Different modes of carbon monoxide binding to acetyl-CoA synthase and the role of a conserved phenylalanine in the coordination environment of nickel

Biochemistry

Volumn 52, Issue 10, 2013, Pages 1705-1716

  Gencic, Simonida ^a   Kelly, Kayla ^b,d   Ghebreamlak, Selamawit ^c   Duin, Evert C ^c   Grahame, David A ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b Holton Arms School   (United States)

^c AUBURN UNIVERSITY   (United States)

^d GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC PROPERTIES; CONFORMATIONAL CHANGE; COORDINATION ENVIRONMENT; METHYLATION REACTION; MULTIENZYME COMPLEXES; PROTEIN CONFORMATIONAL CHANGES; STOPPED-FLOW METHOD; SUBSTRATE REACTIVITIES;

ALKYLATION; AMINO ACIDS; CARBON MONOXIDE; ENZYMES; MAGNETIC RESONANCE; PARAMAGNETISM; SUBSTRATES;

NICKEL;

ACETYL COENZYME A; ACETYL COENZYME A SYNTHETASE; CARBON MONOXIDE; COORDINATION COMPOUND; CORRINOID; NICKEL; PHENYL GROUP; PHENYLALANINE;

ARTICLE; CATALYSIS; CHEMICAL BINDING; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTRON SPIN RESONANCE; ENZYME SUBSTRATE; ENZYME SYNTHESIS; METHYLATION; NUCLEOPHILICITY; PRIORITY JOURNAL; REACTION OPTIMIZATION; STEADY STATE; TITRIMETRY;

ALDEHYDE OXIDOREDUCTASES; ARCHAEAL PROTEINS; BACTERIAL PROTEINS; CARBON MONOXIDE; COENZYME A LIGASES; CONSERVED SEQUENCE; ELECTRON SPIN RESONANCE SPECTROSCOPY; KINETICS; METHANOSARCINA; MODELS, MOLECULAR; MOORELLA; MULTIENZYME COMPLEXES; MUTAGENESIS, SITE-DIRECTED; NICKEL; PHENYLALANINE; PROTEIN CONFORMATION; PROTEIN SUBUNITS;

EID: 84874954687     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3016718     Document Type: Article

References (44)

1. Doukov, T. I., Iverson, T. M., Seravalli, J., Ragsdale, S. W., and Drennan, C. L. (2002) A Ni-Fe-Cu center in a bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase Science 298, 567-572
2. 4] clusters in closed and open subunits of acetyl-CoA synthase/carbon monoxide dehydrogenase Nat. Struct. Biol. 10, 271-279
3. Svetlitchnyi, V., Dobbek, H., Meyer-Klaucke, W., Meins, T., Thiele, B., Romer, P., Huber, R., and Meyer, O. (2004) A functional Ni-Ni-[4Fe-4S] cluster in the monomeric acetyl-CoA synthase from Carboxydothermus hydrogenoformans Proc. Natl. Acad. Sci. U.S.A. 101, 446-451
4. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C., Gonzales, N. R., Gwadz, M., Hurwitz, D. I., Jackson, J. D., Ke, Z., Lanczycki, C. J., Lu, F., Marchler, G. H., Mullokandov, M., Omelchenko, M. V., Robertson, C. L., Song, J. S., Thanki, N., Yamashita, R. A., Zhang, D., Zhang, N., Zheng, C., and Bryant, S. H. (2011) CDD: A Conserved Domain Database for the functional annotation of proteins Nucleic Acids Res. 39, D225-D229
5. 2 tunnel gating mechanism in the bifunctional carbon monoxide dehydrogenase/acetyl coenzyme A synthase from Moorella thermoacetica J. Biol. Inorg. Chem. 9, 525-532
6. Gencic, S., Duin, E. C., and Grahame, D. A. (2010) Tight coupling of partial reactions in the acetyl-CoA decarbonylase/synthase (ACDS) multienzyme complex from Methanosarcina thermophila: Acetyl C-C bond fragmentation at the A cluster promoted by protein conformational changes J. Biol. Chem. 285, 15450-15463
7. Zou, X., Evans, D. R., and Brown, K. L. (1995) Efficient and convenient method for axial nucleotide removal from vitamin B12 and its derivatives Inorg. Chem. 34, 1634-1635
8. Gencic, S. and Grahame, D. A. (2008) Two separate one-electron steps in the reductive activation of the A cluster in subunit β of the ACDS complex in Methanosarcina thermophila Biochemistry 47, 5544-5555
9. Gencic, S. and Grahame, D. A. (2003) Nickel in subunit β of the acetyl-CoA decarbonylase/synthase multienzyme complex in methanogens. Catalytic properties and evidence for a binuclear Ni-Ni site J. Biol. Chem. 278, 6101-6110
10. Grahame, D. A. (2011) Methods for analysis of acetyl-CoA synthase: Applications to bacterial and archaeal systems Methods Enzymol. 494, 189-217
11. Tonomura, B., Nakatani, H., Ohnishi, M., Yamaguchi-Ito, J., and Hiromi, K. (1978) Test reactions for a stopped-flow apparatus. Reduction of 2,6-dichlorophenolindophenol and potassium ferricyanide by l -ascorbic acid Anal. Biochem. 84, 370-383
12. Dean, J. A. (1992) Lange's Handbook of Chemistry, 14th ed., McGraw-Hill, Inc., New York.
13. Lu, W. P. and Ragsdale, S. W. (1991) Reductive activation of the coenzyme A/acetyl-CoA isotopic exchange reaction catalyzed by carbon monoxide dehydrogenase from Clostridium thermoaceticum and its inhibition by nitrous oxide and carbon monoxide J. Biol. Chem. 266, 3554-3564
14. Seravalli, J., Kumar, M., and Ragsdale, S. W. (2002) Rapid kinetic studies of acetyl-CoA synthesis: Evidence supporting the catalytic intermediacy of a paramagnetic NiFeC species in the autotrophic Wood-Ljungdahl pathway Biochemistry 41, 1807-1819
15. Bhaskar, B., DeMoll, E., and Grahame, D. A. (1998) Redox-dependent acetyl transfer partial reaction of the acetyl-CoA decarbonylase/synthase complex: Kinetics and mechanism Biochemistry 37, 14491-14499
16. 2 pressures J. Am. Chem. Soc. 123, 4697-4703
17. Tan, X. S., Sewell, C., and Lindahl, P. A. (2002) Stopped-flow kinetics of methyl group transfer between the corrinoid-iron-sulfur protein and acetyl-coenzyme A synthase from Clostridium thermoaceticum J. Am. Chem. Soc. 124, 6277-6284
18. Tan, X., Sewell, C., Yang, Q., and Lindahl, P. A. (2003) Reduction and methyl transfer kinetics of the α subunit from acetyl coenzyme A synthase J. Am. Chem. Soc. 125, 318-319
19. Tan, X., Loke, H. K., Fitch, S., and Lindahl, P. A. (2005) The tunnel of acetyl-coenzyme A synthase/carbon monoxide dehydrogenase regulates delivery of CO to the active site J. Am. Chem. Soc. 127, 5833-5839
20. Tan, X., Surovtsev, I. V., and Lindahl, P. A. (2006) Kinetics of CO insertion and acetyl group transfer steps, and a model of the acetyl-CoA synthase catalytic mechanism J. Am. Chem. Soc. 128, 12331-12338
21. Bender, G. and Ragsdale, S. W. (2011) Evidence that ferredoxin interfaces with an internal redox shuttle in acetyl-CoA synthase during reductive activation and catalysis Biochemistry 50, 276-286
22. Ragsdale, S. W., Ljungdahl, L. G., and DerVartanian, D. V. (1982) EPR evidence for nickel-substrate interaction in carbon monoxide dehydrogenase from Clostridium thermoaceticum Biochem. Biophys. Res. Commun. 108, 658-663
23. 61Ni isotope substitutions confirm the presence of a nickel (III)-carbon species in acetogenic CO dehydrogenases Biochem. Biophys. Res. Commun. 115, 658-665
24. Ragsdale, S. W., Wood, H. G., and Antholine, W. E. (1985) Evidence that an iron-nickel-carbon complex is formed by reaction of CO with the CO dehydrogenase from Clostridium thermoaceticum Proc. Natl. Acad. Sci. U.S.A. 82, 6811-6814
25. 2 and argon atmospheres J. Biol. Chem. 265, 3873-3879
26. Grahame, D. A., Khangulov, S., and DeMoll, E. (1996) Reactivity of a paramagnetic enzyme-CO adduct in acetyl-CoA synthesis and cleavage Biochemistry 35, 593-600
27. Terlesky, K. C., Barber, M. J., Aceti, D. J., and Ferry, J. G. (1987) EPR properties of the Ni-Fe-C center in an enzyme complex with carbon monoxide dehydrogenase activity from acetate-grown Methanosarcina thermophila. Evidence that acetyl-CoA is a physiological substrate J. Biol. Chem. 262, 15392-15395
28. Barondeau, D. P. and Lindahl, P. A. (1997) Methylation of carbon monoxide dehydrogenase from Clostridium thermoaceticum and mechanism of acetyl coenzyme A synthesis J. Am. Chem. Soc. 119, 3959-3970
29. Bender, G., Stich, T. A., Yan, L., Britt, R. D., Cramer, S. P., and Ragsdale, S. W. (2010) Infrared and EPR spectroscopic characterization of a Ni(I) species formed by photolysis of a catalytically competent Ni(I)-CO intermediate in the acetyl-CoA synthase reaction Biochemistry 49, 7516-7523
30. Shin, W., Stafford, P. R., and Lindahl, P. A. (1992) Redox titrations of carbon monoxide dehydrogenase from Clostridium thermoaceticum Biochemistry 31, 6003-6011
31. 2 Biochemistry 37, 10016-10026
32. Fraser, D. M. and Lindahl, P. A. (1999) Stoichiometric CO reductive titrations of acetyl-CoA synthase (carbon monoxide dehydrogenase) from Clostridium thermoaceticum Biochemistry 38, 15697-15705
33. 2 Metallomics 3, 797-815
34. Fontecilla-Camps, J. C., Amara, P., Cavazza, C., Nicolet, Y., and Volbeda, A. (2009) Structure-function relationships of anaerobic gas-processing metalloenzymes Nature 460, 814-822
35. p(0)-based mechanism of catalysis J. Biol. Inorg. Chem. 9, 516-524
36. 3): Relevance to the mechanism of acetyl coenzyme A synthase J. Am. Chem. Soc. 129, 9286-9287
37. Ito, M., Kotera, M., Matsumoto, T., and Tatsumi, K. (2009) Dinuclear nickel complexes modeling the structure and function of the acetyl CoA synthase active site Proc. Natl. Acad. Sci. U.S.A. 106, 11862-11866
38. Seravalli, J. and Ragsdale, S. W. (2008) Pulse-chase studies of the synthesis of acetyl-CoA by carbon monoxide dehydrogenase/acetyl-CoA synthase: Evidence for a random mechanism of methyl and carbonyl addition J. Biol. Chem. 283, 8384-8394
39. George, S. J., Seravalli, J., and Ragsdale, S. W. (2005) EPR and infrared spectroscopic evidence that a kinetically competent paramagnetic intermediate is formed when acetyl-coenzyme A synthase reacts with CO J. Am. Chem. Soc. 127, 13500-13501
40. Gorst, C. M. and Ragsdale, S. W. (1991) Characterization of the NiFeCO complex of carbon monoxide dehydrogenase as a catalytically competent intermediate in the pathway of acetyl-coenzyme A synthesis J. Biol. Chem. 266, 20687-20693
41. Bar-Even, A. (2012) Does acetogenesis really require especially low reduction potential? Biochim. Biophys. Acta 24, 01055-01059
42. Doukov, T. I., Blasiak, L. C., Seravalli, J., Ragsdale, S. W., and Drennan, C. L. (2008) Xenon in and at the end of the tunnel of bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase Biochemistry 47, 3474-3483
43. Segel, I. H. (1975) Enzyme kinetics: Behavior and analysis of rapid equilibrium and steady-state systems, Wiley-Interscience, New York.
44. Hagen, W. R. (2009) Biomolecular EPR Spectroscopy, CRC Press, Boca Raton, FL.