Bipartite recognition and conformational sampling mechanisms for hydride transfer from nicotinamide coenzyme to FMN in pentaerythritol tetranitrate reductase

FEBS Journal

Volumn 276, Issue 17, 2009, Pages 4780-4789

  Pudney, Christopher R ^a   Hay, Sam ^a   Scrutton, Nigel S ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Bipartite recognition; Coenzyme binding; Flavoprotein; Pentaerythritol tetranitrate reductase; Reduction in dimensionality

Indexed keywords

NICOTINAMIDE COENZYME; NUCLEOTIDE DERIVATIVE; OXIDOREDUCTASE; PENTAERYTHRITOL TETRANITRATE REDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; COENZYME; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME CONFORMATION; ENZYME KINETICS; MOLECULAR RECOGNITION; PRIORITY JOURNAL; REDUCTION; STEADY STATE;

COENZYMES; FLAVIN MONONUCLEOTIDE; KINETICS; NAD; NADP; NIACINAMIDE; OXIDOREDUCTASES; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY;

EID: 68849107333     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07179.x     Document Type: Article

References (26)

1. Neeli R, Sabri M, McLean KJ, Dunford AJ, Scrutton NS, Leys D Munro AW (2008) Trp(359) regulates flavin thermodynamics and coenzyme selectivity in Mycobacterium tuberculosis FprA. Biochem J 411, 563 570.
2. Sabri M, Dunford AJ, McLean KJ, Neeli R, Scrutton NS, Leys D Munro AW (2009) Characterization of coenzyme binding and selectivity determinants in Mycobacterium tuberculosis flavoprotein reductase A: analysis of Arg(199) and Arg(200) mutants at the NADP(H) 2'-phosphate binding site. Biochem J 417, 103 112.
3. van den Heuvel RHH, Westphal AH, Heck AJR, Walsh MA, Rovida S, van Berkel WJH Mattevi A (2004) Structural studies on flavin reductase PheA2 reveal binding of NAD in an unusual folded conformation and support novel mechanism of action. J Biol Chem 279, 12860 12867.
4. Wang J, Ortiz-Maldonado M, Entsch B, Massey V, Ballou D Gatti DL (2002) Protein and ligand dynamics in 4-hydroxybenzoate hydroxylase. Proc Natl Acad Sci USA 99, 608 613.
5. Mirza I, Yachin BJ, Wang S, Grosse S, Bergeron H, Imura A, Iwaki H, Hasegawa Y, Lau PC Berghuis AM (2009) Crystal structures of cyclohexanone monooxygenase reveal complex domain movements and a sliding cofactor. J Am Chem Soc 31, 8848 8854.
6. Deng Z, Aliverti A, Zanetti G, Arakaki AK, Ottado J, Orellano EG, Calcaterra NB, Ceccarelli EA, Carrilli N Karplus PA (1999) A productive NADP(+) binding mode of ferredoxin-NADP(+) reductase revealed by protein engineering and crystallographic studies. Nat Struct Biol 6, 847 853.
7. Basran J, Harris RJ, Sutcliffe MJ Scrutton NS (2003) H-tunneling in the multiple H-transfers of the catalytic cycle of morphinone reductase and in the reductive half-reaction of the homologous pentaerythritol tetranitrate reductase. J Biol Chem 278, 43973 43982.
8. Massey V Schopfer LM (1986) Reactivity of old yellow enzyme with alpha-NADPH and other pyridine-nucleotide derivatives. J Biol Chem 261, 1215 1222.
9. French CE, Nicklin S Bruce NC (1996) Sequence and properties of pentaerythritol tetranitrate reductase from Enterobacter cloacae PB2. J Bacteriol 178, 6623 6627. (Pubitemid 26374732)
10. French CE, Nicklin S Bruce NC (1998) Aerobic degradation of 2,4,6-trinitrotoluene by Enterobacter cloacae PB2 and by pentaerythritol tetranitrate reductase. Appl Environ Microb 64, 2864 2868.
11. Khan H, Harris RJ, Barna T, Craig DH, Bruce NC, Munro AW, Moody PCE Scrutton NS (2002) Kinetic and structural basis of reactivity of pentaerythritol tetranitrate reductase with NADPH, 2-cyclohexenone, nitroesters, and nitroaromatic explosives. J Biol Chem 277, 21906 21912.
12. Khan H, Barna T, Bruce NC, Munro AW, Leys D Scrutton NS (2005) Proton transfer in the oxidative half-reaction of pentaerythritol tetranitrate reductase. FEBS J 272, 4660 4671.
13. Basran A, French CE, Williams RE, Nicklin S Bruce NC (1998) Degradation of nitrate ester and nitroaromatic explosives by Enterobacter cloacae PB2. Biochem Soc T 26, 680 685.
14. French CE, Rosser SJ, Davies GJ, Nicklin S Bruce NC (1999) Biodegradation of explosives by transgenic plants expressing pentaerythritol tetranitrate reductase. Nat Biotechnol 17, 491 494.
15. Buckman J Miller SM (2000) Transient kinetics and intermediates formed during the electron transfer reaction catalyzed by Candida albicans estrogen binding protein. Biochemistry 39, 10521 10531.
16. Deng H, Zhadin N Callender R (2001) Dynamics of protein ligand binding on multiple time scales: NADH binding to lactate dehydrogenase. Biochemistry 40, 3767 3773.
17. Barna TM, Khan H, Bruce NC, Barsukov I, Scrutton NS Moody PCE (2001) Crystal structure of pentaerythritol tetranitrate reductase: 'flipped' binding geometries for steroid substrates in different redox states of the enzyme. J Mol Biol 310, 433 447.
18. Fox KM Karplus PA (1994) Old yellow enzyme at 2-angstrom resolution - overall structure, ligand-binding, and comparison with related flavoproteins. Structure 2, 1089 1105.
19. Barna T, Messiha HL, Petosa C, Bruce NC, Scrutton NS Moody PCE (2002) Crystal structure of bacterial morphinone reductase and properties of the C191A mutant enzyme. J Biol Chem 277, 30976 30983.
20. Pudney CR, Hay S, Pang JY, Costello C, Leys D, Sutcliffe MJ Scrutton NS (2007) Mutagenesis of morphinone reductase induces multiple reactive configurations and identifies potential ambiguity in kinetic analysis of enzyme tunneling mechanisms. J Am Chem Soc 129, 13949 13956.
21. Pudney CR, Hay S, Sutcliffe MJ Scrutton NS (2006) alpha-Secondary isotope effects as probes of 'tunneling-ready' configurations in enzymatic H-tunneling: insight from environmentally coupled tunneling models. J Am Chem Soc 128, 14053 14058.
22. Fersht A (2003) Structure and Mechanism in Protein Science, 5th edn. WH Freeman, New York, NY.
23. Pudney C, McGrory T, Pang J, Lafite P, Hay S, Sutcliffe MJ Scrutton NS (2009) Parallel pathways and free energy landscapes for enzymatic hydride transfer probed by hydrostatic pressure. ChemBioChem 10, 1379 1384.
24. Leys D, Basran J, Talfournier F, Sutcliffe MJ Scrutton NS (2003) Extensive conformational sampling in a ternary electron transfer complex. Nat Struct Biol 10, 219 225.
25. Toogood HS, van Thiel A, Basran J, Sutcliffe MJ, Scrutton NS Leys D (2004) Extensive domain motion and electron transfer in the human electron transferring flavoprotein center dot medium chain acyl-CoA dehydrogenase complex. J Biol Chem 279, 32904 32912.
26. Toogood HS, Leys D Scrutton NS (2007) Dynamics driving function - new insights from electron transferring flavoproteins and partner complexes. FEBS J 274, 5481 5504.