Abstract
Nature uses dioxygen as a key oxidant in the transformation of biomolecules. Among the enzymes that are utilized for these reactions are copper-containing metalloenzymes, which are responsible for important biological functions such as the regulation of neurotransmitters, dioxygen transport, and cellular respiration. Enzymatic and model system studies work in tandem in order to gain an understanding of the fundamental reductive activation of dioxygen by copper complexes. This review covers the most recent advancements in the structures, spectroscopy, and reaction mechanisms for dioxygen-activating copper proteins and relevant synthetic models thereof. An emphasis has also been placed on cofactor biogenesis, a fundamentally important process whereby biomolecules are post-translationally modified by the pro-enzyme active site to generate cofactors which are essential for the catalytic enzymatic reaction. Significant questions remaining in copper-ion-mediated O2-activation in copper proteins are addressed.
Similar content being viewed by others
References
Kroneck PMH, Torres MES (eds) (2015) Sustaining life on planet earth: metalloenzymes mastering dioxygen and other chewy gases. Springer International Publishing, Switzerland
Campbell AN, Stahl SS (2012) Acc Chem Res 45:851–863
Mccann SD, Stahl SS (2015) Acc Chem Res 48:1756–1766
Gubelmann MH, Williams AF (1983) Struct Bonding, vol 55. Berlin, pp 1–65
Sawyer DT (1991) Oxygen chemistry. Oxford University Press, New York
Bakac A (2010) Inorg Chem 49:3584–3593
Armstrong DA, Huie RE, Koppenol WH, Lymar SV, Merenyi G, Neta P, Ruscic B, Stanbury DM, Steenken S, Wardman P (2015) Pure Appl Chem 87:1139–1150
Sheldon RA, Kochi JK (1981) Metal-catalyzed oxidations of organic compounds. Academic Press, Inc, New York
Ray K, Pfaff FF, Wang B, Nam W (2014) J Am Chem Soc 136:13942–13958
Engelmann X, Monte-Pérez I, Ray K (2016) Angew Chem Int Ed 55:7632–7649
Sahu S, Goldberg DP (2016) J Am Chem Soc 138:11410–11428
Solomon EI, Heppner DE, Johnston EM, Ginsbach JW, Cirera J, Qayyum M, Kieber-Emmons MT, Kjaergaard CH, Hadt RG, Tian L (2014) Chem Rev 114:3659–3853
Mirica LM, Ottenwaelder X, Stack TDP (2004) Chem Rev 104:1013–1045
Lewis EA, Tolman WB (2004) Chem Rev 104:1047–1076
Hatcher LQ, Karlin KD (2004) J Biol Inorg Chem 9:669–683
Itoh S (2011) In: Karlin KD, Itoh S (eds) Copper-oxygen chemistry. Wiley, Hoboken, pp 225–282
Liu JJ, Diaz DE, Quist DA, Karlin KD (2016) Isr J Chem 56:738–755
Jacobson RR, Tyeklar Z, Farooq A, Karlin KD, Liu S, Zubieta J (1988) J Am Chem Soc 110:3690–3692
Kitajima N, Fujisawa K, Morooka Y, Toriumi K (1989) J Am Chem Soc 111:8975–8976
Halfen JA, Mahapatra S, Wilkinson EC, Kaderli S, Young VG, Que L, Zuberbühler AD, Tolman WB (1996) Science 271:1397–1400
Mahapatra S, Halfen JA, Wilkinson EC, Pan G, Wang X, Young VG, Cramer CJ, Que L, Tolman WB (1996) J Am Chem Soc 118:11555–11574
Dubois JL, Mukherjee P, Collier AM, Mayer JM, Solomon EI, Hedman B, Stack TDP, Hodgson KO (1997) J Am Chem Soc 119:8578–8579
Mahadevan V, Hou Z, Cole AP, Root DE, Lal TK, Solomon EI, Stack TDP (1997) J Am Chem Soc 119:11996–11997
Karlin KD, Cruse RW, Gultneh Y, Hayes JC, Zubieta J (1984) J Am Chem Soc 106:3372–3374
Pate JE, Cruse RW, Karlin KD, Solomon EI (1987) J Am Chem Soc 109:2624–2630
Mahroof-Tahir M, Murthy NN, Karlin KD, Blackburn NJ, Shaikh SN, Zubieta J (1992) Inorg Chem 31:3001–3003
Cao R, Saracini C, Ginsbach JW, Kieber-Emmons MT, Siegler MA, Solomon EI, Fukuzumi S, Karlin KD (2016) J Am Chem Soc 138:7055–7066
Kindermann N, Bill E, Dechert S, Demeshko S, Reijerse EJ, Meyer F (2015) Angew Chem Int Ed 54:1738–1743
Baldwin MJ, Root DE, Pate JE, Fujisawa K, Kitajima N, Solomon EI (1992) J Am Chem Soc 114:10421–10431
Tyeklar Z, Jacobson RR, Wei N, Murthy NN, Zubieta J, Karlin KD (1993) J Am Chem Soc 115:2677–2689
Karlin KD, Wei N, Jung B, Kaderli S, Zuberbühler AD (1991) J Am Chem Soc 113:5868–5870
Fujisawa K, Tanaka M, Moro-oka Y, Kitajima N (1994) J Am Chem Soc 116:12079–12080
Würtele C, Gaoutchenova E, Harms K, Holthausen MC, Sundermeyer J, Schindler S (2006) Angew Chem Int Ed 45:3867–3869
Aboelella NW, Lewis EA, Reynolds AM, Brennessel WW, Cramer CJ, Tolman WB (2002) J Am Chem Soc 124:10660–10661
Donoghue PJ, Tehranchi J, Cramer CJ, Sarangi R, Solomon EI, Tolman WB (2011) J Am Chem Soc 133:17602–17605
Gagnon N, Tolman WB (2015) Acc Chem Res 48:2126–2131
Dhar D, Yee GM, Spaeth AD, Boyce DW, Zhang H, Dereli B, Cramer CJ, Tolman WB (2016) J Am Chem Soc 138:356–368
Prigge ST, Eipper BA, Mains RE, Amzel LM (2004) Science 304:864–867
Li X, Beeson WT IV, Phillips CM, Marletta MA, Cate JHD (2012) Structure 20:1051–1061
Magnus KA, Hazes B, Ton-That H, Bonaventura C, Bonaventura J, Hol WGJ (1994) Proteins Struct Funct Genet 19:302–309
Wilmot CM, Hajdu J, McPherson MJ, Knowles PF, Phillips SEV (1999) Science 286:1724–1728
Atherton NM, Gibson QH, Greenwood C (1963) Biochem J 86:541–555
Brunori M, Noble RW, Antonini E, Wyman J (1966) J Biol Chem 241:5238–5243
Noble RW, Gibson QH, Brunori M, Antonini E, Wyman J (1969) J Biol Chem 244:3905–3908
Greenwood C, Gibson QH (1967) J Biol Chem 242:1782–1787
Ferguson-Miller S, Babcock GT (1996) Chem Rev 96:2889–2907
Szundi I, Liao GL, Einarsdóttir O (2001) Biochemistry 40:2332–2339
Fry HC, Scaltrito DV, Karlin KD, Meyer GJ (2003) J Am Chem Soc 125:11866–11871
Saracini C, Liakos DG, Zapata Rivera JE, Neese F, Meyer GJ, Karlin KD (2014) J Am Chem Soc 136:1260–1263
Momenteau M, Reed CA (1994) Chem Rev 94:659–698
Zhang CX, Kaderli S, Costas M, Kim E-I, Neuhold Y-M, Karlin KD, Zuberbühler AD (2003) Inorg Chem 42:1807–1824
Kunishita A, Ertem MZ, Okubo Y, Tano T, Sugimoto H, Ohkubo K, Fujieda N, Fukuzumi S, Cramer CJ, Itoh S (2012) Inorg Chem 51:9465–9480
Andrew CR, McKillop KP, Sykes AG (1993) Biochim Biophys Acta 1162:105–114
Rodriguez-Lopez JN, Fenoll LG, Garcia-Ruiz PA, Varon R, Tudela J, Thorneley RNF, Garcia-Canovas F (2000) Biochemistry 39:10497–10506
Karlin KD, Haka MS, Cruse RW, Gultneh Y (1985) J Am Chem Soc 107:5828–5829
Park GY, Qayyum MF, Woertink J, Hodgson KO, Hedman B, Sarjeant AAN, Solomon EI, Karlin KD (2012) J Am Chem Soc 134:8513–8524
Osborne RL, Klinman JP (2011) In: Karlin KD, Itoh S (eds) Copper-oxygen chemistry. Wiley, Hoboken, pp 1–22
Kline CD, Blackburn NJ (2016) Biochemistry. doi:10.1021/acs.biochem.6b00845
Vendelboe TV, Harris P, Zhao Y, Walter TS, Harlos K, El Omari K, Christensen HEM (2016) Sci Adv 2:e1500980
Evans JP, Ahn K, Klinman JP (2003) J Biol Chem 278:49691–49698
Chen P, Solomon EI (2004) J Am Chem Soc 126:4991–5000
Itoh S (2015) Acc Chem Res 48:2066–2074
Peterson RL, Himes RA, Kotani H, Suenobu T, Tian L, Siegler MA, Solomon EI, Fukuzumi S, Karlin KD (2011) J Am Chem Soc 133:1702–1705
Lee JY, Peterson RL, Ohkubo K, Garcia-Bosch I, Himes RA, Woertink J, Moore CD, Solomon EI, Fukuzumi S, Karlin KD (2014) J Am Chem Soc 136:9925–9937
Kunishita A, Kubo M, Sugimoto H, Ogura T, Sato K, Takui T, Itoh S (2009) J Am Chem Soc 131:2788–2789
May SW, Phillips RS, Mueller PW, Herman HH (1981) J Biol Chem 256:8470–8475
Kim S, Lee JY, Cowley RE, Ginsbach JW, Siegler MA, Solomon EI, Karlin KD (2015) J Am Chem Soc 137:2796–2799
Kodera M, Kita T, Miura I, Nakayama N, Kawata T, Kano K, Hirota S (2001) J Am Chem Soc 123:7715–7716
Tubbs KJ, Fuller AL, Bennett B, Arif Atta M, Makowska-Grzyska MM, Berreau LM (2003) Dalton Trans, pp 3111–3116
Aboelella NW, Gherman BF, Cramer CJ, Tolman WB (2006) J Am Chem Soc 128:3445–3458
Zhou L, Powell D, Nicholas KM (2006) Inorg Chem 45:3840–3842
Zhou L, Powell D, Nicholas KM (2007) Inorg Chem 46:7789–7799
Zhou L, Nicholas KM (2008) Inorg Chem 47:4356–4367
Park GY, Lee Y, Lee D-H, Woertink JS, Narducci Sarjeant AA, Solomon EI, Karlin KD (2010) Chem Commun 46:91–93
Tano T, Mieda K, Sugimoto H, Ogura T, Itoh S (2014) Dalton Trans 43:4871–4877
Maji RC, Bhandari A, Singh R, Roy S, Chatterjee SK, Bowles FL, Ghiassi KB, Maji M, Olmstead MM, Patra AK (2015) Dalton Trans 44:17587–17599
Beeson WT, Vu VV, Span EA, Phillips CM, Marletta MA (2015) Annu Rev Biochem 84:923–946
Frandsen KEH, Simmons TJ, Dupree P, Poulsen JN, Hemsworth GR, Ciano L, Johnston EM, Tovborg M, Johansen KS, von Freiesleben P, Marmuse L, Fort S, Cottaz S, Driguez H, Henrissat B, Lenfant N, Tuna F, Baldansuren A, Davies GJ, Lo Leggio L, Walton PH (2016) Nat Chem Biol 12:298–303
Span EA, Marletta MA (2015) Curr Opin Struct Biol 35:93–99
Hemsworth GR, Johnston EM, Davies GJ, Walton PH (2015) Trends Biotechnol 33:747–761
Kim S, Ståhlberg J, Sandgren M, Paton RS, Beckham GT (2014) Proc Natl Acad Sci USA 111:149–154
Walton PH, Davies GJ (2016) Curr Opin Chem Biol 31:195–207
Dhar D, Tolman WB (2015) J Am Chem Soc 137:1322–1329
Phillips CM, Beeson WT, Cate JH, Marletta MA (2011) ACS Chem Biol 6:1399–1406
Peterson RL, Kim S, Karlin KD (2013) In: Reedijk J, Poeppelmeier K (eds) Comprehensive inorganic chemistry II, 2nd edn. Elsevier, Oxford, pp 149–177
Parsons MR, Convery MA, Wilmot CM, Yadav KDS, Blakeley V, Corner AS, Phillips S, McPherson MJ, Knowles PF (1995) Structure 3:1171–1184
Wilce MCJ, Dooley DM, Freeman HC, Guss JM, Matsunami H, McIntire WS, Ruggiero CE, Tanizawa K, Yamaguchi H (1997) Biochemistry 36:16116–16133
Li R, Klinman JP, Mathews FS (1998) Structure 6:293–307
Cai D, Klinman JP (1994) J Biol Chem 269:32039–32042
Kim M, Okajima T, Kishishita S, Yoshimura M, Kawamori A, Tanizawa K, Yamaguchi H (2002) Nat Struct Biol 9:591–596
Rokhsana D, Shepard EM, Brown DE, Dooley DM (2011) In: Karlin KD, Itoh S (eds) Copper-oxygen chemistry. Wiley, Hoboken, pp 53–106
Mills SA, Klinman JP (2000) J Am Chem Soc 122:9897–9904
Mure M, Mills SA, Klinman JP (2002) Biochemistry 41:9269–9278
Shepard EM, Okonski KM, Dooley DM (2008) Biochemistry 47:13907–13920
Liu Y, Mukherjee A, Nahumi N, Ozbil M, Brown D, Angeles-Boza AM, Dooley DM, Prabhakar R, Roth JP (2013) J Phys Chem B 117:218–229
Tabuchi K, Ertem MZ, Sugimoto H, Kunishita A, Tano T, Fujieda N, Cramer CJ, Itoh S (2011) Inorg Chem 50:1633–1647
Mure M, Klinman JP (1995) J Am Chem Soc 117:8698–8706
Whittaker MM, Whittaker JW (1988) J Biol Chem 263:6074–6080
Whittaker MM, Whittaker JW (2003) J Biol Chem 278:22090–22101
Kelleher FM, Bhavanandan VP (1986) J Biol Chem 261:11045–11048
Ito N, Phillips SEV, Stevens C, Ogel ZB, McPherson MJ, Keen JN, Yadav KDS, Knowles PF (1991) Nature 350:87–90
Johnson JM, Halsall HB, Heineman WR (1985) Biochemistry 24:1579–1585
Stubbe J, van der Donk WA (1998) Chem Rev 98:705–762
Whittaker JW (2003) Chem Rev 103:2347–2363
Thomas F, Gellon G, Gautier-Luneau I, Saint-Aman E, Pierre J-L (2002) Angew Chem Int Ed 41:3047–3050
Thomas F (2007) Eur J Inorg Chem 2007:2379–2404
Jazdzewski BA, Reynolds AM, Holland PL, Young VG, Kaderli S, Zuberbühler AD, Tolman WB (2003) J Biol Inorg Chem 8:381–393
Lyons CT, Stack TDP (2013) Coord Chem Rev 257:528–540
Itoh S, Taki M, Fukuzumi S (2000) Coord Chem Rev 198:3–20
John A, Shaikh MM, Ghosh P (2008) Dalton Trans, pp 2815–2824
Ghorai S, Sarmah A, Roy RK, Tiwari A, Mukherjee C (2016) Inorg Chem 55:1370–1380
Fusetti F, Schröter KH, Steiner RA, Van Noort PI, Pijning T, Rozeboom HJ, Kalk KH, Egmond MR, Dijkstra BW (2002) Structure 10:259–268
Gopal B, Madan LL, Betz SF, Kossiakoff AA (2005) Biochemistry 44:193–201
Schaab M, Barney B, Francisco W (2006) Biochemistry 45:1009–1016
Merkens H, Kappl R, Jakob RP, Schmid FX, Fetzner S (2008) Biochemistry 47:12185–12196
Steiner RA, Kalk KH, Dijkstra BW (2002) Proc Natl Acad Sci USA 99:16625–16630
Steiner RA, Kooter IM, Dijkstra BW (2002) Biochemistry 41:7955–7962
Kaizer J, Pap JS, Speier G (2011) In: Karlin KD, Itoh S (eds) Copper-oxygen chemistry. Wiley, Hoboken, pp 23–52
Balogh-Hergovich E, Speier G (2001) J Org Chem 66:7974–7978
Balogh-Hergovich E, Kaizer J, Speier G, Fulop V, Parkanyi L (1999) Inorg Chem 38:3787–3795
Barhács L, Kaizer J, Pap J, Speier G (2001) Inorg Chim Acta 320:83–91
Matuz A, Giorgi M, Speier G, Kaizer J (2013) Polyhedron 63:41–49
Balogh-Hergovich E, Kaizer J, Speier G (2003) J Mol Catal A Chem 206:83–87
Sun Y-J, Huang Q-Q, Tano T, Itoh S (2013) Inorg Chem 52:10936–10948
Sun Y-J, Huang Q-Q, Li P, Zhang J-J (2015) Dalton Trans 73:13926–13938
Siegbahn PEM (2004) Biochemistry 43:16625–16630
Saito T, Kawakami T, Yamanaka S, Okumura M (2015) J Phys Chem B 119:6952–6962
Liddington R, Derewenda Z, Dodson E, Hubbard R, Dodson G (1992) J Mol Biol 228:551–579
Holmes MA, Le Trong I, Turley S, Sieker LC, Stenkamp RE (1991) J Mol Biol 218:583–593
Cuff ME, Miller KI, van Holde KE, Hendrickson WA (1998) J Mol Biol 278:855–870
Eickman NC, Himmelwright RS, Solomon EI (1979) Proc Natl Acad Sci USA 76:2094–2098
Karlin KD, Haka MS, Cruse RW, Meyer GJ, Farooq A, Gultneh Y, Hayes JC, Zubieta J (1988) J Am Chem Soc 110:1196–1207
Karlin KD, Tyeklár Z, Farooq A, Haka MS, Ghosh P, Cruse RW, Gultneh Y, Hayes JC, Toscano PJ, Zubieta J (1992) Inorg Chem 31:1436–1451
Magnus KA, Ton-That H, Carpenter JE (1994) Chem Rev 94:727–735
Metz M, Solomon EI (2001) J Am Chem Soc 123:4938–4950
Loehr JS, Freedman TB, Loehr TM (1974) Biochem Biophys Res Commun 56:510–515
Brown JM, Powers L, Kincaid B, Larrabee JA, Spiro TG (1980) J Am Chem Soc 102:4210–4216
Eccles TK (1981) J Am Chem Soc 103:984–986
Dooley DM, Scott RA, Ellinghaus J, Solomon EI, Gray B, Dooley DM, Scott RA, Ellinghaust JOE, Solomon EI, Gray HB (1978) Proc Natl Acad Sci USA 75:3019–3022
Salvato B, Santamaria M, Beltramini M, Alzuet G, Casella L (1998) Biochemistry 37:14065–14077
Zlateva T, Di Muro P, Salvato B, Beltramini M (1996) FEBS Lett 384:251–254
Nillius D, Jaenicke E, Decker H (2008) FEBS Lett 582:749–754
Decker H, Ryan M, Jaenicke E, Terwilliger N (2001) J Biol Chem 276:17796–17799
Baird S, Kelly SM, Price NC, Jaenicke E, Meesters C, Nillius D, Decker H, Nairn J (2007) Biochim Biophys Acta Proteins Proteomics 1774:1380–1394
Morioka C, Tachi Y, Suzuki S, Itoh S (2006) J Am Chem Soc 128:6788–6789
Suzuki K, Shimokawa C, Morioka C, Itoh S (2008) Biochemistry 47:7108–7115
Decker H, Rimke T (1998) J Biol Chem 273:25889–25892
Lee SY, Lee BL, Söderhäll K (2004) Biochem Biophys Res Commun 322:490–496
Nagai T, Kawabata SI (2000) J Biol Chem 275:29264–29267
Nagai T, Osaki T, Kawabata SI (2001) J Biol Chem 276:27166–27170
Saracini C, Ohkubo K, Suenobu T, Meyer GJ, Karlin KD, Fukuzumi S (2015) J Am Chem Soc 137:15865–15874
Klabunde T, Eicken C, Sacchettini JC, Krebs B (1998) Nat Struct Biol 5:1084–1090
Virador VM, Grajeda JPR, Blanco-Labra A, Mendiola-Olaya E, Smith GM, Moreno A, Whitaker JR (2010) J Agric Food Chem 58:1189–1201
Matoba Y, Kumagai T, Yamamoto A, Yoshitsu H, Sugiyama M (2006) J Biol Chem 281:8981–8990
Sendovski M, Kanteev M, Ben-Yosef VS, Adir N, Fishman A (2011) J Mol Biol 405:227–237
Ismaya WT, Rozeboom J, Weijn A, Mes JJ, Fusetti F (2011) Biochemistry 50:5477–5486
Fujimoto K, Okino N, Kawabata S, Iwanaga S, Ohnishi E (1995) Proc Natl Acad Sci USA 92:7769–7773
Li Y, Wang Y, Jiang H, Deng J (2009) Proc Natl Acad Sci USA 106:17002–17006
Morrison R, Mason K, Frostmason S (1994) Pigment Cell Res 7:388–393
Eickman NC, Solomon EI, Larrabee JA, Spiro TG, Lerch K (1978) J Am Chem Soc 100:6529–6531
Peñalver MJ, Rodríguez-López JN, García-Ruiz PA, García-Cánovas F, Tudela J (2003) Biochim Biophys Acta Proteins Proteomics 1650:128–135
Fenoll LG, Peñalver MJ, Rodríguez-López JN, García-Ruiz PA, García-Cánovas F, Tudela J (2004) Biochem J 380:643–650
Yamazaki SI, Itoh S (2003) J Am Chem Soc 125:13034–13035
Fujieda N, Murata M, Yabuta S, Ikeda T, Shimokawa C, Nakamura Y, Hata Y, Itoh S (2013) J Biol Inorg Chem 18:19–26
Tripathi RK, Hearing VJ, Urabe K, Aroca P, Spritz RA (1992) J Biol Chem 267:23707–23712
Olivares C, García-Borrón JC, Solano F (2002) Biochemistry 41:679–686
Ben-Yosef VS, Sendovski M, Fishman A (2010) Enzyme Microb Technol 47:372–376
Goldfeder M, Kanteev M, Isaschar-Ovdat S, Adir N, Fishman A (2014) Nat Commun 5:4505
Kanteev M, Goldfeder M, Fishman A (2015) Protein Sci 24:1360–1369
Solem E, Tuczek F, Decker H (2016) Angew Chem Int Ed 55:2884–2888
Mirica LM, Vance M, Rudd DJ, Hedman B, Hodgson KO, Solomon EI, Stack TDP (2005) Science 308:1890–1892
Curse RW, Kaderli S, Karlin KD, Zuberbühler AD (1988) J Am Chem 110:6882–6883
Nasir MS, Cohen BI, Karlin KD (1992) J Am Chem Soc 114:2482–2494
Karlin KD, Nasir MS, Cohen BI, Cruse RW, Kaderli S, Zuberbühler AD (1994) J Am Chem Soc 116:1324–1336
Itoh S, Kumei H, Taki M, Nagatomo S, Kitagawa T, Fukuzumi S (2001) J Am Chem Soc 123:6708–6709
Osako T, Ohkubo K, Taki M, Tachi Y, Fukuzumi S, Itoh S (2003) J Am Chem Soc 125:11027–11033
Mirica LM, Rudd DJ, Vance MA, Solomon EI, Hodgson KO, Hedman B, Stack TDP (2006) J Am Chem Soc 128:2654–2665
Noguchi A, Kitamura T, Onaka H, Horinouchi S, Ohnishi Y (2010) Nat Chem Biol 6:641–643
Ginsbach JW, Kieber-Emmons MT, Nomoto R, Noguchi A, Ohnishi Y, Solomon EI (2012) Proc Natl Acad Sci USA 109:10793–10797
Toussaint O, Lerch K (1987) Biochemistry 26:8567–8571
Makris TM, Vu VV, Meier KK, Komor AJ, Rivard BS, Münck E, Que L, Lipscomb JD (2015) J Am Chem Soc 137:1608–1617
Komor AJ, Rivard BS, Fan R, Guo Y, Que L, Lipscomb JD (2016) J Am Chem Soc 138:7411–7421
Olah GA, Goeppert A, Prakash GKS (2005) Angew Chem Int Ed 44:2636–2639
Sirajuddin S, Rosenzweig AC (2015) Biochemistry 54:2283–2294
Lawton TJ, Rosenzweig AC (2016) J Am Chem Soc 138:9327–9340
Lieberman RL, Rosenzweig AC (2005) Nature 434:177–182
Hakemian AS, Kondapalli KC, Telser J, Hoffman BM, Stemmler TL, Rosenzweig AC (2008) Biochemistry 47:6793–6801
Balasubramanian R, Smith SM, Rawat S, Yatsunyk LA, Stemmler TL, Rosenzweig AC (2010) Nature 465:115–119
Citek C, Lin B, Phelps TE, Wasinger EC, Stack TDP (2014) J Am Chem Soc 136:14405–14408
Citek C, Gary JB, Wasinger EC, Stack TDP (2015) J Am Chem Soc 137:6991–6994
Citek C, Herres-Pawlis S, Stack TDP (2015) Acc Chem Res 48:2424–2433
Gary JB, Citek C, Brown TA, Zare RN, Wasinger EC, Stack TDP (2016) J Am Chem Soc 138:9986–9995
Roberts SA, Weichsel A, Grass G, Thakali K, Hazzard JT, Tollin G, Rensing C, Montfort WR (2002) Proc Natl Acad Sci USA 99:2766–2771
Cole J, Ballou D, Solomon E (1991) J Am Chem Soc 113:8544–8546
Palmer AE, Quintanar L, Severance S, Wang TP, Kosman DJ, Solomon EI (2002) Biochemistry 41:6438–6448
Kataoka K, Kitagawa R, Inoue M, Naruse D, Sakurai T, Huang HW (2005) Biochemistry 44:7004–7012
Ueki Y, Inoue M, Kurose S, Kataoka K, Sakurai T (2006) FEBS Lett 580:4069–4072
Silva CS, Damas JM, Chen ZJ, Brissos V, Marcins LO, Soares CM, Lindley PF, Bento I (2012) Acta Crystallogr Sect D Biol Crystallogr 68:186–193
Yoon J, Solomon EI (2007) J Am Chem Soc 129:13127–13136
Augustine AJ, Kjaergaard C, Qayyum M, Ziegler L, Kosman DJ, Hodgson KO, Hedman B, Solomon EI (2010) J Am Chem Soc 132:6057–6067
Shin W, Sundaram UM, Cole JL, Zhang HH, Hedman B, Hodgson KO, Solomon EI (1996) J Am Chem Soc 118:3202–3215
Solomon EI, Ginsbach JW, Heppner DE, Kieber-Emmons MT, Kjaergaard CH, Smeets PJ, Tian L, Woertink JS (2011) Faraday Discuss 148:11–39
Suh MP, Han MY, Lee JH, Min KS, Hyeon C (1998) J Am Chem Soc 120:3819–3820
Yoon J, Mirica LM, Stack TDP, Solomon EI (2004) J Am Chem Soc 126:12586–12595
Mirica LM, Stack TDP (2005) Inorg Chem 44:2131–2133
Yoon J, Solomon EI (2005) Inorg Chem 44:8076–8086
Yoon J, Mirica LM, Stack TDP, Solomon EI (2005) J Am Chem Soc 127:13680–13693
Yoon J, Liboiron BD, Sarangi R, Hodgson KO, Hedman B, Solomon EI (2007) Proc Natl Acad Sci USA 104:13609–13614
Solomon EI, Augustine AJ, Yoon J (2008) Dalton Trans 9226:3921–3932
Taki M, Teramae S, Nagatomo S, Tachi Y, Kitagawa T, Itoh S, Fukuzumi S (2002) J Am Chem Soc 124:6367–6377
Gupta AK, Tolman WB (2012) Inorg Chem 51:1881–1888
Lionetti D, Day MW, Agapie T (2013) Chem Sci 4:785–790
Di Francesco GN, Gaillard A, Ghiviriga I, Abboud KA, Murray LJ (2014) Inorg Chem 53:4647–4654
Murray LJ, Weare WW, Shearer J, Mitchell AD, Abboud KA (2014) J Am Chem Soc 136:13502–13505
Feig A, Lippard S (1994) Chem Rev 94:759–805
Kim E, Chufa EE, Kamaraj K, Karlin KD (2004) Chem Rev 104:1077–1133
Yoshikawa S, Shimada A (2015) Chem Rev 115:1936–1989
Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S (1995) Science 269:1069–1074
Yano N, Muramoto K, Shimada A, Takemura S, Baba J, Fujisawa H, Mochizuki M, Shinzawa-Itoh K, Yamashita E, Tsukihara T, Yoshikawa S (2016) J Biol Chem 291:23882–23894
Nath I, Chakraborty J, Verpoort F (2016) Chem Soc Rev 45:4127–4170
Cracknell JA, Vincent KA, Armstrong FA (2008) Chem Rev 108:2439–2461
Varotsis C, Woodruff WH (1989) J Am Chem Soc 111:6439–6440
Han SW, Ching YC, Rousseau DL (1990) Proc Natl Acad Sci USA 87:2491–2495
Ogura T, Takahashi S, Shinzawa-Itoh K, Yoshikawa S, Kitagawa T (1990) J Biol Chem 265:14721–14723
Proshlyakov DA, Ogura T, Shinzawa-Itoh K, Yoshikawa S, Appelman EH, Kitagawa T (1994) J Biol Chem 269:29385–29388
Proshlyakov DA, Pressler MA, Babcock GT (1998) Proc Natl Acad Sci USA 95:8020–8025
Proshlyakov DA, Pressler MA, DeMaso C, Leykam JF, DeWitt DL, Babcock GT (2000) Science 290:1588–1591
Sucheta A, Szundi I, Einarsdottir O (1998) Biochemistry 37:17905–17914
Ogura T, Takahashi S, Hirota S, Shinzawa-Itoh K, Yoshikawa S, Appelman EH, Kitagawa T (1993) J Am Chem Soc 115:8527–8536
Ogura T, Hirota S, Proshlyakov DA, Shinzawa-Itoh K, Yoshikawa S, Kitagawa T (1996) J Am Chem Soc 118:5443–5449
Das TK, Pecoraro C, Tomson FL, Gennis RB, Rousseau DL (1998) Biochemistry 37:14471–14476
Sigman JA, Kwok BC, Lu Y, Sigman JA, Kwok BC, Lu Y (2000) J Am Chem Soc 122:8192–8196
Bhagi-Damodaran A, Petrik I, Lu Y (2016) Isr J Chem 56:773–790
Sigman JA, Kim HK, Zhao X, Carey JR, Lu Y (2003) Proc Natl Acad Sci USA 100:3629–3634
Miner KD, Mukherjee A, Gao YG, Null EL, Petrik ID, Zhao X, Yeung N, Robinson H, Lu Y (2012) Angew Chem Int Ed 51:5589–5592
Petrik ID, Davydov R, Ross M, Zhao X, Hoffman B, Lu Y (2016) J Am Chem Soc 138:1134–1137
Liu X, Yu Y, Hu C, Zhang W, Lu Y, Wang J (2012) Angew Chem Int Ed 51:4312–4316
Bhagi-Damodaran A, Michael MA, Zhu Q, Reed J, Sandoval BA, Mirts EN, Chakraborty S, Moënne-Loccoz P, Zhang Y, Lu Y (2016) Nat Chem. doi:10.1038/nchem.2643
Collman JP, Sunderland CJ, Berg KE, Vance MA, Solomon EI (2003) J Am Chem Soc 125:6648–6649
Collman JP, Decréau RA, Sunderland CJ (2006) Chem Commun, pp 3894–3896
Boulatov R, Collman JP, Shiryaeva IM, Sunderland CJ (2002) J Am Chem Soc 124:11923–11935
Chishiro T, Shimazaki Y, Tani F, Tachi Y, Naruta Y, Karasawa S, Hayami S, Maeda Y (2003) Angew Chem Int Ed 42:2788–2791
Liu J-G, Naruta Y, Tani F (2005) Angew Chem Int Ed 44:1836–1840
Ghiladi RA, Hatwell KR, Karlin KD, Huang HW, Moënne-Loccoz P, Krebs C, Huynh BH, Marzilli LA, Cotter RJ, Kaderli S, Zuberbühler AD (2001) J Am Chem Soc 123:6183–6184
Chatterjee S, Sengupta K, Hematian S, Karlin KD, Dey A (2015) J Am Chem Soc 137:12897–12905
Collman JP, Decréau RA (2008) Chem Commun, pp 5065–5076
Halime Z, Kieber-Emmons MT, Qayyum MF, Mondal B, Gandhi T, Puiu SC, Chufan EE, Sarjeant AAN, Hodgson KO, Hedman B, Solomon EI, Karlin KD (2010) Inorg Chem 49:3629–3645
Garcia-Bosch I, Adam SM, Schaefer AW, Sharma SK, Peterson RL, Solomon EI, Karlin KD (2015) J Am Chem Soc 137:1032–1035
Sheng Y, Abreu IA, Cabelli DE, Maroney MJ, Miller AF, Teixeira M, Valentine JS (2014) Chem Rev 114:3854–3918
Hough MA, Hasnain SS (2003) Structure 11:937–946
Hough MA, Hasnain SS (1999) J Mol Biol 287:579–592
Valentine JS, Doucette PA, Zittin Potter S (2005) Annu Rev Biochem 74:563–593
Paulsen CE, Carroll KS (2013) Chem Rev 113:4633–4679
Nagy P, Kettle AJ, Winterbourn CC (2009) J Biol Chem 284:14723–14733
Das AB, Nagy P, Abbott HF, Winterbourn CC, Kettle AJ (2010) Free Radic Biol Med 48:1540–1547
Nagy P, Lechte TP, Das AB, Winterbourn CC (2012) J Biol Chem 287:26068–26076
Das AB, Nauser T, Koppenol WH, Kettle AJ, Winterbourn CC, Nagy P (2014) Free Radic Biol Med 70:86–95
Hart PJ, Balbirnie MM, Ogihara NL, Nersissian AM, Weiss MS, Valentine JS, Eisenberg D (1999) Biochemistry 38:2167–2178
Smirnov VV, Roth JP (2006) J Am Chem Soc 128:16424–16425
Maji RC, Das PP, Mishra S, Bhandari A, Maji M, Patra AK (2016) Dalton Trans 45:11898–11910
Kolks G, Frihart CR, Rabinowitz HN, Lippard SJ (1976) J Am Chem Soc 98:5720–5721
O’Young C-L, Dewan JC, Lilienthal HR, Lippard SJ (1978) J Am Chem Soc 100:7291–7300
Strothkamp KG, Lippard SJ (1982) Acc Chem Res 15:318–326
Sato M, Nagae S, Uehara M, Nakaya J (1984) J Chem Soc Chem Comm, pp 1661–1663
Pierre J-L, Chautemps P, Refaif S, Beguin C, Marzouki AE, Serratrice G, Saint-Aman E, Rey P (1995) J Am Chem Soc 117:1965–1973
Mao Z-W, Chen M-Q, Tan X-S, Liu J, Tang W-X (1995) Inorg Chem 34:2889–2893
Ohtsu H, Shimazaki Y, Odani A, Yamauchi O, Mori W, Itoh S, Fukuzumi S (2000) J Am Chem Soc 122:5733–5741
Ohtsu H, Fukuzumi S, Itoh S, Nagatomo S, Kitagawa T, Ogo S, Watanabe Y (2000) Chem Commun, pp 1051–1052
Halcrow MA (2001) Angew Chem Int Ed 40:346–349
Hemp J, Robinson DE, Ganesan KB, Martinez TJ, Kelleher NL, Gennis RB (2006) Biochemistry 45:15405–15410
Davidson VL (2007) Biochemistry 46:5283–5292
Yukl ET, Wilmot CM (2012) Curr Opin Chem Biol 16:54–59
Klinman JP, Bonnot F (2014) Chem Rev 114:4343–4365
DuBois JL, Klinman JP (2005) Arch Biochem Biophys 433:255–265
Moore RH, Spies MA, Culpepper MB, Murakawa T, Hirota S, Okajima T, Tanizawa K, Mure M (2007) J Am Chem Soc 129:11524–11534
Dove JE, Schwartz B, Williams NK, Klinman JP (2000) Biochemistry 39:3690–3698
Ghosh S, Cirera J, Vance MA, Ono T, Fujisawa K, Solomon EI (2008) J Am Chem Soc 130:16262–16273
Chen ZW, Datta S, Dubois JL, Klinman JP, Mathews FS (2010) Biochemistry 49:7393–7402
Finney J, Moon HJ, Ronnebaum T, Lantz M, Mure M (2014) Arch Biochem Biophys 546:19–32
Firbank SJ, Rogers MS, Wilmot CM, Dooley DM, Halcrow MA, Knowles PF, McPherson MJ, Phillips SE (2001) Proc Natl Acad Sci USA 98:12932–12937
Rogers MS, Hurtado-Guerrero R, Firbank SJ, Halcrow MA, Dooley DM, Phillips SEV, Knowles PF, McPherson MJ (2008) Biochemistry 47:10428–10439
Cowley RE, Cirera J, Qayyum MF, Rokhsana D, Hedman B, Hodgson KO, Dooley DM, Solomon EI (2016) J Am Chem Soc 138:13219–13229
Fujieda N, Ikeda T, Murata M, Yanagisawa S, Aono S, Ohkubo K, Nagao S, Ogura T, Hirota S, Fukuzumi S, Nakamura Y, Hata Y, Itoh S (2011) J Am Chem Soc 133:1180–1183
Fujieda N, Yabuta S, Ikeda T, Oyama T, Muraki N, Kurisu G, Itoh S (2013) J Biol Chem 288:22128–22140
Fujieda N, Itoh S (2016) Bull Chem Soc Jpn 89:733–742
Sprakel VSI, Feiters MC, Meyer-Klaucke W, Klopstra M, Brinksma J, Feringa BL, Karlin KD, Nolte RJM (2005) Dalton Trans, pp 3522–3534
Walli A, Dechert S, Bauer M, Demeshko S, Meyer F (2014) Eur J Inorg Chem 2014:4660–4676
Ravikiran B, Mahalakshmi R (2014) RSC Adv 4:33958–33974
Uchida T, Mogi T, Nakamura H, Kitagawa T (2004) J Biol Chem 279:53613–53620
Acknowledgements
This work was supported by research Grants from National Institutes of Health (R01 GM 028962 and R01 GM 060353 to K.D.K).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Quist, D.A., Diaz, D.E., Liu, J.J. et al. Activation of dioxygen by copper metalloproteins and insights from model complexes. J Biol Inorg Chem 22, 253–288 (2017). https://doi.org/10.1007/s00775-016-1415-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00775-016-1415-2