Single-molecule measurements of the CCR5 mRNA unfolding pathways

Biophysical Journal

Volumn 106, Issue 1, 2014, Pages 244-252

  De Messieres, Michel ^a   Chang, Jen Chien ^a   Belew, Ashton Trey ^a   Meskauskas, Arturas ^a   Dinman, Jonathan D ^a   La Porta, Arthur ^a  

^a University of Maryland   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCR5 PROTEIN, HUMAN; CHEMOKINE RECEPTOR CCR5; MESSENGER RNA;

ARTICLE; CHEMISTRY; GENETICS; HUMAN; MOLECULAR GENETICS; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE; OPTICAL TWEEZERS; RNA FOLDING; THERMODYNAMICS;

BASE SEQUENCE; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEOTIDE MOTIFS; OPTICAL TWEEZERS; RECEPTORS, CCR5; RNA FOLDING; RNA, MESSENGER; THERMODYNAMICS;

EID: 84891878362     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.09.036     Document Type: Article

References (52)

1. F.H.C. Crick, and L. Barnett R.J. Watts-Tobin General nature of the genetic code for proteins Nature 192 1961 1227 1232
2. J.-D. Wen, and L. Lancaster I. Tinoco Following translation by single ribosomes one codon at a time Nature 452 2008 598 603
3. P.-Y. Liao, and Y.S. Choi K.H. Lee The many paths to frameshifting: kinetic modeling and analysis of the effects of different elongation steps on programmed -1 ribosomal frameshifting Nucleic Acids Res. 39 2011 300 312
4. C.W.A. Pleij, K. Rietveld, and L. Bosch A new principle of RNA folding based on pseudoknotting Nucleic Acids Res. 13 1985 1717 1731
5. D.P. Giedroc, and P.V. Cornish Frameshifting RNA pseudoknots: structure and mechanism Virus Res. 139 2009 193 208
6. O. Namy, and S.J. Moran I. Brierley A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting Nature 441 2006 244 247
7. Z. Tsuchihashi, and A. Kornberg Translational frameshifting generates the γ-subunit of DNA polymerase III holoenzyme Proc. Natl. Acad. Sci. USA 87 1990 2516 2520
8. P.J. Farabaugh Programmed translational frameshifting Annu. Rev. Genet. 30 1996 507 528
9. J.W. Harger, A. Meskauskas, and J.D. Dinman An "integrated model" of programmed ribosomal frameshifting Trends Biochem. Sci. 27 2002 448 454
10. G. Chen, and K.-Y. Chang I. Tinoco Jr. Triplex structures in an RNA pseudoknot enhance mechanical stability and increase efficiency of -1 ribosomal frameshifting Proc. Natl. Acad. Sci. USA 106 2009 12706 12711
11. J.D. Lopinski, J.D. Dinman, and J.A. Bruenn Kinetics of ribosomal pausing during programmed -1 translational frameshifting Mol. Cell. Biol. 20 2000 1095 1103
12. I. Brierley, and F.J. Dos Ramos Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV Virus Res. 119 2006 29 42
13. T. Jacks, and M.D. Power H.E. Varmus Characterization of ribosomal frameshifting in HIV-1 Gag-Pol expression Nature 331 1988 280 283
14. J.D. Dinman, and R.B. Wickner Ribosomal frameshifting efficiency and Gag/Gag-Pol ratio are critical for yeast M1 double-stranded RNA virus propagation J. Virol. 66 1992 3669 3676
15. P. Biswas, and X. Jiang S.W. Peltz The human immunodeficiency virus type 1 ribosomal frameshifting site is an invariant sequence determinant and an important target for antiviral therapy J. Virol. 78 2004 2082 2087
16. I. Brierley, S. Pennell, and R.J.C. Gilbert Viral RNA pseudoknots: versatile motifs in gene expression and replication Nat. Rev. Microbiol. 5 2007 598 610
17. E.P. Plant, and R. Rakauskaite J.D. Dinman Achieving a golden mean: mechanisms by which coronaviruses ensure synthesis of the correct stoichiometric ratios of viral proteins J. Virol. 84 2010 4330 4340
18. T. Jacks, and H.E. Varmus Expression of the Rous sarcoma virus Pol gene by ribosomal frameshifting Science 230 1985 1237 1242
19. A.T. Belew, V.M. Advani, and J.D. Dinman Endogenous ribosomal frameshift signals operate as mRNA destabilizing elements through at least two molecular pathways in yeast Nucleic Acids Res. 39 2011 2799 2808
20. 4+ cells is mediated by the chemokine receptor CC-CKR-5 Nature 381 1996 667 673
21. R.E. Atchison, and J. Gosling M.A. Goldsmith Multiple extracellular elements of CCR5 and HIV-1 entry: dissociation from response to chemokines Science 274 1996 1924 1926
22. D.C. Erik The design of drugs for HIV and HCV Nat. Rev. Drug Disc. 6 2007 1001 1018
23. M. Samson, and F. Libert M. Parmentier Resistance to HIV-1 infection in Caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene Nature 382 1996 722 725
24. T.M. Hansen, and S.N.S. Reihani M.A. Sørensen Correlation between mechanical strength of messenger RNA pseudoknots and ribosomal frameshifting Proc. Natl. Acad. Sci. USA 104 2007 5830 5835
25. K.H. White, and M. Orzechowski K. Visscher Mechanical unfolding of the beet Western yellow virus -1 frameshift signal J. Am. Chem. Soc. 133 2011 9775 9782
26. L. Green, and C.-H. Kim I. Tinoco Jr. Characterization of the mechanical unfolding of RNA pseudoknots J. Mol. Biol. 375 2008 511 528
27. D.B. Ritchie, D.A.N. Foster, and M.T. Woodside Programmed -1 frameshifting efficiency correlates with RNA pseudoknot conformational plasticity, not resistance to mechanical unfolding Proc. Natl. Acad. Sci. USA 109 2012 16167 16172
28. X. Qu, and J.-D. Wen I. Tinoco Jr. The ribosome uses two active mechanisms to unwind messenger RNA during translation Nature 475 2011 118 121
29. H. Kontos, S. Napthine, and I. Brierley Ribosomal pausing at a frameshifter RNA pseudoknot is sensitive to reading phase but shows little correlation with frameshift efficiency Mol. Cell. Biol. 21 2001 8657 8670
30. C.-H. Yu, and M.H. Noteborn R.C.L. Olsthoorn Stem-loop structures can effectively substitute for an RNA pseudoknot in -1 ribosomal frameshifting Nucleic Acids Res. 39 2011 8952 8959
31. J. Tholstrup, L.B. Oddershede, and M.A. Sørensen mRNA pseudoknot structures can act as ribosomal roadblocks Nucleic Acids Res. 40 2012 303 313
32. P.S. Pallan, and W.S. Marshall M. Egli Crystal structure of a luteoviral RNA pseudoknot and model for a minimal ribosomal frameshifting motif Biochemistry 44 2005 11315 11322
33. S. Napthine, and J. Liphardt I. Brierley The role of RNA pseudoknot stem 1 length in the promotion of efficient -1 ribosomal frameshifting J. Mol. Biol. 288 1999 305 320
34. M. de Messieres, B. Brawn-Cinani, and A. La Porta Measuring the folding landscape of a harmonically constrained biopolymer Biophys. J. 100 2011 2736 2744
35. S.J. Koch, and A. Shundrovsky M.D. Wang Probing protein-DNA interactions by unzipping a single DNA double helix Biophys. J. 83 2002 1098 1105
36. M.P. Landry, and P.M. McCall Y.R. Chemla Characterization of photoactivated singlet oxygen damage in single-molecule optical trap experiments Biophys. J. 97 2009 2128 2136
37. K. Svoboda, and S.M. Block Biological applications of optical forces Annu. Rev. Biophys. Biomol. Struct. 23 1994 247 285
38. J.F. Marko, and E.D. Siggia Stretching DNA Macromolecules 28 1995 8759 8770
39. W. Saenger Principles of Nucleic Acid Structure 1988 Springer-Verlag New York
40. M.D. Wang, and H. Yin S.M. Block Stretching DNA with optical tweezers Biophys. J. 72 1997 1335 1346
41. J.-D. Wen, and M. Manosas I. Tinoco Jr. Force unfolding kinetics of RNA using optical tweezers. I. Effects of experimental variables on measured results Biophys. J. 92 2007 2996 3009
42. J. Liphardt, and B. Onoa C. Bustamante Reversible unfolding of single RNA molecules by mechanical force Science 292 2001 733 737
43. A.T. Belew, and N.L. Hepler J.D. Dinman PRFDB: a database of computationally predicted eukaryotic programmed -1 ribosomal frameshift signals BMC Genomics 9 2008 339
44. M. Zuker MFOLD web server for nucleic acid folding and hybridization prediction Nucleic Acids Res. 31 2003 3406 3415
45. A. La Porta, N. Denesyuk, and M. de Messieres Optimal reconstruction of the folding landscape using differential energy surface analysis Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 87 2013 032716
46. O.K. Dudko, G. Hummer, and A. Szabo Intrinsic rates and activation free energies from single-molecule pulling experiments Phys. Rev. Lett. 96 2006 108101
47. E. Evans Probing the relation between force - lifetime - and chemistry in single molecular bonds Annu. Rev. Biophys. Biomol. Struct. 30 2001 105 128
48. C. Jarzynski Nonequilibrium equality for free energy differences Phys. Rev. Lett. 78 1997 2690 2693
49. G.E. Crooks Entropy production fluctuation theorem and the nonequilibrium work relation for free energy differences Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 60 1999 2721 2726
50. G. Hummer, and A. Szabo Free energy profiles from single-molecule pulling experiments Proc. Natl. Acad. Sci. USA 107 2010 21441 21446
51. M.T. Woodside, and W.M. Behnke-Parks S.M. Block Nanomechanical measurements of the sequence-dependent folding landscapes of single nucleic acid hairpins Proc. Natl. Acad. Sci. USA 103 2006 6190 6195
52. S. Biyun, S.S. Cho, and D. Thirumalai Folding of human telomerase RNA pseudoknot using ion-jump and temperature-quench simulations J. Am. Chem. Soc. 133 2011 20634 20643