Skip to main content
SpringerLink
Log in

Analysis of protein partners of the human nucleolar protein SURF6 in HeLa cells by a GST pull-down assay

  • Published:
Russian Journal of Bioorganic Chemistry Aims and scope Submit manuscript

Abstract

Proteins of the SURF6 family are evolutionary conservative house-keeping nucleolar proteins, but the functional role of human SURF6 and its protein partners are still unknown. In this study, we use the affinity adsorption (GST pull-down) assay in order to answer these questions. The recombinant human SURF6 and the recombinant conservative C-terminal domain of the mouse Surf6 (Surf6-dom), which has 85% homology with the human SURF6 domain, were fused with glutathione-S-transferase (GST) and used as acceptors. We demonstrated that GST-SURF6 interacts with several RNA processing factors (B23/nucleophosmin, nucleolin, and EBP2), and also with the cofactor of RNA-polymerase I, the UBF protein. The same protein partners were bound to GST-Surf6-dom. These data are the first experimental evidences in favor of the participation of human SURF6 in ribosomal biogenesis, including transcription of rDNA and processing of rRNA. In addition, the set of the protein partners of GST-Surf6-dom in the HeLa cells pointed to a possible interaction of human SURF6 with the nucleolar and nuclear proteins of other functional groups, i.e., to its multifunctionality.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

DTT:

dithiothreitol

GST:

glutathione-S-transferase

IPTG:

isopropylthiogalactoside

PMSF:

phenylmethylsulfonylfluoride

rRNA and rDNA:

ribosomal RNA and DNA, respectively

Surf6:

family of the surfeit locus proteins 6

SURF6-dom:

conservative domain of proteins of the Surf6 family

References

  1. Polzikov, M., Zatsepina, O., and Magoulas, C., Biochem. Biophys. Res. Commun., 2005, vol. 327, pp. 143–149.

    Article  CAS  PubMed  Google Scholar 

  2. Magoulas, C. and Fried, M., DNA Cell. Biol., 1996, vol. 15, pp. 305–316.

    Article  CAS  PubMed  Google Scholar 

  3. Magoulas, C. and Fried, M., Gene, 2000, vol. 243, pp. 115–123.

    Article  CAS  PubMed  Google Scholar 

  4. Wade, C.H., Umbarger, M.A., and McAlear, M.A., Yeast, 2006, vol. 23, pp. 293–306.

    Article  CAS  PubMed  Google Scholar 

  5. Oeffinger, M., Fatica, A., Rout, M.P., and Tollervey, D., Nucleic Acids Res., 2007, vol. 35, pp. 1354–1366.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Yamada, H., Horigome, C., Okada, T., Shirai, C., and Mizuta, K., RNA, 2007, vol. 13, pp. 1977–1987.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Adams, M.D., Celniker, S.E., Holt, R.A., Evans, C.A., Gocayne, J.D., Amanatides, P.G., Scherer, S.E., Li, P.W., Hoskins, R.A., Galle, R.F., et al., Science, 2000, vol. 287, pp. 2185–2195.

    Article  PubMed  Google Scholar 

  8. Milan, D.J., Kim, A.M., Winterfield, J.R., Jones, I.L., Pfeufer, A., Sanna, S., Arking, D.E., Amsterdam, A.H., Sabeh, K.M., Mably, J.D., et al., Circulation, 2009, vol. 120, pp. 553–559.

    Article  PubMed Central  PubMed  Google Scholar 

  9. Wolff, C.M., Nguyen, V.K., and Remy, P., DNA Seq., 2002, vol. 13, pp. 149–152.

    Article  CAS  PubMed  Google Scholar 

  10. Caldwell, R.B., Kierzek, A.M., Arakawa, H., Bezzubov, Y., Zaim, J., Fiedler, P., Kutter, S., Blagodatski, A., Kostovska, D., Koter, M., et al., Genome Biol., 2005, vol. 6, p. 6.

    Article  Google Scholar 

  11. Strausberg, R.L., Feingold, E.A., Grouse, L.H., Derge, J.G., Klausner, R.D., Collins, F.S., Wagner, L., Shenmen, C.M., Schuler, G.D., et al., Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 16899–16903.

    Article  PubMed  Google Scholar 

  12. Zimin, A.V., Delcher, A.L., Florea, L., Kelley, D.R., Schatz, M.C., Puiu, D., Hanrahan, F., Pertea, G., Van Tassell, C.P., Sonstegard, T.S., et al., Genome Biol., 2009, vol. 10, p. 42.

    Article  Google Scholar 

  13. Yan, G., Zhang, G., Fang, X., Zhang, Y., Li, C., Ling, F., Cooper, D.N., Li, Q., Li, Y., van Gool, A.J., et al., Nat. Biotechnol., 2011, vol. 29, pp. 1019–1023.

    Article  CAS  PubMed  Google Scholar 

  14. Tabata, S., Kaneko, T., Nakamura, Y., Kotani, H., Kato, T., Asamizu, E., Miyajima, N., Sasamoto, S., Kimura, T., Hosouchi, T., et al., Nature, 2000, vol. 408, pp. 823–826.

    Article  CAS  PubMed  Google Scholar 

  15. Polzikov, M., Magoulas, C., and Zatsepina, O., Mol. Biol. Rep., 2007, vol. 34, pp. 155–160.

    Article  CAS  PubMed  Google Scholar 

  16. Romanova, L.G., Anger, M., Zatsepina, O.V., and Schultz, R.M., Biol. Reprod., 2006, vol. 75, pp. 690–696.

    Article  CAS  PubMed  Google Scholar 

  17. Magoulas, C., Zatsepina, O.V., Jordan, P.W., Jordan, E.G., and Fried, M., Eur. J. Cell Biol., 1998, vol. 75, pp. 174–183.

    Article  CAS  PubMed  Google Scholar 

  18. Gurchenkov, V.V., Polzikov, M.A., Magoulas, K.B., Romanova, L.G., and Zatsepina, O.V., Russ. J. Bioorg. Chem., 2005, vol. 31, pp. 521–528.

    Article  CAS  Google Scholar 

  19. Wong, D.J., Liu, H., Ridky, T.W., Cassarino, D., Segal, E., and Chang, H.Y., Cell. Stem Cell, 2008, vol. 2, pp. 333–344.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Ji, H., Wu, G., Zhan, X., Nolan, A., Koh, C., De Marzo, A., Doan, H.M., Fan, J., Cheadle, C., Fallahi, M., Cleveland, J.L., Dang, C.V., and Zeller, K.I., PLoS One, 2011, vol. 6, p. e26057.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Moraleva, A.A., Malysheva, M.V., Magoulas, Kh., Polzikov, M.A., and Zatsepina, O.V., Bull. Exp. Biol. Med., 2009, vol. 147, pp. 507–511.

    Article  Google Scholar 

  22. Malysheva, M.V., Moraleva, A.A., Deineko, N.L., Bulycheva, T.I., and Zatsepina, O.V., Immunologiya, 2010, vol. 31, pp. 13–17.

    CAS  Google Scholar 

  23. Wan, D., Gong, Y., Qin, W., Zhang, P., Li, J., Wei, L., Zhou, X., Li, H., Qiu, X., Zhong, F., et al., Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 15724–15729.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Jones, S., Zhang, X., Parsons, D.W., Lin, J.C., Leary, R.J., Angenendt, P., Mankoo, P., Carter, H., Kamiyama, H., Jimeno, A., et al., Science, 2008, vol. 321, pp. 1801–1806.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Cancer Genome Atlas Research Network, Nature, 2011, vol. 474, pp. 609–615.

    Article  Google Scholar 

  26. Cancer Genome Atlas Network, Nature, 2012, vol. 487, pp. 330–337.

    Article  Google Scholar 

  27. Kordyukova, M.Yu., Zatsepina, O.V., and Polzikov, M.A., Appl. Biochem. Microbiol., 2011, vol. 47, pp. 123–127.

    Article  CAS  Google Scholar 

  28. Horsey, E.W., Jakovljevic, J., Miles, T.D., Harnpicharnchai, P., and Woolford, J.L., RNA, 2004, vol. 10, pp. 813–827.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Mattern, K.A., Humbel, B.M., Muijsers, A.O., de Jong, L., and van Driel, R., J. Cell. Biochem., 1996, vol. 62, pp. 275–289.

    Article  CAS  PubMed  Google Scholar 

  30. Albrethsen, J., Knol, J.C., and Jimenez, C.R., J. Proteomics, 2009, vol. 72, pp. 71–81.

    Article  CAS  PubMed  Google Scholar 

  31. Lindström, M.S., Biochem. Res. Int., 2011, vol. 2011, pp. 195–209.

    Article  Google Scholar 

  32. Tajrishi, M.M., Tuteja, R., and Tuteja, N., Commun. Integr. Biol., 2011, vol. 4, pp. 267–275.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Tsujii, R., Miyoshi, K., Tsuno, A., Matsui, Y., Tohe, A., Miyakawa, T., and Mizuta, K., Genes Cells, 2000, vol. 5, pp. 543–553.

    Article  CAS  PubMed  Google Scholar 

  34. Shirai, C., Takai, T., Nariai, M., Horigome, C., and Mizuta, K., J. Biol. Chem., 2004, vol. 279, pp. 25353–25358.

    Article  CAS  PubMed  Google Scholar 

  35. Hirano, Y., Ishii, K., Kumeta, M., Furukawa, K., Takeyasu, K., and Horigome, T., Genes Cells, 2009, vol. 14, pp. 155–166.

    Article  CAS  PubMed  Google Scholar 

  36. Savino, T.M., Bastos, R., Jansen, E., and Hernandez-Verdun, D., J. Cell Sci., 1999, vol. 112, pp. 1889–1900.

    CAS  PubMed  Google Scholar 

  37. Russell, J. and Zomerdijk, J.C., Trends Biochem. Sci., 2005, vol. 30, pp. 87–96.

    Article  CAS  PubMed  Google Scholar 

  38. Jurica, M.S., Licklider, L.J., Gygi, S.R., Grigorieff, N., and Moore, M.J., RNA, 2002, vol. 8, pp. 426–439.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Xiao, R., Tang, P., Yang, B., Huang, J., Zhou, Y., Shao, C., Li, H., Sun, H., Zhang, Y., and Fu, X.D., Mol. Cell, 2012, vol. 45, pp. 656–668.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Braun, R.J. and Zischka, H., Biochim. Biophys. Acta, 2008, vol. 1783, pp. 1418–1435.

    Article  CAS  PubMed  Google Scholar 

  41. Franz, A., Orth, M., Pirson, P.A., Sonneville, R., Blow, J.J., Gartner, A., Stemmann, O., and Hoppe, T., Mol. Cell, 2011, vol. 44, pp. 85–96.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Kressler, D., Hurt, E., Bergler, H., and Bassler, J., Biochim. Biophys. Acta, 2012, vol. 1823, pp. 92–100.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Koike, M., J. Radiat. Res., 2002, vol. 43, pp. 223–236.

    Article  CAS  PubMed  Google Scholar 

  44. Grummt, I., Genes Dev., 2003, vol. 17, pp. 1691–1702.

    Article  CAS  PubMed  Google Scholar 

  45. Rampakakis, E., Di Paola, D., and Zannis-Hadjopoulos, M., J. Cell Sci., 2008, vol. 121, pp. 590–600.

    Article  CAS  PubMed  Google Scholar 

  46. Hill, R. and Lee, P.W., Cell Cycle, 2010, vol. 9, pp. 3460–3469.

    Article  CAS  PubMed  Google Scholar 

  47. Hill, R., Madureira, P.A., Waisman, D.M., and Lee, P.W., Oncotarget, 2011, vol. 2, pp. 1094–1108.

    PubMed Central  PubMed  Google Scholar 

  48. Maiorano, D., Lutzmann, M., and Mechali, M., Curr. Opin. Cell. Biol., 2006, vol. 18, pp. 130–136.

    Article  CAS  PubMed  Google Scholar 

  49. Damoc, E., Fraser, C.S., Zhou, M., Videler, H., Mayeur, G.L., Hershey, J.W., Doudna, J.A., Robinson, C.V., and Leary, J.A., Mol. Cell. Proteomics, 2007, vol. 6, pp. 1135–1146.

    Article  CAS  PubMed  Google Scholar 

  50. Goldman, R.D., Cleland, M.M., Murthy, S.N., Mahammad, S., and Kuczmarski, E.R., J. Struct. Biol., 2012, vol. 177, pp. 14–23.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Holzmann, K., Korosec, T., Gerner, C., Grimm, R., and Sauermann, G., Eur. J. Biochem., 1997, vol. 244, pp. 479–486.

    Article  CAS  PubMed  Google Scholar 

  52. Le Sourd, F., Boulben, S., Le Bouffant, R., Cormier, P., Morales, J., Belle, R., and Mulner-Lorillon, O., Biochim. Biophys. Acta, 2006, vol. 1759, pp. 13–31.

    Article  PubMed  Google Scholar 

  53. Yu, Y., Ji, H., Doudna, J.A., and Leary, J.A., Protein Sci., 2005, vol. 14, pp. 1438–1446.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Odintsova, T.I., Muller, E.C., Ivanov, A.V., Egorov, T.A., Bienert, R., Vladimirov, S.N., Kostka, S., Otto, A., Wittmann-Liebold, B., and Karpova, G.G., J. Protein Chem., 2003, vol. 22, pp. 249–258.

    Article  CAS  PubMed  Google Scholar 

  55. Robledo, S., Idol, R.A., Crimmins, D.L., Ladenson, J.H., Mason, P.J., and Bessler, M., RNA, 2008, vol. 14, pp. 1918–1929.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  56. Chen, J., Guo, K., and Kastan, M.B., J. Biol. Chem., 2012, vol. 287, pp. 16467–16476.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Yaneva, M. and Jhiang, S., Biochim. Biophys. Acta, 1991, vol. 1090, pp. 181–187.

    Article  CAS  PubMed  Google Scholar 

  58. Ahmad, Y., Boisvert, F.M., Gregor, P., Cobley, A., and Lamond, A.I., Nucleic Acids Res., 2009, vol. 37, pp. 181–184.

    Article  Google Scholar 

  59. Schneiter, R., Kadowaki, T., and Tartakofft, A.M., Mol. Cell. Biol., 1995, vol. 6, pp. 357–370.

    Article  CAS  Google Scholar 

  60. Pederson, T., Cold Spring Harb. Perspect. Biol., 2011, vol. 3, p. a000638.

    PubMed Central  PubMed  Google Scholar 

  61. Lebaron, S., Froment, C., Fromont-Racine, M., Rain, J.C., Monsarrat, B., Caizergues-Ferrer, M., and Henry, Y., Mol. Cell. Biol., 2005, vol. 25, pp. 9269–9282.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. Polzikov, M.A., Kordyukova, M.Y., Zavalishina, L.E., Magoulas, C., and Zatsepina, O.V., Hybridoma, 2012, vol. 31, pp. 48–53.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, ul. Miklukho-Maklaya 16/10, GSP-7, Moscow, 117997, Russia

    M. Yu. Kordyukova, M. A. Polzikov, K. V. Shishova & O. V. Zatsepina

Authors
  1. M. Yu. Kordyukova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. A. Polzikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. V. Shishova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. O. V. Zatsepina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. V. Zatsepina.

Additional information

Original Russian Text © M.Yu. Kordyukova, M.A. Polzikov, K.V. Shishova, O.V. Zatsepina, 2014, published in Bioorganicheskaya Khimiya, 2014, Vol. 40, No. 4, pp. 421–432.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kordyukova, M.Y., Polzikov, M.A., Shishova, K.V. et al. Analysis of protein partners of the human nucleolar protein SURF6 in HeLa cells by a GST pull-down assay. Russ J Bioorg Chem 40, 390–400 (2014). https://doi.org/10.1134/S1068162014040062

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1068162014040062

Keywords

Search

Navigation