Unique Spectroscopic Features and Electronic Structures of Copper Proteins: Relation to Reactivity

  • Jungjoo Yoon
  • Edward I. Solomon
Part of the Biological Magnetic Resonance book series (BIMR, volume 28)

Copper active sites play a major role in a wide range of biological processes. These include long-range electron transfer, binding, activation, and two-/four-electron reduction of dioxygen, and two-electron reduction of nitrous oxide. Traditionally, copper sites have been classified into three types based on their EPR features: the type 1 “blue,” the type 2 “normal,” and the type 3 “coupled binuclear” sites. However, more recent discoveries of the mixed-valent binuclear CuA, the trinuclear Cu cluster in the multicopper oxidases, and the tetranuclear CuZ sites show that biological copper centers are even more diverse than previously believed. In this review, EPR and other spectral features of the different copper active sites are developed and compared. The origins of the unique spectroscopic features are discussed with respect to the novel geometric and electronic structures that are intimately coupled to their catalytic functions. High covalency is shown to activate specific pathways for long-range electron transfer and exchange interactions between copper centers to control the two vs. one electron activation of O2 for different chemistries and the four-electron reduction of O2 to H2O. In addition, electron delocalization between mixed-valent copper centers can lower reorganization energy and activate copper clusters for catalysis.


Lower Unoccupied Molecular Orbitral Magnetic Circular Dichroism Copper Protein Multicopper Oxidase Nitrous Oxide Reductase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Solomon EI, Sundaram UM, Machonkin TE. 1996. Multicopper oxidases and oxygenases. Chem Rev 96:2563–2605.PubMedCrossRefGoogle Scholar
  2. 2.
    Malmstrom BG. 1994. Rack-induced bonding in blue copper proteins. Eur J Biochem 223:711–718.PubMedCrossRefGoogle Scholar
  3. 3.
    Vallee BL, Williams RJP. 1968. Metalloenzymes: the entatic nature of their active sites. Proc Nat Acad Sci USA 59:498–505.PubMedCrossRefGoogle Scholar
  4. 4.
    Solomon EI, Hanson MA. 1999. Bioinorganic spectroscopy. In Inorganic electronic structure and spectroscopy, pp. 1–129. Ed EI Solomon and ABP Lever. New York: John Wiley & Sons.Google Scholar
  5. 5.
    Solomon EI. 1984. Inorganic spectroscopy: an overview. Comments Inorg Chem 3:225–320.Google Scholar
  6. 6.
    Malkin R, Malmstrom BG. 1970. State and function of copper in biological systems. Adv Enzymol 33:177–244.PubMedGoogle Scholar
  7. 7.
    Holm RH, Kennepohl P, Solomon EI. 1996. Structural and functional aspects of metal sites in biology. Chem Rev 96:2239–2314.PubMedCrossRefGoogle Scholar
  8. 8.
    Lieberman RA, Sands RH, Fee JA. 1982. A study of the electron paramagnetic resonance properties of single monoclinic crystals of bovine superoxide dismutase. J Biol Chem 257:336–344.PubMedGoogle Scholar
  9. 9.
    Valentine JS, Pantoliano MW, McDonnell PJ, Burger AR, Lippard SJ. 1979. pHdependent migration of copper(II) to the vacant zinc-binding site of zinc-free bovine erythrocyte superoxide-dismutase. Proc Nat Acad Sci USA 76:4245–4249.PubMedCrossRefGoogle Scholar
  10. 10.
    Tocheva EI, Rosell FI, Mauk AG, Murphy MEP. 2004. Side-on copper-nitrosyl coordination by nitrite reductase. Science 304:867–870.PubMedCrossRefGoogle Scholar
  11. 11.
    Matsuzaki R, Fukui T, Sato H, Ozaki Y, Tanizawa K. 1994. Generation of the topa quinone cofactor in bacterial monoamine oxidase by cupric ion-dependent autooxidation of a specific tyrosyl residue. FEBS Lett 351:360–364.PubMedCrossRefGoogle Scholar
  12. 12.
    Dove JE, Schwartz B, Williams NK, Klinman JP. 2000. Investigation of spectroscopic intermediates during copper-binding and tpq formation in wild-type and active site mutants of a copper containing amine oxidase from yeast. Biochemistry 39:3690–3698.PubMedCrossRefGoogle Scholar
  13. 13.
    Whittaker JW. 2003. Free radical catalysis by galactose oxidase. Chem Rev 103:2347–2363.PubMedCrossRefGoogle Scholar
  14. 14.
    Klinman JP. 1996. Mechanisms whereby mononuclear copper proteins functionalize organic substrates. Chem Rev 96:2541–2561.PubMedCrossRefGoogle Scholar
  15. 15.
    Branchaud BP, Montaguesmith MP, Kosman DJ, McLaren FR. 1993. Mechanismbased inactivation of galactose oxidase: evidence for a radical mechanism. J Am Chem Soc 115:798–800.CrossRefGoogle Scholar
  16. 16.
    Solomon EI, Szilagyi RK, George SD, Basumallick L. 2004. Electronic structures of metal sites in proteins and models: contributions to function in blue copper proteins. Chem Rev 104:419–458.PubMedCrossRefGoogle Scholar
  17. 17.
    Solomon EI, Baldwin MJ, Lowery MD. 1992. Electronic structures of active sites in copper proteins: contributions to reactivity. Chem Rev 92:521–542.CrossRefGoogle Scholar
  18. 18.
    Chen P, Solomon EI. 2004. O2 activation by binuclear Cu sites: noncoupled versus exchange coupled reaction mechanisms. Proc Nat Acad Sci USA 101:13105–13110.PubMedCrossRefGoogle Scholar
  19. 19.
    Prigge ST, Kolhekar AS, Eipper BA, Mains RE, Amzel LM. 1997. Amidation of bioactive peptides: the structure of peptidylglycine α-hydroxylating monooxygenase. Science 278:1300–1305.PubMedCrossRefGoogle Scholar
  20. 20.
    Prigge ST, Kolhekar AS, Eipper BA, Mains RE, Amzel LM. 1999. Substrate-mediated electron transfer in peptidylglycine α-hydroxylating monooxygenase. Nat Struct Biol 6:976–983.PubMedCrossRefGoogle Scholar
  21. 21.
    Chen P, Solomon EI. 2004. Oxygen activation by the noncoupled binuclear copper site in peptidylglycine α-hydroxylating monooxygenase: reaction mechanism and role of the noncoupled nature of the active site. J Am Chem Soc 126:4991–5000.PubMedCrossRefGoogle Scholar
  22. 22.
    Lee SK, George SD, Antholine WE, Hedman B, Hodgson KO, Solomon EI. 2002. Nature of the intermediate formed in the reduction of O2 to H2O at the trinuclear copper cluster active site in native laccase. J Am Chem Soc 124:6180–6193.PubMedCrossRefGoogle Scholar
  23. 23.
    Iwata S, Ostermeier C, Ludwig B, Michel H. 1995. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376:660–669.PubMedCrossRefGoogle Scholar
  24. 24.
    Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawaitoh K, Nakashima R, Yaono R, Yoshikawa S. 1995. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å. Science 269:1069–1074.PubMedCrossRefGoogle Scholar
  25. 25.
    Brown K, Djinovic-Carugo K, Haltia T, Cabrito I, Saraste M, Moura JJG, Moura I, Tegoni M, Cambillau C. 2000. Revisiting the catalytic Cuz cluster of nitrous oxide (N2O) reductase: evidence of a bridging inorganic sulfur. J Biol Chem 275:41133–41136.PubMedCrossRefGoogle Scholar
  26. 26.
    Brown K, Tegoni M, Prudencio M, Pereira AS, Besson S, Moura JJ, Moura I, Cambillau C. 2000. A novel type of catalytic copper cluster in nitrous oxide reductase. Nat Struct Biol 7:191–195.PubMedCrossRefGoogle Scholar
  27. 27.
    Yoshikawa S, Shinzawa-Itoh K, Nakashima R, Yaono R, Yamashita E, Inoue N, Yao M, Fei MJ, Libeu CP, Mizushima T, Yamaguchi H, Tomizaki T, Tsukihara T. 1998. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280:1723–1729.PubMedCrossRefGoogle Scholar
  28. 28.
    Robin MB, Day P. 1967. Mixed valence chemistry: a survey and classification. Adv Inorg Chem Radiochem 10:247–423.CrossRefGoogle Scholar
  29. 29.
    Zumft WG. 1997. Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616.PubMedGoogle Scholar
  30. 30.
    Chen P, Gorelsky SI, Ghosh S, Solomon EI. 2004. N2O reduction by the μ4-sulfidebridged tetranuclear Cuz cluster active site. Angew Chem, Int Ed 43:4132–4140.CrossRefGoogle Scholar
  31. 31.
    Chen P, George SD, Cabrito I, Antholine WE, Moura JJG, Moura I, Hedman B, Hodgson KO, Solomon EI. 2002. Electronic structure description of the μ4-sulfide bridged tetranuclear Cuz center in N2O reductase. J Am Chem Soc 124:744–745.PubMedCrossRefGoogle Scholar
  32. 32.
    Chen P, Cabrito I, Moura JJG, Moura I, Solomon EI. 2002. Spectroscopic and electronic structure studies of the μ4-sulfide bridged tetranuclear Cuz cluster in N2O reductase: molecular insight into the catalytic mechanism. J Am Chem Soc 124:10497–10507.PubMedCrossRefGoogle Scholar
  33. 33.
    Blumberg WE, Peisach J. 1966. Optical and magnetic properties of copper in chenopodium album plastocyanin. Biochim Biophys Acta 126:269–273.PubMedCrossRefGoogle Scholar
  34. 34.
    Dodd FE, Abraham ZHL, Eady RR, Hasnain SS. 2000. Structures of oxidized and reduced azurin II from alcaligenes xylosoxidans at 1.75 Å resolution. Acta Cryst Sect D 56:690–696.CrossRefGoogle Scholar
  35. 35.
    Baker EN. 1988. Structure of azurin from alcaligenes denitrificans refinement at 1.8 Å resolution and comparison of the 2 crystallographically independent molecules. J Mol Biol 203:1071–1095.PubMedCrossRefGoogle Scholar
  36. 36.
    Guss JM, Bartunik HD, Freeman HC. 1992. Accuracy and precision in proteinstructure analysis: restrained least-squares refinement of the structure of poplar plastocyanin at 1.33 Å resolution. Acta Cryst Sect B 48:790–811.CrossRefGoogle Scholar
  37. 37.
    Guss JM, Freeman HC. 1983. Structure of oxidized poplar plastocyanin at 1.6 Å resolution. J Mol Biol 169:521–563.PubMedCrossRefGoogle Scholar
  38. 38.
    Inoue T, Sugawara H, Hamanaka S, Tsukui H, Suzuki E, Kohzuma T, Kai Y. 1999. Crystal structure determinations of oxidized and reduced plastocyanin from the cyanobacterium synechococcus sp pcc 7942. Biochemistry 38:6063–6069.PubMedCrossRefGoogle Scholar
  39. 39.
    Kohzuma T, Inoue T, Yoshizaki F, Sasakawa Y, Onodera K, Nagatomo S, Kitagawa T, Uzawa S, Isobe Y, Sugimura Y, Gotowda M, Kai Y. 1999. The structure and unusual pH dependence of plastocyanin from the fern dryopteris crassirhizoma: the protonation of an active site histidine is hindered by π-π interactions. J Biol Chem 274:11817–11823.PubMedCrossRefGoogle Scholar
  40. 40.
    Colman PM, Freeman HC, Guss JM, Murata M, Norris VA, Ramshaw JAM, Venkatappa MP. 1978. X-ray crystal structure analysis of plastocyanin at 2.7 Å resolution. Nature 272:319–324.CrossRefGoogle Scholar
  41. 41.
    Hakulinen N, Kiiskinen LL, Kruus K, Saloheimo M, Paananen A, Koivula A, Rouvinen J. 2002. Crystal structure of a laccase from melanocarpus albomyces with an intact trinuclear copper site. Nat Struct Biol 9:601–605.PubMedGoogle Scholar
  42. 42.
    Ducros V, Brzozowski AM, Wilson KS, Brown SH, Ostergaard P, Schneider P, Yaver DS, Pedersen AH, Davies GJ. 1998. Crystal structure of the type 2 Cu depleted laccase from coprinus cinereus at 2.2 Å resolution. Nat Struct Biol 5:310–316.PubMedCrossRefGoogle Scholar
  43. 43.
    Ducros V, Brzozowski AM, Wilson KS, Ostergaard P, Schneider P, Svendson A, Davies GJ. 2001. Structure of the laccase from coprinus cinereus at 1.68 Å resolution: evidence for different “type 2 Cu-depleted” isoforms. Acta Cryst Sect D 57:333–336.CrossRefGoogle Scholar
  44. 44.
    Piontek K, Antorini M, Choinowski T. 2002. Crystal structure of a laccase from the fungus trametes versicolor at 1.90 Å resolution containing a full complement of coppers. J Biol Chem 277:37663–37669.PubMedCrossRefGoogle Scholar
  45. 45.
    Penfield KW, Gay RR, Himmelwright RS, Eickman NC, Norris VA, Freeman HC, Solomon EI. 1981. Spectroscopic studies on plastocyanin single crystals: a detailed electronic structure determination of the blue copper active site. J Am Chem Soc 103:4382–4388.CrossRefGoogle Scholar
  46. 46.
    George SJ, Lowery MD, Solomon EI, Cramer SP. 1993. Copper L-edge spectral studies: a direct experimental probe of the ground state covalency in the blue copper site in plastocyanin. J Am Chem Soc 115:2968–2969.CrossRefGoogle Scholar
  47. 47.
    Roberts JE, Brown TG, Hoffman BM, Peisach J. 1980. Electron nuclear double resonance spectra of stellacyanin: blue copper protein. J Am Chem Soc 102:825–829.CrossRefGoogle Scholar
  48. 48.
    Scott RA, Hahn JE, Doniach S, Freeman HC, Hodgson KO. 1982. Polarized x-ray absorption spectra of oriented plastocyanin single crystals: investigation of methionine copper coordination. J Am Chem Soc 104:5364–5369.CrossRefGoogle Scholar
  49. 49.
    Shadle SE, Pennerhahn JE, Schugar HJ, Hedman B, Hodgson KO, Solomon EI. 1993. X-ray absorption spectroscopic studies of the blue copper site: metal and ligand K-edge studies to probe the origin of the EPR hyperfine splitting in plastocyanin. J Am Chem Soc 115:767–776.CrossRefGoogle Scholar
  50. 50.
    Penfield KW, Gewirth AA, Solomon EI. 1985. Electronic structure and bonding of the blue copper site in plastocyanin. J Am Chem Soc 107:4519–4529.CrossRefGoogle Scholar
  51. 51.
    Wasinger EC, de Groot FMF, Hedman B, Hodgson KO, Solomon EI. 2003. L-edge xray absorption spectroscopy of non-heme iron sites: experimental determination of differential orbital covalency. J Am Chem Soc 125:12894–12906.PubMedCrossRefGoogle Scholar
  52. 52.
    Solomon EI, Hedman B, Hodgson KO, Dey A, Szilagyi RK. 2005. Ligand K-edge xray absorption spectroscopy: Covalency of ligand-metal bonds. Coord Chem Rev 249:97–129.CrossRefGoogle Scholar
  53. 53.
    Hughey JL, Fawcett TG, Rudich SM, Lalancette RA, Potenza JA, Schugar HJ. 1979. Preparation and characterization of [rac-5,7,7,12,14,14-hexamethyl-1,4,8,11-tetraazocyclotetradecane]copper(II) o-mercaptobenzoate hydrate, [Cu(tet b)(o-SC6H4CO2)]•H2O, a complex with a CuN4S (mercaptide) chromophore. J Am Chem Soc 101:2617–2623.CrossRefGoogle Scholar
  54. 54.
    George SD, Basumallick L, Szilagyi RK, Randall DW, Hill MG, Nersissian AM, Valentine JS, Hedman B, Hodgson KO, Solomon EI. 2003. Spectroscopic investigation of stellacyanin mutants: axial ligand interactions at the blue copper site. J Am Chem Soc 125:11314–11328.CrossRefGoogle Scholar
  55. 55.
    Gewirth AA, Solomon EI. 1988. Electronic structure of plastocyanin: excited state spectral features. J Am Chem Soc 110:3811–3819.CrossRefGoogle Scholar
  56. 56.
    Solomon EI, Randall DW, Glaser T. 2000. Electronic structures of active sites in electron transfer metalloproteins: Contributions to reactivity. Coord Chem Rev 200:595–632.CrossRefGoogle Scholar
  57. 57.
    LaCroix LB, Randall DW, Nersissian AM, Hoitink CWG, Canters GW, Valentine JS, Solomon EI. 1998. Spectroscopic and geometric variations in perturbed blue copper centers: electronic structures of stellacyanin and cucumber basic protein. J Am Chem Soc 120:9621–9631.CrossRefGoogle Scholar
  58. 58.
    Randall DW, Gamelin DR, LaCroix LB, Solomon EI. 2000. Electronic structure contributions to electron transfer in blue Cu and CuA. J Bio Inorg Chem 5:16–29.Google Scholar
  59. 59.
    LaCroix LB, Shadle SE, Wang YN, Averill BA, Hedman B, Hodgson KO, Solomon EI. 1996. Electronic structure of the perturbed blue copper site in nitrite reductase: spectroscopic properties, bonding, and implications for the entatic/rack state. J Am Chem Soc 118:7755–7768.CrossRefGoogle Scholar
  60. 60.
    Suzuki S, Kohzuma T, Deligeer, Yamaguchi K, Nakamura N, Shidara S, Kobayashi K, Tagawa S. 1994. Pulse radiolysis studies on nitrite reductase from achromobacter cycloclastes IAM 1013: evidence for intramolecular electron transfer from type 1 Cu to type 2 Cu. J Am Chem Soc 116:11145–11146.Google Scholar
  61. 61.
    Gewirth AA, Cohen SL, Schugar HJ, Solomon EI. 1987. Spectroscopic and theoretical studies of the unusual electron paramagnetic resonance parameters of distorted tetrahedral cupric sites: correlations to x-ray spectral features of core levels. Inorg Chem 26:1133–1146.CrossRefGoogle Scholar
  62. 62.
    Beinert H, Wharton DC, Griffiths DE, Sands RH. 1962. Properties of copper associated with cytochrome oxidase as studied by paramagnetic resonance spectroscopy. J Biol Chem 237:2337–2346.PubMedGoogle Scholar
  63. 63.
    Peisach J, Blumberg WE. 1974. Structural implications derived from analysis of electron paramagnetic resonance spectra of natural and artificial copper proteins. Arch Biochem Biophys 165:691–708.PubMedCrossRefGoogle Scholar
  64. 64.
    Kroneck PMH, Antholine WE, Kastrau DHW, Buse G, Steffens GCM, Zumft WG. 1990. Multifrequency EPR evidence for a bimetallic center at the CuA site in cytochrome c oxidase. FEBS Lett 268:274–276.PubMedCrossRefGoogle Scholar
  65. 65.
    Kroneck PMH, Antholine WA, Riester J, Zumft WG. 1988. The cupric site in nitrous oxide reductase contains a mixed-valence [Cu(II),Cu(I)] binuclear center: a multifrequency electron paramagnetic resonance investigation. FEBS Lett 242:70–74.PubMedCrossRefGoogle Scholar
  66. 66.
    Antholine WE, Kastrau DHW, Steffens GCM, Buse G, Zumft WG, Kroneck PMH. 1992. A comparative EPR investigation of the multicopper proteins nitrous-oxide reductase and cytochrome c oxidase. Eur J Biochem 209:875–881.PubMedCrossRefGoogle Scholar
  67. 67.
    Blackburn NJ, Barr ME, Woodruff WH, Vanderooost J, Devries S. 1994. Metal–metal bonding in biology: EXAFS evidence for a 2.5 Å copper–copper bond in the CuA center of cytochrome oxidase. Biochemistry 33:10401–10407.PubMedCrossRefGoogle Scholar
  68. 68.
    Blackburn NJ, deVries S, Barr ME, Houser RP, Tolman WB, Sanders D, Fee JA. 1997. X-ray absorption studies on the mixed-valence and fully reduced forms of the soluble CuA domains of cytochrome c oxidase. J Am Chem Soc 119:6135–6143.CrossRefGoogle Scholar
  69. 69.
    Gamelin DR, Randall DW, Hay MT, Houser RP, Mulder TC, Canters GW, de Vries S, Tolman WB, Lu Y, Solomon EI. 1998. Spectroscopy of mixed-valence CuA type centers: Ligand field control of ground state properties related to electron transfer. J Am Chem Soc 120:5246–5263.CrossRefGoogle Scholar
  70. 70.
    Farrar JA, Neese F, Lappalainen P, Kroneck PMH, Saraste M, Zumft WG, Thomson AJ. 1996. The electronic structure of CuA: a novel mixed-valence dinuclear copper electron transfer center. J Am Chem Soc 118:11501–11514.CrossRefGoogle Scholar
  71. 71.
    George SD, Metz M, Szilagyi RK, Wang HX, Cramer SP, Lu Y, Tolman WB, Hedman B, Hodgson KO, Solomon EI. 2001. A quantitative description of the ground state wave function of CuA by x-ray absorption spectroscopy: comparison to plastocyanin and relevance to electron transfer. J Am Chem Soc 123:5757–5767.CrossRefGoogle Scholar
  72. 72.
    Gamelin DR, Bominaar EL, Mathoniere C, Kirk ML, Wieghardt K, Girerd JJ, Solomon EI. 1996. Excited-state distortions and electron delocalization in mixed-valence dimers: vibronic analysis of the near IR absorption and resonance Raman profiles of [Fe2(OH)3(tmtacn)2]2+. Inorg Chem 35:4323–4335.PubMedCrossRefGoogle Scholar
  73. 73.
    Houser RP, Young VG, Tolman WB. 1996. Thiolate-bridged, fully delocalized mixedvalence dicopper(I,II) complex that models the CuA biological electron transfer site. J Am Chem Soc 118:2101–2102.CrossRefGoogle Scholar
  74. 74.
    Williams KR, Gamelin DR, LaCroix LB, Houser RP, Tolman WB, Mulder TC, deVries S, Hedman B, Hodgson KO, Solomon EI. 1997. Influence of copper–sulfur covalency and copper–copper bonding on valence delocalization and electron transfer in the CuA site of cytochrome c oxidase. J Am Chem Soc 119:613–614.CrossRefGoogle Scholar
  75. 75.
    Gurbiel RJ, Fann YC, Surerus KK, Werst MM, Musser SM, Doan PE, Chan SI, Fee JA, Hoffman BM. 1993. Detection of 2 histidyl ligands to CuA of cytochrome oxidase by 35 GHz ENDOR: 14,15N and 63,65Cu ENDOR studies of the CuA site in bovine heart cytochrome-aa3 and cytochrome-caa3 and cytochrome-ba3 from thermus thermophilus. J Am Chem Soc 115:10888–10894.CrossRefGoogle Scholar
  76. 76.
    Solomon EI, Chen P, Metz M, Lee SK, Palmer AE. 2001. Oxygen binding, activation, and reduction to water by copper proteins. Angew Chem Int Ed 40:4570–4590.CrossRefGoogle Scholar
  77. 77.
    Co MS, Hodgson KO, Eccles TK, Lontie R. 1981. Copper site of molluscan oxyhemocyanins: structural evidence from x-ray absorption spectroscopy. J Am Chem Soc 103:984–986.CrossRefGoogle Scholar
  78. 78.
    Matoba Y, Kumagai T, Yamamoto A, Yoshitsu H, Sugiyama M. 2006. Crystallographic evidence that dinuclear copper center of tyrosinase is flexible during catalysis. J Biol Chem 281:8981–8990.PubMedCrossRefGoogle Scholar
  79. 79.
    Magnus KA, Hazes B, Tonthat H, Bonaventura C, Bonaventura J, Hol WGJ. 1994. Crystallographic analysis of oxygenated and deoxygenated states of arthropod hemocyanin shows unusual differences. Proteins 19:302–309.PubMedCrossRefGoogle Scholar
  80. 80.
    Dooley DM, Scott RA, Ellinghaus J, Solomon EI, Gray HB. 1978. Magnetic susceptibility studies of laccase and oxyhemocyanin. Proc Nat Acad Sci USA 75:3019–3022.PubMedCrossRefGoogle Scholar
  81. 81.
    Crawford VH, Richardson HW, Wasson JR, Hodgson DJ, Hatfield WE. 1976. Relationship between singlet–triplet splitting and Cu–O–Cu bridge angle in hydroxobridged copper dimers. Inorg Chem 15:2107–2110.CrossRefGoogle Scholar
  82. 82.
    Hay PJ, Thibeault JC, Hoffmann R. 1975. Orbital interactions in metal dimer complexes. J Am Chem Soc 97:4884–4899.CrossRefGoogle Scholar
  83. 83.
    Pate JE, Cruse RW, Karlin KD, Solomon EI. 1987. Vibrational, electronic, and resonance Raman spectral studies of [Cu2(XYL−O−)O2]+, a copper(II) peroxide model complex of oxyhemocyanin. J Am Chem Soc 109:2624–2630.CrossRefGoogle Scholar
  84. 84.
    Eickman NC, Himmelwright RS, Solomon EI. 1979. Geometric and electronic structure of oxyhemocyanin: spectral and chemical correlations to met apo, half met, met, and dimer active sites. Proc Nat Acad Sci USA 76:2094–2098.PubMedCrossRefGoogle Scholar
  85. 85.
    Baldwin MJ, Root DE, Pate JE, Fujisawa K, Kitajima N, Solomon EI. 1992. Spectroscopic studies of side-on peroxide-bridged binuclear copper(II) model complexes of relevance to oxyhemocyanin and oxytyrosinase. J Am Chem Soc 114:10421–10431.CrossRefGoogle Scholar
  86. 86.
    Metz M, Solomon EI. 2001. Dioxygen binding to deoxyhemocyanin: electronic structure and mechanism of the spin-forbidden two-electron reduction of O2. J Am Chem Soc 123:4938–4950.PubMedCrossRefGoogle Scholar
  87. 87.
    Prigge ST, Eipper BA, Mains RE, Amzel LM. 2004. Dioxygen binds end-on to mononuclear copper in a precatalytic enzyme complex. Science 304:864–867.PubMedCrossRefGoogle Scholar
  88. 88.
    Jaron S, Blackburn NJ. 1999. Does superoxide channel between the copper centers in peptidylglycine monooxygenase? a new mechanism based on carbon monoxide reactivity. Biochemistry 38:15086–15096.PubMedCrossRefGoogle Scholar
  89. 89.
    Bell J, El Meskini R, D’Amato D, Mains RE, Eipper BA. 2003. Mechanistic investigation of peptidylglycine α-hydroxylating monooxygenase via intrinsic tryptophan fluorescence and mutagenesis. Biochemistry 42:7133–7142.PubMedCrossRefGoogle Scholar
  90. 90.
    Boswell JS, Reedy BJ, Kulathila R, Merkler D, Blackburn NJ. 1996. Structural investigations on the coordination environment of the active site copper centers of recombinant bifunctional peptidylglycine α-amidating enzyme. Biochemistry 35:12241–12250.PubMedCrossRefGoogle Scholar
  91. 91.
    Blackburn NJ, Rhames FC, Ralle M, Jaron S. 2000. Major changes in copper coordination accompany reduction of peptidylglycine monooxygenase: implications for electron transfer and the catalytic mechanism. J Biol Inorg Chem 5:341–353.PubMedCrossRefGoogle Scholar
  92. 92.
    Eipper BA, Quon ASW, Mains RE, Boswell JS, Blackburn NJ. 1995. The catalytic core of peptidylglycine α-hydroxylating monooxygenase: investigation by site-directed mutagenesis, Cu x-ray absorption spectroscopy, and electron paramagnetic resonance. Biochemistry 34:2857–2865.PubMedCrossRefGoogle Scholar
  93. 93.
    Chen P, Bell J, Eipper BA, Solomon EI. 2004. Oxygen activation by the noncoupled binuclear copper site in peptidylglycine α-hydroxylating monooxygenase: spectroscopic definition of the resting sites and the putative CuM(II)-OOH intermediate. Biochemistry 43:5735–5747.PubMedCrossRefGoogle Scholar
  94. 94.
    Blackburn NJ, Concannon M, Shahiyan SK, Mabbs FE, Collison D. 1988. Active site of dopamine β-hydroxylase: comparison of enzyme derivatives containing 4 and 8 copper atoms per tetramer using potentiometry and electron paramagnetic resonance spectroscopy. Biochemistry 27:6001–6008.PubMedCrossRefGoogle Scholar
  95. 95.
    Tian GC, Berry JA, Klinman JP. 1994. O-18 kinetic isotope effects in the dopamine β- monooxygenase reaction: evidence for a new chemical mechanism in nonheme metallomonooxygenases. Biochemistry 33:226–234.PubMedCrossRefGoogle Scholar
  96. 96.
    Evans JP, Ahn K, Klinman JP. 2003. Evidence that dioxygen and substrate activation are tightly coupled in dopamine β-monooxygenase: implications for the reactive oxygen species. J Biol Chem 278:49691–49698.PubMedCrossRefGoogle Scholar
  97. 97.
    Marcus RA, Sutin N. 1985. Electron transfers in chemistry and biology. Biochim Biophys Acta 811:265–322.Google Scholar
  98. 98.
    Tuczek F, Solomon EI. 1994. Charge transfer states and antiferromagnetism of bridged Cu dimers: application to oxyhemocyanin. J Am Chem Soc 116:6916–6924.CrossRefGoogle Scholar
  99. 99.
    Tuczek F, Solomon EI. 2001. Excited electronic states of transition metal dimers and the VBCI model: an overview. Coord Chem Rev 219:1075–1112.CrossRefGoogle Scholar
  100. 100.
    Messerschmidt A, Ladenstein R, Huber R, Bolognesi M, Avigliano L, Petruzzelli R, Rossi A, Finazziagro A. 1992. Refined crystal structure of ascorbate oxidase at 1.9 Å resolution. J Mol Biol 224:179–205.PubMedCrossRefGoogle Scholar
  101. 101.
    Cole JL, Ballou DP, Solomon EI. 1991. Spectroscopic characterization of the peroxide intermediate in the reduction of dioxygen catalyzed by the multicopper oxidases. J Am Chem Soc 113:8544–8546.CrossRefGoogle Scholar
  102. 102.
    Palmer AE, Lee SK, Solomon EI. 2001. Decay of the peroxide intermediate in laccase: reductive cleavage of the O-O bond. J Am Chem Soc 123:6591–6599.PubMedCrossRefGoogle Scholar
  103. 103.
    Quintanar L, Yoon J, Aznar CP, Palmer AE, Andersson KK, Britt RD, Solomon EI. 2005. Spectroscopic and electronic structure studies of the trinuclear Cu cluster active site of the multicopper oxidase laccase: nature of its coordination unsaturation. J Am Chem Soc 127:13832–13845.PubMedCrossRefGoogle Scholar
  104. 104.
    Cole JL, Clark PA, Solomon EI. 1990. Spectroscopic and chemical studies of the laccase trinuclear copper active site: geometric and electronic structure. J Am Chem Soc 112:9534–9548.CrossRefGoogle Scholar
  105. 105.
    Clark PA, Solomon EI. 1992. Magnetic circular dichroism spectroscopic definition of the intermediate produced in the reduction of dioxygen to water by native laccase. J Am Chem Soc 114:1108–1110.CrossRefGoogle Scholar
  106. 106.
    Aasa R, Branden R, Deinum J, Malmstrom BG, Reinhammar B, Vanngard T. 1976. 17O effect on EPR spectrum of intermediate in dioxygen–laccase reaction. Biochem Biophys Res Comm 70:1204–1209.PubMedCrossRefGoogle Scholar
  107. 107.
    Yoon J, Mirica LM, Stack TDP, Solomon EI. 2004. Spectroscopic demonstration of a large antisymmetric exchange contribution to the spin-frustrated ground state of a D3 symmetric hydroxy-bridged trinuclear Cu(II) complex: ground-to-excited state superexchange pathways. J Am Chem Soc 126:12586–12595.PubMedCrossRefGoogle Scholar
  108. 108.
    Mirica LM, Stack TDP. 2005. A tris(μ-hydroxy)tricopper(II) complex as a model of the native intermediate in laccase and its relationship to a binuclear analogue. Inorg Chem 44:2131–2133.PubMedCrossRefGoogle Scholar
  109. 109.
    Dzyaloshinsky I. 1958. A thermodynamic theory of weak ferromagnetism of antiferromagnetics. J Phys Chem Solids 4:241–255.CrossRefGoogle Scholar
  110. 110.
    Moriya T. 1960. Anisotropic superexchange interaction and weak ferromagnetism. Phys Rev 120:91–98.CrossRefGoogle Scholar
  111. 111.
    Moriya T. 1963. Weak ferromagnetism. In Magetism, pp. 85–125. Ed GT Rado and H Suhl. New York: Academic Press.Google Scholar
  112. 112.
    Tsukerblat BS, Belinskii MI, Fainzil’berg VE. 1987. Magnetochemistry and spectroscopy of transition metals exchange clusters. Sov Sci Rev B Chem 9:337–481.Google Scholar
  113. 113.
    Murao T. 1974. Jahn-Teller effect in trinuclear complexes. Phys Lett A 49:33–35.CrossRefGoogle Scholar
  114. 114.
    Yoon J, Solomon EI. 2005. Ground-state electronic and magnetic properties of a μ3- oxo-bridged trinuclear Cu(II) complex: correlation to the native intermediate of the multicopper oxidases. Inorg Chem 44:8076–8086.PubMedCrossRefGoogle Scholar
  115. 115.
    Suh MP, Han MY, Lee JH, Min KS, Hyeon C. 1998. One-pot template synthesis and properties of a molecular bowl: dodecaaza macrotetracycle with μ3-oxo and μ3-hydroxo tricopper(II) cores. J Am Chem Soc 120:3819–3820.CrossRefGoogle Scholar
  116. 116.
    Yoon J, Mirica LM, Stack TDP, Solomon EI. 2005. Variable-temperature, variablefield magnetic circular dichroism studies of tris-hydroxy- and μ3-oxo-bridged trinuclear Cu(II) complexes: evaluation of proposed structures of the native intermediate of the multicopper oxidases. J Am Chem Soc 127:13680–13693.PubMedCrossRefGoogle Scholar
  117. 117.
    Farrar JA, Thomson AJ, Cheesman MR, Dooley DM, Zumft WG. 1991. A model of the copper centers of nitrous-oxide reductase (pseudomonas-stutzeri): evidence from optical, EPR and MCD spectroscopy. FEBS Lett 294:11–15.PubMedCrossRefGoogle Scholar
  118. 118.
    Farrar JA, Zumft WG, Thomson AJ. 1998. CuA and CuZ are variants of the electron transfer center in nitrous oxide reductase. Proc Nat Acad Sci USA 95:9891–9896.PubMedCrossRefGoogle Scholar
  119. 119.
    Prudencio M, Pereira AS, Tavares P, Besson S, Cabrito I, Brown K, Samyn B, Devreese B, Van Beeumen J, Rusnak F, Fauque G, Moura JJG, Tegoni M, Cambillau C, Moura I. 2000. Purification, characterization, and preliminary crystallographic study of copper containing nitrous oxide reductase from pseudomonas nautica 617. Biochemistry 39:3899–3907.PubMedCrossRefGoogle Scholar
  120. 120.
    Froncisz W, Hyde JS. 1980. Broadening by strains of lines in the g|| region of Cu2+ electron paramagnetic resonance. J Chem Phys 73:3123–3131.CrossRefGoogle Scholar
  121. 121.
    Oganesyan VS, Rasmussen T, Fairhurst S, Thomson AJ. 2004. Characterisation of [Cu4S], the catalytic site in nitrous oxide reductase, by EPR spectroscopy. Dalton Trans 996–1002.Google Scholar
  122. 122.
    Gorelsky SI, Ghosh S, Solomon EI. 2006. Mechanism of N2O reduction by the μ4-S tetranuclear Cuz cluster of nitrous oxide reductase. J Am Chem Soc 128:278–290.PubMedCrossRefGoogle Scholar
  123. 123.
    Ghosh S, Gorelsky SI, Chen P, Cabrito I, Moura JJG, Moura I, Solomon EI. 2003. Activation of N2O reduction by the fully reduced μ4-sulfide bridged tetranuclear CuZ cluster in nitrous oxide reductase. J Am Chem Soc 125:15708–15709.PubMedCrossRefGoogle Scholar

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© Springer-Verlag New York 2009

Authors and Affiliations

  1. 1.Department of ChemistryStanford UniversityStanfordUSA

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