The activity of barley NADPH-dependent thioredoxin reductase C is independent of the oligomeric state of the protein: Tetrameric structure determined by cryo-electron microscopy

Biochemistry

Volumn 50, Issue 18, 2011, Pages 3713-3723

  Wulff, Ragna Peterson ^a,b   Lundqvist, Joakim ^a   Rutsdottir, Gudrun ^a   Hansson, Andreas ^c   Stenbaek, Anne ^c   Elmlund, Dominika ^d,e   Elmlund, Hans ^e   Jensen, Poul Erik ^c   Hansson, Mats ^a  

^a CARLSBERG LABORATORY   (Denmark)

^b LUND UNIVERSITY   (Sweden)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHETIC PATHWAY; CATALYTIC ABILITY; CELL METABOLISM; COFACTORS; CRYO-ELECTRON MICROSCOPY; CYCLASES; DISULFIDE BRIDGE; ENZYMATIC FUNCTIONS; ENZYME ASSAYS; ENZYME SYSTEMS; HOMODIMERS; HORDEUM VULGARE; N-TERMINALS; OLIGOMERIC STATE; PROTOPORPHYRIN IX; QUATERNARY STRUCTURE; REDOX REGULATION; REDOX STATUS; SINGLE-PARTICLE; STRUCTURAL MODELS; TETRAMERIC STRUCTURES; THIOREDOXIN REDUCTASE; THIOREDOXINS;

ASSAYS; CHLOROPHYLL; COVALENT BONDS; ELECTRON MICROSCOPES; ENZYMES; ESTERS; METABOLISM; MODEL STRUCTURES;

OLIGOMERS;

RECOMBINANT ENZYME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; THIOREDOXIN REDUCTASE; THIOREDOXIN REDUCTASE C; UNCLASSIFIED DRUG;

ARTICLE; BARLEY; CRYOELECTRON MICROSCOPY; ENZYME PURIFICATION; ENZYME STRUCTURE; GENE SEQUENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; STRUCTURE ANALYSIS;

CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HORDEUM; MAGNESIUM; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; NADP; OXIDATION-REDUCTION; PEROXIDES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; THIOREDOXIN-DISULFIDE REDUCTASE; THIOREDOXINS;

HORDEUM; HORDEUM VULGARE SUBSP. VULGARE;

EID: 79955589109     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200058a     Document Type: Article

References (32)

1. Gelhaye, E., Rouhier, N., Navrot, N., and Jacquot, J. P. (2005) The plant thioredoxin system Cell. Mol. Life Sci. 62, 24-35 (Pubitemid 40933089)
2. Schürmann, P. and Buchanan, B. B. (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis Antioxid. Redox Signaling 10, 1235-1273 (Pubitemid 351620306)
3. Holmgren, A. and Arnér, E. S. J. (2000) Physiological functions of thioredoxin and thioredoxin reductase Eur. J. Biochem. 267, 6102-6109
4. Balmer, Y., Koller, A., del Val, G., Manieri, W., Schürmann, P., and Buchanan, B. B. (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins Proc. Natl. Acad. Sci. U.S.A. 100, 370-375 (Pubitemid 36078081)
5. Sturm, N., Jortzik, E., Mailu, B. M., Koncarevic, S., Deponte, M., Forchhammer, K., Rahlfs, S., and Becker, K. (2009) Identification of proteins targeted by the thioredoxin superfamily in Plasmodium falciparum PLoS Pathog. 5 e1000383
6. Ikegami, A., Yoshimura, N., Motohashi, K., Takahashi, S., Romano, P. G. N., Hisabori, T., Takamiya, K.-i., and Masuda, T. (2007) The CHLI1 subunit of Arabidopsis thaliana magnesium chelatase is a target protein of the chloroplast thioredoxin J. Biol. Chem. 282, 19282-19291 (Pubitemid 47100075)
7. Kobayashi, K., Mochizuki, N., Yoshimura, N., Motohashi, K., Hisaboric, T., and Masuda, T. (2008) Functional analysis of Arabidopsis thaliana isoforms of the Mg-chelatase CHLI subunit Photochem. Photobiol. Sci. 7, 1188-1195
8. Serrato, A. J., Perez-Ruiz, J. M., Spinola, M. C., and Cejudo, F. J. (2004) A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana J. Biol. Chem. 279, 43821-43827 (Pubitemid 39390688)
9. Pérez-Ruiz, J. M., Gonzáleza, M., Spínola, M. C., Sandalioc, L. M., and Francisco, J. C. (2009) The quaternary structure of NADPH thioredoxin reductase C is redox-sensitive Mol. Plant 1-11
10. Alkhalfioui, F., Renard, M., and Montrichard, F. (2007) Unique properties of NADP-thioredoxin reductase C in legumes J. Exp. Bot. 58, 969-978 (Pubitemid 46623306)
11. Moon, J. C., Jang, H. H., Chae, H. B., Lee, J. R., Lee, S. Y., Jung, Y. J., Shin, M. R., Lim, H. S., Chung, W. S., Yun, D. J., Lee, K. O., and Lee, S. Y. (2006) The C-type Arabidopsis thioredoxin reductase ANTR-C acts as an electron donor to 2-Cys peroxiredoxins in chloroplasts Biochem. Biophys. Res. Commun. 348, 478-484 (Pubitemid 44188594)
12. Perez-Ruiz, J. M., Spinola, M. C., Kirchsteiger, K., Moreno, J., Sahrawy, M., and Cejudo, F. J. (2006) Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage Plant Cell 18, 2356-2368 (Pubitemid 44484731)
13. Pulido, P., Spinola, M. C., Kirchsteiger, K., Guinea, M., Pascual, M. B., Sahrawy, M., Sandalio, L. M., Dietz, K. J., Gonzalez, M., and Cejudo, F. J. (2010) Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts J. Exp. Bot. 61, 4043-4054
14. Dietz, K.-J., Jacob, S., Oelze, M.-L., Laxa, M., Tognetti, V., de Miranda, S. M. N., Baier, M., and Finkemeier, I. (2006) The function of peroxiredoxins in plant organelle redox metabolism J. Exp. Bot. 57, 1697-1709 (Pubitemid 43992219)
15. Mittler, R., Vanderauwera, S., Gollery, M., and Van Breusegem, F. (2004) Reactive oxygen gene network of plants Trends Plant Sci. 9, 490-498 (Pubitemid 39301187)
16. Baier, M. and Dietz, K.-J. (1997) The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: Its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants Plant J. 12, 179-190 (Pubitemid 27312774)
17. Dietz, K.-J. (2003) Plant peroxiredoxins Annu. Rev. Plant Biol. 54, 93-109
18. Hall, A., Karplus, P. A., and Poole Leslie, B. (2009) Typical 2-Cys peroxiredoxins: Structures, mechanisms and functions FEBS J. 276, 2469-2477
19. 2 is not reflected in its reaction with other oxidants and thiol reagents J. Biol. Chem. 282, 11885-11892 (Pubitemid 47100684)
20. Stenbaek, A., Hansson, A., Wulff, R. P., Hansson, M., Dietz, K.-J., and Jensen, P. E. (2008) NADPH-dependent thioredoxin reductase and 2-Cys peroxiredoxins are needed for the protection of Mg-protoporphyrin monomethyl ester cyclase FEBS Lett. 582, 2773-2778
21. Gough, S. P., Rzeznicka, K., Peterson Wulff, R., Francisco, J. d. C., Hansson, A., Jensen, P. E., and Hansson, M. (2007) A new method for isolating physiologically active Mg-protoporphyrin monomethyl ester, the substrate of the cyclase enzyme of the chlorophyll biosynthetic pathway Plant Physiol. Biochem. 45, 932-936 (Pubitemid 350138439)
22. Holmgren, A. and Björnstedt, M. (1995) Thioredoxin and thioredoxin reductase Methods Enzymol. 252, 199-208
23. Ludtke, S. J., Baldwin, P. R., and Chiu, W. (1999) EMAN: Semiautomated software for high-resolution single-particle reconstructions J. Struct. Biol. 128, 82-97 (Pubitemid 30013436)
24. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M., and Leith, A. (1996) SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116, 190-199 (Pubitemid 26093143)
25. Elmlund, D., Davis, R., and Elmlund, H. (2010) Ab initio structure determination from electron microscopic images of single molecules coexisting in different functional states Structure 18, 777-786
26. Elmlund, D. and Elmlund, H. (2009) High-resolution single-particle orientation refinement based on spectrally self-adapting common lines J. Struct. Biol. 167, 83-94
27. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence J. Mol. Biol. 300, 1005-1016
28. Warburg, O. and Christian, W. (1938) Bemerkung über gelbe Fermente Biochem. Z. 298, 368-377
29. Elmlund, H., Lundqvist, J., Al-Karadaghi, S., Hansson, M., Hebert, H., and Lindahl, M. (2008) A new cryo-EM single-particle ab initio reconstruction method visualizes secondary structure elements in an ATP-fueled AAA+ motor J. Mol. Biol. 375, 934-947 (Pubitemid 50010798)
30. Stenbaek, A. and Jensen, P. E. (2010) Redox regulation of chlorophyll biosynthesis Phytochemistry 71, 853-859
31. Lepistö, A., Kangasjärvi, S., Luomala, E.-M., Brader, G., Sipari, N., Keränen, M., Keinänen, M., and Rintamäki, E. (2009) Chloroplast NADPH-thioredoxin reductase interacts with photoperiodic development in Arabidopsis Plant Physiol. 149, 1261-1276
32. Michalska, J., Zauber, H., Buchanan, B. B., Cejudo, F. J., and Geigenberger, P. (2009) NTRC links built-in thioredoxin to light and sucrose in regulating starch synthesis in chloroplasts and amyloplasts Proc. Natl. Acad. Sci. U.S.A. 106, 9908-9913