Short circuiting a sulfite oxidising enzyme with direct electrochemistry: Active site substitutions and their effect on catalysis and electron transfer

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1807, Issue 1, 2011, Pages 108-118

  Rapson, Trevor D ^a   Kappler, Ulrike ^a   Hanson, Graeme R ^a   Bernhardt, Paul V ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Enzyme; Molybdenum; Voltammetry

Indexed keywords

ENZYME VARIANT; HEME; MOLYBDENUM; SULFITE DEHYDROGENASE;

AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; ELECTROCHEMISTRY; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; OXIDATION REDUCTION POTENTIAL; PH; POTENTIOMETRY; PRIORITY JOURNAL;

AMINO ACID SUBSTITUTION; ARGININE; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ELECTROCHEMISTRY; ELECTRON TRANSPORT; GENETIC VARIATION; HEME; HISTIDINE; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTEIN CONFORMATION; SULFITE DEHYDROGENASE;

STARKEYA NOVELLA;

EID: 78249234155     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.09.005     Document Type: Article

References (50)

1. Kappler U. Bacterial sulfite dehydrogenases - enzymes for chemolithtrophs only?. Microbial Sulfur Metabolism 2007, Springer, Berlin. C.G. Friedrich, C. Dahl (Eds.).
2. Hille R. Molybdenum enzymes. Essays Biochem. 1999, 34:125-137.
3. Kappler U., Bailey S. Molecular basis of intramolecular electron transfer in sulfite-oxidizing enzymes is revealed by high resolution structure of a heterodimeric complex of the catalytic molybdopterin subunit and a c-type cytochrome subunit. J. Biol. Chem. 2005, 280:24999-25007.
4. Kappler U., Bailey S. Crystallization and preliminary x-ray analysis of sulfite dehydrogenase from Starkeya novella. Acta Crystallogr., Sect D: Biol. Crystallogr. D 2004, 60:2070-2072.
5. Hille R. The mononuclear molybdenum enzymes. Chem. Rev. 1996, 96:2757-2816.
6. Hille R. Molybdenum enzymes containing the pyranopterin cofactor: an overview. Molybdenum and Tungsten: Their Roles in Biological Processes 2002, 39:187-226.
7. Bernhardt P.V. Communicating with the mononuclear molybdoenzymes: emerging opportunities and applications in redox enzyme biosensors. Royal Society of Chemistry 2009, J.J. Davis (Ed.).
8. Kisker C., Schindelin H., Pacheco A., Wehbi W.A., Garrett R.M., Rajagopalan K.V., Enemark J.H., Rees D.C. Molecular basis of sulfite oxidase deficiency from the structure of sulfite oxidase. Cell 1997, 91:973-983.
9. Mendel R.R., Bittner F. Cell biology of molybdenum. Biochim. Biophys. Acta Mol. Cell Res. 2006, 1763:621-635.
10. Kappler U., Bennett B., Rethmeier J., Schwarz G., Deutzmann R., McEwan A.G., Dahl C. Sulfite:cytochrome c oxidoreductase from Thiobacillus novellus. Purification, characterization, and molecular biology of a heterodimeric member of the sulfite oxidase family. J. Biol. Chem. 2000, 275:13202-13212.
11. Wilson J.J., Kappler U. Sulfite oxidation in Sinorhizobium meliloti. Biochim. Biophys. Acta Bioenerg. 2009, 1787:1516-1525.
12. Feng C.J., Tollin G., Enemark J.H. Sulfite oxidizing enzymes. Biochim. Biophys. Acta: Proteins Proteomics 2007, 1774:527-539.
13. Bailey S., Rapson T., Johnson-Winters K., Astashkin A.V., Enemark J.H., Kappler U. Molecular basis for enzymatic sulfite oxidation: how three conserved active site residues shape enzyme activity. J. Biol. Chem. 2009, 284:2053-2063.
14. Kappler U., Bailey S., Feng C., Honeychurch M.J., Hanson G.R., Bernhardt P.V., Tollin G., Enemark J.H. Kinetic and structural evidence for the importance of Tyr236 for the integrity of the Mo active site in a bacterial sulfite dehydrogenase. Biochemistry 2006, 45:9696-9705.
15. Emesh S., Rapson T.D., Rajapakshe A., Kappler U., Bernhardt P.V., Tollin G., Enemark J.H. Intramolecular electron transfer in sulfite-oxidizing enzymes: elucidating the role of a conserved active site arginine. Biochemistry 2009, 48:2156-2163.
16. Leger C., Bertrand P. Direct electrochemistry of redox enzymes as a tool for mechanistic studies. Chem. Rev. 2008, 108:2379-2438.
17. Bernhardt P.V. Enzyme electrochemistry - biocatalysis on an electrode. Aust. J. Chem. 2006, 59:233-256.
18. Armstrong F.A. Recent developments in dynamic electrochemical studies of adsorbed enzymes and their active sites. Curr. Opin. Chem. Biol. 2005, 9:110-117.
19. Aguey-Zinsou K.-F., Bernhardt P.V., Kappler U., McEwan A.G. Direct electrochemistry of a bacterial sulfite dehydrogenase. J. Am. Chem. Soc. 2003, 125:530-535.
20. Rapson T.D., Kappler U., Bernhardt P.V. Direct catalytic electrochemistry of sulfite dehydrogenase: mechanistic insights and contrasts with related Mo enzymes. Biochim. Biophys. Acta Bioenerg. 2008, 1777:1319-1325.
21. Elliott S.J., McElhaney A.E., Feng C.J., Enemark J.H., Armstrong F.A. A voltammetric study of interdomain electron transfer within sulfite oxidase. J. Am. Chem. Soc. 2002, 124:11612-11613.
22. Kappler U., McEwan A.G. A system for the heterologous expression of complex redox proteins in Rhodobacter capsulatus: characterisation of recombinant sulphite:cytochrome c oxidoreductase from Starkeya novella. FEBS Lett. 2002, 529:208-214.
23. Codd R., Astashkin A.V., Pacheco A., Raitsimring A.M., Enemark J.H. Pulsed ELDOR spectroscopy of the Mo(V)/Fe(III) state of sulfite oxidase prepared by one-electron reduction with Ti(III) citrate. J. Biol. Inorg. Chem. 2002, 7:338-350.
24. Bernhardt P.V., Chen K.-I., Sharpe P.C. Transition metal complexes as mediator-titrants in protein redox potentiometry. J. Biol. Inorg. Chem. 2006, 11:930-936.
25. Heering H.A., Hirst J., Armstrong F.A. Interpreting the catalytic voltammetry of electroactive enzymes adsorbed on electrodes. J. Phys. Chem. B 1998, 102:6889-6902.
26. Leger C., Elliott S.J., Hoke K.R., Jeuken L.J.C., Jones A.K., Armstrong F.A. Enzyme electrokinetics: using protein film voltammetry to investigate redox enzymes and their mechanisms. Biochemistry 2003, 42:8653-8662.
27. Brody M.S., Hille R. The kinetic behavior of chicken liver sulfite oxidase. Biochemistry 1999, 38:6668-6677.
28. Heffron K., Leger C., Rothery R.A., Weiner J.H., Armstrong F.A. Determination of an optimal potential window for catalysis by E. coli dimethyl sulfoxide reductase and hypothesis on the role of Mo(V) in the reaction pathway. Biochemistry 2001, 40:3117-3126.
29. Spence J.T., Kipke C.A., Enemark J.H., Sunde R.A. Stoichiometry of electron uptake and the effect of anions and pH on the molybdenum and heme reduction potentials of sulfite oxidase. Inorg. Chem. 1991, 30:3011-3015.
30. Ferapontova E.E., Christenson A., Hellmark A., Ruzgas T. Spectroelectrochemical study of heme- and molybdopterin cofactor-containing chicken liver sulphite oxidase. Bioelectrochemistry 2004, 63:49-53.
31. Feng C., Kappler U., Tollin G., Enemark J.H. Intramolecular electron transfer in a bacterial sulfite dehydrogenase. J. Am. Chem. Soc. 2003, 125:14696-14697.
32. Sullivan E.P., Hazzard J.T., Tollin G., Enemark J.H. Electron transfer in sulfite oxidase: effects of pH and anions on transient kinetics. Biochemistry 1993, 32:12465-12470.
33. Pacheco A., Hazzard J.T., Tollin G., Enemark J.H. The pH dependence of intramolecular electron transfer rates in sulfite oxidase at high and low anion concentrations. J. Biol. Inorg. Chem. 1999, 4:390-401.
34. Feng C., Kedia R.V., Hazzard J.T., Hurley J.K., Tollin G., Enemark J.H. Effect of solution viscosity on intramolecular electron transfer in sulfite oxidase. Biochemistry 2002, 41:5816-5821.
35. Feng C.J., Wilson H.L., Tollin G., Astashkin A.V., Hazzard J.T., Rajagopalan K.V., Enemark J.H. The pathogenic human sulfite oxidase mutants G473D and A208D are defective in intramolecular electron transfer. Biochemistry 2005, 44:13734-13743.
36. Coury L.A., Oliver B.N., Egekeze J.O., Sosnoff C.S., Brumfield J.C., Buck R.P., Murray R.W. Mediated, anaerobic voltammetry of sulfite oxidase. Anal. Chem. 1990, 62:452-458.
37. Coury L.A., Murray R.W., Johnson J.L., Rajagopalan K.V. Electrochemical study of kinetics of electron transfer between synthetic electron acceptors and reduced molybdoheme protein sulfite oxidase. J. Phys. Chem. 1991, 95:6034-6040.
38. Coury L.A., Yang L., Murray R.W. Electrochemical study of the rate of activation of the molybdoheme protein sulfite oxidase by organic electron acceptors. Anal. Chem. 1993, 65:242-246.
39. Ferapontova E.E., Ruzgas T., Gorton L. Direct electron transfer of heme- and molybdopterin cofactor-containing chicken liver sulfite oxidase on alkanethiol-modified gold electrodes. Anal. Chem. 2003, 75:4841-4850.
40. Dronov R., Kurth D.G., Mohwald H., Spricigo R., Leimkuehler S., Wollenberger U., Rajagopalan K.V., Scheller F.W., Lisdat F. Layer-by-layer arrangement by protein-protein interaction of sulfite oxidase and cytochrome c catalyzing oxidation of sulfite. J. Am. Chem. Soc. 2008, 130:1122.
41. Spricigo R., Dronov R., Rajagopalan K.V., Lisdat F., Leimkuehler S., Scheller F.W., Wollenberger U. Electrocatalytically functional multilayer assembly of sulfite oxidase and cytochrome c. Soft Matter 2008, 4:972-978.
42. Spricigo R., Dronov R., Lisdat F., Leimkuehler S., Scheller F.W., Wollenberger U. Electrocatalytic sulfite biosensor with human sulfite oxidase co-immobilized with cytochrome c in a polyelectrolyte-containing multilayer. Anal. Bioanal. Chem. 2009, 393:225-233.
43. Elliott S.J., Leger C., Pershad H.R., Hirst J., Heffron K., Ginet N., Blasco F., Rothery R.A., Weiner J.H., Armstrong F.A. Detection and interpretation of redox potential optima in the catalytic activity of enzymes. Biochim. Biophys. Acta Bioenerg. 2002, 1555:54-59.
44. Leger C., Lederer F., Guigliarelli B., Bertrand P. Electron flow in multicenter enzymes: theory, applications, and consequences on the natural design of redox chains. J. Am. Chem. Soc. 2006, 128:180-187.
45. Anderson L.J., Richardson D.J., Butt J.N. Using direct electrochemistry to probe rate limiting events during nitrate reductase turnover. Faraday Discuss. 2000, 116:155-169.
46. Anderson L.J., Richardson D.J., Butt J.N. Catalytic protein film voltammetry from a respiratory nitrate reductase provides evidence for complex electrochemical modulation of enzyme activity. Biochemistry 2001, 40:11294-11307.
47. Butt J.N., Anderson L.J., Rubio L.M., Richardson D.J., Flores E., Herrero A. Enzyme-catalysed nitrate reduction-themes and variations as revealed by protein film voltammetry. Bioelectrochemistry 2002, 56:17-18.
48. Elliott S.J., Hoke K.R., Heffron K., Palak M., Rothery R.A., Weiner J.H., Armstrong F.A. Voltammetric studies of the catalytic mechanism of the respiratory nitrate reductase from Escherichia coli: how nitrate reduction and inhibition depend on the oxidation state of the active site. Biochemistry 2004, 43:799-807.
49. Frangioni B., Arnoux P., Sabaty M., Pignol D., Bertrand P., Guigliarelli B., Leger C. In Rhodobacter sphaeroides respiratory nitrate reductase, the kinetics of substrate binding favors intramolecular electron transfer. J. Am. Chem. Soc. 2004, 126:1328-1329.
50. Davis J.J., Hill H.A.O. The scanning probe microscopy of metalloproteins and metalloenzymes. Chem. Commun. 2002, 393-401.