Structural insights into the N-terminal GIY-YIG endonuclease activity of Arabidopsis glutaredoxin AtGRXS16 in chloroplasts

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

Volumn 110, Issue 23, 2013, Pages 9565-9570

  Liu, Xi ^a   Liu, Shian ^b,e   Feng, Yingang ^c   Liu, Jian Zhong ^d   Chen, Yuling ^a   Pham, Khanh ^b   Deng, Haiteng ^a   Hirschi, Kendal D ^b   Wang, Xinquan ^a   Cheng, Ninghui ^b  

^a TSINGHUA UNIVERSITY   (China)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c QINGDAO INSTITUTE OF BIOENERGY AND BIOPROCESS TECHNOLOGY   (China)

^d ZHEJIANG NORMAL UNIVERSITY   (China)

^e TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Nuclear magnetic resonance; Reactive oxygen species

Indexed keywords

ATGRXS16 PROTEIN; CYSTEINE; ENDONUCLEASE; GENOMIC DNA; GIY YIG ENDONUCLEASE; GLUTAREDOXIN; REACTIVE OXYGEN METABOLITE; SERINE; UNCLASSIFIED DRUG;

AMINO TERMINAL DOMAIN; AMINO TERMINAL SEQUENCE; ANTIFUNGAL SUSCEPTIBILITY; ARABIDOPSIS THALIANA; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHLOROPLAST; CONTROLLED STUDY; DISULFIDE BOND; DNA CLEAVAGE; DNA METABOLISM; ENZYME ACTIVITY; ENZYME STRUCTURE; FUNGAL CELL; GENE EXPRESSION REGULATION; GENE MUTATION; GENE REPRESSION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; REDOX STRESS; REGULATORY DNA SEQUENCE; YEAST;

NUCLEAR MAGNETIC RESONANCE; REACTIVE OXYGEN SPECIES;

AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CHLOROPLASTS; CHROMATOGRAPHY, GEL; DNA; ENDONUCLEASES; GLUTAREDOXINS; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; MUTATION, MISSENSE; OXIDATION-REDUCTION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE PROTEINS; SPECTROPHOTOMETRY, ULTRAVIOLET; YEASTS;

ARABIDOPSIS;

EID: 84878719539     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1306899110     Document Type: Article

References (36)

1. Apel K, Hirt H (2004) Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373-399.
2. Buchanan BB, Balmer Y (2005) Redox regulation: A broadening horizon. Annu Rev Plant Biol 56:187-220.
3. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408(6809):239-247.
4. Niyogi KK (1999) PHOTOPROTECTION REVISITED: Genetic and Molecular Approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333-359.
5. Foyer CH, Noctor G (2011) Ascorbate and glutathione: The heart of the redox hub. Plant Physiol 155(1):2-18.
6. Lillig CH, Berndt C, Holmgren A (2008) Glutaredoxin systems. Biochim Biophys Acta 1780(11):1304-1317.
7. Herrero E, de la Torre-Ruiz MA (2007) Monothiol glutaredoxins: A common domain for multiple functions. Cell Mol Life Sci 64(12):1518-1530.
8. Molina-Navarro MM, Casas C, Piedrafita L, Bellí G, Herrero E (2006) Prokaryotic and eukaryotic monothiol glutaredoxins are able to perform the functions of Grx5 in the biogenesis of Fe/S clusters in yeast mitochondria. FEBS Lett 580(9):2273-2280.
9. Tripathi T, Rahlfs S, Becker K, Bhakuni V (2008) Structural and stability characteristics of a monothiol glutaredoxin: Glutaredoxin-like protein e1 from Plasmodium falciparum. Biochim Biophys Acta 1784(6):946-952.
10. Sundaram S, Rathinasabapathi B, Ma LQ, Rosen BP (2008) An arsenate-activated glutaredoxin from the arsenic hyperaccumulator fern Pteris vittata L. regulates intracellular arsenite. J Biol Chem 283(10):6095-6101.
11. Belfort M, Roberts RJ (1997) Homing endonucleases: Keeping the house in order. Nucleic Acids Res 25(17):3379-3388.
12. Dunin-Horkawicz S, Feder M, Bujnicki JM (2006) Phylogenomic analysis of the GIY- YIG nuclease superfamily. BMC Genomics 7:98.
13. Oppermann T, Hong TH, Surzycki SJ (1989) Chloroplast and nuclear genomes of Chlamydomonas reinhardtii share homology with Escherichia coli genes for DNA replication, repair and transcription. Curr Genet 15(1):39-46.
14. Kwon T, Huq E, Herrin DL (2010) Microhomology-mediated and nonhomologous repair of a double-strand break in the chloroplast genome of Arabidopsis. Proc Natl Acad Sci USA 107(31):13954-13959.
15. Robbins JB, Smith D, Belfort M (2011) Redox-responsive zinc finger fidelity switch in homing endonuclease and intron promiscuity in oxidative stress. Curr Biol 21(3):243-248.
16. Cheng NH, Hirschi KD (2003) Cloning and characterization of CXIP1, a novel PICOT domaincontaining Arabidopsis protein that associates with CAX1. J Biol Chem 278(8):6503-6509.
17. Cheng NH, Liu JZ, Brock A, Nelson RS, Hirschi KD (2006) AtGRXcp, an Arabidopsis chloroplastic glutaredoxin, is critical for protection against protein oxidative damage. J Biol Chem 281(36):26280-26288.
18. Cheng NH (2008) AtGRX4, an Arabidopsis chloroplastic monothiol glutaredoxin, is able to suppress yeast grx5 mutant phenotypes and respond to oxidative stress. FEBS Lett 582(6):848-854.
19. Mak AN, Lambert AR, Stoddard BL (2010) Folding, DNA recognition, and function of GIY-YIG endonucleases: Crystal structures of R.Eco29kI. Structure 18(10):1321-1331.
20. Iwema T, et al. (2009) Structural basis for delivery of the intact [Fe2S2] cluster by monothiol glutaredoxin. Biochemistry 48(26):6041-6043.
21. Li L, Cheng N, Hirschi KD, Wang X (2010) Structure of Arabidopsis chloroplastic monothiol glutaredoxin AtGRXcp. Acta Crystallogr D Biol Crystallogr 66(Pt 6):725-732.
22. Rodríguez-Manzaneque MT, Tamarit J, Bellí G, Ros J, Herrero E (2002) Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes. Mol Biol Cell 13(4):1109-1121.
23. Johansson C, et al. (2011) The crystal structure of human GLRX5: Iron-sulfur cluster coordination, tetrameric assembly and monomer activity. Biochem J 433(2):303-311.
24. Couturier J, et al. (2011) Arabidopsis chloroplastic glutaredoxin C5 as a model to explore molecular determinants for iron-sulfur cluster binding into glutaredoxins. J Biol Chem 286(31):27515-27527.
25. Bandyopadhyay S, et al. (2008) Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters. EMBO J 27(7):1122-1133.
26. Truglio JJ, Croteau DL, Van Houten B, Kisker C (2006) Prokaryotic nucleotide excision repair: The UvrABC system. Chem Rev 106(2):233-252.
27. Bell-Pedersen D, Quirk SM, Bryk M, Belfort M (1991) I-TevI, the endonuclease encoded by the mobile td intron, recognizes binding and cleavage domains on its DNA target. Proc Natl Acad Sci USA 88(17):7719-7723.
28. Van Roey P, Meehan L, Kowalski JC, Belfort M, Derbyshire V (2002) Catalytic domain structure and hypothesis for function of GIY-YIG intron endonuclease I-TevI. Nat Struct Biol 9(11):806-811.
29. Bryk M, et al. (1993) The td intron endonuclease I-TevI makes extensive sequencetolerant contacts across the minor groove of its DNA target. EMBO J 12(10): 4040-4041.
30. Bryk M, Belisle M, Mueller JE, Belfort M (1995) Selection of a remote cleavage site by I-tevI, the td intron-encoded endonuclease. J Mol Biol 247(2):197-210.
31. Berndt C, et al. (2007) How does iron-sulfur cluster coordination regulate the activity of human glutaredoxin 2? Antioxid Redox Signal 9(1):151-157.
32. Johansson C, Kavanagh KL, Gileadi O, Oppermann U (2007) Reversible sequestration of active site cysteines in a 2Fe-2S-bridged dimer provides a mechanism for glutaredoxin 2 regulation in human mitochondria. J Biol Chem 282(5):3077-3082.
33. Li H, et al. (2011) Histidine 103 in Fra2 is an iron-sulfur cluster ligand in the [2Fe-2S] Fra2-Grx3 complex and is required for in vivo iron signaling in yeast. J Biol Chem 286(1):867-876.
34. White MF, Dillingham MS (2012) Iron-sulphur clusters in nucleic acid processing enzymes. Curr Opin Struct Biol 22(1):94-100.
35. Wu Y, Brosh RM, Jr. (2012) DNA helicase and helicase-nuclease enzymes with a conserved iron-sulfur cluster. Nucleic Acids Res 40(10):4247-4260.
36. Kuper J, Kisker C (2012) Damage recognition in nucleotide excision DNA repair. Curr Opin Struct Biol 22(1):88-93.