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On the different sources of cooperativity in pH titrating sites of a membrane protein channel

  • Antonio Alcaraz
  • María Queralt-Martín
Regular Article

Abstract.

Cooperative interactions play a central role in the regulation of protein functions. Here we show that in multi-site systems like ion channels the application of the Hill formalism could require a combination of different experiments, even involving site-directed mutagenesis, to identify the different sources of cooperativity and to discriminate between genuine and apparent cooperativity. We discuss the implications for the channel function in the bacterial porins PorA (N. meningitidis) and OmpF (E. coli) and the viroporin SARS-CoV E.

Graphical abstract

Keywords

Living systems: Structure and Function 

References

  1. 1.
    B. Hille, Ion Channels of Excitable Membranes, third edition (Sinauer Associates Inc, Sunderland, MA, 2001)Google Scholar
  2. 2.
    D.J. Aidley, P.R. Stanfield, Ion Channels: Molecules in Action, 1st edition (Cambridge University Press, 1996)Google Scholar
  3. 3.
    B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, P. Walter, Molecular Biology of the Cell, 4th edition (Garland Science, New York, 2002)Google Scholar
  4. 4.
    J.C. Todt, W.J. Rocque, E.J. McGroarty, Biochemistry 31, 10471 (1992)CrossRefGoogle Scholar
  5. 5.
    A.N. Thompson, D.J. Posson, P.V. Parsa, C.M. Nimigean, Proc. Natl. Acad. Sci. U.S.A. 105, 6900 (2008)ADSCrossRefGoogle Scholar
  6. 6.
    A. Alcaraz, M. Queralt-Martín, E. García-Giménez, V.M. Aguilella, Biochim. Biophys. Acta-Biomembranes 1818, 2777 (2012)CrossRefGoogle Scholar
  7. 7.
    F. Diez-Gonzalez, J.B. Russell, Microbiology 143, 1175 (1997)CrossRefGoogle Scholar
  8. 8.
    K.N. Jordan, L. Oxford, C.P. O’Byrne, Appl. Environ. Microbiol. 65, 3048 (1999)Google Scholar
  9. 9.
    P. Aryal, M.S.P. Sansom, S.J. Tucker, J. Mol. Biol. 427, 121 (2015)CrossRefGoogle Scholar
  10. 10.
    A. Horovitz, A.R. Fersht, J. Mol. Biol. 214, 613 (1990)CrossRefGoogle Scholar
  11. 11.
    Q. Cui, M. Karplus, Protein Sci. 17, 1295 (2008)CrossRefGoogle Scholar
  12. 12.
    J.E. Ferrell, J. Biol. 8, 53 (2009)CrossRefGoogle Scholar
  13. 13.
    T.K. Rostovtseva, T.T. Liu, M. Colombini, V.A. Parsegian, S.M. Bezrukov, Proc. Natl. Acad. Sci. U.S.A. 97, 7819 (2000)ADSCrossRefGoogle Scholar
  14. 14.
    A. Alcaraz, E.M. Nestorovich, M. Aguilella-Arzo, V.M. Aguilella, S.M. Bezrukov, Biophys. J. 87, 943 (2004)CrossRefGoogle Scholar
  15. 15.
    V.M. Aguilella, M. Queralt-Martín, M. Aguilella-Arzo, A. Alcaraz, Integr. Biol. 3, 159 (2011)CrossRefGoogle Scholar
  16. 16.
    A. Alcaraz, M. Queralt-Martín, C. Verdiá-Báguena, V.M. Aguilella, S. Mafé, Nanoscale 6, 15210 (2014)ADSCrossRefGoogle Scholar
  17. 17.
    E.M. Nestorovich, T.K. Rostovtseva, S.M. Bezrukov, Biophys. J. 85, 3718 (2003)CrossRefGoogle Scholar
  18. 18.
    A.V. Hill, J. Physiol. 40, iv (1910)Google Scholar
  19. 19.
    J.S. Lolkema, D.-J. Slotboom, J. Gen. Physiol. 145, 565 (2015)CrossRefGoogle Scholar
  20. 20.
    A. Ben-Naim, Statistical Thermodynamics for Chemistry and Biochemistry (Plenum, New York, 1992)Google Scholar
  21. 21.
    A. Ben-Naim, Cooperativity and Regulation in Biochemical Processes (Springer US, Boston, MA, 2001)Google Scholar
  22. 22.
    M. Vrouenraets, J. Wierenga, W. Meijberg, H. Miedema, Biophys. J. 90, 1202 (2006)ADSCrossRefGoogle Scholar
  23. 23.
    A. Alcaraz, E.M. Nestorovich, M.L. López, E. García-Giménez, S.M. Bezrukov, V.M. Aguilella, Biophys. J. 96, 56 (2009)ADSCrossRefGoogle Scholar
  24. 24.
    J. Cervera, A.G. Komarov, V.M. Aguilella, Biophys. J. 94, 1194 (2008)CrossRefGoogle Scholar
  25. 25.
    O. Teijido, S.M. Rappaport, A. Chamberlin, S.Y. Noskov, V.M. Aguilella, T.K. Rostovtseva, S.M. Bezrukov, J. Biol. Chem. 289, 23670 (2014)CrossRefGoogle Scholar
  26. 26.
    V.M. Aguilella, C. Verdiá-Báguena, A. Alcaraz, Phys. Chem. Chem. Phys. 16, 3881 (2014)CrossRefGoogle Scholar
  27. 27.
    L. Raymond, S.L. Slatin, A. Finkelstein, J. Membr. Biol. 84, 173 (1985)CrossRefGoogle Scholar
  28. 28.
    C. Verdiá-Báguena, J.L. Nieto-Torres, A. Alcaraz, M.L. Dediego, L. Enjuanes, V.M. Aguilella, Biochim. Biophys. Acta 1828, 2026 (2013)CrossRefGoogle Scholar
  29. 29.
    C. Verdiá-Báguena, J.L. Nieto-Torres, A. Alcaraz, M.L. DeDiego, J. Torres, V.M. Aguilella, L. Enjuanes, Virology 432, 485 (2012)CrossRefGoogle Scholar
  30. 30.
    S.J. Edelstein, Annu. Rev. Biochem. 44, 209 (1975)MathSciNetCrossRefGoogle Scholar
  31. 31.
    M. Aguilella-Arzo, J.J. García-Celma, J. Cervera, A. Alcaraz, V.M. Aguilella, Bioelectrochemistry 70, 320 (2007)CrossRefGoogle Scholar
  32. 32.
    T.L. Hill, J. Am. Chem. Soc. 78, 3330 (1956)CrossRefGoogle Scholar
  33. 33.
    D.H. Williams, C.T. Calderone, D.P. O’Brien, R. Zerella Chem. Commun. (Camb.), 1266 (2002) DOI:10.1039/b201428a CrossRefGoogle Scholar
  34. 34.
    C.A. Hunter, S. Tomas, Chem. Biol. 10, 1023 (2003)CrossRefGoogle Scholar
  35. 35.
    E. Yamashita, M.V Zhalnina, S.D. Zakharov, O. Sharma, W.A. Cramer, EMBO J. 27, 2171 (2008)CrossRefGoogle Scholar
  36. 36.
    M. Queralt-Martín, C. Verdiá-Báguena, V.M. Aguilella, A. Alcaraz, Langmuir 29, 15320 (2013)CrossRefGoogle Scholar

Copyright information

© EDP Sciences, SIF, Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Physics, Laboratory of Molecular BiophysicsUniversitat Jaume ICastellónSpain

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