Methane Monooxygenase: Functionalizing Methane at Iron and Copper

Chapter
Part of the Metal Ions in Life Sciences book series (MILS, volume 15)

Abstract

Methane monooxygenases (MMOs) catalyze the conversion of methane to methanol as the first committed step in the assimilation of this hydrocarbon into biomass and energy by methanotrophs, thus playing a significant role in the biogeochemistry of this potent greenhouse gas. Two distinct enzymes, a copper-dependent membrane protein, particulate methane monooxygenase (pMMO), and an iron-dependent cytosolic protein, soluble methane monooxygenase (sMMO), carry out this transformation using large protein scaffolds that help to facilitate the timely transport of hydrocarbon, O2, proton, and electron substrates to buried dimetallic active sites. For both enzymes, reaction of the reduced metal centers with O2 leads to intermediates that activate the relatively inert C–H bonds of hydrocarbons to yield oxidized products. Among synthetic and biological catalysts, MMOs are unique because they are the only ones known to hydroxylate methane at ambient temperatures. As a need for new industrial catalysts and green chemical transformations increases, understanding how the different MMO metal centers efficiently accomplish this challenging chemistry has become the focus of intense study. This chapter examines current understanding of the sMMO and pMMO protein structures, their methods for substrate channeling, and mechanisms for the dimetallic activation of O2 and C–H bonds.

Keywords

bacterial multicomponent monooxygenase dicopper diiron mechanism particulate methane monooxygenase protein complexes soluble methane monooxygenase 

References

  1. 1.
    US Environmental Protection Agency, in “Methane and Nitrous Oxide Emissions From Natural Sources”, Ed US Environmental Protection Agency, Washington DC, USA, 2010.Google Scholar
  2. 2.
    R. S. Hanson, T. E. Hanson, Microbiol. Rev. 1996, 60, 439–471.PubMedPubMedCentralGoogle Scholar
  3. 3.
    H. Jiang, Y. Chen, P. X. Jiang, C. Zhang, T. J. Smith, J. C. Murrell, X. H. Xing, Biochem. Eng. J. 2010, 49, 277–288.Google Scholar
  4. 4.
    R. Balasubramanian, A. C. Rosenzweig, Acc. Chem. Res. 2007, 40, 573–580.PubMedGoogle Scholar
  5. 5.
    M. A. Culpepper, A. C. Rosenzweig, Crit. Rev. Biochem. Mol. 2012, 47, 483–492.Google Scholar
  6. 6.
    A. S. Hakemian, A. C. Rosenzweig, Annu. Rev. Biochem. 2007, 76, 223–241.PubMedGoogle Scholar
  7. 7.
    R. L. Lieberman, A. C. Rosenzweig, Crit. Rev. Biochem. Mol. 2004, 39, 147–164.Google Scholar
  8. 8.
    M. Merkx, D. A. Kopp, M. H. Sazinsky, J. L. Blazyk, J. Müller, S. J. Lippard, Angew. Chem. Int. Edit. 2001, 40, 2782–2807.Google Scholar
  9. 9.
    C. E. Tinberg, S. J. Lippard, Acc. Chem. Res. 2011, 44, 280–288.PubMedPubMedCentralGoogle Scholar
  10. 10.
    B. J. Wallar, J. D. Lipscomb, Chem. Rev. 1996, 96, 2625–2657.PubMedGoogle Scholar
  11. 11.
    M.-H. Baik, M. Newcomb, R. A. Friesner, S. J. Lippard, Chem. Rev. 2003, 103, 2385–2419.PubMedGoogle Scholar
  12. 12.
    J. D. Semrau, A. A. DiSpirito, S. Yoon, FEMS Microbiol. Rev. 2010, 34, 496–531.PubMedGoogle Scholar
  13. 13.
    H. Ali, J. C. Murrell, Microbiology 2009, 155, 761–771.PubMedGoogle Scholar
  14. 14.
    D. W. Choi, R. C. Kunz, E. S. Boyd, J. D. Semrau, W. E. Antholine, J. I. Han, J. A. Zahn, J. M. Boyd, A. M. de la Mora, A. A. DiSpirito, J. Bacteriol. 2003, 185, 5755–5764.PubMedPubMedCentralGoogle Scholar
  15. 15.
    S. H. Stanley, S. D. Prior, D. J. Leak, H. Dalton, Biotechnol. Lett. 1983, 5, 487–492.Google Scholar
  16. 16.
    S. D. Prior, H. Dalton, J. Gen. Microbiol. 1985, 131, 155–163.Google Scholar
  17. 17.
    R. Balasubramanian, A. C. Rosenzweig, Curr. Opin. Chem. Biol. 2008, 12, 245–249.PubMedPubMedCentralGoogle Scholar
  18. 18.
    M. W. Fitch, D. W. Graham, R. G. Arnold, S. K. Agarwal, P. Phelps, G. E. Speitel, G. Georgiou, Appl. Environ. Microbiol. 1993, 59, 2771–2776.PubMedPubMedCentralGoogle Scholar
  19. 19.
    A. A. DiSpirito, J. A. Zahn, D. W. Graham, H. J. Kim, C. K. Larive, T. S. Derrick, C. D. Cox, A. Taylor, J. Bacteriol. 1998, 180, 3606–3613.PubMedPubMedCentralGoogle Scholar
  20. 20.
    C. M. Tellez, K. P. Gaus, D. W. Graham, R. G. Arnold, R. Z. Guzman, Appl. Environ. Microbiol. 1998, 64, 1115–1122.PubMedPubMedCentralGoogle Scholar
  21. 21.
    J. Colby, D. I. Stirling, H. Dalton, Biochem. J. 1977, 165, 395–402.PubMedPubMedCentralGoogle Scholar
  22. 22.
    I. J. Higgins, D. J. Best, R. C. Hammond, Nature 1980, 286, 561–564.PubMedGoogle Scholar
  23. 23.
    J. Green, H. Dalton, J. Biol. Chem. 1989, 264, 17698–17703.PubMedGoogle Scholar
  24. 24.
    B. G. Fox, J. G. Borneman, L. P. Wackett, J. D. Lipscomb, Biochemistry 1990, 29, 6419–6427.PubMedGoogle Scholar
  25. 25.
    K. K. Andersson, W. A. Froland, S. K. Lee, J. D. Lipscomb, New J. Chem. 1991, 15, 411–415.Google Scholar
  26. 26.
    M. J. Rataj, J. E. Kauth, M. I. Donnelly, J. Biol. Chem. 1991, 266, 18684–18690.PubMedGoogle Scholar
  27. 27.
    S. I. Chan, K. H. C. Chen, S. S. F. Yu, C. L. Chen, S. S. J. Kuo, Biochemistry 2004, 43, 4421–4430.PubMedGoogle Scholar
  28. 28.
    K. Burrows, A. Cornish, D. Scott, I. J. Higgins, J. Gen. Microbiol. 1984, 130, 327–333.Google Scholar
  29. 29.
    D. D. Smith, H. Dalton, Eur. J. Biochem. 1989, 182, 667–671.PubMedGoogle Scholar
  30. 30.
    R. L. Lieberman, A. C. Rosenzweig, Nature 2005, 434, 177–182.PubMedGoogle Scholar
  31. 31.
    S. Stolyar, A. M. Costello, T. L. Peeples, M. E. Lidstrom, Microbiology 1999, 145, 1235–1244.PubMedGoogle Scholar
  32. 32.
    D. J. Arp, L. A. Sayavedra-Soto, N. G. Hommes, Arch. Microbiol. 2002, 178, 250–255.PubMedGoogle Scholar
  33. 33.
    P. Basu, B. Katterle, K. K. Andersson, H. Dalton, Biochem. J. 2003, 369, 417–427.PubMedPubMedCentralGoogle Scholar
  34. 34.
    R. L. Lieberman, D. B. Shrestha, P. E. Doan, B. M. Hoffman, T. L. Stemmler, A. C. Rosenzweig, Proc. Natl. Acad. Sci. USA 2003, 100, 3820–3825.PubMedPubMedCentralGoogle Scholar
  35. 35.
    H. H. T. Nguyen, S. J. Elliott, J. H. K. Yip, S. I. Chan, J. Biol. Chem. 1998, 273, 7957–7966.PubMedGoogle Scholar
  36. 36.
    S. S. F. Yu, K. H. C. Chen, M. Y. H. Tseng, Y. S. Wang, C. F. Tseng, Y. J. Chen, D. S. Huang, S. I. Chan, J. Bacteriol. 2003, 185, 5915–5924.PubMedPubMedCentralGoogle Scholar
  37. 37.
    A. Miyaji, T. Kamachi, I. Okura, Biotechnol. Lett. 2002, 24, 1883–1887.Google Scholar
  38. 38.
    J. A. Zahn, A. A. DiSpirito, J. Bacteriol. 1996, 178, 1018–1029.PubMedPubMedCentralGoogle Scholar
  39. 39.
    S. M. Smith, S. Rawat, J. Telser, B. M. Hoffman, T. L. Stemmler, A. C. Rosenzweig, Biochemistry 2011, 50, 10231–10240.PubMedPubMedCentralGoogle Scholar
  40. 40.
    R. L. Lieberman, A. C. Rosenzweig, Dalton Trans. 2005, 3390–3396.Google Scholar
  41. 41.
    A. Kitmitto, N. Myronova, P. Basu, H. Dalton, Biochemistry 2005, 44, 10954–10965.PubMedGoogle Scholar
  42. 42.
    N. Myronova, A. Kitmitto, R. F. Collins, A. Miyaji, H. Dalton, Biochemistry 2006, 45, 11905–11914.PubMedGoogle Scholar
  43. 43.
    H. J. Op den Camp, T. Islam, M. B. Stott, H. R. Harhangi, A. Hynes, S. Schouten, M. S. M. Jetten, N. K. Birkeland, A. Pol, P. F. Dunfield, Environ. Microbiol. Rep. 2009, 1, 293–306.PubMedGoogle Scholar
  44. 44.
    R. L. Lieberman, K. C. Kondapalli, D. B. Shrestha, A. S. Hakemian, S. M. Smith, J. Telser, J. Kuzelka, R. Gupta, A. S. Borovik, S. J. Lippard, B. M. Hoffman, A. C. Rosenzweig, T. L. Stemmler, Inorg. Chem. 2006, 45, 8372–8381.PubMedPubMedCentralGoogle Scholar
  45. 45.
    A. S. Hakemian, K. C. Kondapalli, J. Telser, B. M. Hoffman, T. L. Stemmler, A. C. Rosenzweig, Biochemistry 2008, 47, 6793–6801.PubMedGoogle Scholar
  46. 46.
    S. I. Chan, S. S. F. Yu, Acc. Chem. Res. 2008, 41, 969–979.PubMedGoogle Scholar
  47. 47.
    H. H. T. Nguyen, A. K. Shiemke, S. J. Jacobs, B. J. Hales, M. E. Lidstrom, S. I. Chan, J. Biol. Chem. 1994, 269, 14995–15005.PubMedGoogle Scholar
  48. 48.
    H. H. T. Nguyen, K. H. Nakagawa, B. Hedman, S. J. Elliott, M. E. Lidstrom, K. O. Hodgson, S. I. Chan, J. Am Chem. Soc. 1996, 118, 12766–12776.Google Scholar
  49. 49.
    A. C. Rosenzweig, M. H. Sazinsky, Curr. Opin. Struc. Biol. 2006, 16, 729–735.Google Scholar
  50. 50.
    H. H. A. T. Nguyen, M. Zhu, S. J. Elliott, K. H. Nakagawa, B. Hedman, A. M. Costello, T. L. Peeples, B. Wilkinson, H. Morimoto, P. G. Williams, H. G. Floss, M. E. Lidstrom, K. O. Hodgson, S. I. Chan, Microbial Growth on C(1) Compounds 1996, 150–158.Google Scholar
  51. 51.
    M. Takeguchi, K. Miyakawa, I. Okura, J. Mol. Catal. A-Chem. 1998, 132, 145–153.Google Scholar
  52. 52.
    M. Takeguchi, I. Okura, Catal. Surv. Jpn. 2000, 4, 51–63.Google Scholar
  53. 53.
    H. Yuan, M. L. P. Collins, W. E. Antholine, J. Am Chem. Soc. 1997, 119, 5073–5074.Google Scholar
  54. 54.
    H. Yuan, M. L. P. Collins, W. E. Antholine, Biophys. J. 1999, 76, 2223–2229.PubMedPubMedCentralGoogle Scholar
  55. 55.
    S. S. Lemos, M. L. P. Collins, S. S. Eaton, G. R. Eaton, W. E. Antholine, Biophys. J. 2000, 79, 1085–1094.PubMedPubMedCentralGoogle Scholar
  56. 56.
    L. V. Tumanova, I. A. Tukhvatullin, D. S. Burbaev, R. I. Gvozdev, K. K. Andersson, Russ. J. Bioinorg. Chem. 2005, 34, 177–185.Google Scholar
  57. 57.
    M. Martinho, D. W. Choi, A. A. DiSpirito, W. E. Antholine, J. D. Semrau, E. Münck, J. Am Chem. Soc. 2007, 129, 15783–15785.PubMedPubMedCentralGoogle Scholar
  58. 58.
    O. A. Karlsen, J. R. Lillehaug, H. B. Jensen, Mol. Microbiol. 2008, 70, 15–26.PubMedGoogle Scholar
  59. 59.
    S. M. Smith, R. Balasubramanian, A. C. Rosenzweig, Meth. Enzymol. 2011 , 495, 195–210.PubMedPubMedCentralGoogle Scholar
  60. 60.
    R. Balasubramanian, S. M. Smith, S. Rawat, L. A. Yatsunyk, T. L. Stemmler, A. C. Rosenzweig, Nature 2010, 465, 115–U131.PubMedPubMedCentralGoogle Scholar
  61. 61.
    A. Miyaji, T. Kamachi, I. Okura, T. Baba, J. Mol. Catal. B-Enzym. 2010, 62, 121–121.Google Scholar
  62. 62.
    J. C. Murrell, T. J. Smith, in Handbook of Hydrocarbon and Lipid Microbiology, Ed K. N. Timmis, Springer, Heidelberg, Germany, 2010, Vol. 1, pp. 1045–1055.Google Scholar
  63. 63.
    A. Miyaji, T. Miyoshi, K. Motokura, T. Baba, Biotechnol. Lett. 2011, 33, 2241–2246.PubMedGoogle Scholar
  64. 64.
    S. J. Elliott, M. Zhu, L. Tso, H. H. T. Nguyen, J. H. K. Yip, S. I. Chan, J. Am Chem. Soc. 1997, 119, 9949–9955.Google Scholar
  65. 65.
    W. J. Song, G. Gucinski, M. H. Sazinsky, S. J. Lippard, Proc. Natl. Acad. Sci. USA 2011, 108, 14795–14800.PubMedPubMedCentralGoogle Scholar
  66. 66.
    K. H. C. Chen, H. H. Wu, S. F. Ke, Y. T. Rao, C. M. Tu, Y. P. Chen, K. H. Kuei, Y. S. Chen, V. C. C. Wang, W. C. Kao, S. I. Chan, J. Inorg. Biochem. 2012, 111, 10–17.PubMedGoogle Scholar
  67. 67.
    S. A. Cook, A. K. Shiemke, Arch. Biochem. Biophys. 2002, 398, 32–40.PubMedGoogle Scholar
  68. 68.
    M. R. Hyman, P. M. Wood, Biochem. J. 1985, 227, 719–725.PubMedPubMedCentralGoogle Scholar
  69. 69.
    M. R. Hyman, D. J. Arp, J. Biol. Chem. 1992, 267, 1534–1545.PubMedGoogle Scholar
  70. 70.
    S. Gilch, M. Vogel, M. W. Lorenz, O. Meyer, I. Schmidt, Microbiology 2009, 155, 279–284.PubMedGoogle Scholar
  71. 71.
    G. M. Tonge, D. E. F. Harrison, C. J. Knowles, I. Higgins, FEBS Lett. 1975, 58, 293–299.PubMedGoogle Scholar
  72. 72.
    M. A. Culpepper, G. E. Cutsail, B. M. Hoffman, A. C. Rosenzweig, J. Am Chem. Soc. 2012, 134, 7640–7643.PubMedPubMedCentralGoogle Scholar
  73. 73.
    E. I. Solomon, U. M. Sundaram, T. E. Machonkin, Chem. Rev. 1996, 96, 2563–2605.PubMedGoogle Scholar
  74. 74.
    E. I. Solomon, J. W. Ginsbach, D. E. Heppner, M. T. Kieber-Emmons, C. H. Kjaergaard, P. J. Smeets, L. Tian, J. S. Woertink, Faraday Discuss. 2011, 148, 11–39.PubMedPubMedCentralGoogle Scholar
  75. 75.
    C. R. Andrew, K. P. McKillop, A. G. Sykes, Biochim. Biophys. Acta 1993, 1163, 17–25.PubMedGoogle Scholar
  76. 76.
    T. Zalateva, L. Santagostini, L. Bubacco, L. Casella, B. Salvato, M. Beltramini, J. Inorg. Biochem. 1998, 72, 211–215.Google Scholar
  77. 77.
    Y. Shiota, K. Yoshizawa, Inorg. Chem. 2009, 48, 838–845.PubMedGoogle Scholar
  78. 78.
    K. Yoshizawa, Y. Shiota, J. Am. Chem. Soc. 2006, 128, 9873–9881.PubMedGoogle Scholar
  79. 79.
    P. P. Y. Chen, S. I. Chan, J. Inorg. Biochem. 2006, 100, 801–809.PubMedGoogle Scholar
  80. 80.
    R. A. Himes, K. D. Karlin, Curr. Opin. Chem. Biol. 2009, 13, 119–131.PubMedPubMedCentralGoogle Scholar
  81. 81.
    M. H. Groothaert, P. J. Smeets, B. F. Sels, P. A. Jacombs, R. A. Schoonheydt, J. Am. Chem. Soc. 2005, 127, 1394–1395.PubMedGoogle Scholar
  82. 82.
    P. J. Smeets, R. G. Hadt, J. S. Woertink, P. Vanelderen, R. A. Schoonheydt, B. F. Sels, E. I. Solomon, J. Am. Chem. Soc. 2010, 132, 14736–14738.PubMedPubMedCentralGoogle Scholar
  83. 83.
    J. S. Woertink, P. J. Smeets, M. H. Groothaert, M. A. Vance, B. F. Sels, R. A. Schoonheydt, E. I. Solomon, Proc. Natl. Acad. Sci. USA 2009, 106, 18908–18913.PubMedPubMedCentralGoogle Scholar
  84. 84.
    P. Vanelderen, R. G. Hadt, P. J. Smeets, E. I. Solomon, R. A. Schoonheydt, B. F. Sels, J. Catal. 2011, 284, 157–164.PubMedPubMedCentralGoogle Scholar
  85. 85.
    B. Wilkinson, M. Zhu, N. D. Priestley, H. H. T. Nguyen, H. Morimoto, P. G. Williams, S. I. Chan, H. G. Floss, J. Am. Chem. Soc. 1996, 118, 921–922.Google Scholar
  86. 86.
    S. S. F. Yu, L. Y. Wu, K. H. C. Chen, W. I. Luo, D. S. Huang, S. I. Chan, J. Biol. Chem. 2003, 278, 40658–40669.PubMedGoogle Scholar
  87. 87.
    R. Csaki, L. Bodrossy, J. Klem, J. C. Murrell, K. L. Kovacs, Microbiology 2003, 149, 1785–1795.PubMedGoogle Scholar
  88. 88.
    T. Nakamura, T. Hoaki, S. Hanada, A. Maruyama, Y. Kamagata, H. Fuse, FEMS Microbiol. Lett. 2007, 277, 157–164.PubMedGoogle Scholar
  89. 89.
    G. P. Stafford, J. Scanlan, I. R. McDonald, J. C. Murrell, Microbiology 2003, 149, 1771–1784.PubMedGoogle Scholar
  90. 90.
    A. R. Theisen, M. H. Ali, S. Radajewski, M. G. Dumont, P. F. Dunfield, I. R. McDonald, S. N. Dedysh, C. B. Miguez, J. C. Murrell, Mol. Microbiol. 2005, 58, 682–692.PubMedGoogle Scholar
  91. 91.
    M. Merkx, S. J. Lippard, J. Biol. Chem. 2002, 277, 5858–5865.PubMedGoogle Scholar
  92. 92.
    M. H. Sazinsky, M. Merkx, E. Cadieux, S. Y. Tang, S. J. Lippard, Biochemistry 2004, 43, 16263–16276.PubMedGoogle Scholar
  93. 93.
    V. Izzo, G. Leo, R. Scognamiglio, L. Troncone, L. Birolo, A. Di Donato, Arch. Biochem. Biophys. 2011, 505, 48–59.PubMedGoogle Scholar
  94. 94.
    U. E. Ukaegbu, S. Henery, A. C. Rosenzweig, Biochemistry 2006, 45, 10191–10198.PubMedGoogle Scholar
  95. 95.
    U. E. Ukaegbu, A. C. Rosenzweig, Biochemistry 2009, 48, 2207–2215.PubMedPubMedCentralGoogle Scholar
  96. 96.
    J. Scanlan, M. G. Dumont, J. C. Murrell, FEMS Microbiol. Lett. 2009, 301, 181–187.PubMedGoogle Scholar
  97. 97.
    V. Cafaro, V. Izzo, R. Scognamiglio, E. Notomista, P. Capasso, A. Casbarra, P. Pucci, A. Di Donato, Appl. Environ. Microbiol. 2004, 70, 2211–2219.PubMedPubMedCentralGoogle Scholar
  98. 98.
    J. D. Pikus, J. M. Studts, C. Achim, K. E. Kauffmann, E. Münck, R. J. Steffan, K. McClay, B. G. Fox, Biochemistry 1996, 35, 9106–9119.PubMedGoogle Scholar
  99. 99.
    V. Cafaro, R. Scognamiglio, A. Viggiani, V. Izzo, I. Passaro, E. Notomista, F. D. Piaz, A. Amoresano, A. Casbarra, P. Pucci, A. Di Donato, Eur. J. Biochem. 2002, 269, 5689–5699.PubMedGoogle Scholar
  100. 100.
    J. G. Leahy, P. J. Batchelor, S. M. Morcomb, FEMS Microbiol. Rev. 2003, 27, 449–479.PubMedGoogle Scholar
  101. 101.
    E. Notomista, A. Lahm, A. Di Donato, A. Tramontano, J. Mol. Evol. 2003, 56, 435–445.PubMedGoogle Scholar
  102. 102.
    M. H. Sazinsky, J. Bard, A. Di Donato, S. J. Lippard, J. Biol. Chem. 2004, 279, 30600–30610.PubMedGoogle Scholar
  103. 103.
    M. H. Sazinsky, P. W. Dunten, M. S. McCormick, A. DiDonato, S. J. Lippard, Biochemistry 2006, 45, 15392–15404.PubMedPubMedCentralGoogle Scholar
  104. 104.
    L. J. Bailey, J. G. Mccoy, G. N. Phillips, B. G. Fox, Proc. Natl. Acad. Sci. USA 2008, 105, 19194–19198.PubMedPubMedCentralGoogle Scholar
  105. 105.
    B. L. Dubbels, L. A. Sayavedra-Soto, D. J. Arp, Microbiology 2007, 153, 1808–1816.PubMedGoogle Scholar
  106. 106.
    N. Elango, R. Radhakrishnan, W. A. Froland, B. J. Wallar, C. A. Earhart, J. D. Lipscomb, D. H. Ohlendorf, Protein Sci. 1997, 6, 556–568.PubMedPubMedCentralGoogle Scholar
  107. 107.
    A. C. Rosenzweig, C. A. Frederick, S. J. Lippard, P. Nordlund, Nature 1993, 366, 537–543.PubMedGoogle Scholar
  108. 108.
    S. J. Lee, M. S. McCormick, S. J. Lippard, U. S. Cho, Nature 2013, 494, 380–384.PubMedPubMedCentralGoogle Scholar
  109. 109.
    M. H. Sazinsky, S. J. Lippard, J. Am. Chem. Soc. 2005, 127, 5814–5825.PubMedGoogle Scholar
  110. 110.
    D. A. Whittington, A. C. Rosenzweig, C. A. Frederick, S. J. Lippard, Biochemistry 2001, 40, 3476–3482.PubMedGoogle Scholar
  111. 111.
    G. T. Gassner, S. J. Lippard, Biochemistry 1999, 38, 12768–12785.PubMedGoogle Scholar
  112. 112.
    L. L. Chatwood, J. Müller, J. D. Gross, G. Wagner, S. J. Lippard, Biochemistry 2004, 43, 11983–11991.PubMedGoogle Scholar
  113. 113.
    J. Müller, A. A. Lugovskoy, G. Wagner, S. J. Lippard, Biochemistry 2002, 41, 42–51.PubMedGoogle Scholar
  114. 114.
    J. L. Blazyk, G. T. Gassner, S. J. Lippard, J. Am. Chem. Soc. 2005, 127, 17364–17376.PubMedPubMedCentralGoogle Scholar
  115. 115.
    J. L. Blazyk, S. J. Lippard, Biochemistry 2002, 41, 15780–15794.PubMedGoogle Scholar
  116. 116.
    J. L. Blazyk, S. J. Lippard, J. Biol. Chem. 2004, 279, 5630–5640.PubMedGoogle Scholar
  117. 117.
    D. A. Kopp, G. T. Gassner, J. L. Blazyk, S. J. Lippard, Biochemistry 2001, 40, 14932–14941.PubMedGoogle Scholar
  118. 118.
    K. J. Walters, G. T. Gassner, S. J. Lippard, G. Wagner, Proc. Natl. Acad. Sci. USA 1999, 96, 7877–7882.PubMedPubMedCentralGoogle Scholar
  119. 119.
    S.-L. Chang, B. J. Wallar, J. D. Lipscomb, K. H. Mayo, Biochemistry 1999, 38, 5799–5812.PubMedGoogle Scholar
  120. 120.
    B. G. Fox, Y. Liu, J. E. Dege, J. D. Lipscomb, J. Biol. Chem. 1991, 266, 540–550.PubMedGoogle Scholar
  121. 121.
    Y. Liu, J. C. Nesheim, S. K. Lee, J. D. Lipscomb, J. Biol. Chem. 1995, 270, 24662–24665.PubMedGoogle Scholar
  122. 122.
    M. H. Sazinsky, S. J. Lippard, Accounts Chem. Res. 2006, 39, 558–566.Google Scholar
  123. 123.
    K. H. Mitchell, J. M. Studts, B. G. Fox, Biochemistry 2002, 41, 3176–3188.PubMedGoogle Scholar
  124. 124.
    E. Cadieux, V. Vrajmasu, C. Achim, J. Powlowski, E. Münck, Biochemistry 2002, 41, 10680–10691.PubMedGoogle Scholar
  125. 125.
    J. Kazlauskaite, H. A. O. Hill, P. C. Wilkins, H. Dalton, Eur. J. Biochem. 1996, 241, 552–556.PubMedGoogle Scholar
  126. 126.
    S. Chang, B. J. Wallar, J. D. Lipcomb, J. D. Mayo, Biochemistry 2001, 40, 9539–9551.PubMedGoogle Scholar
  127. 127.
    H. Brandstetter, D. A. Whittington, S. J. Lippard, C. A. Frederick, Chem. Biol. 1999, 6, 441–449.PubMedGoogle Scholar
  128. 128.
    J. Y. Zhang, J. D. Lipscomb, Biochemistry 2006, 45, 1459–1469.PubMedGoogle Scholar
  129. 129.
    A. C. Rosenzweig, P. Nordlund, P. M. Takahara, C. A. Frederick, S. J. Lippard, Chem. Biol. 1995, 2, 632.Google Scholar
  130. 130.
    D. A. Whittington, S. J. Lippard, J. Am. Chem. Soc. 2001, 123, 827–838.PubMedGoogle Scholar
  131. 131.
    M. P. Woodland, D. S. Patil, R. Cammack, H. Dalton, Biochim. Biophys. Acta. 1986, 873, 237–242.Google Scholar
  132. 132.
    J. G. Dewitt, J. G. Bentsen, A. C. Rosenzweig, B. Hedman, J. Green, S. Pilkington, G. C. Papaefthymiou, H. Dalton, K. O. Hodgson, S. J. Lippard, J. Am. Chem. Soc. 1991, 113, 9219–9235.Google Scholar
  133. 133.
    B. G. Fox, J. D. Lipscomb, Biochem. Biophys. Res. Comm. 1988, 154, 165–170.PubMedGoogle Scholar
  134. 134.
    B. G. Fox, K. K. Surerus, E. Münck, J. D. Lipscomb, J. Biol. Chem. 1988, 263, 10553–10556.PubMedGoogle Scholar
  135. 135.
    J. G. Dewitt, A. C. Rosenzweig, A. Salifoglou, B. Hedman, S. J. Lippard, K. O. Hodgson, Inorg. Chem. 1995, 34, 2505–2515.Google Scholar
  136. 136.
    B. G. Fox, M. P. Hendrich, K. K. Surerus, K. K. Andersson, W. A. Froland, J. D. Lipscomb, E. Münck, J. Am Chem. Soc. 1993, 115, 3688–3701.Google Scholar
  137. 137.
    M. P. Hendrich, E. Münck, B. G. Fox, J. D. Lipscomb, J. Am. Chem. Soc. 1990, 112, 5861–5865.Google Scholar
  138. 138.
    B. M. Hoffman, B. E. Sturgeon, P. E. Doan, V. J. DeRose, K. E. Liu, S. J. Lippard, J. Am. Chem. Soc. 1994, 116, 6023–6024.Google Scholar
  139. 139.
    D. A. Kopp, E. A. Berg, C. E. Costello, S. J. Lippard, J. Biol. Chem. 2003, 278, 20939–20945.PubMedGoogle Scholar
  140. 140.
    K. E. Liu, S. J. Lippard, J. Biol. Chem. 1991, 266, 12836–12839.PubMedGoogle Scholar
  141. 141.
    K. E. Liu, A. M. Valentine, D. L. Wang, B. H. Huynh, D. E. Edmondson, A. Salifoglou, S. J. Lippard, J. Am. Chem. Soc. 1995, 117, 10174–10185.Google Scholar
  142. 142.
    Y. Liu, J. C. Nesheim, K. E. Paulsen, M. T. Stankovich, J. D. Lipscomb, Biochemistry 1997, 36, 5223–5233.PubMedGoogle Scholar
  143. 143.
    K. E. Paulsen, Y. Liu, B. G. Fox, J. D. Lipscomb, E. Münck, M. T. Stankovich, Biochemistry 1994, 33, 713–722.PubMedGoogle Scholar
  144. 144.
    W. Wang, S. J. Lippard, J. Am. Chem. Soc. 2014, 136, 2244–2247.PubMedPubMedCentralGoogle Scholar
  145. 145.
    C. C. Page, C. C. Moser, P. L. Dutton, Curr. Opin. Chem. Biol. 2003, 7, 551–556.PubMedGoogle Scholar
  146. 146.
    L. Shu, Y. Lui, J. D. Lipscomb, L. J. Que, J. Biol. Inorg. Chem. 1996, 1, 297–304.Google Scholar
  147. 147.
    D. Jackson Rudd, M. H. Sazinsky, M. Merkx, S. J. Lippard, B. Hedman, K. O. Hodgson, Inorg. Chem. 2004, 43, 4579–4589.Google Scholar
  148. 148.
    R. Davydov, A. M. Valentine, S. Komar-Panicucci, B. M. Hoffman, S. J. Lippard, Biochemistry 1999, 38, 4188–4197.PubMedGoogle Scholar
  149. 149.
    S. C. Pulver, W. A. Froland, J. D. Lipscomb, E. I. Solomon, J. Am. Chem. Soc. 1997, 119, 387–395.Google Scholar
  150. 150.
    N. Mitic, J. K. Schwartz, B. J. Brazeau, J. D. Lipscomb, E. I. Solomon, Biochemistry 2008, 47, 8386–8397.PubMedPubMedCentralGoogle Scholar
  151. 151.
    W. A. Froland, K. K. Andersson, S. K. Lee, Y. Liu, J. D. Lipscomb, J. Biol. Chem. 1992, 267, 17588–17597.PubMedGoogle Scholar
  152. 152.
    J. D. Pikus, J. M. Studts, K. McClay, R. J. Steffan, B. G. Fox, Biochemistry 1997, 36, 9283–9289.PubMedGoogle Scholar
  153. 153.
    M. S. McCormick, M. H. Sazinsky, K. L. Condon, S. J. Lippard, J. Am. Chem. Soc. 2006, 128, 15108–15110.PubMedPubMedCentralGoogle Scholar
  154. 154.
    D. A. Whittington, M. H. Sazinsky, S. J. Lippard, J. Am. Chem. Soc. 2001, 123, 1794–1795.PubMedGoogle Scholar
  155. 155.
    A. C. Rosenzweig, H. Brandstetter, D. A. Whittington, P. Nordlund, S. J. Lippard, C. A. Frederick, Protein Struct. Funct. Genet. 1997, 29, 141–152.Google Scholar
  156. 156.
    B. J. Wallar, J. D. Lipscomb, Biochemistry 2001, 40, 2220–2233.PubMedGoogle Scholar
  157. 157.
    C. E. Tinberg, S. J. Lippard, Biochemistry 2009, 48, 12145–12158.PubMedPubMedCentralGoogle Scholar
  158. 158.
    S. Y. Lee, J. D. Lipscomb, Biochemistry 1999, 38, 4423–4432.PubMedGoogle Scholar
  159. 159.
    W. J. Song, M. S. McCormick, R. K. Behan, M. H. Sazinsky, W. Jiang, J. Lin, C. Krebs, S. J. Lippard, J. Am. Chem. Soc. 2010, 132, 13582–13585.PubMedPubMedCentralGoogle Scholar
  160. 160.
    J. D. Pikus, K. H. Mitchell, J. M. Studts, K. McClay, R. J. Steffan, B. G. Fox, Biochemistry 2000, 39, 791–799.PubMedGoogle Scholar
  161. 161.
    N. L. Elsen, L. J. Bailey, A. D. Hauser, B. G. Fox, Biochemistry 2009, 48, 3838–3846.PubMedGoogle Scholar
  162. 162.
    W. J. Song, R. K. Behan, S. G. Naik, B. H. Huynh, S. J. Lippard, J. Am. Chem. Soc. 2009, 131, 6074–6075.PubMedPubMedCentralGoogle Scholar
  163. 163.
    S. K. Lee, J. C. Nesheim, J. D. Lipscomb, J. Biol. Chem. 1993, 268, 21569–21577.PubMedGoogle Scholar
  164. 164.
    S. S. Stahl, W. A. Francisco, M. Merkx, J. P. Klinman, S. J. Lippard, J. Biol. Chem. 2001, 276, 4549–4553.PubMedGoogle Scholar
  165. 165.
    K. E. Liu, D. Wang, B. H. Huynh, D. E. Edmondson, A. Salifoglou, S. J. Lippard, J. Am. Chem. Soc. 1994, 116, 7465–7466.Google Scholar
  166. 166.
    L. J. Shu, J. C. Nesheim, K. Kauffmann, E. Münck, J. D. Lipscomb, L. Que, Science 1997, 275, 515–518.PubMedGoogle Scholar
  167. 167.
    A. M. Valentine, S. S. Stahl, S. J. Lippard, J. Am. Chem. Soc. 1999, 121, 3876–3887.Google Scholar
  168. 168.
    R. Banerjee, K. K. Meier, E. Münck, J. D. Lipcomb, Biochemistry 2013, 52, 4331–4342.PubMedPubMedCentralGoogle Scholar
  169. 169.
    B. J. Brazeau, J. D. Lipcomb, Biochemistry 2000, 39, 13503–13515.PubMedGoogle Scholar
  170. 170.
    D. Jahng, A. K. Sun, C. S. Kim, T. K. Wood, J. Cell. Biochem. 1995, 59, 44–44.Google Scholar
  171. 171.
    W. G. Han, L. Noodleman, Inorg. Chem. 2008, 47, 2975–2986.PubMedGoogle Scholar
  172. 172.
    A. D. Bochevarov, J. N. Li, W. J. Song, R. A. Friesner, S. J. Lippard, J. Am. Chem. Soc. 2011, 133, 7384–7397.PubMedPubMedCentralGoogle Scholar
  173. 173.
    L. J. Murray, R. Garcia-Serres, S. Naik, B. H. Huynh, S. J. Lippard, J. Am. Chem. Soc. 2006, 128, 7458–7459.PubMedPubMedCentralGoogle Scholar
  174. 174.
    L. J. Murray, S. J. Lippard, Accounts Chem. Res. 2007, 40, 466–474.Google Scholar
  175. 175.
    K. P. Jensen, C. B. Bell, III., M. D. Clay, E. I. Solomon, J. Am. Chem. Soc. 2009, 131, 12155–12171.Google Scholar
  176. 176.
    L. G. Beauvais, S. J. Lippard, J. Am. Chem. Soc. 2005, 127, 7370–7378.PubMedGoogle Scholar
  177. 177.
    C. E. Tinberg, S. J. Lippard, Biochemistry 2010, 49, 7902–7912.PubMedPubMedCentralGoogle Scholar
  178. 178.
    S.-K. Lee, B. G. Fox, W. A. Froland, J. D. Lipcomb, E. Münck, J. Am. Chem. Soc. 1993, 115, 6450–6451.Google Scholar
  179. 179.
    B. F. Gherman, M. H. Baik, S. J. Lippard, R. A. Friesner, J. Am. Chem. Soc. 2004, 126, 2978–2990.PubMedGoogle Scholar
  180. 180.
    D. Rinalde, D. M. Phillip, S. J. Lippard, R. A. Friesner, J. Am. Chem. Soc. 2007, 129, 3135–3147.Google Scholar
  181. 181.
    G. T. Rowe, E. V. Rybak-Akimova, J. P. Caradonna, Inorg. Chem. 2007, 46, 10594–10606.PubMedGoogle Scholar
  182. 182.
    G. Xue, R. De Hont, E. Münck, L. Que, Nature Chem. 2010, 2, 400–405.Google Scholar
  183. 183.
    G. Q. Xue, D. Wang, R. De Hont, A. T. Fiedler, X. P. Shan, E. Münck, L. Que, Proc. Natl. Acad. Sci. USA 2007, 104, 20713–20718.PubMedPubMedCentralGoogle Scholar
  184. 184.
    S. K. Smoukov, D. A. Kopp, A. M. Valentine, R. Davydov, S. J. Lippard, B. M. Hoffman, J. Am. Chem. Soc. 2002, 124, 2657–2663.PubMedGoogle Scholar
  185. 185.
    K. K. Andersson, T. E. Elgren, L. Que, J. D. Lipcomb, J. Am. Chem. Soc. 1992, 114, 8711–8713.Google Scholar
  186. 186.
    N. D. Priestley, H. G. Floss, W. A. Froland, J. D. Lipcomb, P. G. Williams, H. Morimoto, J. Am. Chem. Soc. 1992, 114, 7561–7562.Google Scholar
  187. 187.
    A. M. Valentine, B. Wilkinson, K. E. Liu, S. KomarPanicucci, N. D. Priestley, P. G. Williams, H. Morimoto, H. G. Floss, S. J. Lippard, J. Am. Chem. Soc. 1997, 119, 1818–1827.Google Scholar
  188. 188.
    T. J. Sears, P. M. Johnson, P. Jin, S. Oatis, J. Chem. Phys. 1996, 104, 781–792.Google Scholar
  189. 189.
    B. F. Gherman, B. D. Dunietz, D. A. Whittington, S. J. Lippard, R. A. Friesner, J. Am. Chem. Soc. 2001, 123, 3836–3837.PubMedGoogle Scholar
  190. 190.
    J. M. Bollinger, Jr., C. Krebs, A. Vicol, S. Chen, B. A. Ley, D. E. Edmondson, B. H. Huynh, J. Am. Chem. Soc. 1998, 120, 1094–1095.Google Scholar
  191. 191.
    P. Moënne-Loccoz, J. Baldwin, B. A. Ley, T. M. Loehr, J. M. Bollinger, Jr., Biochemistry 1998, 37, 14659–14663.PubMedGoogle Scholar
  192. 192.
    J. A. Broadwater, C. Achim, E. Münck, B. G. Fox, Biochemistry 1999, 38, 12197–12204.PubMedGoogle Scholar
  193. 193.
    J. A. Broadwater, J. Y. Ai, T. M. Loehr, J. Sanders-Loehr, B. G. Fox, Biochemistry 1998, 37, 14664–14671.PubMedGoogle Scholar
  194. 194.
    A. S. Pereira, W. Small, C. Krebs, P. Tavares, D. E. Edmondson, E. C. Theil, B. H. Huynh, Biochemistry 1998, 37, 9871–9876.PubMedGoogle Scholar
  195. 195.
    P. Moënne-Loccoz, C. Krebs, K. Herlihy, D. E. Edmondson, E. C. Theil, B. H. Huynh, T. M. Loehr, Biochemistry 1999, 38, 5290–5295.PubMedGoogle Scholar
  196. 196.
    V. V. Vu, J. P. Emerson, M. Martinho, Y. S. Kim, E. Münck, M. H. Park, L. J. Que, Proc. Natl. Acad. Sci. USA 2009, 106, 14814–14819.PubMedPubMedCentralGoogle Scholar
  197. 197.
    K. Kim, S. J. Lippard, J. Am. Chem. Soc. 1996, 118, 4914–4915.Google Scholar
  198. 198.
    X. Zhang, H. Furutachi, S. Fujinami, S. Nagatomo, Y. Maeda, Y. Watanabe, T. Kitagawa, M. Suzuki, J. Am. Chem. Soc. 2005, 127, 826–827.PubMedGoogle Scholar
  199. 199.
    Y. Dong, Y. Zhang, L. Shu, E. C. Wilkinson, L. Que, Jr., K. Kauffmann, E. Münck, J. Am. Chem. Soc. 1997, 119, 12683–12684.Google Scholar
  200. 200.
    Y. Dong, H. Fujii, M. P. Hendrich, R. A. Leising, G. Pan, C. R. Randall, E. C. Wilkinson, Y. Zang, L. Que, Jr., J. Am. Chem. Soc. 1995, 117, 2778–2792.Google Scholar
  201. 201.
    Y. Dong, L. Que, Jr., K. Kauffmann, E. Münck, J. Am. Chem. Soc. 1995, 117, 11377–11378.Google Scholar
  202. 202.
    H.-F. Hsu, Y. Dong, L. Shu, V. G. Young, Jr., L. Que, Jr., J. Am. Chem. Soc. 1999, 121, 5230–5237.Google Scholar
  203. 203.
    B. D. Dunietz, M. D. Beachy, Y. Cao, D. A. Whittington, S. J. Lippard, R. A. Friesner, J. Am. Chem. Soc. 2000, 122, 2828–2839.Google Scholar
  204. 204.
    W. Wang, R. E. Iacob, R. P. Luoh, J. R. Engen, S. J. Lippard, J. Am. Chem. Soc. 2014, 136, 9754–9762.Google Scholar
  205. 205.
    C. E. Tinberg, S. J. Lippard, Biochemistry 2010, 49, 7902–7912.PubMedPubMedCentralGoogle Scholar

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© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Department of ChemistryPomona CollegeClaremontUSA
  2. 2.Department of ChemistryMassachusetts Institute of TechnologyCambridgeUSA

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