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Computational and Mathematical Methods in Medicine
Volume 2012, Article ID 569870, 9 pages
http://dx.doi.org/10.1155/2012/569870
Review Article

Revealing −1 Programmed Ribosomal Frameshifting Mechanisms by Single-Molecule Techniques and Computational Methods

Institute of Molecular and Cellular Biology, National Taiwan University, Taipei 10617, Taiwan

Received 25 November 2011; Accepted 16 January 2012

Academic Editor: Shang-Te Danny Hsu

Copyright © 2012 Kai-Chun Chang. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. F. Curran and M. Yarus, “Base substitutions in the tRNA anticodon arm do not degrade the accuracy of reading frame maintenance,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 17, pp. 6538–6542, 1986. View at Google Scholar · View at Scopus
  2. J. F. Atkins, D. Elseviers, and L. Gorini, “Low activity of −galactosidase in frameshift mutants of Escherichia coli,” Proceedings of the National Academy of Sciences of the United States of America, vol. 69, no. 5, pp. 1192–1195, 1972. View at Google Scholar · View at Scopus
  3. T. Jacks, M. D. Power, F. R. Masiarz, P. A. Luciw, P. J. Barr, and H. E. Varmus, “Characterization of ribosomal frameshifting in HIV-1 gag-pol expression,” Nature, vol. 331, no. 6153, pp. 280–283, 1988. View at Google Scholar · View at Scopus
  4. P. Biswas, X. Jiang, A. L. Pacchia, J. P. Dougherty, and S. W. Peltz, “The Human Immunodeficiency Virus Type 1 Ribosomal Frameshifting Site Is an Invariant Sequence Determinant and an Important Target for Antiviral Therapy,” Journal of Virology, vol. 78, no. 4, pp. 2082–2087, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. Y. N. Vaishnav and F. Wong-Staal, “The biochemistry of AIDS,” Annual Review of Biochemistry, vol. 60, pp. 577–630, 1991. View at Google Scholar · View at Scopus
  6. R. J. Marcheschi, M. Tonelli, A. Kumar, and S. E. Butcher, “Structure of the HIV-1 frameshift site RNA bound to a small molecule inhibitor of viral replication,” ACS Chemical Biology, vol. 6, no. 8, pp. 857–864, 2011. View at Publisher · View at Google Scholar
  7. J. Tholstrup, L. B. Oddershede, and M. A. Sørensen, “MRNA pseudoknot structures can act as ribosomal roadblocks,” Nucleic Acids Research, vol. 40, no. 1, pp. 303–313, 2012. View at Publisher · View at Google Scholar
  8. P. J. Farabaugh, “Programmed translational frameshifting,” Microbiological Reviews, vol. 60, no. 1, pp. 103–134, 1996. View at Google Scholar · View at Scopus
  9. J. D. Dinman, T. Icho, and R. B. Wickner, “A −1 ribosomal frameshift in a double-stranded RNA virus of yeast forms a gag-pol fusion protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 1, pp. 174–178, 1991. View at Publisher · View at Google Scholar · View at Scopus
  10. E. B. Dam, C. W. A. Pleij, and L. Bosch, “RNA pseudoknots: translational frameshifting and readthrough on viral RNAs,” Virus Genes, vol. 4, no. 2, pp. 121–136, 1990. View at Google Scholar · View at Scopus
  11. I. Brierley, A. J. Jenner, and S. C. Inglis, “Mutational analysis of the 'slippery-sequence' component of a coronavirus ribosomal frameshifting signal,” Journal of Molecular Biology, vol. 227, no. 2, pp. 463–479, 1992. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Jacks, H. D. Madhani, F. R. Masiarz, and H. E. Varmus, “Signals for ribosomal frameshifting in the rous sarcoma virus gag-pol region,” Cell, vol. 55, no. 3, pp. 447–458, 1988. View at Google Scholar · View at Scopus
  13. D. P. Giedroc, C. A. Theimer, and P. L. Nixon, “Structure, stability and function of RNA pseudoknots involved in stimulating ribosomal frameshifting,” Journal of Molecular Biology, vol. 298, no. 2, pp. 167–185, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Green, C. H. Kim, C. Bustamante, and I. Tinoco, “Characterization of the Mechanical Unfolding of RNA Pseudoknots,” Journal of Molecular Biology, vol. 375, no. 2, pp. 511–528, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. I. Brierley and S. Pennell, “Structure and function of the stimulatory RNAs involved in programmed eukaryotic −1 ribosomal frameshifting,” Cold Spring Harbor Symposia on Quantitative Biology, vol. 66, pp. 233–248, 2001. View at Google Scholar · View at Scopus
  16. D. P. Giedroc and P. V. Cornish, “Frameshifting RNA pseudoknots: structure and mechanism,” Virus Research, vol. 139, no. 2, pp. 193–208, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. P. L. Nixon and D. P. Giedroc, “Energetics of a strongly pH dependent RNA tertiary structure a frameshifting pseudoknot,” Journal of Molecular Biology, vol. 296, no. 2, pp. 659–671, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. C. A. Theimer, C. A. Blois, and J. Feigon, “Structure of the human telomerase RNA pseudoknot reveals conserved tertiary interactions essential for function,” Molecular Cell, vol. 17, no. 5, pp. 671–682, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. C.-H. Yu, M. H. Noteborn, C. W. A. Pleij, and R. C. L. Olsthoorn, “Stem-loop structures can effectively substitute for an RNA pseudoknot in −1 ribosomal frameshifting,” Nucleic Acids Research, vol. 39, no. 20, pp. 8952–8959, 2011. View at Publisher · View at Google Scholar
  20. D. W. Staple and S. E. Butcher, “Solution structure and thermodynamic investigation of the HIV-1 frameshift inducing element,” Journal of Molecular Biology, vol. 349, no. 5, pp. 1011–1023, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Hung, P. Patel, S. Davis, and S. R. Green, “Importance of ribosomal frameshifting for human immunodeficiency virus type 1 particle assembly and replication,” Journal of Virology, vol. 72, no. 6, pp. 4819–4824, 1998. View at Google Scholar · View at Scopus
  22. D. Dulude, Y. A. Berchiche, K. Gendron, L. Brakier-Gingras, and N. Heveker, “Decreasing the frameshift efficiency translates into an equivalent reduction of the replication of the human immunodeficiency virus type 1,” Virology, vol. 345, no. 1, pp. 127–136, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Shehu-Xhilaga, S. M. Crowe, and J. Mak, “Maintenance of the Gag/Gag-Pol ratio is important for human immunodeficiency virus type 1 RNA dimerization and viral infectivity,” Journal of Virology, vol. 75, no. 4, pp. 1834–1841, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. I. Brierley and F. J. dos Ramos, “Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV,” Virus Research, vol. 119, no. 1, pp. 29–42, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Brierley, A. J. Jenner, and S. C. Inglis, “Mutational analysis of the 'slippery-sequence' component of a coronavirus ribosomal frameshifting signal,” Journal of Molecular Biology, vol. 227, no. 2, pp. 463–479, 1992. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Kwak, M. W. Park, and S. Jeong, “Annexin A2 binds RNA and reduces the frameshifting efficiency of Infectious Bronchitis Virus,” PLoS ONE, vol. 6, no. 8, 2011. View at Publisher · View at Google Scholar
  27. S.-J. Park, Y.-G. Kim, and H.-J. Park, “Identification of rna pseudoknot-binding ligand that inhibits the −1 ribosomal frameshifting of SARS-coronavirus by structure-based virtual screening,” Journal of the American Chemical Society, vol. 133, no. 26, pp. 10094–10100, 2011. View at Publisher · View at Google Scholar
  28. G. Z. Yusupova, M. M. Yusupov, J. H. D. Cate, and H. F. Noller, “The path of messenger RNA through the ribosome,” Cell, vol. 106, no. 2, pp. 233–241, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Takyar, R. P. Hickerson, and H. F. Noller, “mRNA helicase activity of the ribosome,” Cell, vol. 120, no. 1, pp. 49–58, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Bidou, G. Stahl, B. Grima, H. Liu, M. Cassan, and J. P. Rousset, “In vivo HIV-1 frameshifting efficiency is directly related to the stability of the stem-loop stimulatory signal,” RNA, vol. 3, no. 10, pp. 1153–1158, 1997. View at Google Scholar · View at Scopus
  31. T. M. Hansen, S. Nader S Reihani, L. B. Oddershede, and M. A. Sørensen, “Correlation between mechanical strength of messenger RNA pseudoknots and ribosomal frameshifting,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 14, pp. 5830–5835, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. G. Chen, K. Y. Chang, M. Y. Chou, C. Bustamante, and I. Tinoco, “Triplex structures in an RNA pseudoknot enhance mechanical stability and increase efficiency of −1 ribosomal frameshifting,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 31, pp. 12706–12711, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. X. Chen, M. Chamorro, S. I. Lee et al., “Structural and functional studies of retroviral RNA pseudoknots involved in ribosomal frameshifting: nucleotides at the junction of the two stems are important for efficient ribosomal frameshifting,” EMBO Journal, vol. 14, no. 4, pp. 842–852, 1995. View at Google Scholar · View at Scopus
  34. C. A. Theimer and D. P. Giedroc, “Contribution of the intercalated adenosine at the helical junction to the stability of the gag-pro frameshifting pseudoknot from mouse mammary tumor virus,” RNA, vol. 6, no. 3, pp. 409–421, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. E. P. Plant and J. D. Dinman, “Torsional restraint: a new twist on frameshifting pseudoknots,” Nucleic Acids Research, vol. 33, no. 6, pp. 1825–1833, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. J. D. Dinman, “Ribosomal frameshifting in yeast viruses,” Yeast, vol. 11, no. 12, pp. 1115–1127, 1995. View at Publisher · View at Google Scholar · View at Scopus
  37. K. C. Neuman and S. M. Block, “Optical trapping,” Review of Scientific Instruments, vol. 75, no. 9, pp. 2787–2809, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. K. C. Neuman and A. Nagy, “Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy,” Nature Methods, vol. 5, no. 6, pp. 491–505, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. W. J. Greenleaf, M. T. Woodside, and S. M. Block, “High-resolution, single-molecule measurements of biomolecular motion,” Annual Review of Biophysics and Biomolecular Structure, vol. 36, pp. 171–190, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Dulude, M. Baril, and L. Brakier-Gingras, “Characterization of the frameshift stimulatory signal controlling a programmed −1 ribosomal frameshift in the human immunodeficiency virus type 1,” Nucleic Acids Research, vol. 30, no. 23, pp. 5094–5102, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Mihalusova, J. Y. Wu, and X. Zhuang, “Functional importance of telomerase pseudoknot revealed by single-molecule analysis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 51, pp. 20339–20344, 2011. View at Publisher · View at Google Scholar
  42. G. Chen, J. D. Wen, and I. Tinoco, “Single-molecule mechanical unfolding and folding of a pseudoknot in human telomerase RNA,” RNA, vol. 13, no. 12, pp. 2175–2188, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. E. F. Pettersen, T. D. Goddard, C. C. Huang et al., “UCSF Chimera—a visualization system for exploratory research and analysis,” Journal of Computational Chemistry, vol. 25, no. 13, pp. 1605–1612, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. O. Namy, S. J. Moran, D. I. Stuart, R. J. C. Gilbert, and I. Brierley, “A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting,” Nature, vol. 441, no. 7090, pp. 244–247, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. R. E. Stanley, G. Blaha, R. L. Grodzicki, M. D. Strickler, and T. A. Steitz, “The structures of the anti-tuberculosis antibiotics viomycin and capreomycin bound to the 70S ribosome,” Nature Structural and Molecular Biology, vol. 17, no. 3, pp. 289–293, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. O. Kurkcuoglu, P. Doruker, T. Z. Sen, A. Kloczkowski, and R. L. Jernigan, “The ribosome structure controls and directs mRNA entry, translocation and exit dynamics,” Physical Biology, vol. 5, no. 4, Article ID 046005, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. N. Kirthi, B. Roy-Chaudhuri, T. Kelley, and G. M. Culver, “A novel single amino acid change in small subunit ribosomal protein S5 has profound effects on translational fidelity,” RNA, vol. 12, no. 12, pp. 2080–2091, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Liphardt, B. Onoa, S. B. Smith, Tinoco, and C. Bustamante, “Reversible unfolding of single RNA molecules by mechanical force,” Science, vol. 292, no. 5517, pp. 733–737, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Napthine, J. Liphardt, A. Bloys, S. Routledge, and I. Brierley, “The role of RNA pseudoknot stem 1 length in the promotion of efficient −1 ribosomal frameshifting,” Journal of Molecular Biology, vol. 288, no. 3, pp. 305–320, 1999. View at Publisher · View at Google Scholar · View at Scopus
  50. F. Vanzi, Y. Takagi, H. Shuman, B. S. Cooperman, and Y. E. Goldman, “Mechanical studies of single ribosome/mRNA complexes,” Biophysical Journal, vol. 89, no. 3, pp. 1909–1919, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. P. V. Cornish, D. N. Ermolenko, D. W. Staple et al., “Following movement of the L1 stalk between three functional states in single ribosomes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 8, pp. 2571–2576, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. C. E. Aitken and J. D. Puglisi, “Following the intersubunit conformation of the ribosome during translation in real time,” Nature Structural and Molecular Biology, vol. 17, no. 7, pp. 793–800, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Y. Fei, A. C. Richard, J. E. Bronson, and R. L. Gonzalez Jr, “Transfer RNA-mediated regulation of ribosome dynamics during protein synthesis,” Nature Structural and Molecular Biology, vol. 18, no. 9, pp. U1043–U1051, 2011. View at Publisher · View at Google Scholar
  54. J. Fei, P. Kosuri, D. D. MacDougall, and R. L. Gonzalez, “Coupling of Ribosomal L1 Stalk and tRNA Dynamics during Translation Elongation,” Molecular Cell, vol. 30, no. 3, pp. 348–359, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Fei, J. E. Bronson, J. M. Hofman, R. L. Srinivas, C. H. Wiggins, and R. L. Gonzalez, “Allosteric collaboration between elongation factor G and the ribosomal L1 stalk directs tRNA movements during translation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 37, pp. 15702–15707, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. J. B. Munro, R. B. Altman, C. S. Tung, J. H. D. Cate, K. Y. Sanbonmatsu, and S. C. Blanchard, “Spontaneous formation of the unlocked state of the ribosome is a multistep process,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 2, pp. 709–714, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. S. H. Sternberg, J. Fei, N. Prywes, K. A. McGrath, and R. L. Gonzalez, “Translation factors direct intrinsic ribosome dynamics during translation termination and ribosome recycling,” Nature Structural and Molecular Biology, vol. 16, no. 8, pp. 861–868, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. R. Roy, S. Hohng, and T. Ha, “A practical guide to single-molecule FRET,” Nature Methods, vol. 5, no. 6, pp. 507–516, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Sarkar, R. B. Robertson, and J. M. Fernandez, “Simultaneous atomic force microscope and fluorescence measurements of protein unfolding using a calibrated evanescent wave,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 35, pp. 12882–12886, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. G. Kim, L. Su, S. Maas, A. O'Neill, and A. Rich, “Specific mutations in a viral RNA pseudoknot drastically change ribosomal frameshifting efficiency,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 25, pp. 14234–14239, 1999. View at Publisher · View at Google Scholar · View at Scopus
  61. N. Dolzhanskaya, G. Merz, and R. B. Denman, “Alternative splicing modulates protein arginine methyltransferase-dependent methylation of fragile X syndrome mental retardation protein,” Biochemistry, vol. 45, no. 34, pp. 10385–10393, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Levitt, C. Sander, and P. S. Stern, “Protein normal-mode dynamics: trypsin inhibitor, crambin, ribonuclease and lysozyme,” Journal of Molecular Biology, vol. 181, no. 3, pp. 423–447, 1985. View at Google Scholar · View at Scopus
  63. M. Delarue and Y. H. Sanejouand, “Simplified normal mode analysis of conformational transitions in DNA-dependent polymerases: the Elastic Network Model,” Journal of Molecular Biology, vol. 320, no. 5, pp. 1011–1024, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Wang, A. J. Rader, I. Bahar, and R. L. Jernigan, “Global ribosome motions revealed with elastic network model,” Journal of Structural Biology, vol. 147, no. 3, pp. 302–314, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. B. Brooks and M. Karplus, “Harmonic dynamics of proteins: normal modes and fluctuations in bovine pancreatic trypsin inhibitor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 80, no. 21 I, pp. 6571–6575, 1983. View at Google Scholar · View at Scopus
  66. I. Bahar, A. R. Atilgan, M. C. Demirel, and B. Erman, “Vibrational dynamics of folded proteins: significance of slow and fast motions in relation to function and stability,” Physical Review Letters, vol. 80, no. 12, pp. 2733–2736, 1998. View at Google Scholar · View at Scopus
  67. T. Haliloglu, I. Bahar, and B. Erman, “Gaussian dynamics of folded proteins,” Physical Review Letters, vol. 79, no. 16, pp. 3090–3093, 1997. View at Google Scholar · View at Scopus
  68. K. W. Plaxco, S. Larson, I. Ruczinski et al., “Evolutionary conservation in protein folding kinetics,” Journal of Molecular Biology, vol. 298, no. 2, pp. 303–312, 2000. View at Publisher · View at Google Scholar · View at Scopus
  69. D. K. Klimov and D. Thirumalai, “Native topology determines force-induced unfolding pathways in globular proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 13, pp. 7254–7259, 2000. View at Publisher · View at Google Scholar · View at Scopus
  70. I. Bahar, T. R. Lezon, L. W. Yang, and E. Eyal, “Global dynamics of proteins: bridging between structure and function,” Annual Review of Biophysics, vol. 39, no. 1, pp. 23–42, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. F. Tama, M. Valle, J. Frankt, and C. L. Brooks, “Dynamic reorganization of the functionally active ribosome explored by normal mode analysis and cryo-electron microscopy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 16, pp. 9319–9323, 2003. View at Publisher · View at Google Scholar · View at Scopus
  72. I. Bahar, T. R. Lezon, A. Bakan, and I. H. Shrivastava, “Normal mode analysis of biomolecular structures: functional mechanisms of membrane proteins,” Chemical Reviews, vol. 110, no. 3, pp. 1463–1497, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. E. Eyal and I. Bahar, “Toward a molecular understanding of the anisotropic response of proteins to external forces: insights from elastic network models,” Biophysical Journal, vol. 94, no. 9, pp. 3424–3435, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Frank and R. K. Agrawal, “A ratchet-like inter-subunit reorganization of the ribosome during translocation,” Nature, vol. 406, no. 6793, pp. 318–322, 2000. View at Publisher · View at Google Scholar · View at Scopus
  75. A. Matsumoto and H. Ishida, “Global Conformational Changes of Ribosome Observed by Normal Mode Fitting for 3D Cryo-EM Structures,” Structure, vol. 17, no. 12, pp. 1605–1613, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. S. Uemura, C. E. Aitken, J. Korlach, B. A. Flusberg, S. W. Turner, and J. D. Puglisi, “Real-time tRNA transit on single translating ribosomes at codon resolution,” Nature, vol. 464, no. 7291, pp. 1012–1017, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. A. Kidera, M. Ikeguchi, J. Ueno, and M. Sato, “Protein structural change upon ligand binding: linear response theory,” Physical Review Letters, vol. 94, no. 7, Article ID 078102, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. X. Qu, J.-D. Wen, L. Lancaster, H. F. Noller, C. Bustamante, and I. Tinoco, “The ribosome uses two active mechanisms to unwind messenger RNA during translation,” Nature, vol. 475, no. 7354, pp. 118–121, 2011. View at Publisher · View at Google Scholar
  79. J.-D. Wen, L. Lancaster, C. Hodges et al., “Following translation by single ribosomes one codon at a time,” Nature, vol. 452, no. 7187, pp. 598–603, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. L. G. Trabuco, E. Schreiner, J. Eargle et al., “The Role of L1 Stalk-tRNA Interaction in the Ribosome Elongation Cycle,” Journal of Molecular Biology, vol. 402, no. 4, pp. 741–760, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. F. Grater, J. Shen, H. Jiang, M. Gautel, and H. Grubmüller, “Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations,” Biophysical Journal, vol. 88, no. 2, pp. 790–804, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. E. M. Puchner, A. Alexandrovich, L. K. Ay et al., “Mechanoenzymatics of titin kinase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 36, pp. 13385–13390, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. S. Lange, F. Xiang, A. Yakovenko et al., “Cell biology: the kinase domain of titin controls muscle gene expression and protein turnover,” Science, vol. 308, no. 5728, pp. 1599–1603, 2005. View at Publisher · View at Google Scholar · View at Scopus
  84. M. S. Z. Kellermayer, S. B. Smith, H. L. Granzier, and C. Bustamante, “Folding-unfolding transitions in single titin molecules characterized with laser tweezers,” Science, vol. 276, no. 5315, pp. 1112–1116, 1997. View at Publisher · View at Google Scholar · View at Scopus
  85. E. A. Shank, C. Cecconi, J. W. Dill, S. Marqusee, and C. Bustamante, “The folding cooperativity of a protein is controlled by its chain topology,” Nature, vol. 465, no. 7298, pp. 637–640, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. C. M. Kaiser, D. H. Goldman, J. D. Chodera, I. Tinoco Jr, and C. Bustamante, “The ribosome modulates nascent protein folding,” Science, vol. 334, no. 6063, pp. 1723–1727, 2011. View at Publisher · View at Google Scholar
  87. M. Steiner, K. S. Karunatilaka, R. K. O. Sigel, and D. Rueda, “Single-molecule studies of group II intron ribozymes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 37, pp. 13853–13858, 2008. View at Publisher · View at Google Scholar · View at Scopus
  88. P. Mangeol, T. Bizebard, C. Chiaruttini, M. Dreyfus, M. Springer, and U. Bockelmann, “Probing ribosomal protein-RNA interactions with an external force,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 45, pp. 18272–18276, 2011. View at Publisher · View at Google Scholar
  89. T. G. Kinzy, J. W. Harger, A. Carr-Schmid et al., “New targets for antivirals: the ribosomal A-site and the factors that interact with it,” Virology, vol. 300, no. 1, pp. 60–70, 2002. View at Publisher · View at Google Scholar · View at Scopus
  90. J. D. Dinman, M. J. Ruiz-Echevarria, K. Czaplinski, and S. W. Peltz, “Peptidyl-transferase inhibitors have antiviral properties by altering programmed −1 ribosomal frameshifting efficiencies: development of model systems,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 13, pp. 6606–6611, 1997. View at Publisher · View at Google Scholar · View at Scopus
  91. E. Manktelow, K. Shigemoto, and I. Brierley, “Characterization of the frameshift signal of Edr, a mammalian example of programmed −1 ribosomal frameshifting,” Nucleic Acids Research, vol. 33, no. 5, pp. 1553–1563, 2005. View at Publisher · View at Google Scholar · View at Scopus
  92. N. M. Wills, B. Moore, A. Hammer, R. F. Gesteland, and J. F. Atkins, “A functional −1 ribosomal frameshift signal in the human paraneoplastic Ma3 gene,” Journal of Biological Chemistry, vol. 281, no. 11, pp. 7082–7088, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. M. B. Clark, M. Jänicke, U. Gottesbühren et al., “Mammalian gene PEG10 expresses two reading frames by high efficiency −1 Frameshifting in embryonic-associated tissues,” Journal of Biological Chemistry, vol. 282, no. 52, pp. 37359–37369, 2007. View at Publisher · View at Google Scholar · View at Scopus