Mutagenesis of a conserved glutamate reveals the contribution of electrostatic energy to adenosylcobalamin Co-C bond homolysis in ornithine 4,5-aminomutase and methylmalonyl-CoA mutase

Biochemistry

Volumn 52, Issue 5, 2013, Pages 878-888

  Makins, Caitlyn ^a   Pickering, Alex V ^a   Mariani, Chloe ^a   Wolthers, Kirsten R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ABSORBANCE SPECTROSCOPY; ADENOSYLCOBALAMIN; ASPARTATES; CATALYTIC TURNOVER; CO-C BOND; COFACTORS; ELECTROSTATIC ENERGIES; GLUTAMATE SIDE CHAIN; HOMOLYSIS; METHYLMALONYL-COA MUTASE; NATIVE ENZYMES; PHYSIOLOGICAL SUBSTRATE; RADICAL SPECIES; STOPPED FLOW; UV VISIBLE SPECTROSCOPY;

AMINO ACIDS; CATALYSIS; ENZYMES; ULTRAVIOLET VISIBLE SPECTROSCOPY;

REDUCTION;

ALANINE; ASPARTIC ACID; COBAMAMIDE; GLUTAMIC ACID; GLUTAMINE; HOLOENZYME; ISOMERASE; METHYLMALONYL COENZYME A MUTASE; ORNITHINE 4,5 AMINOMUTASE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CLOSTRIDIUM STICKLANDII; COVALENT BOND; DISSOCIATION CONSTANT; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; MUTAGENESIS; PRIORITY JOURNAL; STATIC ELECTRICITY; STEADY STATE; ULTRAVIOLET SPECTROSCOPY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CLOSTRIDIUM STICKLANDII; COBAMIDES; GLUTAMIC ACID; HUMANS; INTRAMOLECULAR TRANSFERASES; KINETICS; METHYLMALONYL-COA MUTASE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POINT MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; STATIC ELECTRICITY;

EID: 84873345184     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3012719     Document Type: Article

References (44)

1. Brown, K. L. (2005) Chemistry and enzymology of vitamin B-12 Chem. Rev. 105, 2075-2149
2. Banerjee, R. (2001) Radical peregrinations catalyzed by coenzyme B12-dependent enzymes Biochemistry 40, 6191-6198 (Pubitemid 32472706)
3. Larsson, K. M., Logan, D. T., and Nordlund, P. (2010) Structural Basis for Adenosylcobalamin Activation in AdoCbl-Dependent Ribonucleotide Reductases ACS Chem. Biol. 5, 933-942
4. Banerjee, R. (2003) Radical carbon skeleton rearrangements: Catalysis by coenzyme B12-dependent mutases Chem. Rev. 103, 2083-2094
5. 12 dependent glutamate mutase Curr. Opin. Chem. Biol. 6, 598-603 (Pubitemid 35284190)
6. Toraya, T. (2003) Radical catalysis in coenzyme B12-dependent isomerization (eliminating) reactions Chem. Rev. 103, 2095-2127
7. Bandarian, V. and 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, 12069-12075
8. Chen, H. P., Wu, S. H., Lin, Y. L., Chen, C. M., and Tsay, S. S. (2001) Cloning, sequencing, heterologous expression, purification, and characterization of adenosylcobalamin-dependent d -ornithine aminomutase from Clostridium sticklandii J. Biol. Chem. 276, 44744-44750
9. Chang, C. H. and Frey, P. A. (2000) Cloning, sequencing, heterologous expression, purification, and characterization of adenosylcobalamin-dependent d -lysine 5,6-aminomutase from Clostridium sticklandii J. Biol. Chem. 275, 106-114 (Pubitemid 30038959)
10. Berkovitch, F., Behshad, E., Tang, K. H., Enns, E. A., Frey, P. A., and Drennan, C. L. (2004) A locking mechanism preventing radical damage in the absence of substrate, as revealed by the X-ray structure of lysine 5,6-aminomutase Proc. Natl. Acad. Sci. U.S.A. 101, 15870-15875 (Pubitemid 39507894)
11. Mancia, F. and Evans, P. R. (1998) Conformational changes on substrate binding to methylmalonyl CoA mutase and new insights into the free radical mechanism Structure 6, 711-720 (Pubitemid 28301205)
12. Wolthers, K. R., Rigby, S. E., and Scrutton, N. S. (2008) Mechanism of radical-based catalysis in the reaction catalyzed by adenosylcobalamin-dependent ornithine 4,5-aminomutase J. Biol. Chem. 283, 34615-34625
13. Maity, A. N., Hsieh, C. P., Huang, M. H., Chen, Y. H., Tang, K. H., Behshad, E., Frey, P. A., and Ke, S. C. (2009) Evidence for conformational movement and radical mechanism in the reaction of 4-thia- l -lysine with lysine 5,6-aminomutase J. Phys. Chem. B 113, 12161-12163
14. Shibata, N., Masuda, J., Morimoto, Y., Yasuoka, N., and Toraya, T. (2002) Substrate-induced conformational change of a coenzyme B12-dependent enzyme: Crystal structure of the substrate-free form of diol dehydratase Biochemistry 41, 12607-12617 (Pubitemid 35192490)
15. Pang, J., Li, X., Morokuma, K., Scrutton, N. S., and Sutcliffe, M. J. (2012) Large-scale domain conformational change is coupled to the activation of the Co-C bond in the B12-dependent enzyme ornithine 4,5-aminomutase: A computational study J. Am. Chem. Soc. 134, 2367-2377
16. Wolthers, K. R., Levy, C., Scrutton, N. S., and Leys, D. (2010) Large-scale domain dynamics and adenosylcobalamin reorientation orchestrate radical catalysis in ornithine 4,5-aminomutase J. Biol. Chem. 285, 13942-13950
17. Mancia, F., Keep, N. H., Nakagawa, A., Leadlay, P. F., McSweeney, S., Rasmussen, B., Bosecke, P., Diat, O., and Evans, P. R. (1996) How coenzyme B12 radicals are generated: The crystal structure of methylmalonyl-coenzyme A mutase at 2 Å resolution Structure 4, 339-350
18. Reitzer, R., Gruber, K., Jogl, G., Wagner, U. G., Bothe, H., Buckel, W., and Kratky, C. (1999) Glutamate mutase from Clostridium cochlearium: The structure of a coenzyme B12-dependent enzyme provides new mechanistic insights Structure 7, 891-902 (Pubitemid 29372511)
19. 12 Dependent Enzyme Glutamate Mutase Angew. Chem., Int. Ed. 40, 3377-3380 (Pubitemid 32916604)
20. Ludwig, M. L. and Matthews, R. G. (1997) Structure-based perspectives on B12-dependent enzymes Annu. Rev. Biochem. 66, 269-313
21. Froese, D. S., Kochan, G., Muniz, J. R., Wu, X., Gileadi, C., Ugochukwu, E., Krysztofinska, E., Gravel, R. A., Oppermann, U., and Yue, W. W. (2010) Structures of the human GTPase MMAA and vitamin B12-dependent methylmalonyl-CoA mutase and insight into their complex formation J. Biol. Chem. 285, 38204-38213
22. Sharma, P. K., Chu, Z. T., Olsson, M. H., and Warshel, A. (2007) A new paradigm for electrostatic catalysis of radical reactions in vitamin B12 enzymes Proc. Natl. Acad. Sci. U.S.A. 104, 9661-9666 (Pubitemid 47175323)
23. Bucher, D., Sandala, G. M., Durbeej, B., Radom, L., and Smith, D. M. (2012) The elusive 5′-deoxyadenosyl radical in coenzyme-B12-mediated reactions J. Am. Chem. Soc. 134, 1591-1599
24. Makins, C., Miros, F. N., Scrutton, N. S., and Wolthers, K. R. (2012) Role of histidine 225 in adenosylcobalamin-dependent ornithine 4,5-aminomutase Bioorg. Chem. 40, 39-47
25. Taoka, S., Padmakumar, R., Lai, M. T., Liu, H. W., and Banerjee, R. (1994) Inhibition of the human methylmalonyl-CoA mutase by various CoA-esters J. Biol. Chem. 269, 31630-31634 (Pubitemid 24379526)
26. McKie, N., Keep, N. H., Patchett, M. L., and Leadlay, P. F. (1990) Adenosylcobalamin-dependent methylmalonyl-CoA mutase from Propionibacterium shermanii. Active holoenzyme produced from Escherichia coli Biochem. J. 269, 293-298 (Pubitemid 20236014)
27. Padmakumar, R., Padmakumar, R., and 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 (Pubitemid 27143527)
28. Chowdhury, S. and Banerjee, R. (1999) Role of the dimethylbenzimidazole tail in the reaction catalyzed by coenzyme B12-dependent methylmalonyl-CoA mutase Biochemistry 38, 15287-15294 (Pubitemid 129520362)
29. Jensen, K. P. and Ryde, U. (2005) How the Co-C bond is cleaved in coenzyme B12 enzymes: A theoretical study J. Am. Chem. Soc. 127, 9117-9128 (Pubitemid 40903108)
30. Durbeej, B., Sandala, G. M., Bucher, D., Smith, D. M., and Radom, L. (2009) On the importance of ribose orientation in the substrate activation of the coenzyme B12-dependent mutases Eur. J. Chem. 15, 8578-8585
31. Marsh, E. N. and Melendez, G. D. (2012) Adenosylcobalamin enzymes: Theory and experiment begin to converge Biochim. Biophys. Acta 1824, 1154-1164
32. Marsh, E. N. and Ballou, D. P. (1998) Coupling of cobalt-carbon bond homolysis and hydrogen atom abstraction in adenosylcobalamin-dependent glutamate mutase Biochemistry 37, 11864-11872 (Pubitemid 28400058)
33. Kozlowski, P. M., Kamachi, T., Toraya, T., and Yoshizawa, K. (2007) Does Cob(II)alamin act as a conductor in coenzyme B12 dependent mutases? Angew. Chem., Int. Ed. 46, 980-983 (Pubitemid 46195092)
34. 12 J. Inorg. Biochem. 40, 19-22 (Pubitemid 20329672)
35. Halpern, J. (1985) Mechanisms of coenzyme B12-dependent rearrangements Science 227, 869-875
36. Dong, S. L., Padmakumar, R., Banerjee, R., and Spiro, T. G. (1999) Co-C bond activation in B-12-dependent enzymes: Cryogenic resonance Raman studies of methylmalonyl-coenzyme A mutase J. Am. Chem. Soc. 121, 7063-7070
37. Huhta, M. S., Chen, H. P., Hemann, C., Hille, C. R., and Marsh, E. N. (2001) Protein-coenzyme interactions in adenosylcobalamin-dependent glutamate mutase Biochem. J. 355, 131-137 (Pubitemid 32304243)
38. Calafat, A. M., Taoka, S., Puckett, J. M., Jr., Semerad, C., Yan, H., Luo, L., Chen, H., Banerjee, R., and Marzilli, L. G. (1995) Structural and electronic similarity but functional difference in methylmalonyl-CoA mutase between coenzyme B12 and the analog 2′,5′-dideoxyadenosylcobalamin Biochemistry 34, 14125-14130
39. Toraya, T. and Fukui, S. (1977) Immunochemical evidence for the difference between coenzyme-B12-dependent diol dehydratase and glycerol dehydratase Eur. J. Biochem. 76, 285-289 (Pubitemid 8117421)
40. 12-dependent ethanolamine ammonia-lyase catalyzed reaction of S-2-aminopropanol Biochemistry 41, 8580-8588 (Pubitemid 34743297)
41. Abend, A., Bandarian, V., Reed, G. H., and Frey, P. A. (2000) Identification of cis-ethanesemidione as the organic radical derived from glycolaldehyde in the suicide inactivation of dioldehydrase and of ethanolamine ammonia-lyase Biochemistry 39, 6250-6257 (Pubitemid 30327103)
42. Mansoorabadi, S. O., Magnusson, O. T., Poyner, R. R., Frey, P. A., and Reed, G. H. (2006) Analysis of the cob(II)alamin-5′-deoxy-3′, 4′-anhydroadenosyl radical triplet spin system in the active site of diol dehydrase Biochemistry 45, 14362-14370 (Pubitemid 44865192)
43. Bothe, H., Darley, D. J., Albracht, S. P., Gerfen, G. J., Golding, B. T., and Buckel, W. (1998) Identification of the 4-glutamyl radical as an intermediate in the carbon skeleton rearrangement catalyzed by coenzyme B12-dependent glutamate mutase from Clostridium cochlearium Biochemistry 37, 4105-4113 (Pubitemid 28166432)
44. 12 coenzyme-dependent ethanolamine deaminase J. Am. Chem. Soc. 123, 8564-8572 (Pubitemid 32808080)