Walking the seven lines: binuclear copper A in cytochrome c oxidase and nitrous oxide reductase

Minireview
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Part of the following topical collections:
  1. Special issue to celebrate the 80th birthday of Helmut Sigel

Abstract

The enzymes nitrous oxide reductase (N2OR) and cytochrome c oxidase (COX) are constituents of important biological processes. N2OR is the terminal reductase in a respiratory chain converting N2O to N2 in denitrifying bacteria; COX is the terminal oxidase of the aerobic respiratory chain of certain bacteria and eukaryotic organisms transforming O2 to H2O accompanied by proton pumping. Different spectroscopies including magnetic resonance techniques, were applied to show that N2OR has a mixed-valent Cys-bridged [Cu1.5+(CyS)2Cu1.5+] copper site, and that such a binuclear center, called CuA, does also exist in COX. A sequence motif shared between the CuA center of N2OR and the subunit II of COX raises the issue of a putative evolutionary relationship of the two enzymes. The suggestion of a binuclear CuA in COX, with one unpaired electron delocalized between two equivalent Cu nuclei, was difficult to accept originally, even though regarded as a clever solution to many experimental observations. This minireview in honor of Helmut Sigel traces several of the critical steps forward in understanding the nature of CuA in N2OR and COX, and discusses its unique electronic features to some extent including the contributions made by the development of methodology and the discovery of a novel multi-copper enzyme.

Graphical Abstract

Left: X-band (9.130 GHz) and C-band (4.530 GHz, 1st harmonic display of experimental spectrum) EPR spectra of bovine heart cytochrome c oxidase, recorded at 20K. Right: Ribbon presentation of the CuA domain in cytochrome c oxidase and nitrous oxide reductase.

Keywords

Binuclear center Copper–copper bond Cytochrome c oxidase Electron transfer Mixed valence Nitrous oxide reductase 
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Notes

Acknowledgements

My sincere thanks go to Jim Hyde and his crew for the exciting time at the National Biomedical EPR Center in Milwaukee, and to all my students, co-workers and collaborators, named in the cited references, for all their valuable contributions. Work in the laboratory was supported by the Deutsche Forschungsgemeinschaft, the National Science Foundation, the Volkswagen-Stiftung, the German–Israel Foundation, and the University of Konstanz.

References

  1. 1.
  2. 2.
    Sigel H, Brintzinger H (1963) Helv Chim Acta 46:701–712Google Scholar
  3. 3.
    Sigel H, Brintzinger HH, Erlenmeyer H (1963) Helv Chim Acta 46:712–719Google Scholar
  4. 4.
    Sigel H, Brintzinger HH (1964) Helv Chim Acta 47:1701–1717.  https://doi.org/10.1002/hlca.19640470706 CrossRefGoogle Scholar
  5. 5.
    McCormick DB, Griesser R, Sigel H (1974) Met Ions Biol Syst 1:213–247Google Scholar
  6. 6.
    Sands RH, Beinert H (1959) Biochem Biophys Commun 1:175–178.  https://doi.org/10.1016/0006-291X(59)90013-0 CrossRefGoogle Scholar
  7. 7.
    Beinert H, Griffiths DE, Wharton DC, Sands RH (1962) J Biol Chem 237:2337–2346PubMedGoogle Scholar
  8. 8.
    Peisach J, Blumberg WE (1974) Arch Biochem Biophys 165:691–708PubMedCrossRefGoogle Scholar
  9. 9.
    Vänngård T (1972) In: Swartz HM, Bolton JR, Borg DC (eds) Copper proteins. Wiley, New York, pp 411–447Google Scholar
  10. 10.
    Stevens TH, Martin CT, Wang H, Brudvig GW, Scholes CP, Chan SI (1982) J Biol Chem 257:12106–12113PubMedGoogle Scholar
  11. 11.
    Chan SI, Li PM (1990) Biochemistry 29:1–12PubMedCrossRefGoogle Scholar
  12. 12.
    Gurbiel RJ, Fann Y-C, Surerus KK, Werst MM, Musser SM, Doan PE, Chan SI, Fee JA, Hoffman BM (1993) J Am Chem Soc 115:10888–10894CrossRefGoogle Scholar
  13. 13.
    Mims WB, Peisach J, Shaw RW, Beinert H (1980) J Biol Chem 255:6843–6846PubMedGoogle Scholar
  14. 14.
    Brudvig GW, Blair DF, Chan SI (1984) J Biol Chem 259:11001–11009PubMedGoogle Scholar
  15. 15.
    Beinert H (1995) Chem Biol 2:781–785PubMedCrossRefGoogle Scholar
  16. 16.
    Beinert H (1997) Eur J Biochem 245:521–532PubMedCrossRefGoogle Scholar
  17. 17.
    Zumft WG, Kroneck PMH (2006) Adv Microb Physiol 52(107–22):7.  https://doi.org/10.1016/S0065-2911(06)52003-X Google Scholar
  18. 18.
    Liu J, Chakraborty S, Hosseinzadeh P, Yu Y, Tian S, Petrik I, Bhagi A, Lu Y (2014) Chem Rev 114:4366–4469PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Solomon EI, Heppner DE, Johnston EM, Ginsbach JW, Cirera J, Qayyum M, Kieber-Emmons MT, Kjaergaard CH, Hadt RG, Tian L (2014) Chem Rev 114:3659–3853.  https://doi.org/10.1021/cr400327t PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
  21. 21.
    Valentine J, O’Halloran TV (1999) Curr Opin Chem Biol 3:129–130PubMedCrossRefGoogle Scholar
  22. 22.
    Holm RH, Solomon EI (2004) Chem Rev 104:347–348PubMedCrossRefGoogle Scholar
  23. 23.
    Hemmerich P, Veeger C, Wood HCS (1965) Angew Chem Int Ed 4:671–687CrossRefGoogle Scholar
  24. 24.
    Beinert H, Massey V (1982) Trends Biochem Sci 7:43–44.  https://doi.org/10.1016/0968-0004(82)90069-X CrossRefGoogle Scholar
  25. 25.
    Hemmerich P (1966) In: Peisach J, Aisen P, Blumberg WE (eds) The biochemistry of copper. Academic Press, New York, pp 15–34Google Scholar
  26. 26.
    Hemmerich P, Beinert H, Vänngård T (1966) Angew Chem Int Ed 5:422–423CrossRefGoogle Scholar
  27. 27.
    Hemmerich P, Sigwart C (1963) Experientia 19:488–489CrossRefGoogle Scholar
  28. 28.
    Sigwart C, Hemmerich P, Spence JT (1968) Inorg Chem 7:2545–2548.  https://doi.org/10.1021/ic50070a015 CrossRefGoogle Scholar
  29. 29.
    Sigwart C, Kroneck PMH, Hemmerich P (1970) Helv Chim Acta 53:177–185.  https://doi.org/10.1002/hlca.19700530125 CrossRefGoogle Scholar
  30. 30.
    Kroneck PMH, Naumann C, Hemmerich P (1971) Inorg Nucl Chem Lett 7:659–666.  https://doi.org/10.1016/0020-1650(71)80052-1 CrossRefGoogle Scholar
  31. 31.
    Kroneck PMH (1975) J Am Chem Soc 97:3839–3841.  https://doi.org/10.1021/ja00846a059 PubMedCrossRefGoogle Scholar
  32. 32.
    Vortisch V, Kroneck PMH, Hemmerich P (1976) J Am Chem Soc 98:2821–2826.  https://doi.org/10.1021/ja00426a025 CrossRefGoogle Scholar
  33. 33.
    Itoh S, Nagagawa M, Fukuzumi S (2001) J Am Chem Soc 123:4087–4088PubMedCrossRefGoogle Scholar
  34. 34.
    Neuba A, Haase R, Meyer-Klaucke W, Flörke U, Henkel G (2012) Angew Chem Int Ed 51:1714–1718CrossRefGoogle Scholar
  35. 35.
    Thomas AM, Lin B-L, Wasinger EC, Stack TDP (2013) J Am Chem Soc 135:18912–18919PubMedCrossRefGoogle Scholar
  36. 36.
    Ording-Wenker ECM, van der Plas M, Siegler MA, Bonnet S, Bickelhaupt FM, Fonseca Guerra C, Bouwman E (2014) Inorg Chem 53:8494–8504.  https://doi.org/10.1021/ic501060w PubMedCrossRefGoogle Scholar
  37. 37.
    Birker PJML, Freeman HC (1976) J Chem Soc Chem Commun 9:312–313.  https://doi.org/10.1039/C39760000312 CrossRefGoogle Scholar
  38. 38.
    Houser RP, Young VG, Tolman WB (1995) J Am Chem Soc 117:10745–10746.  https://doi.org/10.1021/ja00148a018 CrossRefGoogle Scholar
  39. 39.
    Houser RP, Young VG, Tolman WB (1996) J Am Chem Soc 118:2101–2102.  https://doi.org/10.1021/ja953776m CrossRefGoogle Scholar
  40. 40.
  41. 41.
    Person P, Wainio WW, Eichels B (1953) J Biol Chem 202:369–381PubMedGoogle Scholar
  42. 42.
    Elvehjem CA (1931) J Biol Chem 90:111–132Google Scholar
  43. 43.
    Cohen E, Elvehjem CA (1934) J Biol Chem 107:97–105Google Scholar
  44. 44.
    Keilin D, Hartree EF (1939) Proc R Soc (Lond.) B127:167–191CrossRefGoogle Scholar
  45. 45.
    Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Nature 37:660–669CrossRefGoogle Scholar
  46. 46.
    Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S (1995) Science 269:1069–1074PubMedCrossRefGoogle Scholar
  47. 47.
    Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa R (1996) Science 272:1136–1144PubMedCrossRefGoogle Scholar
  48. 48.
    Williams PA, Blackburn NJ, Sanders D, Bellamy H, Stura EA, Fee JA, McRee DE (1999) Nat Struct Biol 6:509–516PubMedCrossRefGoogle Scholar
  49. 49.
    Soulimane T, Buse G, Bourenkov GP, Bartunik H, Huber R, Than ME (2000) EMBO J 19:1766–1777PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
  51. 51.
    Beinert H (1991) J Inorg Biochem 44:173–218.  https://doi.org/10.1016/0162-0134(91)80054-L PubMedCrossRefGoogle Scholar
  52. 52.
    Beinert H (1996) J Inorg Biochem 64:79–100.  https://doi.org/10.1016/0162-0134(96)00083-9 PubMedCrossRefGoogle Scholar
  53. 53.
    Karlin KD, Tyeklár Z (1993) Bioinorganic chemistry of copper. Chapman & Hall, New YorkCrossRefGoogle Scholar
  54. 54.
    Greenwood C, Hill BC, Barber D, Eglinton DG, Thomson AJ (1983) Biochem J 215:303–316PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Thomson AJ, Greenwood C, Peterson J, Barrett CP (1986) J Inorg Biochem 28:195–205PubMedCrossRefGoogle Scholar
  56. 56.
    Greenwood C, Thomson AJ, Barrett CP, Peterson J, George GN, Fee JA, Reichardt J (1988) Ann N Y Acad Sci 550:47–52PubMedCrossRefGoogle Scholar
  57. 57.
    Pan LP, Li Z, Larsen R, Chan SI (1991) J Biol Chem 266:1367–1370PubMedGoogle Scholar
  58. 58.
    Steffens GCM, Soulimane T, Wolff G, Buse G (1993) Eur J Biochem 213:1149–1157PubMedCrossRefGoogle Scholar
  59. 59.
    Adman ET (1991) Adv Protein Chem 42:145–197PubMedCrossRefGoogle Scholar
  60. 60.
    Dennison C, Canters GW (1996) Recl Trav Chim Pays Bas 115:345–351CrossRefGoogle Scholar
  61. 61.
    Vila AJ, Fernandez CO (2001) Copper in electron transfer proteins. In: Bertini I, Sigel A, Sigel H (eds) Handbook on metalloproteins. Marcel Dekker, New York, pp 813–856Google Scholar
  62. 62.
    Lu Y (2003) Cupredoxins. In: Que L, Tolman WB (eds) Biocoordination chemistry. Comprehensive coordination chemistry II: from biology to nanotechnology, vol 8. Elsevier, Oxford, pp 1–32Google Scholar
  63. 63.
    Dennison C, Vijgenboom E, de Vries S, van der Oost J, Canters GW (1995) FEBS Lett 365:92–94PubMedCrossRefGoogle Scholar
  64. 64.
    Hay M, Richards JH, Lu Y (1996) Proc Natl Acad Sci USA 93:461–464PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Robinson H, Ang MC, Gao Y-G, Hay MT, Lu Y, Wang AH-J (1999) Biochemistry 38:5677–5683PubMedCrossRefGoogle Scholar
  66. 66.
    Viebrock A, Zumft WG (1988) J Bacteriol 170:4658–4668PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Zumft WG (1992) The denitrifying prokaryotes. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) The prokaryotes. A handbook on the biology of bacteria: ecophysiology, isolation, identification, applications, vol 1. Springer, New York, pp 554–582Google Scholar
  68. 68.
    Saraste M, Castresana J (1994) FEBS Lett 341:1–4PubMedCrossRefGoogle Scholar
  69. 69.
    van der Oost J, de Boer APN, de Gier JWL, Zumft WG, Stouthamer AH, van Spanning RJM (1994) FEMS Microbiol Lett 121:1–10PubMedCrossRefGoogle Scholar
  70. 70.
    Zumft WG, Matsubara T (1982) FEBS Lett 148:102–107CrossRefGoogle Scholar
  71. 71.
    Zumft WG, Coyle CL, Frunzke K (1985) FEBS Lett 183:240–244CrossRefGoogle Scholar
  72. 72.
    Pomowski A, Zumft WG, Kroneck PMH, Einsle O (2011) Nature 477:234–238.  https://doi.org/10.1038/nature10332 PubMedCrossRefGoogle Scholar
  73. 73.
    Wüst A, Schneider L, Pomowski A, Zumft WG, Kroneck PMH, Einsle O (2012) Biol Chem 393:1067–1077.  https://doi.org/10.1515/hsz-2012-01771 PubMedCrossRefGoogle Scholar
  74. 74.
    Brown K, Tegoni M, Prudêncio M, Pereira AS, Besson S, Moura JJG, Moura I, Cambillau C (2000) Nat Struct Biol 7:191–195PubMedCrossRefGoogle Scholar
  75. 75.
    Rasmussen T, Berks BC, Sanders-Loehr J, Dooley DM, Zumft WG, Thomson AJ (2000) Biochemistry 39:12753–12756PubMedCrossRefGoogle Scholar
  76. 76.
    Brown K, Djinovic-Carugo K, Haltia T, Cabrito I, Saraste M, Moura JJG, Moura I, Tegoni M, Cambillau C (2000) J Biol Chem 275:41133–41136PubMedCrossRefGoogle Scholar
  77. 77.
    Rasmussen T, Berks BC, Butt JN, Thomson AJ (2002) Biochem J 364:807–815PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Haltia T, Brown K, Tegoni M, Cambillau C, Saraste M, Mattila K, Djinovic-Carugo K (2003) Biochem J 369:77–88PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Oganesyan VS, Rasmussen T, Fairhurst S, Thomson AJ (2004) Dalton Trans 7:996–1002CrossRefGoogle Scholar
  80. 80.
    Coyle CL, Zumft WG, Kroneck PMH, Körner H, Jakob W (1985) Eur J Biochem 153:459–467.  https://doi.org/10.1111/j.1432-1033.1985.tb09324.x PubMedCrossRefGoogle Scholar
  81. 81.
    Riester J, Zumft WG, Kroneck PMH (1989) Eur J Biochem 178:751–762.  https://doi.org/10.1111/j.1432-1033.1989.tb14506.x PubMedCrossRefGoogle Scholar
  82. 82.
    Hagen WR (2006) Dalton Trans 37:4415–4434.  https://doi.org/10.1039/B608163K CrossRefGoogle Scholar
  83. 83.
    Solomon EI, Lowery MD (1993) Science 259:1575–1581PubMedCrossRefGoogle Scholar
  84. 84.
    Froncisz W, Scholes CP, Hyde JS, Wei Y-H, King TE, Shaw RW, Beinert H (1979) J Biol Chem 254:7482–7484PubMedGoogle Scholar
  85. 85.
    Malkin R, Malmström BG (1970) Adv Enzymol 33:177–244PubMedGoogle Scholar
  86. 86.
    Froncisz W, Hyde JS (1980) J Chem Phys 73:3123–3131CrossRefGoogle Scholar
  87. 87.
    Froncisz W, Hyde JS (1982) J Magn Reson 47:515–521Google Scholar
  88. 88.
    Kroneck PMH, Antholine WE, Riester J, Zumft WG (1988) FEBS Lett 242:70–74PubMedCrossRefGoogle Scholar
  89. 89.
    Westmoreland TD, Wilcox DE, Baldwin MJ, Mims WB, Solomon EI (1989) J Am Chem Soc 111:6106–6123CrossRefGoogle Scholar
  90. 90.
    Mims WB (1976) The linear electric field effect in paramagnetic resonance. Clarendon Press, OxfordGoogle Scholar
  91. 91.
    Gerstman BS, Brill AS (1988) Phys Rev A 37:2151–2164CrossRefGoogle Scholar
  92. 92.
    Neese F (1997) Electronic structure and spectroscopy of novel copper chromophores in biology. Ph.D. Dissertation, University of Konstanz, GermanyGoogle Scholar
  93. 93.
    Kroneck PMH, Antholine WE, Kastrau DHW, Buse G, Steffens GCM, Zumft WG (1990) FEBS Lett 268:274–276.  https://doi.org/10.1016/0014-5793(90)81026-K PubMedCrossRefGoogle Scholar
  94. 94.
    Antholine WE, Kastrau DHW, Steffens GCM, Buse G, Zumft WG, Kroneck PMH (1992) Eur J Biochem 209:875–881.  https://doi.org/10.1111/j.1432-1033.1992.tb17360.x PubMedCrossRefGoogle Scholar
  95. 95.
    Hay MT, Lu Y (2000) J Biol Inorg Chem 5:699–712PubMedCrossRefGoogle Scholar
  96. 96.
    Savelieff MG, Wilson TD, Elias Y, Nilges MJ, Garner DK, Lu Y (2008) Proc Natl Acad Sci (USA) 105:7919–7924CrossRefGoogle Scholar
  97. 97.
    Savelieff M, Lu Y (2010) J Biol Inorg Chem 15:461–483PubMedCrossRefGoogle Scholar
  98. 98.
    Lukoyanov D, Berry SM, Lu Y, Antholine WE, Scholes CP (2002) Biophys J 82:2758–2766PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Zickermann V, Verkhovsky M, Morgan J, Wikström M, Anemüller S, Bill E, Steffens GCM, Ludwig B (1995) Eur J Biochem 234:686–693PubMedCrossRefGoogle Scholar
  100. 100.
    Li PM, Malmström BG, Chan SI (1989) FEBS Lett 248:210–211PubMedCrossRefGoogle Scholar
  101. 101.
    Kroneck PMH, Antholine WE, Riester J, Zumft WG (1989) FEBS Lett 248:212–213PubMedCrossRefGoogle Scholar
  102. 102.
    Malmström BG (1990) Arch Biochem Biophys 280:233–241PubMedCrossRefGoogle Scholar
  103. 103.
    Yoshikawa S, Shimada A, Shinzawa-Itoh K (2015) Met Ions Life Sci 15:89–130PubMedGoogle Scholar
  104. 104.
    Wilmanns M, Lappalainen P, Kelly M, Sauer-Eriksson E, Saraste M (1995) Proc Natl Acad Sci USA 92:11955–11959PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Sinnecker S, Neese F (2007) Top Curr Chem 268:47–83.  https://doi.org/10.1007/128_2006_081 CrossRefGoogle Scholar
  106. 106.
    Neese F, Zumft WG, Antholine WE, Kroneck PMH (1996) J Am Chem Soc 118:8692–8699CrossRefGoogle Scholar
  107. 107.
    Farrar JA, Neese F, Lappalainen P, Kroneck PMH, Saraste M, Zumft WG, Thomson AJ (1996) J Am Chem Soc 118:11501–11514CrossRefGoogle Scholar
  108. 108.
    Neese F, Kappl R, Hüttermann J, Zumft WG, Kroneck PMH (1998) J Biol Inorg Chem 3:53–67Google Scholar
  109. 109.
    Gamelin DR, Randall DW, Hay MT, Houser RP, Mulder TC, Canters GW, de Vries S, Tolman WB, Lu Y, Solomon EI (1998) J Am Chem Soc 120:5246–5526CrossRefGoogle Scholar
  110. 110.
    Randall GW, Gamelin DR, LaCroix LB, Solomon EI (2000) J Biol Inorg Chem 5:16–19PubMedGoogle Scholar
  111. 111.
    DeBeer George S, Metz M, Szilagyi RK, Wang H, Cramer SP, Lu Y, Tolman WB, Hedman B, Hodgson KO, Solomon EI (2001) J Am Chem Soc 123:5757–5767CrossRefGoogle Scholar
  112. 112.
    Olsson MHM, Ryde U (2001) J Am Chem Soc 123:7866–7876PubMedCrossRefGoogle Scholar
  113. 113.
    Mchaourab HS, Pfenninger S, Antholine WE, Felix CC, Hyde JS, Kroneck PMH (1993) Biophys J 64:1576–1579PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Pfenninger S, Antholine WE, Barr ME, Hyde JS, Kroneck PMH, Zumft WG (1995) Biophys J 69:2761–2769PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Bertini I, Bren KL, Clemente A, Fee JA, Gray HB, Luchinat C, Malmström BG, Richards JH, Sanders D, Slutter CE (1996) J Am Chem Soc 118:11658–11659CrossRefGoogle Scholar
  116. 116.
    Luchinat C, Soriano A, Djinovic-Carugo K, Saraste M, Malmström BG, Bertini I (1997) J Am Chem Soc 119:11023–11027CrossRefGoogle Scholar
  117. 117.
    Salgado J, Warmerdam G, Bubacco L, Canters GW (1998) Biochemistry 19:7378–7389CrossRefGoogle Scholar
  118. 118.
    Abriata LA, Ledesma GN, Pierattelli R, Vila AJ (2009) J Am Chem Soc 131:1939–1946PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Zaballa M-E, Luciano LA, Donaire A, Vila AJ (2012) Proc Natl Acad Sci USA 109:9254–9259PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Alvarez-Paggi D, Zitare UA, Szuster J, Morgada MN, Leguto AJ, Vila AJ, Murgida DH (2017) J Am Chem Soc 139:9803–9806PubMedCrossRefGoogle Scholar
  121. 121.
    Holz RC, Alvarez ML, Zumft WG, Dooley DM (1999) Biochemistry 38:11164–11171PubMedCrossRefGoogle Scholar
  122. 122.
    Blackburn NJ, de Vries S, Barr ME, Houser RP, Tolman WB, Sanders D, Fee JA (1997) J Am Chem Soc 119:6135–6143CrossRefGoogle Scholar
  123. 123.
    Larsson S, Källebring B, Wittung P, Malmström BG (1995) Proc Natl Acad Sci USA 92:7167–7171PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Ramirez BE, Malmström BG, Winkler JR, Gray HB (1995) Proc Natl Acad Sci USA 92:11949–11951PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Henkel G, Müller A, Weissgräber S, Buse G, Soulimane T, Steffens GCM, Nolting H-F (1995) Angew Chem Int Ed 34:1488–1492CrossRefGoogle Scholar
  126. 126.
    Toftlund H, Becher J, Olesen PH, Pedersen JZ (1985) Isr J Chem 25:56–65CrossRefGoogle Scholar
  127. 127.
    Harding C, McKee V, Nelson J (1991) J Am Chem Soc 113:9684–9685.  https://doi.org/10.1021/ja00025a050 CrossRefGoogle Scholar
  128. 128.
    Farrar JA, McKee V, Al-Obaidi AHR, McGarvey JJ, Nelson J, Thomson AJ (1995) Inorg Chem 34:1302–1303CrossRefGoogle Scholar
  129. 129.
    Kababya S, Nelson J, Calle C, Neese F, Goldfarb D (2006) J Am Chem Soc 128:2017–2029.  https://doi.org/10.1021/ja056207f PubMedCrossRefGoogle Scholar
  130. 130.
    LeCloux DD, Davydov R, Lippard SJ (1998) Inorg Chem 37:6814–6826PubMedCrossRefGoogle Scholar
  131. 131.
    He C, Lippard SJ (2000) Inorg Chem 39:5225–5231PubMedCrossRefGoogle Scholar
  132. 132.
    Gupta R, Zhang ZH, Powell D, Hendrich MP, Borovik AS (2002) Inorg Chem 41:5100–5106PubMedCrossRefGoogle Scholar
  133. 133.
    Harkins SB, Peters JC (2004) J Am Chem Soc 126:2885–2893PubMedCrossRefGoogle Scholar
  134. 134.
    Witte M, Grimm-Lebsanft B, Goos A, Binder S, Rübhausen M, Bernard M, Neuba A, Gorelsky S, Gerstmann U, Henkel G, Schmidt WG, Herres-Pawlis S (2016) J Comp Chem 37:2181–2192.  https://doi.org/10.1002/jcc.24439 CrossRefGoogle Scholar
  135. 135.
    Zumft WG (1997) Microbiol Mol Biol Rev 61:533–616PubMedPubMedCentralGoogle Scholar
  136. 136.
    Schneider LK, Wüst A, Pomowski A, Zhang L, Einsle O (2014) Met Ions Life Sci 14:177–210PubMedCrossRefGoogle Scholar
  137. 137.
    Michel H (1998) Proc Natl Acad Sci USA 95:12819–12824PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    Belevich I, Verkhovsky MI, Wikström M (2006) Nature 440:829–832PubMedCrossRefGoogle Scholar
  139. 139.
    Yoshikawa S, Muramoto K, Shinzawa-Itoh K (2011) Annu Rev Biophys 40:205–223PubMedCrossRefGoogle Scholar
  140. 140.
    Wilson MT, Lalla-Maharajh W, Darley-Usmar V, Bonaventura J, Bonaventura C, Brunori M (1980) J Biol Chem 255:2722–2728PubMedGoogle Scholar
  141. 141.
    Kornberg A (2000) J Bacteriol 182:3613–3618PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Lu Y (2006) Angew Chem Int Ed 45:5588–5601CrossRefGoogle Scholar
  143. 143.
    Tolman WB, Carrier SM, Ruggiero CE, Antholine WE, Whittacker J (1993) In: Karlin KD, Tyeklár Z (eds) Bioinorganic chemistry of copper. Chapman & Hall, New York, pp 406–418CrossRefGoogle Scholar
  144. 144.
    Tolman WB (2010) Angew Chem Int Ed 49:1018–1024CrossRefGoogle Scholar
  145. 145.
    Farver O, Lu Y, Ang MC, Pecht I (1999) Proc Natl Acad Sci USA 96:899–902PubMedPubMedCentralCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of BiologyUniversity of KonstanzKonstanzGermany

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