Archivum Immunologiae et Therapiae Experimentalis

, Volume 59, Issue 6, pp 441–448 | Cite as

Oxidative and Nitrosative Stress on Phagocytes’ Function: from Effective Defense to Immunity Evasion Mechanisms

  • Carlos K. B. Ferrari
  • Paula C. S. Souto
  • Eduardo L. França
  • Adenilda C. Honorio-França


Although oxygen, nitrogen, and chlorine reactive species have been associated with disease pathogenesis, their partial absence is very harmful to the body’s innate immune defense. Lacking of adequate release of free radicals from activated phagocytes is related to impaired ability on fungi, bacteria, and protozoa killing. We constructed an updated conceptual landmark regarding the paramount role of free radicals in phagocyte defense systems (phagocyte oxidase, myeloperoxidase, and nitric oxide/peroxynitrite system) on natural immunity. Diverse fungal, bacterial and protozoal pathogens evade the phagocytes’ oxidative/nitrosative burst though antioxidant genes, enzymes and proteins. The most important evasion mechanisms were also described and discussed. These interconnected systems were reviewed and discussed on the basis of knowledge from relevant research groups around the globe. Phagocyte-derived free radicals are essential to destroy important human pathogens during the course of innate immunity.


Phagocyte oxidase Macrophage Myeloperoxidase Nitric oxide Peroxynitrite Malaria Candida spp. Mycobacterium tuberculosis Trypanosoma cruzi 


  1. Abegg MA, Alabarse PV, Casanova A et al (2010) Response to oxidative stress in eight pathogenic yeast species of the genus Candida. Mycopathologia 170:11–20PubMedCrossRefGoogle Scholar
  2. Ackerman HC, Beaudry SD, Fairhurst RM (2009) Antioxidant therapy: reducing malaria severity? Crit Care Med 37:758–760PubMedCrossRefGoogle Scholar
  3. Aikawa C, Nozawa T, Maruyama F et al (2010) Reactive oxygen species induced by Streptococcus pyogenes invasion trigger apoptotic cell death in infected epithelial cells. Cell Microbiol 12:814–830PubMedCrossRefGoogle Scholar
  4. Alvarez MN, Peluffo G, Piacenza L et al (2011) Intraphagosomal peroxinitrite as a macrophage-derived cytotoxin against internalized Trypanosoma cruzi. Consequences for oxidative killing and role of microbial peroxiredoxins in infectivity. J Biol Chem 286:6627–6640Google Scholar
  5. Ano Y, Sakudo A, Kimata T et al (2010) Oxidative damage to neurons caused by the induction of microglial NADPH oxidase in encephalomycarditis virus infection. Neurosci Lett 469:39–43PubMedCrossRefGoogle Scholar
  6. Aratani Y, Kura F, Watanabe H et al (2006) Contribution of the myeloperoxidase-dependent oxidative system to host defense against Cryptococcus neoformans. J Med Microbiol 55(Pt 9):1291–1299PubMedCrossRefGoogle Scholar
  7. Balishi E, Warner TF, Nicholas PJ et al (2005) Susceptibility of germfree phagocyte oxidase- and nitric oxide synthase 2-deficient mice, defective in the production of reactive metabolites of both oxygen and nitrogen, to mucosal and systemic candidiasis of endogenous origin. Infect Immun 73:1313–1320CrossRefGoogle Scholar
  8. Balmer P, Phillips HM, Maestre AE et al (2000) The effect of nitric oxide on the growth of Plasmodium falciparum, P. chabaudi and P. berghei in vitro. Parasite Immunol 22:97–106PubMedCrossRefGoogle Scholar
  9. Barth KR, Isabella VM, Wright LF et al (2009) Resistance to peroxynitrite in Neisseria gonorhoeae. Microbiology 155(Pt 8):2532–2545PubMedCrossRefGoogle Scholar
  10. Bastos KRB, Barboza R, Elias RM et al (2002) Impaired macrophages responses may contribute to exacerbation of blood-stage Plasmodium chabaudi malaria in interleukin-12-deficient mice. J Interferon Cytokine Res 22:1191–1199PubMedCrossRefGoogle Scholar
  11. Biesalski HK, Grune T, Tinz J et al (2010) Reexamination of meta-analysis of the effect of antioxidant supplementation on mortality and health in randomized trials. Nutrients 2:929–949CrossRefGoogle Scholar
  12. Boncompain G, Schneider B, Delevoye C et al (2010) Production of reactive oxygen species is turned on and rapidly shut down in epithelial cells infected with Chlamydia trachomatis. Infect Immun 78:80–87PubMedCrossRefGoogle Scholar
  13. Boutlis CS, Tjitra E, Maniboey H et al (2003) Nitric oxide production and mononuclear cell nitric oxide synthase activity in malaria-tolerant Papuan adults. Infect Immun 71:3682–3689PubMedCrossRefGoogle Scholar
  14. Brovkovych V, Gao X-P, Ong E et al (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–L103PubMedCrossRefGoogle Scholar
  15. Bryk R, Griffin P, Nathan C (2000) Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407:211–215PubMedCrossRefGoogle Scholar
  16. Cao W, Baniecki ML, McGrath WJ et al (2003) Nitric oxide inhibits the adenovirus proteinase in vitro and viral infectivity in vivo. FASEB J 17:2345–2346PubMedGoogle Scholar
  17. Cardinale JA, Clark VL (2005) Determinants of nitric oxide steady-state levels during anaerobic respiration by Neisseria gonorhoeae. Mol Microbiol 58:177–188PubMedCrossRefGoogle Scholar
  18. Charunwatthana P, Faiz MA, Ruangveerayut R et al (2009) N-acetylcysteine as adjunctive treatment in severe malaria: a randomized double blinded placebo controlled clinical trial. Crit Care Med 37:516–522PubMedCrossRefGoogle Scholar
  19. Chen J, Fontes G, Saxena G et al (2010) Lack of TXNIP protects against mitochondria-mediated apoptosis but not against fatty acid-induced ER stress-mediated beta cell death. Diabetes 59:440–447PubMedCrossRefGoogle Scholar
  20. Chokshi NK, Guner YS, Hunter CJ et al (2008) The role of nitric oxide in intestinal epithelial injury and restitution in neonatal necrotizing enterocolitis. Semin Perinatol 32:92–99PubMedCrossRefGoogle Scholar
  21. Chuang MH, Wu MS, Lo WL et al (2006) The antioxidant protein alkylhydroperoxide reductase of Helicobacter pylori switches from a peroxide reductase to a molecular chaperone function. Proc Natl Acad Sci USA 103:2552–2557PubMedCrossRefGoogle Scholar
  22. Colasanti M, Gradoni L, Mattu M et al (2002) Molecular basis for the anti-parasitic effect of NO. Int J Mol Med 9:131–134PubMedGoogle Scholar
  23. Cosgrove K, Coutts G, Jonsson IM et al (2007) Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory role in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J Bacteriol 189:1025–1035PubMedCrossRefGoogle Scholar
  24. Craig M, Slauch JM (2009) Phagocytic superoxide specifically damages an extracytoplasmic target to inhibit or kill Salmonella. PLoS One 4:e4975PubMedCrossRefGoogle Scholar
  25. De Palma C, Falcone S, Panzeri C et al (2008) Endothelial nitric oxide synthase overexpression by neuronal cells in neurodegeneration: a link between inflammation and protection. J Neurochem 106:193–204PubMedCrossRefGoogle Scholar
  26. De Souza K, Silva MS, Tavira LT (2008) Variation of nitric oxide levels in imported Plasmodium falciparum malaria episodes. Afr J Biotechnol 7:796–799Google Scholar
  27. Divangahi M, Chen M, Gan H et al (2009) Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat Immunol 10:899–906PubMedCrossRefGoogle Scholar
  28. Escorza MA, Salinas JV (2009) La capacidad antioxidante total. Bases y aplicaciones. REB 28:89–101Google Scholar
  29. Ferrari CK, França EL, Honorio-França AC (2009) Nitric oxide, health and disease. J Appl Biomed 7:163–173Google Scholar
  30. França EL, Feliciano ND, Silva KA et al (2009) Modulatory role of melatonin on superoxide release by spleen macrophages isolated from alloxan-induced diabetic rats. Bratisl Lek Listy 110:517–522PubMedGoogle Scholar
  31. França-Botelho AC, França EL, Honório-França AC et al (2006) Phagocytosis of Giardia lamblia trophozoites by human colostral leucocytes. Acta Paediatr 95:438–443PubMedCrossRefGoogle Scholar
  32. França-Botelho AC, França JL, França EL et al (2010) Relationship between oxidative stress production and virulence capacity of Entamoeba strains. Res J Parasitol 5:139–147CrossRefGoogle Scholar
  33. Gabbay E, Zigmond E, Pappo O et al (2007) Antioxidant therapy for chronic hepatitis C after failure of interferon: results of phase II randomized, double-blind placebo controlled clinical trial. World J Gastroenterol 13:5317–5323PubMedGoogle Scholar
  34. Gan H, Lee J, Ren F et al (2008) Mycobacterium tuberculosis blocks crosslinking of annexin-1 and apoptotic envelope formation on infected macrophages to maintain virulence. Nat Immunol 9:1189–1197PubMedCrossRefGoogle Scholar
  35. Garnica MR, Silva JS, Andrade HF Jr (2003) Stromal cell-derived factor-1 production by spleen cells is affected by nitric oxide in protective immunity against blood-stage Plasmodium chabaudi CR in C57BL/6j mice. Immunol Lett 89:133–142PubMedCrossRefGoogle Scholar
  36. Gondwe EN, Molyneux ME, Goodall M et al (2010) Importance of antibody and complement for oxidative burst and killing of invasive nontyphoidal Salmonella by blood cells in Africans. Proc Natl Acad Sci USA 107:3070–3075PubMedCrossRefGoogle Scholar
  37. Gozalo AS, Hofmann VJ, Brinster LR et al (2010) Spontaneous Staphylococcus xylosus infection in mice deficient in NADPH oxidase and comparison with other laboratory mouse strains. J Am Assoc Lab Anim Sci 49:480–486PubMedGoogle Scholar
  38. Gramaglia I, Sobolewski P, Meays D et al (2006) Low nitric oxide bioavailability contributes to the genesis of experimental cerebral malaria. Nat Med 12:1417–1422PubMedCrossRefGoogle Scholar
  39. Gutierrez FR, Mineo TW, Pavanelli WR et al (2009) The effects of nitric oxide on the immune system during Trypanosoma cruzi infection. Mem Inst Oswaldo Cruz 104(suppl1):236–245PubMedCrossRefGoogle Scholar
  40. Gyurko R, Boustany G, Huang PL et al (2003) Mice lacking inducible nitric oxide synthase demonstrate impaired killing of Porphyromonas gingivalis. Infect Immun 71:4917–4924PubMedCrossRefGoogle Scholar
  41. Hall CJ, Bouhafs L, Dizcfalusy U et al (2010) Cryptococcus neoformans causes lipid peroxidation; therefore it is a potential inducer of atherogenesis. Mycologia 102:546–551PubMedCrossRefGoogle Scholar
  42. Hashida S, Yuzawa S, Suzuki NN et al (2004) Binding of FAD to cytochrome b558 is facilitated during activation of the phagocyte NADPH Oxidase, leading to superoxide production. J Biol Chem 279:26378–26386PubMedCrossRefGoogle Scholar
  43. Hii CS, Ferrante A (2007) Regulation of the NADPH oxidase activity and anti-microbial function of neutrophils by arachidonic acid. Arch Immunol Ther Exp 55:99–110CrossRefGoogle Scholar
  44. Hill J, Samuel JE (2011) Coxiella burnetii acid phosphatase: inhibiting the release of reactive oxygen intermediates in polymorphonuclear leukocytes. Infect Immun 79:414–420PubMedCrossRefGoogle Scholar
  45. Hinchey J, Lee S, Jeon BY et al (2007) Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis. J Clin Invest 117:2279–2288PubMedCrossRefGoogle Scholar
  46. Holland SM (2010) Chronic granulomatous disease. Clin Rev Allergy Immunol 38:3–10PubMedCrossRefGoogle Scholar
  47. Hölscher C, Köhler G, Müller U et al (1998) Defective nitric oxide effector functions lead to extreme susceptibility of Trypanosoma cruzi-infected mice deficient in gamma interferon receptor or inducible nitric oxide synthase. Infect Immun 66:1208–1215PubMedGoogle Scholar
  48. Izuhara K, Kanaji S, Arima K et al (2008) Involvement of cysteine protease inhibitors in the defense mechanism against parasites. Med Chem 4:322–327PubMedCrossRefGoogle Scholar
  49. Kim B, Richards SM, Gunn JS et al (2010) Protecting against antimicrobial effectors in the phagosome allows SODCII to contribute to virulence in Salmonella enterica serovar Typhimurium. J Bacteriol 192:2140–2149PubMedCrossRefGoogle Scholar
  50. Klebanoff SJ (2005) Myeloperoxidase: friend and foe. J Leukoc Biol 77:598–625PubMedCrossRefGoogle Scholar
  51. Knapp KG, Swartz JR (2007) Evidence for an additional disulphide reduction pathway in Escherichia coli. J Biosci Bioeng 103:373–376PubMedCrossRefGoogle Scholar
  52. La Carbona S, Savageot N, Giard JC et al (2007) Comparative study of the physiological roles of three peroxidases (NADH peroxidase, alkyl hydroperoxide reductase, and thiol peroxidase) in oxidative stress response, survival inside macrophages and virulence of Enterococcus faecalis. Mol Microbiol 66:1148–1163PubMedCrossRefGoogle Scholar
  53. Lakshmi VM, Nauseef WM, Zenser TV (2005) Myeloperoxidase potentiates nitric oxide-mediated nitrosation. J Biol Chem 280:1746–1753PubMedCrossRefGoogle Scholar
  54. Laver JR, Stevanin TM, Messenger SL et al (2010) Bacterial nitric oxide detoxification prevents host cell S-nitrosothiol formation: a novel mechanism of bacterial pathogenesis. FASEB J 24:286–295PubMedCrossRefGoogle Scholar
  55. LeBlanc JJ, Davidson RJ, Hoffman PS (2006) Compensatory functions of two alkyl hydroperoxide reductases in the oxidative defense system of Legionella pneumophila. J Bacteriol 188:6235–6244PubMedCrossRefGoogle Scholar
  56. Lechardeur D, Fernandez A, Robert B et al (2010) The 2-cys peroxiredoxin alkyl hydroperoxide reductase C binds heme and participates in its availability in Streptococcus agalactiae. J Biol Chem 285:16032–16041PubMedCrossRefGoogle Scholar
  57. Lee E, Oh SH, Kwon JW et al (2010) A case report of chronic granulomatous disease presenting with aspergillus pneumonia in a 2-month old girl. Korean J Pediatr 53:722–726PubMedCrossRefGoogle Scholar
  58. Lopansri BK, Anstey NM, Weinberg JB et al (2003) Low plasma arginine concentrations in children with cerebral malaria and decreased nitric oxide production. Lancet 361:676–678PubMedCrossRefGoogle Scholar
  59. Lykkesfeldt J, Poulsen HE (2009) Is vitamin C supplementation beneficial? Lessons learned from randomized controlled trials. Br J Nutr 103:1251–1259PubMedCrossRefGoogle Scholar
  60. Mastroeni P, Vazquez-Torres A, Fang FC et al (2000) Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo. J Exp Med 192:237–248PubMedCrossRefGoogle Scholar
  61. Mazie D, Idrissa-Boubou M (1999) Immunogenetics and cerebral malaria. Bull Soc Pathol Exot 92:249–255Google Scholar
  62. McCaffrey RL, Schwartz JT, Lindemann SR et al (2010) Multiple mechanisms of NADPH oxidase inhibition by type A and type B Francisella tularensis. J Leukoc Biol 88:791–805PubMedCrossRefGoogle Scholar
  63. McGovern NN, Cowburn AS, Porter L et al (2011) Hypoxia selectively inhibits respiratory burst activity and killing of Staphylococcus aureus in human neutrophils. J Immunol 186:453–463PubMedCrossRefGoogle Scholar
  64. McLean S, Bowman LA, Poole RK (2010) Peroxynitrite stress is exacerbated by flavohaemoglobin-derived oxidative stress in Salmonella typhymurium and is relieved by NO. Microbiology 156(Pt 12):3556–3565PubMedCrossRefGoogle Scholar
  65. Miller JL, Velmurugan K, Cowan MJ et al (2010) The type I NADH dehydrogenase of Mycobacterium tuberculosis counters phagosomal NOX2 activity to inhibit TNF-α-mediated host cell apoptosis. PLoS Pathog 6:e1000864PubMedCrossRefGoogle Scholar
  66. Minakami R, Sumimoto H (2006) Phagocytosis-coupled activation of the superoxide-producing phagocyte oxidase, a member of the nadph oxidase (nox). Int J Hematol 84:193–198PubMedCrossRefGoogle Scholar
  67. Morgan D, Cherny VV, Murphy R et al (2005) The pH dependence of NADPH oxidase in human eosinophils. J Physiol 569(Pt 2):419–431PubMedCrossRefGoogle Scholar
  68. Murray HW, Xiang Z, Ma X (2006) Responses to Leishmania donovani in mice deficient in both phagocyte oxidase and inducible nitric oxide synthase. Am J Trop Med Hyg 74:1013–1015PubMedGoogle Scholar
  69. Nahrevanian H (2006) Immune effector mechanisms of the nitric oxide pathway in malaria: cytotoxicity versus cytoprotection. Braz J Infect Dis 10:283–292PubMedCrossRefGoogle Scholar
  70. Nahrevanian H, Gholizadeh J, Farahmand M et al (2008) Patterns of co-association of C-reactive protein and nitric oxide in malaria in endemic areas of Iran. Mem Inst Oswaldo Cruz 103:39–44PubMedCrossRefGoogle Scholar
  71. Nandi N, Sen A, Banerjee R et al (2010) Hydrogen peroxide induces apoptosis-like death in Entamoeba histolytica trophozoites. Microbiology 156(Pt 7):1926–1941PubMedCrossRefGoogle Scholar
  72. Nappi AJ, Vass E (2002) Interactions of iron with reactive intermediates of oxygen and nitrogen. Dev Neurosci 24:134–142PubMedCrossRefGoogle Scholar
  73. Ng VH, Cox JS, Sousa AO et al (2004) Role of KatG catalase-peroxidase in mycobacterial pathogenesis: countering the phagocyte oxidative burst. Mol Microbiol 52:1291–1302PubMedCrossRefGoogle Scholar
  74. Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315–424PubMedCrossRefGoogle Scholar
  75. Pal S, Dolai S, Yadav RK et al (2010) Ascorbate peroxidase from Leishmania major controls the virulence of infective stage of promastigotes by regulating oxidative stress. PLoS One 5:e11271PubMedCrossRefGoogle Scholar
  76. Parsonage D, Desrosiers DC, Hazlet KR et al (2010) Broad specificity AhpC-like peroxiredoxin and its thioredoxin in the sparse antioxidant defense system of Treponema pallidum. Proc Natl Acad Sci USA 107:6240–6245PubMedCrossRefGoogle Scholar
  77. Piacenza L, Peluffo G, Alvarez MN et al (2008) Peroxiredoxins play a major role in protecting Trypanosoma cruzi against macrophage- and endogenously-derived peroxynitrite. Biochem J 410:359–368PubMedCrossRefGoogle Scholar
  78. Rodriguez-Galán MC, Sotomayor C, Costamagna ME et al (2002) Immunocompetence of macrophages in rats exposed to Candida albicans infection and stress. Am J Physiol Cell Physiol 284:C111–C118PubMedGoogle Scholar
  79. Rosenthal PJ, Sijwali PS, Singh A et al (2002) Cysteine proteases of malaria parasites: targets for chemotherapy. Curr Pharm Des 8:1659–1672PubMedCrossRefGoogle Scholar
  80. Saxena G, Chen J, Shalev A (2010) Intracellular shutting and mitochondrial function of thioredoxin-interacting protein. J Biol Chem 285:3997–4005PubMedCrossRefGoogle Scholar
  81. Segal BH, Han W, Bushey JJ et al (2010) NADPH oxidase limits innate immune responses in the lungs in mice. PLoS One 5:e9631PubMedCrossRefGoogle Scholar
  82. Selemidis S, Dusting GJ, Peshavariya H et al (2007) Nitric oxide suppresses NADPH oxidase-dependent superoxide production by S-nitrosylation in human endothelial cells. Cardiovasc Res 75:349–358PubMedCrossRefGoogle Scholar
  83. Sharma A, Eapen A, Subbarao SK (2004) Parasite killing in Plasmodium vivax by nitric oxide: implication of aspartic protease inhibition. J Biochem 136:329–334PubMedCrossRefGoogle Scholar
  84. Shimada T, Park BG, Wolf AJ et al (2010) Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1beta secretion. Cell Host Microbe 7:38–49PubMedCrossRefGoogle Scholar
  85. Sobolewski P, Gramaglia I, Frangos J et al (2005) Nitric oxide bioavailability in malaria. Trends Parasitol 21:415–422PubMedCrossRefGoogle Scholar
  86. Soucy-Faulkner A, Mukawera E, Fink K et al (2010) Requirement of NOX2 and reactive oxygen species for efficient RIG-I-mediated antiviral response through regulation of MAVS expression. PloS Pathog 6:e1000930PubMedCrossRefGoogle Scholar
  87. Soutourina O, Dubrac S, Poupel O et al (2010) The Pleiotropic CymR regulator of Staphylococcus aureus plays an important role in virulence and stress response. PLoS Pathog 6:e1000894PubMedCrossRefGoogle Scholar
  88. Sumimoto H, Hata K, Mizuki K et al (1996) Assembly and activation of the phagocyte NADPH oxidase. J Biol Chem 271:22152–22158PubMedCrossRefGoogle Scholar
  89. Szabó C, Ischiropoulos H, Radi R (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 6:662–680PubMedCrossRefGoogle Scholar
  90. Talvani A, Machado FS, Santana GC et al (2002) Leukotriene B4 induces nitric oxide synthesis in Trypanosamoa cruzi-infected murine macrophages and mediates resistance to infection. Infect Immun 70:4247–4253PubMedCrossRefGoogle Scholar
  91. Torre D, Pugliese A, Speranza F (2002) Role of nitric oxide in HIV-1 infection: friend or foe? Lancet Infect Dis 2:273–280PubMedCrossRefGoogle Scholar
  92. Vázquez-Torres A, Fang FC (2001) Salmonella evasion of the NADPH phagocyte oxidase. Microbes Infect 3:1313–1320PubMedCrossRefGoogle Scholar
  93. Vázquez-Torres A, Fantuzzi G, Edwards CK et al (2001) Defective localization of the NADPH phagocyte oxidase to Salmonella-containing phagosomes in tumor necrosis factor p55 receptor-deficient macrophages. Proc Natl Acad Sci USA 98:2561–2565PubMedCrossRefGoogle Scholar
  94. Velmurugan K, Chen B, Miller JL et al (2007) Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLoS Pathog 3:e110PubMedCrossRefGoogle Scholar
  95. Venturini G, Colasanti M, Salvati L et al (2000) Nitric oxide inhibits falcipain, the Plasmodium falciparum trophozoite cysteine protease. Biochem Biophys Res Commun 267:190–193PubMedCrossRefGoogle Scholar
  96. Vladimirov YA, Proskurnina EV (2009) Free radicals and cell chemiluminescence. Biochemistry 74:1545–1566PubMedGoogle Scholar
  97. von Köckritz-Blickwede M, Nizet V (2009) Innate immunity turned inside-out: antimicrobial defense by phagocyte extracellular traps. J Mol Med 87:775–783CrossRefGoogle Scholar
  98. Wellington M, Dolan K, Krysan DJ (2009) Live Candida albicans suppresses production of reactive oxygen species in phagocytes. Infect Immun 77:405–413PubMedCrossRefGoogle Scholar
  99. Zhou R, Tardivel A, Thorens B et al (2010) Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 11:136–140PubMedCrossRefGoogle Scholar

Copyright information

© L. Hirszfeld Institute of Immunology and Experimental Therapy, Wroclaw, Poland 2011

Authors and Affiliations

  • Carlos K. B. Ferrari
    • 1
  • Paula C. S. Souto
    • 1
  • Eduardo L. França
    • 1
  • Adenilda C. Honorio-França
    • 1
  1. 1.Biomedical Research GroupICBS, “Campus Universitário do Araguaia”, Federal University of Mato Grosso (UFMT)Pontal do AraguaiaBrazil

Personalised recommendations