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rRNA Mimicry in RNA Regulation of Gene Expression

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  • Author: Michelle M. Meyer1
  • Editors: Gisela Storz2, Kai Papenfort3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biology, Boston College, Chestnut Hill, MA 02467; 2: Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD; 3: Department of Biology I, Microbiology, LMU Munich, Martinsried, Germany
  • Source: microbiolspec March 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0006-2017
  • Received 02 November 2017 Accepted 02 January 2018 Published 16 March 2018
  • Michelle M. Meyer, [email protected]
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  • Abstract:

    The rRNA is the largest and most abundant RNA in bacterial and archaeal cells. It is also one of the best-characterized RNAs in terms of its structural motifs and sequence variation. Production of ribosome components including >50 ribosomal proteins (r-proteins) consumes significant cellular resources. Thus, RNA -regulatory structures that interact with r-proteins to repress further r-protein synthesis play an important role in maintaining appropriate stoichiometry between r-proteins and rRNA. Classically, such mRNA structures were thought to directly mimic the rRNA. However, more than 30 years of research has demonstrated that a variety of different recognition and regulatory paradigms are present. This review will demonstrate how structural mimicry between the rRNA and mRNA -regulatory structures may take many different forms. The collection of mRNA structures that interact with r-proteins to regulate r-protein operons are best characterized in , but are increasingly found within species from nearly all phyla of bacteria and several archaea. Furthermore, they represent a unique opportunity to assess the plasticity of RNA structure in the context of RNA-protein interactions. The binding determinants imposed by r-proteins to allow regulation can be fulfilled in many ways. Some r-protein-interacting mRNAs are immediately obvious as rRNA mimics from primary sequence similarity, others are identifiable only after secondary or tertiary structure determination, and some show no obvious similarity. In addition, across different bacterial species a host of different mechanisms of action have been characterized, showing that there is no simple one-size-fits-all solution.

  • Citation: Meyer M. 2018. rRNA Mimicry in RNA Regulation of Gene Expression. Microbiol Spectrum 6(2):RWR-0006-2017. doi:10.1128/microbiolspec.RWR-0006-2017.

References

1. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289:905–920. [PubMed][CrossRef]
2. Peer A, Margalit H. 2014. Evolutionary patterns of Escherichia coli small RNAs and their regulatory interactions. RNA 20:994–1003. [PubMed][CrossRef]
3. Hoeppner MP, Gardner PP, Poole AM. 2012. Comparative analysis of RNA families reveals distinct repertoires for each domain of life. PLoS Comput Biol 8:e1002752. doi:10.1371/journal.pcbi.1002752. [PubMed][CrossRef]
4. Lindgreen S, Umu SU, Lai AS, Eldai H, Liu W, McGimpsey S, Wheeler NE, Biggs PJ, Thomson NR, Barquist L, Poole AM, Gardner PP. 2014. Robust identification of noncoding RNA from transcriptomes requires phylogenetically-informed sampling. PLoS Comput Biol 10:e1003907. doi:10.1371/journal.pcbi.1003907. [PubMed][CrossRef]
5. Kacharia FR, Millar JA, Raghavan R. 2017. Emergence of new sRNAs in enteric bacteria is associated with low expression and rapid evolution. J Mol Evol 84:204–213. [PubMed][CrossRef]
6. Leontis NB, Westhof E. 2002. The annotation of RNA motifs. Comp Funct Genomics 3:518–524. [PubMed][CrossRef]
7. Klein DJ, Schmeing TM, Moore PB, Steitz TA. 2001. The kink-turn: a new RNA secondary structure motif. EMBO J 20:4214–4221. [PubMed][CrossRef]
8. Lescoute A, Leontis NB, Massire C, Westhof E. 2005. Recurrent structural RNA motifs, isostericity matrices and sequence alignments. Nucleic Acids Res 33:2395–2409. [PubMed][CrossRef]
9. Fox GE, Woese CR. 1975. 5S RNA secondary structure. Nature 256:505–507. [CrossRef]
10. Leontis NB, Westhof E. 1998. A common motif organizes the structure of multi-helix loops in 16 S and 23 S ribosomal RNAs. J Mol Biol 283:571–583. [PubMed][CrossRef]
11. Correll CC, Freeborn B, Moore PB, Steitz TA. 1997. Metals, motifs, and recognition in the crystal structure of a 5S rRNA domain. Cell 91:705–712. [CrossRef]
12. Woese CR, Winker S, Gutell RR. 1990. Architecture of ribosomal RNA: constraints on the sequence of “tetra-loops”. Proc Natl Acad Sci U S A 87:8467–8471. [PubMed][CrossRef]
13. Gutell RR, Larsen N, Woese CR. 1994. Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiol Rev 58:10–26. [PubMed]
14. Wu JC, Gardner DP, Ozer S, Gutell RR, Ren P. 2009. Correlation of RNA secondary structure statistics with thermodynamic stability and applications to folding. J Mol Biol 391:769–783. [PubMed][CrossRef]
15. Serganov A, Huang L, Patel DJ. 2008. Structural insights into amino acid binding and gene control by a lysine riboswitch. Nature 455:1263–1267. [PubMed][CrossRef]
16. Wang J, Nikonowicz EP. 2011. Solution structure of the K-turn and specifier loop domains from the Bacillus subtilis tyrS T-box leader RNA. J Mol Biol 408:99–117. [PubMed][CrossRef]
17. Strobel SA, Adams PL, Stahley MR, Wang J. 2004. RNA kink turns to the left and to the right. RNA 10:1852–1854. [PubMed][CrossRef]
18. Keating KS, Toor N, Perlman PS, Pyle AM. 2010. A structural analysis of the group II intron active site and implications for the spliceosome. RNA 16:1–9. [PubMed][CrossRef]
19. Garst AD, Edwards AL, Batey RT. 2011. Riboswitches: structures and mechanisms. Cold Spring Harb Perspect Biol 3:a003533. doi:10.1101/cshperspect.a003533. [PubMed][CrossRef]
20. Huang L, Lilley DM. 2016. The kink turn, a key architectural element in RNA structure. J Mol Biol 428(5 Pt A):790–801. [PubMed][CrossRef]
21. Chan CW, Chetnani B, Mondragón A. 2013. Structure and function of the T-loop structural motif in noncoding RNAs. Wiley Interdiscip Rev RNA 4:507–522. [PubMed][CrossRef]
22. Aseev LV, Boni IV. 2011. Extraribosomal functions of bacterial ribosomal proteins. Mol Biol 45:739. [CrossRef]
23. Warner JR, McIntosh KB. 2009. How common are extraribosomal functions of ribosomal proteins? Mol Cell 34:3–11. [PubMed][CrossRef]
24. Schmidt A, Kochanowski K, Vedelaar S, Ahrné E, Volkmer B, Callipo L, Knoops K, Bauer M, Aebersold R, Heinemann M. 2016. The quantitative and condition-dependent Escherichia coli proteome. Nat Biotechnol 34:104–110. [PubMed][CrossRef]
25. Li GW, Burkhardt D, Gross C, Weissman JS. 2014. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157:624–635. [PubMed][CrossRef]
26. Fallon AM, Jinks CS, Yamamoto M, Nomura M. 1979. Expression of ribosomal protein genes cloned in a hybrid plasmid in Escherichia coli: gene dosage effects on synthesis of ribosomal proteins and ribosomal protein messenger ribonucleic acid. J Bacteriol 138:383–396. [PubMed]
27. Fallon AM, Jinks CS, Strycharz GD, Nomura M. 1979. Regulation of ribosomal protein synthesis in Escherichia coli by selective mRNA inactivation. Proc Natl Acad Sci U S A 76:3411–3415. [PubMed][CrossRef]
28. Lindahl L, Zengel JM. 1979. Operon-specific regulation of ribosomal protein synthesis in Escherichia coli. Proc Natl Acad Sci U S A 76:6542–6546. [PubMed][CrossRef]
29. Dean D, Yates JL, Nomura M. 1981. Escherichia coli ribosomal protein S8 feedback regulates part of spc operon. Nature 289:89–91. [PubMed][CrossRef]
30. Yates JL, Arfsten AE, Nomura M. 1980. In vitro expression of Escherichia coli ribosomal protein genes: autogenous inhibition of translation. Proc Natl Acad Sci U S A 77:1837–1841. [PubMed][CrossRef]
31. Dean D, Nomura M. 1980. Feedback regulation of ribosomal protein gene expression in Escherichia coli. Proc Natl Acad Sci U S A 77:3590–3594. [PubMed][CrossRef]
32. Brot N, Caldwell P, Weissbach H. 1980. Autogenous control of Escherichia coli ribosomal protein L10 synthesis in vitro. Proc Natl Acad Sci U S A 77:2592–2595. [PubMed][CrossRef]
33. Holowachuk EW, Friesen JD, Fiil NP. 1980. Bacteriophage λ vehicle for the direct cloning of Escherichia coli promoter DNA sequences: feedback regulation of the rplJL-rpoBC operon. Proc Natl Acad Sci U S A 77:2124–2128. [PubMed][CrossRef]
34. Robakis N, Meza-Basso L, Brot N, Weissbach H. 1981. Translational control of ribosomal protein L10 synthesis occurs prior to formation of first peptide bond. Proc Natl Acad Sci U S A 78:4261–4264. [PubMed][CrossRef]
35. Olins PO, Nomura M. 1981. Translational regulation by ribosomal protein S8 in Escherichia coli: structural homology between rRNA binding site and feedback target on mRNA. Nucleic Acids Res 9:1757–1764. [CrossRef]
36. Dean D, Yates JL, Nomura M. 1981. Identification of ribosomal protein S7 as a repressor of translation within the str operon of E. coli. Cell 24:413–419. [PubMed][CrossRef]
37. Jinks-Robertson S, Nomura M. 1982. Ribosomal protein S4 acts in trans as a translational repressor to regulate expression of the α operon in Escherichia coli. J Bacteriol 151:193–202. [PubMed]
38. Singer P, Nomura M. 1985. Stability of ribosomal protein mRNA and translational feedback regulation in Escherichia coli. Mol Gen Genet 199:543–546. [PubMed][CrossRef]
39. Cole JR, Nomura M. 1986. Changes in the half-life of ribosomal protein messenger RNA caused by translational repression. J Mol Biol 188:383–392. [CrossRef]
40. Mattheakis LC, Nomura M. 1988. Feedback regulation of the spc operon in Escherichia coli: translational coupling and mRNA processing. J Bacteriol 170:4484–4492. [CrossRef]
41. Friedman DI, Schauer AT, Baumann MR, Baron LS, Adhya SL. 1981. Evidence that ribosomal protein S10 participates in control of transcription termination. Proc Natl Acad Sci U S A 78:1115–1118. [PubMed][CrossRef]
42. Zengel JM, Lindahl L. 1990. Escherichia coli ribosomal protein L4 stimulates transcription termination at a specific site in the leader of the S10 operon independent of L4-mediated inhibition of translation. J Mol Biol 213:67–78. [CrossRef]
43. Nomura M, Yates JL, Dean D, Post LE. 1980. Feedback regulation of ribosomal protein gene expression in Escherichia coli: structural homology of ribosomal RNA and ribosomal protein mRNA. Proc Natl Acad Sci U S A 77:7084–7088. [PubMed][CrossRef]
44. Olins PO, Nomura M. 1981. Regulation of the S10 ribosomal protein operon in E. coli: nucleotide sequence at the start of the operon. Cell 26:205–211. [CrossRef]
45. Baughman G, Nomura M. 1983. Localization of the target site for translational regulation of the L11 operon and direct evidence for translational coupling in Escherichia coli. Cell 34:979–988. [CrossRef]
46. Lindahl L, Zengel JM. 1986. Ribosomal genes in Escherichia coli. Annu Rev Genet 20:297–326. [PubMed][CrossRef]
47. Johnsen M, Christensen T, Dennis PP, Fiil NP. 1982. Autogenous control: ribosomal protein L10-L12 complex binds to the leader sequence of its mRNA. EMBO J 1:999–1004. [PubMed]
48. Christensen T, Johnsen M, Fiil NP, Friesen JD. 1984. RNA secondary structure and translation inhibition: analysis of mutants in the rplJ leader. EMBO J 3:1609–1612. [PubMed]
49. Deckman IC, Draper DE. 1985. Specific interaction between ribosomal protein S4 and the alpha operon messenger RNA. Biochemistry 24:7860–7865. [CrossRef]
50. Tang CK, Draper DE. 1989. Unusual mRNA pseudoknot structure is recognized by a protein translational repressor. Cell 57:531–536. [CrossRef]
51. Shen P, Zengel JM, Lindahl L. 1988. Secondary structure of the leader transcript from the Escherichia coli S10 ribosomal protein operon. Nucleic Acids Res 16:8905–8924. [PubMed][CrossRef]
52. Merianos HJ, Wang J, Moore PB. 2004. The structure of a ribosomal protein S8/spc operon mRNA complex. RNA 10:954–964. [PubMed][CrossRef]
53. Nevskaya N, Tishchenko S, Gabdoulkhakov A, Nikonova E, Nikonov O, Nikulin A, Platonova O, Garber M, Nikonov S, Piendl W. 2005. Ribosomal protein L1 recognizes the same specific structural motif in its target sites on the autoregulatory mRNA and 23S rRNA. Nucleic Acids Res 33:478–485. [PubMed][CrossRef]
54. Lesage P, Truong HN, Graffe M, Dondon J, Springer M. 1990. Translated translational operator in Escherichia coli. Auto-regulation in the infC-rpmI-rplT operon. J Mol Biol 213:465–475. [CrossRef]
55. Portier C, Dondon L, Grunberg-Manago M. 1990. Translational autocontrol of the Escherichia coli ribosomal protein S15. J Mol Biol 211:407–414. [CrossRef]
56. Parsons GD, Donly BC, Mackie GA. 1988. Mutations in the leader sequence and initiation codon of the gene for ribosomal protein S20 (rpsT) affect both translational efficiency and autoregulation. J Bacteriol 170:2485–2492. [PubMed][CrossRef]
57. Aseev LV, Levandovskaya AA, Tchufistova LS, Scaptsova NV, Boni IV. 2008. A new regulatory circuit in ribosomal protein operons: S2-mediated control of the rpsB-tsf expression in vivo. RNA 14:1882–1894. [PubMed][CrossRef]
58. Aseev LV, Bylinkina NS, Boni IV. 2015. Regulation of the rplY gene encoding 5S rRNA binding protein L25 in Escherichia coli and related bacteria. RNA 21:851–861. [PubMed][CrossRef]
59. Skouv J, Schnier J, Rasmussen MD, Subramanian AR, Pedersen S. 1990. Ribosomal protein S1 of Escherichia coli is the effector for the regulation of its own synthesis. J Biol Chem 265:17044–17049. [PubMed]
60. Aseev LV, Koledinskaya LS, Boni IV. 2016. Regulation of ribosomal protein operons rplM-rpsI, rpmB-rpmG, and rplU-rpmA at the transcriptional and translational levels. J Bacteriol 198:2494–2502. [PubMed][CrossRef]
61. Matelska D, Purta E, Panek S, Boniecki MJ, Bujnicki JM, Dunin-Horkawicz S. 2013. S6:S18 ribosomal protein complex interacts with a structural motif present in its own mRNA. RNA 19:1341–1348. [PubMed][CrossRef]
62. Fu Y, Deiorio-Haggar K, Soo MW, Meyer MM. 2014. Bacterial RNA motif in the 5′ UTR of rpsF interacts with an S6:S18 complex. RNA 20:168–176. [PubMed][CrossRef]
63. Babina AM, Soo MW, Fu Y, Meyer MM. 2015. An S6:S18 complex inhibits translation of E. coli rpsF. RNA 21:2039–2046. [PubMed][CrossRef]
64. Fujita K, Baba T, Isono K. 1998. Genomic analysis of the genes encoding ribosomal proteins in eight eubacterial species and Saccharomyces cerevisiae. Genome Inform Ser Workshop Genome Inform 9:3–12. [PubMed]
65. Coenye T, Vandamme P. 2005. Organisation of the S10, spc and alpha ribosomal protein gene clusters in prokaryotic genomes. FEMS Microbiol Lett 242:117–126. [PubMed][CrossRef]
66. Allen T, Shen P, Samsel L, Liu R, Lindahl L, Zengel JM. 1999. Phylogenetic analysis of L4-mediated autogenous control of the S10 ribosomal protein operon. J Bacteriol 181:6124–6132. [PubMed]
67. Allen TD, Watkins T, Lindahl L, Zengel JM. 2004. Regulation of ribosomal protein synthesis in Vibrio cholerae. J Bacteriol 186:5933–5937. [PubMed][CrossRef]
68. Iben JR, Draper DE. 2008. Specific interactions of the L10(L12)4 ribosomal protein complex with mRNA, rRNA, and L11. Biochemistry 47:2721–2731. [PubMed][CrossRef]
69. Aseev LV, Levandovskaya AA, Skaptsova NV, Boni IV. 2009. Conservation of regulatory elements controlling the expression of the rpsB-tsf operon in γ-proteobacteria. Mol Biol 43:101–107. [CrossRef]
70. Guillier M, Allemand F, Raibaud S, Dardel F, Springer M, Chiaruttini C. 2002. Translational feedback regulation of the gene for L35 in Escherichia coli requires binding of ribosomal protein L20 to two sites in its leader mRNA: a possible case of ribosomal RNA-messenger RNA molecular mimicry. RNA 8:878–889. [PubMed][CrossRef]
71. Fu Y, Deiorio-Haggar K, Anthony J, Meyer MM. 2013. Most RNAs regulating ribosomal protein biosynthesis in Escherichia coli are narrowly distributed to Gammaproteobacteria. Nucleic Acids Res 41:3491–3503. [PubMed][CrossRef]
72. Matelska D, Kurkowska M, Purta E, Bujnicki JM, Dunin-Horkawicz S. 2016. Loss of conserved noncoding RNAs in genomes of bacterial endosymbionts. Genome Biol Evol 8:426–438. [PubMed][CrossRef]
73. Grundy FJ, Henkin TM. 1991. The rpsD gene, encoding ribosomal protein S4, is autogenously regulated in Bacillus subtilis. J Bacteriol 173:4595–4602. [CrossRef]
74. Choonee N, Even S, Zig L, Putzer H. 2007. Ribosomal protein L20 controls expression of the Bacillus subtilis infC operon via a transcription attenuation mechanism. Nucleic Acids Res 35:1578–1588. [PubMed][CrossRef]
75. Deiorio-Haggar K, Anthony J, Meyer MM. 2013. RNA structures regulating ribosomal protein biosynthesis in bacilli. RNA Biol 10:1180–1184. [PubMed][CrossRef]
76. Nawrocki EP, Kolbe DL, Eddy SR. 2009. Infernal 1.0: inference of RNA alignments. Bioinformatics 25:1335–1337. [PubMed][CrossRef]
77. Griffiths-Jones S, Bateman A, Marshall M, Khanna A, Eddy SR. 2003. Rfam: an RNA family database. Nucleic Acids Res 31:439–441. [PubMed][CrossRef]
78. Weinberg Z, Wang JX, Bogue J, Yang J, Corbino K, Moy RH, Breaker RR. 2010. Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol 11:R31. doi:10.1186/gb-2010-11-3-r31. [CrossRef]
79. Weinberg Z, Barrick JE, Yao Z, Roth A, Kim JN, Gore J, Wang JX, Lee ER, Block KF, Sudarsan N, Neph S, Tompa M, Ruzzo WL, Breaker RR. 2007. Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res 35:4809–4819. [PubMed][CrossRef]
80. Yao Z, Barrick J, Weinberg Z, Neph S, Breaker R, Tompa M, Ruzzo WL. 2007. A computational pipeline for high-throughput discovery of cis-regulatory noncoding RNA in prokaryotes. PLoS Comput Biol 3:e126. doi:10.1371/journal.pcbi.0030126. [PubMed][CrossRef]
81. Tseng HH, Weinberg Z, Gore J, Breaker RR, Ruzzo WL. 2009. Finding non-coding RNAs through genome-scale clustering. J Bioinform Comput Biol 7:373–388. [PubMed][CrossRef]
82. Weinberg Z, Lünse CE, Corbino KA, Ames TD, Nelson JW, Roth A, Perkins KR, Sherlock ME, Breaker RR. 2017. Detection of 224 candidate structured RNAs by comparative analysis of specific subsets of intergenic regions. Nucleic Acids Res 45:10811–10823. [PubMed][CrossRef]
83. Dar D, Shamir M, Mellin JR, Koutero M, Stern-Ginossar N, Cossart P, Sorek R. 2016. Term-seq reveals abundant ribo-regulation of antibiotics resistance in bacteria. Science 352:aad9822. [PubMed][CrossRef]
84. Daume M, Uhl M, Backofen R, Randau L. 2017. RIP-Seq suggests translational regulation by L7Ae in Archaea. mBio 8:e00730–17. doi:10.1128/mBio.00730-17. [CrossRef]
85. Mattheakis L, Vu L, Sor F, Nomura M. 1989. Retroregulation of the synthesis of ribosomal proteins L14 and L24 by feedback repressor S8 in Escherichia coli. Proc Natl Acad Sci U S A 86:448–452. [PubMed][CrossRef]
86. Gregory RJ, Cahill PB, Thurlow DL, Zimmermann RA. 1988. Interaction of Escherichia coli ribosomal protein S8 with its binding sites in ribosomal RNA and messenger RNA. J Mol Biol 204:295–307. [CrossRef]
87. Cerretti DP, Mattheakis LC, Kearney KR, Vu L, Nomura M. 1988. Translational regulation of the spc operon in Escherichia coli. Identification and structural analysis of the target site for S8 repressor protein. J Mol Biol 204:309–329. [CrossRef]
88. Wu H, Jiang L, Zimmermann RA. 1994. The binding site for ribosomal protein S8 in 16S rRNA and spc mRNA from Escherichia coli: minimum structural requirements and the effects of single bulged bases on S8-RNA interaction. Nucleic Acids Res 22:1687–1695. [PubMed][CrossRef]
89. Davies C, Ramakrishnan V, White SW. 1996. Structural evidence for specific S8-RNA and S8-protein interactions within the 30S ribosomal subunit: ribosomal protein S8 from Bacillus stearothermophilus at 1.9 Å resolution. Structure 4:1093–1104. [CrossRef]
90. Vysotskaya V, Tischenko S, Garber M, Kern D, Mougel M, Ehresmann C, Ehresmann B. 1994. The ribosomal protein S8 from Thermus thermophilus VK1. Sequencing of the gene, overexpression of the protein in Escherichia coli and interaction with rRNA. Eur J Biochem 223:437–445. [PubMed][CrossRef]
91. Kalurachchi K, Uma K, Zimmermann RA, Nikonowicz EP. 1997. Structural features of the binding site for ribosomal protein S8 in Escherichia coli 16S rRNA defined using NMR spectroscopy. Proc Natl Acad Sci U S A 94:2139–2144. [PubMed][CrossRef]
92. Nevskaya N, Tishchenko S, Nikulin A, al-Karadaghi S, Liljas A, Ehresmann B, Ehresmann C, Garber M, Nikonov S. 1998. Crystal structure of ribosomal protein S8 from Thermus thermophilus reveals a high degree of structural conservation of a specific RNA binding site. J Mol Biol 279:233–244. [PubMed][CrossRef]
93. Tishchenko S, Nikulin A, Fomenkova N, Nevskaya N, Nikonov O, Dumas P, Moine H, Ehresmann B, Ehresmann C, Piendl W, Lamzin V, Garber M, Nikonov S. 2001. Detailed analysis of RNA-protein interactions within the ribosomal protein S8-rRNA complex from the archaeon Methanococcus jannaschii. J Mol Biol 311:311–324. [PubMed][CrossRef]
94. Friesen JD, Tropak M, An G. 1983. Mutations in the rpIJ leader of Escherichia coli that abolish feedback regulation. Cell 32:361–369. [CrossRef]
95. Climie SC, Friesen JD. 1987. Feedback regulation of the rplJL-rpoBC ribosomal protein operon of Escherichia coli requires a region of mRNA secondary structure. J Mol Biol 198:371–381. [CrossRef]
96. Climie SC, Friesen JD. 1988. In vivo and in vitro structural analysis of the rplJ mRNA leader of Escherichia coli. Protection by bound L10-L7/L12. J Biol Chem 263:15166–15175. [PubMed]
97. Yates JL, Dean D, Strycharz WA, Nomura M. 1981. E. coli ribosomal protein L10 inhibits translation of L10 and L7/L12 mRNAs by acting at a single site. Nature 294:190–192. [PubMed][CrossRef]
98. Yakhnin H, Yakhnin AV, Babitzke P. 2015. Ribosomal protein L10(L12)4 autoregulates expression of the Bacillus subtilis rplJL operon by a transcription attenuation mechanism. Nucleic Acids Res 43:7032–7043. [PubMed][CrossRef]
99. Barrick JE, Breaker RR. 2007. The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biol 8:R239. doi:10.1186/gb-2007-8-11-r239. [CrossRef]
100. Baughman G, Nomura M. 1984. Translational regulation of the L11 ribosomal protein operon of Escherichia coli: analysis of the mRNA target site using oligonucleotide-directed mutagenesis. Proc Natl Acad Sci U S A 81:5389–5393. [PubMed][CrossRef]
101. Hanner M, Mayer C, Köhrer C, Golderer G, Gröbner P, Piendl W. 1994. Autogenous translational regulation of the ribosomal MvaL1 operon in the archaebacterium Methanococcus vannielii. J Bacteriol 176:409–418. [PubMed][CrossRef]
102. Kraft A, Lutz C, Lingenhel A, Gröbner P, Piendl W. 1999. Control of ribosomal protein L1 synthesis in mesophilic and thermophilic Archaea. Genetics 152:1363–1372. [PubMed]
103. Köhrer C, Mayer C, Neumair O, Gröbner P, Piendl W. 1998. Interaction of ribosomal L1 proteins from mesophilic and thermophilic Archaea and Bacteria with specific L1-binding sites on 23S rRNA and mRNA. Eur J Biochem 256:97–105. [PubMed][CrossRef]
104. Shimmin LC, Ramirez C, Matheson AT, Dennis PP. 1989. Sequence alignment and evolutionary comparison of the L10 equivalent and L12 equivalent ribosomal proteins from archaebacteria, eubacteria, and eucaryotes. J Mol Evol 29:448–462. [PubMed][CrossRef]
105. Haentjens-Sitri J, Allemand F, Springer M, Chiaruttini C. 2008. A competition mechanism regulates the translation of the Escherichia coli operon encoding ribosomal proteins L35 and L20. J Mol Biol 375:612–625. [PubMed][CrossRef]
106. Nawrocki EP, Eddy SR. 2013. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29:2933–2935. [PubMed][CrossRef]
107. Bruscella P, Shahbabian K, Laalami S, Putzer H. 2011. RNase Y is responsible for uncoupling the expression of translation factor IF3 from that of the ribosomal proteins L35 and L20 in Bacillus subtilis. Mol Microbiol 81:1526–1541. [PubMed][CrossRef]
108. Guillier M, Allemand F, Dardel F, Royer CA, Springer M, Chiaruttini C. 2005. Double molecular mimicry in Escherichia coli: binding of ribosomal protein L20 to its two sites in mRNA is similar to its binding to 23S rRNA. Mol Microbiol 56:1441–1456. [PubMed][CrossRef]
109. Scott LG, Williamson JR. 2001. Interaction of the Bacillus stearothermophilus ribosomal protein S15 with its 5′-translational operator mRNA. J Mol Biol 314:413–422. [PubMed][CrossRef]
110. Philippe C, Eyermann F, Bénard L, Portier C, Ehresmann B, Ehresmann C. 1993. Ribosomal protein S15 from Escherichia coli modulates its own translation by trapping the ribosome on the mRNA initiation loading site. Proc Natl Acad Sci U S A 90:4394–4398. [PubMed][CrossRef]
111. Serganov A, Polonskaia A, Ehresmann B, Ehresmann C, Patel DJ. 2003. Ribosomal protein S15 represses its own translation via adaptation of an rRNA-like fold within its mRNA. EMBO J 22:1898–1908. [PubMed][CrossRef]
112. Slinger BL, Deiorio-Haggar K, Anthony JS, Gilligan MM, Meyer MM. 2014. Discovery and validation of novel and distinct RNA regulators for ribosomal protein S15 in diverse bacterial phyla. BMC Genomics 15:657. doi:10.1186/1471-2164-15-657. [CrossRef]
113. Slinger BL, Newman H, Lee Y, Pei S, Meyer MM. 2015. Co-evolution of bacterial ribosomal protein S15 with diverse mRNA regulatory structures. PLoS Genet 11:e1005720. doi:10.1371/journal.pgen.1005720. [CrossRef]
114. Mathy N, Pellegrini O, Serganov A, Patel DJ, Ehresmann C, Portier C. 2004. Specific recognition of rpsO mRNA and 16S rRNA by Escherichia coli ribosomal protein S15 relies on both mimicry and site differentiation. Mol Microbiol 52:661–675. [PubMed][CrossRef]
115. Scott LG, Williamson JR. 2005. The binding interface between Bacillus stearothermophilus ribosomal protein S15 and its 5′-translational operator mRNA. J Mol Biol 351:280–290. [PubMed][CrossRef]
116. Serganov A, Ennifar E, Portier C, Ehresmann B, Ehresmann C. 2002. Do mRNA and rRNA binding sites of E. coli ribosomal protein S15 share common structural determinants? J Mol Biol 320:963–978. [CrossRef]
117. Ehresmann C, Ehresmann B, Ennifar E, Dumas P, Garber M, Mathy N, Nikulin A, Portier C, Patel D, Serganov A. 2004. Molecular mimicry in translational regulation: the case of ribosomal protein S15. RNA Biol 1:66–73. [PubMed][CrossRef]
118. Cho IM, Lai LB, Susanti D, Mukhopadhyay B, Gopalan V. 2010. Ribosomal protein L7Ae is a subunit of archaeal RNase P. Proc Natl Acad Sci U S A 107:14573–14578. [PubMed][CrossRef]
119. Kuhn JF, Tran EJ, Maxwell ES. 2002. Archaeal ribosomal protein L7 is a functional homolog of the eukaryotic 15.5kD/Snu13p snoRNP core protein. Nucleic Acids Res 30:931–941. [PubMed][CrossRef]
120. Rozhdestvensky TS, Tang TH, Tchirkova IV, Brosius J, Bachellerie JP, Hüttenhofer A. 2003. Binding of L7Ae protein to the K-turn of archaeal snoRNAs: a shared RNA binding motif for C/D and H/ACA box snoRNAs in Archaea. Nucleic Acids Res 31:869–877. [PubMed][CrossRef]
121. Nottrott S, Hartmuth K, Fabrizio P, Urlaub H, Vidovic I, Ficner R, Lührmann R. 1999. Functional interaction of a novel 15.5kD [U4/U6.U5] tri-snRNP protein with the 5′ stem-loop of U4 snRNA. EMBO J 18:6119–6133. [PubMed][CrossRef]
122. Baird NJ, Zhang J, Hamma T, Ferré-D’Amaré AR. 2012. YbxF and YlxQ are bacterial homologs of L7Ae and bind K-turns but not K-loops. RNA 18:759–770. [PubMed][CrossRef]
123. Saito H, Kobayashi T, Hara T, Fujita Y, Hayashi K, Furushima R, Inoue T. 2010. Synthetic translational regulation by an L7Ae-kink-turn RNP switch. Nat Chem Biol 6:71–78. [PubMed][CrossRef]
124. Saito H, Fujita Y, Kashida S, Hayashi K, Inoue T. 2011. Synthetic human cell fate regulation by protein-driven RNA switches. Nat Commun 2:160–168. [PubMed][CrossRef]
125. Berens C, Suess B. 2015. Riboswitch engineering—making the all-important second and third steps. Curr Opin Biotechnol 31:10–15. [PubMed][CrossRef]
126. Slinger BL, Meyer MM. 2016. RNA regulators responding to ribosomal protein S15 are frequent in sequence space. Nucleic Acids Res 44:9331–9341. [PubMed][CrossRef]
127. Pei S, Slinger BL, Meyer MM. 2017. Recognizing RNA structural motifs in HT-SELEX data for ribosomal protein S15. BMC Bioinformatics 18:298. doi:10.1186/s12859-017-1704-y. [CrossRef]
128. Moine H, Cachia C, Westhof E, Ehresmann B, Ehresmann C. 1997. The RNA binding site of S8 ribosomal protein of Escherichia coli: Selex and hydroxyl radical probing studies. RNA 3:255–268. [PubMed]
129. Cannone JJ, Subramanian S, Schnare MN, Collett JR, D’Souza LM, Du Y, Feng B, Lin N, Madabusi LV, Müller KM, Pande N, Shang Z, Yu N, Gutell RR. 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. doi:10.1186/1471-2105-3-2. [PubMed][CrossRef]
130. Dunkle JA, Wang L, Feldman MB, Pulk A, Chen VB, Kapral GJ, Noeske J, Richardson JS, Blanchard SC, Cate JH. 2011. Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science 332:981–984. [PubMed][CrossRef]
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/content/journal/microbiolspec/10.1128/microbiolspec.RWR-0006-2017
2018-03-16
2018-09-22

Abstract:

The rRNA is the largest and most abundant RNA in bacterial and archaeal cells. It is also one of the best-characterized RNAs in terms of its structural motifs and sequence variation. Production of ribosome components including >50 ribosomal proteins (r-proteins) consumes significant cellular resources. Thus, RNA -regulatory structures that interact with r-proteins to repress further r-protein synthesis play an important role in maintaining appropriate stoichiometry between r-proteins and rRNA. Classically, such mRNA structures were thought to directly mimic the rRNA. However, more than 30 years of research has demonstrated that a variety of different recognition and regulatory paradigms are present. This review will demonstrate how structural mimicry between the rRNA and mRNA -regulatory structures may take many different forms. The collection of mRNA structures that interact with r-proteins to regulate r-protein operons are best characterized in , but are increasingly found within species from nearly all phyla of bacteria and several archaea. Furthermore, they represent a unique opportunity to assess the plasticity of RNA structure in the context of RNA-protein interactions. The binding determinants imposed by r-proteins to allow regulation can be fulfilled in many ways. Some r-protein-interacting mRNAs are immediately obvious as rRNA mimics from primary sequence similarity, others are identifiable only after secondary or tertiary structure determination, and some show no obvious similarity. In addition, across different bacterial species a host of different mechanisms of action have been characterized, showing that there is no simple one-size-fits-all solution.

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Figures

Image of FIGURE 1
FIGURE 1

Diagrams of r-protein operons from (A) and (B). Genes are shown in the order in which they appear in the genome and to scale. Gray genes are subject to r-protein autogenous regulation; white genes have no described autogenous regulation. Colored arrows represent r-protein RNA binding structures. Red arrows indicate structures that are widely distributed to many bacterial phyla, blue arrows indicate RNA structures that are confined to , green arrows indicate RNA structures confined to , and purple arrows indicate presumed r-protein binding sites where no explicit RNA secondary structure has been described. For each operon the effector protein is colored to match the RNA site with which it interacts.

Source: microbiolspec March 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0006-2017
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Image of FIGURE 2
FIGURE 2

S8 mRNA binding site in mRNA (A) and rRNA (B) consensus structure. Green nucleotides indicate Shine-Dalgarno sequence and translational start; red nucleotides directly contact S8 in the three-dimensional structure ( 52 ). rRNA nucleotides conserved <90% are shown as filled circles; nucleotides conserved ≥90% are indicated by letters. Numbering corresponds to bacterial consensus sequence ( 129 ). (C) Aligning structural data for each site based on the S8 protein backbone shows that the two binding sites are superimposable. The structure of the S8 with its mRNA binding site is shown in green (1s03.cif [ 52 ]), and the structure of S8 interacting with the rRNA is shown in blue (4v9d.cif [ 130 ]). Bases of the mRNA directly contacting S8 are colored red; a bulged base in the mRNA that differentiates the rRNA and mRNA binding sites is colored orange.

Source: microbiolspec March 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0006-2017
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Image of FIGURE 3
FIGURE 3

L10(L12) mRNA binding sites from (A) , (B) and the rRNA consensus structure (C). Red nucleotides are implicated in binding; rRNA nucleotides conserved <90% are shown as filled circles; nucleotides conserved ≥90% are indicated by letters. Numbering corresponds to bacterial consensus sequence ( 129 ).

Source: microbiolspec March 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0006-2017
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Image of FIGURE 4
FIGURE 4

(A) L1-interacting mRNA structures from and , and the L1 rRNA binding site (bacterial consensus). Red nucleotides directly contact L1 in the three-dimensional structure ( 53 ). rRNA nucleotides conserved <90% are shown as filled circles; nucleotides conserved ≥90% are indicated by letters. Numbering corresponds to bacterial consensus sequence ( 129 ). (B) Diagrams indicating the genomic position of L1 mRNA binding sites in two clades (several species and ) and in bacteria. Proteins encoded by rplJ and rplP0 are homologous. Bacterial genomic positions of L1 binding site are mapped to a 16S rRNA tree.

Source: microbiolspec March 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0006-2017
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Image of FIGURE 5
FIGURE 5

Diagram of operons showing genomic positions of L20-interacting mRNA structures (red arrows) in (A) and (B). Genes regulated by the RNA structure are colored. (C) L20-interacting mRNA structures from (mRNA-I and mRNA-II) and and the consensus rRNA L20 binding site. Red nucleotides are important for L20 interaction. rRNA nucleotides conserved <90% are shown as filled circles; nucleotides conserved ≥90% are indicated by letters. Numbering corresponds to bacterial consensus sequence ( 129 ).

Source: microbiolspec March 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0006-2017
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Image of FIGURE 6
FIGURE 6

S15-interacting mRNA structures in different bacterial phyla and the consensus S15 rRNA binding site. Red nucleotides correspond to the rRNA three-stem junction and its direct mimics. Blue nucleotides correspond to G•U/G-C helix imperfection in the rRNA binding site and its mimics in mRNA structures. Purple nucleotides are important for S15 recognition but do not directly correspond to any rRNA motif. Green nucleotides correspond to Shine-Dalgarno or translational start sequences. rRNA nucleotides conserved <90% are shown as filled circles; nucleotides conserved ≥90% are indicated by letters. Numbering corresponds to bacterial consensus sequence ( 129 ).

Source: microbiolspec March 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0006-2017
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Tables

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TABLE 1

Summary of r-protein-interacting mRNAs that allow regulation of r-protein genes

Source: microbiolspec March 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0006-2017

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