Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-19T07:19:47.982Z Has data issue: false hasContentIssue false
  • English
  • Français

Catalase expression impairs oxidative stress-mediated signalling in Trypanosoma cruzi

Published online by Cambridge University Press:  27 June 2017

ANNA CLÁUDIA GUIMARÃES FREIRE ,
CERES LUCIANA ALVES ,
GRAZIELLE RIBEIRO GOES ,
BRUNO CARVALHO RESENDE ,
NILMAR SILVIO MORETTI ,
VINÍCIUS SANTANA NUNES ,
PEDRO HENRIQUE NASCIMENTO AGUIAR ,
ERICH BIRELLI TAHARA ,
GLÓRIA REGINA FRANCO  and
ANDRÉA MARA MACEDO
...Show all authors
ANNA CLÁUDIA GUIMARÃES FREIRE
Affiliation:
Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
CERES LUCIANA ALVES
Affiliation:
Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
GRAZIELLE RIBEIRO GOES
Affiliation:
Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
BRUNO CARVALHO RESENDE
Affiliation:
Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
NILMAR SILVIO MORETTI
Affiliation:
Departamento de Microbiologia, Imunologia e Parasitologia, Escola Paulista de Medicina, Universidade Federal de São Paulo, São Paulo, SP, Brazil
VINÍCIUS SANTANA NUNES
Affiliation:
Departamento de Microbiologia, Imunologia e Parasitologia, Escola Paulista de Medicina, Universidade Federal de São Paulo, São Paulo, SP, Brazil
PEDRO HENRIQUE NASCIMENTO AGUIAR
Affiliation:
Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
ERICH BIRELLI TAHARA
Affiliation:
Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
GLÓRIA REGINA FRANCO
Affiliation:
Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
ANDRÉA MARA MACEDO
Affiliation:
Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
SÉRGIO DANILO JUNHO PENA
Affiliation:
Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
FERNANDA RAMOS GADELHA
Affiliation:
Departamento de Bioquímica e Biologia Tecidual, Instituto de Biologia, UNICAMP, Campinas, SP, Brazil
ALESSANDRA APARECIDA GUARNERI
Affiliation:
Centro de Pesquisas René Rachou, FIOCRUZ, Belo Horizonte, MG, Brazil
SERGIO SCHENKMAN
Affiliation:
Departamento de Microbiologia, Imunologia e Parasitologia, Escola Paulista de Medicina, Universidade Federal de São Paulo, São Paulo, SP, Brazil
LEDA QUERCIA VIEIRA
Affiliation:
Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
CARLOS RENATO MACHADO*
Affiliation:
Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
*
*Corresponding author: Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Trypanosoma cruzi is exposed to oxidative stresses during its life cycle, and amongst the strategies employed by this parasite to deal with these situations sits a peculiar trypanothione-dependent antioxidant system. Remarkably, T. cruzi’s antioxidant repertoire does not include catalase. In an attempt to shed light on what are the reasons by which this parasite lacks this enzyme, a T. cruzi cell line stably expressing catalase showed an increased resistance to hydrogen peroxide (H2O2) when compared with wild-type cells. Interestingly, preconditioning carried out with low concentrations of H2O2 led untransfected parasites to be as much resistant to this oxidant as cells expressing catalase, but did not induce the same level of increased resistance in the latter ones. Also, presence of catalase decreased trypanothione reductase and increased superoxide dismutase levels in T. cruzi, resulting in higher levels of residual H2O2 after challenge with this oxidant. Although expression of catalase contributed to elevated proliferation rates of T. cruzi in Rhodnius prolixus, it failed to induce a significant increase of parasite virulence in mice. Altogether, these results indicate that the absence of a gene encoding catalase in T. cruzi has played an important role in allowing this parasite to develop a shrill capacity to sense and overcome oxidative stress.

Keywords

Trypanosoma cruzicatalaseoxidative stressoxidative signalling
Type
Research Article
Information
Parasitology , Volume 144 , Issue 11 , September 2017 , pp. 1498 - 1510
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Aft, R. L. and Mueller, G. C. (1983). Hemin-mediated DNA strand scission. Journal of Biological Chemistry 258, 12069–12072.Google Scholar
Aguiar, P. H. N., Furtado, C., Repolês, B. M., Ribeiro, G. A., Mendes, I. C., Peloso, E. F., Gadelha, F. R., Macedo, A. M., Franco, G. R., Pena, S. D. J., Teixeira, S. M. R., Vieira, L. Q., Guarneri, A. A., Andrade, L. O. and Machado, C. R. (2013). Oxidative stress and DNA lesions: the role of 8-oxoguanine lesions in Trypanosoma cruzi cell viability. PLoS Neglected Tropical Disease 7, e2279.Google Scholar
Alcolea, P., Alonso, A., Garcia-Tabares, F., Toraño, A. and Larraga, V. (2014). An insight into the proteome of Crithidia fasciculata choanomastigotes as a comparative approach to axenic growth, peanut lectin agglutination and differentiation of Leishmania spp. promastigotes. PLoS ONE 9, e113837.CrossRefGoogle ScholarPubMed
Alvarez, M. N., Peluffo, G., Piacenza, L. and Radi, R. (2011). Intraphagosomal peroxynitrite as a macrophage-derived cytotoxin against internalized Trypanosoma cruzi: consequences for oxidative killing and role of microbial peroxiredoxins in infectivity. Journal of Biological Chemistry 286, 6627–6640.Google Scholar
Atwood, J. A., Weatherly, D. B., Minning, T. A., Bundy, B., Cavola, C., Opperdoes, F. R., Orlando, R. and Tarleton, R. L. (2005). The Trypanosoma cruzi proteome. Science 309, 473–476.Google Scholar
Augusto, L. S., Moretti, N. S., Ramos, T. C. P., de Jesus, T. C. L., Zhang, M., Castilho, B. A. and Schenkman, S. (2015). A membrane-bound eIF2 alpha kinase located in endosomes is regulated by heme and controls differentiation and ROS levels in Trypanosoma cruzi . PLoS Pathogens 11, 1–27.Google Scholar
Balaban, R. S., Nemoto, S. and Finkel, T. (2005). Mitochondria, oxidants, and aging. Cell 120, 483–495.Google Scholar
Bergeron, M., Blanchette, J., Rouleau, P. and Olivier, M. (2008). Abnormal IFN-gamma-dependent immunoproteasome modulation by Trypanosoma cruzi-infected macrophages. Parasite Immunology 30, 280–292.Google Scholar
Bradford, M. (1976). Rapid and sensitive method for quantification of microgram quantities of protein utilizing principle of protein-dye-binding. Analytical Biochemistry 72, 248–254.Google Scholar
Brener, Z. (1962). Therapeutic activity and criterion of cure on mice experimentally infected with Trypanosoma cruzi . Revista do Instituto de Medicina Tropical de São Paulo 4, 389–396.Google Scholar
Buetler, T. M. (2004). Role of superoxide as a signaling molecule. News in Physiological Sciences 19, 120–123.Google ScholarPubMed
Chelikani, P., Fita, I. and Loewen, P. C. (2004). Diversity of structures and properties among catalases. Cellular and Molecular Life Sciences 61, 192–208.Google Scholar
Dalton, D. K., Pitts-Meek, S., Keshav, S., Figari, I. S., Bradley, A. and Stewart, T. A. (1993). Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259, 1739–1742.CrossRefGoogle ScholarPubMed
DaRocha, W. D., Silva, R. A., Bartholomeu, D. C., Pires, S. F., Freitas, J. M., Macedo, A. M., Vazquez, M. P., Levin, M. J. and Teixeira, S. M. (2004). Expression of exogenous genes in Trypanosoma cruzi: improving vectors and electroporation protocols. Parasitology Research 92, 113–120.Google Scholar
D'Autréaux, B. and Toledano, M. B. (2007). ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nature Reviews Molecular Cell Biology 8, 813–824.Google Scholar
Davies, J. M., Lowry, C. V. and Davies, K. J. (1995). Transient adaptation to oxidative stress in yeast. Archives of Biochemistry and Biophysics 317, 1–6.Google Scholar
Demple, B. and Halbrook, J. (1983). Inducible repair of oxidative DNA damage in Escherichia coli . Nature 304, 466–468.Google Scholar
Elliot, S. L., Rodrigues, J. de O., Lorenzo, M. G., Martins-Filho, O. A. and Guarneri, A. A. (2015). Trypanosoma cruzi, etiological agent of Chagas disease, is virulent to its triatomine vector Rhodnius prolixus in a temperature-dependent manner. PLoS Neglected Tropical Diseases 9, e0003646.CrossRefGoogle Scholar
El-Sayed, N. M., Myler, P. J., Bartholomeu, D. C., Nilsson, D., Aggarwal, G., Tran, A. N., Ghedin, E., Worthey, E. A., Delcher, A. L., Blandin, G., Westenberger, S. J., Caler, E., Cerqueira, G. C., Branche, C., Haas, B., Anupama, A., Arner, E., Aslund, L., Attipoe, P., Bontempi, E., Bringaud, F., Burton, P., Cadag, E., Campbell, D. A., Carrington, M., Crabtree, J., Darban, H., da Silveira, J. F., de Jong, P., Edwards, K., et al. (2005). The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309, 409–415.Google Scholar
Figueiredo, R. C., Rosa, D. S. and Soares, M. J. (2000). Differentiation of Trypanosoma cruzi epimastigotes: metacyclogenesis and adhesion to substrate are triggered by nutritional stress. Journal of Parasitology 86, 1213–1218.CrossRefGoogle ScholarPubMed
Finzi, J. K., Chiavegatto, C. W. M., Corat, K. F., Lopez, J. A., Cabrera, O. G., Mielniczki-Pereira, A. A., Colli, W., Alves, M. J. and Gadelha, F. R. (2004). Trypanosoma cruzi response to the oxidative stress generated by hydrogen peroxide. Molecular and Biochemical Parasitology 133, 37–43.Google Scholar
Gadelha, F. R., Gonçalves, C. C., Mattos, E. C., Alves, M. J. M., Piñeyro, M. D., Robello, C. and Peloso, E. F. (2013). Release of the cytosolic tryparedoxin peroxidase into the incubation medium and a different profile of cytosolic and mitochondrial peroxiredoxin expression in H2O2-treated Trypanosoma cruzi tissue culture-derived trypomastigotes. Experimental Parasitology 133, 287–293.Google Scholar
Garcia, E. S., Macarini, J. D., Garcia, M. L. and Ubatuba, U. F. (1975). Feeding of Rhodnius prolixus in the laboratory. Academia Brasileira de Ciências 47, 537–545.Google Scholar
Goh, J., Enns, L., Fatemie, S., Hopkins, H., Morton, J., Pettan-Brewer, C. and Ladiges, W. (2011). Mitochondrial targeted catalase suppresses invasive breast cancer in mice. BMC Cancer 11, 191.Google Scholar
Gomes, M. L., Araujo, S. M. and Chiari, E. (1991). Trypanosoma cruzi: growth of clones on solid medium using culture and blood forms. Memórias do Instituto Oswaldo Cruz 86, 131–132.Google Scholar
Graça-Souza, A. V., Maya-Monteiro, C., Paiva-Silva, G. O., Braz, G. R. C., Paes, M. C., Sorgine, M. H. F., Oliveira, M. F. and Oliveira, P. L. (2006). Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochemistry and Molecular Biology 36, 322–335.Google Scholar
Gutteridge, J. M. and Smith, A. (1988). Antioxidant protection by haemopexin of haem-stimulated lipid peroxidation. Biochemical Journal 256, 861–865.Google Scholar
Hamanaka, R. B. and Chandel, N. S. (2010). Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends in Biochemical Sciences 35, 505–513.Google Scholar
Hamilton, P. B., Stevens, J. R., Gaunt, M. W., Gidley, J. and Gibson, W. C. (2004). Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. International Journal for Parasitology 34, 1393–1404.CrossRefGoogle ScholarPubMed
Hotez, P. J., Dumonteil, E., Woc-Colburn, L., Serpa, J. A., Bezek, S., Edwards, M. S., Hallmark, C. J., Musselwhite, L. W., Flink, B. J. and Bottazzi, M. E. (2012). Chagas disease: ‘The new HIV/AIDS of the Americas’. PLoS Neglected Tropical Diseases 6, e1498.Google Scholar
Irigoín, F., Cibils, L., Comini, M. A., Wilkinson, S. R., Flohé, L. and Radi, R. (2008). Insights into the redox biology of Trypanosoma cruzi: trypanothione metabolism and oxidant detoxification. Free Radical Biology and Medicine 45, 733–742.Google Scholar
Kraeva, N., Horáková, E., Kostygov, A. Y., Butenko, A., Yurchenko, V. and Luke, J. (2016). Catalase in Leishmaniinae: with me or against me? Infection, Genetics and Evolution 50, 121–127.Google Scholar
Krauth-Siegel, R. L., Bauer, H. and Schirmer, R. H. (2005). Dithiol proteins as guardians of the intracellular redox milieu in parasites: old and new drug targets in trypanosomes and malaria-causing plasmodia. Angewandte Chemie International Edition in English 44, 690–715.Google Scholar
Mateo, H., Marín, C., Pérez-Cordón, G. and Sánchez-Moreno, M. (2008). Purification and biochemical characterization of four iron superoxide dismutases in Trypanosoma cruzi . Memórias do Instituto Oswaldo Cruz 103, 271–276.Google Scholar
Mittra, B. and Andrews, N. W. (2013). IRONy OF FATE: role of iron-mediated ROS in Leishmania differentiation. Trends in Parasitology 29, 489–496.Google Scholar
Morales, J., Mogi, T., Mineki, S., Takashima, E., Mineki, R., Hirawake, H., Sakamoto, K., Omura, S. and Kita, K. (2009). Novel mitochondrial complex II isolated from Trypanosoma cruzi is composed of 12 peptides including a heterodimeric Ip subunit. Jouornal Biol Chem 284, 7255–7263.CrossRefGoogle ScholarPubMed
Mueller, S., Riedel, H. D. and Stremmel, W. (1997). Direct evidence for catalase as the predominant H2O2-removing enzyme in human erythrocytes. Blood 90, 4973–4978.Google Scholar
Nakabeppu, Y., Kajitani, K., Sakamoto, K., Yamaguchi, H. and Tsuchimoto, D. (2006). MTH1, an oxidized purine nucleoside triphosphatase, prevents the cytotoxicity and neurotoxicity of oxidized purine nucleotides. DNA Repair 5, 761–772.Google Scholar
Nathan, C., Nogueira, N., Juangbhanich, C., Ellis, J. and Cohn, Z. (1979). Activation of macrophages in vivo and in vitro. Correlation between hydrogen peroxide release and killing of Trypanosoma cruzi . Journal of Experimental Medicine 149, 1056–1068.Google Scholar
Nogueira, N. and Cohn, Z. A. (1978). Trypanosoma cruzi: in vitro induction of macrophage microbicidal activity. Journal of Experimental Medicine 148, 288–300.Google Scholar
Nogueira, N. P. A., de Souza, C. F., de Souza Saraiva, F. M., Sultano, P. E., Dalmau, S. R., Bruno, R. E., Gonçalves, R. L. S., Laranja, G. A. T., Leal, L. H. M., Coelho, M. G. P., Masuda, C. A., Oliveira, M. F. and Paes, M. C. (2011). Heme-induced ROS in Trypanosoma cruzi activates CamkII-Like that triggers epimastigote proliferation. One helpful effect of ROS. PLoS ONE 6, e25935.CrossRefGoogle ScholarPubMed
Nogueira, N. P., Saraiva, F. M., Sultano, P. E., Cunha, P. R., Laranja, G. A., Justo, G. A., Sabino, K. C., Coelho, M. G., Rossini, A., Atella, G. C. and Paes, M. C. (2015). Proliferation and differentiation of Trypanosoma cruzi inside its vector have a new trigger: redox status. PLoS ONE 10, e0116712.Google Scholar
Novo, E. and Parola, M. (2008). Redox mechanisms in hepatic chronic wound healing and fibrogenesis. Fibrogenesis and Tissue Repair 1, 5.Google Scholar
Paiva, C. N., Feijó, D. F., Dutra, F. F., Carneiro, V. C., Freitas, G. B., Alves, L. S., Mesquita, J., Fortes, G. B., Figueiredo, R. T., Fantappiè, M. R., Lannes-Vieira, J. and Bozza, M. T. (2012). Oxidative stress fuels Trypanosoma cruzi infection in mice. Journal of Clinical Investigation 122, 2531–2542.Google Scholar
Peloso, E. F., Vitor, S. C., Ribeiro, L. H. G., Piñeyro, M. D., Robello, C. and Gadelha, F. R. (2011). Role of Trypanosoma cruzi peroxiredoxins in mitochondrial bioenergetics. Journal of Bioenergetics and Biomembranes 43, 419–424.Google Scholar
Peloso, E. F., Gonçalves, C. C., Silva, T. M., Ribeiro, L. H. G., Piñeyro, M. D., Robello, C. and Gadelha, F. R. (2012). Tryparedoxin peroxidases and superoxide dismutases expression as well as ROS release are related to Trypanosoma cruzi epimastigotes growth phases. Archives of Biochemistry and Biophysics 520, 117–122.Google Scholar
Piacenza, L., Alvarez, M. N., Peluffo, G. and Radi, R. (2009 a). Fighting the oxidative assault: the Trypanosoma cruzi journey to infection. Current Opinion in Microbiology 12, 415–421.Google Scholar
Piacenza, L., Zago, M. P., Peluffo, G., Alvarez, M. N., Basombrio, M. A. and Radi, R. (2009 b). Enzymes of the antioxidant network as novel determiners of Trypanosoma cruzi virulence. International Journal for Parasitology 39, 1455–1464.Google Scholar
Picardo, M., Grammatico, P., Roccella, F., Roccella, M., Grandinetti, M., Porto, G. and Passi, S. (1996). Imbalance in the antioxidant pool in melanoma cells and normal melanocytes from patients with melanoma. Journal of Investigative Dermatology 107, 322–326.Google Scholar
Piñeyro, M. D., Parodi-Talice, A., Arcari, T. and Robello, C. (2008). Peroxiredoxins from Trypanosoma cruzi: virulence factors and drug targets for treatment of Chagas disease? Gene 408, 45–50.Google Scholar
Piñeyro, M. D., Arcari, T., Robello, C., Radi, R. and Trujillo, M. (2011). Tryparedoxin peroxidases from Trypanosoma cruzi: high efficiency in the catalytic elimination of hydrogen peroxide and peroxynitrite. Archives of Biochemistry and Biophysics 507, 287–295.Google Scholar
Rhee, S. G., Bae, Y. S., Lee, S. R. and Kwon, J. (2000). Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Science's STKE 53, pe1.Google Scholar
Sen, S., Kawahara, B. and Chaudhuri, G. (2012). Maintenance of higher H2O2 levels, and its mechanism of action to induce growth in breast cancer cells: important roles of bioactive catalase and PP2A. Free Radical Biology and Medicine 53, 1541–1551.Google Scholar
Setoyama, D., Ito, R., Takagi, Y. and Sekiguchi, M. (2011). Molecular actions of Escherichia coli MutT for control of spontaneous mutagenesis. Mutation Research – Fundamental and Molecular Mechanisms of Mutagenesis 707, 9–14.CrossRefGoogle ScholarPubMed
Simpson, L., Simpson, A. M., Kidane, G., Livingston, L. and Spithill, T. W. (1980). The kinetoplast DNA of the hemoflagellate protozoa. American Journal of Tropical Medicine and Hygiene 29, 1053–1063.Google Scholar
Simpson, A. G. B., Stevens, J. R. and Lukeš, J. (2006). The evolution and diversity of kinetoplastid flagellates. Trends in Parasitology 22, 168–174.Google Scholar
Stevens, J. R. (2008). Kinetoplastid phylogenetics, with special reference to the evolution of parasitic trypanosomes. Parasite 15, 226–232.Google Scholar
Subapriya, R., Kumaraguruparan, R., Ramachandran, C. R. and Nagini, S. (2002). Oxidant-antioxidant status in patients with oral squamous cell carcinomas at different intraoral sites. Clinical Biochemistry 35, 489–493.CrossRefGoogle ScholarPubMed
Sundaresan, M., Yu, Z. X., Ferrans, V. J., Irani, K. and Finkel, T. (1995). Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270, 296–299.CrossRefGoogle ScholarPubMed
Villagrán, M. E., Marín, C., Rodríguez-González, I., De Diego, J. A. and Sánchez-Moreno, M. (2005). Use of a iron superoxide dismutase dismutase excreted by Trypanosoma cruzi in the diagnosis of Chagas disease: seroprevalence in rural zones of the state of Queretaro, Mexico. American Journal of Tropical Medicine and Hygiene 73, 510–516.CrossRefGoogle ScholarPubMed
Von Ossowski, I., Mulvey, M. R., Leco, P. A., Borys, A. and Loewen, P. C. (1991). Nucleotide sequence of Escherichia coli katE, which encodes catalase HPII. Journal of Bacteriology 173, 514–520.Google Scholar
Wallace, D. C. (2005). A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annual Reviews of Genetics 39, 359–407.Google Scholar
Wiese, A. G., Pacifici, R. E. and Davies, K. J. (1995). Transient adaptation of oxidative stress in mammalian cells. Archives of Biochemistry and Biophysics 318, 231–240.Google Scholar
Wilkinson, S. R., Temperton, N. J., Mondragon, A. and Kelly, J. M. (2000). Distinct mitochondrial and cytosolic enzymes mediate trypanothione-dependent peroxide metabolism in Trypanosoma cruzi . Journal of Biological Chemistry 275, 8220–8225.Google Scholar
Wilkinson, S. R., Obado, S. O., Mauricio, I. L. and Kelly, J. M. (2002 a). Trypanosoma cruzi expresses a plant-like ascorbate-dependent hemoperoxidase localized to the endoplasmic reticulum. Proceedings of the National Academy of Sciences of the United States of America 99, 13453–13458.Google Scholar
Wilkinson, S. R., Meyer, D. J., Taylor, M. C., Bromley, E. V., Miles, M. A. and Kelly, J. M. (2002 b). The Trypanosoma cruzi enzyme TcGPXI is a glycosomal peroxidase and can be linked to trypanothione reduction by glutathione or tryparedoxin. Journal of Biological Chemistry 277, 17062–17071.Google Scholar
Wilkinson, S. R., Taylor, M. C., Touitha, S., Mauricio, I. L., Meyer, D. J. and Kelly, J. M. (2002 c). TcGPXII, a glutathione-dependent Trypanosoma cruzi peroxidase with substrate specificity restricted to fatty acid and phospholipid hydroperoxides, is localized to the endoplasmic reticulum. Biochemical Journal 364, 787–794.Google Scholar
Wilson, M. E., Andersen, K. A. and Britigan, B. E. (1994). Response of Leishmania chagasi promastigotes to oxidant stress. Infection and Immunity 62, 5133–5141.Google Scholar
Winterbourn, C. C. (2008). Reconciling the chemistry and biology of reactive oxygen species. Nature Chemical Biology 4, 278–286.Google Scholar
Yoo, D. G., Song, Y. J., Cho, E. J., Lee, S. K., Park, J. B., Yu, J. H., Lim, S. P., Kim, J. M. and Jeon, B. H. (2008). Alteration of APE1/ref-1 expression in non-small cell lung cancer: the implications of impaired extracellular superoxide dismutase and catalase antioxidant systems. Lung Cancer 60, 277–284.Google Scholar