Skip to main content
Log in

Characteristic Features of Protein Interaction with Single- and Double-Stranded RNA

  • REVIEW
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

The review discusses differences between the specific protein interactions with single- and double-stranded RNA molecules using the data on the structure of RNA–protein complexes. Proteins interacting with the single-stranded RNAs form contacts with RNA bases, which ensures recognition of specific nucleotide sequences. Formation of such contacts with the double-stranded RNAs is hindered, so that the proteins recognize unique conformations of the RNA spatial structure and interact mainly with the RNA sugar-phosphate backbone.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.
Fig. 9.

Similar content being viewed by others

Abbreviations

dsRBD:

double-stranded RNA-binding domain

dsRNA:

double-stranded RNA

RNP:

ribonucleoprotein

ssRNA:

single-stranded RNA

References

  1. Fedorov, R., Meshcheryakov, V., Gongadze, G., Fomenkova, N., Nevskaya, N., et al. (2001) Structure of ribosomal protein TL5 complexed with RNA provides new insights into the CTC family of stress proteins, Acta Crystallogr. Sect. D Biol. Crystallogr., 57, 968-976, https://doi.org/10.1107/S0907444901006291.

    Article  CAS  Google Scholar 

  2. Perederina, A., Nevskaya, N., Nikonov, O., Nikulin, A., Dumas, P., et al. (2002) Detailed analysis of RNA–protein interactions within the bacterial ribosomal protein L5/5S rRNA complex, RNA, 8, 1548-1557, https://doi.org/10.1017/s1355838202029953.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Nikulin, A., Eliseikina, I., Tishchenko, S., Nevskaya, N., Davydova, N., et al. (2003) Structure of the L1 protuberance in the ribosome, Nat. Struct. Biol., 10, 104-108, https://doi.org/10.1038/nsb886.

    Article  CAS  PubMed  Google Scholar 

  4. Tishchenko, S., Nikulin, A., Fomenkova, N., Nevskaya, N., Nikonov, O., et al. (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, https://doi.org/10.1006/jmbi.2001.4877.

    Article  CAS  PubMed  Google Scholar 

  5. Nikulin, A., Serganov, A., Ennifar, E., Tishchenko, S., Nevskaya, N., et al. (2000) Crystal structure of the S15–rRNA complex, Nat. Struct. Biol., 7, 273-277, https://doi.org/10.1038/74028.

    Article  CAS  PubMed  Google Scholar 

  6. Gabdulkhakov, A., Mitroshin, I., and Garber, M. (2020) Structure of the ribosomal P stalk base in archaean Methanococcus jannaschii, J. Struct. Biol., 211, 107559, https://doi.org/10.1016/j.jsb.2020.107559.

    Article  CAS  PubMed  Google Scholar 

  7. Kostareva, O. S., Nevskaya, N. A., Tishchenko, S. V., Gabdulkhakov, A. G., Garber, M. B., and Nikonov, S. V. (2018) Influence of nonconserved regions of L1 protuberance of Thermus thermophilus ribosome on the affinity of L1 protein to 23s rRNA, Mol. Biol., 52, 91-95, https://doi.org/10.1134/S0026893318010090.

    Article  CAS  Google Scholar 

  8. Draper, D. E. (1999) Themes in RNA–protein recognition, J. Mol. Biol., 293, 255-270, https://doi.org/10.1006/jmbi.1999.2991.

    Article  CAS  PubMed  Google Scholar 

  9. Corley, M., Burns, M. C., and Yeo, G. W. (2020) How RNA-binding proteins interact with RNA: molecules and mechanisms, Mol. Cell, 78, 9-29, https://doi.org/10.1016/j.molcel.2020.03.011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Iacobuzio-Donahue, C. A., Ashfaq, R., Maitra, A., Adsay, N. V., Shen-Ong, G. L., et al. (2003) Highly expressed genes in pancreatic ductal adenocarcinomas: a comprehensive characterization and comparison of the transcription profiles obtained from three major technologies, Cancer Res., 63, 8614-8622, https://doi.org/10.1126/science.1058040.

    Article  CAS  PubMed  Google Scholar 

  11. Swanson, M. S., Nakagawa, T. Y., LeVan, K., and Dreyfuss, G. (1987) Primary structure of human nuclear ribonucleoprotein particle C proteins: conservation of sequence and domain structures in heterogeneous nuclear RNA, mRNA, and pre-rRNA-binding proteins, Mol. Cell. Biol., 7, 1731-1739, https://doi.org/10.1128/MCB.7.5.1731.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Sillekens, P. T. G., Habets, W. J., Beijer, R. P., and van Venrooij, W. J. (1987) CDNA cloning of the human U1 SnRNA-associated A protein: extensive homology between U1 and U2 SnRNP-specific proteins, EMBO J., 6, 3841-3848.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Muto, Y., and Yokoyama, S. (2012) Structural insight into RNA recognition motifs: versatile molecular lego building blocks for biological systems, Wiley Interdisc. Rev. RNA, 3, 229-246, https://doi.org/10.1002/wrna.1107.

    Article  CAS  Google Scholar 

  14. Messias, A. C., and Sattler, M. (2004) Structural basis of single-stranded RNA recognition, Accounts Chem. Res., 37, 279-287, https://doi.org/10.1021/ar030034m.

    Article  CAS  Google Scholar 

  15. Cléry, A., Blatter, M., and Allain, F. H.-T. (2008) RNA recognition motifs: boring? Not quite, Curr. Opin. Struct. Biol., 18, 290-298, https://doi.org/10.1016/j.sbi.2008.04.002.

    Article  CAS  PubMed  Google Scholar 

  16. León, B., Kashyap, M. K., Chan, W. C., Krug, K. A., Castro, J. E., et al. (2017) A challenging pie to splice: drugging the spliceosome, Angewandte Chemie Int. Edn., 56, 12052-12063, https://doi.org/10.1002/anie.201701065.

    Article  CAS  Google Scholar 

  17. Van der Feltz, C., Anthony, K., Brilot, A., and Pomeranz Krummel, D. A. (2012) Architecture of the spliceosome, Biochemistry, 51, 3321-3333, https://doi.org/10.1021/bi201215r.

    Article  CAS  PubMed  Google Scholar 

  18. Mazza, C., Segref, A., Mattaj, I. W., and Cusack, S. (2002) Large-scale induced fit recognition of an m(7)GpppG Cap analogue by the human nuclear Cap-binding complex, EMBO J., 21, 5548-5557, https://doi.org/10.1093/emboj/cdf538.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Calero, G., Wilson, K. F., Ly, T., Rios-Steiner, J. L., Clardy, J. C., and Cerione, R. A. (2002) Structural basis of M7GpppG Binding to the nuclear Cap-binding protein complex, Nat. Struct. Biol., 9, 912-917, https://doi.org/10.1038/nsb874.

    Article  CAS  PubMed  Google Scholar 

  20. Johansson, C., Finger, L. D., Trantirek, L., Mueller, T. D., Kim, S., et al. (2004) Solution structure of the complex formed by the two N-terminal RNA-binding domains of nucleolin and a pre-rRNA target, J. Mol. Biol., 337, 799-816, https://doi.org/10.1016/j.jmb.2004.01.056.

    Article  CAS  PubMed  Google Scholar 

  21. Allain, F. H., Bouvet, P., Dieckmann, T., and Feigon, J. (2000) Molecular basis of sequence-specific recognition of pre-ribosomal RNA by nucleolin, EMBO J., 19, 6870-6881, https://doi.org/10.1093/emboj/19.24.6870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Price, S. R., Evans, P. R., and Nagai, K. (1998) Crystal structure of the spliceosomal U2B′′–U2A′ protein complex bound to a fragment of U2 small nuclear RNA, Nature, 394, 645-650, https://doi.org/10.1038/29234.

    Article  CAS  PubMed  Google Scholar 

  23. Oubridge, C., Ito, N., Evans, P. R., Teo, C. H., and Nagai, K. (1994) Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin, Nature, 372, 432-438, https://doi.org/10.1038/372432a0.

    Article  CAS  PubMed  Google Scholar 

  24. Handa, N., Nureki, O., Kurimoto, K., Kim, I., Sakamoto, H., et al. (1999) Structural basis for recognition of the Tra mRNA precursor by the sex-lethal protein, Nature, 398, 579-584, https://doi.org/10.1038/19242.

    Article  CAS  PubMed  Google Scholar 

  25. Afroz, T., Cienikova, Z., Cléry, A., and Allain, F. H. T. (2015) One, two, three, four! How multiple RRMs read the genome sequence, Methods Enzymol., 558, 235-278, https://doi.org/10.1016/bs.mie.2015.01.015.

    Article  CAS  PubMed  Google Scholar 

  26. Grishin, N. V. (2001) KH domain: one motif, two folds, Nucleic Acids Res., 29, 638-643, https://doi.org/10.1093/nar/29.3.638.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Oddone, A., Lorentzen, E., Basquin, J., Gasch, A., Rybin, V., et al. (2007) Structural and biochemical characterization of the yeast exosome component Rrp40, EMBO Rep., 8, 63-69, https://doi.org/10.1038/sj.embor.7400856.

    Article  CAS  PubMed  Google Scholar 

  28. Auweter, S. D., Oberstrass, F. C., and Allain, F. H.-T. (2006) Sequence-specific binding of single-stranded RNA: is there a code for recognition?, Nucleic Acids Res., 34, 4943-4959, https://doi.org/10.1093/nar/gkl620.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Nicastro, G., Taylor, I. A., and Ramos, A. (2015) KH-RNA interactions: back in the groove, Curr. Opin. Struct. Biol., 30, 63-70, https://doi.org/10.1016/j.sbi.2015.01.002.

    Article  CAS  PubMed  Google Scholar 

  30. Lewis, H. A., Musunuru, K., Jensen, K. B., Edo, C., Chen, H., et al. (2000) Sequence-specific RNA binding by a nova KH domain, Cell, 100, 323-332, https://doi.org/10.1016/S0092-8674(00)80668-6.

    Article  CAS  PubMed  Google Scholar 

  31. Ryder, S. P., and Massi, F. (2010) Insights into the structural basis of RNA recognition by star domain proteins, Adv. Exp. Med. Biol., 693, 37-53, https://doi.org/10.1007/978-1-4419-7005-3_3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Beuth, B., Pennell, S., Arnvig, K. B., Martin, S. R., and Taylor, I. A. (2005) Structure of a Mycobacterium tuberculosis NusA–RNA complex, EMBO J., 24, 3576-3587, https://doi.org/10.1038/sj.emboj.7600829.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lunde, B. M., Moore, C., and Varani, G. (2007) RNA-binding proteins: modular design for efficient function, Nat. Rev. Mol. Cell Biol., 8, 479-490, https://doi.org/10.1038/nrm2178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Valverde, R., Edwards, L., and Regan, L. (2008) Structure and function of KH domains, FEBS J., 275, 2712-2726, https://doi.org/10.1111/j.1742-4658.2008.06411.x.

    Article  CAS  PubMed  Google Scholar 

  35. Diakun, G. P., Fairall, L., and Klug, A. (1986) EXAFS study of the zinc-binding sites in the protein transcription factor IIIA, Nature, 324, 698-699, https://doi.org/10.1038/324698a0.

    Article  CAS  PubMed  Google Scholar 

  36. Ginsberg, A. M., King, B. O., and Roeder, R. G. (1984) Xenopus 5S gene transcription factor, TFIIIA: characterization of a CDNA clone and measurement of RNA levels throughout development, Cell, 39, 479-489, https://doi.org/10.1016/0092-8674(84)90455-0.

    Article  CAS  PubMed  Google Scholar 

  37. Miller, J., McLachlan, A. D., and Klug, A. (1985) Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes, EMBO J., 4, 1609-1614.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Hudson, B. P., Martinez-Yamout, M. A., Dyson, H. J., and Wright, P. E. (2004) Recognition of the mRNA au-rich element by the zinc finger domain of TIS11d, Nat. Struct. Mol. Biol., 11, 257-264, https://doi.org/10.1038/nsmb738.

    Article  CAS  PubMed  Google Scholar 

  39. Iwanaga, E., Nanri, T., Mitsuya, H., and Asou, N. (2011) Mutation in the RNA binding protein TIS11D/ZFP36L2 is associated with the pathogenesis of acute leukemia, Int. J. Oncology, 38, 25-31, https://doi.org/10.3892/ijo_00000820.

    Article  CAS  Google Scholar 

  40. Dey, A., York, D., Smalls-Mantey, A., and Summers, M. F. (2005) Composition and sequence-dependent binding of RNA to the nucleocapsid protein of Moloney murine leukemia virus, Biochemistry, 44, 3735-3744, https://doi.org/10.1021/bi047639q.

    Article  CAS  PubMed  Google Scholar 

  41. D’Souza, V., and Summers, M. F. (2004) Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus, Nature, 431, 586-590, https://doi.org/10.1038/nature02944.

    Article  CAS  PubMed  Google Scholar 

  42. Wang, X., McLachlan, J., Zamore, P. D., and Hall, T. M. T. (2002) Modular recognition of RNA by a human pumilio-homology domain, Cell, 110, 501-512, https://doi.org/10.1016/s0092-8674(02)00873-5.

    Article  CAS  PubMed  Google Scholar 

  43. de Moor, C. H., Meijer, H., and Lissenden, S. (2005) Mechanisms of translational control by the 3′-UTR in development and differentiation, Semin. Cell Dev. Biol., 16, 49-58, https://doi.org/10.1016/j.semcdb.2004.11.007.

    Article  CAS  PubMed  Google Scholar 

  44. Wickens, M., Bernstein, D. S., Kimble, J., and Parker, R. (2002) A PUF family portrait: 3′UTR regulation as a way of life, Trends Genet. TIG, 18, 150-157, https://doi.org/10.1016/s0168-9525(01)02616-6.

    Article  CAS  PubMed  Google Scholar 

  45. Mackay, J. P., Font, J., and Segal, D. J. (2011) The prospects for designer single-stranded RNA-binding proteins, Nat. Struct. Mol. Biol., 18, 256-261, https://doi.org/10.1038/nsmb.2005.

    Article  CAS  PubMed  Google Scholar 

  46. Cheong, C.-G., and Hall, T. M. T. (2006) Engineering RNA sequence specificity of pumilio repeats, Proc. Natl. Acad. Sci. USA, 103, 13635-13639, https://doi.org/10.1073/pnas.0606294103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Antson, A. A., Dodson, E. J., Dodson, G., Greaves, R. B., Chen, X., and Gollnick, P. (1999) Structure of the Trp RNA-binding attenuation protein, TRAP, bound to RNA, Nature, 401, 235-242, https://doi.org/10.1038/45730.

    Article  CAS  PubMed  Google Scholar 

  48. Babitzke, P. (1997) Regulation of tryptophan biosynthesis: Trp-Ing the TRAP or how Bacillus subtilis reinvented the wheel, Mol. Microbiol., 26, 1-9, https://doi.org/10.1046/j.1365-2958.1997.5541915.x.

    Article  CAS  PubMed  Google Scholar 

  49. Elliott, M. B., Gottlieb, P. A., and Gollnick, P. (1999) Probing the TRAP-RNA interaction with nucleoside analogs, RNA, 5, 1277-1289, https://doi.org/10.1017/s1355838299991057.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Theobald, D. L., Mitton-Fry, R. M., and Wuttke, D. S. (2003) Nucleic acid recognition by OB-fold proteins, Annu. Rev. Biophys. Biomol. Struct., 32, 115-133, https://doi.org/10.1146/annurev.biophys.32.110601.142506.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Skordalakes, E., and Berger, J. M. (2003) Structure of the Rho transcription terminator, Cell, 114, 135-146, https://doi.org/10.1016/S0092-8674(03)00512-9.

    Article  CAS  PubMed  Google Scholar 

  52. Bogden, C. E., Fass, D., Bergman, N., Nichols, M. D., and Berger, J. M. (1999) The structural basis for terminator recognition by the Rho transcription termination factor, Mol. Cell, 3, 487-493, https://doi.org/10.1016/S1097-2765(00)80476-1.

    Article  CAS  PubMed  Google Scholar 

  53. Keto-Timonen, R., Hietala, N., Palonen, E., Hakakorpi, A., Lindström, M., and Korkeala, H. (2016) Cold shock proteins: a minireview with special emphasis on Csp-family of enteropathogenic yersinia, Front. Microbiol., 7, https://doi.org/10.3389/fmicb.2016.01151.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Horn, G., Hofweber, R., Kremer, W., and Kalbitzer, H. R. (2007) Structure and function of bacterial cold shock proteins, Cell. Mol. Life Sci., 64, 1457-1470, https://doi.org/10.1007/s00018-007-6388-4.

    Article  CAS  PubMed  Google Scholar 

  55. Amir, M., Kumar, V., Dohare, R., Islam, A., Ahmad, F., and Hassan, M. I. (2018) Sequence, structure and evolutionary analysis of cold shock domain proteins, a member of OB Fold family, J. Evol. Biol., 31, 1903-1917, https://doi.org/10.1111/jeb.13382.

    Article  CAS  PubMed  Google Scholar 

  56. Lyabin, D. N., Eliseeva, I. A., and Ovchinnikov, L. P. (2014) YB-1 protein: functions and regulation, RNA, 5, 95-110, https://doi.org/10.1002/wrna.1200.

    Article  CAS  PubMed  Google Scholar 

  57. Hermann, H., Fabrizio, P., Raker, V. A., Foulaki, K., Hornig, H., et al. (1995) SnRNP Sm proteins share two evolutionarily conserved sequence motifs which are involved in sm protein–protein interactions, EMBO J., 14, 2076-2088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Pomeranz Krummel, D. A., Oubridge, C., Leung, A. K. W., Li, J., and Nagai, K. (2009) Crystal structure of human spliceosomal U1 SnRNP at 5.5 Å resolution, Nature, 458, 475-480, https://doi.org/10.1038/nature07851.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Yong, J., Golembe, T. J., Battle, D. J., Pellizzoni, L., and Dreyfuss, G. (2004) SnRNAs contain specific SMN-binding domains that are essential for SnRNP assembly, Mol. Cell. Biol., 24, 2747-2756, https://doi.org/10.1128/MCB.24.7.2747-2756.2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Kondo, Y., Oubridge, C., van Roon, A.-M. M., and Nagai, K. (2015) Crystal structure of human U1 SnRNP, a small nuclear ribonucleoprotein particle, reveals the mechanism of 5′ splice site recognition, eLife, 4, e04986, https://doi.org/10.7554/eLife.04986.

    Article  PubMed Central  Google Scholar 

  61. Mura, C., Randolph, P. S., Patterson, J., and Cozen, A. E. (2013) Archaeal and eukaryotic homologs of Hfq, RNA Biol., 10, 636-651, https://doi.org/10.4161/rna.24538.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. He, W., and Parker, R. (2000) Functions of Lsm proteins in mRNA degradation and splicing, Curr. Opin. Cell Biol., 12, 346-350, https://doi.org/10.1016/S0955-0674(00)00098-3.

    Article  CAS  PubMed  Google Scholar 

  63. Sharif, H., and Conti, E. (2013) Architecture of the Lsm1-7-Pat1 complex: a conserved assembly in eukaryotic mRNA turnover, Cell Rep., 5, 283-291, https://doi.org/10.1016/j.celrep.2013.10.004.

    Article  CAS  PubMed  Google Scholar 

  64. Sauer, E. (2013) Structure and RNA-binding properties of the bacterial LSm protein Hfq, RNA Biol., 10, 610-618, https://doi.org/10.4161/rna.24201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Murina, V. N., and Nikulin, A. D. (2011) RNA-binding Sm-electrical proteins of bacteria and archaea: similarity and structure of structures and functions [in Russian], Usp. Biol. Khim., 51, 133-164.

    Google Scholar 

  66. Schumacher, M. A., Pearson, R. F., Møller, T., Valentin-Hansen, P., and Brennan, R. G. (2002) Structures of the pleiotropic translational regulator Hfq and an Hfq–RNA complex: a bacterial sm-like protein, EMBO J., 21, 3546-3556, https://doi.org/10.1093/emboj/cdf322.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Link, T. M., Valentin-Hansen, P., and Brennan, R. G. (2009) Structure of Escherichia coli Hfq bound to polyriboadenylate RNA, Proc. Natl. Acad. Sci. USA, 106, 19292-19297, https://doi.org/10.1073/pnas.0908744106.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Vogel, J., and Luisi, B. F. (2011) Hfq and its constellation of RNA, Nat. Rev. Microbiol., 9, 578-589, https://doi.org/10.1038/nrmicro2615.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Someya, T., Baba, S., Fujimoto, M., Kawai, G., Kumasaka, T., and Nakamura, K. (2012) Crystal structure of Hfq from Bacillus subtilis in complex with SELEX-derived RNA aptamer: insight into RNA-binding properties of bacterial Hfq, Nucleic Acids Res., 40, 1856-1867, https://doi.org/10.1093/nar/gkr892.

    Article  CAS  PubMed  Google Scholar 

  70. Masliah, G., Barraud, P., and Allain, F. H.-T. (2012) RNA recognition by double-stranded RNA binding domains: a matter of shape and sequence, Cell. Mol. Life Sci., 70, 1875-1895, https://doi.org/10.1007/s00018-012-1119-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Gleghorn, M. L., and Maquat, L. E. (2014) “Black sheep” that don’t leave the double-stranded RNA-binding domain fold, Trends Biochem. Sci., 39, 328-340, https://doi.org/10.1016/j.tibs.2014.05.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. St. Johnston, D., Brown, N. H., Gall, J. G., and Jantsch, M. (1992) A conserved double-stranded RNA-binding domain, Proc. Natl. Acad. Sci. USA, 89, 10979-10983, https://doi.org/10.1073/pnas.89.22.10979.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Ryter, J. M., and Schultz, S. C. (1998) Molecular basis of double-stranded RNA–protein interactions: structure of a DsRNA-binding domain complexed with DsRNA, EMBO J., 17, 7505-7513, https://doi.org/10.1093/emboj/17.24.7505.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Stefl, R., Xu, M., Skrisovska, L., Emeson, R. B., and Allain, F. H.-T. (2006) Structure and specific RNA binding of ADAR2 double-stranded RNA binding motifs, Structure, 14, 345-355, https://doi.org/10.1016/j.str.2005.11.013.

    Article  CAS  PubMed  Google Scholar 

  75. Spillmann, S., Dohme, F., and Nierhaus, K. H. (1977) Assembly in vitro of the 50 S subunit from Escherichia coli ribosomes: proteins essential for the first heat-dependent conformational change, J. Mol. Biol., 115, 513-523, https://doi.org/10.1016/0022-2836(77)90168-1.

    Article  CAS  PubMed  Google Scholar 

  76. Held, W. A., and Nomura, M. (1973) Structure and function of bacterial ribosomes. XX. Rate-determining step in the reconstitution of Escherichia coli 30S ribosomal subunits, Biochemistry, 12, 3273-3281, https://doi.org/10.1021/bi00741a020.

    Article  CAS  PubMed  Google Scholar 

  77. Nikulin, A. D. (2002) Studies of interactions of ribosomal proteins with ribosomal RNAs, Usp. Biol. Khim., 42, 61-88.

    CAS  Google Scholar 

  78. Nikulin, A. D. (2018) Structural aspects of ribosomal RNA recognition by ribosomal proteins, Biochemistry (Moscow), 83, S111-S133, https://doi.org/10.1134/S0006297918140109.

    Article  CAS  Google Scholar 

  79. Ban, N., Beckmann, R., Cate, J. H., Dinman, J. D., Dragon, F., et al. (2014) A new system for naming ribosomal proteins, Curr. Opin. Struct. Biol., 24, 165-169, https://doi.org/10.1016/j.sbi.2014.01.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Held, W. A., Ballou, B., Mizushima, S., and Nomura, M. (1974) Assembly mapping of 30 S ribosomal proteins from Escherichia coli. Further studies, J. Biol. Chem., 249, 3103-3111.

    Article  CAS  PubMed  Google Scholar 

  81. Gregory, R. J., Zeller, M. L., Thurlow, D. L., Gourse, R. L., Stark, M. J. R., et al. (1984) Interaction of ribosomal proteins S6, S8, S15 and S18 with the central domain of 16 S ribosomal RNA from Escherichia coli, J. Mol. Biol., 178, 287-302, https://doi.org/10.1016/0022-2836(84)90145-1.

    Article  CAS  PubMed  Google Scholar 

  82. Mougel, M., Eyermann, F., Westhof, E., Romby, P., Expert-Bezançon, A., et al. (1987) Binding of Escherichia coli ribosomal protein S8 to 16 S rRNA. A model for the interaction and the tertiary structure of the RNA binding site, J. Mol. Biol., 198, 91-107, https://doi.org/10.1016/0022-2836(87)90460-8.

    Article  CAS  PubMed  Google Scholar 

  83. Svensson, P., Changchien, L. M., Craven, G. R., and Noller, H. F. (1988) Interaction of ribosomal proteins, S6, S8, S15 and S18 with the central domain of 16 S ribosomal RNA, J. Mol. Biol., 200, 301-308, https://doi.org/10.1016/0022-2836(88)90242-2.

    Article  CAS  PubMed  Google Scholar 

  84. Chen, S. S., Sperling, E., Silverman, J. M., Davis, J. H., and Williamson, J. R. (2012) Measuring the dynamics of E. coli ribosome biogenesis using pulse-labeling and quantitative mass spectrometry, Mol. bioSystems, 8, 3325-3334, https://doi.org/10.1039/c2mb25310k.

    Article  CAS  Google Scholar 

  85. Menichelli, E., Edgcomb, S. P., Recht, M. I., and Williamson, J. R. (2012) The structure of aquifex aeolicus ribosomal protein S8 reveals a unique subdomain that contributes to an extremely tight association with 16S rRNA, J. Mol. Biol., 415, 489-502, https://doi.org/10.1016/j.jmb.2011.10.046.

    Article  CAS  PubMed  Google Scholar 

  86. Geyl, D., Böck, A., and Wittmann, H. G. (1977) Cold-sensitive growth of a mutants of Escherichia coli with an altered ribosomal protein S8: analysis of revertants, Mol. Gen. Genet., 152, 331-336, https://doi.org/10.1007/BF00693088.

    Article  CAS  PubMed  Google Scholar 

  87. Powers, T., and Noller, H. F. (1995) Hydroxyl radical footprinting of ribosomal proteins on 16S rRNA, RNA, 1, 194-209.

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Moine, H., Cachia, C., Westhof, E., Ehresmann, B., and Ehresmann, C. (1997) The RNA binding site of S8 ribosomal protein of Escherichia coli: selex and hydroxyl radical probing studies, RNA, 3, 255-268.

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Kalurachchi, K., Uma, K., Zimmermann, R. A., and Nikonowicz, E. P. (1997) Structural features of the binding site for ribosomal protein S8 in Escherichia coli 16S rRNA defined using NMR spectroscopy, Proc. Natl. Acad. Sci. USA, 94, 2139-2144, https://doi.org/10.1073/pnas.94.6.2139.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Gregory, R. J., Cahill, P. B. F., Thurlow, D. L., and Zimmermann, R. A. (1988) Interaction of Escherichia coli ribosomal protein S8 with its binding sites in ribosomal RNA and messenger RNA, J. Mol. Biol., 204, 295-307, https://doi.org/10.1016/0022-2836(88)90577-3.

    Article  CAS  PubMed  Google Scholar 

  91. Yates, J. L., Arfsten, A. E., and Nomura, M. (1980) In vitro expression of Escherichia coli ribosomal protein genes: autogenous inhibition of translation, Proc. Natl. Acad. Sci. USA, 77, 1837-1841, https://doi.org/10.1073/pnas.77.4.1837.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Cerretti, D. P., Mattheakis, L. C., Kearney, K. R., Vu, L., and Nomura, M. (1988) Translational regulation of the spc operon in Escherichia coli, J. Mol. Biol., 204, 309-325, https://doi.org/10.1016/0022-2836(88)90578-5.

    Article  CAS  PubMed  Google Scholar 

  93. Olins, P. O., and 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, https://doi.org/10.1093/nar/9.7.1757.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Merianos, H. J., Wang, J., and Moore, P. B. (2004) The structure of a ribosomal protein S8/Spc operon mRNA complex, RNA, 10, 954-964, https://doi.org/10.1261/rna.7030704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Agalarov, S. C., Sridhar Prasad, G., Funke, P. M., Stout, C. D., and Williamson, J. R. (2000) Structure of the S15,S6,S18-rRNA complex: assembly of the 30S ribosome central domain, Science, 288, 107-113, https://doi.org/10.1126/science.288.5463.107.

    Article  CAS  PubMed  Google Scholar 

  96. Duss, O., Stepanyuk, G. A., Grot, A., O’Leary, S. E., Puglisi, J. D., and Williamson, J. R. (2018) Real-time assembly of ribonucleoprotein complexes on nascent RNA transcripts, Nat. Commun., 9, 5087, https://doi.org/10.1038/s41467-018-07423-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Portier, C., Dondon, L., and Grunberg-Manago, M. (1990) Translational autocontrol of the Escherichia coli ribosomal protein S15, J. Mol. Biol., 211, 407-414, https://doi.org/10.1016/0022-2836(90)90361-O.

    Article  CAS  PubMed  Google Scholar 

  98. Portier, C., Philippe, C., Dondon, L., Grunberg-Manago, M., Ebel, J. P., et al. (1990) Translational control of ribosomal protein S15, Biochim. Biophys. Acta Gene Struct. Express., 1050, 328-336, https://doi.org/10.1016/0167-4781(90)90190-D.

    Article  CAS  Google Scholar 

  99. Philippe, C., Eyermann, F., Benard, L., Portier, C., Ehresmann, B., and 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. USA, 90, 4394-4398, https://doi.org/10.1073/pnas.90.10.4394.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Philippe, C., Bénard, L., Eyermann, F., Cachia, C., Kirillov, S. V., et al. (1994) Structural elements of RpsO mRNA involved in the modulation of translational initiation and regulation of E. coli ribosomal protein S15, Nucleic Acids Res., 22, 2538-2546, https://doi.org/10.1093/nar/22.13.2538.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Mougel, M., Philippe, C., Ebel, J. P., Ehresmann, B., and Ehresmann, C. (1988) The E. coli 16S rRNA binding site of ribosomal protein S15: higher-order structure in the absence and in the presence of the protein, Nucleic Acids Res., 16, 2825-2839.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Serganov, A., Ennifar, E., Portier, C., Ehresmann, B., and 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, https://doi.org/10.1016/S0022-2836(02)00553-3.

    Article  CAS  PubMed  Google Scholar 

  103. Serganov, A., Polonskaia, A., Ehresmann, B., Ehresmann, C., and Patel, D. J. (2003) Ribosomal protein S15 represses its own translation via adaptation of an rRNA-like fold within its mRNA, EMBO J., 22, 1898-1908, https://doi.org/10.1093/emboj/cdg170.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Springer, M., and Portier, C. (2003) More than one way to skin a cat: translational autoregulation by ribosomal protein S15, Nat. Struct. Biol., 10, 420-422, https://doi.org/10.1038/nsb0603-420.

    Article  CAS  PubMed  Google Scholar 

  105. Mathy, N., Pellegrini, O., Serganov, A., Patel, D. J., Ehresmann, C., and 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, https://doi.org/10.1111/j.1365-2958.2004.04005.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Ehresmann, C., Ehresmann, B., Ennifar, E., Dumas, P., Garber, M., et al. (2004) Molecular mimicry in translational regulation: the case of ribosomal protein S15, RNA Biol., 1, 66-73, https://doi.org/10.4161/rna.1.1.958.

    Article  CAS  PubMed  Google Scholar 

  107. Nikonov, S., Nevskaya, N., Eliseikina, I., Fomenkova, N., Nikulin, A., et al. (1996) Crystal structure of the RNA binding ribosomal protein L1 from Thermus thermophilus, EMBO J., 15, 1350-1359.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Brot, N., Caldwell, P., and Weissbach, H. (1981) Regulation of synthesis of Escherichia coli ribosomal proteins L1 and L11, Arch. Biochem. Biophys., 206, 51-53, https://doi.org/10.1016/0003-9861(81)90064-3.

    Article  CAS  PubMed  Google Scholar 

  109. Yates, J. (1981) Feedback regulation of ribosomal protein synthesis in E. coli: localization of the mRNA target sites for repressor action of ribosomal protein L1, Cell, 24, 243-249, https://doi.org/10.1016/0092-8674(81)90520-1.

    Article  CAS  PubMed  Google Scholar 

  110. Tishchenko, S., Nikonova, E., Kostareva, O., Gabdulkhakov, A., Piendl, W., et al. (2011) Structural analysis of interdomain mobility in ribosomal L1 proteins, Acta Crystallograp. Sect. D, 67, 1023-1027, https://doi.org/10.1107/S0907444911043435.

    Article  CAS  Google Scholar 

  111. Nevskaya, N. (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, https://doi.org/10.1093/nar/gki194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Nevskaya, N., Tishchenko, S., Volchkov, S., Kljashtorny, V., Nikonova, E., et al. (2006) New insights into the interaction of ribosomal protein L1 with RNA, J. Mol. Biol., 355, 747-759, https://doi.org/10.1016/j.jmb.2005.10.084.

    Article  CAS  PubMed  Google Scholar 

  113. Tishchenko, S., Nikonova, E., Nikulin, A., Nevskaya, N., Volchkov, S., et al. (2006) Structure of the ribosomal protein L1–mRNA complex at 2.1 Å resolution: common features of crystal packing of L1-RNA complexes, Acta Crystallogr. Sect. D Biol. Crystallogr., 62, 1545-1554, https://doi.org/10.1107/S0907444906041655.

    Article  CAS  Google Scholar 

  114. Tishchenko, S., Nikonova, E., Kljashtorny, V., Kostareva, O., Nevskaya, N., et al. (2007) Domain I of ribosomal protein L1 is sufficient for specific RNA binding, Nucleic Acids Res., 35, 7389-95, https://doi.org/10.1093/nar/gkm898.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Tishchenko, S., Kostareva, O., Gabdulkhakov, A., Mikhaylina, A., Nikonova, E., et al. (2015) Protein–RNA affinity of ribosomal protein L1 mutants does not correlate with the number of intermolecular interactions, Acta Crystallogr. Sect. D Biol. Crystallogr., 71, 376-386, https://doi.org/10.1107/S1399004714026248.

    Article  CAS  Google Scholar 

  116. Nevskaya, N. A., Nikonov, O. S., Revtovich, S. V., Garber, M. B., and Nikonov, S. V. (2004) Identification of RNA-recognizing modules on the surface of ribosomal proteins, Mol. Biol., 38, 789-798, https://doi.org/10.1023/B:MBIL.0000043948.74962.05.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The author is grateful to S. V. Tishchenko for helpful discussion during writing of this review and to S. V. Nikonov, M. B. Garber, and N. A. Nevskaya for the fundamental studies that served as a foundation for this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexey D. Nikulin.

Ethics declarations

The author declares no conflict of interest in financial or any other sphere. The article contains no description of studies involving animals or humans performed by the author.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nikulin, A.D. Characteristic Features of Protein Interaction with Single- and Double-Stranded RNA. Biochemistry Moscow 86, 1025–1040 (2021). https://doi.org/10.1134/S0006297921080125

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297921080125

Keywords

Navigation