Slow formation of stable complexes during coincubation of minimal rRNA and ribosomal protein S4

Journal of Molecular Biology

Volumn 412, Issue 3, 2011, Pages 453-465

  Mayerle, Megan ^a   Bellur, Deepti L ^a   Woodson, Sarah A ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

conformational change; RNA folding; RNA protein interaction; SHAPE; stable complex

Indexed keywords

PROTEIN S 4; RIBOSOME PROTEIN; RNA 16S; UNCLASSIFIED DRUG;

ACYLATION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; INCUBATION TEMPERATURE; INCUBATION TIME; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN RNA BINDING; PROTEIN STRUCTURE;

EID: 80052390494     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.07.048     Document Type: Article

References (57)

1. Powers T., Daubresse G., and Noller H.F. Dynamics of in vitro assembly of 16S rRNA into 30S ribosomal subunits J. Mol. Biol. 232 1993 362 374 10.1006/jmbi.1993.1396 (Pubitemid 23251165)
2. Talkington M.W., Siuzdak G., and Williamson J.R. An assembly landscape for the 30S ribosomal subunit Nature 438 2005 628 632 10.1038/nature04261 (Pubitemid 41740567)
3. Nowotny V., and Nierhaus K.H. Assembly of the 30S subunit from Escherichia coli ribosomes occurs via two assembly domains which are initiated by S4 and S7 Biochemistry 27 1988 7051 7055
4. Weitzmann C.J., Cunningham P.R., Nurse K., and Ofengand J. Chemical evidence for domain assembly of the Escherichia coli 30S ribosome FASEB J. 7 1993 177 180 (Pubitemid 23034031)
5. Held W.A., Ballou B., Mizushima S., and Nomura M. Assembly mapping of 30S ribosomal proteins from Escherichia coli. Further studies J. Biol. Chem. 249 1974 3103 3111
6. Williamson J.R. Induced fit in RNA-protein recognition Nat. Struct. Biol. 7 2000 834 837 10.1038/79575
7. Draper D.E., and Reynaldo L.P. RNA binding strategies of ribosomal proteins Nucleic Acids Res. 27 1999 381 388 (Pubitemid 29209998)
8. Leulliot N., and Varani G. Current topics in RNA-protein recognition: control of specificity and biological function through induced fit and conformational capture Biochemistry 40 2001 7947 7956 (Pubitemid 32641191)
9. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., and Cate J.H. Structures of the bacterial ribosome at 3.5 Å resolution Science 310 2005 827 834 10.1126/science.1117230 (Pubitemid 41567336)
10. Bellur D.L., and Woodson S.A. A minimized rRNA-binding site for ribosomal protein S4 and its implication for 30S assembly Nucleic Acids Res. 37 2009 1886 10.1093/nar/gkp036
11. Adilakshmi T., Bellur D.L., and Woodson S.A. Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly Nature 455 2008 1268 1272 10.1038/nature07298
12. Powers T., and Noller H.F. A temperature-dependent conformational rearrangement in the ribosomal protein S4•16S rRNA complex J. Biol. Chem. 270 1995 1238 1242
13. Zimmerman R.A., Muto A., Fellner P., Ehresmann C., and Branlant C. Location of ribosomal protein binding sites on 16S ribosomal RNA Proc. Natl Acad. Sci. USA 69 1972 1282 1296
14. Mackie G.A., and Zimmermann R.A. RNA-protein interactions in the ribosome: IV. Structure and properties of binding sites for proteins S4, S16/S17 and S20 in the 16S RNA J. Mol. Biol. 121 1978 17 39 (Pubitemid 8353753)
15. Osswald M., Greuer B., Brimacombe R., Stoffler G., Baumert H., and Fasold H. RNA-protein cross-linking in Escherichia coli 30S ribosomal subunits; determination of sites on 16S RNA that are cross-linked to proteins S3, S4, S5, S7, S8, S9, S11, S13, S19 and S21 by treatment with methyl p-azidophenyl acetimidate Nucleic Acids Res. 15 1987 3221 3240
16. Stern S., Wilson R.C., and Noller H.F. Localization of the binding site for protein S4 on 16S ribosomal RNA by chemical and enzymatic probing and primer extension J. Mol. Biol. 192 1986 101 110
17. Vartikar J.V., and Draper D.E. S4-16S ribosomal RNA complex. Binding constant measurements and specific recognition of a 460-nucleotide region J. Mol. Biol. 209 1989 221 234 (Pubitemid 19237385)
18. Powers T., and Noller H.F. Hydroxyl radical footprinting of ribosomal proteins on 16S rRNA RNA 1 1995 194 209
19. Wimberly B.T., Brodersen D.E., Clemons W.M. Jr, Morgan-Warren R.J., Carter A.P., and Vonrhein C. Structure of the 30S ribosomal subunit Nature 407 2000 327 339 10.1038/35030006
20. Ramaswamy P., and Woodson S.A. Global stabilization of rRNA structure by ribosomal proteins S4, S17, and S20 J. Mol. Biol. 392 2009 666 677 10.1016/j.jmb.2009.07.032
21. Noller H.F. Biochemical characterization of the ribosomal decoding site Biochimie 88 2006 935 941 10.1016/j.biochi.2006.04.006 (Pubitemid 44308503)
22. Gerstner R.B., Pak Y., and Draper D.E. Recognition of 16S rRNA by ribosomal protein S4 from Bacillus stearothermophilus Biochemistry 40 2001 7165 7173 (Pubitemid 32554040)
23. Dutca L.M., Jagannathan I., Grondek J.F., and Culver G.M. Temperature-dependent RNP conformational rearrangements: analysis of binary complexes of primary binding proteins with 16S rRNA J. Mol. Biol. 368 2007 853 869 10.1016/j.jmb.2007.02.064 (Pubitemid 46527627)
24. Orr J.W., Hagerman P.J., and Williamson J.R. Protein and Mg(2+)-induced conformational changes in the S15 binding site of 16S ribosomal RNA J. Mol. Biol. 275 1998 453 464 10.1006/jmbi.1997.1489 (Pubitemid 28055065)
25. Davies C., Gerstner R.B., Draper D.E., Ramakrishnan V., and White S.W. The crystal structure of ribosomal protein S4 reveals a two-domain molecule with an extensive RNA-binding surface: one domain shows structural homology to the ETS DNA-binding motif EMBO J. 17 1998 4545 4558 10.1093/emboj/17.16.4545 (Pubitemid 28377156)
26. Markus M.A., Gerstner R.B., Draper D.E., and Torchia D.A. Refining the overall structure and subdomain orientation of ribosomal protein S4 delta41 with dipolar couplings measured by NMR in uniaxial liquid crystalline phases J. Mol. Biol. 292 1999 375 387 10.1006/jmbi.1999.3061 (Pubitemid 29435773)
27. Markus M.A., Gerstner R.B., Draper D.E., and Torchia D.A. The solution structure of ribosomal protein S4 delta41 reveals two subdomains and a positively charged surface that may interact with RNA EMBO J. 17 1998 4559 4571 10.1093/emboj/17.16.4559 (Pubitemid 28377157)
28. Yusupov M.M., Yusupova G.Z., Baucom A., Lieberman K., Earnest T.N., Cate J.H., and Noller H.F. Crystal structure of the ribosome at 5.5 Å resolution Science 292 2001 883 896 10.1126/science.1060089 (Pubitemid 32422479)
29. Sayers E.W., Gerstner R.B., Draper D.E., and Torchia D.A. Structural preordering in the N-terminal region of ribosomal protein S4 revealed by heteronuclear NMR spectroscopy Biochemistry 39 2000 13602 13613
30. Tocilj A., Schlunzen F., Janell D., Gluhmann M., Hansen H.A., and Harms J. The small ribosomal subunit from Thermus thermophilus at 4.5 Å resolution: pattern fittings and the identification of a functional site Proc. Natl Acad. Sci. USA 96 1999 14252 14257 (Pubitemid 30000637)
31. Schluenzen F., Tocilj A., Zarivach R., Harms J., Gluehmann M., and Janell D. Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution Cell 102 2000 615 623
32. Ben-Shem A., Jenner L., Yusupova G., and Yusupov M. Crystal structure of the eukaryotic ribosome Science 330 2010 1203 1209 10.1126/science.1194294
33. Chen K., Roberts E., and Luthey-Schulten Z. Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4 BMC Evol. Biol. 9 2009 179 10.1186/1471-2148-9-179
34. Newberry V., Yaguchi M., and Garrett R.A. A trypsin-resistant fragment from complexes of ribosomal protein S4 with 16-S RNA of Escherichia coli and from the uncomplexed protein Eur. J. Biochem. 76 1977 51 61 (Pubitemid 8117396)
35. Chen K., Eargle J., Sarkar K., Gruebele M., and Luthey-Schulten Z. Functional role of ribosomal signatures Biophys. J. 99 2010 3930 3940 10.1016/j.bpj.2010.09.062
36. Brimacombe R. RNA-protein interactions in the Escherichia coli ribosome Biochimie 73 1991 927 936
37. Woese C.R., Fox G.E., Zablen L., Uchida T., Bonen L., and Pechman K. Conservation of primary structure in 16S ribosomal RNA Nature 254 1975 83 86
38. Gutell R.R., Weiser B., Woese C.R., and Noller H.F. Comparative anatomy of 16-S-like ribosomal RNA Prog. Nucleic Acid Res. Mol. Biol. 32 1985 155 216
39. Mulder A.M., Yoshioka C., Beck A.H., Bunner A.E., Milligan R.A., and Potter C.S. Visualizing ribosome biogenesis: parallel assembly pathways for the 30S subunit Science 330 2010 673 677 10.1126/science.1193220
40. Adilakshmi T., Ramaswamy P., and Woodson S.A. Protein-independent folding pathway of the 16S rRNA 5′ domain J. Mol. Biol. 351 2005 508 519 10.1016/j.jmb.2005.06.020 (Pubitemid 41021937)
41. Wilkinson K.A., Merino E.J., and Weeks K.M. Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution Nat. Protoc. 1 2006 1610 1616 10.1038/nprot.2006.249
42. Mortimer S.A., and Weeks K.M. A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry J. Am. Chem. Soc. 129 2007 4144 4145 10.1021/ja0704028 (Pubitemid 46595421)
43. Deigan K.E., Li T.W., Mathews D.H., and Weeks K.M. Accurate SHAPE-directed RNA structure determination Proc. Natl Acad. Sci. USA 106 2009 97 102 10.1073/pnas.0806929106
44. Low J.T., and Weeks K.M. SHAPE-directed RNA secondary structure prediction Methods 52 2010 150 158 10.1016/j.ymeth.2010.06.007
45. Gherghe C.M., Shajani Z., Wilkinson K.A., Varani G., and Weeks K.M. Strong correlation between SHAPE chemistry and the generalized NMR order parameter (S2) in RNA J. Am. Chem. Soc. 130 2008 12244 12245 10.1021/ja804541s
46. Brodersen D.E., Clemons W.M. Jr., Carter A.P., Wimberly B.T., and Ramakrishnan V. Crystal structure of the 30S ribosomal subunit from Thermus thermophilus: structure of the proteins and their interactions with 16S RNA J. Mol. Biol. 316 2002 725 768 10.1006/jmbi.2001.5359 (Pubitemid 34729252)
47. Stern S., Powers T., Changchien L.M., and Noller H.F. RNA-protein interactions in 30S ribosomal subunits: folding and function of 16S rRNA Science 244 1989 783 790 (Pubitemid 19164701)
48. Moazed D., Stern S., and Noller H.F. Rapid chemical probing of conformation in 16S ribosomal RNA and 30S ribosomal subunits using primer extension J. Mol. Biol. 187 1986 399 416 (Pubitemid 16083780)
49. Mizushima S., and Nomura M. Assembly mapping of 30S ribosomal proteins from E. coli Nature 226 1970 1214
50. Charette M., and Gray M.W. Pseudouridine in RNA: what, where, how, and why IUBMB Life 49 2000 341 351 10.1080/152165400410182
51. Helm M. Post-transcriptional nucleotide modification and alternative folding of RNA Nucleic Acids Res. 34 2006 721 733 10.1093/nar/gkj471 (Pubitemid 43240258)
52. Chow C.S., Lamichhane T.N., and Mahto S.K. Expanding the nucleotide repertoire of the ribosome with post-transcriptional modifications ACS Chem. Biol. 2 2007 610 619 10.1021/cb7001494 (Pubitemid 350019778)
53. Thurlow D.L., and Zimmermann R.A. Conservation of ribosomal protein binding sites in prokaryotic 16S RNAs Proc. Natl Acad. Sci. USA 75 1978 2859 2863 (Pubitemid 8375008)
54. Powers T., and Noller H.F. A functional pseudoknot in 16S ribosomal RNA EMBO J. 10 1991 2203 2214 (Pubitemid 21905693)
55. Ogle J.M., Brodersen D.E., Clemons W.M. Jr, Tarry M.J., Carter A.P., and Ramakrishnan V. Recognition of cognate transfer RNA by the 30S ribosomal subunit Science 292 2001 897 902 10.1126/science.1060612 (Pubitemid 32422480)
56. Duncan C.D.S., and Weeks K.M. Nonhierarchical ribonucleoprotein assembly suggests a strain-propagation model for protein-facilitated RNA folding Biochemistry 49 2010 5418 5425 10.1021/bi100267g
57. Das R., Laederach A., Pearlman S.M., Herschlag D., and Altman R.B. SAFA: semi-automated footprinting analysis software for high-throughput quantification of nucleic acid footprinting experiments RNA 11 2005 344 354 10.1261/rna.7214405 (Pubitemid 40270826)