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Biochemistry (Moscow)

, Volume 83, Issue 11, pp 1369–1379 | Cite as

Contribution of Eutrema salsugineum Cold Shock Domain Structure to the Interaction with RNA

  • V. V. Taranov
  • N. E. Zlobin
  • K. I. Evlakov
  • A. O. ShamustakimovaEmail author
  • A. V. Babakov
Article
  • 18 Downloads

Abstract

Plant cold shock domain proteins (CSDPs) are DNA/RNA-binding proteins. CSDPs contain the conserved cold shock domain (CSD) in the N-terminal part and a varying number of the CCHC-type zinc finger (ZnF) motifs alternating with glycine-rich regions in the C-terminus. CSDPs exhibit RNA chaperone and RNA-melting activities due to their non-specific interaction with RNA. At the same time, there are reasons to believe that CSDPs also interact with specific RNA targets. In the present study, we used three recombinant CSDPs from the saltwater cress plant (Eutrema salsugineum)-EsCSDP1, EsCSDP2, EsCSDP3 with 6, 2, and 7 ZnF motifs, respectively, and showed that their nonspecific interaction with RNA is determined by their C-terminal fragments. All three proteins exhibited high affinity to the single-stranded regions over four nucleotides long within RNA oligonucleotides. The presence of guanine in the single-or double-stranded regions was crucial for the interaction with CSDPs. Complementation test using E. coli BX04 cells lacking four cold shock protein genes (ΔcspA, ΔcspB, ΔcspE, ΔcspG) revealed that the specific binding of plant CSDPs with RNA is determined by CSD.

Keywords

Eutrema salsugineuArabidopsis thaliana cold shock domain proteins cold shock domain zinc fingers RNA-protein interaction 

Abbreviations

a.a.

amino acid

AtCSDP1-3

Arabidopsis thaliana cold shock domain proteins 1-3

CSD(P)

cold shock domain (protein)

EsCSDP1-3

Eutrema salsugineum cold shock domain proteins 1-3

R6G

fluorescent dye rhodamine

RIF

fluorescently-labelled RNA oligonucleotide

RNP

RNA-binding motif

ZnF

zinc finger motif

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References

  1. 1.
    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.CrossRefPubMedGoogle Scholar
  2. 2.
    Bae, W., Xia, B., Inouye, M., and Severinov, K. (2000) Escherichia coli CspA-family RNA chaperones are transcription antiterminators, Proc. Natl. Acad. Sci. USA, 97, 7784–7789.CrossRefPubMedGoogle Scholar
  3. 3.
    Jiang, W., Hou, Y., and Inouye, M. (1997) CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone, J. Biol. Chem., 272, 196–202.CrossRefPubMedGoogle Scholar
  4. 4.
    Phadtare, S., and Severinov, K. (2010) RNA remodeling and gene regulation by cold shock proteins, RNA Biol., 7, 788–795.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Mihailovich, M., Militti, C., Gabaldon, T., and Gebauer, F. (2010) Eukaryotic cold shock domain proteins: highly versatile regulators of gene expression, Bioessays, 32, 109–118.CrossRefPubMedGoogle Scholar
  6. 6.
    Chaikam, V., and Karlson, D. T. (2010) Comparison of structure, function and regulation of plant cold shock domain proteins to bacterial and animal cold shock domain proteins, Biochem. Mol. Biol. Rep., 43, 1–8.Google Scholar
  7. 7.
    Lasham, A., Moloney, S., Hale, T., Homer, C., Zhang, Y. F., Murison, J. G., Braithwaite, A. W., and Watson, J. (2003) The Y-box-binding protein, YB1, is a potential negative regulator of the p53 tumor suppressor, J. Biol. Chem., 278, 35516–35523.CrossRefPubMedGoogle Scholar
  8. 8.
    Moss, E. G., Lee, R. C., and Ambros, V. (1997) The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA, Cell, 88, 637–646.CrossRefPubMedGoogle Scholar
  9. 9.
    Newman, M. A., Thomson, J. M., and Hammond, S. M. (2008) Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing, RNA, 14, 1539–1549.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Mayr, F., Schutz, A., Doge, N., and Heinemann, U. (2012) The Lin28 cold-shock domain remodels pre-let-7 microRNA, Nucleic Acids Res., 40, 7492–7506.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Sasaki, K., and Imai, R. (2012) Pleiotropic roles of cold shock domain proteins in plants, Front. Plant Sci., 2,116.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Nakaminami, K., Hill, K., Perry, S. E., Sentoku, N., Long, J. A., and Karlson, D. T. (2009) Arabidopsis cold shock domain proteins: relationships to floral and silique development, J. Exp. Bot., 60, 1047–1062.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Chaikam, V., and Karlson, D. T. (2010) Comparison of structure, function and regulation of plant cold shock domain proteins to bacterial and animal cold shock domain proteins, BMB Rep., 43, 1–8.CrossRefPubMedGoogle Scholar
  14. 14.
    Karlson, D., Nakaminami, K., Toyomasu, T., and Imai, R. (2002) A cold regulated nucleic acid binding protein of winter wheat shares a domain with bacterial cold shock proteins, J. Biol. Chem., 277, 35248–35356.CrossRefPubMedGoogle Scholar
  15. 15.
    Radkova, M., Vitamvas, P., Sasaki, K., and Imai, R. (2014) Development- and cold-regulated accumulation of cold shock domain proteins in wheat, Plant Physiol. Biochem., 77, 44–48.CrossRefPubMedGoogle Scholar
  16. 16.
    Chaikman, V., and Karlson, D. (2008) Functional characterization of two cold shock domain proteins from Oryza sativa, Plant Cell Env., 31, 995–1006.CrossRefGoogle Scholar
  17. 17.
    Karlson, D., and Imai, R. (2003) Conservation of the cold shock domain protein family in plants, Plant Physiol., 131, 12–15.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Taranov, V. V., Berdnikova, M. V., Nosov, A. V., Galkin, A. V., and Babakov, A. V. (2010) Cold shock domain proteins in the extremophyte Thellungiella salsuginea (salt cress): gene structure and differential response to cold, Mol. Biol. (Moscow), 44, 787–794.CrossRefGoogle Scholar
  19. 19.
    Choi, M. J., Park, Y. R., Park, S. J., and Kang, H. (2015) Stress-responsive expression patterns and functional characterization of cold shock domain proteins in cabbage (Brassica rapa) under abiotic stress conditions, Plant Physiol. Biochem., 96, 132–140.CrossRefPubMedGoogle Scholar
  20. 20.
    Sasaki, K., Kim, M. H., and Imai, R. (2007) Arabidopsis cold shock domain protein 2 is an RNA chaperone that is regulated by cold and developmental signals, Biochem. Biophys. Res. Commun., 364, 633–638.CrossRefPubMedGoogle Scholar
  21. 21.
    Nakaminami, K., Sasaki, K., Kajita, S., Takeda, H., Karlson, D., Ohgi, K., and Imai, R. (2005) Heat stable ssDNA/RNA-binding activity of a wheat cold shock domain protein, FEBS Lett., 579, 4887–4891.CrossRefPubMedGoogle Scholar
  22. 22.
    Nakaminami, K., Karlson, D. T., and Imai, R. (2006) Functional conservation of cold shock domains in bacteria and higher plants, Proc. Natl. Acad. Sci. USA, 103, 10122–10127.CrossRefPubMedGoogle Scholar
  23. 23.
    Zlobin, N., Evlakov, K., Alekseev, Y., Blagodatskikh, K., Babakov, A., and Taranov, V. (2016) High DNA melting activity of extremophyte Eutrema salsugineum cold shock domain proteins EsCSDP1 and EsCSDP3, Biochem. Biophys. Rep., 5, 502–508.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Juntawong, P., Sorenson, R., and Bailey-Serres, J. (2013) Cold shock protein 1 chaperones mRNAs during translation in Arabidopsis thaliana, Plant J., 74, 1016–1028.CrossRefPubMedGoogle Scholar
  25. 25.
    Stefani, G., Chen, X., Zhao, H., and Slack, F. J. (2015) A novel mechanism of LIN-28 regulation of let-7 microRNA expression revealed by in vivo HITS-CLIP in C. elegans, RNA, 21, 985–996.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Kudryashova, E. V., Gladilin, A. K., and Levashov, A. V. (2002) Proteins in supramolecular assemblies: structure study by time-resolved fluorescence anisotropy, Uspekhi Biol. Khim., 42, 257–294.Google Scholar
  27. 27.
    Xia, B., Ke, H., and Inouye, M. (2001) Acquirement of cold sensitivity by quadruple deletion of the cspA family and its suppression by PNPase S1 domain in Escherichia coli, Mol. Microbiol., 40, 179–188.CrossRefPubMedGoogle Scholar
  28. 28.
    Kim, M. H., and Imai, R. (2015) Determination of RNA chaperone activity using an Escherichia coli mutant, in RNA Remodeling Proteins, Humana Press, New York, NY, pp. 117–123.Google Scholar
  29. 29.
    Nam, Y., Chen, C., Gregory, R. I., Chou, J. J., and Sliz, P. (2011) Molecular basis for interaction of let-7 microRNAs with Lin28, Cell, 147, 1080–1091.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Loughlin, F. E., Gebert, L. F., Towbin, H., Brunschweiger, A., Hall, J., and Allain, F. H. (2012) Structural basis of pre-let-7 miRNA recognition by the zinc knuckles of pluripotency factor Lin28, Nat. Struct. Mol. Biol., 19, 84–89.CrossRefGoogle Scholar
  31. 31.
    Kim, M. H., Sonoda, Y., Sasaki, K., Kaminaka, H., and Imai, R. (2013) Interactome analysis reveals versatile functions of Arabidopsis cold shock domain protein 3 in RNA processing within the nucleus and cytoplasm, Cell Stress Chaperones, 18, 517–525.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Li, C., Sako, Y., Imai, A., Nishiyama, T., Thompson, K., Kubo, M., Hiwatashi, Y., Kabeya, Y., Karlson, D., Wu, S.-H., Ishikawa, M., Murata, T., Benfey, P. N., Sato, Y., Tamada, Y., and Hasebel, M. (2017) A Lin28 homologue reprograms differentiated cells to stem cells in the moss Physcomitrella patens, Nat. Commun., 8, 14242.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Yu, J., Vodyanik, M. A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J. L., Tian, S., Nie, J., Jonsdottir, G. A., Ruotti, V., Stewart, R., Slukvin, I. I., and Thomson, A. (2007) Induced pluripotent stem cell lines derived from human somatic cells, Science, 318, 1917–1920.CrossRefPubMedGoogle Scholar
  34. 34.
    Mayr, F., and Heinemann, U. (2013) Mechanisms of Lin28-mediated miRNA and mRNA regulation-a structural and functional perspective, Int. J. Mol. Sci., 14, 16532–16553.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • V. V. Taranov
    • 1
  • N. E. Zlobin
    • 1
  • K. I. Evlakov
    • 1
  • A. O. Shamustakimova
    • 1
    Email author
  • A. V. Babakov
    • 1
  1. 1.All-Russia Research Institute of Agricultural BiotechnologyMoscowRussia

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