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Effect of Bacillus cereus hemolysin II on hepatocyte cells

  • To the 50th Anniversary of the Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences
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Abstract

We investigated the efficiency of increasing the permeability (permeabilization) of cell membranes in primary liver cells by Bacillus cereus hemolysin II. An assessment of the degree of permeabilization was carried out by measuring the fluorescence intensity of various low molecular weight dyes, which enter through pores into hepatocyte cells cultivated with hemolysin. We uncovered a high efficacy of hemolysin HlyII action on hepatocyte cell walls, which exceeded the effect of nonionic detergent, digitonin, which is commonly employed for pore formation in various cell membranes. Our results also point to the reversibility of membrane permeabilization in primary hepatocytes. The data obtained in this study can be utilized for assessments of pore-forming activity, in studies of hepatic mechanisms of action, and also the determination of the liver toxicity for different low molecular weight drugs.

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References

  1. Ramarao, N. and Sanchis, V., Toxins (Basel), 2013, vol. 5, no. 6, pp.1119–1139.

    Article  CAS  Google Scholar 

  2. Bernheimer, A.W. and Grushoff, P., J. Bacteriol., 1967, vol. 93, no. 5, pp. 1541–1543.

    PubMed Central  CAS  PubMed  Google Scholar 

  3. Vilas-Boas, G.T., Peruca, A.P., and Arantes, O.M., Can. J. Microbiol., 2007, vol. 53, no. 6, pp. 673–687.

    Article  CAS  PubMed  Google Scholar 

  4. Carlson, C.R., Caugant, D.A., and Kolsto, A.B., Appl. Environ. Microbiol., 1994, vol. 60, no. 6, pp. 1719–1725.

    PubMed Central  CAS  PubMed  Google Scholar 

  5. Fossum, K., Acta Pathol. Microbiol. Scand., 1963, vol. 59, pp. 400–406.

    Article  CAS  PubMed  Google Scholar 

  6. Bowman, M.H., Ottolenghi, A.C., and Mengel, C.E., J. Membr. Biol., 1971, vol. 4, no. 1, pp. 156–164.

    Article  CAS  PubMed  Google Scholar 

  7. Sinev, M.A., Budarina, Zh.I., Gavrilenko, I.V., Tomashevskii, A.I., and Kuz’min, N.P., Mol. Biol., 1993, vol. 27, no. 6, pp. 1218–1229.

    CAS  Google Scholar 

  8. Baida, G., Budarina, Z.I., Kuzmin, N.P., and Solonin, A.S., FEMS Microbiol. Letts., 1999, vol. 180, no. 1, pp. 7–14.

    Article  CAS  Google Scholar 

  9. Andreeva, Z.I., Nesterenko, V.F., Yurkov, I.S., Budarina, Z.I., Sineva, E.V., and Solonin, A.S., Protein Expr. Purif., 2006, vol. 47, no. 1, pp. 186–193.

    Article  CAS  PubMed  Google Scholar 

  10. Miles, G., Bayley, H., and Cheley, S., Protein Sci., 2002, vol. 11, no. 7, pp. 1813–1824.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Andreeva-Kovalevskaya, Zh.I., Solonin, A.S., Sineva, E.V., and Ternovskii, V.I., Usp. Biol. Khim., 2008, vol. 48, pp. 267–318.

    CAS  Google Scholar 

  12. Kataev, A.A., Andreeva-Kovalevskaya, Z.I., Solonin, A.S., and Ternovsky, V.I., Biochim. Biophys. Acta, 2012, vol. 1818, no. 5, pp. 1235–1241.

    Article  CAS  PubMed  Google Scholar 

  13. Andreeva, Z.I., Nesterenko, V.F., Fomkina, M.G., Ternovsky, V.I., Suzina, N.E., Bakulina, A.Y., Solonin, A.S., and Sineva, E.V., Biochim. Biophys. Acta, 2007, vol. 1768, no. 2, pp. 253–263.

    Article  CAS  PubMed  Google Scholar 

  14. Sineva, E.V., Andreeva-Kovalevskaya, Z.I., Shadrin, A.M., Gerasimov, Y.L., Ternovsky, V.I., Teplova, V.V., Yurkova, T.V., and Solonin, A.S., FEMS Microbiol. Letts., 2009, vol. 299, no. 1, pp. 101–109.

    Article  Google Scholar 

  15. Tran, S.L., Guillemet, E., Ngo-Camus, M., Clybouw, C., Puhar, A., Moris, A., Gohar, M., Lereclus, D., and Ramarao, N., Cell Microbiol., 2011, vol. 13, no. 1, pp. 92–108.

    Article  CAS  PubMed  Google Scholar 

  16. Read, T.D., Salzberg, S.L., Pop, M., Shumway, M., Umayam, L., Jiang, L., Holtzapple, E., Busch, J.D., Smith, K.L., Schupp, J.M., Solomon, D., Keim, P., and Fraser, C.M., Science, 2002, vol. 296, pp. 2028–2033.

    Article  CAS  PubMed  Google Scholar 

  17. Shadrin, A.M., Shapyrina, E.V., Siunov, A.V., Severinov, K.V., and Solonin, A.S., Mikrobiologiya, 2007, vol. 76, no. 4, pp. 462–470.

    CAS  Google Scholar 

  18. Moumen, B., Nguen-The, C., and Sorokin, A., Genetics Research International, 2012, article ID 543286, p. 9.

    Google Scholar 

  19. Budarina, Z.I., Sinev, M.A., Mayorov, S.G., Tomashevski, A.Y., Shmelev, I.V., and Kuzmin, N.P., Arch. Microbiol., 1994, vol. 161, pp. 252–257.

    CAS  PubMed  Google Scholar 

  20. Cadot, C., Tran, S.L., Vignaud, M.L., De Buyser, M.L., Kolsto, A.B., Brisabois, A., Nguyen-The, C., Lereclus, D., Guinebretiere, M.H., and Ramarao, N., J. Clin. Microbiol., 2010, vol. 48, no. 4, pp. 1358–1365.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Agaisse, H., Gominet, M., Okstad, O.A., Kolsto, A.B., and Lereclus, D., Mol. Microbiol., 1999, vol. 32, no. 5, pp. 1043–1053.

    Article  CAS  PubMed  Google Scholar 

  22. Slamti, L., Perchat, S., Huillet, E., and Lereclus, D., Toxins (Basel), 2014, vol. 6, no. 8, pp. 2239–2255.

    Article  CAS  Google Scholar 

  23. Budarina, Z.I., Nikitin, D.V., Zenkin, N., Zakharova, M., Semenova, E., Shlyapnikov, M.G., Rodikova, E.A., Masyukova, S., Ogarkov, O., Baida, G.E., Solonin, A.S., and Severinov, K., Microbiology, 2004, vol. 150, no. 11, pp. 3691–3701.

    Article  CAS  PubMed  Google Scholar 

  24. Guillemet, E., Tran, S.L., Cadot, C., Rognan, D., Lereclus, D., and Ramarao, N., PLoS One, 2013, vol. 8, p. e55085.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Harvie, D.R., Vilchez, S., Steggles, J.R., and Ellar, D.J., Microbiology, 2005, vol. 151, no. 2, pp. 569–577.

    Article  CAS  PubMed  Google Scholar 

  26. Sineva, E., Shadrin, A., Rodikova, E.A., Andreeva-Kovalevskaya, Z.I., Protsenko, A.S., Mayorov, S.G., Galaktionova, D.Y., Magelky, E., and Solonin, A.S., J. Bacteriol, 2012, vol. 194, no. 13, pp. 3327–3335.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Rodikova, E.A., Kovalevskiy, O.V., Mayorov, S.G., Budarina, Z.I., Marchenkov, V.V., Melnik, B.S., Leech, A.P., Nikitin, D.V., Shlyapnikov, M.G., and Solonin, A.S., FEBS Lett., 2007, vol. 581, no. 6, pp. 1190–1196.

    Article  CAS  PubMed  Google Scholar 

  28. Kovalevskiy, O.V., Lebedev, A.A., Surin, A.K., Solonin, A.S., and Antson, A.A., J. Mol. Biol., 2007, vol. 365, no. 3, pp. 825–834.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Moore, C.M. and Helmann, J.D., Curr. Opin. Microbiol., 2005, vol. 8, no. 2, pp. 188–195.

    Article  CAS  PubMed  Google Scholar 

  30. Horii, T., Notake, S., Tamai, K., and Yanagisawa, H., FEMS Immunol. Med. Microbiol., 2011, vol. 63, no. 2, pp. 202–209.

    Article  CAS  PubMed  Google Scholar 

  31. Dancer, S.J., McNair, D., Finn, P., and Kolsto, A.B., J. Med. Microbiol., 2002, vol. 51, no. 3, pp. 278–281.

    CAS  PubMed  Google Scholar 

  32. Vadia, S., Arnett, E., Haghighat, A.C., Wilson-Kubalek, E.M., Tweten, R.K., and Seveau, S., PloS Pathog., 2011, vol. 7, no. 11, p. e1002356.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Teplova, V.V., Andreeva-Kovalevskaya, Z.I., Sineva, E.V., and Solonin, A.S., Environ Toxicol. Chem., 2010, vol. 29, no. 6, pp. 1345–1348.

    Article  CAS  PubMed  Google Scholar 

  34. Kholodkov, O.A., Solonin, A.S., and Kovalevskaya, Zh.I., RF Patent No. 2504389, 2014.

  35. Husmann, M., Beckmann, E., Boller, K., Kloft, N., Tenzer, S., Bobkiewicz, W., Neukirch, C., Bayley, H., and Bhakdi, S., FEBS Lett., 2009, vol. 583, no. 2, pp. 337–344.

    Article  CAS  PubMed  Google Scholar 

  36. Atanassoff, A.P., Wolfmeier, H., Schoenauer, R., Hostettler, A., Ring, A., Draeger, A., and Babiychuk, E.B., PloS One, 2014, vol. 9, no. 2, p. e89743.

    Article  PubMed Central  PubMed  Google Scholar 

  37. Pries, A.R., Secomb, T.W., and Gaehtgens, P., Pflugers Arch., 2000, vol. 440, no. 5, pp. 653–666.

    Article  CAS  PubMed  Google Scholar 

  38. Roseman, S., Reflections on glycobiology, J. Biol. Chem., 2001, vol. 276, no. 45, pp. 41527–41542.

    Article  CAS  PubMed  Google Scholar 

  39. Tilley, S.J., Orlova, E.V., Gilbert, R.J., Andrew, P.W., and Saibil, H.R., Cell, 2005, vol. 121, no. 2, pp. 247–256.

    Article  CAS  PubMed  Google Scholar 

  40. Post, S.R., Miyazaki, H., and Tager, H.S., J. Biol. Chem., 1992, vol. 267, no. 36, pp. 25776–25785.

    CAS  PubMed  Google Scholar 

  41. Baker, P.R., Cramer, S.D., Kennedy, M., Assimos, D.G., and Holmes, R.P., Am. J. Physiol. Cell Physiol, vol. 287, no. 5, pp. 1359–1365.

  42. Gnoni, G.V., Paglialonga, G., and Siculella, L., Eur. J. Clin. Invest., 2009, vol. 39, no. 9, pp. 761–768.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to A. S. Solonin.

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Original Russian Text © O.A. Kholodkov, Zh.I. Budarina, Zh.I. Andreeva-Kovalevskaya, A.V. Siunov, A.S. Solonin, 2015, published in Prikladnaya Biokhimiya i Mikrobiologiya, 2015, Vol. 51, No. 2, pp. 258–267.

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Kholodkov, O.A., Budarina, Z.I., Andreeva-Kovalevskaya, Z.I. et al. Effect of Bacillus cereus hemolysin II on hepatocyte cells. Appl Biochem Microbiol 51, 255–263 (2015). https://doi.org/10.1134/S000368381502009X

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  • DOI: https://doi.org/10.1134/S000368381502009X

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