Crystal structures of CO and NO adducts of MauG in complex with pre-methylamine dehydrogenase: Implications for the mechanism of dioxygen activation

Biochemistry

Volumn 50, Issue 14, 2011, Pages 2931-2938

  Yukl, Erik T ^a   Goblirsch, Brandon R ^a   Davidson, Victor L ^b   Wilmot, Carrie M ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; CO AND NO; COFACTORS; DIATOMIC OXYGEN; DIOXYGEN ACTIVATION; DISTAL POCKET; METHYLAMINE DEHYDROGENASE; OXYGEN ACTIVATIONS; OXYGEN BINDING;

AMINO ACIDS; CRYSTAL STRUCTURE; HYDROGEN; HYDROGEN BONDS; HYDROGEN PEROXIDE; PORPHYRINS; REACTION INTERMEDIATES;

MOLECULAR OXYGEN;

AMINE DEHYDROGENASE; HEME; HYDROGEN PEROXIDE; NITRIC OXIDE; OXYGEN; TRYPTOPHAN DERIVATIVE; TRYPTOPHAN TRYPTOPHYLQUINONE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CHEMICAL REACTION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME MECHANISM; ENZYME SUBSTRATE; HYDROGEN BOND; OXIDATION; OXYGEN AFFINITY; PARACOCCUS DENITRIFICANS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTON TRANSPORT; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; BIOCATALYSIS; CARBON MONOXIDE; CRYSTALLOGRAPHY, X-RAY; CYTOCHROME-C PEROXIDASE; FERROUS COMPOUNDS; GLUTAMIC ACID; HEME; HEMEPROTEINS; INDOLEQUINONES; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; NITRIC OXIDE; OXIDOREDUCTASES; OXIDOREDUCTASES ACTING ON CH-NH GROUP DONORS; OXYGEN; PARACOCCUS DENITRIFICANS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROPHOTOMETRY; SUBSTRATE SPECIFICITY; TRYPTOPHAN;

EID: 79953683155     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200023n     Document Type: Article

References (38)

1. Wang, Y., Graichen, M. E., Liu, A., Pearson, A. R., Wilmot, C. M., and Davidson, V. L. (2003) MauG, a novel diheme protein required for tryptophan tryptophylquinone biogenesis Biochemistry 42, 7318-7325 (Pubitemid 36735810)
2. Pearson, A. R., De La Mora-Rey, T., Graichen, M. E., Wang, Y., Jones, L. H., Marimanikkupam, S., Agger, S. A., Grimsrud, P. A., Davidson, V. L., and Wilmot, C. M. (2004) Further insights into quinone cofactor biogenesis: probing the role of mauG in methylamine dehydrogenase tryptophan tryptophylquinone formation Biochemistry 43, 5494-5502 (Pubitemid 38620941)
3. Wang, Y., Li, X., Jones, L. H., Pearson, A. R., Wilmot, C. M., and Davidson, V. L. (2005) MauG-dependent in vitro biosynthesis of tryptophan tryptophylquinone in methylamine dehydrogenase J. Am. Chem. Soc. 127, 8258-8259 (Pubitemid 40828124)
4. Li, X., Jones, L. H., Pearson, A. R., Wilmot, C. M., and Davidson, V. L. (2006) Mechanistic possibilities in MauG-dependent tryptophan tryptophylquinone biosynthesis Biochemistry 45, 13276-13283 (Pubitemid 44707687)
5. Shin, S., Abu Tarboush, N., and Davidson, V. L. (2010) Long-range electron transfer reactions between hemes of MauG and different forms of tryptophan tryptophylquinone of methylamine dehydrogenase Biochemistry 49, 5810-5816
6. 2 in the absence of its natural protein substrate Biochemistry 48, 10106-10112
7. Li, X., Fu, R., Lee, S., Krebs, C., Davidson, V. L., and Liu, A. (2008) A catalytic di-heme bis -Fe(IV) intermediate, alternative to an Fe(IV)=O porphyrin radical Proc. Natl. Acad. Sci. U.S.A. 105, 8597-8600 (Pubitemid 351987726)
8. Li, X., Feng, M., Wang, Y., Tachikawa, H., and Davidson, V. L. (2006) Evidence for redox cooperativity between c -type hemes of MauG which is likely coupled to oxygen activation during tryptophan tryptophylquinone biosynthesis Biochemistry 45, 821-828 (Pubitemid 43122246)
9. Pettigrew, G. W., Echalier, A., and Pauleta, S. R. (2006) Structure and mechanism in the bacterial dihaem cytochrome c peroxidases J. Inorg. Biochem. 100, 551-567
10. Jensen, L. M., Sanishvili, R., Davidson, V. L., and Wilmot, C. M. (2010) In crystallo posttranslational modification within a MauG/pre-methylamine dehydrogenase complex Science 327, 1392-1394
11. Lee, S., Shin, S., Li, X., and Davidson, V. (2009) Kinetic mechanism for the initial steps in MauG-dependent tryptophan tryptophylquinone biosynthesis Biochemistry 48, 2442-2447
12. Fu, R., Liu, F., Davidson, V. L., and Liu, A. (2009) Heme iron nitrosyl complex of MauG reveals an efficient redox equilibrium between hemes with only one heme exclusively binding exogenous ligands Biochemistry 48, 11603-11605
13. Fufezan, C., Zhang, J., and Gunner, M. R. (2008) Ligand preference and orientation in b-and c -type heme-binding proteins Proteins 73, 690-704 (Pubitemid 352788650)
14. Lawson, D. M., Stevenson, C. E., Andrew, C. R., and Eady, R. R. (2000) Unprecedented proximal binding of nitric oxide to heme: implications for guanylate cyclase EMBO J. 19, 5661-5671
15. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D 60, 2126-2132 (Pubitemid 41742764)
16. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D 53, 240-255 (Pubitemid 27235885)
17. Vojtechovsky, J., Chu, K., Berendzen, J., Sweet, R. M., and Schlichting, I. (1999) Crystal structures of myoglobin-ligand complexes at near-atomic resolution Biophys. J. 77, 2153-2174 (Pubitemid 29463176)
18. Brucker, E. A., Olson, J. S., Ikeda-Saito, M., and Phillips, G. N., Jr. (1998) Nitric oxide myoglobin: crystal structure and analysis of ligand geometry Proteins 30, 352-356 (Pubitemid 28117655)
19. Nemethy, G., Gibson, K. D., Palmer, K. A., Yoon, C. N., Paterlini, G., Zagari, A., Rumsey, S., and Scheraga, H. A. (1992) Energy parameters in polypeptides. 10. Improved geometrical parameters and nonbonded interactions for use in the ECEPP/3 algorithm, with application to proline-containing peptides J. Phys. Chem. 96, 6472-6484
20. Vitagliano, L., Berisio, R., Mastrangelo, A., Mazzarella, L., and Zagari, A. (2001) Preferred proline puckerings in cis and trans peptide groups: implications for collagen stability Protein Sci. 10, 2627-2632 (Pubitemid 33091586)
21. Sundaramoorthy, M., Terner, J., and Poulos, T. L. (1998) Stereochemistry of the chloroperoxidase active site: crystallographic and molecular-modeling studies Chem. Biol. 5, 461-473 (Pubitemid 28436725)
22. Meunier, B., de Visser, S. P., and Shaik, S. (2004) Mechanism of oxidation reactions catalyzed by cytochrome P450 enzymes Chem. Rev. 104, 3947-3980
23. Raag, R. and Poulos, T. L. (1991) Crystal structures of cytochrome P-450CAM complexed with camphane, thiocamphor, and adamantane: factors controlling P-450 substrate hydroxylation Biochemistry 30, 2674-2684
24. Schlichting, I., Berendzen, J., Chu, K., Stock, A. M., Maves, S. A., Benson, D. E., Sweet, R. M., Ringe, D., Petsko, G. A., and Sligar, S. G. (2000) The catalytic pathway of cytochrome P450cam at atomic resolution Science 287, 1615-1622 (Pubitemid 30127756)
25. Nagano, S. and Poulos, T. L. (2005) Crystallographic study on the dioxygen complex of wild-type and mutant cytochrome P450cam. Implications for the dioxygen activation mechanism J. Biol. Chem. 280, 31659-31663 (Pubitemid 41291912)
26. Shimizu, H., Schuller, D. J., Lanzilotta, W. N., Sundaramoorthy, M., Arciero, D. M., Hooper, A. B., and Poulos, T. L. (2001) Crystal structure of Nitrosomonas europaea cytochrome c peroxidase and the structural basis for ligand switching in bacterial di-heme peroxidases Biochemistry 40, 13483-13490 (Pubitemid 33130776)
27. Fulop, V., Ridout, C. J., Greenwood, C., and Hajdu, J. (1995) Crystal structure of the di-haem cytochrome c peroxidase from Pseudomonas aeruginosa Structure 3, 1225-1233 (Pubitemid 3001428)
28. De Smet, L., Savvides, S. N., Van Horen, E., Pettigrew, G., and Van Beeumen, J. J. (2006) Structural and mutagenesis studies on the cytochrome c peroxidase from Rhodobacter capsulatus provide new insights into structure-function relationships of bacterial di-heme peroxidases J. Biol. Chem. 281, 4371-4379 (Pubitemid 43847869)
29. Sundaramoorthy, M., Terner, J., and Poulos, T. L. (1995) The crystal structure of chloroperoxidase: a heme peroxidase-cytochrome P450 functional hybrid Structure 3, 1367-1377 (Pubitemid 3012264)
30. Kuhnel, K., Derat, E., Terner, J., Shaik, S., and Schlichting, I. (2007) Structure and quantum chemical characterization of chloroperoxidase compound 0, a common reaction intermediate of diverse heme enzymes Proc. Natl. Acad. Sci. U.S.A. 104, 99-104 (Pubitemid 46067991)
31. Ling, Y., Davidson, V. L., and Zhang, Y. (2010) Unprecedented Fe(IV) species in a diheme protein MauG: A quantum chemical investigation on the unusual Mössbauer spectroscopic properties J. Phys. Chem. Lett. 1, 2936-2939
32. Carlsson, G. H., Nicholls, P., Svistunenko, D., Berglund, G. I., and Hajdu, J. (2005) Complexes of horseradish peroxidase with formate, acetate, and carbon monoxide Biochemistry 44, 635-642 (Pubitemid 40105494)
33. Rutter, R., Hager, L. P., Dhonau, H., Hendrich, M., Valentine, M., and Debrunner, P. (1984) Chloroperoxidase compound I: Electron paramagnetic resonance and Mössbauer studies Biochemistry 23, 6809-6816
34. Sivaraja, M., Goodin, D. B., Smith, M., and Hoffman, B. M. (1989) Identification by ENDOR of Trp191 as the free-radical site in cytochrome c peroxidase compound ES Science 245, 738-740 (Pubitemid 19214005)
35. Dolphin, D., Forman, A., Borg, D. C., Fajer, J., and Felton, R. H. (1971) Compounds I of catalase and horse radish peroxidase: pi-cation radicals Proc. Natl. Acad. Sci. U.S.A. 68, 614-618
36. Arciero, D. M. and Hooper, A. B. (1994) A di-heme cytochrome c peroxidase from Nitrosomonas europaea catalytically active in both the oxidized and half-reduced states J. Biol. Chem. 269, 11878-11886 (Pubitemid 24196676)
37. Abu Tarboush, N., Jensen, L. M., Feng, M., Tachikawa, H., Wilmot, C. M., and Davidson, V. L. (2010) Functional importance of tyrosine 294 and the catalytic selectivity for the bis -Fe(IV) state of MauG revealed by replacement of this axial heme ligand with histidine Biochemistry 49, 9783-9791
38. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291