Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-15T17:12:33.726Z Has data issue: false hasContentIssue false
  • English
  • Français

Expression, characterization and crystal structure of thioredoxin from Schistosoma japonicum

Published online by Cambridge University Press:  26 March 2015

YONGDONG LI ,
PAN LI ,
YUN PENG ,
QUNFENG WU ,
FUYAN HUANG ,
XIANG LIU ,
XUN LI ,
HUI ZHOU ,
DAOYI GUO  and
DASHUANG SHI
...Show all authors
YONGDONG LI
Affiliation:
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai 200025, People's Republic of China Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China Key Laboratory on Biology of Parasite and Vector, Ministry of Health, and WHO Collaborating Center for Malaria, Schistosomiasis and Filariasis, Shanghai 200025, People's Republic of China
PAN LI
Affiliation:
Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China
YUN PENG
Affiliation:
Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China
QUNFENG WU
Affiliation:
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai 200025, People's Republic of China Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China Key Laboratory on Biology of Parasite and Vector, Ministry of Health, and WHO Collaborating Center for Malaria, Schistosomiasis and Filariasis, Shanghai 200025, People's Republic of China
FUYAN HUANG
Affiliation:
Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China
XIANG LIU
Affiliation:
Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China
XUN LI
Affiliation:
Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China
HUI ZHOU
Affiliation:
Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China
DAOYI GUO
Affiliation:
Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China
DASHUANG SHI
Affiliation:
Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China Center for Genetic Medicine Research and Department of Integrative Systems Biology, Children's National Medical Center, The George Washington University, Washington, District of Columbia 20010, USA
XIAO-NONG ZHOU*
Affiliation:
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai 200025, People's Republic of China Key Laboratory on Biology of Parasite and Vector, Ministry of Health, and WHO Collaborating Center for Malaria, Schistosomiasis and Filariasis, Shanghai 200025, People's Republic of China
XIAOLIN FAN*
Affiliation:
Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China
*
* Corresponding authors. Key Laboratory on Biology of Parasite and Vector, Ministry of Health, and WHO Collaborating Center for Malaria, Schistosomiasis and Filariasis, Shanghai 200025, People's Republic of China, Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China. E-mail: [email protected] and [email protected]
* Corresponding authors. Key Laboratory on Biology of Parasite and Vector, Ministry of Health, and WHO Collaborating Center for Malaria, Schistosomiasis and Filariasis, Shanghai 200025, People's Republic of China, Key Laboratory of Organo-Pharmaceutical Chemistry, Jiangxi Province, Chemistry and Chemical Engineering College, Gannan Normal University, Ganzhou 341000, People's Republic of China. E-mail: [email protected] and [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Schistosoma japonicum, a human blood fluke, causes a parasitic disease affecting millions of people in Asia. Thioredoxin–glutathione system of S. japonicum plays a critical role in maintaining the redox balance in parasite, which is a potential target for development of novel antischistosomal agents. Here we cloned the gene of S. japonicum thioredoxin (SjTrx), expressed and purified the recombinant SjTrx in Escherichia coli. Functional assay shows that SjTrx catalyses the dithiothreitol (DTT) reduction of insulin disulphide bonds. The coupling assay of SjTrx with its endogenous reductase, thioredoxin glutathione reductase from S. japonicum (SjTGR), supports its biological function to maintain the redox homeostasis in the cell. Furthermore, the crystal structure of SjTrx in the oxidized state was determined at 2·0 Å resolution, revealing a typical architecture of thioredoxin fold. The structural information of SjTrx provides us important clues for understanding the maintenance function of redox homeostasis in S. japonicum and pathogenesis of this chronic disease.

Keywords

thioredoxincrystal structureSchistosoma japonicum
Type
Research Article
Information
Parasitology , Volume 142 , Issue 8 , July 2015 , pp. 1044 - 1052
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mccoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C. and Zwart, P. H. (2010). PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica, Section D (Biological Crystallography) 66, 213–221.Google Scholar
Alger, H. M. and Williams, D. L. (2002). The disulfide redox system of Schistosoma mansoni and the importance of a multifunctional enzyme, thioredoxin glutathione reductase. Molecular and Biochemical Parasitology 121, 129–139.Google Scholar
Alger, H. M., Sayed, A. A., Stadecker, M. J. and Williams, D. L. (2002). Molecular and enzymatic characterisation of Schistosoma mansoni thioredoxin. International Journal of Parasitology 32, 1285–1292.CrossRefGoogle ScholarPubMed
Andersen, K. M., Madsen, L., Prag, S., Johnsen, A. H., Semple, C. A., Hendil, K. B. and Hartmann-Petersen, R. (2009). Thioredoxin Txnl1/TRP32 is a redox-active cofactor of the 26 S proteasome. Journal of Biological Chemistry 284, 15246–15254.Google Scholar
Angelucci, F., Dimastrogiovanni, D., Boumis, G., Brunori, M., Miele, A. E., Saccoccia, F. and Bellelli, A. (2010). Mapping the catalytic cycle of Schistosoma mansoni thioredoxin glutathione reductase by X-ray crystallography. Journal of Biological Chemistry 285, 32557–32567.Google Scholar
Arner, E. S. and Holmgren, A. (2000). Physiological functions of thioredoxin and thioredoxin reductase. European Journal of Biochemistry 267, 6102–6109.Google Scholar
Boumis, G., Angelucci, F., Bellelli, A., Brunori, M., Dimastrogiovanni, D. and Miele, A. E. (2011). Structural and functional characterization of Schistosoma mansoni Thioredoxin. Protein Science 20, 1069–1076.Google Scholar
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.Google Scholar
Butterworth, A. E. (1984). Cell-mediated damage to helminths. Advance in Parasitology 23, 143–235.Google Scholar
Capron, M. and Capron, A. (1986). Rats, mice and men – models for immune effector mechanisms against schistosomiasis. Parasitology Today 2, 69–75.Google Scholar
Cheng, Z., Zhang, J., Ballou, D. P. and Willams, C. H. Jr (2011). On the reactivity of thioredoxin as a protein thiol-disulfide oxidoreductase. Chemical Reviews 111(9), 5768–5783.Google Scholar
Emsley, P. and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallographica, Section D (Biological Crystallography) 60, 2126–2132.Google Scholar
Han, Y., Zhang, M., Hong, Y., Zhu, Z., Li, D., Li, X., Fu, Z. and Lin, J. (2012). Characterization of thioredoxin glutathione reductase in Schistosoma japonicum . Parasitology International 61, 475–480.Google Scholar
Hatahet, F. and Ruddock, L. W. (2009). Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxidants and Redox Signaling 11, 2807–2850.CrossRefGoogle ScholarPubMed
Hayashi, T., Ueno, Y. and Okamoto, T. (1993). Oxidoreductive regulation of nuclear factor kappa B. Involvement of a cellular reducing catalyst thioredoxin. Journal of Biological Chemistry 268, 11380–11388.Google Scholar
Holmgren, A. (1979). Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. Journal of Biological Chemistry 254, 9627–9632.Google Scholar
Holmgren, A. (1984). Enzymatic reduction–oxidation of protein disulfides by thioredoxin. Methods in Enzymology 107, 295–300.Google Scholar
Hu, W., Yan, Q., Shen, D. K., Liu, F., Zhu, Z. D., Song, H. D., Xu, X. R., Wang, Z. J., Rong, Y. P., Zeng, L. C., Wu, J., Zhang, X., Wang, J. J., Xu, X. N., Wang, S. Y., Fu, G., Zhang, X. L., Wang, Z. Q., Brindley, P. J., Mcmanus, D. P., Xue, C. L., Feng, Z., Chen, Z. and Han, Z. G. (2003). Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nature Genetics 35, 139–147.Google Scholar
Ishrat, T., Mohamed, I. N., Pillai, B., Soliman, S., Fouda, A. Y., Ergul, A., El-Remessy, A. B. and Fagan, S. C. (2014). Thioredoxin-interacting protein: a novel target for neuroprotection in experimental thromboembolic stroke in mice. Molecular Neurobiology. Epub ahead of print, doi:10.1007/s12035-014-8766-x.Google Scholar
Jensen, K. S., Hansen, R. E. and Winther, J. R. (2009). Kinetic and thermodynamic aspects of cellular thiol-disulfide redox regulation. Antioxidants and Redox Signaling 11, 1047–1058.Google Scholar
Jonsson, T. J., Johnson, L. C. and Lowther, W. T. (2008). Structure of the sulphiredoxin-peroxiredoxin complex reveals an essential repair embrace. Nature 451, 98–101.Google Scholar
Kaimul Ahsan, M., Nakamura, H., Tanito, M., Yamada, K., Utsumi, H. and Yodoi, J. (2005). Thioredoxin-1 suppresses lung injury and apoptosis induced by diesel exhaust particles (DEP) by scavenging reactive oxygen species and by inhibiting DEP-induced downregulation of Akt. Free Radical Biology and Medicine 39, 1549–1559.Google Scholar
Kazura, J. W., Fanning, M. M., Blumer, J. L. and Mahmoud, A. A. (1981). Role of cell-generated hydrogen peroxide in granulocyte-mediated killing of schistosomula of Schistosoma mansoni in vitro . Journal of Clinical Investigation 67, 93–102.CrossRefGoogle ScholarPubMed
Kumar, J. K., Tabor, S. and Richardson, C. C. (2004). Proteomic analysis of thioredoxin-targeted proteins in Escherichia coli . Proceedings of National Academy of Sciences of the United States of America 101, 3759–3764.Google Scholar
Kuntz, A. N., Davioud-Charvet, E., Sayed, A. A., Califf, L. L., Dessolin, J., Arner, E. S. and Williams, D. L. (2007). Thioredoxin glutathione reductase from Schistosoma mansoni: an essential parasite enzyme and a key drug target. PLoS Medicine 4, e206.Google Scholar
Laskowski, R. A., Macarthur, M. W., Moss, D. S. and Thornton, J. M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. Journal of Applied Crystallography 26, 283–291.Google Scholar
Lee, K. K., Murakawa, M., Takahashi, S., Tsubuki, S., Kawashima, S., Sakamaki, K. and Yonehara, S. (1998). Purification, molecular cloning, and characterization of TRP32, a novel thioredoxin-related mammalian protein of 32 kDa. Journal of Biological Chemistry 273, 19160–19166.CrossRefGoogle Scholar
Lennon, B. W., Williams, C. H. Jr. and Ludwig, M. L. (2000). Twists in catalysis: alternating conformations of Escherichia coli thioredoxin reductase. Science 289, 1190–1194.Google Scholar
Lillig, C. H. and Holmgren, A. (2007). Thioredoxin and related molecules – from biology to health and disease. Antioxidant and Redox Signal 9, 25–47.Google Scholar
Liu, H., Nishitoh, H., Ichijo, H. and Kyriakis, J. M. (2000). Activation of apoptosis signal-regulating kinase 1 (ASK1) by tumor necrosis factor receptor-associated factor 2 requires prior dissociation of the ASK1 inhibitor thioredoxin. Molecular and Cellular Biology 20, 2198–2208.CrossRefGoogle ScholarPubMed
Liu Jian, X. B., Zhang, X., Liu, L., Hu, W., Wang, X.-N. (2012). Cloning, expression and function analysis of thioredoxin-1 protein of Schistosoma japonicum . Chinese Journal of Parasitology and Parasitic Diseases 30, 335–340.Google Scholar
Long, F., Vagin, A. A., Young, P. and Murshudov, G. N. (2008). BALBES: a molecular-replacement pipeline. Acta Crystallographica, Section D (Biological Crystallography) 64, 125–132.Google Scholar
Loverde, P. T. (1998). Do antioxidants play a role in schistosome host–parasite interactions? Parasitology Today 14, 284–289.CrossRefGoogle ScholarPubMed
Lu, Y., Xu, B., Ju, C., Mo, X. J., Chen, S. B., Feng, Z., Wang, X. N. and Hu, W. (2012). Immunoscreening of Schistosoma japonicum egg cDNA library and identification of positive clones. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 30, 109–115.Google Scholar
Michelet, L., Zaffagnini, M., Marchand, C., Collin, V., Decottignies, P., Tsan, P., Lancelin, J. M., Trost, P., Miginiac-Maslow, M., Noctor, G. and Lemaire, S. D. (2005). Glutathionylation of chloroplast thioredoxin f is a redox signaling mechanism in plants. Proceedings of National Academy of Sciences of the United States of America 102, 16478–16483.Google Scholar
Otwinowski, Z. and Minor, W. (1997). Processing of x-ray diffraction data collected in oscillation mode. Methods in Enzymology 276, 307–326.Google Scholar
Powis, G. and Montfort, W. R. (2001). Properties and biological activities of thioredoxins. Annual Review of Pharmacology and Toxicology 41, 261–295.Google Scholar
Puigbo, P., Guzman, E., Romeu, A. and Garcia-Vallve, S. (2007). OPTIMIZER: a web server for optimizing the codon usage of DNA sequences. Nucleic Acids Research 35, W126–W131.Google Scholar
Puigbo, P., Romeu, A. and Garcia-Vallve, S. (2008). HEG-DB: a database of predicted highly expressed genes in prokaryotic complete genomes under translational selection. Nucleic Acids Research 36, D524–D527.Google Scholar
Richardson, C. C. (1983). Bacteriophage T7: minimal requirements for the replication of a duplex DNA molecule. Cell 33, 315–317.Google Scholar
Russel, M. and Model, P. (1985). Thioredoxin is required for filamentous phage assembly. Proceedings of National Academy of Sciences of the United States of America 82, 29–33.Google Scholar
Ryter, S. W. and Tyrrell, R. M. (2000). The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radical and Biological Medicine 28, 289–309.Google Scholar
Sanger, F. (1949). Fractionation of oxidized insulin. Biochemical Journal 44, 126–128.Google Scholar
Schenk, H., Klein, M., Erdbrugger, W., Droge, W. and Schulze-Osthoff, K. (1994). Distinct effects of thioredoxin and antioxidants on the activation of transcription factors NF-kappa B and AP-1. Proceedings of National Academy of Sciences of the United States of America 91, 1672–1676.CrossRefGoogle ScholarPubMed
Schurmann, P. (2003). Redox signaling in the chloroplast: the ferredoxin/thioredoxin system. Antioxidant and Redox Signal 5, 69–78.CrossRefGoogle ScholarPubMed
Song, L., Li, J., Xie, S., Qian, C., Wang, J., Zhang, W., Yin, X., Hua, Z. and Yu, C. (2012). Thioredoxin glutathione reductase as a novel drug target: evidence from Schistosoma japonicum . PLoS One 7, e31456.Google Scholar
Wahl, M. C., Irmler, A., Hecker, B., Schirmer, R. H. and Becker, K. (2005). Comparative structural analysis of oxidized and reduced thioredoxin from Drosophila melanogaster . Journal of Molecular Biology 345, 1119–1130.Google Scholar
WHO (2014). Schistosomiasis Fact sheet N°115. World Health Organization, Geneva, Switzerland.Google Scholar
Yoshioka, J., Schreiter, E. R. and Lee, R. T. (2006). Role of thioredoxin in cell growth through interactions with signaling molecules. Antioxidant and Redox Signal 8, 2143–2151.Google Scholar