Proton-coupled electron transfer in Fe-superoxide dismutase and Mn-superoxide dismutase
Fe-containing superoxide dismutase (FeSOD) and MnSOD are widely assumed to employ the same catalytic mechanism. However this has not been completely tested. In 1985, Bull and Fee showed that FeSOD took up a proton upon reduction [J. Am. Chem. Soc. 107 (1985) 3295]. We now demonstrate that MnSOD inco...
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| Published in | Journal of inorganic biochemistry Vol. 93; no. 1; pp. 71 - 83 |
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| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
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United States
Elsevier Inc
2003
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| Abstract | Fe-containing superoxide dismutase (FeSOD) and MnSOD are widely assumed to employ the same catalytic mechanism. However this has not been completely tested. In 1985, Bull and Fee showed that FeSOD took up a proton upon reduction [J. Am. Chem. Soc. 107 (1985) 3295]. We now demonstrate that MnSOD incorporates the same crucial coupling between electron transfer and proton transfer. The redox-coupled H
+ acceptor has been presumed to be the coordinated solvent molecule, in both FeSOD and MnSOD, however this is very difficult to test experimentally. We have now examined the most plausible alternative: that Tyr34 accepts a proton upon SOD reduction. We report specific incorporation of
13C in the C
ζ positions of Tyr residues, assignment of the C
ζ signal of Tyr34 in each of oxidized FeSOD and MnSOD, and direct NMR observations showing that in both cases, Tyr34 is in the neutral protonated state. Thus Tyr34 cannot accept a proton upon SOD reduction, and coordinated solvent is concluded to be the redox-coupled H
+ acceptor instead, in both FeSOD and MnSOD. We have also confirmed by direct
13C observation that the p
K of 8.5 of reduced FeSOD corresponds to deprotonation of Tyr34. This work thus provides experimental proof of important commonalities between the detailed mechanisms of FeSOD and MnSOD. |
|---|---|
| AbstractList | Fe-containing superoxide dismutase (FeSOD) and MnSOD are widely assumed to employ the same catalytic mechanism. However this has not been completely tested. In 1985, Bull and Fee showed that FeSOD took up a proton upon reduction [J. Am. Chem. Soc. 107 (1985) 3295]. We now demonstrate that MnSOD incorporates the same crucial coupling between electron transfer and proton transfer. The redox-coupled H
+ acceptor has been presumed to be the coordinated solvent molecule, in both FeSOD and MnSOD, however this is very difficult to test experimentally. We have now examined the most plausible alternative: that Tyr34 accepts a proton upon SOD reduction. We report specific incorporation of
13C in the C
ζ positions of Tyr residues, assignment of the C
ζ signal of Tyr34 in each of oxidized FeSOD and MnSOD, and direct NMR observations showing that in both cases, Tyr34 is in the neutral protonated state. Thus Tyr34 cannot accept a proton upon SOD reduction, and coordinated solvent is concluded to be the redox-coupled H
+ acceptor instead, in both FeSOD and MnSOD. We have also confirmed by direct
13C observation that the p
K of 8.5 of reduced FeSOD corresponds to deprotonation of Tyr34. This work thus provides experimental proof of important commonalities between the detailed mechanisms of FeSOD and MnSOD. Fe-containing superoxide dismutase (FeSOD) and MnSOD are widely assumed to employ the same catalytic mechanism. However this has not been completely tested. In 1985, Bull and Fee showed that FeSOD took up a proton upon reduction [J. Am. Chem. Soc. 107 (1985) 3295]. We now demonstrate that MnSOD incorporates the same crucial coupling between electron transfer and proton transfer. The redox-coupled H(+) acceptor has been presumed to be the coordinated solvent molecule, in both FeSOD and MnSOD, however this is very difficult to test experimentally. We have now examined the most plausible alternative: that Tyr34 accepts a proton upon SOD reduction. We report specific incorporation of 13C in the C(zeta) positions of Tyr residues, assignment of the C(zeta) signal of Tyr34 in each of oxidized FeSOD and MnSOD, and direct NMR observations showing that in both cases, Tyr34 is in the neutral protonated state. Thus Tyr34 cannot accept a proton upon SOD reduction, and coordinated solvent is concluded to be the redox-coupled H(+) acceptor instead, in both FeSOD and MnSOD. We have also confirmed by direct 13C observation that the pK of 8.5 of reduced FeSOD corresponds to deprotonation of Tyr34. This work thus provides experimental proof of important commonalities between the detailed mechanisms of FeSOD and MnSOD. |
| Author | Miller, Anne-Frances Padmakumar, K. Sorkin, David L. Karapetian, A. Vance, Carrie K. |
| Author_xml | – sequence: 1 givenname: Anne-Frances surname: Miller fullname: Miller, Anne-Frances email: afm@pop.uky.edu organization: Departments of Chemistry and Biochemistry, University of Kentucky, Rose Street, Lexington, KY 40506-0055, USA – sequence: 2 givenname: K. surname: Padmakumar fullname: Padmakumar, K. organization: Departments of Chemistry and Biochemistry, University of Kentucky, Rose Street, Lexington, KY 40506-0055, USA – sequence: 3 givenname: David L. surname: Sorkin fullname: Sorkin, David L. organization: Department of Chemistry, The Johns Hopkins University, Baltimore, MD 21218, USA – sequence: 4 givenname: A. surname: Karapetian fullname: Karapetian, A. organization: Departments of Chemistry and Biochemistry, University of Kentucky, Rose Street, Lexington, KY 40506-0055, USA – sequence: 5 givenname: Carrie K. surname: Vance fullname: Vance, Carrie K. organization: Jenkins Department of Biophysics, The Johns Hopkins University, Baltimore, MD 21218, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/12538055$$D View this record in MEDLINE/PubMed |
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| Keywords | FeSOD Superoxide dismutase Proton-coupled electron transfer MnSOD |
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1458 Rogers (10.1016/S0162-0134(02)00621-9_BIB60) 1988; 228 Valcour (10.1016/S0162-0134(02)00621-9_BIB44) 1986; 66 Miller (10.1016/S0162-0134(02)00621-9_BIB6) 2001 Bull (10.1016/S0162-0134(02)00621-9_BIB10) 1991; 113 Burgess (10.1016/S0162-0134(02)00621-9_BIB69) 1990; 90 Vance (10.1016/S0162-0134(02)00621-9_BIB36) 1998; 37 Joshi (10.1016/S0162-0134(02)00621-9_BIB73) 1993; 175 Barrette (10.1016/S0162-0134(02)00621-9_BIB5) 1983; 22 Hsu (10.1016/S0162-0134(02)00621-9_BIB42) 1996; 271 10.1016/S0162-0134(02)00621-9_BIB75 Ingraham (10.1016/S0162-0134(02)00621-9_BIB7) 1985 Hirst (10.1016/S0162-0134(02)00621-9_BIB63) 1998; 120 Whittaker (10.1016/S0162-0134(02)00621-9_BIB29) 1997; 36 Leitch (10.1016/S0162-0134(02)00621-9_BIB15) 1984; 23 Bull (10.1016/S0162-0134(02)00621-9_BIB9) 1985; 107 Shaka (10.1016/S0162-0134(02)00621-9_BIB46) 1983; 53 Smallcombe (10.1016/S0162-0134(02)00621-9_BIB48) 1995; 117 Barker (10.1016/S0162-0134(02)00621-9_BIB61) 1992; 114 Beyer (10.1016/S0162-0134(02)00621-9_BIB39) 1987; 26 Li (10.1016/S0162-0134(02)00621-9_BIB57) 1996; 35 Carlioz (10.1016/S0162-0134(02)00621-9_BIB33) 1986; 5 |
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| Snippet | Fe-containing superoxide dismutase (FeSOD) and MnSOD are widely assumed to employ the same catalytic mechanism. However this has not been completely tested. In... |
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| SubjectTerms | Binding Sites Electron Transport Electrons FeSOD Hydrogen-Ion Concentration Iron - metabolism Magnetic Resonance Spectroscopy Manganese - metabolism MnSOD Models, Molecular Protein Conformation Proton-coupled electron transfer Protons Superoxide dismutase Superoxide Dismutase - chemistry Superoxide Dismutase - metabolism |
| Title | Proton-coupled electron transfer in Fe-superoxide dismutase and Mn-superoxide dismutase |
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