Evidence of non-functional redundancy between two pea h-type thioredoxins by specificity and stability studies

Journal of Plant Physiology

Volumn 167, Issue 6, 2010, Pages 423-429

  Traverso, José A ^a   López Jaramillo, Francisco J ^b   Serrato, Antonio J ^a   Ortega Muñoz, Mariano ^b   Aguado Llera, David ^c   Sahrawy, Mariam ^a   Santoyo Gonzalez, Francisco ^b   Neira, José L ^c,d   Chueca, Ana ^a  

^a CSIC   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

^c MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^d UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

Protein stability; Protein structure; Protein target; Proteomics; Thioredoxin

Indexed keywords

THIOREDOXIN; VEGETABLE PROTEIN;

AFFINITY CHROMATOGRAPHY; ARTICLE; CIRCULAR DICHROISM; GENETICS; METABOLISM; METHODOLOGY; PEA; PROTEOMICS;

CHROMATOGRAPHY, AFFINITY; CIRCULAR DICHROISM; PEAS; PLANT PROTEINS; PROTEOMICS; THIOREDOXINS;

PISUM SATIVUM;

EID: 77649183734     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2009.10.017     Document Type: Article

References (44)

1. Balmer Y., Vensel W.H., Cai N., Manieri W., Schürmann P., Hurkman W.J., et al. A complete ferredoxin/thioredoxin system regulates fundamental processes in amyloplasts. Proc Natl Acad Sci USA 103 (2006) 2988-2993
2. Barranco-Medina S., Krell T., Bernier-Villamor L., Sevilla F., Lazaro J.J., and Dietz KJ. Hexameric oligomerization of mitochondrial peroxiredoxin PrxIIF and formation of an ultrahigh affinity complex with its electron donor thioredoxin Trx-o. J Exp Bot 59 (2008) 3259-3269
3. Barranco-Medina S., Krell T., Finkemeier I., Sevilla F., Lazaro J.J., and Dietz KJ. Biochemical and molecular characterization of the mitochondrial peroxiredoxin PsPrxII F from Pisum sativum. Plant Physiol Biochem 45 (2007) 729-739
4. Bernier-Villamor L., Navarro E., Sevilla F., and Lazaro JJ. Cloning and characterization of a 2-Cys peroxiredoxin from Pisum sativum. J Exp Bot 55 (2004) 2191-2199
5. Besse I., Wong J.H., Kobrehel K., and Buchanan BB. Thiocalsin: a thioredoxinlinked, substrate-specific protease dependent on calcium. Proc Natl Acad Sci USA 93 (1996) 3169-3175
6. Buchanan B.B., and Balmer Y. Redox regulation: a broadening horizon. Annu Rev Plant Biol 56 (2005) 187-220
7. Buchanan B.B. Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol 31 (1980) 341-374
8. Bueno M., Cremades N., Neira J.L., and Sancho J. Filling small, empty protein cavities: structural and energetic consequences. J Mol Biol 358 (2006) 701-712
9. Clarke J., and Fersht AR. Engineered disulfide bonds as probes of the folding pathway of barnase: increasing the stability of proteins against the rate of denaturation. Biochemistry 32 (1993) 4322-4329
10. Collin V., Issakidis-Bourguet E., Marchand C., Hirasawa M., Lancelin J.M., Knaff D.B., et al. The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. J Biol Chem 278 (2003) 23747-23752
11. Collin V., Lamkemeyer P., Miginiac-Maslow M., Hirasawa M., Knaff D.B., Dietz K.J., et al. Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type. Plant Physiol 136 (2004) 4088-4095
12. Eklund H., Gleason F.K., and Holmgren A. Structural and functional relations among thioredoxins of different species. Proteins: Struct Funct Genet 11 (1991) 13-28
13. Florencio F.J., Yee B.C., Johnson T.C., and Buchanan BB. An NADP/thioredoxin system in leaves: purification and characterization of NADP-thioredoxin reductase and thioredoxin h from spinach. Arch Biochem Biophys 266 (1988) 496-507
14. Gelhaye E., Rouhier N., Gerard J., Jolivet Y., Gualberto J., Navrot N., et al. A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc Natl Acad Sci USA 101 (2004) 14545-14550
15. Georgescu R.E., Braswell E.H., Zhu D., and Tasayco ML. Energetics of assembling an artificial heterodimer with an alpha/beta motif: cleaved versus uncleaved Escherichia coli thioredoxin. Biochemistry 38 (1999) 13355-13366
16. Gill S.C., and von Hippel P.H. Calculation of extinction coefficients from amino acid sequence data. Anal Biochem 182 (1989) 319-326
17. Holmgren A. Thioredoxin and glutaredoxin systems. J Biol Chem 264 (1989) 13963-13966
18. Issakidis-Bourguet E., Mouaheb N., Meyer Y., and Miginiac-Maslow M. Heterologous complementation of yeast reveals a new putative function for chloroplast m-type thioredoxin. Plant J 25 (2001) 127-135
19. Itzhaki L.S., Neira J.L., and Fersht AR. Hydrogen exchange in chymotrypsin inhibitor 2 probed by denaturants and temperature. J Mol Biol 270 (1997) 89-98
20. Jackson S.E., and Fersht AR. Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition. Biochemistry 30 (1991) 10428-10435
21. Kelley R.F., and Stellwagen E. Conformational transitions of thioredoxin in guanidine hydrochloride. Biochemistry 23 (1984) 5095-5102
22. Kobrehel K., Wong J.H., Balogh A., Kiss F., Yee B.C., and Buchanan BB. Specific reduction of wheat storage proteins by thioredoxin h. Plant Physiol 99 (1992) 919-924
23. Laloi C., Rayapuram N., Chartier Y., Grienenberger J.M., Bonnard G., and Meyer Y. Identification and characterization of a mitochondrial thioredoxin system in plants. Proc Natl Acad Sci USA 98 (2001) 14144-14149
24. López-Jaramillo J., Chueca A., Jacquot J.P., Hermoso R., Lázaro J.J., Sahrawy M., et al. High-yield expression of pea thioredoxin m and assessment of its efficiency in chloroplast fructose-1,6-bisphosphatase activation. Plant Physiol 114 (1997) 1169-1175
25. Maeda K., Finnie C., and Svensson B. Cy5 maleimide labelling for sensitive detection of free thiols in native protein extracts: identification of seed proteins targeted by barley thioredoxin h isoforms. Biochem J 378 (2004) 497-507
26. Meyer Y., Reichheld J., and Vignols F. Thioredoxins in Arabidopsis and other plants. Photosynth Res 86 (2005) 419-433
27. Meyer Y., Riondet C., Constans L., Ragab-Abdelgawwad M., Reichheld J.P., and Vignols F. Evolution of redoxin genes in the green lineage. Photosynth Res 89 (2006) 179-192
28. Meyer Y., Vignols F., and Reichheld JP. Classification of plant thioredoxins by sequence similarity and intron position. Methods Enzymol 347 (2002) 394-402
29. Montrichard F., Renard M., Alkhalfioui F., Duval F.D., and Macherel D. Identification and differential expression of two thioredoxin h isoforms in germinating seeds from pea. Plant Physiol 132 (2003) 1707-1715
30. Mouhaeb N., Thomas D., Verdoucq L., Monfort P., and Meyer Y. In vivo functional discrimation between plant thioredoxins by heterologous expression in the yeast Saccharomyces cerevisae. Proc Natl Acad Sci USA 95 (1998) 3312-3317
31. Neira J.L., González C., Toiron C., Prat-Gay G., and Rico M. Three-dimensional solution structure and stability of thioredoxin m from spinach. Biochemistry 40 (2001) 15246-15256
32. Pagano E.A., Chueca A., and López-Gorgé J. Expression of thioredoxins f and m, and of their targets fructose-1,6-bisphosphatase and NADP-malate dehydrogenase, in pea plants grown under normal and light/temperature stress conditions. J Exp Bot 51 (2000) 1299-1307
33. Pedone E., Bartolucci S., Rossi M., and Saviano M. Computational analysis of the thermal stability in thioredoxins: a molecular dynamics approach. J Biomol Struct Dynam 2 (1998) 437-446
34. Pedroso I., Irún M.P., Machicado C., and Sancho J. Four-state equilibrium unfolding of an scFv antibody fragment. Biochemistry 41 (2002) 9873-9884
35. Perkins D.N., Pappin D.J.C., Creasy D.M., and Cottrell JS. Probability-based protein identification by searching sequence database using mass spectrometry data. Electroforesis 20 (1999) 3551-3567
36. Reichheld J.P., Khafif M., Riondet C., Droux M., Bonnard G., and Meyer Y. Inactivation of thioredoxin reductases reveals a complex interplay between thioredoxin and glutathione pathways in Arabidopsis development. Plant Cell 19 (2007) 1851-1865
37. Royer CA. Fluorescence spectroscopy. In: Shirley B.A. (Ed). Protein stability and folding (1995), Humana Press, Totowa, New Jersey
38. Santoyo-Gonzalez F, Hernández-Mateo F, López-Jaramillo J, Ortega-Muñoz M, Morales-Sanfrutos J. Patent number: P200702542; 2007.
39. Serrato A.J., and Cejudo FJ. Type-h thioredoxins accumulate in the nucleus of developing wheat seed tissues suffering oxidative stress. Planta 217 (2003) 392-399
40. Sweat T.A., and Wolpert T.J. Thioredoxin h5 is required for victorin sensitivity mediated by a CC-NBS-LRR gene in Arabidopsis. Plant Cell 19 (2007) 673-687
41. Traverso J.A., Vignols F., Cazalis R., Pulido A., Sahrawy M., and Cejudo F.J. PsTRXh1 and PsTRXh2 are both pea (Pisum sativum) h-type thioredoxins with antagonistic behaviour in redox imbalances. Plant Physiol 143 (2007) 300-331
42. Traverso J.A., Vignols F., and Chueca A. Thioredoxin and redox control within the new concept of oxidative signaling. Plant Signal Behav 2 (2007) 425-426
43. Traverso J.A., Vignols F., Cazalis R., Serrato A.J., Pulido P., and Sahrawy M. Immunocytochemical localization of Pisum sativum TRXs f and m in non-photosynthetic tissues. J Exp Bot 59 (2008) 1267-1277
44. Wangensteen O.S., Chueca A., Hirasawa M., Sahrawy M., Knaff D.B., and López-Gorgé J. Binding features of chloroplast fructose-1,6-bisphosphatase-thioredoxin interaction. Biochim Biophys Acta 1547 (2001) 156-166