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Journal for Biophysical Chemistry

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Electrochemical switching of the flavoprotein dodecin at gold surfaces modified by flavin-DNA hybrid linkers

Abstract

Dodecin from Halobacterium salinarum is a dodecameric, hollow-spherical protein, which unspecifically adopts flavin molecules. Reduction of flavin dodecin holocomplexes induces dissociation into apododecin and free flavin. Unspecific binding and dissociation upon reduction were used as key properties to construct an electrochemically switchable surface, which was able to bind and release dodecin apoprotein depending on the applied potential. A flavin modified electrode surface (electrode-DNA-flavin) was generated by direct adsorption of double stranded DNA (ds-DNA) equipped with flavin and disulfide modifications at opposite ends. While the disulfide functionality enabled anchoring the ds-DNA at the gold surface, the flavin exposed at the surface served as the redox-active dodecin docking site. The structures of protein and flavin-DNA hybrid ligands were optimized and characterized by x-ray structural analysis of the holocomplexes. By surface plasmon resonance (SPR) spectroscopy, the adsorption of flavin modified DNA as well as the binding and the electrochemically induced release of dodecin apoprotein could be shown. When the surface immobilization protocol was changed from direct immobilization of the modified ds-DNA to a protocol, which included the hybridization of flavin and thiol modified DNA at the surface, the resulting monolayer was electrochemically inactive. A possible explanation for the strong influence of the surface immobilization protocol on addressing dodecin by the applied potential is that electron transfer is rather mediated by defects in the monolayer than modified ds-DNA.

References

  1. 1

    B. Bieger, L. O. Essen, and D. Oesterhelt, Structure (London) 11, 375 (2003).

    Article  CAS  Google Scholar 

  2. 2

    M. Grininger, F. Seiler, K. Zeth, and D. Oesterhelt, J. Mol. Biol. 364, 561 (2006).

    Article  CAS  Google Scholar 

  3. 3

    M. Grininger, K. Zeth, and D. Oesterhelt, J. Mol. Biol. 357, 842 (2006).

    Article  CAS  Google Scholar 

  4. 4

    D. Zhong and A. H. Zewail, Proc. Natl. Acad. Sci. U.S.A. 98, 11867 (2001).

    Article  CAS  Google Scholar 

  5. 5

    B. Meissner, E. Schleicher, S. Weber, and L.-O. Essen, J. Biol. Chem. 282, 33142 (2007).

    Article  CAS  Google Scholar 

  6. 6

    G. Nöll, E. Kozma, R. Grandori, J. Carey, T. Schoedl, G. Hauska, and J. Daub, Langmuir 22, 2378 (2006).

    Article  Google Scholar 

  7. 7

    O. Dym and D. Eisenberg, Protein Sci. 10, 1712 (2001).

    Article  CAS  Google Scholar 

  8. 8

    A. Lostao, M. El Harrous, F. Daoudi, A. Romero, A. Parody-Morreale, and J. Sancho, J. Biol. Chem. 275, 9518 (2000).

    Article  CAS  Google Scholar 

  9. 9

    F. Patolsky, Y. Weizmann, and I. Willner, Angew. Chem., Int. Ed. 43, 2113 (2004).

    Article  CAS  Google Scholar 

  10. 10

    J. J. Gooding, R. Wibowo, J. Liu, W. Yang, D. Losic, S. Orbons, F. J. Mearns, J. G. Shapter, and D. B. Hibbert, J. Am. Chem. Soc. 125, 9006 (2003).

    Article  CAS  Google Scholar 

  11. 11

    C. Wang, A. S. Batsanov, and M. R. Bryce, J. Org. Chem. 71, 108 (2006).

    Article  CAS  Google Scholar 

  12. 12

    C. Wang, A. S. Batsanov, M. R. Bryce, and I. Sage, Org. Lett. 6, 2181 (2004).

    Article  CAS  Google Scholar 

  13. 13

    Y. Xiao, F. Patolsky, E. Katz, J. F. Hainfeld, and I. Willner, Science 299, 1877 (2003).

    Article  CAS  Google Scholar 

  14. 14

    G. Hartwich, D. J. Caruana, T. de Lumley-Woodyear, Y. Wu, C. N. Campbell, and A. Heller, J. Am. Chem. Soc. 121, 10803 (1999).

    Article  CAS  Google Scholar 

  15. 15

    M. Inouye, R. Ikeda, M. Takase, T. Tsuri, and J. Chiba, Proc. Natl. Acad. Sci. U.S.A. 102, 11606 (2005).

    Article  CAS  Google Scholar 

  16. 16

    S. O. Kelley, N. M. Jackson, M. G. Hill, and J. K. Barton, Angew. Chem., Int. Ed. 38, 941 (1999).

    Article  CAS  Google Scholar 

  17. 17

    T. G. Drummond, M. G. Hill, and J. K. Barton, J. Am. Chem. Soc. 126, 15010 (2004).

    Article  CAS  Google Scholar 

  18. 18

    Y.-T. Long, C.-Z. Li, T. C. Sutherland, M. H. Chahma, J. S. Lee, and H.-B. Kraatz, J. Am. Chem. Soc. 125, 8724 (2003).

    Article  CAS  Google Scholar 

  19. 19

    E. L. S. Wong and J. J. Gooding, J. Am. Chem. Soc. 129, 8950 (2007).

    Article  CAS  Google Scholar 

  20. 20

    E. L. S. Wong and J. J. Gooding, Anal. Chem. 78, 2138 (2006).

    Article  CAS  Google Scholar 

  21. 21

    S. O. Kelley, E. M. Boon, J. K. Barton, N. M. Jackson, and M. G. Hill, Nucleic Acids Res. 27, 4830 (1999).

    Article  CAS  Google Scholar 

  22. 22

    T. G. Drummond, M. G. Hill, and J. K. Barton, Nat. Biotechnol. 21, 1192 (2003).

    Article  CAS  Google Scholar 

  23. 23

    T. M. Herne and M. J. Tarlov, J. Am. Chem. Soc. 119, 8916 (1997).

    Article  CAS  Google Scholar 

  24. 24

    R. Levicky, T. M. Herne, M. J. Tarlov, and S. K. Satija, J. Am. Chem. Soc. 120, 9787 (1998).

    Article  CAS  Google Scholar 

  25. 25

    M. Bockrath, N. Markovic, A. Shepard, M. Tinkham, L. Gurevich, L. P. Kouwenhoven, M. W. Wu, and L. L. Sohn, Nano Lett. 2, 187 (2002).

    Article  CAS  Google Scholar 

  26. 26

    C. Dekker and M. A. Ratner, Phys. World 14, 29 (2001).

    CAS  Google Scholar 

  27. 27

    C. Gomez-Navarro, F. Moreno-Herrero, P. J. De Pablo, J. Colchero, J. Gomez-Herrero, and A. M. Baro, Proc. Natl. Acad. Sci. U.S.A. 99, 8484 (2002).

    Article  CAS  Google Scholar 

  28. 28

    K. Keren, U. Sivan, and E. Braun, in Bioelectronics: From Theory to Applications, edited by I. Willner and E. Katz (Wiley, New York, 2005), p. 265.

    Google Scholar 

  29. 29

    H.-A. Wagenknecht, Angew. Chem., Int. Ed. 42, 2454 (2003).

    Article  CAS  Google Scholar 

  30. 30

    T. Ito, A. Kondo, S. Terada, and S.-I. Nishimoto, J. Am. Chem. Soc. 128, 10934 (2006).

    Article  CAS  Google Scholar 

  31. 31

    A. Manetto, S. Breeger, C. Chatgilialoglu, and T. Carell, Angew. Chem., Int. Ed. 45, 318 (2006).

    Article  CAS  Google Scholar 

  32. 32

    L. Wachter, J. A. Jablonski, and K. L. Ramachandran, Nucleic Acids Res. 14, 7985 (1986).

    Article  CAS  Google Scholar 

  33. 33

    P. Aich, S. L. Labiuk, L. W. Tari, L. J. T. Delbaere, W. J. Roessler, K. J. Falk, R. P. Steer, and J. S. Lee, J. Mol. Biol., 294, 477 (1999).

    Article  CAS  Google Scholar 

  34. 34

    Y. Wang, N. Farrell, and J. D. Burgess, J. Am. Chem. Soc. 123, 5576 (2001).

    Article  CAS  Google Scholar 

  35. 35

    A. B. Steel, R. L. Levicky, T. M. Herne, and M. J. Tarlov, Biophys. J. 79, 975 (2000).

    Article  CAS  Google Scholar 

  36. 36

    K. A. Peterlinz, R. M. Georgiadis, T. M. Herne, and M. J. Tarlov, J. Am. Chem. Soc. 119, 3401 (1997).

    Article  CAS  Google Scholar 

  37. 37

    K. Wang, C. Goyer, A. Anne, and C. Demaille, J. Phys. Chem. B 111, 6051 (2007).

    Article  CAS  Google Scholar 

  38. 38

    A. Anne, C. Bonnaudat, C. Demaille, and K. Wang, J. Am. Chem. Soc. 129, 2734 (2007).

    Article  CAS  Google Scholar 

  39. 39

    T. Liu and J. K. Barton, J. Am. Chem. Soc. 127, 10160 (2005).

    Article  CAS  Google Scholar 

  40. 40

    H. C. M. Yau, H. L. Chan, and M. Yang, Biosens. Bioelectron. 18, 873 (2003).

    Article  CAS  Google Scholar 

  41. 41

    K. J. Stine, D. M. Andrauskas, A. R. Khan, P. Forgo, V. T. D’Souza, J. Liu, and R. M. Friedman, J. Electroanal. Chem. 472, 147 (1999).

    Article  CAS  Google Scholar 

  42. 42

    C. Nogues, S. R. Cohen, S. S. Daube, and R. Naaman, Phys. Chem. Chem. Phys. 6, 4459 (2004).

    Article  CAS  Google Scholar 

  43. 43

    R. Levicky and A. Horgan, Trends Biotechnol. 23, 143 (2005).

    Article  CAS  Google Scholar 

  44. 44

    A. Anne, A. Bouchardon, and J. Moiroux, J. Am. Chem. Soc. 125, 1112 (2003).

    Article  CAS  Google Scholar 

  45. 45

    H. Kimura-Suda, D. Y. Petrovykh, M. J. Tarlov, and L. J. Whitman, J. Am. Chem. Soc. 125, 9014 (2003).

    Article  CAS  Google Scholar 

  46. 46

    F. Shao, K. Augustyn, and J. K. Barton, J. Am. Chem. Soc. 127, 17445 (2005).

    Article  CAS  Google Scholar 

  47. 47

    C. Wagner and H.-A. Wagenknecht, Chem.-Eur. J. 11, 1871 (2005).

    Article  CAS  Google Scholar 

  48. 48

    F. Leng, R. Savkur, I. Fokt, T. Przewloka, W. Priebe, and J. B. Chaires, J. Am. Chem. Soc. 118, 4731 (1996).

    Article  CAS  Google Scholar 

  49. 49

    E. M. Boon, N. M. Jackson, M. D. Wightman, S. O. Kelley, M. G. Hill, and J. K. Barton, J. Phys. Chem. B 107, 11805 (2003).

    Article  CAS  Google Scholar 

  50. 50

    A. Anne and C. Demaille, J. Am. Chem. Soc. 128, 542 (2006).

    Article  CAS  Google Scholar 

  51. 51

    B. Bornemann and A. Marx, Bioorg Med. Chem. 14, 6235 (2006).

    Article  CAS  Google Scholar 

  52. 52

    B. Willner and I. Willner, in Bioelectronics: From Theory to Applications, edited by I. Willner and E. Katz (Wiley, New York, 2005), p. 35.

    Google Scholar 

  53. 53

    See EPAPS Document No. E-BJIOBN-3-003803 for further experimental details and a description of the experimental setup. This document can be reached through a direct link in the online article’s HTML reference section or via the EPAPS homepage (http://www.aip.org/pubservs/epaps.html).

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Grininger, M., Nöll, G., Trawöger, S. et al. Electrochemical switching of the flavoprotein dodecin at gold surfaces modified by flavin-DNA hybrid linkers. Biointerphases 3, 51–58 (2008). https://doi.org/10.1116/1.2965134

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