JBIC Journal of Biological Inorganic Chemistry

, Volume 21, Issue 5–6, pp 619–644 | Cite as

Mono- and binuclear non-heme iron chemistry from a theoretical perspective

  • Tibor András Rokob
  • Jakub Chalupský
  • Daniel Bím
  • Prokopis C. Andrikopoulos
  • Martin Srnec
  • Lubomír Rulíšek
Minireview
Part of the following topical collections:
  1. E.I. Solomon: Papers in Celebration of His 2016 ACS Alfred Bader Award in Bioorganic or Bioinorganic Chemistry

Abstract

In this minireview, we provide an account of the current state-of-the-art developments in the area of mono- and binuclear non-heme enzymes (NHFe and NHFe2) and the smaller NHFe(2) synthetic models, mostly from a theoretical and computational perspective. The sheer complexity, and at the same time the beauty, of the NHFe(2) world represents a challenge for experimental as well as theoretical methods. We emphasize that the concerted progress on both theoretical and experimental side is a conditio sine qua non for future understanding, exploration and utilization of the NHFe(2) systems. After briefly discussing the current challenges and advances in the computational methodology, we review the recent spectroscopic and computational studies of NHFe(2) enzymatic and inorganic systems and highlight the correlations between various experimental data (spectroscopic, kinetic, thermodynamic, electrochemical) and computations. Throughout, we attempt to keep in mind the most fascinating and attractive phenomenon in the NHFe(2) chemistry, which is the fact that despite the strong oxidative power of many reactive intermediates, the NHFe(2) enzymes perform catalysis with high selectivity. We conclude with our personal viewpoint and hope that further developments in quantum chemistry and especially in the field of multireference wave function methods are needed to have a solid theoretical basis for the NHFe(2) studies, mostly by providing benchmarking and calibration of the computationally efficient and easy-to-use DFT methods.

Keywords

Non-heme iron Density functional theory Multireference methods Dioxygen activation Reactivity 

References

  1. 1.
    Williams RJP, Fraústo da Silva JJR (2000) Coord Chem Rev 200–202:247–348CrossRefGoogle Scholar
  2. 2.
    Poulos TL (2014) Chem Rev 114:3919–3962PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Zheng L, Cash VL, Flint DH, Dean DR (1998) J Biol Chem 273:13264–13272PubMedCrossRefGoogle Scholar
  4. 4.
    Broderick JB, Duffus BR, Duschene KS, Shepard EM (2014) Chem Rev 114:4229–4317PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Solomon EI, Brunold TC, Davis MI, Kemsley JN, Lee SK, Lehnert N, Neese F, Skulan AJ, Yang YS, Zhou J (2000) Chem Rev 100:235–350PubMedCrossRefGoogle Scholar
  6. 6.
    Solomon EI, Light KM, Liu LV, Srnec M, Wong SD (2013) Acc Chem Res 46:2725–2739PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Blomberg MRA, Borowski T, Himo F, Liao R-L, Siegbahn PEM (2014) Chem Rev 114:3601–3658PubMedCrossRefGoogle Scholar
  8. 8.
    Nam W (2007) Acc Chem Res 40:522–531PubMedCrossRefGoogle Scholar
  9. 9.
    Oloo WN, Que L Jr (2015) Acc Chem Res 48:2612–2621PubMedCrossRefGoogle Scholar
  10. 10.
    Friedle S, Reisner E, Lippard SJ (2010) Chem Soc Rev 39:2768–2779PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Liu LV, Hong S, Cho J, Nam W, Solomon EI (2013) J Am Chem Soc 135:3286–3299PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Swart M, Costas M (eds) (2016) Spin states in biochemistry and inorganic chemistry: influence on structure and reactivity. Wiley, UKGoogle Scholar
  13. 13.
    Johansson AJ, Blomberg MRA, Siegbahn PEM (2008) J Chem Phys 129:154301PubMedCrossRefGoogle Scholar
  14. 14.
    Rokob TA, Srnec M, Rulíšek L (2012) Dalton Trans 41:5754–5768PubMedCrossRefGoogle Scholar
  15. 15.
    Neese F (2009) Coord Chem Rev 253:526CrossRefGoogle Scholar
  16. 16.
    England J, Bigelow JO, Van Heuvelen KM, Farquhar ER, Martinho M, Meier KK, Frisch JR, Münck E, Que L Jr (2014) Chem Sci 5:1204–1215CrossRefPubMedGoogle Scholar
  17. 17.
    Light KM, Hangasky JA, Knapp MJ, Solomon EI (2013) J Am Chem Soc 135:9665PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Biswas AN, Puri M, Meier KK, Oloo WN, Rohde GT, Bominaar EL, Münck E, Que L Jr (2015) J Am Chem Soc 137:2428PubMedCrossRefGoogle Scholar
  19. 19.
    Bochevarov AD, Li J, Song WJ, Friesner RA, Lippard SJ (2011) J Am Chem Soc 133:7384–7397PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Bonnot F, Molle T, Ménage S, Moreau Y, Duval S, Favaudon V, Levin-Houée C, Nivière V (2012) J Am Chem Soc 134:5120PubMedCrossRefGoogle Scholar
  21. 21.
    Diebold AR, Straganz GD, Solomon EI (2011) J Am Chem Soc 133:15979–15991PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Jayapal P, Ansari A, Rajaraman G (2015) Inorg Chem 54:11077PubMedCrossRefGoogle Scholar
  23. 23.
    Srnec M, Rokob TA, Schwartz JK, Kwak Y, Rulíšek L, Solomon EI (2012) Inorg Chem 51:2806PubMedCrossRefGoogle Scholar
  24. 24.
    Chachiyo T, Rodriguez JH (2012) Dalton Trans 41:995PubMedCrossRefGoogle Scholar
  25. 25.
    Harris TV, Morokuma K (2013) Inorg Chem 52:8551PubMedCrossRefGoogle Scholar
  26. 26.
    Kwak Y, Jiang W, Dassama LMK, Park K, Bell CB III, Liu LV, Wong SD, Saito M, Kobayashi Y, Kitao S, Seto M, Yoda Y, Alp EE, Zhao J, Bollinger JM Jr, Krebs C, Solomon EI (2013) J Am Chem Soc 135:17573PubMedCrossRefGoogle Scholar
  27. 27.
    Hirao H, Morokuma K (2010) J Phys Chem Lett 1:901CrossRefGoogle Scholar
  28. 28.
    Wörsdörfer B, Conner DA, Yokoyama K, Livada J, Seyedsayamdost M, Jiang W, Silakov A, Stubbe J, Bollinger JM Jr, Krebs C (2013) J Am Chem Soc 135:8585PubMedCrossRefGoogle Scholar
  29. 29.
    Light KM, Yamanaka Y, Odaka M, Solomon EI (2015) Chem Sci 6:6280PubMedCrossRefGoogle Scholar
  30. 30.
    Diebold AR, Brown-Marshall CD, Neidig ML, Brownlee JM, Moran GR, Solomon EI (2011) J Am Chem Soc 133:18148–18160PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    McQuilken AC, Ha Y, Sutherlin KD, Siegler MA, Hodgson KO, Hedman B, Solomon EI, Jameson GNL, Goldberg DP (2013) J Am Chem Soc 135:14024PubMedCrossRefGoogle Scholar
  32. 32.
    Gutman CT, Guzei IA, Brunold TC (2013) Inorg Chem 52:8909PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Sandala GM, Hopmann KH, Ghosh A, Noodleman L (2011) J Chem Theory Comput 7:3232PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Pápai M, Vankó G (2013) J Chem Theory Comput 9:5004PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Borgogno A, Rastrelli F, Bagno A (2015) Chem Eur J 21:12960PubMedCrossRefGoogle Scholar
  36. 36.
    Roemelt M, Maganas D, DeBeer S, Neese F (2013) J Chem Phys 138:204101PubMedCrossRefGoogle Scholar
  37. 37.
    Pollock CJ, Debeer S (2011) J Am Chem Soc 133:5594PubMedCrossRefGoogle Scholar
  38. 38.
    Chandrasekaran P, Stieber SCE, Collins TJ, Que L Jr, Neese F, DeBeer S (2011) Dalt Trans 40:11070CrossRefGoogle Scholar
  39. 39.
    Lee N, Petrenko T, Bergmann U, Neese F, Debeer S (2010) J Am Chem Soc 132:9715PubMedCrossRefGoogle Scholar
  40. 40.
    Sun N, Liu LV, Dey A, Villar-Acevedo G, Kovacs JA, Darensbourg MY, Hodgson KO, Hedman B, Solomon EI (2011) Inorg Chem 50:427PubMedCrossRefGoogle Scholar
  41. 41.
    Sun N, Dey A, Xiao Z, Wedd AG, Hodgson KO, Hedman B, Solomon EI (2010) J Am Chem Soc 132:12639PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Park K, Bell CB III, Liu LV, Wang D, Xue G, Kwak Y, Wong SD, Light KM, Zhao J, Alp EE, Yoda Y, Saito M, Kobayashi Y, Ohta T, Seto M, Que L Jr, Solomon EI (2013) Proc Natl Acad Sci 110:6275PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Park K, Tsugawa T, Furutachi H, Kwak Y, Liu LV, Wong SD, Yoda Y, Kobayashi Y, Saito M, Kurokuzu M, Seto M, Suzuki M, Solomon EI (2013) Angew Chem Int Ed 52:1294CrossRefGoogle Scholar
  44. 44.
    Wong SD, Srnec M, Matthews ML, Liu LV, Kwak Y, Park K, Bell CB III, Alp EE, Zhao J, Yoda Y, Kitao S, Seto M, Krebs C, Bollinger JM Jr, Solomon EI (2013) Nature 499:320–323PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Liu LV, Bell CB III, Wong SD, Wilson SA, Kwak Y, Chow MS, Zhao J, Hodgson KO, Hedman B, Solomon EI (2010) Proc Natl Acad Sci 107:22419–22424PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Wong SD, Bell CB III, Liu LV, Kwak Y, England J, Alp EE, Zhao J, Que L Jr, Solomon EI (2011) Angew Chem Int Ed 50:3215CrossRefGoogle Scholar
  47. 47.
    Park K, Solomon EI (2014) Can J Chem 92:975CrossRefGoogle Scholar
  48. 48.
    Han WG, Noodleman L (2010) Theor Chem Acc 125:305PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Taylor PR (1992) In: Roos BO (ed) Lecture notes in quantum chemistry, vol 58. Springer, BerlinGoogle Scholar
  50. 50.
    Hampel C, Werner HJ (1996) J Chem Phys 104:6286–6297CrossRefGoogle Scholar
  51. 51.
    Neese F, Wennmohs F, Hansen A (2009) J Chem Phys 130:18CrossRefGoogle Scholar
  52. 52.
    Eriksen JJ, Baudin P, Ettenhuber P, Kristensen K, Kjærgaard T, Jørgensen P (2015) J Chem Theory Comput 11:2984–2993PubMedCrossRefGoogle Scholar
  53. 53.
    Dieterich JM, Werner HJ, Mata RA, Metz S, Thiel W (2010) J Chem Phys 132:035101PubMedCrossRefGoogle Scholar
  54. 54.
    Neese F, Hansen A, Liakos DG (2009) J Chem Phys 131:064103PubMedCrossRefGoogle Scholar
  55. 55.
    Kowalski K, Piecuch P (2000) J Chem Phys 113:5644–5652CrossRefGoogle Scholar
  56. 56.
    Cramer CJ, Włoch M, Piecuch P, Puzzarini C, Gagliardi L (2006) J Phys Chem A 110:1991–2004PubMedCrossRefGoogle Scholar
  57. 57.
    Roos BO, Veryazov V, Conradie J, Taylor PR, Ghosh A (2008) J Phys Chem B 112:14099–14102CrossRefPubMedGoogle Scholar
  58. 58.
    Chen H, Ikeda-Saito M, Shaik S (2008) J Am Chem Soc 130:14778–14790PubMedCrossRefGoogle Scholar
  59. 59.
    Nemukhin AV, Grigorenko BL, Topol IA, Burt SK (2006) Int J Quantum Chem 106:2184–2190CrossRefGoogle Scholar
  60. 60.
    Malmqvist P-Å, Pierloot K, Shahi ARM, Cramer CJ, Gagliardi L (2008) J Chem Phys 128:204109PubMedCrossRefGoogle Scholar
  61. 61.
    Fleig T, Olsen J, Visscher L (2003) J Chem Phys 119:2963–2971CrossRefGoogle Scholar
  62. 62.
    Ma D, Li Manni G, Gagliardi L (2011) J Chem Phys 135:044128Google Scholar
  63. 63.
    White SR (1992) Phys Rev Lett 69:2863–2866PubMedCrossRefGoogle Scholar
  64. 64.
    Legeza Ö, Noack R, Sólyom J, Tincani L (2008) In: Fehske H, Schneider R, Weibe A (eds) Computational many-particle physics, vol 739., Lecture notes in physics, Springer, BerlinCrossRefGoogle Scholar
  65. 65.
    Marti KH, Reiher M (2010) Z Phys Chem 224:583–599CrossRefGoogle Scholar
  66. 66.
    Chan GKL, Sharma S (2011) Annu Rev Phys Chem 62:465–481PubMedCrossRefGoogle Scholar
  67. 67.
    Kurashige Y (2014) Mol Phys 112:1485–1494CrossRefGoogle Scholar
  68. 68.
    Yanai T, Kurashige Y, Mizukami W, Chalupský J, Lan TN, Saitow M (2015) Int J Quantum Chem 115:283–299CrossRefGoogle Scholar
  69. 69.
    Kurashige Y, Chan GKL, Yanai T (2013) Nat Chem 5:660–666PubMedCrossRefGoogle Scholar
  70. 70.
    Sharma S, Sivalingam K, Neese F, Chan GKL (2014) Nature Chem 6:927–933CrossRefGoogle Scholar
  71. 71.
    Stein CJ, Reiher M (2016) arXiv:1602.03835 [physics.chem-ph]
  72. 72.
    Neuscamman E, Yanai T, Chan GKL (2010) J Chem Phys 132:024106PubMedCrossRefGoogle Scholar
  73. 73.
    Kurashige Y, Chalupský J, Lan TN, Yanai T (2014) J Chem Phys 141:174111PubMedCrossRefGoogle Scholar
  74. 74.
    Yanai T, Kurashige Y, Neuscamman E, Chan GKL (2010) J Chem Phys 132:024105PubMedCrossRefGoogle Scholar
  75. 75.
    Saitow M, Kurashige Y, Yanai T (2013) J Chem Phys 139:044118PubMedCrossRefGoogle Scholar
  76. 76.
    Saitow M, Kurashige Y, Yanai T (2015) J Chem Theory Comput 11:5120–5131PubMedCrossRefGoogle Scholar
  77. 77.
    Miralles J, Castell O, Caballol R, Malrieu JP (1993) Chem Phys 172:33–43CrossRefGoogle Scholar
  78. 78.
    Neese F (2003) J Chem Phys 119:9428–9443CrossRefGoogle Scholar
  79. 79.
    Pierloot K (2001) In: Cundari TR (ed) Computational organometallic chemistry. Marcel Dekker, New YorkGoogle Scholar
  80. 80.
    Ghigo G, Roos BO, Malmqvist PA (2004) Chem Phys Lett 396:142–149CrossRefGoogle Scholar
  81. 81.
    Srnec M, Wong SD, England J, Que L Jr, Solomon EI (2012) Proc Natl Acad Sci 109:14326–14331PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Delcey MG, Pierloot K, Phung QM, Vancoillie S, Lindh R, Ryde U (2014) Phys Chem Chem Phys 16:7927–7938PubMedCrossRefGoogle Scholar
  83. 83.
    Radoń M, Broclawik E, Pierloot K (2010) J Phys Chem B 114:1518–1528PubMedCrossRefGoogle Scholar
  84. 84.
    Ye S, Xue G, Krivokapic I, Petrenko T, Bill E, Que L Jr, Neese F (2015) Chem Sci 6:2909–2921PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Chalupský J, Rokob TA, Kurashige Y, Yanai T, Solomon EI, Rulíšek L, Srnec M (2014) J Am Chem Soc 136:15977–15991PubMedCrossRefGoogle Scholar
  86. 86.
    Neese F (2006) J Am Chem Soc 128:10213–10222PubMedCrossRefGoogle Scholar
  87. 87.
    Neese F (2004) J Phys Chem Solids 65:781–785CrossRefGoogle Scholar
  88. 88.
    Andrikopoulos PC, Michel C, Chouzier S, Sautet P (2015) ACS Catal 5:2490–2499CrossRefGoogle Scholar
  89. 89.
    Bím D, Rulíšek L, Srnec M (2016) J Phys Chem Lett 7:7–13PubMedCrossRefGoogle Scholar
  90. 90.
    Light KM, Hangasky JA, Knapp MJ, Solomon EI (2014) Dalton Trans 43:1505–1508PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Cortopassi WA, Simion R, Honsby CE, França TCC, Paton RS (2015) Chem Eur J 21:18983–18992PubMedCrossRefGoogle Scholar
  92. 92.
    Ma G, Zhu W, Su H, Cheng N, Liu Y (2015) ACS Catal 5:5556–5566CrossRefGoogle Scholar
  93. 93.
    Quesne MG, Latifi R, Gonzalez-Ovalle LE, Kumar D, de Visser SP (2014) Chem Eur J 20:435–446PubMedCrossRefGoogle Scholar
  94. 94.
    Ye S, Riplinger C, Hansen A, Krebs C, Bollinger JM, Neese F (2012) Chem Eur J 18:6555–6567PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Meier KK, Rogers MS, Kovaleva EG, Mbughuni MM, Bominaar EL, Lipscomb JD, Münck E (2015) Inorg Chem 54:10269–10280PubMedCrossRefGoogle Scholar
  96. 96.
    Dong G, Lai W (2014) J Phys Chem B 118:1791–1798PubMedCrossRefGoogle Scholar
  97. 97.
    Dong G, Shaik S, Lai W (2013) Chem Sci 4:3624–3635CrossRefGoogle Scholar
  98. 98.
    Christian GJ, Ye S, Neese F (2012) Chem Sci 3:1600–1611CrossRefGoogle Scholar
  99. 99.
    Brkić H, Kovačević B, Tomić S (2015) Mol BioSyst 11:898–907PubMedCrossRefGoogle Scholar
  100. 100.
    Borowski T, Wójcik A, Miłaczewska A, Georgiev V, Blomberg MRA, Siegbahn PEM (2012) J Biol Inorg Chem 17:881–890PubMedCrossRefGoogle Scholar
  101. 101.
    Borowski T, Georgiev V, Siegbahn PEM (2010) J Mol Model 16:1673–1677PubMedCrossRefGoogle Scholar
  102. 102.
    Roy S, Kästner J (2016) Angew Chem Int Ed 55:1168–1172CrossRefGoogle Scholar
  103. 103.
    Jastrzebski R, Quesne MG, Weckhuysen BM, de Visser SP, Bruijnincx PCA (2014) Chem Eur J 20:15686–15691PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Georgiev V, Noack H, Borowski T, Blomberg MRA, Siegbahn PEM (2010) J Phys Chem B 114:5878–5885PubMedCrossRefGoogle Scholar
  105. 105.
    Wójcik A, Borowski T, Broclawik E (2011) Catal Today 169:207–216CrossRefGoogle Scholar
  106. 106.
    Attia AAAA, Cioloboc D, Lupan A, Silaghi-Dumitrescu R (2013) J Biol Inorg Chem 18:95–101PubMedCrossRefGoogle Scholar
  107. 107.
    Surawatanawong P, Tye JW, Hall MB (2010) Inorg Chem 49:188–192PubMedCrossRefGoogle Scholar
  108. 108.
    Dey A, Solomon EI (2010) Inorg Chim Acta 363:2762–2767CrossRefGoogle Scholar
  109. 109.
    Tremey E, Bonnot F, Moreau Y, Berthomieu C, Desbois A, Favaudon V, Blondin G, Houée-Levin C, Nivière V (2013) J Biol Inorg Chem 18:815–830PubMedCrossRefGoogle Scholar
  110. 110.
    Sit PH-L, Migliore A, Ho M-H, Klein ML (2010) J Chem Theory Comput 6:2896–2909Google Scholar
  111. 111.
    Kumar D, Thiel W, De Visser SP (2011) J Am Chem Soc 133:3869–3882PubMedCrossRefGoogle Scholar
  112. 112.
    Kumar D, Sastry GN, Goldberg DP, De Visser SP (2012) J Phys Chem A 116:582–591PubMedCrossRefGoogle Scholar
  113. 113.
    Che X, Gao J, Zhang D, Liu C (2012) J Phys Chem A 116:5510–5517PubMedCrossRefGoogle Scholar
  114. 114.
    Blaesi EJ, Gardner JD, Fox BG, Brunold TC (2013) Biochemistry 52:6040–6051PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Che X, Gao J, Liu Y, Liu C (2013) J Inorg Biochem 122:1–7PubMedCrossRefGoogle Scholar
  116. 116.
    Olsson E, Martinez A, Teigen K, Jensen VR (2011) Chem Eur J 17:3746–3758PubMedCrossRefGoogle Scholar
  117. 117.
    Haahr LT, Jensen KP, Boesen J, Christensen HEM (2010) J Inorg Biochem 104:136–145PubMedCrossRefGoogle Scholar
  118. 118.
    Olsson E, Martinez A, Teigen K, Jensen VR (2010) Eur J Inorg Chem 3:351–356CrossRefGoogle Scholar
  119. 119.
    Du L, Gao J, Liu Y, Liu C (2012) J Phys Chem B 116:11837–11844PubMedCrossRefGoogle Scholar
  120. 120.
    Hirao H, Morokuma K (2010) J Am Chem Soc 132:17901–17909PubMedCrossRefGoogle Scholar
  121. 121.
    Borowski T, Brocławik E (2003) J Phys Chem B 107:4639CrossRefGoogle Scholar
  122. 122.
    Bushnell EAC, Jamil R, Gauld JW (2013) J Biol Inorg Chem 18:343–355PubMedCrossRefGoogle Scholar
  123. 123.
    Kawatsu T, Lundberg M, Morokuma K (2011) J Chem Theory Comput 7:390–401PubMedCrossRefGoogle Scholar
  124. 124.
    Miłaczewska A, Broclawik E, Borowski T (2013) Chem Eur J 19:771–781PubMedCrossRefGoogle Scholar
  125. 125.
    Wang C, Chang W-C, Guo Y, Huang H, Peck SC, Pandelia ME, Lin G, Liu H-W, Krebs C, Bollinger JM Jr (2013) Science 342:991–995PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Hirao H (2011) J Phys Chem B 115:11278–11285PubMedCrossRefGoogle Scholar
  127. 127.
    Roos K, Siegbahn PEM (2011) J Biol Inorg Chem 16:553–565PubMedCrossRefGoogle Scholar
  128. 128.
    Oloo WN, Meier KK, Wang Y, Shaik S, Münck E, Que L Jr (2014) Nat Commun 5:3046PubMedCrossRefGoogle Scholar
  129. 129.
    Wang Y, Janardanan D, Usharani D, Han K, Que L Jr, Shaik S (2013) ACS Catal 3:1334–1341CrossRefGoogle Scholar
  130. 130.
    Prat I, Company A, Postils V, Ribas X, Que L Jr, Luis JM, Costas M (2013) Chem Eur J 19:6724–6738PubMedCrossRefGoogle Scholar
  131. 131.
    Kim YM, Cho KB, Cho J, Wang B, Li C, Shaik S, Nam W (2013) J Am Chem Soc 135:8838–8841PubMedCrossRefGoogle Scholar
  132. 132.
    Chen H, Cho KB, Lai W, Nam W, Shaik S (2012) J Chem Theory Comput 8:915–926PubMedCrossRefGoogle Scholar
  133. 133.
    Petit AS, Pennifold RCR, Harvey JN (2014) Inorg Chem 53:6473–6481PubMedCrossRefGoogle Scholar
  134. 134.
    Hirao H, Li F, Que L Jr, Morokuma K (2011) Inorg Chem 50:6637–6648PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Nam W (2015) Acc Chem Res 48:2415–2423PubMedCrossRefGoogle Scholar
  136. 136.
    McDonald AR, Que L Jr (2013) Coord Chem Rev 257:414–428CrossRefGoogle Scholar
  137. 137.
    Lundberg M, Borowski T (2013) Cood Chem Rev 257:277–289CrossRefGoogle Scholar
  138. 138.
    Shaik S, Hirao H, Kumar D (2007) Acc Chem Res 40:532–542PubMedCrossRefGoogle Scholar
  139. 139.
    Usharani D, Janardanan D, Li C, Shaik S (2013) Acc Chem Res 46:471–482PubMedCrossRefGoogle Scholar
  140. 140.
    Srnec M, Wong SD, Solomon EI (2014) Dalton Trans 43:17567–17577PubMedPubMedCentralCrossRefGoogle Scholar
  141. 141.
    Decker A, Rohde J-U, Klinker EJ, Wong SD, Que L Jr, Solomon EI (2007) J Am Chem Soc 129:15983–15996PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Ye S, Neese F (2011) Proc Natl Acad Sci 108:1228–1233PubMedPubMedCentralCrossRefGoogle Scholar
  143. 143.
    Krebs C, Fujimori DG, Walsh CT, Bollinger JM (2007) Acc Chem Res 40:484–492PubMedCrossRefGoogle Scholar
  144. 144.
    Neidig ML, Decker A, Choroba OW, Huang F, Kavana M, Moran GR, Spencer JB, Solomon EI (2006) Proc Natl Acad Sci 103:12966–12973PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Srnec M, Wong SD, Matthews ML, Krebs C, Bollinger M Jr, Solomon EI (2016) J Am Chem Soc 138:5110–5122PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Wilson SA, Chen J, Hong S, Lee Y-M, Clémancey M, Garcia-Serres R, Nomura T, Ogura T, Latour J-M, Hedman B, Hodgson KO, Nam W, Solomon EI (2012) J Am Chem Soc 134:11791–11806PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Grapperhaus CA, Mienert B, Bill E, Weyhermüller T, Wieghardt K (2000) Inorg Chem 39:5306–5317PubMedCrossRefGoogle Scholar
  148. 148.
    Rohde J-U, In J-H, Lim MH, Brennessel WW, Bukowski MR, Stubna A, Münck E, Nam W, Que L Jr (2003) Science 299:1037–1039Google Scholar
  149. 149.
    Buda F, Ensing B, Gribnau MCM, Baerends EJ (2003) Chem Eur J 9:3436–3444PubMedCrossRefGoogle Scholar
  150. 150.
    Bernasconi L, Louwerse MJ, Baerends EJ (2007) Eur J Inorg Chem 19:3023–3033CrossRefGoogle Scholar
  151. 151.
    Michel C, Baerends EJ (2009) Inorg Chem 48:3628–3638PubMedCrossRefGoogle Scholar
  152. 152.
    England J, Prakash J, Cranswick MA, Mandal D, Guo Y, Münck E, Shaik S, Que L Jr (2015) Inorg Chem 54:7828–7839PubMedCrossRefGoogle Scholar
  153. 153.
    Mitra M, Nimir H, Demeshko S, Bhat SS, Malinkin SO, Haukka M, Lloret-Fillol J, Lisensky GC, Meyer F, Shteinman AA, Browne WR, Hrovat DA, Richmond MG, Costas M, Nordlander E (2015) Inorg Chem 54:7152–7164PubMedCrossRefGoogle Scholar
  154. 154.
    Mayer JM (1998) Acc Chem Res 31:441–450CrossRefGoogle Scholar
  155. 155.
    de Visser SP (2010) J Am Chem Soc 132:1087–1097PubMedCrossRefGoogle Scholar
  156. 156.
    Saouma CT, Mayer JM (2014) Chem Sci 5:21–31CrossRefGoogle Scholar
  157. 157.
    Karlsson A, Parales JV, Parales RE, Gibson DT, Eklund H, Ramaswamy S (2003) Science 299:1039–1042PubMedCrossRefGoogle Scholar
  158. 158.
    Neibergall MB, Stubna A, Mekmouche Y, Münck E, Lipscomb JD (2007) Biochemistry 46:8004–8016PubMedPubMedCentralCrossRefGoogle Scholar
  159. 159.
    Chow MS, Liu LV, Solomon EI (2008) Proc Natl Acad Sci 105:13241–13245PubMedPubMedCentralCrossRefGoogle Scholar
  160. 160.
    Chakrabarty S, Austin RN, Deng DY, Groves JT, Lipscomb JD (2007) J Am Chem Soc 129:3514–3515PubMedPubMedCentralCrossRefGoogle Scholar
  161. 161.
    Ferraro DJ, Gakhar L, Ramaswamy S (2005) Biochem Biophys Res Commun 338:175–190PubMedCrossRefGoogle Scholar
  162. 162.
    Brown CD, Neidig ML, Neibergall MB, Lipscomb JD, Solomon EI (2007) J Am Chem Soc 129:7427–7438PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    Zhu H, Peck SC, Bonnot F, van der Donk WA, Klinman JP (2015) J Am Chem Soc 137:10448–10451PubMedPubMedCentralCrossRefGoogle Scholar
  164. 164.
    Mbughuni MM, Chakrabarti M, Hayden JA, Bominaar EL, Hendrich MP, Münck E, Lipscomb JD (2010) Proc Natl Acad Sci 107:16788–16793PubMedPubMedCentralCrossRefGoogle Scholar
  165. 165.
    Hong S, Sutherlin KD, Park J, Kwon E, Siegler MA, Solomon EI, Nam W (2014) Nat Commun 5:5440PubMedPubMedCentralCrossRefGoogle Scholar
  166. 166.
    Blaesi EJ, Fox BG, Brunold TC (2014) Biochemistry 53:5759–5770PubMedPubMedCentralCrossRefGoogle Scholar
  167. 167.
    Lundberg M, Kawatsu T, Vreven T, Frisch MJ, Morokuma K (2009) J Chem Theory Comput 5:222–234PubMedCrossRefGoogle Scholar
  168. 168.
    Hirao H, Morokuma K (2011) J Am Chem Soc 133:14550–14553PubMedCrossRefGoogle Scholar
  169. 169.
    Chung LW, Li X, Hirao H, Morokuma K (2011) J Am Chem Soc 133:20076–20079PubMedCrossRefGoogle Scholar
  170. 170.
    Sturgeon BE, Burdi D, Chen SX, Huynh BH, Edmondson DE, Stubbe J, Hoffman BM (1996) J Am Chem Soc 118:7551–7557CrossRefGoogle Scholar
  171. 171.
    Wörsdörfer B, Lingaraju M, Yennawar NH, Boal AK, Krebs C, Bollinger JM, Pandelia M-E (2013) Proc Natl Acad Sci 110:18874–18879PubMedPubMedCentralCrossRefGoogle Scholar
  172. 172.
    Xing G, Diao Y, Hoffart LM, Barr EW, Prabhu KS, Arner RJ, Reddy CC, Krebs C, Bollinger JM (2006) Proc Natl Acad Sci 103:6130–6135PubMedPubMedCentralCrossRefGoogle Scholar
  173. 173.
    Hirao H, Morokuma K (2009) J Am Chem Soc 131:17206–17214PubMedCrossRefGoogle Scholar
  174. 174.
    Sastri CV, Lee J, Oh K, Lee YJ, Lee J, Jackson TA, Ray K, Hirao H, Shin W, Halfen JA, Kim J, Que L Jr, Shaik S, Nam W (2007) Proc Natl Acad Sci 104:19181–19186PubMedPubMedCentralCrossRefGoogle Scholar
  175. 175.
    Lacy DC, Gupta R, Stone KL, Greaves J, Ziller JW, Hendrich MP, Borovik AS (2010) J Am Chem Soc 132:12188–12190PubMedPubMedCentralCrossRefGoogle Scholar
  176. 176.
    Kwon E, Cho K-B, Hong S, Nam W (2014) Chem Commun 50:5572–5575CrossRefGoogle Scholar
  177. 177.
    Ghosh M, Singh KK, Panda C, Weitz A, Hendrich MP, Collins TJ, Dhar BB, Gupta SS (2014) J Am Chem Soc 136:9524–9527PubMedCrossRefGoogle Scholar
  178. 178.
    Yosca TH, Rittle J, Krest CM, Onderko EL, Silakov A, Calixto JC, Behan RK, Green MT (2013) Science 342:825–8297PubMedPubMedCentralCrossRefGoogle Scholar
  179. 179.
    Usharani D, Lacy DC, Borovik AS, Shaik S (2013) J Am Chem Soc 135:17090–17104PubMedCrossRefGoogle Scholar
  180. 180.
    Hammes-Schiffer S, Stuchebrukhov AA (2010) Chem Rev 110:6939–6960PubMedPubMedCentralCrossRefGoogle Scholar
  181. 181.
    Hammes-Schiffer S (2015) J Am Chem Soc 137:8860–8871PubMedPubMedCentralCrossRefGoogle Scholar
  182. 182.
    Wang LP, Van Voorhis TA (2012) J Chem Theory Comput 8:610–617PubMedCrossRefGoogle Scholar
  183. 183.
    Li JL, Farrokhnia M, Rulíšek L, Ryde U (2015) J Phys Chem B 119:8268–8284PubMedCrossRefGoogle Scholar
  184. 184.
    Rulíšek L (2013) J Phys Chem C 117:16871–16877CrossRefGoogle Scholar
  185. 185.
    Riggs-Gelasco PJ, Price JC, Guyer RB, Brehm JH, Barr EW, Bollinger JM, Krebs C (2004) J Am Chem Soc 126:8108–8109PubMedCrossRefGoogle Scholar
  186. 186.
    Hoffart LM, Barr EW, Guyer RB, Bollinger JM, Krebs C (2006) Proc Natl Acad Sci 103:14738–14743PubMedPubMedCentralCrossRefGoogle Scholar
  187. 187.
    Karamzadeh B, Kumar D, Sastry GN, de Visser SP (2010) J Phys Chem A 114:13234–13243PubMedCrossRefGoogle Scholar
  188. 188.
    Mandal D, Ramanan R, Usharani D, Janardanan D, Wang B, Shaik S (2015) J Am Chem Soc 137:722–733PubMedCrossRefGoogle Scholar
  189. 189.
    Truong TN, Truhlar DG (1990) J Chem Phys 93:1761–1769CrossRefGoogle Scholar
  190. 190.
    Duncan WT, Bell RL, Troung TN (1998) J Comput Chem 19:1039–1052CrossRefGoogle Scholar
  191. 191.
    Layfield JP, Hammes-Schiffer S (2014) Chem Rev 114:3466–3494PubMedCrossRefGoogle Scholar
  192. 192.
    Meyer MP, Tomchick DR, Klinman JP (2008) Proc Natl Acad Sci 105:1146–1151PubMedPubMedCentralCrossRefGoogle Scholar
  193. 193.
    Hu S, Sharma SC, Scouras AD, Soudackov AV, Carr CAM, Hammes-Schiffer S, Alber T, Klinman JP (2014) J Am Chem Soc 136:8157–8160PubMedPubMedCentralCrossRefGoogle Scholar
  194. 194.
    Eser BE, Barr EW, Frantom PA, Saleh L, Bollinger JM Jr, Krebs C, Fitzpatrick PF (2007) J Am Chem Soc 129:11334–11335PubMedPubMedCentralCrossRefGoogle Scholar
  195. 195.
    Panay AJ, Lee M, Krebs C, Bollinger JM Jr, Fitzpatrick PF (2011) Biochemistry 50:1928–1933PubMedPubMedCentralCrossRefGoogle Scholar
  196. 196.
    Bassan A, Blomberg MRA, Siegbahn PEM (2003) Chem Eur J 9:106–115PubMedCrossRefGoogle Scholar
  197. 197.
    Moran GR, Derecskei-Kovacs A, Hillas PJ, Fitzpatrick PF (2000) J Am Chem Soc 122:4535–4541CrossRefGoogle Scholar
  198. 198.
    Borowski T, Bassan A, Siegbahn PEM (2004) Biochemistry 43:12331–12342PubMedCrossRefGoogle Scholar
  199. 199.
    Ye S, Wu X, Wei L, Tang D, Sun P, Bartlam M, Rao Z (2007) J Biol Chem 282:3391–3402PubMedCrossRefGoogle Scholar
  200. 200.
    Crawford JA, Li W, Pierce BS (2011) Biochemistry 50:10241–10253PubMedCrossRefGoogle Scholar
  201. 201.
    Cho KB, Shaik S, Nam W (2010) Chem Commun 46:4511–4513CrossRefGoogle Scholar
  202. 202.
    England J, Martinho M, Farquhar ER, Frisch JR, Bominaar EL, Münck E, Que L Jr (2009) Angew Chem Int Ed Engl 48:3622–3626PubMedPubMedCentralCrossRefGoogle Scholar
  203. 203.
    England J, Guo Y, Farquhar ER, Young VG Jr, Münck E, Que L Jr (2010) J Am Chem Soc 132:8635–8644PubMedPubMedCentralCrossRefGoogle Scholar
  204. 204.
    Bigi JP, Harman WH, Lassalle-Kaiser B, Robles DM, Stich TA, Yano J, Britt RD, Chang CJ (2012) J Am Chem Soc 134:1536–1542PubMedCrossRefGoogle Scholar
  205. 205.
    England J, Guo Y, Van Heuvelen KM, Cranswick MA, Rohde GT, Bominaar EL, Münck E, Que L Jr (2011) J Am Chem Soc 133:11880–11883PubMedPubMedCentralCrossRefGoogle Scholar
  206. 206.
    Wang D, Ray K, Collins MJ, Farquhar ER, Frisch JR, Gomez L, Jackson TA, Kerscher M, Waleska A, Comba P, Costas M, Que L Jr (2013) Chem Sci 4:282–291PubMedPubMedCentralCrossRefGoogle Scholar
  207. 207.
    Hong S, Lee Y-M, Cho K-B, Sundaravel K, Cho J, Kim MJ, Shin W, Nam W (2011) J Am Chem Soc 133:11876–11879PubMedCrossRefGoogle Scholar
  208. 208.
    Hong S, So H, Yoon H, Cho K-B, Lee Y-M, Fukuzumi S, Nam W (2013) Dalton Trans 42:7842–7845PubMedCrossRefGoogle Scholar
  209. 209.
    Fukuzumi S, Morimoto Y, Kotani H, Naumov P, Lee Y-M, Nam W (2010) Nat Chem 2:756–759PubMedCrossRefGoogle Scholar
  210. 210.
    Morimoto Y, Kotani H, Park J, Lee YM, Nam W, Fukuzumi S (2011) J Am Chem Soc 133:403–405PubMedCrossRefGoogle Scholar
  211. 211.
    Park J, Morimoto Y, Lee Y, Nam W, Fukuzumi S (2011) J Am Chem Soc 133:5236–5239PubMedCrossRefGoogle Scholar
  212. 212.
    Park J, Morimoto Y, Lee YM, Nam W, Fukuzumi S (2012) J Am Chem Soc 134:3903–3911PubMedCrossRefGoogle Scholar
  213. 213.
    Swart M (2013) Chem Commun 49:6650–6652CrossRefGoogle Scholar
  214. 214.
    Prakash J, Rohde GT, Meier KK, Jasniewski AJ, Van Hauvelen KM, Munck E, Que L Jr (2015) J Am Chem Soc 137:3478–3481PubMedPubMedCentralCrossRefGoogle Scholar
  215. 215.
    Widger LR, Davies CG, Yang T, Siegler MA, Troeppner O, Jameson GNL, Ivanović-Burmazović I, Goldberg DP (2014) J Am Chem Soc 136:2699–2702PubMedPubMedCentralCrossRefGoogle Scholar
  216. 216.
    Sahu S, Widger LR, Quesne MG, de Visser SP, Matsumura H, Moënne-Loccoz P, Siegler MA, Goldberg DP (2013) J Am Chem Soc 135:10590–10593PubMedPubMedCentralCrossRefGoogle Scholar
  217. 217.
    Bassan A, Blomberg MRA, Siegbahn PEM (2004) J Biol Inorg Chem 9:439–452PubMedCrossRefGoogle Scholar
  218. 218.
    Tarasev M, Ballou DP (2005) Biochemistry 44:6197–6207PubMedCrossRefGoogle Scholar
  219. 219.
    Que L Jr, Ho RYN (1996) Chem Rev 96:2607–2624PubMedCrossRefGoogle Scholar
  220. 220.
    Chen K, Que L Jr (1999) Chem Commun 15:1375–1376CrossRefGoogle Scholar
  221. 221.
    Chen K, Que L Jr (2001) J Am Chem Soc 123:6327–6337PubMedCrossRefGoogle Scholar
  222. 222.
    Ansari A, Kaushik A, Rajaraman G (2013) J Am Chem Soc 135:4235–4249PubMedCrossRefGoogle Scholar
  223. 223.
    Park MJ, Lee J, Sun Y, Kim J, Nam W (2006) J Am Chem Soc 128:2630–2634PubMedCrossRefGoogle Scholar
  224. 224.
    Seo MS, Kamachi T, Kuono T, Murata K, Park MJ, Yoshizawa K, Nam W (2007) Angew Chem Int Ed Engl 46:2291–2294PubMedCrossRefGoogle Scholar
  225. 225.
    Jiang Y, Telser J, Goldberg DP (2009) Chem Commun 6828–6830Google Scholar
  226. 226.
    Cho J, Jeon S, Wilson SA, Liu LV, Kang EA, Braymer JJ, Lim MH, Hedman B, Hodgson KO, Valentine JS, Solomon EI, Nam W (2011) Nature 478:502–505PubMedPubMedCentralCrossRefGoogle Scholar
  227. 227.
    Rat S, Ménage S, Thomas F, Nivière V (2014) Chem Commun 50:14213–14216CrossRefGoogle Scholar
  228. 228.
    Wójcik A, Broclawik E, Siegbahn PEM, Borowski T (2012) Biochemistry 51:9570–9580PubMedCrossRefGoogle Scholar
  229. 229.
    Wójcik A, Broclawik E, Siegbahn PEM, Lundberg M, Moran G, Borowski T (2014) J Am Chem Soc 136:14472–14485PubMedCrossRefGoogle Scholar
  230. 230.
    De Visser SP, Latifi R, Tahsini L, Nam W (2011) Chem Asian J 6:493–504PubMedCrossRefGoogle Scholar
  231. 231.
    Matthews ML, Neumann CS, Miles LA, Grove TL, Booker SJ, Krebs C, Walsh CT, Bollinger JM Jr (2009) Proc Natl Acad Sci 106:17723–17728PubMedPubMedCentralCrossRefGoogle Scholar
  232. 232.
    Borowski T, Noack H, Radoń M, Zych K, Siegbahn PEM (2010) J Am Chem Soc 132:12887–12898PubMedCrossRefGoogle Scholar
  233. 233.
    Martinie RJ, Livada J, Chang W, Green MT, Krebs C, Bollinger JM Jr, Silakov A (2015) J Am Chem Soc 137:6912–6919PubMedPubMedCentralCrossRefGoogle Scholar
  234. 234.
    Quesne MG, De Visser SP (2012) J Biol Inorg Chem 17:841–852PubMedCrossRefGoogle Scholar
  235. 235.
    Puri M, Biswas AN, Fan R, Guo Y, Que L Jr (2016) J Am Chem Soc 138:2484–2487PubMedCrossRefGoogle Scholar
  236. 236.
    Usharani D, Janardanan D, Shaik S (2011) J Am Chem Soc 133:176–179PubMedCrossRefGoogle Scholar
  237. 237.
    Ji L, Faponle AS, Quesne MG, Sainna MA, Zhang J, Franke A, Kumar D, van Eldik R, Liu W, de Visser SP (2015) Chem Eur J 21:9083–9092PubMedCrossRefGoogle Scholar
  238. 238.
    Brown-Marshall CD, Diebold AR, Solomon EI (2010) Biochemistry 49:1176–1182PubMedPubMedCentralCrossRefGoogle Scholar
  239. 239.
    Roos K, Siegbahn PEM (2013) Inorg Chem 52:4173–4184PubMedCrossRefGoogle Scholar
  240. 240.
    Mas-Ballesté R, McDonald AR, Reed D, Usharani D, Schyman P, Milko P, Shaik S, Que L Jr (2012) Chem Eur J 18:11747–11760PubMedPubMedCentralCrossRefGoogle Scholar
  241. 241.
    Suardíaz R, Masgrau L, Lluch JM, González-Lafont À (2014) ChemPhysChem 15:4049–4054PubMedCrossRefGoogle Scholar
  242. 242.
    Postils V, Company A, Solà M, Costas M, Luis JM (2015) Inorg Chem 54:8223–8236PubMedCrossRefGoogle Scholar

Copyright information

© SBIC 2016

Authors and Affiliations

  • Tibor András Rokob
    • 3
  • Jakub Chalupský
    • 1
  • Daniel Bím
    • 1
  • Prokopis C. Andrikopoulos
    • 1
  • Martin Srnec
    • 2
  • Lubomír Rulíšek
    • 1
  1. 1.Institute of Organic Chemistry and BiochemistryAcademy of Sciences of the Czech Republic, Gilead Sciences & IOCB Research CenterPrague 6Czech Republic
  2. 2.J. Heyrovský Institute of Physical ChemistryAcademy of Sciences of the Czech RepublicPrague 8Czech Republic
  3. 3.Institute of Organic ChemistryResearch Centre for Natural Sciences, HASBudapestHungary

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