Galactonolactone oxidoreductase from Trypanosoma cruzi employs a FAD cofactor for the synthesis of vitamin C

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1814, Issue 5, 2011, Pages 545-552

  Kudryashova, Elena V ^a,b   Leferink, Nicole G H ^a,c   Slot, Ilse G M ^a   Van Berkel, Willem J H ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Flavoprotein; Galactonolactone oxidoreductase; Refolding; Reverse micelles; Trypanosoma cruzi; Vitamin C

Indexed keywords

ASCORBIC ACID; FLAVINE ADENINE NUCLEOTIDE; FLAVINE ADENINE NUCLEOTIDE COFACTOR; GALACTONOLACTONE OXIDOREDUCTASE; LACTONE DERIVATIVE; OXIDOREDUCTASE; OXYGEN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CATALYSIS; CONTROLLED STUDY; ELECTRON; ENZYME ACTIVITY; MICELLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; TRYPANOSOMA CRUZI;

AMINO ACID SEQUENCE; ASCORBIC ACID; CHROMATOGRAPHY, THIN LAYER; CIRCULAR DICHROISM; FLAVIN-ADENINE DINUCLEOTIDE; MOLECULAR SEQUENCE DATA; OXIDOREDUCTASES; PROTOZOAN PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SUGAR ACIDS; TRYPANOSOMA CRUZI;

PYRONIA TITHONUS; TRYPANOSOMA CRUZI;

EID: 79953197199     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2011.03.001     Document Type: Article

References (39)

1. F. Irigoín, L. Cibils, M.A. Comini, S.R. Wilkinson, L. Flohé, and R. Radi Insights into the redox biology of Trypanosoma cruzi: Trypanothione metabolism and oxidant detoxification Free Radic Biol Med 45 2008 733 742
2. R.L. Krauth-Siegel, and M.A. Comini Redox control in trypanosomatids, parasitic protozoa with trypanothione-based thiol metabolism Biochim Biophys Acta 1780 2008 1236 1248
3. H. Castro, and A.M. Tomás Peroxidases of trypanosomatids Antioxid Redox Signal 10 2008 1593 1606 (Pubitemid 351934269)
4. S.R. Wilkinson, S.O. Obado, I.L. Mauricio, and J.M. Kelly Trypanosoma cruzi expresses a plant-like ascorbate-dependent hemoperoxidase localized to the endoplasmic reticulum Proc Natl Acad Sci U S A 99 2002 13453 13458 (Pubitemid 35215402)
5. F.J. Logan, M.C. Taylor, S.R. Wilkinson, H. Kaur, and J.M. Kelly The terminal step in vitamin C biosynthesis in Trypanosoma cruzi is mediated by a FMN-dependent galactonolactone oxidase Biochem. J. 407 2007 419 426 (Pubitemid 350058475)
6. S.R. Wilkinson, S.R. Prathalingam, M.C. Taylor, D. Horn, and J.M. Kelly Vitamin C biosynthesis in trypanosomes: a role for the glycosome Proc Natl Acad Sci U S A 102 2005 11645 11650 (Pubitemid 41170780)
7. I.B. Chatterjee Evolution and the biosynthesis of ascorbic acid Science 182 1973 1271 1272
8. M. Nishikimi, R. Fukuyama, S. Minoshima, N. Shimizu, and K. Yagi Cloning and chromosomal mapping of the human nonfunctional gene for l-gulono-γ- lactone oxidase, the enzyme for l-ascorbic acid biosynthesis missing in man J Biol Chem 269 1994 13685 13688
9. M.W. Fraaije, W.J.H. van Berkel, J.A.E. Benen, J. Visser, and A. Mattevi A novel oxidoreductase family sharing a conserved FAD-binding domain Trends Biochem Sci 23 1998 206 207 (Pubitemid 28302616)
10. N.G.H. Leferink, D.P.H.M. Heuts, M.W. Fraaije, and W.J.H. van Berkel The growing VAO flavoprotein family Arch Biochem Biophys 474 2008 292 301
11. N.G.H. Leferink, E. van Duijn, A. Barendregt, A.J.R. Heck, and W.J.H. van Berkel Galactonolactone dehydrogenase requires a redox-sensitive thiol for optimal production of vitamin C Plant Physiol 150 2009 596 605
12. N.G.H. Leferink, W.A.M. van den Berg, and W.J.H. van Berkel l-Galactono-γ-lactone dehydrogenase from Arabidopsis thaliana, a flavoprotein involved in vitamin C biosynthesis FEBS J 275 2008 713 726 (Pubitemid 351160964)
13. E. De Bernardez Clark, E. Schwarz, and R. Rudolph Inhibition of aggregation side reactions during in vitro protein folding Methods in enzymology 309 1999 217 236 (Pubitemid 29446452)
14. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
15. K. Ôba, S. Ishikawa, M. Nishikawa, H. Mizuno, and T. Yamamoto Purification and properties of L-galactono-γ-lactone dehydrogenase, a key enzyme for ascorbic acid biosynthesis, from sweet potato roots J Biochem (Tokyo) 117 1995 120 124
16. R. Köhling, J. Woenckhaus, N.L. Klyachko, and R. Winter Small-angle neutron scattering study of the effect of pressure on AOT - n-octane - water mesophases and the effect of α-chymotrypsin incorporation Langmuir 18 2002 8626 8632 (Pubitemid 35289576)
17. A.V. Levashov, and N.L. Klyachko Reverse micellar systems E.N. Vulfson, P.J. Halling, H.L. Holland, Methods in Biotechnology, vol. 15: Enzymes in Nonaqueous Solvents: Methods and Protocols 2001 Humana Press Totowa, NJ 575 586
18. N.L. Klyachko, and A.V. Levashov Bioorganic synthesis in reverse micelles and related systems Curr Opin Colloid Interface Sci 8 2003 179 186 (Pubitemid 39665702)
19. M.-P. Pileni, T. Zemb, and C. Petit Solubilization by reverse micelles: solute localization and structure perturbation Chemical Physics Letters 118 1985 414 420
20. K. Vos, C. Laane, S.R. Weijers, A. Van Hoek, C. Veeger, and A.J.W.G. Visser Time-resolved fluorescence and circular dichroism of porphyrin cytochrome c and Zn-porphyrin cytochrome c incorporated in reversed micelles Eur J Biochem 169 1987 259 268
21. J. Frébortová, M.W. Fraaije, P. Galuszka, M. Šebela, P. Peč, J. Hrbáč, O. Novák, K.D. Bilyeu, J.T. English, and I. Frébort Catalytic reaction of cytokinin dehydrogenase: preference for quinones as electron acceptors Biochem J 380 2004 121 130 (Pubitemid 38725736)
22. N.L. Klyachko, V.A. Shchedrina, A.V. Efimov, S.V. Kazakov, I.G. Gazaryan, B.S. Kristal, and A.M. Brown pH-dependent substrate preference of pig heart lipoamide dehydrogenase varies with oligomeric state: response to mitochondrial matrix acidification J Biol Chem 280 2005 16106 16114 (Pubitemid 40616735)
23. N.G.H. Leferink, M.W. Fraaije, H.J. Joosten, P.J. Schaap, A. Mattevi, and W.J.H. van Berkel Identification of a gatekeeper residue that prevents dehydrogenases from acting as oxidases J Biol Chem 284 2009 4392 4397
24. P. Polverino de Laureto, E. Frare, R. Gottardo, H. van Dael, and A. Fontana Partly folded states of members of the lysozyme/lactalbumin superfamily: a comparative study by circular dichroism spectroscopy and limited proteolysis Protein Science 11 2002 2932 2946 (Pubitemid 35365259)
25. E. De Bernardez Clark Refolding of recombinant proteins Curr Opin Biotechnol 9 1998 157 163 (Pubitemid 28195001)
26. H. Lilie, E. Schwarz, and R. Rudolph Advances in refolding of proteins produced in E. coli Curr Opin Biotechnol 9 1998 497 501 (Pubitemid 28478971)
27. S. Misawa, and I. Kumagai Refolding of therapeutic proteins produced in Escherichia coli as inclusion bodies Biopolymers 51 1999 297 307 (Pubitemid 30014252)
28. A.A. Vinogradov, E.V. Kudryashova, A.V. Levashov, and W.M.A.M. van Dongen Solubilization and refolding of inclusion body proteins in reverse micelles Anal Biochem 320 2003 234 238 (Pubitemid 36962847)
29. E.V. Kudryashova, V.L. Bronza, A.A. Vinogradov, A. Kamyshny, S. Magdassi, and A.V. Levashov Regulation of acid phosphatase in reverse micellar system by lipids additives: structural aspects J Coll Int Sci 353 2011 490 497
30. E.V. Kudryashova, A.K. Gladilin, and A.V. Levashov Proteins (enzymes) in supramolecular assembles: investigation of structural organization by time-resolved fluorescence anisotropy Prog. Biol. Chem. (Rus.) 42 2002 257 294
31. M. Sakono, Y.M. Kawashima, H. Ichinose, T. Maruyama, N. Kamiya, and M. Goto Direct refolding of inclusion bodies using reversed micelles Biotechnol Prog 20 2004 1783 1787 (Pubitemid 39606462)
32. F. Baneyx, and M. Mujacic Recombinant protein folding and misfolding in Escherichia coli Nat Biotechnol 22 2004 1399 1408
33. A. Mattevi, M.W. Fraaije, A. Mozzarelli, L. Olivi, A. Coda, and W.J.H. van Berkel Crystal structures and inhibitor binding in the octameric flavoenzyme vanillyl-alcohol oxidase: the shape of the active-site cavity controls substrate specificity Structure 5 1997 907 920 (Pubitemid 27324509)
34. N.G.H. Leferink, M.D.F. Jose, W.A.M. van den Berg, and W.J.H. van Berkel Functional assignment of Glu386 and Arg388 in the active site of L-galactono-γ-lactone dehydrogenase FEBS Lett 583 2009 3199 3203
35. R. Baron, C. Riley, P. Chenprakhon, K. Thotsaporn, R.T. Winter, A. Alfieri, F. Forneris, W.J.H. van Berkel, P. Chaiyen, M.W. Fraaije, A. Mattevi, and J.A. McCammon Multiple pathways guide oxygen diffusion into flavoenzyme active sites Proc Natl Acad Sci U S A 106 2009 10603 10608
36. A. Aliverti, B. Curti, and M.A. Vanoni Identifying and quantitating FAD and FMN in simple and in iron-sulur-containing flavoproteins S.K. Chapman, G.A. Reid, Flavoprotein protocols 1999 Humana Press Totowa 9 23
37. Y.S. Li, J.Y. Ho, C.C. Huang, S.Y. Lyu, C.Y. Lee, Y.T. Huang, C.J. Wu, H.C. Chan, C.J. Huang, N.S. Hsu, M.D. Tsai, and T.L. Li A unique flavin mononucleotide-linked primary alcohol oxidase for glycopeptide A40926 maturation J Am Chem Soc 129 2007 13384 13385
38. F. Forneris, D.P.H.M. Heuts, M. Delvecchio, S. Rovida, M.W. Fraaije, and A. Mattevi Structural analysis of the catalytic mechanism and stereoselectivity in Streptomyces coelicolor alditol oxidase Biochemistry 47 2008 978 985
39. J.D. Thompson, D.G. Higgins, and T.J. Gibson CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res 22 1994 4673 4680 (Pubitemid 24354800)