Skip to main content
Log in

Identification of proteins specifically interacting with YB-1 mRNA 3′ UTR and the effect of hnRNP Q on YB-1 mRNA translation

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

Abstract

In this study, proteins specifically interacting with the 3′ untranslated region (UTR) of mRNA of the multifunctional Y-box-binding protein 1 (YB-1) were identified. One of these, hnRNP Q, was shown to specifically interact with the regulatory element (RE) in YB-1 mRNA 3′ UTR and to inhibit translation of this mRNA. Its binding to the RE was accompanied by displacement from this element of the poly(A)-binding protein (PABP), a positive regulator of YB-1 mRNA translation, and by enhanced binding of the negative YB-1 mRNA translation regulator — YB-1 itself.

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.

Similar content being viewed by others

Abbreviations

CRD:

BP (Coding Region Determinant-Binding Protein)

RNA:

binding protein

DTT:

dithiothreitol

EPRS:

glutamyl-prolyl-tRNA-synthetase

hnRNP Q:

heterogeneous nuclear RNP protein Q

IPTG:

isopropyl 1-thio-β-D-galactopyranoside

PABP:

poly(A)-binding protein

RE:

regulatory element

SDS:

sodium dodecyl sulfate

UNR (upstream of N-Ras):

RNA-binding protein from the family of cold shock domain-containing proteins

UTR:

untranslated region

VRC:

vanadyl-ribonucleoside complex

YB-1:

Y-box-binding protein 1

References

  1. Skabkin, M. A., Skabkina, O. V., and Ovchinnikov, L. P. (2004) Uspekhi Biol. Khim., 44, 3–52.

    CAS  Google Scholar 

  2. Eliseeva, I. A., Kim, E. R., Guryanov, S. G., Ovchinnikov, L. P., and Lyabin, D. N. (2011) Biochemistry (Moscow), 76, 1402–1433.

    Article  CAS  Google Scholar 

  3. Lu, Z. H., Books, J. T., and Ley, T. J. (2005) Mol. Cell Biol., 25, 4625–4637.

    Article  PubMed  CAS  Google Scholar 

  4. Ohga, T., Koike, K., Ono, M., Makino, Y., Itagaki, Y., Tanimoto, M., Kuwano, M., and Kohno, K. (1996) Cancer Res., 56, 4224–4228.

    PubMed  CAS  Google Scholar 

  5. Bargou, R. C., Jurchott, K., Wagener, C., Bergmann, S., Metzner, S., Bommert, K., Mapara, M. Y., Winzer, K. J., Dietel, M., Dorken, B., and Royer, H. D. (1997) Nat. Med., 3, 447–450.

    Article  PubMed  CAS  Google Scholar 

  6. Kuwano, M., Oda, Y., Izumi, H., Yang, S. J., Uchiumi, T., Iwamoto, Y., Toi, M., Fujii, T., Yamana, H., Kinoshita, H., Kamura, T., Tsuneyoshi, M., Yasumoto, K., and Kohno, K. (2004) Mol. Cancer Ther., 3, 1485–1492.

    PubMed  CAS  Google Scholar 

  7. Gaudreault, I., Guay, D., and Lebel, M. (2004) Nucleic Acids Res., 32, 316–327.

    Article  PubMed  CAS  Google Scholar 

  8. Levenson, V. V., Davidovich, I. A., and Roninson, I. B. (2000) Cancer Res., 60, 5027–5030.

    PubMed  CAS  Google Scholar 

  9. Pestryakov, P., Zharkov, D. O., Grin, I., Fomina, E. E., Kim, E. R., Hamon, L., Eliseeva, I. A., Petruseva, I. O., Curmi, P. A., Ovchinnikov, L. P., and Lavrik, O. I. (2012) J. Mol. Recognit., 25, 224–233.

    Article  PubMed  CAS  Google Scholar 

  10. Chansky, H. A., Hu, M., Hickstein, D. D., and Yang, L. (2001) Cancer Res., 61, 3586–3590.

    PubMed  CAS  Google Scholar 

  11. Raffetseder, U., Frye, B., Rauen, T., Jurchott, K., Royer, H. D., Jansen, P. L., and Mertens, P. R. (2003) J. Biol. Chem., 278, 18241–18248.

    Article  PubMed  CAS  Google Scholar 

  12. Evdokimova, V., Ruzanov, P., Anglesio, M. S., Sorokin, A. V., Ovchinnikov, L. P., Buckley, J., Triche, T. J., Sonenberg, N., and Sorensen, P. H. (2006) Mol. Cell Biol., 26, 277–292.

    Article  PubMed  CAS  Google Scholar 

  13. Evdokimova, V., Ruzanov, P., Imataka, H., Raught, B., Svitkin, Y., Ovchinnikov, L. P., and Sonenberg, N. (2001) EMBO J., 20, 5491–5502.

    Article  PubMed  CAS  Google Scholar 

  14. Minich, W. B., and Ovchinnikov, L. P. (1992) Biochimie, 74, 477–483.

    Article  PubMed  CAS  Google Scholar 

  15. Nekrasov, M. P., Ivshina, M. P., Chernov, K. G., Kovrigina, E. A., Evdokimova, V. M., Thomas, A. A., Hershey, J. W., and Ovchinnikov, L. P. (2003) J. Biol. Chem., 278, 13936–13943.

    Article  PubMed  CAS  Google Scholar 

  16. Svitkin, Y. V., Evdokimova, V. M., Brasey, A., Pestova, T. V., Fantus, D., Yanagiya, A., Imataka, H., Skabkin, M. A., Ovchinnikov, L. P., Merrick, W. C., and Sonenberg, N. (2009) EMBO J., 28, 58–68.

    Article  PubMed  CAS  Google Scholar 

  17. Koike, K., Uchiumi, T., Ohga, T., Toh, S., Wada, M., Kohno, K., and Kuwano, M. (1997) FEBS Lett., 417, 390–394.

    Article  PubMed  CAS  Google Scholar 

  18. Stein, U., Jurchott, K., Walther, W., Bergmann, S., Schlag, P. M., and Royer, H. D. (2001) J. Biol. Chem., 276, 28562–28569.

    Article  PubMed  CAS  Google Scholar 

  19. Jurchott, K., Bergmann, S., Stein, U., Walther, W., Janz, M., Manni, I., Piaggio, G., Fietze, E., Dietel, M., and Royer, H. D. (2003) J. Biol. Chem., 278, 27988–27996.

    Article  PubMed  Google Scholar 

  20. Higashi, K., Inagaki, Y., Fujimori, K., Nakao, A., Kaneko, H., and Nakatsuka, I. (2003) J. Biol. Chem., 278, 43470–43479.

    Article  PubMed  CAS  Google Scholar 

  21. Stenina, O. I., Shaneyfelt, K. M., and DiCorleto, P. E. (2001) Proc. Natl. Acad. Sci. USA, 98, 7277–7282.

    Article  PubMed  CAS  Google Scholar 

  22. Frye, B. C., Halfter, S., Djudjaj, S., Muehlenberg, P., Weber, S., Raffetseder, U., En-Nia, A., Knott, H., Baron, J. M., Dooley, S., Bernhagen, J., and Mertens, P. R. (2009) EMBO Rep., 10, 783–789.

    Article  PubMed  CAS  Google Scholar 

  23. Rauen, T., Raffetseder, U., Frye, B. C., Djudjaj, S., Muhlenberg, P. J., Eitner, F., Lendahl, U., Bernhagen, J., Dooley, S., and Mertens, P. R. (2009) J. Biol. Chem., 284, 26928–26940.

    Article  PubMed  CAS  Google Scholar 

  24. Ohashi, S., Fukumura, R., Higuchi, T., and Kobayashi, S. (2009) Mol. Cell. Biochem., 327, 267–275.

    Article  PubMed  CAS  Google Scholar 

  25. Shiota, M., Izumi, H., Onitsuka, T., Miyamoto, N., Kashiwagi, E., Kidani, A., Yokomizo, A., Naito, S., and Kohno, K. (2008) Cancer Res., 68, 98–105.

    Article  PubMed  CAS  Google Scholar 

  26. Uramoto, H., Izumi, H., Ise, T., Tada, M., Uchiumi, T., Kuwano, M., Yasumoto, K., Funa, K., and Kohno, K. (2002) J. Biol. Chem., 277, 31694–31702.

    Article  PubMed  CAS  Google Scholar 

  27. Eliseeva, I. A., Ovchinnikov, L. P., and Lyabin, D. N. (2012) RNA Biol., 9, 1473–1487.

    Article  PubMed  CAS  Google Scholar 

  28. Kato, M., Wang, L., Putta, S., Wang, M., Yuan, H., Sun, G., Lanting, L., Todorov, I., Rossi, J. J., and Natarajan, R. (2010) J. Biol. Chem., 285, 34004–34015.

    Article  PubMed  CAS  Google Scholar 

  29. Lyabin, D. N., Eliseeva, I. A., and Ovchinnikov, L. P. (2012) PloS One, 7, e52527.

    Article  PubMed  CAS  Google Scholar 

  30. Lyabin, D. N., Eliseeva, I. A., Skabkina, O. V., and Ovchinnikov, L. P. (2011) RNA Biol., 8, 883–892.

    Article  PubMed  CAS  Google Scholar 

  31. Skabkina, O. V., Lyabin, D. N., Skabkin, M. A., and Ovchinnikov, L. P. (2005) Mol. Cell Biol., 25, 3317–3323.

    Article  PubMed  CAS  Google Scholar 

  32. Skabkina, O. V., Skabkin, M. A., Popova, N. V., Lyabin, D. N., Penalva, L. O., and Ovchinnikov, L. P. (2003) J. Biol. Chem., 278, 18191–18198.

    Article  PubMed  CAS  Google Scholar 

  33. Mazumder, B., Seshadri, V., and Fox, P. L. (2003) Trends Biochem. Sci., 28, 91–98.

    Article  PubMed  CAS  Google Scholar 

  34. Dmitriev, S. E., Terenin, I. M., Rubtsova, M. P., and Shatskii, I. N. (2003) Mol. Biol., 37, 494–503.

    Article  CAS  Google Scholar 

  35. Wakiyama, M., Futami, T., and Miura, K. (1997) Biochimie, 79, 781–785.

    Article  PubMed  CAS  Google Scholar 

  36. Pokrovskaya, I. D., and Gurevich, V. V. (1994) Anal. Biochem., 220, 420–423.

    Article  PubMed  CAS  Google Scholar 

  37. Pelham, H. R., and Jackson, R. J. (1976) Eur. J. Biochem., 67, 247–256.

    Article  PubMed  CAS  Google Scholar 

  38. Mourelatos, Z., Abel, L., Yong, J., Kataoka, N., and Dreyfuss, G. (2001) EMBO J., 20, 5443–5452.

    Article  PubMed  CAS  Google Scholar 

  39. Chang, T. C., Yamashita, A., Chen, C. Y., Yamashita, Y., Zhu, W., Durdan, S., Kahvejian, A., Sonenberg, N., and Shyu, A. B. (2004) Genes Dev., 18, 2010–2023.

    Article  PubMed  CAS  Google Scholar 

  40. Noubissi, F. K., Nikiforov, M. A., Colburn, N., and Spiegelman, V. S. (2010) Genes Cancer, 1, 1074–1082.

    Article  PubMed  CAS  Google Scholar 

  41. Mazumder, B., Sampath, P., and Fox, P. L. (2005) Mol. Cells, 20, 167–172.

    Article  PubMed  CAS  Google Scholar 

  42. Gorlach, M., Burd, C. G., and Dreyfuss, G. (1994) Exp. Cell Res., 211, 400–407.

    Article  PubMed  CAS  Google Scholar 

  43. Mizutani, A., Fukuda, M., Ibata, K., Shiraishi, Y., and Mikoshiba, K. (2000) J. Biol. Chem., 275, 9823–9831.

    Article  PubMed  CAS  Google Scholar 

  44. Moraes, K. C., Quaresma, A. J., Maehnss, K., and Kobarg, J. (2003) Biol. Chem., 384, 25–37.

    Article  PubMed  CAS  Google Scholar 

  45. Weidensdorfer, D., Stohr, N., Baude, A., Lederer, M., Kohn, M., Schierhorn, A., Buchmeier, S., Wahle, E., and Huttelmaier, S. (2009) RNA, 15, 104–115.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. P. Ovchinnikov.

Additional information

Published in Russian in Biokhimiya, 2013, Vol. 78, No. 6, pp. 840–850.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lyabin, D.N., Nigmatullina, L.F., Doronin, A.N. et al. Identification of proteins specifically interacting with YB-1 mRNA 3′ UTR and the effect of hnRNP Q on YB-1 mRNA translation. Biochemistry Moscow 78, 651–659 (2013). https://doi.org/10.1134/S0006297913060102

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297913060102

Key words

Navigation