Quantum catalysis in B12-dependent methylmalonyl-CoA mutase: Experimental and computational insights

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 361, Issue 1472, 2006, Pages 1333-1339

  Banerjee, Ruma ^a   Dybala Defratyka, Agnieszka ^b   Paneth, Piotr ^b  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b LODZ UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

B12; Cobalamin; Methylmalonyl CoA mutase; Tunnelling

Indexed keywords

BORON ISOTOPE; CARBON; CATALYSIS; COBALT; DEUTERIUM; ENZYME ACTIVITY; EXPERIMENTAL STUDY; HYDROGEN; ISOTOPIC ANALYSIS; OPTIMIZATION; RADICAL;

CARBON; COBALT; COBAMAMIDE; HYDROGEN; METHYLMALONYL COENZYME A MUTASE;

ARTICLE; CHEMICAL MODEL; CHEMISTRY; COMPARATIVE STUDY; KINETICS; TEMPERATURE; THERMODYNAMICS;

CARBON; COBALT; COBAMIDES; HYDROGEN; KINETICS; METHYLMALONYL-COA MUTASE; MODELS, CHEMICAL; TEMPERATURE; THERMODYNAMICS;

EID: 33748360330     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2006.1866     Document Type: Conference Paper

References (33)

1. Allen, S. H. G., Kellermeyer, R. W., Stjernholm, R. & Wood, H. G. 1964 Purification and properties of enzymes involved in the propionic acid fermentation. J. Bacteriol. 87, 171-187.
2. Bandarian, V. & Reed, G. H. 2000 Isotope effects in the transient phases of the reaction catalyzed by ethanolamine ammonia-lyase: determination of the number of exchangeable hydrogens in the enzyme-cofactor complex. Biochemistry 39, 12 069-12 075. (doi:10.1021/bi001014k)
3. 12-dependent mutases. Chem. Rev. 103, 2083-2094. (doi:10.1021/cr0204395)
4. 12: catalysis by cobalamin-dependent enzymes. Ann. Rev. Biochem. 72, 209-247. (doi:10.1146/annurev.biochem.72.121801.161828)
5. Chowdhury, S. & Banerjee, R. 2000a Evidence for quantum mechanical tunneling in the coupled cobalt carbon bond homolysis-substrate radical generation reaction catalyzed by methylmalonyl-CoA mutase. J. Am. Chem. Soc. 122, 5417-5418. (doi:10.1021/ja994302g)
6. 12-dependent methylmalonyl-CoA mutase. Biochemistry 39, 7998-8006. (doi:10.1021/bi992535e)
7. 12 analog 5′-deoxyadenosylcobinamide-GDP supports catalysis by methylmalonyl-CoA mutase in the absence of trans-ligand coordination. J. Biol. Chem. 276, 1015-1019. (doi:10.1074/jbc.M006842200)
8. Doll, K. M. & Finke, R. G. 2003 A compelling experimental test of the hypothesis that enzymes have evolved to enhance quantum mechanical tunneling in hydrogen transfer reactions; the beta-neopentylcobalamin system combined with prior adocobalamin data. J. Inorg. Chem. 42, 4849-4856.
9. Doll, K. M., Bender, B. R. & Finke, R. G. 2003 The first experimental test of the hypothesis that enzymes have evolved to enhance hydrogen tunneling. J. Am. Chem. Soc. 125, 10 877-10 884. (doi:10.1021/ja030120h)
10. Dybala-Defratyka, A., Paneth, P., Pu, J. & Truhlar, D. G. 2004 Benchmark results for hydrogen atom transfer between carbon centers and validation of electronic structure methods for bond energies and barrier heights. J. Phys. Chem. A108, 2475-2486.
11. Finke, R. G. & Hay, B. P. 1984 Thermolysis of adenosylcobalamin: a product, kinetic and Co-C5′ bond dissociation energy study. Inorg. Chem. 23, 3041-3043. (doi:10.1021/ic00188a002)
12. Gao, J., Amara, P., Alhambra, C. & Field, M. J. 1998 A generalized hybrid orbital (GHO) approach for the treatment of link-atoms using combined QM/MM potentials. J. Phys. Chem. 102, 4714-4721.
13. 12 stereospecifically deuterated in position 5′. Eur. J. Biochem. 119, 279-285. (doi:10.1111/j.1432-1033.1981.tb05605.x)
14. 12-dependent rearrangements. Science 227, 869-875.
15. Keep, N. H., Smith, G. A., Evans, M. C. W., Diakun, G. P. & Leadlay, P. F. 1993 The synthetic substrate succinyl (carbadethia)-CoA generates cob(II)alamin on adenosylcobalamin-dependent methylmalonyl-CoA mutase. Biochem. J. 295, 387-392.
16. Kim, Y. & Kreevoy, M. M. 1992 The experimental manifestations of corner cutting tunneling. J. Am. Chem. Soc. 114, 7116-7123. (doi:10.1021/ ja00044a024)
17. 12-dependent methylmalonyl-CoA mutase. J. Am. Chem. Soc. 128, 1287-1292. (doi:10.1021/ja056333j)
18. Loferer, M. J., Webb, B. M., Grant, G. H. & Liedl, K. R. 2003 Energetic and stereochemical effects of the protein environment on substrate: a theoretical study of methylmalonyl-CoA mutase. J. Am. Chem. Soc. 125, 1072-1078. (doi:10.1021/ja028906n)
19. Lynch, B. J. & Truhlar, D. G. 2003 Small representative benchmarks for thermochemical calculations. J. Phys. Chem. A 107, 8996-8999. (doi:10.1021/jp035287b)
20. Mancia, F. & Evans, P. 1998 Conformational changes on substrate binding to methylmalonyl CoA mutase and new insights into the free radical mechanism. Structure 6, 711-720. (doi:10.1016/S0969-2126(98)00073-2)
21. 12 radicals are generated: the crystal structure of methylmalonyl-coenzyme A mutase at 2 Å resolution. Structure 4, 339-350. (doi:10.1016/S0969-2126(96)00037-8)
22. Mancia, F., Smith, G. A. & Evans, P. R. 1999 Crystal structure of substrate complexes of methylmalonyl-CoA mutase. Biochemistry 38, 7999-8005. (doi:10.1021/bi9903852)
23. Mansoorabadi, S. O., Padmakumar, R., Fazliddinova, N., Vlasie, M., Banerjee, R. & Reed, G. H. 2005 Characterization of a succinyl-CoA radical-cob(II)alamin spin triplet intermediate in the reaction catalyzed by adenosylcobalamin-dependent methylmalonyl-CoA mutase. Biochemistry 44, 3153-3158. (doi:10.1021/bi0482102)
24. Marsh, E. N. G. & Ballou, D. P. 1998 Coupling of cobalt-carbon bond homolysis and hydrogen atom abstraction in adenosylcobalamin-dependent glutamate mutase. Biochemistry 37, 11 864-11 872. (doi:10.1021/bi980512e)
25. Meier, T. W., Thomä, N. H. & Leadlay, P. F. 1996 Tritium isotope effects in adenosylcobalamin-dependent methylmalonyl-CoA mutase. Biochemistry 35, 11 791-11 796. (doi:10.1021/bi961250o)
26. Michenfelder, M., Hull, W. E. & Retey, J. 1987 Quantitative measurement of the error in the cryptic stereospecificity of methylmalonyl-CoA mutase. Eur. J. Biochem. 168, 659-667. (doi:10.1111/j.1432-1033.1987.tb13467.x)
27. Padmakumar, R. & Banerjee, R. 1995 Evidence from EPR spectroscopy of the participation of radical intermediates in the reaction catalyzed by methylmalonyl-CoA mutase. J. Biol. Chem. 270, 9295-9300. (doi:10.1074/jbc.270. 16.9295)
28. Padmakumar, R., Padmakumar, R. & Banerjee, R. 1997 Evidence that cobalt-carbon bond homolysis is coupled to hydrogen atom abstraction from substrate in methylmalonyl-CoA mutase. Biochemistry 36, 3713-3718. (doi:10.1021/bi962503g)
29. Paneth, P. 1985 On the application of the steady-state to kinetic isotope effects. J. Am. Chem. Soc. 107, 7070-7071. (doi:10.1021/ja00310a051)
30. Thomä, N. H., Meier, T. W., Evans, P. R. & Leadlay, P. F. 1998 Stabilization of radical intermediates by an active site tyrosine residue in methylmalonyl-CoA mutase. Biochemistry 37, 14 386-14 393. (doi:10.1021/ bi981375o)
31. Truhlar, D. G., Gao, J., Alhambra, C., Garcia-Viloca, M., Corchado, J., Sanchez, M. L. & Villa, J. 2002 The incorporation of quantum effects in enzyme kinetics modeling. Acc. Chem. Res. 35, 341-349. (doi:10.1021/ar0100226)
32. Valleau, J. P. & Torrie, G. M. 1977 Statistical mechanics. New York, NY: Plenum.
33. Zhao, Y., Abend, A., Kunz, M., Such, P. & Retey, J. 1994 Electron paramagnetic resonance studies of the methylmalonyl-CoA mutase reaction: evidence for radical intermediates using the natural and artificial substrates as well as the competitive inhibitor 3-carboxypropyl-CoA. Eur. J. Biochem. 225, 891-896. (doi:10.1111/j.1432-1033.1994.0891b.x)