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NMR Tools to Decipher Dynamic Structure of RNA

  • Received : 2017.04.05
  • Accepted : 2017.05.07
  • Published : 2017.06.20

Abstract

It is now well established that RNAs exhibit fundamental roles in regulating cellular processes. Many of these RNAs do not exist in a single conformation. Rather, they undergo dynamic transitions among many different conformations to mediate critical interactions with other biomolecules such as proteins, RNAs, DNAs, or small molecules. Here, we briefly review NMR techniques that describe the dynamic behavior of RNA by determining structural, kinetic, and thermodynamic properties.

Keywords

References

  1. G. J. Hannon, F. V. Rivas, E. P. Murchison, and J. A. Steitz, Cold Spring Harb. Sym. 71, 551 (2006) https://doi.org/10.1101/sqb.2006.71.064
  2. A. F. Bompfunewere, C. Flamm, C. Fried, G. Fritzsch, I. L. Hofacker, J. Lehmann, K. Missal, A. Mosig, B. Muller, S. J. Prohaska, B. M. Stadler, P. F. Stadler, A. Tanzer, S. Washietl, and C. Witwer, Theor. Biosci. 123, 301 (2005) https://doi.org/10.1016/j.thbio.2005.01.002
  3. A. Serganov, and D. J. Patel, Nat. Rev. Genet. 8, 776 (2007) https://doi.org/10.1038/nrg2172
  4. Q. Zhou, T. Li, and D. H. Price, Annu. Rev. Biochem. 81, 119 (2012) https://doi.org/10.1146/annurev-biochem-052610-095910
  5. B. Wiedenheft, S. H. Sternberg, and J. A. Doudna, Nature 482, 331 (2012) https://doi.org/10.1038/nature10886
  6. H. Dong, J. Lei, L. Ding, Y. Wen, H. Ju, and X. Zhang, Chem. Rev. 113, 6207 (2013) https://doi.org/10.1021/cr300362f
  7. E. A. Dethoff, J. Chugh, A. M. Mustoe, and H. M. Al-Hashimi, Nature 482, 322 (2012) https://doi.org/10.1038/nature10885
  8. J. A. Cruz and E. Westhof, Cell 136, 604 (2009) https://doi.org/10.1016/j.cell.2009.02.003
  9. A. Haller, M. F. Soulière, and R. Micura, Acc. Chem. Res. 44, 1339 (2011) https://doi.org/10.1021/ar200035g
  10. W. Winkler, A. Nahvi, and R. R. Breaker, Nature 419, 952 (2002) https://doi.org/10.1038/nature01145
  11. M. J. Cromie, Y. Shi, T. Latifi, and E. A. Groisman, Cell 125, 71 (2006) https://doi.org/10.1016/j.cell.2006.01.043
  12. G. Nechooshtan, M. Elgrably-Weiss, A. Sheaffer, E. Westhof, and S. Altuvia, Gene. Dev. 23, 2650 (2009) https://doi.org/10.1101/gad.552209
  13. J. D. Puglisi, R. Tan, B. J. Calnan, A. D. Frankel, and J. R. Williamson, Science 257, 76 (1992) https://doi.org/10.1126/science.1621097
  14. A. Nocker, Nucleic Acids Res. 29, 4800 (2001) https://doi.org/10.1093/nar/29.23.4800
  15. A. M. Pyle and J. B. Green, Curr. Opin. Struct. Biol. 5, 303 (1995) https://doi.org/10.1016/0959-440X(95)80091-3
  16. J. N. Kim, and R. R. Breaker, Biol. Cell 100, 1 (2008) https://doi.org/10.1042/BC20070088
  17. R. K. Montange and R. T. Batey, Annu. Rev. Biophys. 37, 117 (2008) https://doi.org/10.1146/annurev.biophys.37.032807.130000
  18. R. Giege, Nat. Struct. Mol. Biol. 15, 1007 (2008) https://doi.org/10.1038/nsmb.1498
  19. A. M. Mulder, C. Yoshioka, A. H. Beck, A. E. Bunner, R. A. Milligan, C. S. Potter, B. Carragher, and J. R. Williamson, Science 330, 673 (2010) https://doi.org/10.1126/science.1193220
  20. D. J. Patel, Curr. Opin. Struct. Biol. 9, 74 (1999) https://doi.org/10.1016/S0959-440X(99)80010-4
  21. W. A. Held, B. Ballou, S. Mizushima, and M. Nomura, J. Biol. Chem. 249, 3103 (1974)
  22. S. C. Agalarov, G. S. Prasad, P. M. Funke, C. D. Stout, and J. R. Williamson, Science 288, 107 (2000) https://doi.org/10.1126/science.288.5463.107
  23. D. Fourmy, M. I. Recht, S. C. Blanchard, and J. D. Puglisi, Science 274, 1367 (1996) https://doi.org/10.1126/science.274.5291.1367
  24. S. Yoshizawa, D. Fourmy, and J. D. Puglisi, Science 285, 1722 (1999) https://doi.org/10.1126/science.285.5434.1722
  25. T. M. Schmeing and V. Ramakrishnan, Nature 461, 1234 (2009) https://doi.org/10.1038/nature08403
  26. T. A. Cooper, L. Wan, and G. Dreyfuss, Cell 136, 777 (2009) https://doi.org/10.1016/j.cell.2009.02.011
  27. W.-J. Kim, J. Shin, K. Bang, H. K. Song, and N.-K. Kim, J. Kor. Magn. Reson. 20, 46 (2016)
  28. N.-K. Kim, Y.-S. Nam, and K.-B. Lee, J. Kor. Magn. Reson. Soc. 18, 5 (2014) https://doi.org/10.6564/JKMRS.2014.18.1.005
  29. F. J. Grundy, W. C. Winkler, and T. M. Henkin, Proc. Natl. Acad. Sci. U.S.A. 99, 11121 (2002) https://doi.org/10.1073/pnas.162366799
  30. D. Herschlag, M. Khosla, Z. Tsuchihashi, and R. L. Karpel, EMBO J. 13, 2913 (1994)
  31. Q. Yang and E. Jankowsky, Biochemistry 44, 13591 (2005) https://doi.org/10.1021/bi0508946
  32. C. G. Hoogstraten, J. R. Wank, and A. Pardi, Biochemistry 39, 9951 (2000) https://doi.org/10.1021/bi0007627
  33. H. Blad, N. J. Reiter, F. Abildgaard, J. L. Markley, and S. E. Butcher, J. Mol. Biol. 353, 540 (2005) https://doi.org/10.1016/j.jmb.2005.08.030
  34. H. M. Al-Hashimi and N. G. Walter, Curr. Opin. Struct. Biol. 18, 321 (2008) https://doi.org/10.1016/j.sbi.2008.04.004
  35. A. G. Palmer III, C. D. Kroenke, and J. P. Loria, Methods Enzymol. 339, 204 (2001)
  36. A. Sekhar and L. E. Kay, Proc. Natl. Acad. Sci. U.S.A. 110, 12867 (2013) https://doi.org/10.1073/pnas.1305688110
  37. A. G. Palmer and F. Massi, Chem. Rev. 106, 1700 (2006) https://doi.org/10.1021/cr0404287
  38. V. Z. Miloushev and A. G. Palmer III, J. Magn. Reson. 177, 221 (2005) https://doi.org/10.1016/j.jmr.2005.07.023
  39. D. M. Korzhnev and L. E. Kay, Acc. Chem. Res. 41, 442 (2008) https://doi.org/10.1021/ar700189y
  40. P. Neudecker, P. Lundstrom, and L. E. Kay, Biophys. J. 96, 2045 (2009) https://doi.org/10.1016/j.bpj.2008.12.3907
  41. J. P. Loria, M. Rance, and A. G. Palmer, J. Am. Chem. Soc. 121, 2331 (1999) https://doi.org/10.1021/ja983961a
  42. Y. Xue, D. Kellogg, I. J. Kimsey, B. Sathyamoorthy, Z. W. Stein, M. McBrairty, and H. M. Al-Hashimi, Methods Enzymol. 558, 39 (2015)
  43. M. Akke and A. G. Palmer, J. Am. Chem. Soc. 118, 911 (1996) https://doi.org/10.1021/ja953503r
  44. A. L. Hansen, E. N. Nikolova, A. Casiano-Negroni, and H. M. Al-Hashimi, J. Am. Chem. Soc. 131, 3818 (2009) https://doi.org/10.1021/ja8091399
  45. N. R. Skrynnikov, F. W. Dahlquist, and L. E. Kay, J. Am. Chem. Soc. 124, 12352 (2002) https://doi.org/10.1021/ja0207089
  46. B. Goswami, B. L. Gaffney, and R. A. Jones, J. Am. Chem. Soc. 115, 3832 (1993) https://doi.org/10.1021/ja00062a082
  47. X.-P. Xu and S. C. F. Au-Yeung, J. Phys. Chem. B 104, 5641 (2000) https://doi.org/10.1021/jp0007538
  48. C. Fares, I. Amata, and T. Carlomagno, J. Am. Chem. Soc. 129, 15814 (2007) https://doi.org/10.1021/ja0727417
  49. M. Ebrahimi, P. Rossi, C. Rogers, and G. S. Harbison, J. Magn. Reson. 150, 1 (2001) https://doi.org/10.1006/jmre.2001.2314
  50. P. Buchner, W. Maurer, and H. Ruterjans, J. Magn. Reson. 29, 45 (1978)
  51. T. Yamazaki, R. Muhandiram, and L. E. Kay, J. Am. Chem. Soc. 116, 8266 (1994) https://doi.org/10.1021/ja00097a037
  52. J. E. Johnson and C. G. Hoogstraten, J. Am. Chem. Soc. 130, 16757 (2008) https://doi.org/10.1021/ja805759z
  53. C. H. Wunderlich, R. Spitzer, T. Santner, K. Fauster, M. Tollinger, and C. Kreutz, J. Am. Chem. Soc. 134, 7558 (2012) https://doi.org/10.1021/ja302148g
  54. J. R. Tolman, J. M. Flanagan, M. A. Kennedy, and J. H. Prestegard, Proc. Natl Acad. Sci. U.S.A. 92, 9279 (1995) https://doi.org/10.1073/pnas.92.20.9279
  55. N. Tjandra and A. Bax, J. Magn. Reson. 124, 512 (1997) https://doi.org/10.1006/jmre.1996.1088
  56. M. R. Hansen, L. Mueller, and A. Pardi, Nat. Struct. Biol. 5, 1065 (1998) https://doi.org/10.1038/4176
  57. J. A. Losonczi, M. Andrec, M. W. F. Fischer, and J. H. Prestegard, J. Magn. Reson. 138, 334 (1999) https://doi.org/10.1006/jmre.1999.1754
  58. B. E. Ramirez and A. Bax, J. Am. Chem. Soc. 120, 9106 (1998) https://doi.org/10.1021/ja982310b
  59. H. M. Al-Hashimi, H. Valafar, M. Terrell, E. R. Zartler, M. K. Eidsness, and J. H. Prestegard, J. Magn. Reson. 143, 402 (2000) https://doi.org/10.1006/jmre.2000.2049
  60. K. Bondensgaard, E. T. Mollova, and A. Pardi, Biochemistry 41, 11532 (2002) https://doi.org/10.1021/bi012167q
  61. M. Zweckstetter, G. Hummer, and A. Bax, Biophys. J. 86, 3444 (2004) https://doi.org/10.1529/biophysj.103.035790
  62. Q. Zhang, X. Sun, E. D. Watt, and H. M. Al-Hashimi, Science 311, 653 (2006) https://doi.org/10.1126/science.1119488
  63. L. Salmon, G. M. Giambasu, E. N. Nikolova, K. Petzold, A. Bhattacharya, D. A. Case, and H. M. Al-Hashimi, J. Am. Chem. Soc. 137, 12954 (2015) https://doi.org/10.1021/jacs.5b07229
  64. A. T. Frank, A. C. Stelzer, H. M. Al-Hashimi, and I. Andricioaei, Nucleic Acids Res. 37, 3670 (2009) https://doi.org/10.1093/nar/gkp156
  65. M. H. Bailor, C. Musselman, A. L. Hansen, K. Gulati, D. J. Patel, and H. M. Al-Hashimi, Nat. Protoc. 2, 1536 (2007) https://doi.org/10.1038/nprot.2007.221
  66. Q. Zhang, A. C. Stelzer, C. K. Fisher, and H. M. Al-Hashimi, Nature 450, 1263 (2007) https://doi.org/10.1038/nature06389
  67. A. C. Stelzer, A. T. Frank, J. D. Kratz, M. D. Swanson, M. J. Gonzalez-Hernandez, J. Lee, I. Andricioaei, D. M. Markovitz, and H. M. Al-Hashimi, Nat. Chem. Biol. 7, 553 (2011) https://doi.org/10.1038/nchembio.596
  68. M. Gueron and J.-L. Leroy, Methods Enzymol. 261, 383 (1995)
  69. M. Gueron, M. Kochoyan, and J.-L. Leroy, Nature 328, 89 (1987) https://doi.org/10.1038/328089a0
  70. B. S. Choi and A. G. Redfield, Biochemistry 25, 1529 (1986) https://doi.org/10.1021/bi00355a010
  71. N. Figueroa, G. Keith, J. L. Leroy, P. Plateau, S. Roy, and M. Gueron, Proc. Natl Acad. Sci. U.S.A. 80, 4330 (1983) https://doi.org/10.1073/pnas.80.14.4330
  72. P. D. Johnston, N. Figueroa, and A. G. Redfield, Proc. Natl Acad. Sci. U.S.A. 76, 3130 (1979) https://doi.org/10.1073/pnas.76.7.3130
  73. K. Snoussi and J. L. Leroy, Biochemistry 40, 8898 (2001) https://doi.org/10.1021/bi010385d
  74. J. L. Leroy, N. Bolo, N. Figueroa, P. Plateau, and M. Gueron, J. Biomol. Struct. Dyn. 2, 915 (1985) https://doi.org/10.1080/07391102.1985.10507609
  75. J.-H. Lee and A. Pardi, Nucleic Acids Res. 35, 2965 (2007) https://doi.org/10.1093/nar/gkm184
  76. J.-H. Lee, F. Jucker, and A. Pardi, FEBS Lett. 582, 1835 (2008) https://doi.org/10.1016/j.febslet.2008.05.003
  77. M.-K. Lee, H.-E. Kim, E.-B. Park, J. Lee, K.-H. Kim, K. Lim, S. Yum, Y.-H. Lee, S.-J. Kang, J.-H. Lee, and B.-S. Choi, Nucleic Acids Res. 44, 8407 (2016) https://doi.org/10.1093/nar/gkw525
  78. B. Zhao and Q. Zhang, J. Am. Chem. Soc. 137, 13480 (2015) https://doi.org/10.1021/jacs.5b09014
  79. G. M. Clore, Mol. Biosyst. 4, 1058 (2008) https://doi.org/10.1039/b810232e
  80. G. L. Olsen, D. C. Echodu, Z. Shajani, M. F. Bardaro, G. Varani, and G. P. Drobny, J. Am. Chem. Soc. 130, 2896 (2008) https://doi.org/10.1021/ja0778803
  81. G. L. Olsen, M. F. Bardaro, D. C. Echodu, G. P. Drobny, and G. Varani, J. Am. Chem. Soc. 132, 303 (2010) https://doi.org/10.1021/ja907515s