Abstract
The reaction enthalpy and entropy for the one-electron reduction of the ferric heme in horse heart and sperm whale aquometmyoglobins (Mb) have been determined exploiting a spectroelectrochemical approach. Also investigated were the T67R, T67K, T67R/S92D and T67R/S92D Mb-H variants (the latter containing a protoheme-l-histidine methyl ester) of sperm whale Mb, which feature peroxidase-like activity. The reduction potential (E°′) in all species consists of an enthalpic term which disfavors Fe3+ reduction and a larger entropic contribution which instead selectively stabilizes the reduced form. This behavior differs from that of the heme redox enzymes and electron transport proteins investigated so far. The reduction thermodynamics in the series of sperm whale Mb variants show an almost perfect enthalpy–entropy compensation, indicating that the mutation-induced changes in \( \Delta H^{{{^\circ }\ifmmode{'}\else$'$\fi }}_{{{\text{rc}}}} \;{\text{and }}\Delta S^{{{^\circ }\ifmmode{'}\else$'$\fi }}_{{{\text{rc}}}} {\text{ }} \) are dominated by reduction-induced solvent reorganization effects. The modest changes in E°′ originate from the enthalpic effects of the electrostatic interactions of the heme with the engineered charged residues. The small influence that the mutations exert on the reduction potential of myoglobin suggests that the increased peroxidase activity of the variants is not related to changes in the redox reactivity of the heme iron, but are likely related to a more favored substrate orientation within the distal heme cavity.
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References
Cowan JA (1997) Inorganic biochemistry an introduction. Wiley-VCH, New York
Voet D, Voet JG (1995) Biochemistry. Wiley, New York
Messerschmidt A, Huber R, Poulos T, Wieghardt K (eds) (2001) Handbook of metalloproteins, vol 1. Wiley, Chichester
Reedy CJ, Gibney BR (2004) Chem Rev 104:617–649
Gray HB, Winkler JR (1996) Annu Rev Biochem 65:537–561
Gray HB, Winkler JR (2003) Q Rev Biophys 36:341–372
Zhou H-X (1997) J Biol Inorg Chem 2:109–113
Mauk AG, Moore GR (1997) J Biol Inorg Chem 2:119–125
Gunner MR, Alexov E, Torres E, Lipovaca S (1997) J Biol Inorg Chem 2:126–134
Armstrong FA (1997) J Biol Inorg Chem 2:139–142
Warshel A, Papazyan A, Muegge I (1997) J Biol Inorg Chem 2:143–152
Muegge I, Qi PX, Wand AJ, Chu ZT, Warshel A (1997) J Phys Chem B 101:825–836
Winkler JR, Wittung-Stafshede P, Lerckner J, Malmström BG, Gray HB (1997) Proc Natl Acad Sci USA 94:4246–4249
Battistuzzi G, Borsari M, Cowan JA, Ranieri A, Sola M (2002) J Am Chem Soc 124:5315–5324
Battistuzzi G, Borsari M, Di Rocco G, Ranieri A, Sola M (2004) J Biol Inorg Chem 9:23–26
Battistuzzi G, Borsari M, Ranieri A, Sola M (2004) J Biol Inorg Chem 9:781–787
Moore GR, Pettigrew GW (1990) Cytochromes c: evolutionary, structural and physicochemical aspects. Springer, Berlin
Wittung-Stafshede P, Gomez E, Ohman A, Aasa R, Villahermosa RM, Leckner J, Karlsson BG, Sanders D, Fee JA, Winkler JR, Malmstrom BG, Gray HB, Hill MG (1998) Biochim Biophys Acta 1388:437–443
Eidsness MK, Burden AE, Richie KA, Kurtz DM, Scott RA, Smith ET, Ichiye T, Beard B, Min T, Kang C (1999) Biochemistry 38:14803–14809
Mao J, Hauser K, Gunner MR (2003) Biochemistry 42:9829–9840
Bertrand P, Mbarki O, Asso M, Blanchard L, Guerlesquin F, Tegoni M (1995) Biochemistry 34:11071–11079
Battistuzzi G, Borsari M, Francia F, Sola M (1997) Biochemistry 36:16247–16258
Battistuzzi G, Borsari M, Loschi L, Sola M (1999) J Biol Inorg Chem 4:601–607
Battistuzzi G, Borsari M, Rossi G, Sola M (1998) Inorg Chim Acta 272:397–402
Battistuzzi G, Borsari M, Cowan JA, Eicken C, Loschi L, Sola M (1999) Biochemistry 38:5553–5562
Terui N, Tachiiri N, Matsuo H, Hasegawa J, Uchiyama S, Kobayashi Y, Igarashi Y, Sambongi Y, Yamamoto Y (2003) J Am Chem Soc 125:13650–13651
Grealis C, Magner E (2003) Langmuir 19:1282–1286
O’Reilly NJ, Magner E (2005) Langmuir 21:1009–1014
Ivanova EV, Magner E (2005) Electrochem Commun 7:323–327
Bartalesi I, Bertini I, Di Rocco G, Ranieri A, Rosato A, Vanarotti M, Vasos PR, Viezzoli MS (2004) J Biol Inorg Chem 9:600–608
Duah-Williams L, Hawkridge FM (1999) J Elecroanal Chem 466:177–186
Ray A, Feng M, Tachikawa H (2005) Langmuir 21:1009–1014
Bortolotti CA, Battistuzzi G, Borsari M, Facci P, Ranieri A, Sola M (2006) J Am Chem Soc 128:5444–5451
Battistuzzi G, Borsari M, Ranieri A, Sola M (2002) J Am Chem Soc 124:26–27
Battistuzzi G, Bellei M, Borsari M, Di Rocco G, Ranieri A, Sola M (2005) J Biol Inorg Chem 10:643–651
Bellei M, Jakopitsch C, Battistuzzi G, Sola M, Obinger C (2006) Biochemistry 45:4768–4774
Battistuzzi G, Bellei M, De Rienzo F, Sola M (2006) J Biol Inorg Chem 11:586–592
Battistuzzi G, Bellei M, Zederbauer M, Furtmüller P, Sola M, Obinger C (2006) Biochemistry 45:12750–12755
Phillips GN Jr (2001) In: Messerschmidt A, Huber R, Poulos T, Wieghardt K (eds) Handbook of metalloproteins, vol 1. Wiley, Chichester, pp 5–15
Roncone R, Monzani E, Nicolis S, Casella L (2004) Eur J Inorg Chem:2203–2213
Brunori M (2001) Trends Biochem Sci 26:21–23
Wittenberg JB, Wittenberg BA (1990) Annu Rev Biochem Biophys Chem 19:217–241
Nakamura M, Nakamura S (1996) Biophys Biochim Acta 1289:329–335
Lu Y, Berry SM, Pfister TD (2001) Chem Rev 101:3047–3080
Ozaki S, Matsui T, Roach MP, Watanabe Y (2000) Coord Chem Rev 198:39–59
Watanabe Y (2002) Curr Opin Chem Biol 6:1–9
Roncone R, Monzani E, Labò S, Sanangelantoni AM, Casella L (2005) J Biol Inorg Chem 10:11–24
Redaelli C, Monzani E, Santagostini L, Casella L, Sanangelantoni AM, Pierattelli R, Banci L (2002) ChemBioChem 3:226–233
Roncone R, Monzani E, Murtas M, Battaini G, Pennati A, Sanangelantoni AM, Zuccotti S, Bolognesi M, Casella L (2004) Biochem J 377:717–724
Dong S, Niu J, Cotton TM (1995) Methods Enzymol 246:701–735
Yee EL, Cave RJ, Guyer KL, Tyma PD, Weaver MJ (1979) J Am Chem Soc 101:1131–1137
Heineman WR, Meckstroth ML, Norris BJ, Su C-H (1979) Bioelectrochem Bioenerg 6:577–585
Millis CV, Cai D, Stankovic MT, Tien M (1989) Biochemistry 28:8484–8489
Farhangrazi ZS, Fossett ME, Powers LS, Ellis WR Jr (1995) Biochemistry 34:2866–2871
Varadarajan R, Zewert TE, Gray HB, Boxer SG (1989) Science 243:69–71
King BC, Hawkridge FM, Hoffman BM (1992) J Am Chem Soc 114:10603–10608
Dangi B, Blankman JI, Miller CJ, Volkman BF, Guiles RD (1998) J Phys Chem B 102:8201–8208
Evans SV, Brayer GD (1990) J Mol Biol 213:885–897
Quillin ML, Arduini RM, Olson JS, Phillips GN Jr (1993) J Mol Biol 234:140–155
Yang F, Phillips GN Jr (1996) J Mol Biol 256:762–774
Maurus R, Overall CM, Bogumil R, Luo Y, Mauk AG, Smith M, Brayer GD (1997) Biochim Biophys Acta 1341:1–13
Sola M, Battistuzzi G, Borsari M (2005) Chemtracts Inorg Chem 18:73–86
Brunori M, Bourgeois D, Vallone B (2004) J Struct Biol 147:223–234
Cao W, Christian JF, Champion PM, Rosca F, Sage JT (2001) Biochemistry 40:5728–5737
Battistuzzi G, Borsari M, Loschi L, Menziani MC, De Rienzo F, Sola M (2001) Biochemistry 40:6422–6430
Grunwald E, Steel C (1995) J Am Chem Soc 117:5687–5692
Liu L, Guo Q-X (2001) Chem Rev 101:673–695
Blokzijl W, Engberts JBNF (1993) Angew Chem Int Ed Engl 32:1545–1579
Lumry R, Rajender S (1970) Biopolymers 9:1125–1227
Battistuzzi G, Bellei M, Borsari M, Canters GW, de Waal E, Jeuken LJC, Ranieri A, Sola M (2003) Biochemistry 42:9214–9220
Thanabal V, de Ropp JS, La Mar GN (1988) J Am Chem Soc 110:3027–3035
de Ropp JS, Sham S, Asokan A, Newmyer S, Ortiz de Montellano P, La Mar GN (2002) J Am Chem Soc 124:11029–11037
Bolognesi M, Rosano C, Losso R, Borassi D, Rizzi M, Wittenberg JB, Boffi A, Ascenzi P (1999) Biophys J 77:1093–1099
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This work was supported by the Ministero dell’Universitá e della Ricerca Scientifica e Tecnologica of Italy and Fondazione Cassa di Risparmio di Modena 16/4/2002 and by the COST D21 action of the European Community (WG D21/0011/01).
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Battistuzzi, G., Bellei, M., Casella, L. et al. Redox reactivity of the heme Fe3+/Fe2+ couple in native myoglobins and mutants with peroxidase-like activity. J Biol Inorg Chem 12, 951–958 (2007). https://doi.org/10.1007/s00775-007-0267-1
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DOI: https://doi.org/10.1007/s00775-007-0267-1