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Enzymatic antioxidant systems in helminth parasites

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Abstract

Parasitic helminths have a coexistence with mammalian hosts whereby they survive for several years in known hostile conditions of their hosts. Many explanations exist describing how these parasitic helminths are able to survive. In the last years, a lot of studies have focused on both enzymatic and non-enzymatic antioxidant systems now shown to exist in these parasites and which may serve as defence tactics against the host-generated oxygen radicals. The relevance of antioxidant enzymes is confirmed by the fact that some of these molecules represent putative protective anti-parasite vaccines (i.e. in schistosomiasis). This review tries to compile what is known to date of the enzymatic antioxidant systems in selected parasitic helminths.

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Abbreviations

ROS:

Reactive oxygen species

UV:

Ultraviolet light

NO:

Nitric oxide

O2 :

Molecular oxygen

H2O2 :

Hydrogen peroxide

SOD:

Superoxide dismutase

CAT:

Catalase

GPx:

Glutathione peroxidase

NADPH:

Nicotinamide adenine dinucleotide phosphate, reduced form

Prx:

Peroxiredoxins

Cys:

Cysteine

TRX:

Thioredoxins

GSH:

Glutathione

GSTs:

Glutathione-S-transferases

TRXPx:

Thioredoxin peroxidase

CT-SOD:

Cytosolic superoxide dismutase

SP-SOD:

Extracellular or with peptide signal superoxide dismutase

SmGST:

Schistosoma mansoni GST

SmGSTO:

S. mansoni ω class GST

Sm28GST:

28 kDa GST of Schistosoma mansoni

OvTPx:

TRXPx of O. volvulus

TsGST24:

GST of 24 kDa of T. spiralis

References

  • Alger HM, Sayed AA, Stadecker MJ, Williams DL (2002) Molecular and enzymatic characterization of Schistosoma mansoni thioredoxin. Int J Parasitol 32:1285–1292

    Article  CAS  PubMed  Google Scholar 

  • Angeli V, Faveeuw C, Roye O, Fontaine J, Teissier E, Capron A, Wolowczuk I, Capron M, Trottein F (2001) Role of the parasite-derived prostaglandin D2 in the inhibition of epidermal Langerhans cell migration during schistosomiasis infection. J Exp Med 193:1135–47

    Article  CAS  PubMed  Google Scholar 

  • Bahuon C, Blaga R, Fu BaoQuan, Chiumiento L, Ming Yuan L, Le Rhun D, Glemarec A, Boireau P (2007) Isolation, biochemical analysis and localization of a 24kDa Glutathione S-Transferase from Trichinella. 21 WAAVP August 15–19 2007, Abstract Book, Ghent, Belgium

  • Bass DA, Szejda P (1979) Mechanisms of killing of newborn larvae of Trichinella spiralis by neutrophils and eosinophils. Killing by generation of hydrogen peroxide in vitro. J Clin Invest 64(1558):1564

    Google Scholar 

  • Batra S, Singh SP, Gupta S, Katiyar JC, Srivastava VM (1990) Reactive oxygen intermediates metabolizing enzymes in Ancylostoma ceylanicuin and Nippostrongilus brasiliensis. Free Radic Biol Med 8:271–274

    Article  CAS  PubMed  Google Scholar 

  • Batra S, Srivastava JK, Gupta S, Katiyar JC, Srivastava VM (1993) Role of reactive oxygen species in expulsion of Nippostrongylus brasiliensis from rats. Parasitology 106:185–192

    Article  CAS  PubMed  Google Scholar 

  • Boulanger D, Reid GD, Sturrock RF, Wolowczuk I, Balloul JM, Grezel D, Pierce RJ, Otieno MF, Guerret S, Grimaud JA (1991) Immunization of mice and baboons with the recombinant Sm28GST affects both worm viability and fecundity after experimental infection with Schistosoma mansoni. Parasite Immunol 13:473–490

    Article  CAS  PubMed  Google Scholar 

  • Briviba K, Klotz LO, Sies H (1999) Defenses against peroxynitrite. Methods Enzymol 301:301–11

    Article  CAS  PubMed  Google Scholar 

  • Brophy PM, Pritchard DI (1994) Parasitic helminth glutathione S-transferases: an update on their potential as targets for immuno- and chemotherapy. Exp Parasitol 79:89–96

    Article  CAS  PubMed  Google Scholar 

  • Brophy PM, Patterson LH, Pritchard DL (1995a) Secretory nematode SOD—offensive or defensive? Int J Parasitol 25(7):865–6

    Article  CAS  PubMed  Google Scholar 

  • Brophy PM, Ben-Smith A, Brown A, Behnke JM, Pritchard DI (1995b) Differential expression of glutathione S-transferase (GST) by adult Heligmosomoides polygyrus during primary infection in fast and slow responding hosts. Int J Parasitol 25(5):641–5

    Article  CAS  PubMed  Google Scholar 

  • Callahan HL, Crouch RK, James ER (1988) Helminth anti-oxidant enzymes: a protective mechanism against host oxidants? Parasitol Today 4:218–225

    Article  CAS  PubMed  Google Scholar 

  • Callahan HL, Crouch RK, James ER (1990) Hydrogen peroxide is the most toxic oxygen species for Onchocerca cervicalis microfilariae. Parasitology 100:407–415

    Article  CAS  PubMed  Google Scholar 

  • Callahan HL, Crouch RK, James ER (1991) Dirofilaria immitis superoxide dismutase: purification and characterization. Mol Biochem Parasitol 49:245–251

    Article  CAS  PubMed  Google Scholar 

  • Callahan HL, Hazen-Martin D, Crouch RK, James ER (1993) Immunolocalization of superoxide dismutase in Dirofilaria immitis adult worms. Infect Immun 61:1157–1163

    CAS  PubMed  Google Scholar 

  • Campos EG, Hermes-Lima M, Smith JM, Prichard RK (1999) Characterisation of Fasciola hepatica cytochrome c peroxidase as an enzyme with potential antioxidant activity in vitro. Int J Parasitol 29:655–662

    Article  CAS  PubMed  Google Scholar 

  • Capron A, Capron M, Riveau G (2002) Vaccine development against schistosomiasis from concepts to clinical trials. Br Med Bull 62:139–148

    Article  PubMed  Google Scholar 

  • Capron A, Riveau G, Capron M, Trottein F (2005) Schistosomes: the road from host–parasite interactions to vaccines in clinical trials. Trends Parasitol 21(3):143–9

    Article  CAS  PubMed  Google Scholar 

  • Chalar C, Martinez C, Agorio A, Salina G, Soto J, Ehrlich R (1999) Molecular cloning and characterization of a thioredoxin gene from Echinococcus granulosus. Biochem Biophys Res Commun 262:302–307

    Article  CAS  PubMed  Google Scholar 

  • Devaney E, Jecock RM (1991) The expression of the Mr 30000 antigen in the third stage larvae of Brugia pahangi. Parasite Immunol 13:75–87

    Article  CAS  PubMed  Google Scholar 

  • Donnelly S, O’Neill SM, Sekiya M, Mulcahy G, Dalton JP (2005) Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infect Immun 73(1):166–73

    Article  CAS  PubMed  Google Scholar 

  • Dzik JM (2006) Molecules released by helminth parasites involved in host colonization. Acta Biochim Pol 53(1):33–64

    CAS  PubMed  Google Scholar 

  • Eckelt VH, Liebau E, Walter RD, Henkle-Dürsen K (1998) Primary sequence and activity analyses of a catalase from Ascaris suum. Mol Biochem Parasitol 95:203–214

    Article  CAS  PubMed  Google Scholar 

  • El-Bassiouni EA, Helmy MH, Saad EI, El-Nabi Kamel MA, Abdel-Meguid E, Hussein HS (2007) Modulation of the antioxidant defence in different developmental stages of Schistosoma mansoni by praziquantel and artemether. Br J Biomed Sci 64:168–74

    CAS  PubMed  Google Scholar 

  • Giovannini C, Filesi C, D’Archivio M, Scazzocchio B, Santangelo C, Masella R (2006) Polifenoli e difese antiossidanti endogene: effetti sul glutatione e sugli enzimi ad esso correlati. Ann Ist Super Sanità 42:336–347

    CAS  PubMed  Google Scholar 

  • Girardini J, Amirante A, Zemzoumi K, Serra E (2002) Characterization of an Omega-class glutathione S-transferase from Schistosoma mansoni with glutaredoxin-like dehydroascorbate reductase and thiol transferase activities. Eur J Biochem 269(22):5512–21

    Article  CAS  PubMed  Google Scholar 

  • Grzych JM, De Bont J, Liu J, Neyrinck JL, Fontaine J, Vercruysse J, Capron A (1998) Relationship of impairment of schistosome 28-kilodalton GST activity to expression of immunity to Schistosoma mattheei in calves vaccinated with recombinant Schistosoma bovis 28-kilodalton GST. Infect Immun 66:1142–1148

    CAS  PubMed  Google Scholar 

  • Gutteridge JMC (1993) Free radicals in diseases processes: a compilation of cause and consequence. Free Radic Res Commun 19:141–58

    Article  CAS  PubMed  Google Scholar 

  • Hadas E, Rodriguez-Caabeiro F, Jimenez Gonzales A (1993) Superoxide dismutase of Trichinella spiralis and Trichinella pseudospiralis larvae. Trop Med Parasitol 44(3):195–6

    CAS  PubMed  Google Scholar 

  • Henkle-Dührsen K, Kampkötter A (2001) Antioxidant enzyme families in parasitic nematodes. Mol Biochem Parasitol 114(2):129–42

    Article  PubMed  Google Scholar 

  • Henkle KJ, Liebau E, Muller B, Bergmann B, Walter RD (1991) Characterization and molecular cloning of a Cu/Zn superoxide dismutase from the human parasite Onchocerca volvulus. Infect Immun 59:2063–2069

    CAS  PubMed  Google Scholar 

  • Henkle-Duhrsen K, Tawe W, Warnecke C, Walter RD (1995) Characterisation of manganese superoxide dismutase cDNA and gene from the human parasite Onchocerca volvulus. Biochem J 308:441–446

    PubMed  Google Scholar 

  • Henkle-Duhrsen K, Eckelt VH, Wildenburg G, Blaxter M, Walter RD (1998) Gene structure, activity and localisation of a catalase from intracellular bacteria in Onchocerca volvulus. Mol Biochem Parasitol 96:69–81

    Article  CAS  PubMed  Google Scholar 

  • Holy JM, O’Leary KA, Oaks JA, Tracy JW (1989) Immunocytochemical localisation of major glutathione S-transferase in adult Schistosoma mansoni. J Parasitol 75:181–190

    Article  CAS  PubMed  Google Scholar 

  • Hong Z, Kosman DJ, Thakur A, Rekosh D, LoVerde PT (1992) Identification and purification of a second form of Cu/Zn superoxide dismutase from Schistosoma mansoni. Infect Immun 60:3641–3651

    CAS  PubMed  Google Scholar 

  • Ichihashi M, Ueda M, Budiyanto A, Bito T, Oka M, Fukunaga M, Tsuru K, Honkawa T (2003) UV-induced skin damage. Toxicology 189:21–39

    Article  CAS  PubMed  Google Scholar 

  • Kalyanaraman B, Karoui H, Singh RJ, Felix CC (1996) Detection of thiyl radical adducts formed during hydroxyl radical- and peroxynitrite-mediated oxidation of thiols—a high resolution ESR spin-trapping study at Q-band. Anal Biochem 241:75–81

    Article  CAS  PubMed  Google Scholar 

  • Kampkötter A, Volkmann TE, de Castro SH, Leiers B, Klotz LO, Johnson TE, Link CD, Henkle-Dührsen K (2003) Functional analysis of the glutathione S-transferase 3 from Onchocerca volvulus (Ov-GST-3): a parasite GST confers increased resistance to oxidative stress in Caenorhabditis elegans. J Mol Biol 325(1):25–37

    Article  PubMed  Google Scholar 

  • Kang SW, Baines IC, Rhee SG (1998) Characterization of mammalian peroxiredoxin that contains one conserved cysteine. J Biol Chem 273:6303–6311

    Article  CAS  PubMed  Google Scholar 

  • Kazura JW (1981) Host defence mechanisms against nematode parasites: destruction of newborn Trichinella spiralis larvae by human antibodies and granulocytes. J Infect Dis 143:712–718

    CAS  PubMed  Google Scholar 

  • Kazura JW, Meshnick SR (1984) Scavenger enzymes and resistance to oxygen-mediated damage in Trichinella spiralis. Mol Biochem Parasitol 10:1–10

    Article  CAS  PubMed  Google Scholar 

  • Kehrer J (1993) Free radicals as mediators of tissue injury and disease. Crit Rev Toxicol 23:21–48

    Article  CAS  PubMed  Google Scholar 

  • Kim TS, Jung Y, Na BK, Kim KS, Chung PR (2000) Molecular cloning and expression of Cu/Zn-containing superoxide dismutase from Fasciola hepatica. Infect Immun 68:3941–3948

    Article  CAS  PubMed  Google Scholar 

  • Kotze AC, McClure SJ (2001) Haemonchus contortus utilises catalase in defence against exogenous hydrogen peroxide in vitro. Int J Parasitol 31:1563–1571

    Article  CAS  PubMed  Google Scholar 

  • Kunchithapautham K, Padmavathi B, Narayanan RB, Kaliraj P, Scott AL (2003) Thioredoxin from Brugia malayi: defining a 16-kilodalton class of thioredoxins from nematodes. Infect Immun 71(7):4119–26

    Article  CAS  PubMed  Google Scholar 

  • Kwatia MA, Botkin DJ, Williams DL (2000) Molecular and enzymatic characterization of Schistosoma mansoni thioredoxin peroxidase. J Parasitol 86:908–915

    CAS  PubMed  Google Scholar 

  • Leid RW, Suquet CM (1986) A superoxide dismutase of metacestodes of Taenia taeniaeformis. Mol Biochem Parasitol 18:301–311

    Article  CAS  PubMed  Google Scholar 

  • Liebau E, Wildenburg G, Walter RD, Henkle-Duhrsen K (1994) A novel type of glutathione S-transferase in Onchocerca volvulus. Infect Immun 62:4762–4767

    CAS  PubMed  Google Scholar 

  • Liebau E, Müller V, Lucius R, Walter RD, Henkle-Dührsen K (1996) Molecular cloning, expression and characterization of a recombinant glutathione S-transferase from Echinococcus multilocularis. Mol Biochem Parasitol 77(1):49–56

    Article  CAS  PubMed  Google Scholar 

  • Liebau E, Eckelt VH, Wildenburg G, Teesdale-Spittle P, Brophy PM, Walter RD, Henkle-Dührsen K (1997) Structural and functional analysis of a glutathione S-transferase from Ascaris suum. Biochem J 324:659–66

    CAS  PubMed  Google Scholar 

  • Liebau E, Eschbach ML, Tawe W, Sommer A, Fischer P, Walter RD, Henkle-Duhrsen K (2000) Identification of a stress-responsive Onchocerca volvulus glutathione S-transferase (Ov-GST-3) by RT-PCR differential display. Mol Biochem Parasitol 109:101–110

    Article  CAS  PubMed  Google Scholar 

  • Liu JL, Fontaine J, Capron A, Grzych JM (1996) Ultrastructural localisation of Sm28 GST protective antigen in Schistosoma mansoni adult worms. Parasitology 113:377–391

    Article  PubMed  Google Scholar 

  • LoVerde PT, Carvalho-Queiroz C, Cook R (2004) Vaccination with antioxidant enzymes confers protective immunity against challenge infection with Schistosoma mansoni. Mem Inst Oswaldo Cruz 99:37–43

    Article  CAS  PubMed  Google Scholar 

  • Lu W, Egerton GL, Bianco AE, Williams SA (1998) Thioredoxin peroxidase from Onchocerca volvulus: a major hydrogen peroxide detoxifying enzyme in filarial parasites. Mol Biochem Parasitol 91:221–235

    Article  CAS  PubMed  Google Scholar 

  • McGonigle S, Curley GP, Dalton JP (1997) Cloning of peroxiredoxin, a novel antioxidant enzyme, from the helminth parasite Fasciola hepatica. Parasitology 115:101–104

    Article  CAS  PubMed  Google Scholar 

  • McGonigle S, Dalton JP, James ER (1998) Peroxidoxins: a new antioxidant family. Parasitol Today 14:139–145

    Article  CAS  PubMed  Google Scholar 

  • Mei H, LoVerde PT (1997) Schistosoma mansoni: the developmental regulation and immunolocalization of antioxidant enzymes. Exp Parasitol 86:69–78

    Article  CAS  PubMed  Google Scholar 

  • Meister A, Anderson ME (1983) Glutathione. Ann Rev Biochem 52:711–60

    Article  CAS  PubMed  Google Scholar 

  • Mkojii GM, Smith JM, Prichard RK (1988) Anti-oxidant systems in Schistosoma mansoni: correlation between susceptibility to oxidant killing and the levels of scavengers of hydrogen per oxide and oxygen free radicals. Int J Parasitol 18:661–666

    Article  Google Scholar 

  • Nakashima I, Takeda K, Kawamoto Y, Okuno Y, Kato M, Suzuki H (2005) Redox control of catalytic activities of membrane-associated protein tyrosine kinases. Arch Biochem Biophys 434:3–10

    Article  CAS  PubMed  Google Scholar 

  • Nare B, Smith JM, Prichard RK (1990) Schistosoma mansoni: levels of antioxidants and resistance to oxidants increase during development. Exp Parasitol 70:389–397

    Article  CAS  PubMed  Google Scholar 

  • O’Leary KA, Tracy JW (1988) Purification of three cytosolic glutathione S-transferase from adult Schistosoma mansoni. Arch Biochem Biophys 264:1–12

    Article  PubMed  Google Scholar 

  • O’Leary KA, Hathaway KM, Tracy JW (1992) Schistosoma mansoni: single-step purification and characterization of glutathione S-transferase isoenzyme 4. Exp Parasitol 75:47–55

    Article  PubMed  Google Scholar 

  • Oliveira PL, Oliveira MF (2002) Vampires, Pasteur and reactive oxygen species. Is the switch from aerobic to anaerobic metabolism a preventive antioxidant defence in blood-feeding parasites. FEBS Lett 525(1-3):3–6

    Article  CAS  PubMed  Google Scholar 

  • Ou X, Thomas GR, Chacon MR, Tang L, Selkirk ME (1995a) Brugia malayi: differential susceptibility to the metabolism of hydrogen peroxide in adults and microfilariae. Exp Parasitol 80:530–540

    Article  CAS  PubMed  Google Scholar 

  • Ou X, Tang L, McCrossan M, Henkle-Dührsen K, Selkirk ME (1995b) Brugia malayi: localisation and differential expression of extracellular and cytoplasmic CuZn superoxide dismutases in adults and microfilariae. Exp Parasitol 80:515–529

    Article  CAS  PubMed  Google Scholar 

  • Piacenza L, Radi R, Goni F, Carmona C (1998) Cu/Zn superoxide dismutase activities from Fasciola hepatica. Parasitology 117:555–562

    Article  CAS  PubMed  Google Scholar 

  • Piedrafita D, Spithill TW, Dalton JP, Brindley PJ, Sandeman MR, Wood PR, Parsons JC (2000) Juvenile Fasciola hepatica are resistant to killing in vitro by free radicals compared with larvae of Schistosoma mansoni. Parasite Immunol 22:287–295

    Article  CAS  PubMed  Google Scholar 

  • Pompella A, Visvikis A, Paolicchi A, de Tata V, Casini AF (2003) The changing faces of glutathione, a cellular protagonist. Biochem Pharmacol 66:1499–503

    Article  CAS  PubMed  Google Scholar 

  • Poulin R, Morand S (2005) Parasite biodiversity. Smithsonian Books, Washington, DC

    Google Scholar 

  • Rao UR, Salinas G, Mehta K, Klei TR (2000) Identification and localization of glutathione S transferase as a potential target enzyme in Brugia species. Parasitol Res 86:908–915

    Article  CAS  PubMed  Google Scholar 

  • Rhoads ML (1983) Trichinella spiralis: identification and purification of superoxide dismutase. Exp Parasitol 56:41–54

    Article  CAS  PubMed  Google Scholar 

  • Rojas J, Rodriguez-Osorio M, Gomez-Garcia V (1997) Immunological characteristics and localization of the Trichinella spiralis glutathione-S-transferase. J Parasitol 83:630–635

    Article  CAS  PubMed  Google Scholar 

  • Rzepczyk CM, Bishop CJ (1984) Immunological and structural aspects of the cell mediated killing of Dirofilaria immitis microfilariae. Parasite Immunol 6:443–457

    Article  CAS  PubMed  Google Scholar 

  • Salazar-Calderon M, Nfartin-Alonso JM, Ruiz de Eguino AD, Casais R, Marin MS, Parra F (2000) Fasciola hepatica: heterogenous expression and functional characterisation of a thioredoxin peroxidase. Exp Parasitol 95:63–70

    Article  CAS  PubMed  Google Scholar 

  • Salinas G, Cardozo S (2000) Echinococcus granulosus: heterogeneity and differential expression of superoxide dismutases. Exp Parasitol 94:56–59

    Article  CAS  PubMed  Google Scholar 

  • Salinas G, Fernández V, Fernández C, Selkirk ME (1998) Echinococcus granulosus: cloning of a thioredoxin peroxidase. Exp Parasitol 90:298–301

    Article  CAS  PubMed  Google Scholar 

  • Salvatore L, Wijffels G, Sexton JL, Panaccio M, Mailer S, McCauley I (1995) Biochemical analysis of recombinant glutathione S-transferase of Fasciola hepatica. Mol Biochem Parasitol 69:281–288

    Article  CAS  PubMed  Google Scholar 

  • Sayed AA, Williams DL (2004) Biochemical characterization of 2-Cys peroxiredoxins from Schistosoma mansoni. J Biol Chem 279:26159–26166

    Article  CAS  PubMed  Google Scholar 

  • Selkirk ME, Smith VP, Thomas GR, Gounaris K (1998) Resistance of filarial nematode parasites to oxidative stress. Int J Parasitol 28(9):1315–32

    Article  CAS  PubMed  Google Scholar 

  • Sexton JL, Milner AR, Panaccio M, Waddington J, Wijffels G, Chandler D, Thompson C, Wilson L, Spithill TW, Mitchell G et al (1990) Glutathione S-transferase: novel vaccine against Fasciola hepatica infection in sheep. J Immunol 145:3905–3910

    CAS  PubMed  Google Scholar 

  • Smith NC, Bryant C (1986) The role of host generated free radicals in helminth infections: Nippostrongylus brasiliensis and Nematospiroides dubius compared. Int J Parasitol 16:617–622

    Article  CAS  PubMed  Google Scholar 

  • Smith NC, Bryant C (1989) The effect of antioxidants on the rejection of Nippostrongylus brasiliensis. Parasite Immunol 11:161–167

    Article  CAS  PubMed  Google Scholar 

  • Smith VP, Selkirk ME, Gounaris K (1998) Brugia malayi: resistance of cuticular lipids to oxidant-induced damage and detection of α-tocopherol in the neutral lipid fraction. Exp Parasitol 88:103–110

    Article  CAS  PubMed  Google Scholar 

  • Taiwo FA, Brophy PM, Pritchard DI, Brown A, Wardlaw A, Patterson LH (1999) Cu/Zn superoxide dismutase in excretory-secretory products of human hookworm Necator americanus. An electron paramagnetic spectrometry study. Eur J Biochem 264:434–438

    Article  CAS  PubMed  Google Scholar 

  • Tang L, Ou X, Henkle-Dührsen K, Selkirk ME (1994) Extracellular and cytoplasmic CuZn superoxide dismutases from Brugia lymphatic filarial nematode parasites. Infect Immun 62(3):961–7

    CAS  PubMed  Google Scholar 

  • Tang L, Smith VP, Gounaris K, Selkirk ME (1996) Brugia pahangi: the cuticular glutathione peroxidase (gp29) protects heterologous membranes from lipid peroxidation. Exp Parasitol 82:329–332

    Article  CAS  PubMed  Google Scholar 

  • Tsuji N, Kasuga-Aoki H, Isobe T, Yoshihara S (2000) Cloning and characterisation of a peroxiredoxin from the swine roundworm Ascaris suum. Int J Parasitol 30(2):125–8

    Article  CAS  PubMed  Google Scholar 

  • van Rossum AJ, Jefferies JR, Rijsewijk FA, LaCourse EJ, Teesdale-Spittle P, Barrett J, Tait A, Brophy PM (2004) Binding of hematin by a new class of glutathione transferase from the blood-feeding parasitic nematode Haemonchus contortus. Infect Immun 72(5):2780–90

    Article  PubMed  Google Scholar 

  • Wijffels GL, Sexton JL, Salvatore L, Pettitt JM, Humphris DC, Panaccio M, Spithill TW (1992) Primary sequence heterogeneity and tissue expression of glutathione S-transferase of Fasciola hepatica. Exp Parasitol 74:87–99

    Article  CAS  PubMed  Google Scholar 

  • Wildenburg G, Liebau E, Henkle-Duhrsen K (1998) Onchocerca volvulus: ultralocalisation of two glutathione S-transferases. Exp Parasitol 88:34–42

    Article  CAS  PubMed  Google Scholar 

  • Zipfel RE, Schrum S, Bialonski A, Buttner DW (1998) The peroxidoxin 2 protein of the human parasite Onchocerca volvulus: recombinant expression, immunolocalisation, and demonstration of homologous molecules in other species. Parasitol Res 84:623–631

    Article  CAS  PubMed  Google Scholar 

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  1. Department of Experimental Pathology, M.B.I.E., Università di Pisa, Scuola Medica, Via Roma, 55, 56126, Pisa, Italy

    Lorena Chiumiento & Fabrizio Bruschi

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  1. Lorena Chiumiento
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  2. Fabrizio Bruschi
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Correspondence to Fabrizio Bruschi.

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Chiumiento, L., Bruschi, F. Enzymatic antioxidant systems in helminth parasites. Parasitol Res 105, 593–603 (2009). https://doi.org/10.1007/s00436-009-1483-0

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