Skip to main content
SpringerLink
Log in

ABCC Subfamily Vacuolar Transporters are Involved in Pb (Lead) Detoxification in Saccharomyces cerevisiae

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

The present work has as objective to contribute for the elucidation of the mechanism associated with Pb detoxification, using the yeast Saccharomyces cerevisiae as a model organism. The deletion of GTT1 or GTT2 genes, coding for functional glutathione transferases (GST) enzymes in S. cerevisiae, caused an increased susceptibility to high Pb concentrations (500–1000 μmol L−1). These results suggest that the formation of glutathione-Pb conjugate (GS-Pb), dependent of GSTs, is important in Pb detoxification. The involvement of ATP-binding cassette (ABC) vacuolar transporters, belonging to class C subfamily (ABCC) in vacuolar compartmentalization of Pb, was evaluated. For this purpose, mutant strains disrupted in YCF1, VMR1, YBT1 or BPT 1 genes were used. All mutants tested, without vacuolar ABCC transporters, presented an increased sensitivity to 500–1000 μmol L−1 Pb comparative to wild-type strain. Taken together, the obtained results suggest that Pb detoxification, by vacuolar compartmentalization, can occur as a result of the concerted action of GSTs and vacuolar ABCC transporters. Pb is conjugated with glutathione, catalysed by glutathione transferases and followed to the transport of GS-Pb conjugate to the vacuole by ABCC transporters.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. ATSDR (2007). Toxicological profile for lead, Agency for Toxic Substances and Disease Registry (ATSDR). U.S. Department of Health and Human Services—Public Health Service.

  2. Rossi, E. (2008). Clinical Biochemistry Reviews, 29, 63–70.

    Google Scholar 

  3. Avery, S. V. (2011). Biochemistry Journal, 434, 201–210.

    Article  CAS  Google Scholar 

  4. Soares, E. V., Duarte, A. P. S. R., Boaventura, R. A., & Soares, H. M. V. M. (2002). Applied Microbiology and Biotechnology, 58, 836–841.

    Article  CAS  Google Scholar 

  5. Soares, E. V., Hebbelinck, K., & Soares, H. M. V. M. (2003). Canadian Journal of Microbiology, 49, 336–343.

    Article  CAS  Google Scholar 

  6. Bussche, J. V., & Soares, E. V. (2011). Applied Microbiology and Biotechnology, 90, 679–687.

    Article  Google Scholar 

  7. Yuan, X. F., & Tang, C. C. (1999). Journal of Environmental Science and Health Part A-Toxic/Hazardous Substances & Environmental Engineering, 34, 1117–1128.

    Article  Google Scholar 

  8. Yu, S. S., Qin, W., Zhuang, G. Q., Zhang, X. E., Chen, G. J., & Liu, W. F. (2009). Current Microbiology, 58, 504–510.

    Article  CAS  Google Scholar 

  9. Cui, Q. H., & Tang, C. C. (2000). Environmental Science Health Part A-Toxic/Hazardous Substance Environmental Engineering, 35, 1663–1671.

    Article  Google Scholar 

  10. Perez, R. R., Sousa, C. A., Vankeersbilck, T., Machado, M. D., & Soares, E. V. (2013). Current Microbiology, 67, 300–305.

    Article  CAS  Google Scholar 

  11. Wysocki, R., & Tamás, M. J. (2010). FEMS Microbiology Reviews, 34, 925–951.

    Article  CAS  Google Scholar 

  12. Avery, S. V. (2001). Advances in Applied Microbiology, 49, 111–142.

    Article  CAS  Google Scholar 

  13. Ramsay, L. M., & Gadd, G. M. (1997). FEMS Microbiology Letters, 152, 293–298.

    Article  CAS  Google Scholar 

  14. Sousa, C. A., Perez, R. R., & Soares, E. V. (2014). Current Microbiology, 68, 113–119.

    Article  CAS  Google Scholar 

  15. Li, Z. S., Lu, Y. P., Zhen, R. G., Szczypka, M., Thiele, D. J., & Rea, P. A. (1997). Proceedings of the National Academy of Sciences of the United States of America, 94, 42–47.

    Article  CAS  Google Scholar 

  16. Szczypka, M. S., Wemmie, J. A., Moyerowley, W. S., & Thiele, D. J. (1994). Journal of Biological Chemistry, 269, 22853–22857.

    CAS  Google Scholar 

  17. Gueldry, O., Lazard, M., Delort, F., Dauplais, M., Grigoras, I., Blanquet, S., & Plateau, P. (2003). European Journal of Biochemistry, 270, 2486–2496.

    Article  CAS  Google Scholar 

  18. Choi, J. H., Lou, W., & Vancura, A. (1998). Journal of Biological Chemistry, 273, 29915–29922.

    Article  CAS  Google Scholar 

  19. Paumi, C. M., Chuk, M., Snider, J., Stagljar, I., & Michaelis, S. (2009). Microbiology and Molecular Biology Reviews, 73, 577–593.

    Article  CAS  Google Scholar 

  20. Wawrzycka, D., Sobczak, I., Bartosz, G., Bocer, T., Ulaszewski, S., & Goffeau, A. (2010). FEMS Yeast Research, 10, 828–838.

    Article  CAS  Google Scholar 

  21. Petrovic, S., Pascolo, L., Gallo, R., Cupelli, F., Ostrow, J. D., Goffeau, A., Tiribelli, C., & Bruschi, C. V. (2000). Yeast, 16, 561–571.

    Article  CAS  Google Scholar 

  22. Ortiz, D. F., StPierre, M. V., Abdulmessih, A., & Arias, I. M. (1997). Journal of Biological Chemistry, 272, 15358–15365.

    Article  CAS  Google Scholar 

  23. Sasser, T. L., Padolina, M., & Fratti, R. A. (2012). Biochemical Journal, 448, 365–372.

    Article  CAS  Google Scholar 

  24. Mason, D. L., Mallampalli, M. P., Huyer, G., & Michaelis, S. (2003). Eukaryotic Cell, 2, 588–598.

    Article  CAS  Google Scholar 

  25. Li, Z. S., Szczypka, M., Lu, Y. P., Thiele, D. J., & Rea, P. A. (1996). Journal of Biological Chemistry, 271, 6509–6517.

    Article  CAS  Google Scholar 

  26. Haugland, R. P. (2005). The handbook—a guide to fluorescent probes and labeling technologies, 10th edition. Eugene, OR, USA: Invitrogen Corp.

    Google Scholar 

  27. Board, P. G., & Menon, D. (2013). Biochimica et Biophysica Acta-General Subjects, 1830, 3267–3288.

  28. Adamis, P. D. B., Gomes, D. S., Pinto, M., Panek, A. D., & Eleutherio, E. C. A. (2004). Toxicology Letters, 154, 81–88.

    Article  CAS  Google Scholar 

  29. Sharma, K. G., Mason, D. L., Liu, G. S., Rea, P. A., Bachhawat, A. K., & Michaelis, S. (2002). Eukaryotic Cell, 1, 391–400.

    Article  CAS  Google Scholar 

  30. Ghosh, M., Shen, J., & Rosen, B. P. (1999). Proceedings of the National Academy of Sciences of the United States of America, 96, 5001–5006.

    Article  CAS  Google Scholar 

  31. Song, W. Y., Sohn, E. J., Martinoia, E., Lee, Y. J., Yang, Y. Y., Jasinski, M., Forestier, C., Hwang, I., & Lee, Y. (2003). Nature Biotechnology, 21, 914–919.

    Article  CAS  Google Scholar 

  32. Prévéral, S., Ansoborlo, E., Mari, S., Vavasseur, A., & Forestier, C. (2006). Biochimie, 88, 1651–1663.

    Article  Google Scholar 

  33. Soares, H. M. V. M., Conde, P. C. F. L., Almeida, A. A. N., & Vasconcelos, M. T. S. D. (1999). Analytica Chimica Acta, 394, 325–335.

    Article  CAS  Google Scholar 

  34. Soares, E. V., Duarte, A., & Soares, H. (2000). Chemical Speciation and Bioavailability, 12, 59–65.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the FCT Strategic Project PEst-OE/EQB/LA0023/2013.

Author information

Authors and Affiliations

  1. Bioengineering Laboratory-CIETI, Chemical Engineering Department, ISEP-School of Engineering of Polytechnic Institute of Porto, Rua Dr António Bernardino de Almeida, 431, 4200-072, Porto, Portugal

    Cátia A. Sousa, Simon Hanselaer & Eduardo V. Soares

  2. Faculty of Engineering Technology, KU Leuven, Gebroeders Desmetstraat 1, 9000, Ghent, Belgium

    Simon Hanselaer

  3. CEB-Centre of Biological Engineering, University of Minho, 4710-057, Braga, Portugal

    Eduardo V. Soares

Authors
  1. Cátia A. Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Simon Hanselaer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eduardo V. Soares
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eduardo V. Soares.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sousa, C.A., Hanselaer, S. & Soares, E.V. ABCC Subfamily Vacuolar Transporters are Involved in Pb (Lead) Detoxification in Saccharomyces cerevisiae . Appl Biochem Biotechnol 175, 65–74 (2015). https://doi.org/10.1007/s12010-014-1252-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-014-1252-0

Keywords

Search

Navigation