Direct evidence for a covalent ene adduct intermediate in NAD(P)H-dependent enzymes

Nature Chemical Biology

Volumn 10, Issue 1, 2014, Pages 50-55

  Rosenthal, Raoul G ^a   Ebert, Marc Olivier ^a   Kiefer, Patrick ^a   Peter, Dominik M ^a   Vorholt, Julia A ^a   Erb, Tobias J ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ADDUCTION; ARTICLE; CATALYSIS; COVALENT BOND; ENZYME KINETICS; FATTY ACID SYNTHESIS; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL;

CATALYSIS; ENZYMES; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; NADP;

EID: 84890976588     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1385     Document Type: Article

References (42)

1. Westheimer, F.H., Fisher, H.F., Conn, E.E. & Vennesland, B. The enzymatic transfer of hydrogen from alcohol to Dpn. J. Am. Chem. Soc. 73, 2403-2408(1951).
2. Cheng, J.P., Lu, Y., Zhu, X.Q. & Mu, L.J. Energetics of multistep versus one-step hydride transfer reactions of reduced nicotinamide adenine dinucleotide (NADH) models with organic cations and p-quinones. J. Org. Chem. 63, 6108-6114(1998). (Pubitemid 128498340)
3. Westheimer, F.H. Mechanism of action of the pyridine nucleotides. in Pyridine Nucleotide Coenzymes: Chemical, Biochemical, and Medical aspects Vol. 2 (eds. Dolphin, D., Poulson, R. & Avramovic, O.) 253-322 (Wiley, New York, 1986).
4. Abeles, R.H., Hutton, R.F. & Westheimer, F.H. The reduction of thioketones by a model for a coenzyme. J. Am. Chem. Soc. 79, 712-716(1957).
5. Wu, Y.D. & Houk, K.N. Theoretical transition structures for hydride transfer to methyleniminium ion from methylamine and dihydropyridine. On the nonlinearity of hydride transfers. J. Am. Chem. Soc. 109, 2226-2227(1987).
6. Bugg, T. Introduction to Enzyme and Coenzyme Chemistry (Wiley-Blackwell, Oxford, 2012).
7. Hamilton, G.A. in Progress in Bioorganic Chemistry Vol. 1 (eds. Kaiser, E.T. & Kezdy, F.J.) 83-157(1971).
8. MacInnes, I., Nonhebel, D.C., Orszulik, S.T. & Suckling, C.J. On the mechanism of hydrogen transfer by nicotinamide coenzymes and alcohol-dehydrogenase. J. Chem. Soc., Perkin Trans. 1 1983, 2777-2779(1983).
9. Hedlund, J., Jornvall, H. & Persson, B. Subdivision of the MDR superfamily of medium-chain dehydrogenases/reductases through iterative hidden Markov model refinement. BMC Bioinformatics 11, 534(2010).
10. Agarwal, P.K., Webb, S.P. & Hammes-Schiffer, S. Computational studies of the mechanism for proton and hydride transfer in liver alcohol dehydrogenase. J. Am. Chem. Soc. 122, 4803-4812(2000). (Pubitemid 30331699)
11. Bahnson, B.J., Park, D.H., Kim, K., Plapp, B.V. & Klinman, J.P. Unmasking of hydrogen tunneling in the horse liver alcohol dehydrogenase reaction by site-directed mutagenesis. Biochemistry 32, 5503-5507(1993). (Pubitemid 23178513)
12. Roston, D. & Kohen, A. Elusive transition state of alcohol dehydrogenase unveiled. Proc. Natl. Acad. Sci. USA 107, 9572-9577(2010).
13. Youn, B. et al. Mechanistic and structural studies of apoform, binary, and ternary complexes of the Arabidopsis alkenal double bond reductase At5g16970. J. Biol. Chem. 281, 40076-40088(2006). (Pubitemid 46041813)
14. Porté, S. et al. Kinetic and structural evidence of the alkenal/one reductase specificity of human ζ-crystallin. Cell Mol. Life Sci. 68, 1065-1077(2011).
15. Schlegel, B.P., Ratnam, K. & Penning, T.M. Retention of NADPH-linked quinone reductase activity in an aldo-keto reductase following mutation of the catalytic tyrosine. Biochemistry 37, 11003-11011(1998). (Pubitemid 28368925)
16. Airenne, T.T. et al. Structure-function analysis of enoyl thioester reductase involved in mitochondrial maintenance. J. Mol. Biol. 327, 47-59(2003). (Pubitemid 36297038)
17. Chen, Z.J. et al. Structural enzymological studies of 2-enoyl thioester reductase of the human mitochondrial FAS II pathway: new insights into its substrate recognition properties. J. Mol. Biol. 379, 830-844(2008).
18. Wallace, K.K. et al. Purification of crotonyl-CoA reductase from Streptomyces collinus and cloning, sequencing and expression of the corresponding gene in Escherichia coli. Eur. J. Biochem. 233, 954-962(1995).
19. Erb, T.J. et al. Synthesis of C5-dicarboxylic acids from C2-units involving crotonyl-CoA carboxylase/reductase: the ethylmalonyl-CoA pathway. Proc. Natl. Acad. Sci. USA 104, 10631-10636(2007). (Pubitemid 47185716)
20. Erb, T.J., Brecht, V., Fuchs, G., Muller, M. & Alber, B.E. Carboxylation mechanism and stereochemistry of crotonyl-CoA carboxylase/ reductase, a carboxylating enoyl-thioester reductase. Proc. Natl. Acad. Sci. USA 106, 8871-8876(2009).
21. Wilson, M.C. & Moore, B.S. Beyond ethylmalonyl-CoA: the functional role of crotonyl-CoA carboxylase/reductase homologs in expanding polyketide diversity. Nat. Prod. Rep. 29, 72-86(2012).
22. Erb, T.J. et al. Synthesis of C5-dicarboxylic acids from C2-units involving crotonyl-CoA carboxylase/reductase: The ethylmalonyl-CoA pathway. Proc. Natl. Acad. Sci. USA 104, 10631-10636(2007). (Pubitemid 47185716)
23. Quade, N., Huo, L., Rachid, S., Heinz, D.W. & Muller, R. Unusual carbon fixation gives rise to diverse polyketide extender units. Nat. Chem. Biol. 8, 117-124(2012).
24. Yoo, H.G. et al. Characterization of 2-octenoyl-CoA carboxylase/reductase utilizing pteB from Streptomyce avermitilis. Biosci. Biotechnol. Biochem. 75, 1191-1193(2011).
25. Torkko, J.M. et al. Candida tropicalis Etr1p and Saccharomyces cerevisiae Ybr026p (Mrf1′p), 2-enoyl thioester reductases essential for mitochondrial respiratory competence. Mol. Cell Biol. 21, 6243-6253(2001). (Pubitemid 34263524)
26. Todd, J.D., Curson, A.R., Sullivan, M.J., Kirkwood, M. & Johnston, A.W. The Ruegeria pomeroyi acuI gene has a role in DMSP catabolism and resembles yhdH of E. coli and other bacteria in conferring resistance to acrylate. PLoS ONE 7, e35947(2012).
27. Schneider, K., Asao, M., Carter, M.S. & Alber, B.E. Rhodobacter sphaeroides uses a reductive route via propionyl coenzyme A to assimilate 3-hydroxypropionate. J. Bacteriol. 194, 225-232(2012).
28. Asao, M. & Alber, B.E. Acrylyl-CoA reductase, an enzyme involved in the assimilation of 3-hydroxypropionate by Rhodobacter sphaeroides. J. Bacteriol. 195, 4716-4725(2013).
29. Alder, K., Pascher, F. & Schmitz, A. Absorption of maleic acid-anhydride and azodicarbon acid-ester in simple unsaturated carbohydrogens. Information on the substitution processes in the allyl position. Chem. Ber. 76, 27-53(1943).
30. Pindur, U. & Schneider, G.H. Pericyclic key reactions in biological-systems and biomimetic syntheses. Chem. Soc. Rev. 23, 409-415(1994). (Pubitemid 24986160)
31. Lamb, A.L. Pericyclic reactions catalyzed by chorismate-utilizing enzymes. Biochemistry 50, 7476-7483(2011).
32. Chook, Y.M., Gray, J.V., Ke, H. & Lipscomb, W.N. The monofunctional chorismate mutase from Bacillus subtilis. Structure determination of chorismate mutase and its complexes with a transition state analog and prephenate, and implications for the mechanism of the enzymatic reaction. J. Mol. Biol. 240, 476-500(1994).
33. DeClue, M.S., Baldridge, K.K., Kunzler, D.E., Kast, P. & Hilvert, D. Isochorismate pyruvate lyase: a pericyclic reaction mechanism? J. Am. Chem. Soc. 127, 15002-15003(2005). (Pubitemid 41547348)
34. Libby, R.D. & Mehl, R.A. Characterization of covalent Ene adduct intermediates in "hydride equivalent" transfers in a dihydropyridine model for NADH reduction reactions. Bioorg. Chem. 40, 57-66(2012).
35. Jacobson, B.M. Aromatization of 1,4-cyclohexadiene with tetracyanoethylene-Ene reaction. J. Am. Chem. Soc. 102, 886-887(1980).
36. Sulzbach, R.A. & Iqbal, F.M. Addition of acrylonitrile to derivatives of 1,4-dihydropyridine. Angew. Chem. Int. Ed. Engl. 10, 733(1971).
37. Inagaki, S. & Hirabayashi, Y. Mechanism of NAD(P)H reduction reactions. Bull. Chem. Soc. Jpn. 50, 3360-3364(1977).
38. Rozwarski, D.A., Grant, G.A., Barton, D.H., Jacobs, W.R. Jr. & Sacchettini, J.C. Modification of the NADH of the isoniazid target (InhA) from Mycobacterium tuberculosis. Science 279, 98-102(1998). (Pubitemid 28079164)
39. Bull, H.G. et al. Mechanism-based inhibition of human steroid 5 α-reductase by finasteride: enzyme-catalyzed formation of NADP-dihydrofinasteride, a potent bisubstrate analog inhibitor. J. Am. Chem. Soc. 118, 2359-2365(1996).
40. Wolfenden, R. Transition state analogues for enzyme catalysis. Nature 223, 704-705(1969).
41. Kapmeyer, H., Pfleiderer, G. & Trommer, W.E. A transition state analogue for two pyruvate metabolizing enzymes, lactate dehydrogenase and alanine dehydrogenase. Biochemistry 15, 5024-5028(1976).
42. Harden, A. & Young, W.J. The alcoholic ferment of yeast-juice. Proc. R. Soc. Lond., B 77, 405-420(1906).