Diradical intermediate within the context of tryptophan tryptophylquinone biosynthesis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 12, 2013, Pages 4569-4573

  Yukl, Erik T ^a   Liu, Fange ^b   Krzystek, J ^c   Shin, Sooim ^d   Jensen, Lyndal M R ^a   Davidson, Victor L ^d   Wilmot, Carrie M ^a   Liu, Aimin ^b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b GEORGIA STATE UNIVERSITY   (United States)

^c FLORIDA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Cofactor biosynthesis; Electron transfer; Heme; Posttranslational modification; Tryptophan radical

Indexed keywords

OXIDOREDUCTASE; PREMETHYLAMINE DEHYDROGENASE; QUINONE DERIVATIVE; RADICAL; TRYPTOPHAN; TRYPTOPHAN DERIVATIVE; TRYPTOPHAN TRYPTOPHYLQUINONE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON; ELECTRON SPIN RESONANCE; MASS SPECTROMETRY; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MODIFICATION; ULTRAVIOLET SPECTROSCOPY;

BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; INDOLEQUINONES; MASS SPECTROMETRY; OXIDATION-REDUCTION; OXIDOREDUCTASES; PARACOCCUS DENITRIFICANS; SUBSTRATE SPECIFICITY; TRYPTOPHAN;

EID: 84875243197     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1215011110     Document Type: Article

References (43)

1. Stubbe J, van Der Donk WA (1998) Protein radicals in enzyme catalysis. Chem Rev 98(2):705-762.
2. Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521-565.
3. Svistunenko DA, Wilson MT, Cooper CE (2004) Tryptophan or tyrosine? On the nature of the amino acid radical formed following hydrogen peroxide treatment of cytochrome c oxidase. Biochim Biophys Acta 1655(1-3):372-380.
4. Stubbe J, Nocera DG, Yee CS, Chang MC (2003) Radical initiation in the class I ribonucleotide reductase: Long-range proton-coupled electron transfer? Chem Rev 103(6):2167-2201.
5. Aubert C, Vos MH, Mathis P, Eker APM, Brettel K (2000) Intraprotein radical transfer during photoactivation of DNA photolyase. Nature 405(6786):586-590.
6. Davidson VL (2011) Generation of protein-derived redox cofactors by posttranslational modification. Mol Biosyst 7(1):29-37.
7. Pearson AR, et al. (2004) Further insights into quinone cofactor biogenesis: Probing the role of MauG in methylamine dehydrogenase tryptophan tryptophylquinone formation. Biochemistry 43(18):5494-5502.
8. Wang YT, et al. (2005) MauG-dependent in vitro biosynthesis of tryptophan tryptophylquinone in methylamine dehydrogenase. J Am Chem Soc 127(23):8258-8259.
9. Li XH, et al. (2008) A catalytic di-heme bis-Fe(IV) intermediate, alternative to an Fe (IV)=O porphyrin radical. Proc Natl Acad Sci USA 105(25):8597-8600.
10. Jensen LMR, Sanishvili R, Davidson VL, Wilmot CM (2010) In crystallo posttranslational modification within a MauG/pre-methylamine dehydrogenase complex. Science 327(5971):1392-1394.
11. Li XH, Jones LH, Pearson AR, Wilmot CM, Davidson VL (2006) Mechanistic possibilities in MauG-dependent tryptophan tryptophylquinone biosynthesis. Biochemistry 45(44): 13276-13283.
12. Hamburger R, Azaz E, Donbrow M (1975) Autoxidation of polyoxyethylenic non-ionic surfactants and of polyethylene glycols. Pharm Acta Helv 50(1-2):10-17.
13. Choi M, Shin S, Davidson VL (2012) Characterization of electron tunneling and hole hopping reactions between different forms of MauG and methylamine dehydrogenase within a natural protein complex. Biochemistry 51(35):6942-6949.
14. Tarboush NA, et al. (2011) Mutagenesis of tryptophan199 suggests that hopping is required for MauG-dependent tryptophan tryptophylquinone biosynthesis. Proc Natl Acad Sci USA 108(41):16956-16961.
15. Husain M, Davidson VL, Gray KA, Knaff DB (1987) Redox properties of the quinoprotein methylamine dehydrogenase from Paracoccus denitrificans. Biochemistry 26(13):4139-4143.
16. Bleifuss G, et al. (2001) Tryptophan and tyrosine radicals in ribonucleotide reductase: A comparative high-field EPR study at 94 GHz. Biochemistry 40(50):15362-15368.
17. Dorlet P, et al. (2002) High-field EPR study of tyrosyl radicals in prostaglandin H(2) synthase-1. Biochemistry 41(19):6107-6114.
18. Liu AM, Barra AL, Rubin H, Lu GZ, Gräslund A (2000) Heterogeneity of the local electrostatic environment of the tyrosyl radical in Mycobacterium tuberculosis ribonucleotide reductase observed by high-field electron paramagnetic resonance. J Am Chem Soc 122(9):1974-1978.
19. Smith AT, Doyle WA, Dorlet P, Ivancich A (2009) Spectroscopic evidence for an engineered, catalytically active Trp radical that creates the unique reactivity of lignin peroxidase. Proc Natl Acad Sci USA 106(38):16084-16089.
20. Stoll S, et al. (2011) Hydrogen bonding of tryptophan radicals revealed by EPR at 700 GHz. J Am Chem Soc 133(45):18098-18101.
21. Yokoyama K, Smith AA, Corzilius B, Griffin RG, Stubbe J (2011) Equilibration of tyrosyl radicals (Y(356)•, Y(731)•, Y(730)•) in the radical propagation pathway of the Escherichia coli class la ribonucleotide reductase. J Am Chem Soc 133(45):18420-18432.
22. Walden SE, Wheeler RA (1997) First evidence of anchimeric spin delocalization in tryptophan radical cation. J Am Chem Soc 119(13):3175-3176.
23. Connor HD, Sturgeon BE, Mottley C, Sipe HJ, Jr., Mason RP (2008) L-tryptophan radical cation electron spin resonance studies: Connecting solution-derived hyperfine coupling constants with protein spectral interpretations. J Am Chem Soc 130(20): 6381-6387.
24. Bernini C, et al. (2011) EPR parameters of amino acid radicals in P. eryngii versatile peroxidase and its W164Y variant computed at the QM/MM level. Phys Chem Chem Phys 13(11):5078-5098.
25. Lendzian F, et al. (1996) Electronic structure of neutral tryptophan radicals in ribonucleotide reductase studied by EPR and ENDOR spectroscopy. J Am Chem Soc 118(34):8111-8120.
26. Pogni R, et al. (2006) A tryptophan neutral radical in the oxidized state of versatile peroxidase from Pleurotus eryngii: A combined multifrequency EPR and density functional theory study. J Biol Chem 281(14):9517-9526.
27. Un S (2005) The g-values and hyperfine coupling of amino acid radicals in proteins: comparison of experimental measurements with ab initio calculations. Magn Reson Chem 43(Spec no):S229-S236.
28. Lee SY, Shin S, Li XH, Davidson VL (2009) Kinetic mechanism for the initial steps in MauG-dependent tryptophan tryptophylquinone biosynthesis. Biochemistry 48(11): 2442-2447.
29. Williams-Smith DL, Bray RC, Barber MJ, Tsopanakis AD, Vincent SP (1977) Changes in apparent pH on freezing aqueous buffer solutions and their relevance to biochemical electron-paramagnetic-resonance spectroscopy. Biochem J 167(3):593-600.
30. Douzou P (1977) Cryobiochemistry: An Introduction (Academic, London).
31. Mazur P (1970) Cryobiology: The freezing of biological systems. Science 168(3934): 939-949.
32. 2- radicals in light-water and heavy-water solutions - a pulse-radiolysis study. J Phys Chem 95(9):3639-3643.
33. Baldwin J, et al. (2000) Mechanism of rapid electron transfer during oxygen activation in the R2 subunit of Escherichia coli ribonucleotide reductase. 1. Evidence for a transient tryptophan radical. J Am Chem Soc 122(49):12195-12206.
34. Jensen GM, Goodin DB, Bunte SW (1996) Density functional and MP2 calculations of spin densities of oxidized 3-methylindole: Models for tryptophan radicals. J Phys Chem 100(3):954-959.
35. Wang YT, et al. (2003) MauG, a novel diheme protein required for tryptophan tryptophylquinone biogenesis. Biochemistry 42(24):7318-7325.
36. Graichen ME, et al. (1999) Heterologous expression of correctly assembled methylamine dehydrogenase in Rhodobacter sphaeroides. J Bacteriol 181(14):4216-4222.
37. Hassan AK, et al. (2000) Ultrawide band multifrequency high-field EMR technique: A methodology for increasing spectroscopic information. J Magn Reson 142(2):300-312.
38. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326.
39. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53(Pt 3): 240-255.
40. Bailey S (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D Biol 50(Pt 5):760-763.
41. Emsley P, Cowtan K (2004) COOT: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Pt 12, Pt 1):2126-2132.
42. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.
43. Adams PD, et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66(Pt 2):213-221.