571
Views
5
CrossRef citations to date
0
Altmetric
Award Review

His-Cys and Trp-Cys cross-links generated by post-translational chemical modification

ORCID Icon
Pages 445-454 | Received 30 Sep 2019, Accepted 19 Nov 2019, Published online: 27 Nov 2019

References

  • Walsh CT, Garneau-Tsodikova S, Gatto GJ. Protein posttranslational modifications: the chemistry of proteome diversifications. Angew Chemie Int Ed. 2005;44:7342–7372.
  • Heuts DPHM, Scrutton NS, McIntire WS, et al. What’s in a covalent bond? On the role and formation of covalently bound flavin cofactors. Febs J. 2009;276:3405–3427.
  • Steenkamp DJ, McIntire W, Kenney WC. Structure of the covalently bound coenzyme of trimethylamine dehydrogenase. Evidence for a 6-substituted flavin. J Biol Chem. 1978;253:2818–2824.
  • Fujieda N, Satoh A, Tsuse N, et al. 6-S-cysteinyl flavin mononucleotide-containing histamine dehydrogenase from Nocardioides simplex: molecular cloning, sequencing, overexpression, and characterization of redox centers of enzyme. Biochemistry. 2004;43:10800–10808.
  • Fujieda N, Tsuse N, Satoh A, et al. Production of completely flavinylated histamine dehydrogenase, unique covalently bound flavin, and iron-sulfur cluster-containing enzyme of nocardioides simplex in Escherichia coli, and its properties. Biosci Biotechnol Biochem. 2005;69:2459–2462.
  • Zhou BP, Lewis DA, Kwan SW, et al. Flavinylation of monoamine oxidase B. J Biol Chem. 1995;270:23653–23660.
  • Coulombe R, Yue KQ, Ghisla S, et al. Oxygen access to the active site of cholesterol oxidase through a narrow channel is gated by an Arg-Glu pair. J Biol Chem. 2001;276:30435–30441.
  • Fraaijet MW, Van Den Heuvel RHH, Van Berkel WJH, et al. Covalent flavinylation is essential for efficient redox catalysis in vanillyl-alcohol oxidase. J Biol Chem. 1999;274:35514–35520.
  • Scott Mathews F, Chen ZW, Bellamy HD, et al. Three-dimensional structure of p-cresol methylhydroxylase (flavocytochrome c) from Pseudomonas putida at 3.0-Å resolution. Biochemistry. 1991;30:238–247.
  • Huang CH, Lai WL, Lee MH, et al. Crystal structure of glucooligosaccharide oxidase from Acremonium strictum: a novel flavinylation of 6-S-cysteinyl, 8α-N1-histidyl FAD. J Biol Chem. 2005;280:38831–38838.
  • Mewies M, McIntire WS, Scrutton NS. Covalent attachment of flavin adenine dinucleotide (FAD) and flavin mononucleotide (FMN) to enzymes: the current state of affairs. Protein Sci. 1998;7:7–21.
  • Jin J, Mazon H, van den Heuvel RH, et al. Covalent flavinylation of vanillyl-alcohol oxidase is an autocatalytic process. Febs J. 2008;275:5191–5200.
  • Sevier CS, Kaiser CA. Formation and transfer of disulphide bonds in living cells. Nat Rev Mol Cell Biol. 2002;3:836–847.
  • Arnison PG, Bibb MJ, Bierbaum G, et al. Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep. 2013;30:108–160.
  • Okeley NM, Van Der Donk WA. Novel cofactors via post-translational modifications of enzyme active sites. Chem Biol. 2000;7:R159–R171.
  • Halcrow MA. Chemically modified amino acids in copper proteins that bind or activate dioxygen. Angew Chem. 2001;40:346–349.
  • Davidson VL. Protein-derived cofactors. Expanding the scope of post-translational modifications. Biochemistry. 2007;46:5283–5292.
  • Davidson VL. Generation of protein-derived redox cofactors by posttranslational modification. Mol Biosyst. 2011;7:29–37.
  • Yukl ET, Wilmot CM. Cofactor biosynthesis through protein post-translational modification. Curr Opin Chem Biol. 2012;16:54–59.
  • Davidson VL, Wilmot CM. Posttranslational biosynthesis of the protein-derived cofactor tryptophan tryptophylquinone. Annu Rev Biochem. 2013;82:531–550.
  • Ravikiran B, Mahalakshmi R. Unusual post-translational protein modifications: the benefits of sophistication. RSC Adv. 2014;4:33958–33974.
  • Jones LH, Narayanan A, Hett EC. Understanding and applying tyrosine biochemical diversity. Mol Biosyst. 2014;10:952–969.
  • Klinman JP, Bonnot F. Intrigues and intricacies of the biosynthetic pathways for the enzymatic quinocofactors: PQQ, TTQ, CTQ, TPQ, and LTQ. Chem Rev. 2014;114:4343–4365.
  • Ormö M, Cubitt AB, Kallio K, et al. Crystal structure of the Aequorea victoria green fluorescent protein. Science. 1996;273:1392–1395.
  • Oke M, Ching R, Carter L, et al. Unusual chromophore and cross-links in ranasmurfin: a blue protein from the foam nests of a tropical frog. Angew Chem Int Educ. 2008;47:7853–7856.
  • Schwede TF, Rétey J, Schulz GE. Crystal structure of histidine ammonia-lyase revealing a novel polypeptide modification as the catalytic electrophile. Biochemistry. 1999;38:5355–5361.
  • Datta S, Mori Y, Takagi K, et al. Structure of a quinohemoprotein amine dehydrogenase with an uncommon redox cofactor and highly unusual crosslinking. Proc Natl Acad Sci. 2001;98:14268–14273.
  • Satoh A, Kim JK, Miyahara I, 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. 2002;277:2830–2834.
  • McIntire W, Wemmer D, Chistoserdov A, et al. A new cofactor in a prokaryotic enzyme: tryptophan tryptophylquinone as the redox prosthetic group in methylamine dehydrogenase. Science. 1991;252:817–824.
  • Ito N, Phillips SEV, Stevens C, et al. Novel thioether bond revealed by a 1.7 A crystal structure of galactose oxidase. Nature. 1991;350:87–90.
  • Whittaker MM, Kersten PJ, Cullen D, et al. Identification of catalytic residues in glyoxal oxidase by targeted mutagenesis. J Biol Chem. 1999;274:36226–36232.
  • McCoy JG, Bailey LJ, Bitto E, et al. Structure and mechanism of mouse cysteine dioxygenase. Proc Natl Acad Sci U S A. 2006;103:3084–3089.
  • Schnell R, Sandalova T, Hellman U, et al. Siroheme- and [Fe4-S4]-dependent NirA from Mycobacterium tuberculosis is a sulfite reductase with a covalent Cys-Tyr bond in the active site. J Biol Chem. 2005;280:27319–27328.
  • Polyakov KM, Boyko KM, Tikhonova TV, et al. High-resolution structural analysis of a novel octaheme cytochrome c nitrite reductase from the haloalkaliphilic bacterium Thioalkalivibrio nitratireducens. J Mol Biol. 2009;389:846–862.
  • Whittaker JW. Free radical catalysis by galactose oxidase. Chem Rev. 2003;103:2347–2363.
  • Ye S, Wu X, Wei L, et al. An insight into the mechanism of human cysteine dioxygenase. Key roles of the thioether-bonded tyrosine-cysteine cofactor. J Biol Chem. 2007;282:3391–3402.
  • Seebeck FP. In vitro reconstitution of mycobacterial ergothioneine biosynthesis. J Am Chem Soc. 2010;132:6632–6633.
  • Lerch K, Il E. Amino acid sequence of tyrosinase from Neurospora crassa. Proc Natl Acad Sci. 1978;75:3635–3639.
  • Cuff ME, Miller KI, van Holde KE, et al. Crystal structure of a functional unit from Octopus hemocyanin. J Mol Biol. 1998;278:855–870.
  • Klabunde T, Eicken C, Sacchettini JC, et al. Crystal structure of a plant catechol oxidase containing a dicopper center. Nat Struct Biol. 1998;5:1084–1090.
  • Ismaya WT, Rozeboom HJ, Weijn A, et al. Crystal structure of Agaricus bisporus mushroom tyrosinase: identity of the tetramer subunits and interaction with tropolone. Biochemistry. 2011;50:5477–5486.
  • Nakamura M, Nakajima T, Ohba Y, et al. Identification of copper ligands in Aspergillus oryzae tyrosinase by site-directed mutagenesis. Biochem J. 2000;350(Pt 2):537–545.
  • Virador VM, Reyes Grajeda JP, Blanco-Labra A, et al. Cloning, sequencing, purification, and crystal structure of Grenache (Vitis vinifera) polyphenol oxidase. J Agric Food Chem. 2010;58:1189–1201.
  • Obata H, Ishida H, Hata Y, et al. Cloning of a novel tyrosinase-encoding gene (Melb) from Aspergillus oryzae and its overexpression in solid-state culture (Rice Koji). J Biosci Bioeng. 2004;97:400–405.
  • Fujieda N, Ikeda T, Murata M, et al. Post-translational his-cys cross-linkage formation in tyrosinase induced by copper(II)-peroxo species. J Am Chem Soc. 2011;133:1180–1183.
  • Fujieda N, Murata M, Yabuta S, et al. Multifunctions of MelB, a fungal tyrosinase from Aspergillus oryzae. Chembiochem. 2012;13:193–201.
  • Fujieda N, Yabuta S, Ikeda T, et al. Crystal structures of copper-depleted and copper-bound fungal pro-tyrosinase: insights into endogenous cysteine-dependent copper incorporation. J Biol Chem. 2013;288:22128–22140.
  • Solomon EI, Heppner DE, Johnston EM, et al. Copper active sites in biology. Chem Rev. 2014;114:3659–3853.
  • Firbank SJ, Rogers MS, Wilmot CM, et al. Crystal structure of the precursor of galactose oxidase: an unusual self-processing enzyme. Proc Natl Acad Sci. 2001;98:12932–12937.
  • Whittaker MM, Whittaker JW. Cu(I)-dependent biogenesis of the galactose oxidase redox cofactor. J Biol Chem. 2003;278:22090–22101.
  • O’Halloran TV, Culotta VC. Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem. 2000;275:25057–25060.
  • Prohaska JR, Gybina AA. Intracellular copper transport in mammals. J Nutr. 2004;134:1003–1006.
  • Mauracher SG, Molitor C, Al-Oweini R, et al. Latent and active abPPO4 mushroom tyrosinase cocrystallized with hexatungstotellurate(VI) in a single crystal. Acta Crystallogr Sect D Biol Crystallogr. 2014;70:2301–2315.
  • Davies CG, Fellner M, Tchesnokov EP, et al. The Cys-Tyr cross-link of cysteine dioxygenase changes the optimal pH of the reaction without a structural change. Biochemistry. 2014;53:7961–7968.
  • Janes S, Mu D, Wemmer D, et al. A new redox cofactor in eukaryotic enzymes: 6-hydroxydopa at the active site of bovine serum amine oxidase. Science. 1990;248:981–987.
  • Wang SX, Mure M, Medzihradszky KF, et al. A crosslinked cofactor in lysyl oxidase: redox function for amino acid side chains. Science. 1996;273:1078–1084.
  • Fujieda N, Mori M, Kano K, et al. Spectroelectrochemical evaluation of redox potentials of cysteine tryptophylquinone and two hemes c in quinohemoprotein amine dehydrogenase from Paracoccus denitrificans. Biochemistry. 2002;41:13736–13743.
  • Takagi K, Torimura M, Kawaguchi K, et al. Biochemical and electrochemical characterization of quinohemoprotein amine dehydrogenase from Paracoccus denitrificans. Biochemistry. 1999;38:6935–6942.
  • Okazaki S, Nakano S, Matsui D, et al. X-ray crystallographic evidence for the presence of the cysteine tryptophylquinone cofactor in L-lysine epsilon-oxidase from Marinomonas mediterranea. J Biochem. 2013;154:233–236.
  • Sehanobish E, Williamson HR, Davidson VL. Roles of conserved residues of the glycine oxidase GoxA in controlling activity, cooperativity, subunit composition, and cysteine tryptophylquinone biosynthesis. J Biol Chem. 2016;291:23199–23207.
  • Andreo-Vidal A, Mamounis KJ, Sehanobish E, et al. Structure and enzymatic properties of an unusual cysteine tryptophylquinone-dependent glycine oxidase from Pseudoalteromonas luteoviolacea. Biochemistry. 2018;57:1155–1165.
  • Ma Z, Davidson VL. The redox properties of a cysteine tryptophylquinone-dependent glycine oxidase are distinct from those of tryptophylquinone-dependent dehydrogenases. Biochemistry. 2019;58:2243–2249.
  • Nakai T, Ito H, Kobayashi K, et al. The radical S-Adenosyl-L-methionine enzyme QhpD catalyzes sequential formation of intra-protein sulfur-to-methylene carbon thioether bonds. J Biol Chem. 2015;290:11144–11166.
  • Ono K, Okajima T, Tani M, et al. Involvement of a putative [Fe-S]-cluster-binding protein in the biogenesis of quinohemoprotein amine dehydrogenase. J Biol Chem. 2006;281:13672–13684.
  • Nakai T, Ono K, Kuroda S, et al. An unusual subtilisin-like serine protease is essential for biogenesis of quinohemoprotein amine dehydrogenase. J Biol Chem. 2012;287:6530–6538.
  • Nakai T, Deguchi T, Frébort I, et al. Identification of genes essential for the biogenesis of quinohemoprotein amine dehydrogenase. Biochemistry. 2014;53:895–907.
  • Chacón-Verdú MD, Campillo-Brocal JC, Lucas-Elío P, et al. Characterization of recombinant biosynthetic precursors of the cysteine tryptophylquinone cofactors of l-lysine-epsilon-oxidase and glycine oxidase from Marinomonas mediterranea. Biochim Biophys Acta - Proteins Proteomics. 2015;1854:1123–1131.
  • Fujieda N, Mori M, Ikeda T, et al. The silent form of quinohemoprotein amine dehydrogenase from Paracoccus denitrificans. Biosci Biotechnol Biochem. 2009;73:524–529.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.