How is the distal pocket of a heme protein optimized for binding of tryptophan?

FEBS Journal

Volumn 279, Issue 24, 2012, Pages 4501-4509

  Chauhan, Nishma ^a   Basran, Jaswir ^a   Rafice, Sara A ^a   Efimov, Igor ^a   Millett, Elizabeth S ^a   Mowat, Christopher G ^b   Moody, Peter C E ^b   Handa, Sandeep ^a   Raven, Emma L ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

dioxygenase; heme; iron; N formylkynurenine; tryptophan

Indexed keywords

ARGININE; HEMOPROTEIN; HISTIDINE; INDOLEAMINE 2,3 DIOXYGENASE; TRYPTOPHAN; TRYPTOPHAN 2,3 DIOXYGENASE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SUBSTRATE COMPLEX; HUMAN; HYDROPHOBICITY; LIGAND BINDING; MUTATIONAL ANALYSIS; NONHUMAN; OXIDATION REDUCTION STATE; POTENTIOMETRY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MODIFICATION; PROTEIN STRUCTURE; STEADY STATE;

CATALYTIC DOMAIN; HEMEPROTEINS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; OXIDATION-REDUCTION; PROTEIN BINDING; SUBSTRATE SPECIFICITY; TRYPTOPHAN; TRYPTOPHAN OXYGENASE;

EID: 84870555504     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12036     Document Type: Article

References (34)

1. Kotake Y, &, Masayama I, (1936) The intermediary metabolism of tryptophan. XVIII. The mechanism of formation of kynurenine from tryptophan. Z Physiol Chem 243, 237-244.
2. Tanaka T, &, Knox WE, (1959) The nature and mechanism of the tryptophan pyrrolase (peroxidase-oxidase) reaction of Pseudomonas and of rat liver. J Biol Chem 234, 1162-1170.
3. Yamamoto S, &, Hayaishi O, (1967) Tryptophan pyrrolase of rabbit intestine. d-and l -tryptophan-cleaving enzyme or enzymes. J Biol Chem 242, 5260-5266.
4. Knox WE, &, Mehler AH, (1950) The conversion of tryptophan to kynurenine in liver. I. The coupled tryptophan peroxidase-oxidase system forming formylkynurenine. J Biol Chem 187, 419-430.
5. Sono M, Roach MP, Coulter ED, &, Dawson JH, (1996) Heme-containing oxygenases. Chem Rev 96, 2841-2887.
6. Efimov I, Basran J, Thackray SJ, Handa S, Mowat CG, &, Raven EL, (2011) Structure and reaction mechanism in the heme dioxygenases. Biochemistry 50, 2717-2724.
7. Millett ES, Efimov I, Basran J, Handa S, Mowat CG, &, Raven EL, (2012) Heme-containing dioxygenases involved in tryptophan oxidation. Curr Opin Chem Biol 16, 60-66.
8. 2 incorporation by a heme-containing dioxygenase. Proc Natl Acad Sci USA 103, 2611-2616.
9. Papadopoulou ND, Mewies M, McLean KJ, Seward HE, Svistunenko DA, Munro AW, &, Raven EL, (2005) Redox and spectroscopic properties of human indoleamine 2,3-dioxygenase and a His303Ala variant: implications for catalysis. Biochemistry 44, 14318-14328.
10. Sono M, &, Dawson JH, (1984) Extensive studies of the heme coordination structure of indoleamine 2,3-dioxygenase and of tryptophan binding with magnetic and natural circular dichroism and electron paramagnetic resonance spectroscopy. Biochim Biophys Acta 789, 170-187.
11. Terentis AC, Thomas SR, Takikawa O, Littlejohn TK, Truscott RJW, Armstrong RS, Yeh S-R, &, Stocker R, (2002) The heme environment of recombinant human indoleamine 2,3-dioxygenase: structural properties and substrate-ligand interactions. J Biol Chem 277, 15788-15794.
12. Chauhan N, Basran J, Efimov I, Svistunenko DA, Seward HE, Moody PCE, &, Raven EL, (2008) The role of serine 167 in human indoleamine 2,3-dioxygenase: a comparison with tryptophan 2,3-dioxygenase. Biochemistry 47, 4761-4769.
13. Forouhar F, Anderson JL, Mowat CG, Vorobiev SM, Hussain A, Abashidze M, Bruckmann C, Thackray SJ, Seetharaman J, Tucker T, et al,. (2007) Molecular insights into substrate recognition and catalysis by tryptophan 2,3-dioxygenase. Proc Natl Acad Sci USA 104, 473-478.
14. Zhang Y, Kang SA, Mukherjee T, Bale S, Crane BR, Begley TP, &, Ealick SE, (2007) Crystal structure and mechanism of tryptophan 2,3-dioxygenase, a heme enzyme involved in tryptophan catabolism and in quinolinate biosynthesis. Biochemistry 46, 145-155.
15. Dunford HB, (2010) Peroxidases and Catalases: Biochemistry, Biophysics, Biotechnology and Physiology, 2nd edn. John Wiley, Chichester.
16. Springer BA, Sligar SG, Olson JS, &, Phillips GN Jr, (1994) Mechanisms of ligand recognition in myoglobin. Chem Rev 94, 699-714.
17. Biegert A, Mayer C, Remmert M, Söding J, &, Lupas A, (2006) The MPI Toolkit for protein sequence analysis. Nucleic Acids Res 34, W335-W339.
18. Basran J, Rafice SA, Chauhan N, Efimov I, Cheesman MR, Ghamsari L, &, Raven EL, (2008) A kinetic, spectroscopic, and redox study of human tryptophan 2,3-dioxygenase. Biochemistry 47, 4752-4760.
19. Efimov I, Basran J, Sun X, Chauhan N, Chapman SK, Mowat CG, &, Raven EL, (2012) The mechanism of substrate inhibition in human indoleamine 2,3-dioxygenase. J Am Chem Soc 134, 3034-3041.
20. Littlejohn TK, Takikawa O, Truscott RJW, &, Walker MJ, (2003) Asp274 and His346 are essential for heme binding and catalytic function of human indoleamine 2,3-dioxygenase. J Biol Chem 278, 29525-29531.
21. Batabyal D, &, Yeh S-R, (2009) Substrate-protein interaction in human tryptophan dioxygenase: the critical role of H76. J Am Chem Soc 131, 3260-3270.
22. Thackray SJ, Bruckmann C, Anderson JL, Campbell LP, Xiao R, Zhao L, Mowat CG, Forouhar F, Tong L, &, Chapman SK, (2008) Histidine 55 of tryptophan 2,3-dioxygenase is not an active site base but regulates catalysis by controlling substrate binding. Biochemistry 47, 10677-10684.
23. Capece L, Lewis-Ballester A, Marti MA, Estrin DA, &, Yeh SR, (2011) Molecular basis for the substrate stereoselectivity in tryptophan dioxygenase. Biochemistry 50, 10910-10918.
24. Cady SG, &, Sono M, (1991) 1-Methyl- dl -tryptophan, beta-(3-benzofuranyl)- dl -alanine (the oxygen analog of tryptophan), and beta-[3-benzo(b)thienyl]- dl -alanine (the sulfur analog of tryptophan) are competitive inhibitors for indoleamine 2,3-dioxygenase. Arch Biochem Biophys 291, 326-333.
25. Chauhan N, Thackray SJ, Rafice SA, Eaton G, Lee M, Efimov I, Basran J, Jenkins PR, Mowat CG, Chapman SK, et al,. (2009) Reassessment of the reaction mechanism in the heme dioxygenases. J Am Chem Soc 131, 4186-4187.
26. Capece L, Lewis-Ballester A, Batabyal D, Di Russo N, Yeh SR, Estrin DA, &, Marti MA, (2010) The first step of the dioxygenation reaction carried out by tryptophan dioxygenase and indoleamine 2,3-dioxygenase as revealed by quantum mechanical/molecular mechanical studies. J Biol Inorg Chem 15, 811-823.
27. Chung LW, Li X, Sugimoto H, Shiro Y, &, Morokuma K, (2008) Density functional theory study on a missing piece in understanding of heme chemistry: the reaction mechanism for indoleamine 2,3-dioxygenase and tryptophan 2,3-dioxygenase. J Am Chem Soc 130, 12299-12309.
28. Chung LW, Li X, Sugimoto H, Shiro Y, &, Morokuma K, (2010) ONIOM study on a missing piece in our understanding of heme chemistry: bacterial tryptophan 2,3-dioxygenase with dual oxidants. J Am Chem Soc 132, 11993-12005.
29. Lewis-Ballester A, Batabyal D, Egawa T, Lu C, Lin Y, Marti MA, Capece L, Estrin DA, &, Yeh SR, (2009) Evidence for a ferryl intermediate in a heme-based dioxygenase. Proc Natl Acad Sci USA 106, 17371-17376.
30. Davydov RM, Chauhan N, Thackray SJ, Anderson JL, Papadopoulou ND, Mowat CG, Chapman SK, Raven EL, &, Hoffman BM, (2010) Probing the ternary complexes of indoleamine and tryptophan 2,3-dioxygenases by cryoreduction EPR and ENDOR spectroscopy. J Am Chem Soc 132, 5494-5500.
31. Antonini M, &, Brunori E, (1971) Hemoglobin and Myoglobin and their Reactions with Ligands. North Holland Publishers, Amsterdam.
32. Shimizu T, Nomiyama S, Hirata F, &, Hayaishi O, (1978) Indoleamine 2,3-dioxygenase. Purification and some propertie. J Biol Chem 253, 4700-4706.
33. Patel N, Jones DK, &, Raven EL, (2000) Investigation of the heme-nicotinate interaction in leghemoglobin. Role of hydrogen bonding. Eur J Biochem 267, 2581-2587.
34. Massey V, (1991) A simple method for the determination of redox potentials. In Flavins and flavoproteins (, Curti B, Ronchi S, &, Zanetti G, eds), pp. 59-66. Walter de Gruyter & Co, New York, NY.