Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-07T21:21:20.023Z Has data issue: false hasContentIssue false
  • English
  • Français

Two novel phospholipid hydroperoxide glutathione peroxidase genes of Paragonimus westermani induced by oxidative stress

Published online by Cambridge University Press:  05 March 2009

S.-H. KIM ,
G.-B. CAI ,
Y.-A. BAE ,
E.-G. LEE ,
Y.-S. LEE  and
Y. KONG
S.-H. KIM
Affiliation:
Department of Molecular Parasitology, Sungkyunkwan University School of Medicine, Suwon, 440-746, Korea Center for Molecular Medicine, Samsung Biomedical Research Institute, Suwon, 440-746, Korea
G.-B. CAI
Affiliation:
Department of Molecular Parasitology, Sungkyunkwan University School of Medicine, Suwon, 440-746, Korea Present affiliation: Department of Parasitology, School of Medicine, Wuhan University, Wuhan 430071, China.
Y.-A. BAE
Affiliation:
Department of Molecular Parasitology, Sungkyunkwan University School of Medicine, Suwon, 440-746, Korea Center for Molecular Medicine, Samsung Biomedical Research Institute, Suwon, 440-746, Korea
E.-G. LEE
Affiliation:
Department of Molecular Parasitology, Sungkyunkwan University School of Medicine, Suwon, 440-746, Korea Center for Molecular Medicine, Samsung Biomedical Research Institute, Suwon, 440-746, Korea
Y.-S. LEE
Affiliation:
Department of Pharmacology, Sungkyunkwan University School of Medicine, Suwon, 440-746, Korea Center for Molecular Medicine, Samsung Biomedical Research Institute, Suwon, 440-746, Korea
Y. KONG*
Affiliation:
Department of Molecular Parasitology, Sungkyunkwan University School of Medicine, Suwon, 440-746, Korea Center for Molecular Medicine, Samsung Biomedical Research Institute, Suwon, 440-746, Korea
*
*Corresponding author: Department of Molecular Parasitology, Sungkyunkwan University School of Medicine, 300 Cheoncheon-dong, Suwon, Gyeonggi-do 440-746, Korea. Tel: +82 31 299 6261. Fax: +82 31 299 6269. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Phospholipid hydroperoxide glutathione peroxidase (PHGPx; GPx4) plays unique roles in the protection of cells against oxidative stress by catalysing reduction of lipid hydroperoxides. We characterized 2 novel GPx genes from a lung fluke, Paragonimus westermani (designated PwGPx1 and PwGPx2). These single copy genes spanned 6559 and 12 371 bp, respectively, and contained each of 5 intervening introns. The PwGPx2 harboured a codon for Sec and a Sec insertion sequence motif. Proteins encoded by the Paragonimus genes demonstrated a primary structure characteristic to the PHGPx family, including preservation of catalytic and glutathione-binding domains and absence of the subunit interaction domain. Expression of PwGPx1 increased gradually as the parasite matured, whereas that of PwGPx2 was temporally regulated. PwGPx2 was expressed at the basal level from the metacercariae to the 3-week-old juveniles; however, the expression was significantly induced in the 7-week-old immature worms and reached a plateau in the 12-week-old adults and eggs. PwGPx1 and PwGPx2 were largely localized in vitellocytes within vitelline glands and eggs. Oxidative stress-inducible paraquat, juglone and H2O2 substantially augmented the PwGPx1 and PwGPx2 expressions in viable worms by 1·5- to 11-fold. Our results strongly suggested that PwGPxs may actively participate in detoxification of oxidative hazards in P. westermani.

Keywords

Paragonimus westermaniantioxidantsphospholipid hydroperoxide glutathione peroxidasevitellocytesoxidative stress
Type
Research Article
Information
Parasitology , Volume 136 , Issue 5 , April 2009 , pp. 553 - 565
Copyright
Copyright © 2009 Cambridge University Press

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

Arthur, J. R. (2000). The glutathione peroxidases. Cellular and Molecular Life Sciences 57, 1825–1835.Google Scholar
Blair, D., Xu, Z. B. and Agatsuma, T. (1999). Paragonimiasis and the genus Paragonimus. Advances in Parasitology 42, 113–222.Google Scholar
Brigelius-Flohé, R., Aumann, K. D., Blöcker, H., Gross, G., Kiess, M., Klöppel, K. D., Maiorino, M., Roveri, A., Schuckelt, R., Ursini, F., Wingender, E. and Flohé, L. (1994). Phospholipid-hydroperoxide glutathione peroxidase. Genomic DNA, cDNA, and deduced amino acid sequence. Journal of Biological Chemistry 269, 7342–7348.CrossRefGoogle ScholarPubMed
Cai, G. B., Bae, Y. A., Kim, S. H., Sohn, W. M., Lee, Y. S., Jiang, M. S., Kim, T. S. and Kong, Y. (2008). Vitellocye-specific expression of hydroperoxide glutathione peroxidases in Clonorchis sinensis. International Journal for Parasitology 38, 1613–1623.CrossRefGoogle ScholarPubMed
Callahan, H. L., Crouch, R. K. and James, E. R. (1988). Helminth anti-oxidant enzymes: a protective mechanism against host oxidants? Parasitology Today 4, 218–225.CrossRefGoogle ScholarPubMed
Chi, C., Tanaka, R., Okuda, Y., Ikota, N., Yamamoto, H., Urano, S., Ozawa, T. and Anzai, K. (2005). Quantitative measurements of oxidative stress in mouse skin induced by X-ray irradiation. Chemical and Pharmaceutical Bulletin 53, 1411–1415.Google Scholar
Chung, Y. B., Lee, H. S., Song, C. Y. and Cho, S. Y. (1992). Activities of scavenging enzymes of oxygen radicals in early maturation stages of Paragonimus westermani. Korean Journal of Parasitology 30, 355–358.Google Scholar
Comhair, A. A. and Erzurum, S. C. (2005). The regulation and role of extracellular glutathione peroxidase. Antioxidants & Redox Signaling 7, 72–79.CrossRefGoogle ScholarPubMed
Cookson, E., Blaxter, M. L. and Selkirk, M. E. (1992). Identification of the major soluble cuticular glycoprotein of lymphatic filarial nematode parasites (gp29) as a secretory homolog of glutathione peroxidase, Proceedings of the National Academy of Sciences, USA 89, 5837–5841.Google Scholar
Dröge, W. (2002). Free radicals in the physiological control of cell function. Physiological Reviews 82, 47–95.CrossRefGoogle ScholarPubMed
Epp, O., Ladenstein, R. and Wendel, A. (1983). The refined structure of the selenoenzyme glutathione peroxidase at 0·2-nm resolution. European Journal of Biochemistry 133, 51–69.CrossRefGoogle ScholarPubMed
Grossmann, A. and Wendel, A. (1983). Non-reactivity of the selenoenzyme glutathione peroxidase with enzymatically hydroperoxidized phospholipids. European Journal of Biochemistry 135, 549–552.CrossRefGoogle ScholarPubMed
Hancok, J. T., Desikan, R. and Neill, S. J. (2001). Role of reactive oxygen species in cell signalling pathways. Biochemistry Society Transactions 29, 345–350.CrossRefGoogle Scholar
Henkle-Dührsen, K. and Kampkötter, A. (2001). Antioxidant enzyme families in parasitic nematodes. Molecular and Biochemical Parasitology 114, 129–142.CrossRefGoogle ScholarPubMed
Hong, S. J., Kang, S. Y., Chung, Y. B., Chung, M. H., Oh, Y. J., Kang, I., Bahk, Y. Y., Kong, Y. and Cho, S. Y. (2000). Paragonimus westermani: a cytosolic glutathione S-transferase of a sigma-class in adult stage. Experimental Parasitology 94, 180–189.CrossRefGoogle ScholarPubMed
Imai, H. and Nakagawa, Y. (2003). Biological significance of phospholipids hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radical Biology & Medicine 34, 145–169.Google Scholar
Jackson, M. J. (2005). Reactive oxygen species and redox-regulation of skeletal muscle adaptations to exercise. Philosophical Transactions of the Royal Society of London, B 360, 2285–2291.CrossRefGoogle ScholarPubMed
Kryukov, G. V., Castellano, S., Novoselov, S. V., Lobanov, A. V., Zehtab, O., Guigó, R. and Gladyshev, V. N. (2003). Characterization of mammalian selenoproteomes, Science 300, 1439–1443.Google Scholar
Li, A. H., Na, B. K., Kong, Y., Cho, S. H., Zhao, Q. P. and Kim, T. S. (2005). Molecular cloning and characterization of copper/zinc-superoxide dismutase of Paragonimus westermani. Journal of Parasitology 91, 293–299.Google Scholar
Mei, H. and LoVerde, P. T. (1995). Schistosoma mansoni: cloning the gene encoding glutathione peroxidase. Experimental Parasitology 80, 319–322.CrossRefGoogle ScholarPubMed
Nakamura-Uchiyama, F., Mukae, H. and Nawa, Y. (2002). Paragonimiasis: a Japanese perspective. Clinics in Chest Medicine 23, 409–420.Google Scholar
O'Brien, P. J. (1991). Molecular mechanisms of quinone cytotoxicity. Chemico-biological Interactions 80, 1–41.Google Scholar
Roche, C., Liu, J. L., LePresle, T., Capron, A. and Pierce, R. J. (1996). Tissue localization and stage-specific expression of the phospholipid hydroperoxide glutathione peroxidase of Schistosoma mansoni. Molecular and Biochemical Parasitology 75, 187–195.Google Scholar
Salinas, G., Selkirk, M. E., Chalar, C., Maizels, R. M. and Fernandez, C. (2004). Linked thioredoxin-glutathione systems in platyhelminths. Trends in Parasitology 20, 340–346.CrossRefGoogle ScholarPubMed
Sayed, A. A., Cook, S. K. and Williams, D. L. (2006). Redox balance mechanisms in Schistosoma mansoni rely on peroxiredoxins and albumin and implicate peroxiredoxins as novel drug targets. Journal of Biological Chemistry 281, 17001–17010.Google Scholar
Selkirk, M. E., Smith, V. P., Thomas, G. R. and Gounaris, K. (1998). Resistance of filarial nematode parasites to oxidative stress. International Journal for Parasitology 28, 1315–1332.Google Scholar
Sim, S., Yong, T. S., Park, S. J., Im, K. I., Kong, Y., Ryu, J. S., Min, D. Y. and Shin, M. H. (2005). NADPH oxidase-derived reactive oxygen species-mediated activation of ERK1/2 is required for apoptosis of human neutrophils induced by Entamoeba histolytica. Journal of Immunology 174, 4279–4288.Google Scholar
Stadtman, T. C. (1996). Selenocysteine. Annual Review of Biochemistry 65, 83–100.Google Scholar
Tawe, W. N., Eschbach, M. L., Walter, R. D. and Henkle-Dührsen, K. (1998). Identification of stress-responsive genes in Caenorhabditis elegans using RT-PCR differential display. Nucleic acids Research 26, 1621–1627.Google Scholar
Thannickal, V. J. and Fanburg, B. L. (2000). Reactive oxygen species in cell signaling. American Journal of Physiology. Lung Cellular and Molecular Physiology 279, L1005–1028.CrossRefGoogle ScholarPubMed
Ursini, F. and Bindoli, A. (1987). The role of selenium peroxidases in the protection against oxidative damage of membranes. Chemistry and Physics of Lipids 44, 255–276.CrossRefGoogle ScholarPubMed
Utomo, A., Jiang, X., Furuta, S., Yun, J., Levin, D. S., Wang, Y. C., Desai, K. V., Green, J. E., Chen, P. L. and Lee, W. H. (2004). Identification of a novel putative non-selenocysteine containing phospholipids hydroperoxide glutathione peroxidase (NPGPx) essential for alleviating oxidative stress generated from polyunsaturated fatty acids in breast cancer cells. Journal of Biological Chemistry 279, 43522–43529.CrossRefGoogle ScholarPubMed
Williams, D. L., Pierce, R. J., Cookson, E. and Capron, A. (1992). Molecular cloning and sequencing of glutathione peroxidase from Schistosoma mansoni. Molecular and Biochemical Parasitology 52, 127–130.Google Scholar
World Health Organization (1995). Report on control of food-borne trematode infections. WHO Technical Report Series No. 849. World Health Organization, Geneva.Google Scholar
Zelck, U. E. and von Janowsky, B. (2004). Antioxidant enzymes in intramolluscan Schistosoma mansoni and ROS-induced changes in expression. Parasitology 128, 493–501.CrossRefGoogle ScholarPubMed