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Proton-coupled electron hopping in Ru-modified P. aeruginosa azurin

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Abstract

We constructed two artificial multiple-step electron transfer (hopping) systems based on Pseudomonas aeruginosa azurin where a tyrosine (YOH) is situated between Ru(2,2′-bipyridine)2(imidazole)(histidine) and the native copper site: RuH107YOH109 and RuH124-YOH122. We investigated the rates of CuI oxidation by flash-quench generated RuIII over a range of conditions that probed the role of proton-coupled oxidation/reduction of YOH in the reaction. Rates of CuI oxidation were enhanced over single-step electron transfer by factors between 3 and 80, depending on specific scaffold and buffer conditions.

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References

  1. Hammes-Schiffer S (2010) Chem Rev 110:6937–7100

  2. Rappaport F, Diner BA (2008) Coord Chem Rev 252:259–272

    Article  CAS  Google Scholar 

  3. McEvoy JP, Brudvig GW (2006) Chem Rev 106:4455–4483

    Article  CAS  PubMed  Google Scholar 

  4. Siegbahn PEM (2009) Dalton Trans 45:10063–10068

    Article  PubMed  Google Scholar 

  5. Stubbe J, Nocera DG, Yee CS, Chang MCY (2003) Chem Rev 103:2167–2201

    Article  CAS  PubMed  Google Scholar 

  6. Jiang W, Saleh L, Barr EW, Xie J, Gardner MM, Krebs C, Bollinger JM (2008) Biochemistry 47:8477–8484

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Yokoyama K, Smith AA, Corzilius B, Griffin RG, Stubbe J (2011) J Am Chem Soc 133:18420–18432

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Kaila VRI, Verkhovsky MI, Wikström M (2010) Chem Rev 110:7062–7081

    Article  CAS  PubMed  Google Scholar 

  9. Brzezinski P, Aedelroth P (2006) Curr Opin Struct Biol 16:465–472

    Article  CAS  PubMed  Google Scholar 

  10. Hosler JP, Ferguson-Miller S, Mills DA (2006) Annu Rev Biochem 75:165–187

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Gray HB, Malmström BG, Williams RJP (2000) J Biol Inorg Chem 5:551–559

    Article  CAS  PubMed  Google Scholar 

  12. Edwards PP, Gray HB, Lodge MTJ, Williams RJP (2008) Angew Chem Int Ed 47:6758–6765

    Article  CAS  Google Scholar 

  13. Weinberg DR, Gagliardi CJ, Hull JF, Murphy CF, Kent CA, Westlake BC, Paul A, Ess DH, McCafferty DG, Meyer TJ (2012) Chem Rev 112:4016–4093

    Article  CAS  PubMed  Google Scholar 

  14. Warren JJ, Tronic TA, Mayer JM (2010) Chem Rev 110:6961–7001

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Krishtalik LI (2003) Biochim Biophys Acta 1604:13–21

    Article  CAS  PubMed  Google Scholar 

  16. Irebo T, Reece SY, Sjoedin M, Nocera DG, Hammarström L (2007) J Am Chem Soc 129:15462–15464

    Article  CAS  PubMed  Google Scholar 

  17. Sjödin M, Irebo T, Utas JE, Lind J, Merényi G, Åkermark B, Hammarström L (2006) J Am Chem Soc 128:13076–13083

    Article  PubMed  Google Scholar 

  18. Irebo T, Zhang M-T, Markle TF, Scott AM, Hammarström L (2012) J Am Chem Soc 134:16247–16254

    Article  CAS  PubMed  Google Scholar 

  19. Fecenko CJ, Meyer TJ, Thorp HH (2006) J Am Chem Soc 128:11020–11021

    Article  CAS  PubMed  Google Scholar 

  20. Fecenko CJ, Thorp HH, Meyer TJ (2007) J Am Chem Soc 129:15098–15099

    Article  CAS  PubMed  Google Scholar 

  21. Song N, Gagliardi CJ, Binstead RA, Zhang M-T, Thorp H, Meyer TJ (2012) J Am Chem Soc 134:18538–18541

    Article  CAS  PubMed  Google Scholar 

  22. Song N, Stanbury DM (2008) Inorg Chem 47:11458–11460

    Article  CAS  PubMed  Google Scholar 

  23. Song N, Stanbury DM (2012) Inorg Chem 51:4909–4911

    Article  CAS  PubMed  Google Scholar 

  24. Bonin J, Costentin C, Robert M, Savéant J-M (2011) Org Biomol Chem 9:4064–4069

    Article  CAS  PubMed  Google Scholar 

  25. Bonin J, Costentin C, Louault C, Robert M, Routier M, Savéant J-M (2010) Proc Natl Acad Sci USA 107:3367–3372

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Costentin C, Louault C, Robert M, Savéant J-M (2009) Proc Natl Acad Sci USA 106:18143–18148

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Mayer JM (2004) Annu Rev Phys Chem 55:363–390

    Article  CAS  PubMed  Google Scholar 

  28. Biczók L, Gupta N, Linschitz H (1997) J Am Chem Soc 119:12601–12609

    Article  Google Scholar 

  29. Rhile IJ, Mayer JM (2004) J Am Chem Soc 126:12718–12719

    Article  CAS  PubMed  Google Scholar 

  30. Rhile IJ, Markle TF, Nagao H, DiPasquale AG, Lam OP, Lockwood MA, Rotter K, Mayer JM (2006) J Am Chem Soc 128:6075–6088

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Sibert RS, Josowicz M, Barry BA (2010) ACS Chem Biol 5:1157–1168

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Martínez-Rivera MC, Berry BW, Valentine KG, Westerlund K, Hay S, Tommos C (2011) J Am Chem Soc 133:17786–17795

    Article  PubMed Central  PubMed  Google Scholar 

  33. Minnihan EC, Nocera DG, Stubbe J (2013) Acc Chem Res 46:2524–2535

    Article  CAS  PubMed  Google Scholar 

  34. Warren JJ, Herrera N, Hill MG, Winkler JR, Gray HB (2013) J Am Chem Soc 135:11151–11158

    Article  CAS  PubMed  Google Scholar 

  35. Faham S, Day MW, Connick WB, Crane BR, Di B, Angel J, Schaefer WP, Rees DC, Gray HB (1999) Acta Cryst D 55:379–385

    Article  CAS  Google Scholar 

  36. Edelhoch H (1967) Biochemistry 6:1948–1954

    Article  CAS  PubMed  Google Scholar 

  37. Regan JJ, Di Bilio AJ , Langen R, Skov LK, Winkler JR, Gray HB, Onuchic JN (1995) Chem Biol 2:489–496

    Article  CAS  PubMed  Google Scholar 

  38. Langen R, Chang I-J, Germanas JP, Richards JH, Winkler JR, Gray HB (1995) Science 268:1733–1735

    Article  CAS  PubMed  Google Scholar 

  39. Langen R (1995) Ph.D. Dissertation “Electron transfer in proteins: theory and experiment” California Institute of Technology

  40. Winkler JR, Gray HB (2014) Chem Rev 114:3369–3380

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. Winkler JR, Gray HB (2003) Q Rev Biophys 36:341–372

    Article  PubMed  Google Scholar 

  42. Shih C, Museth AK, Abrahamsson M, Blanco-Rodriguez AM, Di Bilio AJ, Sudhamsu J, Crane BR, Ronayne KL, Towrie M, Vlček A Jr, Richards JH, Winkler JR, Gray HB (2008) Science 320:1760–1762

    Article  CAS  PubMed  Google Scholar 

  43. Di Bilio AJ, Hill MG, Bonander N, Karlsson BG, Villahermosa RM, Malmström BG, Winkler JR, Gray HB (1997) J Am Chem Soc 119:9921–9922

    Article  Google Scholar 

  44. Warren JJ, Ener ME, Vlcek A Jr, Winkler JR, Gray HB (2012) Coord Chem Rev 256:2478–2487

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Meyer TJ, Taube H (1968) Inorg Chem 7:2369–2379

    Article  CAS  Google Scholar 

  46. Dempsey JL, Winkler JR, Gray HB (2009) J Am Chem Soc 132:1060–1065

    Article  Google Scholar 

Download references

Acknowledgments

Research reported in this publication was supported by The National Institute of Diabetes and Digestive and Kidney Diseases of the National Institutes of Health under Award Number R01DK019038 to HBG and JRW. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Additional support was provided by the Arnold and Mabel Beckman Foundation.

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Author notes

  1. Jeffrey J. Warren

    Present address: Department of Chemistry, Simon Fraser University, 8888 University Drive, Burnaby, BC, V5A 1S6, Canada

Authors and Affiliations

  1. Beckman Institute, California Institute of Technology, Pasadena, CA, 91125, USA

    Jeffrey J. Warren, Oliver S. Shafaat, Jay R. Winkler & Harry B. Gray

Authors
  1. Jeffrey J. Warren
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  2. Oliver S. Shafaat
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  3. Jay R. Winkler
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  4. Harry B. Gray
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Corresponding author

Correspondence to Harry B. Gray.

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Dedicated to the memory of Robert J. P. (Bob) Williams.

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Warren, J.J., Shafaat, O.S., Winkler, J.R. et al. Proton-coupled electron hopping in Ru-modified P. aeruginosa azurin. J Biol Inorg Chem 21, 113–119 (2016). https://doi.org/10.1007/s00775-016-1332-4

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  • DOI: https://doi.org/10.1007/s00775-016-1332-4

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