Peroxynitrite, a potent macrophage-derived oxidizing cytotoxin to combat invading pathogens

BioFactors

Volumn 40, Issue 2, 2014, Pages 215-225

  Prolo, Carolina ^a   Álvarez, María Noel ^a   Radi, Rafael ^a  

^a DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

Author keywords

Free radicals; Nitric oxide; Oxidants; Peroxynitrite; Superoxide

Indexed keywords

PEROXYNITROUS ACID;

ANIMAL; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; MACROPHAGE; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PHAGOCYTOSIS; PHAGOSOME; PHYSIOLOGY;

ANIMALS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; MACROPHAGES; OXIDATION-REDUCTION; PEROXYNITROUS ACID; PHAGOCYTOSIS; PHAGOSOMES;

EID: 84899092424     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.1150     Document Type: Review

References (92)

1. Murray, P. J. and Wynn, T. A. (2011) Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11, 723-737.
2. O'Garra, A. and Arai, N. (2000) The molecular basis of T helper 1 and T helper 2 cell differentiation. Trends Cell Biol. 10, 542-550.
3. Kleinert, H., Pautz, A., Linker, K., and Schwarz, P. M. (2004) Regulation of the expression of inducible nitric oxide synthase. Eur. J. Pharmacol. 500, 255-266.
4. Coccia, E. M., Stellacci, E., Marziali, G., Weiss, G., and Battistini, A. (2000) IFN-gamma and IL-4 differently regulate inducible NO synthase gene expression through IRF-1 modulation. Int. Immunol. 12, 977-985.
5. Bogdan, C., Thuring, H., Dlaska, M., Rollinghoff, M., and Weiss, G. (1997) Mechanism of suppression of macrophage nitric oxide release by IL-13: influence of the macrophage population. J. Immunol. 159, 4506-4513.
6. Schroder, K., Hertzog, P. J., Ravasi, T., and Hume, D. A. (2004) Interferon-gamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 75, 163-189.
7. Rottenberg, M. E., Castanos-Velez, E., de Mesquita, R., Laguardia, O. G., Biberfeld, P., and Orn, A. (1996) Intracellular co-localization of Trypanosoma cruzi and inducible nitric oxide synthase (iNOS): evidence for dual pathway of iNOS induction. Eur. J. Immunol. 26, 3203-3213.
8. Oliveira, A. C., de Alencar, B. C., Tzelepis, F., Klezewsky, W., da Silva, R. N., Neves, F. S., Cavalcanti, G. S., Boscardin, S., Nunes, M. P., Santiago, M. F., Nobrega, A., Rodrigues, M. M., and Bellio, M. (2010) Impaired innate immunity in Tlr4(-/-) mice but preserved CD8+ T cell responses against Trypanosoma cruzi in Tlr4-, Tlr2-, Tlr9- or Myd88-deficient mice. PLoS Pathog. 6, e1000870.
9. Ischiropoulos, H., Zhu, L., and Beckman, J. S. (1992) Peroxynitrite formation from macrophage-derived nitric oxide. Arch. Biochem. Biophys. 298, 446-451.
10. Alvarez, M. N., Trujillo, M., and Radi, R. (2002) Peroxynitrite formation from biochemical and cellular fluxes of nitric oxide and superoxide, Methods Enzymol. 359, 353-366.
11. Vodovotz, Y., Russell, D., Xie, Q. W., Bogdan, C., and Nathan, C. (1995) Vesicle membrane association of nitric oxide synthase in primary mouse macrophages. J. Immunol. 154, 2914-2925.
12. Moller, M., Botti, H., Batthyany, C., Rubbo, H., Radi, R., and Denicola, A. (2005) Direct measurement of nitric oxide and oxygen partitioning into liposomes and low density lipoprotein. J. Biol. Chem. 280, 8850-8854.
13. Stuehr, D. J., Gross, S. S., Sakuma, I., Levi, R., and Nathan, C. F. (1989) Activated murine macrophages secrete a metabolite of arginine with the bioactivity of endothelium-derived relaxing factor and the chemical reactivity of nitric oxide. J. Exp. Med. 169, 1011-1020.
14. Bredt, D. S. and Snyder, S. H. (1994) Nitric oxide: a physiologic messenger molecule. Annu. Rev. Biochem. 63, 175-195.
15. Hill, B. G., Dranka, B. P., Bailey, S. M., Lancaster, J. R., Jr., and Darley-Usmar, V. M. (2010) What part of NO don't you understand? Some answers to the cardinal questions in nitric oxide biology. J. Biol. Chem. 285, 19699-19704.
16. Babior, B. M. (1995) The respiratory burst oxidase. Curr. Opin. Hematol. 2, 55-60.
17. El-Benna, J., Dang, P. M., and Gougerot-Pocidalo, M. A. (2008) Priming of the neutrophil NADPH oxidase activation: role of p47phox phosphorylation and NOX2 mobilization to the plasma membrane. Semin. Immunopathol. 30, 279-289.
18. Singh, A., Zarember, K. A., Kuhns, D. B., and Gallin, J. I. (2009) Impaired priming and activation of the neutrophil NADPH oxidase in patients with IRAK4 or NEMO deficiency. J. Immunol. 182, 6410-6417.
19. Ferrer-Sueta, G. and Radi, R. (2009) Chemical biology of peroxynitrite: kinetics, diffusion, and radicals. ACS Chem. Biol. 4, 161-177.
20. Quijano, C., Alvarez, B., Gatti, R. M., Augusto, O., and Radi, R. (1997) Pathways of peroxynitrite oxidation of thiol groups. Biochem. J. 322 (Pt 1), 167-173.
21. Radi, R., Beckman, J. S., Bush, K. M., and Freeman, B. A. (1991) Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J. Biol. Chem. 266, 4244-4250.
22. Castro, L., Rodriguez, M., and Radi, R. (1994) Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide. J. Biol. Chem. 269, 29409-29415.
23. Carballal, S., Bartesaghi, S., and Radi, R. (2013) Kinetic and mechanistic considerations to assess the biological fate of peroxynitrite. Biochim. Biophys. Acta. doi:10.1016/j.bbagen.2013.07.005. [Epub ahead of print]
24. Souza, J. M. and Radi, R. (1998) Glyceraldehyde-3-phosphate dehydrogenase inactivation by peroxynitrite. Arch. Biochem. Biophys. 360, 187-194.
25. Rubbo, H., Denicola, A., and Radi, R. (1994) Peroxynitrite inactivates thiol-containing enzymes of Trypanosoma cruzi energetic metabolism and inhibits cell respiration. Arch. Biochem. Biophys. 308, 96-102.
26. Augusto, O., Gatti, R. M., and Radi, R. (1994) Spin-trapping studies of peroxynitrite decomposition and of 3-morpholinosydnonimine N-ethylcarbamide autooxidation: direct evidence for metal-independent formation of free radical intermediates. Arch. Biochem. Biophys. 310, 118-125.
27. Beckman, J. S., Beckman, T. W., Chen, J., Marshall, P. A., and Freeman, B. A. (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 87, 1620-1624.
28. Radi, R. (1998) Peroxynitrite reactions and diffusion in biology. Chem. Res. Toxicol. 11, 720-721.
29. Denicola, A., Freeman, B. A., Trujillo, M., and Radi, R. (1996) Peroxynitrite reaction with carbon dioxide/bicarbonate: kinetics and influence on peroxynitrite-mediated oxidations. Arch. Biochem. Biophys. 333, 49-58.
30. Brennan, M. L., Wu, W., Fu, X., Shen, Z., Song, W., Frost, H., Vadseth, C., Narine, L., Lenkiewicz, E., Borchers, M. T., Lusis, A. J., Lee, J. J., Lee, N. A., Abu-Soud, H. M., Ischiropoulos, H., and Hazen, S. L. (2002) A tale of two controversies: defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species. J. Biol. Chem. 277, 17415-17427.
31. Hurst, J. K. (2012) What really happens in the neutrophil phagosome? Free Radic. Biol. Med. 53, 508-520.
32. van der Vliet, A., Eiserich, J. P., Halliwell, B., and Cross, C. E. (1997) Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite. A potential additional mechanism of nitric oxide-dependent toxicity. J. Biol. Chem. 272, 7617-7625.
33. Brovkovych, V., Gao, X. P., Ong, E., Brovkovych, S., Brennan, M. L., Su, X., Hazen, S. L., Malik, A. B., and Skidgel, R. A. (2008) Augmented inducible nitric oxide synthase expression and increased NO production reduce sepsis-induced lung injury and mortality in myeloperoxidase-null mice. Am. J. Physiol. Lung Cell Mol. Physiol. 295, L96-L103.
34. Zhang, R., Brennan, M. L., Shen, Z., MacPherson, J. C., Schmitt, D., Molenda, C. E., and Hazen, S. L. (2002) Myeloperoxidase functions as a major enzymatic catalyst for initiation of lipid peroxidation at sites of inflammation. J. Biol. Chem. 277, 46116-46122.
35. Evans, T. J., Buttery, L. D., Carpenter, A., Springall, D. R., Polak, J. M., and Cohen, J. (1996) Cytokine-treated human neutrophils contain inducible nitric oxide synthase that produces nitration of ingested bacteria. Proc. Natl. Acad. Sci. USA 93, 9553-9558.
36. Pfeiffer, S., Lass, A., Schmidt, K., and Mayer, B. (2001) Protein tyrosine nitration in cytokine-activated murine macrophages. Involvement of a peroxidase/nitrite pathway rather than peroxynitrite. J. Biol. Chem. 276, 34051-34058.
37. Pfeiffer, S., Lass, A., Schmidt, K., and Mayer, B. (2001) Protein tyrosine nitration in mouse peritoneal macrophages activated in vitro and in vivo: evidence against an essential role of peroxynitrite. FASEB J. 15, 2355-2364.
38. 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. J. Biol. Chem. 286, 6627-6640.
39. Gookin, J. L., Allen, J., Chiang, S., Duckett, L., and Armstrong, M. U. (2005) Local peroxynitrite formation contributes to early control of Cryptosporidium parvum infection. Infect. Immun. 73, 3929-3936.
40. Giorgio, S., Linares, E., Ischiropoulos, H., Von Zuben, F. J., Yamada, A., and Augusto, O. (1998) In vivo formation of electron paramagnetic resonance-detectable nitric oxide and of nitrotyrosine is not impaired during murine leishmaniasis. Infect. Immun. 66, 807-814.
41. Linares, E., Giorgio, S., Mortara, R. A., Santos, C. X., Yamada, A. T., and Augusto, O. (2001) Role of peroxynitrite in macrophage microbicidal mechanisms in vivo revealed by protein nitration and hydroxylation. Free Radic. Biol. Med. 30, 1234-1242.
42. Quijano, C., Romero, N., and Radi, R. (2005) Tyrosine nitration by superoxide and nitric oxide fluxes in biological systems: modeling the impact of superoxide dismutase and nitric oxide diffusion. Free Radic. Biol. Med. 39, 728-741.
43. Trostchansky, A. and Rubbo, H. (2008) Nitrated fatty acids: mechanisms of formation, chemical characterization, and biological properties. Free Radic. Biol. Med. 44, 1887-1896.
44. Trostchansky, A., Bonilla, L., Gonzalez-Perilli, L., and Rubbo, H. (2012) Nitro-fatty acids: formation, redox signaling, and therapeutic potential. Antioxid. Redox Signal. 19, 1257-1265.
45. Gonzalez-Perilli, L., Alvarez, M. N., Prolo, C., Radi, R., Rubbo, H., and Trostchansky, A. (2013) Nitroarachidonic acid prevents NADPH oxidase assembly and superoxide radical production in activated macrophages. Free Radic. Biol. Med. 58, 126-133.
46. Brunelli, L., Crow, J. P., and Beckman, J. S. (1995) The comparative toxicity of nitric oxide and peroxynitrite to Escherichia coli. Arch. Biochem. Biophys. 316, 327-334.
47. Zhu, L., Gunn, C., and Beckman, J. S. (1992) Bactericidal activity of peroxynitrite. Arch. Biochem. Biophys. 298, 452-457.
48. McLean, S., Bowman, L. A., Sanguinetti, G., Read, R. C., and Poole, R. K. (2010) Peroxynitrite toxicity in Escherichia coli K12 elicits expression of oxidative stress responses and protein nitration and nitrosylation. J. Biol. Chem. 285, 20724-20731.
49. De Groote, M. A., Ochsner, U. A., Shiloh, M. U., Nathan, C., McCord, J. M., Dinauer, M. C., Libby, S. J., Vazquez-Torres, A., Xu, Y., and Fang, F. C. (1997) Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc. Natl. Acad. Sci. USA 94, 13997-14001.
50. Shiloh, M. U., MacMicking, J. D., Nicholson, S., Brause, J. E., Potter, S., Marino, M., Fang, F., Dinauer, M., and Nathan, C. (1999) Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 10, 29-38.
51. Jiang, X., Leonard, B., Benson, R., and Baldwin, C. L. (1993) Macrophage control of Brucella abortus: role of reactive oxygen intermediates and nitric oxide. Cell Immunol. 151, 309-319.
52. Ko, J., Gendron-Fitzpatrick, A., and Splitter, G. A. (2002) Susceptibility of IFN regulatory factor-1 and IFN consensus sequence binding protein-deficient mice to brucellosis. J. Immunol. 168, 2433-2440.
53. Hickman-Davis, J., Gibbs-Erwin, J., Lindsey, J. R., and Matalon, S. (1999) Surfactant protein A mediates mycoplasmacidal activity of alveolar macrophages by production of peroxynitrite. Proc. Natl. Acad. Sci. USA 96, 4953-4958.
54. Darrah, P. A., Hondalus, M. K., Chen, Q., Ischiropoulos, H., and Mosser, D. M. (2000) Cooperation between reactive oxygen and nitrogen intermediates in killing of Rhodococcus equi by activated macrophages. Infect. Immun. 68, 3587-3593.
55. Bose, M., Saha, R., Sen Santara, S., Mukherjee, S., Roy, J., and Adak, S. (2012) Protection against peroxynitrite by pseudoperoxidase from Leishmania major. Free Radic. Biol. Med. 53, 1819-1828.
56. Murray, H. W. and Nathan, C. F. (1999) Macrophage microbicidal mechanisms in vivo: reactive nitrogen versus oxygen intermediates in the killing of intracellular visceral Leishmania donovani. J. Exp. Med. 189, 741-746.
57. Barr, S. D. and Gedamu, L. (2003) Role of peroxidoxins in Leishmania chagasi survival. Evidence of an enzymatic defense against nitrosative stress. J. Biol. Chem. 278, 10816-10823.
58. Padalko, E., Ohnishi, T., Matsushita, K., Sun, H., Fox-Talbot, K., Bao, C., Baldwin, W. M. III, and Lowenstein, C. J. (2004) Peroxynitrite inhibition of Coxsackievirus infection by prevention of viral RNA entry. Proc. Natl. Acad. Sci. USA 101, 11731-11736.
59. Vazquez-Torres, A., Jones-Carson, J., and Balish, E. (1996) Peroxynitrite contributes to the candidacidal activity of nitric oxide-producing macrophages. Infect. Immun. 64, 3127-3133.
60. Thomas, G. R., McCrossan, M., and Selkirk, M. E. (1997) Cytostatic and cytotoxic effects of activated macrophages and nitric oxide donors on Brugia malayi. Infect. Immun. 65, 2732-2739.
61. Gupta, R., Bajpai, P., Tripathi, L. M., Srivastava, V. M., Jain, S. K., and Misra-Bhattacharya, S. (2004) Macrophages in the development of protective immunity against experimental Brugia malayi infection. Parasitology 129, 311-323.
62. Brito, C., Naviliat, M., Tiscornia, A. C., Vuillier, F., Gualco, G., Dighiero, G., Radi, R., and Cayota, A. M. (1999) Peroxynitrite inhibits T lymphocyte activation and proliferation by promoting impairment of tyrosine phosphorylation and peroxynitrite-driven apoptotic death. J. Immunol. 162, 3356-3366.
63. Nicholson, S., Bonecini-Almeida Mda, G., Lapa e Silva, J. R., Nathan, C., Xie, Q. W., Mumford, R., Weidner, J. R., Calaycay, J., Geng, J., Boechat, N., Linhares, C., Rom, W., and Ho, J. L. (1996) Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J. Exp. Med. 183, 2293-2302.
64. Choi, H. S., Rai, P. R., Chu, H. W., Cool, C., and Chan, E. D. (2002) Analysis of nitric oxide synthase and nitrotyrosine expression in human pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 166, 178-186.
65. Wang, C. H., Liu, C. Y., Lin, H. C., Yu, C. T., Chung, K. F., and Kuo, H. P. (1998) Increased exhaled nitric oxide in active pulmonary tuberculosis due to inducible NO synthase upregulation in alveolar macrophages. Eur. Respir. J. 11, 809-815.
66. Nathan, C. (2002) Inducible nitric oxide synthase in the tuberculous human lung. Am. J. Respir. Crit. Care Med. 166, 130-131.
67. Vieira, O. V., Botelho, R. J., and Grinstein, S. (2002) Phagosome maturation: aging gracefully. Biochem. J. 366, 689-704.
68. Denicola, A., Souza, J. M., and Radi, R. (1998) Diffusion of peroxynitrite across erythrocyte membranes. Proc. Natl. Acad. Sci. USA 95, 3566-3571.
69. Alvarez, M. N., Piacenza, L., Irigoin, F., Peluffo, G., and Radi, R. (2004) Macrophage-derived peroxynitrite diffusion and toxicity to Trypanosoma cruzi. Arch. Biochem. Biophys. 432, 222-232.
70. Cape, J. L. and Hurst, J. K. (2009) The role of nitrite ion in phagocyte function-perspectives and puzzles. Arch. Biochem. Biophys. 484, 190-196.
71. Lodge, R., Diallo, T. O., and Descoteaux, A. (2006) Leishmania donovani lipophosphoglycan blocks NADPH oxidase assembly at the phagosome membrane. Cell Microbiol. 8, 1922-1931.
72. Vazquez-Torres, A., Xu, Y., Jones-Carson, J., Holden, D. W., Lucia, S. M., Dinauer, M. C., Mastroeni, P., and Fang, F. C. (2000) Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287, 1655-1658.
73. Cao, W., Bao, C., and Lowenstein, C. J. (2003) Inducible nitric oxide synthase expression inhibition by adenovirus E1A. Proc. Natl. Acad. Sci USA 100, 7773-7778.
74. Seabra, S. H., de Souza, W., and Damatta, R. A. (2004) Toxoplasma gondii exposes phosphatidylserine inducing a TGF-beta1 autocrine effect orchestrating macrophage evasion. Biochem. Biophys. Res. Commun. 324, 744-752.
75. Balestieri, F. M., Queiroz, A. R., Scavone, C., Costa, V. M., Barral-Netto, M., and Abrahamsohn Ide, A. (2002) Leishmania (L.) amazonensis-induced inhibition of nitric oxide synthesis in host macrophages. Microbes. Infect. 4, 23-29.
76. Das, P., Lahiri, A., and Chakravortty, D. (2010) Modulation of the arginase pathway in the context of microbial pathogenesis: a metabolic enzyme moonlighting as an immune modulator. PLoS Pathog. 6, e1000899.
77. Lewis, N. D., Asim, M., Barry, D. P., de Sablet, T., Singh, K., Piazuelo, M. B., Gobert, A. P., Chaturvedi, R., and Wilson, K. T. (2011) Immune evasion by Helicobacter pylori is mediated by induction of macrophage arginase II. J. Immunol. 186, 3632-3641.
78. Lahiri, A., Das, P., and Chakravortty, D. (2008) Arginase modulates Salmonella induced nitric oxide production in RAW264.7 macrophages and is required for Salmonella pathogenesis in mice model of infection. Microbes Infect. 10, 1166-1174.
79. Couture, M., Yeh, S. R., Wittenberg, B. A., Wittenberg, J. B., Ouellet, Y., Rousseau, D. L., and Guertin, M. (1999) A cooperative oxygen-binding hemoglobin from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 96, 11223-11228.
80. Ouellet, H., Ouellet, Y., Richard, C., Labarre, M., Wittenberg, B., Wittenberg, J., and Guertin, M. (2002) Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide. Proc. Natl. Acad. Sci. USA 99, 5902-5907.
81. Fabozzi, G., Ascenzi, P., Renzi, S. D., and Visca, P. (2006) Truncated hemoglobin GlbO from Mycobacterium leprae alleviates nitric oxide toxicity. Microb. Pathog. 40, 211-220.
82. Gardner, P. R. (2005) Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. J. Inorg. Biochem. 99, 247-266.
83. Piacenza, L., Peluffo, G., Alvarez, M. N., Martinez, A., and Radi, R. (2012) Trypanosoma cruzi antioxidant enzymes as virulence factors in Chagas disease. Antioxid. Redox Signal. 19, 723-734.
84. Piacenza, L., Zago, M. P., Peluffo, G., Alvarez, M. N., Basombrio, M. A., and Radi, R. (2009) Enzymes of the antioxidant network as novel determiners of Trypanosoma cruzi virulence. Int. J. Parasitol. 39, 1455-1464.
85. Daneshvar, H., Wyllie, S., Phillips, S., Hagan, P., and Burchmore, R. (2012) Comparative proteomics profiling of a gentamicin-attenuated Leishmania infantum cell line identifies key changes in parasite thiol-redox metabolism. J. Proteomics 75, 1463-1471.
86. Harder, S., Bente, M., Isermann, K., and Bruchhaus, I. (2006) Expression of a mitochondrial peroxiredoxin prevents programmed cell death in Leishmania donovani. Eukaryot. Cell 5, 861-870.
87. Fridovich, I. (1995) Superoxide radical and superoxide dismutases. Annu. Rev. Biochem. 64, 97-112.
88. Korshunov, S. S. and Imlay, J. A. (2002) A potential role for periplasmic superoxide dismutase in blocking the penetration of external superoxide into the cytosol of gram-negative bacteria. Mol. Microbiol. 43, 95-106.
89. Sanjay, M. K., Srideshikan, S. M., Vanishree, V. L., Usha, M. S., Raj, A. P., Gaddad, S. M., and Shivannavar, C. T. (2011) Copper, zinc-superoxide dismutase from clinically isolated Escherichia coli: cloning, analysis of sodC and its possible role in pathogenicity. Ind. J. Microbiol. 51, 326-331.
90. Fang, F. C., DeGroote, M. A., Foster, J. W., Baumler, A. J., Ochsner, U., Testerman, T., Bearson, S., Giard, J. C., Xu, Y., Campbell, G., and Laessig, T. (1999) Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases. Proc. Natl. Acad. Sci. USA 96, 7502-7507.
91. Mateo, H., Sanchez-Moreno, M., and Marin, C. (2010) Enzyme-linked immunosorbent assay with purified Trypanosoma cruzi excreted superoxide dismutase. Clin. Biochem. 43, 1257-1264.
92. Lopez-Cespedes, A., Longoni, S. S., Sauri-Arceo, C. H., Rodriguez-Vivas, R. I., Villegas, N., Escobedo-Ortegon, J., Barrera-Perez, M. A., Sanchez-Moreno, M., Bolio Gonzalez, M. E., and Marin, C. (2013) Seroprevalence of antibodies against the excreted antigen superoxide dismutase by Trypanosoma cruzi in dogs from the Yucatan Peninsula (Mexico). Zoonoses Public Health 60, 277-283.