Single-molecule mechanical unfolding and folding of a pseudoknot in human telomerase RNA

RNA

Volumn 13, Issue 12, 2007, Pages 2175-2188

  Chen, Gang ^a   Wen, Jin Der ^a   Tinoco Jr , Ignacio ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Folding pathways; Force jump drop; Optical tweezers; Single molecule; Telomerase RNA pseudoknot; Unfolding folding kinetics

Indexed keywords

RNA; SODIUM CHLORIDE; TELOMERASE;

ARTICLE; PRIORITY JOURNAL; ROOM TEMPERATURE;

CLONING, MOLECULAR; FREEZING; HUMANS; KINETICS; NUCLEIC ACID CONFORMATION; OPERON; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; RNA; TELOMERASE;

EID: 36248968677     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.676707     Document Type: Article

References (72)

1. Ansari, A., Kuznetsov, S.V., and Shen, Y. 2001. Configurational diffusion down a folding funnel describes the dynamics of DNA hairpins. Proc. Natl. Acad. Sci. 98: 7771-7776.
2. Antal, M., Boros, E., Solymosy, F., and Kiss, T. 2002. Analysis of the structure of human telomerase RNA in vivo. Nucleic Acids Res. 30: 912-920. doi: 10.1093/nar/30.4.912.
3. Autexier, C. and Lue, N.F. 2006. The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem. 75: 493-517.
4. Batey, R.T. and Williamson, J.R. 1998. Effects of polyvalent cations on the folding of an rRNA three-way junction and binding of ribosomal protein S15. RNA 4: 984-997.
5. Blackburn, E.H. 2006. Telomerase RNA. In The RNA world (eds. R.F. Gesteland et al.), pp. 419-436. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
6. Bokinsky, G., Rueda, D., Misra, V.K., Rhodes, M.M., Gordus, A., Babcock, H.P., Walter, N.G., and Zhuang, X. 2003. Single-molecule transition-state analysis of RNA folding. Proc. Natl. Acad. Sci. 100: 9302-9307.
7. Buchmueller, K.L. and Weeks, K.M. 2003. Near native structure in an RNA collapsed state. Biochemistry 42: 13869-13878.
8. Bustamante, C., Marko, J.F., Siggia, E.D., and Smith, S. 1994. Entropic elasticity of λ-phage DNA. Science 265: 1599-1600.
9. Bustamante, C., Chemla, Y.R., Forde, N.R., and Izhaky, D. 2004. Mechanical processes in biochemistry. Annu. Rev. Biochem. 73: 705-748.
10. Cao, S. and Chen, S.J. 2007. Biphasic folding kinetics of RNA pseudoknots and telomerase RNA activity. J. Mol. Biol. 367: 909-924.
11. +-induced changes in the HIV-1 TAR conformational dynamics using NMR residual dipolar couplings: New insights into the role of counterions and electrostatic interactions in adaptive recognition. Biochemistry 46: 6525-6535.
12. Cech, T.R. 2004. Beginning to understand the end of the chromosome. Cell 116: 273-279.
13. Chadalavada, D.M., Senchak, S.E., and Bevilacqua, P.C. 2002. The folding pathway of the genomic hepatitis delta virus ribozyme is dominated by slow folding of the pseudoknots. J. Mol. Biol. 317: 559-575.
14. Chen, J.L. and Greider, C.W. 2004. Telomerase RNA structure and function: Implications for dyskeratosis congenita. Trends Biochem. Sci. 29: 183-192.
15. Chen, J.L. and Greider, C.W. 2005. Functional analysis of the pseudoknot structure in human telomerase RNA. Proc. Natl. Acad. Sci. 102: 8080-8085.
16. Chen, G. and Turner, D.H. 2006. Consecutive GA pairs stabilize medium-size RNA internal loops. Biochemistry 45: 4025-4043.
17. Collins, K. 2006. The biogenesis and regulation of telomerase holoenzymes. Nat. Rev. Mol. Cell Biol. 7: 484-494.
18. Comolli, L.R., Smirnov, I., Xu, L., Blackburn, E.H., and James, T.L. 2002. A molecular switch underlies a human telomerase disease. Proc. Natl. Acad. Sci. 99: 16998-17003.
19. Fang, X.W., Thiyagarajan, P., Sosnick, T.R., and Pan, T. 2002. The rate-limiting step in the folding of a large ribozyme without kinetic traps. Proc. Natl. Acad. Sci. 99: 8518-8523.
20. Gavory, G., Symmons, M.F., Krishnan Ghosh, Y., Klenerman, D., and Balasubramanian, S. 2006. Structural analysis of the catalytic core of human telomerase RNA by FRET and molecular modeling. Biochemistry 45: 13304-13311.
21. Gesteland, R.F., Cech, T.R., and Atkins, J.F., eds. 2006. The RNA world. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
22. Green, L., Kim, C.H., Bustamante, C., and Tinoco Jr., I. 2007. Characterization of the mechanical unfolding of RNA pseudoknots. J. Mol. Biol. (in press). doi: 10.1016/j.jmb.2007.05.058.
23. Ha, T., Zhuang, X., Kim, H.D., Orr, J.W., Williamson, J.R., and Chu, S. 1999. Ligand-induced conformational changes observed in single RNA molecules. Proc. Natl. Acad. Sci. 96: 9077-9082.
24. Hansen, T.M., Reihani, S.N., Oddershede, L.B., and Sorensen, M.A. 2007. Correlation between mechanical strength of messenger RNA pseudoknots and ribosomal frameshifting. Proc. Natl. Acad. Sci. 104: 5830-5835.
25. Hodak, J.H., Downey, C.D., Fiore, J.L., Pardi, A., and Nesbitt, D.J. 2005. Docking kinetics and equilibrium of a GAAA tetraloop-receptor motif probed by single-molecule FRET. Proc. Natl. Acad. Sci. 102: 10505-10510.
26. Hyeon, C. and Thirumalai, D. 2006. Forced-unfolding and force-quench refolding of RNA hairpins. Biophys. J. 90: 3410-3427.
27. Legassie, J.D. and Jarstfer, M.B. 2006. The unmasking of telomerase. Structure 14: 1603-1609.
28. Leontis, N.B., Lescoute, A., and Westhof, E. 2006. The building blocks and motifs of RNA architecture. Curr. Opin. Struct. Biol. 16: 279-287.
29. Leulliot, N. and Varani, G. 2001. Current topics in RNA-protein recognition: Control of specificity and biological function through induced fit and conformational capture. Biochemistry 40: 7947-7956.
30. Li, P.T.X., Bustamante, C., and Tinoco Jr., I. 2006a. Unusual mechanical stability of a minimal RNA kissing complex. Proc. Natl. Acad. Sci. 103: 15847-15852.
31. Li, P.T.X., Collin, D., Smith, S.B., Bustamante, C., and Tinoco Jr., I. 2006b. Probing the mechanical folding kinetics of TAR RNA by hopping, force-jump, and force-ramp methods. Biophys. J. 90: 250-260.
32. Li, P.T.X., Bustamante, C., and Tinoco Jr., I. 2007. Real-time control of the energy landscape by force directs the folding of RNA molecules. Proc. Natl. Acad. Sci. 104: 7039-7044.
33. Liphardt, J., Onoa, B., Smith, S.B., Tinoco Jr., I., and Bustamante, C. 2001. Reversible unfolding of single RNA molecules by mechanical force. Science 292: 733-737.
34. Lu, Z.J., Turner, D.H., and Mathews, D.H. 2006. A set of nearest neighbor parameters for predicting the enthalpy change of RNA secondary structure formation. Nucleic Acids Res. 34: 4912-4924. doi: 10.1093/nar/gkl472.
35. Ma, H., Proctor, D.J., Kierzek, E., Kierzek, R., Bevilacqua, P.C., and Gruebele, M. 2006. Exploring the energy landscape of a small RNA hairpin. J. Am. Chem. Soc. 128: 1523-1530.
36. Ma, H., Wan, C., Wu, A., and Zewail, A.H. 2007. DNA folding and melting observed in real time redefine the energy landscape. Proc. Natl. Acad. Sci. 104: 712-716.
37. Manosas, M., Collin, D., and Ritort, F. 2006. Force-dependent fragility in RNA hairpins. Phys. Rev. Lett. 96: 218-301.
38. Manosas, M., Wen, J.D., Li, P.T.X., Smith, S.B., Bustamante, C., Tinoco Jr., I., and Ritort, F. 2007. Force unfolding kinetics of RNA using optical tweezers. II. Modeling experiments. Biophys. J. 92: 3010-3021.
39. Mathews, D.H., Disney, M.D., Childs, J.L., Schroeder, S.J., Zuker, M., and Turner, D.H. 2004. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc. Natl. Acad. Sci. 101: 7287-7292.
40. Nahas, M.K., Wilson, T.J., Hohng, S., Jarvie, K., Lilley, D.M.J., and Ha, T. 2004. Observation of internal cleavage and ligation reactions of a ribozyme. Nat. Struct. Mol. Biol. 11: 1107-1113.
41. Onoa, B., Dumont, S., Liphardt, J., Smith, S.B., Tinoco Jr., I., and Bustamante, C. 2003. Identifying kinetic barriers to mechanical unfolding of the T. thermophila ribozyme. Science 299: 1892-1895.
42. Perez-Salas, U.A., Rangan, P., Krueger, S., Briber, R.M., Thirumalai, D., and Woodson, S.A. 2004. Compaction of a bacterial group I ribozyme coincides with the assembly of core helices. Biochemistry 43: 1746-1753.
43. Pleij, C.W., Rietveld, K., and Bosch, L. 1985. A new principle of RNA folding based on pseudoknotting. Nucleic Acids Res. 13: 1717-1731. doi: 10.1093/nar/13.5.1717.
44. Puglisi, J.D., Wyatt, J.R., and Tinoco Jr., I. 1988. A pseudoknotted RNA oligonucleotide. Nature 331: 283-286.
45. Reipa, V., Niaura, G., and Atha, D.H. 2007. Conformational analysis of the telomerase RNA pseudoknot hairpin by Raman spectroscopy. RNA 13: 108-115.
46. Russell, R., Das, R., Suh, H., Travers, K.J., Laederach, A., Engelhardt, M.A., and Herschlag, D. 2006. The paradoxical behavior of a highly structured misfolded intermediate in RNA folding. J. Mol. Biol. 363: 531-544.
47. Serra, M.J., Axenson, T.J., and Turner, D.H. 1994. A model for the stabilities of RNA hairpins based on a study of the sequence dependence of stability for hairpins of six nucleotides. Biochemistry 33: 14289-14296.
48. Smith, S.B., Cui, Y., and Bustamante, C. 1996. Overstretching B-DNA: The elastic response of individual double-stranded and single-stranded DNA molecules. Science 271: 795-799.
49. 2+ ions. Biochemistry 46: 2973-2983.
50. Staple, D.W. and Butcher, S.E. 2005. Pseudoknots: RNA structures with diverse functions. PLoS Biol. 3: e213. doi: 10.1371/journal.pbio. 0030213.
51. Stone, M.D., Mihalusova, M., O'Connor, C.M., Prathapam, R., Collins, K., and Zhuang, X. 2007. Stepwise protein-mediated RNA folding directs assembly of telomerase ribonucleoprotein. Nature 446: 458-461.
52. Su, L., Chen, L., Egli, M., Berger, J.M., and Rich, A. 1999. Minor groove RNA triplex in the crystal structure of a ribosomal frameshifting viral pseudoknot. Nat. Struct. Biol. 6: 285-292.
53. Tan, E., Wilson, T.J., Nahas, M.K., Clegg, R.M., Lilley, D.M.J., and Ha, T. 2003. A four-way junction accelerates hairpin ribozyme folding via a discrete intermediate. Proc. Natl. Acad. Sci. 100: 9308-9313.
54. Theimer, C.A. and Feigon, J. 2006. Structure and function of telomerase RNA. Curr. Opin. Struct. Biol. 16: 307-318.
55. Theimer, C.A. and Giedroc, D.P. 2000. Contribution of the intercalated adenosine at the helical junction to the stability of the gagpro frameshifting pseudoknot from mouse mammary tumor virus. RNA 6: 409-421.
56. Theimer, C.A., Finger, L.D., Trantirek, L., and Feigon, J. 2003. Mutations linked to dyskeratosis congenita cause changes in the structural equilibrium in telomerase RNA. Proc. Natl. Acad. Sci. 100: 449-454.
57. Theimer, C.A., Blois, C.A., and Feigon, J. 2005. Structure of the human telomerase RNA pseudoknot reveals conserved tertiary interactions essential for function. Mol. Cell 17: 671-682.
58. Tinoco Jr., I. 1996. Nucleic acid structures, energetics, and dynamics. J. Phys. Chem. 100: 13311-13322.
59. Tinoco Jr., I. 2004. Force as a useful variable in reactions: Unfolding RNA. Annu. Rev. Biophys. Biomol. Struct. 33: 363-385.
60. Tinoco Jr., I. and Bustamante, C. 1999. How RNA folds. J. Mol. Biol. 293: 271-281.
61. Tinoco Jr., I., Uhlenbeck, O.C., and Levine, M.D. 1971. Estimation of secondary structure in ribonucleic acids. Nature 230: 362-367.
62. Tinoco Jr., I., Li, P.T.X., and Bustamante, C. 2006. Determination of thermodynamics and kinetics of RNA reactions by force. Q. Rev. Biophys. 39: 325-360.
63. Turner, D.H. 2000. Conformational changes. In Nucleic acids: Structures, properties, and functions (eds. V.A. Bloomfield et al.), pp. 259-334. University Science Books, Sausalito, CA.
64. Vieregg, J.R. and Tinoco Jr., I. 2006. Modeling RNA folding under mechanical tension. Mol. Phys. 104: 1343-1352.
65. Walther, K.A., Grater, F., Dougan, L., Badilla, C.L., Berne, B.J., and Fernandez, J.M. 2007. Signatures of hydrophobic collapse in extended proteins captured with force spectroscopy. Proc. Natl. Acad. Sci. 104: 7916-7921.
66. Weeks, K.M. and Cech, T.R. 1996. Assembly of a ribonucleoprotein catalyst by tertiary structure capture. Science 271: 345-348.
67. Wen, J.D., Manosas, M., Li, P.T.X., Smith, S.B., Bustamante, C., Ritort, F., and Tinoco Jr., I. 2007. Force unfolding kinetics of RNA using optical tweezers. I. Effects of experimental variables on measured results. Biophys. J. 92: 2996-3009.
68. Woodside, M.T., Anthony, P.C., Behnke-Parks, W.M., Larizadeh, K., Herschlag, D., and Block, S.M. 2006a. Direct measurement of the full, sequence-dependent folding landscape of a nucleic acid. Science 314: 1001-1004.
69. Woodside, M.T., Behnke-Parks, W.M., Larizadeh, K., Travers, K., Herschlag, D., and Block, S.M. 2006b. Nanomechanical measurements of the sequence-dependent folding landscapes of single nucleic acid hairpins. Proc. Natl. Acad. Sci. 103: 6190-6195.
70. Wyatt, J.R., Puglisi, J.D., and Tinoco Jr., I. 1990. RNA pseudoknots: Stability and loop size requirements. J. Mol. Biol. 214: 455-470.
71. Xia, T., SantaLucia Jr., J., Burkard, M.E., Kierzek, R., Schroeder, S.J., Jiao, X., Cox, C., and Turner, D.H. 1998. Thermodynamic parameters for an expanded nearest-neighbor model for formation of RNA duplexes with Watson-Crick base pairs. Biochemistry 37: 14719-14735.
72. Yingling, Y.G. and Shapiro, B.A. 2005. Dynamic behavior of the telomerase RNA hairpin structure and its relationship to dyskeratosis congenita. J. Mol. Biol. 348: 27-42.