Uncovering novel biochemistry in the mechanism of tryptophan tryptophylquinone cofactor biosynthesis

Current Opinion in Chemical Biology

Volumn 13, Issue 4, 2009, Pages 469-474

  Wilmot, Carrie M ^a   Davidson, Victor L ^b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINE DEHYDROGENASE; AMINO ACID; CATION; CYTOCHROME C PEROXIDASE; HEME OXYGENASE; MAUG PROTEIN; PEROXIDASE; PORPHYRIN; PROTEIN DERIVATIVE; QUINONE DERIVATIVE; TRYPTOPHAN; TRYPTOPHAN TRYPTOPHYLQUINONE; UNCLASSIFIED DRUG;

BIOCHEMISTRY; BIOSYNTHESIS; ELECTRON; HUMAN; KINETICS; NONHUMAN; OXIDATION; PARACOCCUS DENITRIFICANS; PROTEIN PROCESSING; REVIEW;

EID: 70349083704     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2009.06.026     Document Type: Review

References (40)

1. Davidson V.L. Protein-derived cofactors. Expanding the scope of post-translational modifications. Biochemistry 46 (2007) 5283-5292. This review is a great introduction and overview to the breadth of cofactors derived through the post-translational modification of protein polypeptides, along with the emerging research into their biosynthesis.
2. Okeley N.M., and van der Donk W.A. Novel cofactors via post-translational modifications of enzyme active sites. Chem Biol 7 (2000) R159-171
3. Davidson V.L. Structure and mechanism of tryptophylquinone enzymes. Bioorg Chem 33 (2005) 159-170
4. McIntire W.S., Wemmer D.E., Chistoserdov A., and Lidstrom M.E. A new cofactor in a prokaryotic enzyme: tryptophan tryptophylquinone as the redox prosthetic group in methylamine dehydrogenase. Science 252 (1991) 817-824
5. Datta S., Mori Y., Takagi K., Kawaguchi K., Chen Z.W., Okajima T., Kuroda S., Ikeda T., Kano K., Tanizawa K., et al. Structure of a quinohemoprotein amine dehydrogenase with an uncommon redox cofactor and highly unusual crosslinking. Proc Natl Acad Sci U S A 98 (2001) 14268-14273
6. Satoh A., Kim J.K., Miyahara I., Devreese B., Vandenberghe I., Hacisalihoglu A., Okajima T., Kuroda S., Adachi O., Duine J.A., et al. Crystal structure of quinohemoprotein amine dehydrogenase from Pseudomonas putida. Identification of a novel quinone cofactor encaged by multiple thioether cross-bridges. J Biol Chem 277 (2002) 2830-2834
7. Mure M. Tyrosine-derived quinone cofactors. Acc Chem Res 37 (2004) 131-139
8. Salmi M., and Jalkanen S. Cell-surface enzymes in control of leukocyte trafficking. Nat Rev Immunol 5 (2005) 760-771
9. Janes S.M., Mu D., Wemmer D., Smith A.J., Kaur S., Maltby D., Burlingame A.L., and Klinman J.P. A new redox cofactor in eukaryotic enzymes: 6-hydroxydopa at the active site of bovine serum amine oxidase. Science 248 (1990) 981-987
10. Kagan H.M., and Trackman P.C. Properties and function of lysyl oxidase. Am J Respir Cell Mol Biol 5 (1991) 206-210
11. Wang S.X., Mure M., Medzihradszky K.F., Burlingame A.L., Brown D.E., Dooley D.M., Smith A.J., Kagan H.M., and Klinman J.P. A crosslinked cofactor in lysyl oxidase: redox function for amino acid side chains. Science 273 (1996) 1078-1084
12. Davidson V.L., Jones L.H., and Graichen M.E. Reactions of benzylamines with methylamine dehydrogenase. Evidence for a carbanionic reaction intermediate and reaction mechanism similar to eukaryotic quinoproteins. Biochemistry 31 (1992) 3385-3390
13. Bollinger J.A., Brown D.E., and Dooley D.M. The formation of lysine tyrosylquinone (LTQ) is a self-processing reaction. Expression and characterization of a Drosophila lysyl oxidase. Biochemistry 44 (2005) 11708-11714
14. Dubois J.L., and Klinman J.P. Mechanism of post-translational quinone formation in copper amine oxidases and its relationship to the catalytic turnover. Arch Biochem Biophys 433 (2005) 255-265
15. Moore R.H., Spies M.A., Culpepper M.B., Murakawa T., Hirota S., Okajima T., Tanizawa K., and Mure M. Trapping of a dopaquinone intermediate in the TPQ cofactor biogenesis in a copper-containing amine oxidase from Arthrobacter globiformis. J Am Chem Soc 129 (2007) 11524-11534
16. Wang Y., Graichen M.E., Liu A., Pearson A.R., Wilmot C.W., and Davidson V.L. MauG, a novel diheme protein required for tryptophan tryptophylquinone biogenesis. Biochemistry 42 (2003) 7318-7325
17. Wang Y., Li X., Jones L.H., Pearson A.R., Wilmot C.M., and Davidson V.L. MauG-dependent in vitro biosynthesis of tryptophan tryptophylquinone in methylamine dehydrogenase. J Am Chem Soc 127 (2005) 8258-8259
18. Ono K., Okajima T., Tani M., Kuroda S., Sun D., Davidson V.L., and Tanizawa K. Involvement of a putative [Fe-S]-cluster-binding protein in the biogenesis of quinohemoprotein amine dehydrogenase. J Biol Chem 281 (2006) 13672-13684
19. van der Palen C.J., Reijnders W.N., de Vries S., Duine J.A., and van Spanning R.J. MauE and MauD proteins are essential in methylamine metabolism of Paracoccus denitrificans. Antonie Van Leeuwenhoek 72 (1997) 219-228
20. van der Palen C.J., Slotboom D.J., Jongejan L., Reijnders W.N., Harms N., Duine J.A., and van Spanning R.J. Mutational analysis of mau genes involved in methylamine metabolism in Paracoccus denitrificans. Eur J Biochem 230 (1995) 860-871
21. van Spanning R.J., Wansell C.W., Reijnders W.N., Oltmann L.F., and Stouthamer A.H. Mutagenesis of the gene encoding amicyanin of Paracoccus denitrificans and the resultant effect on methylamine oxidation. FEBS Lett 275 (1990) 217-220
22. Pearson A.R., de la Mora-Rey T., Graichen M.E., Wang Y., Jones L.H., Marimanikkupam S., Aggar S.A., Grimsrud P.A., Davidson V.L., and Wilmot C.W. Further insights into quinone cofactor biogenesis: probing the role of MauG in methylamine dehydrogenase TTQ formation. Biochemistry 43 (2004) 5494-5502
23. Pettigrew G.W., Echalier A., and Pauleta S.R. Structure and mechanism in the bacterial dihaem cytochrome c peroxidases. J Inorg Biochem 100 (2006) 551-567. This is a wonderful review that uses a common framework of molecular structure to explain the complexities of activation and catalytic mechanism within the different diheme cytochrome c peroxidases. These enzymes are homologous to MauG, but there are significant catalytic differences between these two enzyme families.
24. Stevens J.M., Daltrop O., Allen J.W., and Ferguson S.J. C-type cytochrome formation: chemical and biological enigmas. Acc Chem Res 37 (2004) 999-1007
25. Li X., Feng M., Wang Y., Tachikawa H., and Davidson V.L. Evidence for redox cooperativity between c-type hemes of MauG which is likely coupled to oxygen activation during tryptophan tryptophylquinone biosynthesis. Biochemistry 45 (2006) 821-828. The authors detail the highly unusual negative redox cooperativity in MauG, which arises from the similar intrinsic oxidation-reduction midpoint potentials of the two hemes, and the facile electron transfer between them.
26. Graichen M.E., Jones L.H., Sharma B.V., van Spanning R.J., Hosler J.P., and Davidson V.L. Heterologous expression of correctly assembled methylamine dehydrogenase in Rhodobacter sphaeroides. J Bacteriol 181 (1999) 4216-4222
27. Pearson A.R., Marimanikkuppam S., Li X., Davidson V.L., and Wilmot C.M. Isotope labeling studies reveal the order of oxygen incorporation into the tryptophan tryptophylquinone cofactor of methylamine dehydrogenase. J Am Chem Soc 128 (2006) 12416-12417
28. Backes G., Davidson V.L., Huitema F., Duine J.A., and Sanders-Loehr J. Characterization of the tryptophan-derived quinone cofactor of methylamine dehydrogenase by resonance Raman spectroscopy. Biochemistry 30 (1991) 9201-9210
29. Li X., Jones L.H., Pearson A.R., Wilmot C.M., and Davidson V.L. Mechanistic possibilities in MauG-dependent tryptophan tryptophylquinone biosynthesis. Biochemistry 45 (2006) 13276-13283. This paper details the diversity of electron donors that can be utilized in aerobic MauG-catalyzed TTQ biosynthesis. An intermediate is also identified that is postulated to be O-quinol, the two-electron reduced form of TTQ. This enables for the first time a hypothesized mechanism to be put forward for MauG catalysis.
30. Lee S., Shin S., Li X., and Davidson V.L. Kinetic mechanism for the initial steps in MauG-dependent tryptophan tryptophylquinone biosynthesis. Biochemistry 48 (2009) 2442-2447. The authors demonstrate that the first two-electron cycle of MauG-dependent TTQ biosynthesis follows a random order kinetic mechanism. Rates for different steps in the cycle are defined.
31. Li X., Fu R., Lee S., Krebs C., Davidson V.L., and Liu A. A catalytic diheme bis-Fe(IV)intermediate, alternative to an Fe(IV){double bond, long}O porphyrin radical. Proc Natl Acad Sci U S A 105 (2008) 8597-8600. This paper demonstrates that the catalytically competent MauG oxidant is an unprecedented high-valent bis-Fe(IV) diheme intermediate that is remarkably stable. Mössbauer spectroscopy identifies two distinct Fe(IV) heme species within the intermediate; one consistent with an Fe(IV){double bond, long}O, and the other assigned as an Fe(IV) with two axial ligands from the protein. This latter species has never before been observed in biology. The bis-Fe(IV) diheme intermediate is an Fe(V) equivalent and a cousin to Compound I. Addition of protein substrate to the MauG bis-Fe(IV) diheme intermediate leads to the formation of a long-lived aromatic radical on the protein substrate. This system is remarkable in the level of stabilization the protein environment gives to both a high-valent iron species and a protein-based aromatic radical that in other systems would rapidly decay.
32. Hersleth H.P., Ryde U., Rydberg P., Gorbitz C.H., and Andersson K.K. Structures of the high-valent metal-ion haem-oxygen intermediates in peroxidases, oxygenases and catalases. J Inorg Biochem 100 (2006) 460-476. This review is a detailed synopsis of high-valent heme-oxygen enzyme intermediates defined by X-ray crystallography and tested through quantum mechanical calculations.
33. Meunier B., de Visser S.P., and Shaik S. Mechanism of oxidation reactions catalyzed by cytochrome P450 enzymes. Chem Rev 104 (2004) 3947-3980
34. Davidson V.L., Brooks H.B., Graichen M.E., Jones L.H., and Hyun Y.L. Detection of intermediates in tryptophan tryptophylquinone enzymes. Methods Enzymol 258 (1995) 176-190
35. Li X., Fu R., Liu A., and Davidson V.L. Kinetic and physical evidence that the diheme enzyme MauG tightly binds to a biosynthetic precursor of methylamine dehydrogenase with incompletely formed tryptophan tryptophylquinone. Biochemistry 47 (2008) 2908-2912
36. Echalier A., Brittain T., Wright J., Boycheva S., Mortuza G.B., Fulop V., and Watmough N.J. Redox-linked structural changes associated with the formation of a catalytically competent form of the diheme cytochrome c peroxidase from Pseudomonas aeruginosa. Biochemistry 47 (2008) 1947-1956
37. Echalier A., Goodhew C.F., Pettigrew G.W., and Fulop V. Activation and catalysis of the diheme cytochrome c peroxidase from Paracoccus pantotrophus. Structure 14 (2006) 107-117
38. 1 nitrite reductase and cytochrome c peroxidase. Adv Inorg Chem 51 (2001) 163-204
39. Arciero D.M., and Hooper A.B. A diheme cytochrome c peroxidase from Nitrosomonas europaea catalytically active in both the oxidized and half-reduced states. J Biol Chem 269 (1994) 11878-11886
40. Shimizu H., Schuller D.J., Lanzilotta W.N., Sundaramoorthy M., Arciero D.M., Hooper A.B., and Poulos T.L. Crystal structure of Nitrosomonas europaea cytochrome c peroxidase and the structural basis for ligand switching in bacterial diheme peroxidases. Biochemistry 40 (2001) 13483-13490