The conformational bases for the two functionalities of 2-cysteine peroxiredoxins as peroxidase and chaperone

Journal of Experimental Botany

Volumn 64, Issue 11, 2013, Pages 3483-3497

  König, Janine ^a   Galliardt, Helena ^a   Jütte, Patrick ^a   Schäper, Simon ^a   Dittmann, Lea ^a   Dietz, Karl Josef ^a  

^a BIELEFELD UNIVERSITY   (Germany)

Author keywords

Chaperone; chloroplast; conformation; peroxidase; peroxiredoxin; thiol switch.

Indexed keywords

CHAPERONE; PEROXIDASE; PEROXIREDOXIN; VEGETABLE PROTEIN;

ARTICLE; CHEMISTRY; CHLOROPLAST; CONFORMATION; METABOLISM; PHOSPHORYLATION; THIOL SWITCH.;

CHAPERONE; CHLOROPLAST; CONFORMATION; PEROXIDASE; PEROXIREDOXIN; THIOL SWITCH.;

CHLOROPLASTS; MOLECULAR CHAPERONES; PEROXIDASES; PEROXIREDOXINS; PHOSPHORYLATION; PLANT PROTEINS;

EID: 84882343901     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert184     Document Type: Article

References (43)

1. An BC, Lee SS, Lee JT, Hong SH, Wi SG, Chung BY. 2011. Engineering of 2-Cys peroxiredoxin for enhanced stress-tolerance. Molecules and Cells 32, 257-264.
2. Barranco-Medina S, Kakorin S, Lazaro JJ, Dietz KJ. 2008. Thermodynamics of the dimer-decamer transition of reduced human and plant 2-cys peroxiredoxin. Biochemistry 47, 7196-7204.
3. Barranco-Medina S, Lazaro JJ, Dietz KJ. 2009. The oligomeric conformation of peroxiredoxins links redox state to function. FEBS Letters 583, 1809-1816.
4. Bernier-Villamor L, Navarro E, Sevilla F, Lazaro JJ. 2004. Cloning and characterization of a 2-Cys peroxiredoxin from Pisum sativum. Journal of Experimental Botany 55, 2191-2199.
5. Cao ZB, Tavender TJ, Roszak AW, Cogdell RJ, Bulleid NJ. 2011. Crystal structure of reduced and of oxidized peroxiredoxin IV enzyme reveals a stable oxidized decamer and a non-disulfide-bonded intermediate in the catalytic cycle. Journal of Biological Chemistry 286, 42257-42266.
6. Caporaletti D, D'Alessio AC, Rodriguez-Suarez RJ, Senn AM, Duek PD, Wolosiuk RA. 2007. Non-reductive modulation of chloroplast fructose-1,6- bisphosphatase by 2-Cys peroxiredoxin. Biochemical and Biophysical Research Communications 355, 722-727.
7. Cejudo FJ, Ferrandez J, Cano B, Puerto-Galan L, Guinea M. 2012. The function of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system in plastid redox regulation and signalling. FEBS Letters 586, 2974-2980.
8. Chae HZ, Oubrahim H, Park JW, Rhee SG, Chock PB. 2012. Protein glutathionylation in the regulation of peroxiredoxins: a family of thiol-specific peroxidases that function as antioxidants, molecular chaperones, and signal modulators. Antioxidants & Redox Signaling 16, 506-523.
9. Chen MF, Lee KD, Yeh CH, Chen WC, Huang WS, Chin CC, Lin PY, Wang JY. 2010. Role of peroxiredoxin I in rectal cancer and related to p53 status. International Journal of Radiation Oncology, Biology, Physics 78, 868-878.
10. Chen X, Zhang W, Zhang B, Zhou J, Wang Y, Yang Q, Ke Y, He H. 2011. Phosphoproteins regulated by heat stress in rice leaves. Proteome Science 9, 37.
11. Dietz KJ. 2008. Redox signal integration: from stimulus to networks and genes. Physiologia Plantarum 133, 459-468.
12. Dietz KJ. 2011. Peroxiredoxins in plants and cyanobacteria. Antioxidants & Redox Signaling 15, 1129-1159.
13. Edgar RS, Green EW, Zhao YW, et al. 2012. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485, 459-465.
14. Gerard C, Goldbeter A. 2012. Entrainment of the mammalian cell cycle by the circadian clock: modeling two coupled cellular rhythms. PLoS Computational Biology 8, e1002516
15. Gutscher M, Sobotta MC, Wabnitz GH, Ballikaya S, Meyer AJ, Samstag Y, Dick TP. 2009. Proximity-based protein thiol oxidation by H2O2-scavenging peroxidases. Journal of Biological Chemistry 284, 31532-31540.
16. Iglesias-Baena I, Barranco-Medina S, Lazaro-Payo A, Lopez-Jaramillo FJ, Sevilla F, Lazaro JJ. 2010. Characterization of plant sulfiredoxin and role of sulphinic form of 2-Cys peroxiredoxin. Journal of Experimental Botany 61, 1509-1521.
17. Jang HH, Kim SY, Park SK, et al. 2006. Phosphorylation and concomitant structural changes in human 2-Cys peroxiredoxin isotype I differentially regulate its peroxidase and molecular chaperone functions. FEBS Letters 580, 351-355.
18. Jang HH, Lee KO, Chi YH, et al. 2004. Two enzymes in one: two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117, 625-635.
19. Kim JH, Bogner PN, Baek SH, Ramnath N, Liang P, Kim HR, Andrews C, Park YM. 2008. Up-regulation of peroxiredoxin 1 in lung cancer and its implication as a prognostic and therapeutic target. Clinical Cancer Research 14, 2326-2333.
20. Kim MD, Kim YH, Kwon SY, Jang BY, Lee SY, Yun DJ, Cho JH, Kwak SS, Lee HS. 2011. Overexpression of 2-cysteine peroxiredoxin enhances tolerance to methyl viologen-mediated oxidative stress and high temperature in potato plants. Plant Physiology and Biochemistry 49, 891-897.
21. Kim SY, Jang HH, Lee JR, et al. 2009. Oligomerization and chaperone activity of a plant 2-Cys peroxiredoxin in response to oxidative stress. Plant Science 177, 227-232.
22. Kirchsteiger K, Pulido P, Gonzalez M, Cejudo FJ. 2009. NADPH thioredoxin reductase C controls the redox status of chloroplast 2-Cys peroxiredoxins in Arabidopsis thaliana. Molecular Plant 2, 298-307.
23. König J, Baier M, Horling F, Kahmann U, Harris G, Schurmann P, Dietz KJ. 2002. The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redoxhierarchy of photosynthetic electron flux. Proceedings of the National Academy of Sciences, USA 99, 5738-5743.
24. König J, Fairlamb AH. 2007. A comparative study of type I and type II tryparedoxin peroxidases in Leishmania major. FEBS Journal 274, 5643-5658.
25. König J, Lotte K, Plessow R, Brockhinke A, Baier M, Dietz KJ. 2003. Reaction mechanism of plant 2-Cys peroxiredoxin. Role of the C terminus and the quaternary structure. Journal of Biological Chemistry 278, 24409-24420.
26. König J, Muthuramalingam M, Dietz KJ. 2012. Mechanisms and dynamics in the thiol/disulfide redox regulatory network: transmitters, sensors and targets. Current Opinion in Plant Biology 15, 261-268.
27. Koo KH, Lee S, Jeong SY, Kim ET, Kim HJ, Kim K, Song K, Chae HZ. 2002. Regulation of thioredoxin peroxidase activity by C-terminal truncation. Archives of Biochemistry and Biophysics 397, 312-318.
28. Laxa M, König J, Dietz KJ, Kandlbinder A. 2007. Role of the cysteine residues in Arabidopsis thaliana cyclophilin CYP20-3 in peptidyl-prolyl cis-trans isomerase and redox-related functions. Biochemical Journal 401, 287-297.
29. Matsumura T, Okamoto K, Iwahara S, Hori H, Takahashi Y, Nishino T, Abe Y. 2008. Dimer-oligomer interconversion of wild-type and mutant rat 2-Cys peroxiredoxin: disulfide formation at dimer-dimer interfaces is not essential for decamerization. Journal of Biological Chemistry 283, 284-293.
30. Muthuramalingam M, Seidel T, Laxa M, Nunes de Miranda SM, Gartner F, Stroher E, Kandlbinder A, Dietz KJ. 2009. Multiple redox and non-redox interactions define 2-Cys peroxiredoxin as a regulatory hub in the chloroplast. Molecular Plant 2, 1273-1288.
31. Neumann CA, Krause DS, Carman CV, et al. 2003. Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 424, 561-565.
32. Nogoceke E, Gommel DU, Kiess M, Kalisz HM, Flohe L. 1997. A unique cascade of oxidoreductases catalyses trypanothione-mediated peroxide metabolism in Crithidia fasciculata. Biological Chemistry 378, 827-836.
33. O'Neill JS, van Ooijen G, Dixon LE, Troein C, Corellou F, Bouget FY, Reddy AB, Millar AJ. 2011. Circadian rhythms persist without transcription in a eukaryote. Nature 469, 554-558.
34. Peltier JB, Cai Y, Sun Q, Zabrouskov V, Giacomelli L, Rudella A, Ytterberg AJ, Rutschow H, van Wijk KJ. 2006. The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Molecular & Cellular Proteomics 5, 114-133.
35. Perez-Ruiz JM, Spinola MC, Kirchsteiger K, Moreno J, Sahrawy M, Cejudo FJ. 2006. Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage. Plant Cell 18, 2356-2368.
36. Pulido P, Spinola MC, Kirchsteiger K, Guinea M, Pascual MB, Sahrawy M, Sandalio LM, Dietz KJ, Gonzalez M, Cejudo FJ. 2010. Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts. Journal of Experimental Botany 61, 4043-4054.
37. Rhee SG, Woo HA, Kil IS, Bae SH. 2012. Peroxiredoxin functions as a peroxidase and a regulator and sensor of local peroxides. Journal of Biological Chemistry 287, 4403-4410.
38. Seo JH, Lim JC, Lee DY, et al. 2009. Novel protective mechanism against irreversible hyperoxidation of peroxiredoxin: N-terminal acetylation of human peroxiredoxin II. Journal of Biological Chemistry 284, 13455-13465.
39. Shichita T, Hasegawa E, Kimura A, et al. 2012. Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain. Nature Medicine 18, 911-917.
40. Tetsch L, Koller C, Dönhöfer A, Jung K. (2011) Detection and function of an intramolecular disulfide bond in the pH-responsive CadC of Escherichia coli. BMC Microbiology 11, 74.
41. Wang Y, Gibney PA, West JD, Morano KA. 2012. The yeast Hsp70 Ssa1 is a sensor for activation of the heat shock response by thiol-reactive compounds. Molecular Biology of the Cell 23, 3290-3298.
42. Wood ZA, Schroder E, Harris JR, Poole LB. 2003. Structure, mechanism and regulation of peroxiredoxins. Trends in Biochemical Sciences 28, 32-40.
43. Yoshida Y, Yoshikawa A, Kinumi T, Ogawa Y, Saito Y, Ohara K, Yamamoto H, Imai Y, Niki E. 2009. Hydroxyoctadecadienoic acid and oxidatively modified peroxiredoxins in the blood of Alzheimer's disease patients and their potential as biomarkers. Neurobiology of Aging 30, 174-185.