (2003)
Effect of transcription on folding of the
Tetrahymena ribozyme. RNA 9:722–733.
https://doi.org/10.1261/rna.5200903
36. Varani G (1995) Exceptionally stable nucleic
acid hairpins. Annu Rev Biophys Biomol Struct
24:379–404.
https://doi.org/10.1146/
annurev.bb.24.060195.002115
37. Gutell RR (1994) Collection of small subunit
(16S- and 16S-like) ribosomal RNA structures:
1994. Nucleic Acids Res 22:3502–3507.
https://doi.org/10.1093/nar/22.17.3502
38. Ma H, Proctor DJ, Kierzek E et al (2006)
Exploring the energy landscape of a small
RNA
hairpin.
J
Am
Chem
Soc
128:1523–1530. https://doi.org/10.1021/
ja0553856
39. Proctor DJ, Ma H, Kierzek E et al (2004)
Folding thermodynamics and kinetics of
YNMG RNA hairpins: specific incorporation
of 8-bromoguanosine leads to stabilization by
enhancement of the folding rate. Biochemistry
43:14004–14014. https://doi.org/10.1021/
bi048213e
40. Fiore JL, Nesbitt DJ (2013) An RNA folding
motif: GNRA tetraloop–receptor interactions.
Q Rev Biophys 46:223–264. https://doi.org/
10.1017/S0033583513000048
41. Cate JH, Gooding AR, Podell E et al (1996)
Crystal structure of a group I ribozyme
domain: principles of RNA packing. Science
273:1678–1685. https://doi.org/10.1126/
science.273.5282.1678
42. Cheong C, Varani G, Tinoco I Jr (1990) Solution structure of an unusually stable RNA hairpin, 5
0
GGAC(UUCG)GUCC. Nature
346:680–682.
https://doi.org/10.1038/
346680a0
43. Ennifar E, Nikulin A, Tishchenko S et al
(2000) The crystal structure of UUCG tetraloop. J Mol Biol 304:35–42. https://doi.org/
10.1006/jmbi.2000.4204
44. Moody EM, Feerrar JC, Bevilacqua PC (2004)
Evidence that folding of an RNA tetraloop
hairpin is less cooperative than its DNA counterpart. Biochemistry 43:7992–7998. https://
doi.org/10.1021/bi049350e
45. Liphardt J, Onoa B, Smith SB et al (2001)
Reversible unfolding of single RNA molecules
by mechanical force. Science 292:733–737.
https://doi.org/10.1126/science.1058498
46. Hyeon C, Thirumalai D (2005) Mechanical
unfolding of RNA hairpins. Proc Natl Acad
Sci U S A 102:6789–6794. https://doi.org/
10.1073/pnas.0408314102
47. Hyeon C, Thirumalai D (2007) Mechanical
unfolding of RNA: from hairpins to structures
with
internal
multiloops.
Biophys
J
270
Alla Peselis and Alexander Serganov