Accessibility of 18S rRNA in human 40S subunits and 80S ribosomes at physiological magnesium ion concentrations - Implications for the study of ribosome dynamics

RNA

Volumn 11, Issue 12, 2005, Pages 1898-1908

  Shenvi, Christina L ^a   Dong, Ken C ^a   Friedman, Eric M ^a   Hanson, Jeffrey A ^a   Cate, Jamie H D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Chemical probing; Protein synthesis; Ribosome dynamics; Translation initiation

Indexed keywords

MAGNESIUM ION; RNA 18S;

ARTICLE; CONCENTRATION (PARAMETERS); HEPATITIS C VIRUS; INTERNAL RIBOSOME ENTRY SITE; MOLECULAR PROBE; PRIORITY JOURNAL; RIBOSOME; RIBOSOME SUBUNIT; RNA BINDING; RNA CONFORMATION;

HUMANS; MAGNESIUM; MODELS, GENETIC; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA, RIBOSOMAL; RNA, RIBOSOMAL, 18S;

HEPATITIS C VIRUS; MAMMALIA;

EID: 28344456738     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2192805     Document Type: Article

References (68)

1. Abramoff, M.D., Magelhaes, P.J., and Ram, S.J. 2004. Image processing with ImageJ. Biophotonics International 11: 36-42.
2. +/polyamine system for polyuridine-dependent polyphenylalanine synthesis with near in vivo characteristics. Methods Enzymol. 164: 650-658.
3. Bayfield, M.A., Dahlberg, A.E., Schulmeister, U., Dorner, S., and Barta, A. 2001. A conformational change in the ribosomal peptidyl transferase center upon active/inactivetransition. Proc. Natl. Acad. Sci. 98: 10096-10101.
4. Benne, R. and Hershey, J.W. 1976. Purification and characterization of initiation factor IF-E3 from rabbit reticulocytes. Proc. Natl. Acad. Sci. 73: 3005-3009.
5. Cannone, J.J., Subramanian, S., Schnare, M.N., Collett, J.R., D'Souza, L.M., Du, Y., Feng, B., Lin, N., Madabusi, L.V., Muller, K.M., et al. 2002. The comparative RNA web (CRW) site: An online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3: 2.
6. Cate, J.H., Hanna, R.L., and Doudna, J.A. 1997. A magnesium ion core at the heart of a ribozyme domain. Nat. Struct. Biol. 4: 553-558.
7. Cate, J.H., Yusupov, M.M., Yusupova, G.Z., Earnest, T.N., and Noller, H.F. 1999. X-ray crystal structures of 70S ribosome functional complexes. Science 285: 2095-2104.
8. Dahlberg, A.E. 1974. Two forms of the 30S ribosomal subunit of Escherichia coli. J. Biol. Chem. 249: 7673-7678.
9. Dignam, J.D., Martin, P.L., Shastry, B.S., and Roeder, R.G. 1983. Eukaryotic gene transcription with purified components. Methods Enzymol. 101: 582-598.
10. Dontsova, O., Dokudovskaya, S., Kopylov, A., Bogdanov, A., Rinke-Appel, J., Junke, N., and Brimacombe, R. 1992. Three widely separated positions in the 16S RNA lie in or close to the ribosomal decoding region; a site-directed cross-linking study with mRNA analogues. EMBO J. 11: 3105-3116.
11. Doudna, J.A. 1997. Preparation of homogeneous ribozyme RNA for crystallization. Methods Mol. Biol. 74: 365-370.
12. Falvey, A.K. and Staehelin, T. 1970a. Structure and function of mammalian ribosomes. I. Isolation and characterization of active liver ribosomal subunits. J. Mol. Biol. 53: 1-19.
13. _. 1970b. Structure and function of mammalian ribosomes. II. Exchange of ribosomal subunits at various stages of in vitro polypeptide synthesis. J. Mol. Biol. 53: 21-34.
14. Frank, J. and Agrawal, R.K. 2000. A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406: 318-322.
15. Gao, N., Zavialov, A.V., Li, W., Sengupta, J., Valle, M., Gursky, R.P., Ehrenberg, M., and Frank, J. 2005. Mechanism for the disassembly of the posttermination complex inferred from cryo-EM studies. Mol. Cell 18: 663-674.
16. Goss, D.J. and Harrigan, T. 1986. Magnesium ion dependent equilibria, kinetics, and thermodynamic parameters of Artemia ribosome dissociation and subunit association. Biochemistry 25: 3690-3695.
17. Gromadski, K.B. and Rodnina, M.V. 2004. Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Mol. Cell 13: 191-200.
18. Hoa, G.H.B., Begard, E., Beaudry, P., Maurel, P., Grunberg-Manago, M., and Douzou, P. 1980. Analysis of cosolvent and divalent cation effects on association equilibrium and activity of ribosomes. Biochemistry 19: 3080-3087.
19. Holden, K.L. and Harris, E. 2004. Enhancement of dengue virus translation: Role of the 3′ untranslated region and the terminal 3′ stem-loop domain. Virology 329: 119-133.
20. Holmberg, L., Melander, Y., and Nygard, O. 1994. Probing the conformational changes in 5.8S, 18S and 28S rRNA upon association of derived subunits into complete 80S ribosomes. Nucleic Acids Res. 22: 2776-2783.
21. Jackson, R.J. and Hunt, T. 1983. Preparation and use of nuclease-treated rabbit reticulocyte lysates for the translation of eukaryotic messenger RNA. Methods Enzymol. 96: 50-74.
22. Jan, E. and Sarnow, P. 2002. Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus. J. Mol. Biol. 324: 889-902.
23. Jelenc, P.C. and Kurland, C.G. 1979. Nucleoside triphosphate regeneration decreases the frequency of translation errors. Proc. Natl. Acad. Sci. 76: 3174-3178.
24. Jenner, L., Romby, P., Rees, B., Schulze-Briese, C., Springer, M., Ehresmann, C., Ehresmann, B., Moras, D., Yusupova, G., and Yusupov, M. 2005. Translational operator ofmRNA on the ribosome: How repressor proteins exclude ribosome binding. Science 308: 120-123.
25. Kieft, J.S., Zhou, K., Jubin, R., Murray, M.G., Lau, J.Y., and Doudna, J.A. 1999. The hepatitis C virus internal ribosome entry site adopts an ion-dependent tertiary fold. J. Mol. Biol. 292: 513-529.
26. Klaholz, B.P., Myasnikov, A.G., and Van Heel, M. 2004. Visualization of release factor 3 on the ribosome during termination of protein synthesis. Nature 427: 862-865.
27. Klein, D.J., Moore, P.B., and Steitz, T.A. 2004. The contribution of metal ions to the structural stability of the large ribosomal subunit. RNA 10: 1366-1379.
28. Kozak, M. 1990. Evaluation of the fidelity of initiation of translation in reticulocyte lysates from commercial sources. Nucleic Acids Res. 18: 2828.
29. Merryman, C. and Noller, H.F. 1998. Footprinting and modificationinterference analysis of binding sites on RNA. In RNA:protein interactions-A practical approach (ed. SmithC.W.J. ), pp. 237-253. Oxford University Press, Oxford, UK.
30. Merryman, C., Moazed, D., McWhirter, J., and Noller, H.F. 1999. Nucleotides in 16S rRNA protected by the association of 30S and 50S ribosomal subunits. J. Mol. Biol. 285: 97-105.
31. Moazed, D. and Noller, H.F. 1986. Transfer RNA shields specific nucleotides in 16S ribosomal RNA from attack by chemical probes. Cell 47: 985-994.
32. _. 1987. Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature 327: 389-394.
33. Moazed, D., Van Stolk, B.J., Douthwaite, S., and Noller, H.F. 1986. Interconversion of active and inactive 30 S ribosomal subunits is accompanied by a conformational change in the decoding region of 16 S rRNA. J. Mol. Biol. 191: 483-493.
34. Moine, H., Ehresmann, B., Ehresmann, C., and Romby, P. 1998. Probing RNA structure and function in solution. In RNA structure and function (eds. R.W. Simons and M. Grunberg-Manago), pp. 77-116. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
35. a in the ribosomal peptidyl transferase center. Science 289: 947-950.
36. Muth, G.W., Chen, L., Kosek, A.B., and Strobel, S.A. 2001. pH-dependent conformational flexibility within the ribosomal peptidyl transferase center. RNA 7: 1403-1415.
37. Ogle, J.M., Murphy, F.V., Tarry, M.J., and Ramakrishnan, V. 2002. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111: 721-732.
38. Otto, G.A., Lukavsky, P.J., Lancaster, A.M., Sarnow, P., and Puglisi, J.D. 2002. Ribosomal proteins mediate the hepatitis C virus IRES-HeLa 40S interaction. Mol. Cell. Biol. 8: 913-923.
39. Pape, T., Wintermeyer, W., and Rodnina, M.V. 2000. Conformational switch in the decoding region of 16S rRNA during aminoacyl-tRNA selection on the ribosome. Nat. Struct. Biol. 7: 104-107.
40. Pelham, H.R.B. and Jackson, R.J. 1976. An efficient mRNA-dependent translation system from reticulocyte lysates. Eur. J. Biochem. 67: 247-256.
41. Peske, F., Savelsbergh, A., Katunin, V.I., Rodnina, M.V., and Wintermeyer, W. 2004. Conformational changes of the small ribosomal subunit during elongation factor G-dependent tRNA-mRNA translocation. J. Mol. Biol. 343: 1183-1194.
42. Rinke-Appel, J., Junke, N., Stade, K., and Brimacombe, R. 1991. The path of mRNA through the Escherichia coli ribosome; site-directed cross-linking of mRNA analogues carrying a photoreactive label at various points 3′ to the decoding site. EMBO J. 10: 2195-2202.
43. Savelsbergh, A., Katunin, V.I., Mohr, D., Peske, F., Rodnina, M.V., and Wintermeyer, W. 2003. An elongation factor G-induced ribosome rearrangement precedes tRNA-mRNA translocation. Mol. Cell 11: 1517-1523.
44. Schilling-Bartetzko, S., Bartetzko, A., and Nierhaus, K.H. 1992. Kinetic and thermodynamic parameters for tRNA binding to the ribosome and for the translocation reaction. J. Biol. Chem. 267: 4703-4712.
45. Schuwirth, B.S., Borovinskaya, M.A., Hau, C.W., Zhang, W., Vila-Sanjurjo, A., Holton, J.M., and Cate, J.H.D. 2005. Structures of the bacterial ribosome at 3.5 Å resolution. Science (in press).
46. Sloma, M.S. and Nygard, O. 2001. Chemical accessibility of 18S rRNA in native ribosomal complexes: Interaction sites of mRNA, tRNA and translation factors. Biol. Chem. 382: 661-668.
47. Spahn, C.M., Beckmann, R., Eswar, N., Penczek, P.A., Sali, A., Blobel, G., and Frank, J. 2001a. Structure of the 80S ribosome from Saccharomyces cerevisiae-tRNA-ribosome and subunit-subunit interactions. Cell 107: 373-386.
48. Spahn, C.M., Kieft, J.S., Grassucci, R.A., Penczek, P.A., Zhou, K., Doudna, J.A., and Frank, J. 2001b. Hepatitis C virus IRES RNA-induced changes in the conformation of the 40s ribosomal subunit. Science 291: 1959-1962.
49. Spahn, C.M., Gomez-Lorenzo, M.G., Grassucci, R.A., Jorgensen, R., Andersen, G.R., Beckmann, R., Penczek, P.A., Ballesta, J.P., and Frank, J. 2004a. Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J. 23: 1008-1019.
50. Spahn, C.M., Jan, E., Mulder, A., Grassucci, R.A., Sarnow, P., and Frank, J. 2004b. Cryo-EM visualization of a viral internal ribosome entry site bound to human ribosomes: The IRES functions as an RNA-based translation factor. Cell 118: 465-475.
51. Sperrazza, J.M. and Spremulli, L.L. 1983. Quantitation of cation binding to wheat germ ribosomes: Influences on subunit association equilibria and ribosome activity. Nucleic Acids Res. 11: 2665-2679.
52. Sperrazza, J.M., Russell, D.W., and Spremulli, L.L. 1980. Reversible dissociation of wheat germ ribosomal subunits: Cation-dependent equilibria and thermodynamic parameters. Biochemistry 19: 1053-1058.
53. Stark, H., Rodnina, M.V., Wieden, H.J., van Heel, M., and Wintermeyer, W. 2000. Large-scale movement of elongation factor G and extensive conformational change of the ribosome during translocation. Cell 100: 301-309.
54. Stark, H., Rodnina, M.V., Wieden, H.J., Zemlin, F., Wintermeyer, W., and van Heel, M. 2002. Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex. Nat. Struct. Biol. 9: 849-854.
55. Sundkvist, I.C.,McKeehan,W.L., Schreier,M.H., and Staehelin, T. 1974. Initiation factor activity associated with free 40 S subunits from rat liver and rabbit reticulocytes. J. Biol. Chem. 249: 6512-6516.
56. Triana-Alonso, F.J., Chakraburtty, K., and Nierhaus, K.H. 1995. The elongation factor 3 unique in higher fungi and essential for protein biosynthesis is an E site factor. J. Biol. Chem. 270:20473-20478.
57. Valle, M., Zavialov, A., Li, W., Stagg, S.M., Sengupta, J., Nielsen, R.C., Nissen, P., Harvey, S.C., Ehrenberg, M., and Frank, J. 2003a. Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy. Nat. Struct. Biol. 10: 899-906.
58. Valle, M., Zavialov, A., Sengupta, J., Rawat, U., Ehrenberg, M., and Frank, J. 2003b. Locking and unlocking of ribosomal motions. Cell 114: 123-134.
59. VanLoock, M.S., Agrawal, R.K., Gabashvili, I.S., Qi, L., Frank, J., and Harvey, S.C. 2000. Movement of the decoding region of the 16 S ribosomal RNA accompanies tRNA translocation. J. Mol. Biol. 304: 507-515.
60. Velichutina, I.V., Dresios, J., Hong, J.Y., Li, C., Mankin, A., Synetos, D., and Liebman, S.W. 2000. Mutations in helix 27 of the yeast Saccharomyces cerevisiae 18S rRNA affect the function of the decoding center of the ribosome. RNA 6: 1174-1184.
61. Vila-Sanjurjo, A., Ridgeway, W.K., Seymaner, V., Zhang, W., Santoso, S., Yu, K., and Cate, J.H. 2003. X-ray crystal structures of the WT and a hyper-accurate ribosome from Escherichia coli. Proc. Natl. Acad. Sci. 100: 8682-8687.
62. Wilson, J.E., Pestova, T.V., Hellen, C.U., and Sarnow, P. 2000. Initiation of protein synthesis from the A site of the ribosome. Cell 102: 511-520.
63. Wimberly, B.T., Brodersen, D.E., Clemons Jr., W.M., Morgan-Warren, R.J., Carter, A.P., Vonrhein, C., Hartsch, T., and Ramakrishnan, V. 2000. Structure of the 30S ribosomal subunit. Nature 407: 327-339.
64. Yusupov, M.M., Yusupova, G.Z., Baucom, A., Lieberman, K., Earnest, T.N., Cate, J.H.D., and Noller, H.F. 2001. Crystal structure of the ribosome at 5.5Å resolution. Science 292: 883-896.
65. Yusupova, G.Z., Yusupov, M.M., Cate, J.H., and Noller, H.F. 2001. The path of messenger RNA through the ribosome. Cell 106: 233-241.
66. Zamir, A., Miskin, R., and Elson, D. 1969. Interconversions between inactive and active forms of ribosomal subunits. FEBS Lett. 3: 85-88.
67. _. 1971. Inactivation and reactivation of ribosomal subunits: Amino acyl-transfer RNA binding activity of the 30 S subunit of Escherichia coli. J. Mol. Biol. 60: 347-364.
68. Zamir, A., Miskin, R., Vogel, Z., and Elson, D. 1974. The inactivation and reactivation of Escherichia coli ribosomes. Methods Enzymol. 30: 406-426.