Biochemistry (Moscow)

, Volume 80, Issue 4, pp 441–448 | Cite as

Supramolecular organization of Hfq-like proteins

  • V. N. MurinaEmail author
  • O. M. Selivanova
  • A. O. Mikhaylina
  • A. S. Kazakov
  • E. Yu. Nikonova
  • N. V. Lekontseva
  • S. V. Tishchenko
  • A. D. Nikulin


Bacterial Hfq proteins are structural homologs of archaeal and eukaryotic Sm/Lsm proteins, which are characterized by a 5-stranded β-sheet and an N-terminal α-helix. Previously, it was shown that archaeal Lsm proteins (SmAP) could produce long fibrils spontaneously, in contrast to the Hfq from Escherichia coli that could form similar fibrils only after special treatment. The organization of these fibrils is significantly different, but the reason for the dissimilarity has not been found. In the present work, we studied the process of fibril formation by bacterial protein Hfq from Pseudomonas aeruginosa and archaeal protein SmAP from Methanococcus jannaschii. Both proteins have high homology with E. coli Hfq. We found that Hfq from P. aeruginosa could form fibrils after substitutions in the conserved Sm2 motif only. SmAP from M. jannaschii, like other archaeal Lsm proteins, form fibrils spontaneously. Despite differences in the fibril formation conditions, the architecture of both was similar to that described for E. coli Hfq. Therefore, universal nature of fibril architecture formed by Hfq proteins is suggested.

Key words

Sm-like proteins Hfq quaternary structure of proteins fibrils 


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  1. 1.
    Vogel, J., and Luisi, B. F. (2011) Hfq and its constellation of RNA, Nat. Rev. Microbiol., 9, 578–589.CrossRefPubMedGoogle Scholar
  2. 2.
    Valentin-Hansen, P., and Eriksen, M. (2004) Micro-review: the bacterial Sm-like protein Hfq: a key player in RNA transactions, Mol. Microbiol., 51, 1525–1533.CrossRefPubMedGoogle Scholar
  3. 3.
    Brennan, R. G., and Link, T. M. (2007) Hfq structure, function and ligand binding, Curr. Opin. Microbiol., 10, 125–133.CrossRefPubMedGoogle Scholar
  4. 4.
    Beggs, J. D. (2005) Lsm proteins and RNA processing, Biochem. Soc. Trans., 33, 433–438.CrossRefPubMedGoogle Scholar
  5. 5.
    Spiller, M. P., Boon, K.-L., Reijns, M. M., and Beggs, J. D. (2007) The Lsm2–8 complex determines nuclear localization of the spliceosomal U6 snRNA, Nucleic Acids Res., 35, 923–929.CrossRefPubMedCentralGoogle Scholar
  6. 6.
    Mura, C., Randolph, P. S., Patterson, J., and Cozen, A. E. (2013) A structural and evolutionary perspective on Sm function archaeal and eukaryotic homologs of Hfq, RNA Biol., 10, 636–651.CrossRefPubMedCentralPubMedGoogle Scholar
  7. 7.
    Fischer, S., Benz, J., Spath, B., Maier, L.-K., Straub, J., Granzow, M., Raabe, M., Urlaub, H., Hoffmann, J., Brutschy, B., Allers, T., Soppa, J., and Marchfelder, A. (2010) The archaeal Lsm protein binds to small RNAs, J. Biol. Chem., 285, 34429–34438.CrossRefPubMedCentralPubMedGoogle Scholar
  8. 8.
    Murina, V. N., and Nikulin, A. D. (2011) RNA-binding Sm-like proteins of bacteria and archaea: similarity and difference in structure and function, Biochemistry (Moscow), 76, 1434–1449.Google Scholar
  9. 9.
    Khusial, P., Plaag, R., and Zieve, G. W. (2005) LSm proteins form heptameric rings that bind to RNA via repeating motifs, Trends Biochem. Sci., 30, 522–528.CrossRefPubMedGoogle Scholar
  10. 10.
    Robinson, K. E., Orans, J., Kovach, A. R., Link, T. M., and Brennan, R. G. (2014) Mapping Hfq-RNA interaction surfaces using tryptophan fluorescence quenching, Nucleic Acids Res., 42, 2736–2749.CrossRefPubMedCentralPubMedGoogle Scholar
  11. 11.
    Sauter, C. (2003) Sm-like proteins in Eubacteria: the crystal structure of the Hfq protein from Escherichia coli, Nucleic Acids Res., 31, 4091–4098.CrossRefPubMedCentralPubMedGoogle Scholar
  12. 12.
    Salgado-Garrido, J., Bragado-Nilsson, E., Kandels-Lewis, S., and Seraphin, B. (1999) Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin, EMBO J., 18, 3451–3462.CrossRefPubMedCentralPubMedGoogle Scholar
  13. 13.
    Nikulin, A., Stolboushkina, E., Perederina, A., Vassilieva, I., Blaesi, U., Moll, I., Kachalova, G., Yokoyama, S., Vassylyev, D., Garber, M., and Nikonov, S. (2005) Structure of Pseudomonas aeruginosa Hfq protein, Acta Crystallogr. D. Biol. Crystallogr., 61, 141–146.CrossRefPubMedGoogle Scholar
  14. 14.
    Moskaleva, O., Melnik, B., Gabdulkhakov, A., Garber, M., Nikonov, S., Stolboushkina, E., and Nikulin, A. (2010) The structures of mutant forms of Hfq from Pseudomonas aeruginosa reveal the importance of the conserved His57 for the protein hexamer organization, Acta Crystallogr. F, 66, 760–764.CrossRefGoogle Scholar
  15. 15.
    Murina, V. N., Melnik, B. S., Filimonov, V. V., Uhlein, M., Weiss, M. S., Muller, U., and Nikulin, A. D. (2014) Effect of conserved intersubunit amino acid substitutions on Hfq protein structure and stability, Biochemistry (Moscow), 79, 469–477.CrossRefGoogle Scholar
  16. 16.
    Mura, C., Kozhukhovsky, A., Gingery, M., and Phillips, M. (2003) The oligomerization and ligand-binding properties of Sm-like archaeal proteins (SmAPs), Protein Sci., 12, 832–847.CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    Arluison, V., Mura, C., Guzman, M. R., Liquier, J., Pellegrini, O., Gingery, M., Regnier, P., and Marco, S. (2006) Three-dimensional structures of fibrillar Sm proteins: Hfq and other Sm-like proteins, J. Mol. Biol., 356, 86–96.CrossRefPubMedGoogle Scholar
  18. 18.
    Nielsen, J. S., Boggild, A., Andersen, C. B. F., Nielsen, G., Boysen, A., Brodersen, D. E., and Valentin-Hansen, P. (2007) An Hfq-like protein in archaea: crystal structure and functional characterization of the Sm protein from Methanococcus jannaschii, RNA, 13, 2213–2223.CrossRefPubMedCentralPubMedGoogle Scholar
  19. 19.
    Calderone, T. L., Stevens, R. D., and Oas, T. G. (1996) High-level misincorporation of lysine for arginine at AGA codons in a fusion protein expressed in Escherichia coli, J. Mol. Biol., 262, 407–412.CrossRefPubMedGoogle Scholar
  20. 20.
    Brinkmann, U., Mattes, R. E., and Buckel, P. (1989) High-level expression of recombinant genes in Escherichia coli is dependent on the availability of the dnaY gene product, Gene, 85, 109–114.CrossRefPubMedGoogle Scholar
  21. 21.
    Guryanov, S. G., Selivanova, O. M., Nikulin, A. D., Enin, G. A., Melnik, B. S., Kretov, D. A., Serdyuk, I. N., and Ovchinnikov, L. P. (2012) Formation of amyloid-like fibrils by Y-box binding protein 1 (YB-1) is mediated by its cold shock domain and modulated by disordered terminal domains, PLoS One, 7, e36969.CrossRefPubMedCentralPubMedGoogle Scholar
  22. 22.
    Beznosov, S. N., Pyatibratov, M. G., and Fedorov, O. V. (2009) Archaeal flagellas as new nanomaterial creation matrixes, Russ. Nanotechnol., 4, 94–98.CrossRefGoogle Scholar
  23. 23.
    Beznosov, S. N., Pyatibratov, M. G., Fedorov, O. V., Kulova, T. L., and Skundin, A. M. (2011) Electrochemical characteristics of nanostructured material based on modified flagella of halophilic archaea Halobacterium salinarum for the negative electrode of lithium-ion battery, Russ. Nanotechnol., 6, 43–47.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2015

Authors and Affiliations

  • V. N. Murina
    • 1
    Email author
  • O. M. Selivanova
    • 1
  • A. O. Mikhaylina
    • 1
  • A. S. Kazakov
    • 2
  • E. Yu. Nikonova
    • 1
  • N. V. Lekontseva
    • 1
  • S. V. Tishchenko
    • 1
  • A. D. Nikulin
    • 1
  1. 1.Institute of Protein ResearchRussian Academy of SciencesPushchino, Moscow RegionRussia
  2. 2.Institute for Biological InstrumentationRussian Academy of SciencesPushchino, Moscow RegionRussia

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