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Published in: Malaria Journal 1/2015

Open Access 01-12-2015 | Research

N-acetyl cysteine and mushroom Agaricus sylvaticus supplementation decreased parasitaemia and pulmonary oxidative stress in a mice model of malaria

Authors: Bruno A. Quadros Gomes, Lucio F. D. da Silva, Antonio R. Quadros Gomes, Danilo R. Moreira, Maria Fani Dolabela, Rogério S. Santos, Michael D. Green, Eliete P. Carvalho, Sandro Percário

Published in: Malaria Journal | Issue 1/2015

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Abstract

Background

Malaria infection can cause high oxidative stress, which could lead to the development of severe forms of malaria, such as pulmonary malaria. In recent years, the role of reactive oxygen species in the pathogenesis of the disease has been discussed, as well as the potential benefit of antioxidants supplementation. The aim of this study was to investigate the effects of N-acetyl cysteine (NAC) or mushroom Agaricus sylvaticus supplementation on the pulmonary oxidative changes in an experimental model of malaria caused by Plasmodium berghei strain ANKA.

Methods

Swiss male mice were infected with P. berghei and treated with NAC or AS. Samples of lung tissue and whole blood were collected after one, three, five, seven or ten days of infection for the assessment of thiobarbituric acid reactive substances (TBARS), trolox equivalent antioxidant capacity (TEAC), nitrites and nitrates (NN) and to assess the degree of parasitaemia.

Results

Although parasitaemia increased progressively with the evolution of the disease in all infected groups, there was a significant decrease from the seventh to the tenth day of infection in both antioxidant-supplemented groups. Results showed significant higher levels of TEAC in both supplemented groups, the highest occurring in the group supplemented with A. sylvaticus. In parallel, TBARS showed similar levels among all groups, while levels of NN were higher in animals supplemented with NAC in relation to the positive control groups and A. sylvaticus, whose levels were similar to the negative control group.

Conclusion

Oxidative stress arising from plasmodial infection was attenuated by supplementation of both antioxidants, but A. sylvaticus proved to be more effective and has the potential to become an important tool in the adjuvant therapy of malaria.
Appendix
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Literature
3.
go back to reference Potter SM, Mitchell AJ, Cowden WB, Sanni LA, Dinauer M, Haan JB, et al. Phagocyte-derived reactive oxygen species do not influence the progression of murine blood-stage malaria infections. Infect Immun. 2005;73:4941–7.CrossRefPubMedCentralPubMed Potter SM, Mitchell AJ, Cowden WB, Sanni LA, Dinauer M, Haan JB, et al. Phagocyte-derived reactive oxygen species do not influence the progression of murine blood-stage malaria infections. Infect Immun. 2005;73:4941–7.CrossRefPubMedCentralPubMed
4.
go back to reference Reis PA, Comim CM, Hermani F, Silva B, Barichello T, Portella AC, et al. Cognitive dysfunction is sustained after rescue therapy in experimental cerebral malaria, and is reduced by additive antioxidant therapy. PLoS Pathog. 2010;6, e1000963.CrossRefPubMedCentralPubMed Reis PA, Comim CM, Hermani F, Silva B, Barichello T, Portella AC, et al. Cognitive dysfunction is sustained after rescue therapy in experimental cerebral malaria, and is reduced by additive antioxidant therapy. PLoS Pathog. 2010;6, e1000963.CrossRefPubMedCentralPubMed
5.
go back to reference Lou J, Lucas R, Grau GE. Pathogenesis of cerebral malaria: recent experimental data and possible applications for humans. Clin Microbiol Rev. 2001;14:810–20.CrossRefPubMedCentralPubMed Lou J, Lucas R, Grau GE. Pathogenesis of cerebral malaria: recent experimental data and possible applications for humans. Clin Microbiol Rev. 2001;14:810–20.CrossRefPubMedCentralPubMed
6.
go back to reference Omodeo-Salè F, Motti A, Basilico N, Parapini S, Olliaro P, Taramelli D. Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum. Blood. 2003;102:705–11.CrossRefPubMed Omodeo-Salè F, Motti A, Basilico N, Parapini S, Olliaro P, Taramelli D. Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum. Blood. 2003;102:705–11.CrossRefPubMed
7.
go back to reference Tanneur V, Duranton C, Brand VB, Sandu CD, Akkaya C, Kasinathan RS, et al. Purinoceptors are involved in the induction of an osmolyte permeability in malaria-infected and oxidized human erythrocytes. FASEB J. 2006;20:133–5.PubMed Tanneur V, Duranton C, Brand VB, Sandu CD, Akkaya C, Kasinathan RS, et al. Purinoceptors are involved in the induction of an osmolyte permeability in malaria-infected and oxidized human erythrocytes. FASEB J. 2006;20:133–5.PubMed
8.
go back to reference Jaramillo M, Godbout M, Olivier M. Hemozoin induces macrophage chemokine expression through oxidative stress-dependent and –independent mechanisms. J Immunol. 2005;74:475–84.CrossRef Jaramillo M, Godbout M, Olivier M. Hemozoin induces macrophage chemokine expression through oxidative stress-dependent and –independent mechanisms. J Immunol. 2005;74:475–84.CrossRef
9.
10.
go back to reference Mau JL, Chao GR, Wu KT. Antioxidant properties of methanolic extracts from several ear mushrooms. J Agric Food Chem. 2001;49:5461–7.CrossRefPubMed Mau JL, Chao GR, Wu KT. Antioxidant properties of methanolic extracts from several ear mushrooms. J Agric Food Chem. 2001;49:5461–7.CrossRefPubMed
11.
go back to reference Gennari J, Veronesi R, Felippe Jr J, Gennari MS, Percario S. Effect of Agaricus sylvaticus dietary supplementation on NK cell count in cancer patients. In: Romaine CP, Keil CB, Rinker DL, Royse DJ, editors. Science and cultivation of edible and medicinal fungi. Pennsylvania: Penn State; 2004. p. 633–5. Gennari J, Veronesi R, Felippe Jr J, Gennari MS, Percario S. Effect of Agaricus sylvaticus dietary supplementation on NK cell count in cancer patients. In: Romaine CP, Keil CB, Rinker DL, Royse DJ, editors. Science and cultivation of edible and medicinal fungi. Pennsylvania: Penn State; 2004. p. 633–5.
12.
go back to reference Isah MB, Ibrahim MA. The role of antioxidants treatment on the pathogenesis of malarial infections: a review. Parasitol Res. 2014;113:801–9.CrossRefPubMed Isah MB, Ibrahim MA. The role of antioxidants treatment on the pathogenesis of malarial infections: a review. Parasitol Res. 2014;113:801–9.CrossRefPubMed
13.
go back to reference Liu F, Ooi VE, Chang ST. Free radical scavenging activities of mushroom polysaccharide extracts. Life Sci. 1997;60:761–71.CrossRef Liu F, Ooi VE, Chang ST. Free radical scavenging activities of mushroom polysaccharide extracts. Life Sci. 1997;60:761–71.CrossRef
14.
go back to reference Percario S, Naufal AS, Gennari MS, Gennari JL. Antioxidant activity of edible blushing wood mushroom, Agaricus sylvaticus Schaeff. (Agaricomycetideae) in vitro. Int J Med Mushr. 2009;11:133–9.CrossRef Percario S, Naufal AS, Gennari MS, Gennari JL. Antioxidant activity of edible blushing wood mushroom, Agaricus sylvaticus Schaeff. (Agaricomycetideae) in vitro. Int J Med Mushr. 2009;11:133–9.CrossRef
15.
go back to reference Boulos M, Costa J, Tosta C. Comprometimento pulmonar na malária. Rev Inst Med Trop São Paulo. 1993;35:93–102.PubMed Boulos M, Costa J, Tosta C. Comprometimento pulmonar na malária. Rev Inst Med Trop São Paulo. 1993;35:93–102.PubMed
16.
go back to reference Day N, Dondorp AM. The management of patients with severe malaria. Am J Trop Med Hyg. 2007;77:29–35.PubMed Day N, Dondorp AM. The management of patients with severe malaria. Am J Trop Med Hyg. 2007;77:29–35.PubMed
17.
go back to reference Taylor WR, Canon V, White NJ. Pulmonary manifestations of malaria: recognition and management. Treat Respir Med. 2006;5:419–28.CrossRefPubMed Taylor WR, Canon V, White NJ. Pulmonary manifestations of malaria: recognition and management. Treat Respir Med. 2006;5:419–28.CrossRefPubMed
18.
go back to reference Rojo-Marcos G, Cuadros-González J, Mesa-Latorre JM, Culebras-López AM, Pablo-Sánchez R. Case report: acute respiratory distress syndrome in a case of Plasmodium ovale malaria. Am J Trop Med Hyg. 2008;79:391–3.PubMed Rojo-Marcos G, Cuadros-González J, Mesa-Latorre JM, Culebras-López AM, Pablo-Sánchez R. Case report: acute respiratory distress syndrome in a case of Plasmodium ovale malaria. Am J Trop Med Hyg. 2008;79:391–3.PubMed
19.
go back to reference Gachot B, Wolff M, Nissack G, Veber B, Vachon F. Acute lung injury complicating imported Plasmodium falciparum malaria. Chest. 1995;108:746–9.CrossRefPubMed Gachot B, Wolff M, Nissack G, Veber B, Vachon F. Acute lung injury complicating imported Plasmodium falciparum malaria. Chest. 1995;108:746–9.CrossRefPubMed
20.
go back to reference Gillrie MR, Krishnegowda G, Lee K, Buret AG, Robbins SM, Looareesuwan S, et al. Src-family kinase–dependent disruption of endothelial barrier function by Plasmodium falciparum merozoite proteins. Blood. 2007;110:3426–35.CrossRefPubMedCentralPubMed Gillrie MR, Krishnegowda G, Lee K, Buret AG, Robbins SM, Looareesuwan S, et al. Src-family kinase–dependent disruption of endothelial barrier function by Plasmodium falciparum merozoite proteins. Blood. 2007;110:3426–35.CrossRefPubMedCentralPubMed
21.
go back to reference Pouvelle B, Matarazzo V, Jurzynski C, Nemeth J, Ramharter M, Rougon G, et al. Neural cell adhesion molecule, a new cytoadhesion receptor for Plasmodium falciparum-infected erythrocytes capable of aggregation. Infect Immun. 2007;75:3516–22.CrossRefPubMedCentralPubMed Pouvelle B, Matarazzo V, Jurzynski C, Nemeth J, Ramharter M, Rougon G, et al. Neural cell adhesion molecule, a new cytoadhesion receptor for Plasmodium falciparum-infected erythrocytes capable of aggregation. Infect Immun. 2007;75:3516–22.CrossRefPubMedCentralPubMed
22.
go back to reference Phiri H, Montgomery J, Molyneux M, Craig A. Competitive endothelial adhesion between Plasmodium falciparum isolates under physiological flow conditions. Malar J. 2009;8:214.CrossRefPubMedCentralPubMed Phiri H, Montgomery J, Molyneux M, Craig A. Competitive endothelial adhesion between Plasmodium falciparum isolates under physiological flow conditions. Malar J. 2009;8:214.CrossRefPubMedCentralPubMed
23.
go back to reference Suresh KP. An overview of randomization techniques: an unbiased assessment of outcome in clinical research. J Human Reprod Sci. 2011;4:8–11.CrossRef Suresh KP. An overview of randomization techniques: an unbiased assessment of outcome in clinical research. J Human Reprod Sci. 2011;4:8–11.CrossRef
24.
go back to reference Sadavongvivad C, Aviado D. Pathologic physiology and chemotherapy of Plasmodium berghei. VI. Mechanichal properties and histological features of the lung. Exp Parasitol. 1969;24:313–26.CrossRefPubMed Sadavongvivad C, Aviado D. Pathologic physiology and chemotherapy of Plasmodium berghei. VI. Mechanichal properties and histological features of the lung. Exp Parasitol. 1969;24:313–26.CrossRefPubMed
25.
go back to reference Aviado D, Camber PJ. Pathologic physiology and chemotherapy of Plasmodium berghei. X. Pulmonary edema and naphthoquinones. Exp Parasitol. 1969;26:354–68.CrossRefPubMed Aviado D, Camber PJ. Pathologic physiology and chemotherapy of Plasmodium berghei. X. Pulmonary edema and naphthoquinones. Exp Parasitol. 1969;26:354–68.CrossRefPubMed
26.
go back to reference Weiss ML, Kubat K. Plasmodium berghei: a mouse model for the “sudden death” and “malarial lung” syndromes. Exp Parasitol. 1983;56:143–51.CrossRefPubMed Weiss ML, Kubat K. Plasmodium berghei: a mouse model for the “sudden death” and “malarial lung” syndromes. Exp Parasitol. 1983;56:143–51.CrossRefPubMed
27.
go back to reference Moore BR, Jago JD, Batty KT. Plasmodium berghei: Parasite clearance after treatment with dihydroartemisinin in an asplenic murine malaria model. Exp Parasitol. 2008;118:458–67.CrossRefPubMed Moore BR, Jago JD, Batty KT. Plasmodium berghei: Parasite clearance after treatment with dihydroartemisinin in an asplenic murine malaria model. Exp Parasitol. 2008;118:458–67.CrossRefPubMed
28.
go back to reference Martins YC, Smith MJ, Pelajo-Machado M, Werneck GL, Lenzi HL, Daniel-Ribeiro CD, et al. Characterization of cerebral malaria in the outbred Swiss Webster mouse infected by Plasmodium berghei ANKA. Int J Path. 2009;90:119–30.CrossRef Martins YC, Smith MJ, Pelajo-Machado M, Werneck GL, Lenzi HL, Daniel-Ribeiro CD, et al. Characterization of cerebral malaria in the outbred Swiss Webster mouse infected by Plasmodium berghei ANKA. Int J Path. 2009;90:119–30.CrossRef
29.
go back to reference Miller N, Rice-Evans C, Davies M, Gopinathan V, Milner A. A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clin Sci. 1993;84:407–12.PubMed Miller N, Rice-Evans C, Davies M, Gopinathan V, Milner A. A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clin Sci. 1993;84:407–12.PubMed
30.
go back to reference Re R, Pellegrini R, Protegente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorizaton assay. Free Rad Biol Med. 1999;26:1231–7.CrossRefPubMed Re R, Pellegrini R, Protegente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorizaton assay. Free Rad Biol Med. 1999;26:1231–7.CrossRefPubMed
31.
go back to reference Kohn HI, Liversedge M. On a new aerobic metabolite whose production by brain is inhibited by apomorphine, emetine, ergotamine, epinephrine, and menadione. J Pharmacol Experimen Ther. 1944;82:292–300. Kohn HI, Liversedge M. On a new aerobic metabolite whose production by brain is inhibited by apomorphine, emetine, ergotamine, epinephrine, and menadione. J Pharmacol Experimen Ther. 1944;82:292–300.
32.
go back to reference Percario S, Vital A, Jablonka F. Dosagem do malondialdeido. Newslab. 1994;2:46–50. Percario S, Vital A, Jablonka F. Dosagem do malondialdeido. Newslab. 1994;2:46–50.
33.
go back to reference May JM, Qu ZC, Xia L, Cobb CE. Nitrite uptake and metabolism and oxidant stress in human erythrocytes. Am J Physiol Cell Physiol. 2000;279:1946–54. May JM, Qu ZC, Xia L, Cobb CE. Nitrite uptake and metabolism and oxidant stress in human erythrocytes. Am J Physiol Cell Physiol. 2000;279:1946–54.
35.
go back to reference Van den Steen PE, Geurts N, Deroost K, Van Aelst I, Verhenne S, Heremans H, et al. Immunopathology and dexamethasone therapy in a new model for malaria-associated acute respiratory distress syndrome. Am J Respir Crit Care Med. 2010;181:957–68.CrossRefPubMed Van den Steen PE, Geurts N, Deroost K, Van Aelst I, Verhenne S, Heremans H, et al. Immunopathology and dexamethasone therapy in a new model for malaria-associated acute respiratory distress syndrome. Am J Respir Crit Care Med. 2010;181:957–68.CrossRefPubMed
36.
go back to reference Berk M, Copolov D, Dean O, Lu K, Jeavons S, Schapkaitz I, et al. N-acetyl cysteine as a glutathione precursor for schizophrenia – a double-blind, randomized, placebo-controlled trial. Biol Psy. 2008;64:361–8.CrossRef Berk M, Copolov D, Dean O, Lu K, Jeavons S, Schapkaitz I, et al. N-acetyl cysteine as a glutathione precursor for schizophrenia – a double-blind, randomized, placebo-controlled trial. Biol Psy. 2008;64:361–8.CrossRef
37.
go back to reference Carmeli C, Knyazeva MG, Cuénod M, Do KQ. Glutathione precursor N-acetyl-cysteine modulates EEG synchronization in schizophrenia patients: a double-blind, randomized, placebo-controlled trial. PLoS ONE. 2012;7, e29341.CrossRefPubMedCentralPubMed Carmeli C, Knyazeva MG, Cuénod M, Do KQ. Glutathione precursor N-acetyl-cysteine modulates EEG synchronization in schizophrenia patients: a double-blind, randomized, placebo-controlled trial. PLoS ONE. 2012;7, e29341.CrossRefPubMedCentralPubMed
38.
go back to reference Percario S, Odorizzi VF, Souza DRS, Pinhel MAS, Gennari JL, Gennari MS, et al. Edible mushroom Agaricus sylvaticus can prevent the onset of atheroma plaques in hypercholesterolemia rabbits. Cell Mol Biol. 2008;54:1055–61. Percario S, Odorizzi VF, Souza DRS, Pinhel MAS, Gennari JL, Gennari MS, et al. Edible mushroom Agaricus sylvaticus can prevent the onset of atheroma plaques in hypercholesterolemia rabbits. Cell Mol Biol. 2008;54:1055–61.
39.
go back to reference Fortes VC, Recôva VL, Melo AL, Novaes MRCG. Life quality of postsurgical patients with colorectal cancer after supplemented diet with Agaricus sylvaticus fungus. Nutr Hosp. 2010;25:586–96. Fortes VC, Recôva VL, Melo AL, Novaes MRCG. Life quality of postsurgical patients with colorectal cancer after supplemented diet with Agaricus sylvaticus fungus. Nutr Hosp. 2010;25:586–96.
40.
go back to reference Fortes RC, Silva JRL, Novaes MRCG. Anthropometric assessment of men with colorectal cancer after dietary supplement with Agaricus sylvaticus fungus. J Coloproctol. 2012;23:365–71.CrossRef Fortes RC, Silva JRL, Novaes MRCG. Anthropometric assessment of men with colorectal cancer after dietary supplement with Agaricus sylvaticus fungus. J Coloproctol. 2012;23:365–71.CrossRef
41.
go back to reference Orsine JVC, Brito LM, Silva RC, Almeida MFMS, Novaes MRCG. Cytotoxicity of Agaricus sylvaticus in non-tumor cells (NTH/3T3) and tumor (OSCC-3) using tetrazolium (MTT) assay. Nutr Hosp. 2013;28:1244–54.PubMed Orsine JVC, Brito LM, Silva RC, Almeida MFMS, Novaes MRCG. Cytotoxicity of Agaricus sylvaticus in non-tumor cells (NTH/3T3) and tumor (OSCC-3) using tetrazolium (MTT) assay. Nutr Hosp. 2013;28:1244–54.PubMed
42.
go back to reference Figueira MS, Sa LA, Vasconcelos AS, Moreira DR, Laurindo PSOC, Ribeiro DRG, et al. Nutritional supplementation of mushroom Agaricus sylvaticus reversed oxidative stress in children with HIV. Can J Infec Dis Med Microbiol. 2014;25:257–64. Figueira MS, Sa LA, Vasconcelos AS, Moreira DR, Laurindo PSOC, Ribeiro DRG, et al. Nutritional supplementation of mushroom Agaricus sylvaticus reversed oxidative stress in children with HIV. Can J Infec Dis Med Microbiol. 2014;25:257–64.
43.
go back to reference Couper KN, Blount DG, Hafalla JC, Nico VR, Souza JB, Riley EM. Macrophage-mediated but gamma interferon-independent innate immune responses control the primary wave of Plasmodium yoelii parasitemia. Infect Immun. 2007;75:5806–18.CrossRefPubMedCentralPubMed Couper KN, Blount DG, Hafalla JC, Nico VR, Souza JB, Riley EM. Macrophage-mediated but gamma interferon-independent innate immune responses control the primary wave of Plasmodium yoelii parasitemia. Infect Immun. 2007;75:5806–18.CrossRefPubMedCentralPubMed
44.
go back to reference Agbor-Enoh S, Seudieu C, Davidson E, Dritschilo A, Jung M. Novel inhibitor of Plasmodium histone deacetylase that cures P. berghei-infected mice. Antimicr Agents Chemother. 2009;53:1727–34.CrossRef Agbor-Enoh S, Seudieu C, Davidson E, Dritschilo A, Jung M. Novel inhibitor of Plasmodium histone deacetylase that cures P. berghei-infected mice. Antimicr Agents Chemother. 2009;53:1727–34.CrossRef
45.
go back to reference Epiphanio S, Campos M, Pamplona A, Carapau D, Pena AC, Ataíde R, et al. VEGF promotes malaria-associated acute lung injury in mice. PLoS Path. 2010;6, e1000916.CrossRef Epiphanio S, Campos M, Pamplona A, Carapau D, Pena AC, Ataíde R, et al. VEGF promotes malaria-associated acute lung injury in mice. PLoS Path. 2010;6, e1000916.CrossRef
46.
go back to reference Saxena S, Kumar R, Madan T, Gupta V, Muralidhar K, Sarma PU. Association of polymorphisms in pulmonary surfactant protein A1 and A2 genes with high-altitude pulmonary edema. Chest. 2005;128:1611–9.CrossRefPubMed Saxena S, Kumar R, Madan T, Gupta V, Muralidhar K, Sarma PU. Association of polymorphisms in pulmonary surfactant protein A1 and A2 genes with high-altitude pulmonary edema. Chest. 2005;128:1611–9.CrossRefPubMed
47.
go back to reference Christofidou-Solomidou M, Scherpereel A, Wiewrodt R, Ng K, Sweitzer T, Arguiri E, et al. PECAM-directed delivery of catalase to endothelium protects against pulmonary vascular oxidative stress. Am J Physiol Lung Cell Mol Physiol. 2003;258:283–92.CrossRef Christofidou-Solomidou M, Scherpereel A, Wiewrodt R, Ng K, Sweitzer T, Arguiri E, et al. PECAM-directed delivery of catalase to endothelium protects against pulmonary vascular oxidative stress. Am J Physiol Lung Cell Mol Physiol. 2003;258:283–92.CrossRef
48.
go back to reference Oury TD, Schaefer LM, Fattman CL, Choi A, Weck KE, Watkins SC. Depletion of pulmonary EC-SOD after exposure to hyperoxia. Am J Physiol Lung Cell Mol Physiol. 2002;283:L777–84.CrossRefPubMed Oury TD, Schaefer LM, Fattman CL, Choi A, Weck KE, Watkins SC. Depletion of pulmonary EC-SOD after exposure to hyperoxia. Am J Physiol Lung Cell Mol Physiol. 2002;283:L777–84.CrossRefPubMed
49.
go back to reference Kinsella JP, Parker TA, Davis JM, Abman SH. Superoxide dismutase improves gas exchange and pulmonary hemodynamics in premature lambs. Am J Respir Crit Care Med. 2005;172:745–9.CrossRefPubMedCentralPubMed Kinsella JP, Parker TA, Davis JM, Abman SH. Superoxide dismutase improves gas exchange and pulmonary hemodynamics in premature lambs. Am J Respir Crit Care Med. 2005;172:745–9.CrossRefPubMedCentralPubMed
50.
go back to reference Rahman I, MacNee W. Oxidative stress and regulation of glutathione in lung inflammation. Eur Respir J. 2000;53:534–54.CrossRef Rahman I, MacNee W. Oxidative stress and regulation of glutathione in lung inflammation. Eur Respir J. 2000;53:534–54.CrossRef
51.
go back to reference Hemmer CJ, Lehr HA, Westphal K, Unverricht M, Kratzius M, Reisinger EC. Plasmodium falciparum malaria: reduction of endothelial cell apoptosis in vitro. Infect Immun. 2005;73:1764–70.CrossRefPubMedCentralPubMed Hemmer CJ, Lehr HA, Westphal K, Unverricht M, Kratzius M, Reisinger EC. Plasmodium falciparum malaria: reduction of endothelial cell apoptosis in vitro. Infect Immun. 2005;73:1764–70.CrossRefPubMedCentralPubMed
52.
go back to reference Trivedi V, Chand P, Srivastava K, Puri SK, Maulik PR, Bandyopadhyay U. Clotrimazole inhibits hemoperoxidase of Plasmodium falciparum and induces oxidative stress. J Biol Chem. 2005;280:41129–36.CrossRefPubMed Trivedi V, Chand P, Srivastava K, Puri SK, Maulik PR, Bandyopadhyay U. Clotrimazole inhibits hemoperoxidase of Plasmodium falciparum and induces oxidative stress. J Biol Chem. 2005;280:41129–36.CrossRefPubMed
53.
go back to reference Keller CC, Kremsner PG, Hittner JB, Misukonis MA, Weinberg JB, Perkins DJ. Elevated nitric oxide production in children with malarial anemia: hemozoin-induced nitric oxide synthase type 2 transcripts and nitric oxide in blood mononuclear cells. Infect Immun. 2004;72:4868–73.CrossRefPubMedCentralPubMed Keller CC, Kremsner PG, Hittner JB, Misukonis MA, Weinberg JB, Perkins DJ. Elevated nitric oxide production in children with malarial anemia: hemozoin-induced nitric oxide synthase type 2 transcripts and nitric oxide in blood mononuclear cells. Infect Immun. 2004;72:4868–73.CrossRefPubMedCentralPubMed
54.
go back to reference Chen TH, Chang PC, Chang MC, Lin YF, Lee HM. Chloroquine induces the expression of inducible nitric oxide synthase in C6 glioma cells. Pharmacol Res. 2005;51:329–36.CrossRefPubMed Chen TH, Chang PC, Chang MC, Lin YF, Lee HM. Chloroquine induces the expression of inducible nitric oxide synthase in C6 glioma cells. Pharmacol Res. 2005;51:329–36.CrossRefPubMed
55.
go back to reference Wang Q, Liu Y, Liu J, Chen G, Zheng W, Wang J, et al. Plasmodium yoelii: assessment of production and role of nitric oxide during the early stages of infection in susceptible and resistant mice. Exp Parasitol. 2009;121:268–73.CrossRefPubMed Wang Q, Liu Y, Liu J, Chen G, Zheng W, Wang J, et al. Plasmodium yoelii: assessment of production and role of nitric oxide during the early stages of infection in susceptible and resistant mice. Exp Parasitol. 2009;121:268–73.CrossRefPubMed
56.
go back to reference Bichet C, Cornet S, Larcombe S, Sorci G. Experimental inhibition of nitric oxide increases Plasmodium relictum (lineage SGS1) parasitemia. Exp Parasitol. 2012;132:417–23.CrossRefPubMed Bichet C, Cornet S, Larcombe S, Sorci G. Experimental inhibition of nitric oxide increases Plasmodium relictum (lineage SGS1) parasitemia. Exp Parasitol. 2012;132:417–23.CrossRefPubMed
57.
go back to reference Yeo TW, Lampah DA, Gitawati R, Tjitra E, Kenangalem E, McNeil YR, et al. Impaired nitric oxide bioavailability and L-arginine–reversible endothelial dysfunction in adults with falciparum malaria. JEM. 2007;204:2693–704.CrossRef Yeo TW, Lampah DA, Gitawati R, Tjitra E, Kenangalem E, McNeil YR, et al. Impaired nitric oxide bioavailability and L-arginine–reversible endothelial dysfunction in adults with falciparum malaria. JEM. 2007;204:2693–704.CrossRef
58.
go back to reference Cabrales P, Zanini GM, Meays D, Frangos JA, Carvalho LJ. Nitric oxide protection against murine cerebral malaria is associated with improved cerebral microcirculatory physiology. J Infect Dis. 2011;203:1454–63.CrossRefPubMedCentralPubMed Cabrales P, Zanini GM, Meays D, Frangos JA, Carvalho LJ. Nitric oxide protection against murine cerebral malaria is associated with improved cerebral microcirculatory physiology. J Infect Dis. 2011;203:1454–63.CrossRefPubMedCentralPubMed
59.
go back to reference Janka JJ, Koita OA, Traoré B, Traoré JM, Mzayek F, Sachdev V, et al. Increased pulmonary pressures and myocardial wall stress in children with severe malaria. J Infect Dis. 2010;202:791–800.CrossRefPubMedCentralPubMed Janka JJ, Koita OA, Traoré B, Traoré JM, Mzayek F, Sachdev V, et al. Increased pulmonary pressures and myocardial wall stress in children with severe malaria. J Infect Dis. 2010;202:791–800.CrossRefPubMedCentralPubMed
60.
go back to reference Bisseling TM, Roes ME, Raijmakers MTM, Steegers EAP, Peters WHM, Smits P. N-acetylcysteine restores nitric oxide-mediated effects in the fetoplacental circulation of preeclamptic patients. Am J Obst Gynecol. 2004;191:328–33.CrossRef Bisseling TM, Roes ME, Raijmakers MTM, Steegers EAP, Peters WHM, Smits P. N-acetylcysteine restores nitric oxide-mediated effects in the fetoplacental circulation of preeclamptic patients. Am J Obst Gynecol. 2004;191:328–33.CrossRef
61.
go back to reference Majano PL, Medina J, Zubı́a I, Sunyer L, Lara-Pezzi E, Maldonado-Rodrı́guez A, et al. N-acetyl-cysteine modulates inducible nitric oxide synthase gene expression in human hepatocytes. J Hepatol. 2004;40:632–7.CrossRefPubMed Majano PL, Medina J, Zubı́a I, Sunyer L, Lara-Pezzi E, Maldonado-Rodrı́guez A, et al. N-acetyl-cysteine modulates inducible nitric oxide synthase gene expression in human hepatocytes. J Hepatol. 2004;40:632–7.CrossRefPubMed
62.
go back to reference González-Rubio S, Linares CI, Bello RI, González R, Ferrín G, Hidalgo AB, et al. Calcium-dependent nitric oxide production is involved in the cytoprotective properties of N-acetylcysteine in glycochenodeoxycholic acid-induced cell death in hepatocytes. Toxicol Ap Pharmacol. 2010;242:165–72.CrossRef González-Rubio S, Linares CI, Bello RI, González R, Ferrín G, Hidalgo AB, et al. Calcium-dependent nitric oxide production is involved in the cytoprotective properties of N-acetylcysteine in glycochenodeoxycholic acid-induced cell death in hepatocytes. Toxicol Ap Pharmacol. 2010;242:165–72.CrossRef
63.
go back to reference Straface E, Rivabene R, Masella R, Santulli M, Paganelli R, Malorni W. Structural changes of the erythrocyte as a marker of non-insulin dependent diabetes: protective effects of N-acetylcysteine. Biochem Biophys Res Commun. 2002;290:1393–8.CrossRefPubMed Straface E, Rivabene R, Masella R, Santulli M, Paganelli R, Malorni W. Structural changes of the erythrocyte as a marker of non-insulin dependent diabetes: protective effects of N-acetylcysteine. Biochem Biophys Res Commun. 2002;290:1393–8.CrossRefPubMed
64.
go back to reference Jiang B, Haverty M, Brecher P. N-acetyl-L-cysteine enhances interleukin-1ß–induced nitric oxide synthase expression. Hypertension. 1999;34:574–9.CrossRefPubMed Jiang B, Haverty M, Brecher P. N-acetyl-L-cysteine enhances interleukin-1ß–induced nitric oxide synthase expression. Hypertension. 1999;34:574–9.CrossRefPubMed
65.
go back to reference Jiang B, Brecher P. N-acetyl-L-cysteine potentiates interleukin-1ß induction of nitric oxide synthase: role of p44/42 mitogen-activated protein kinases. Hypertension. 2000;35:914–8.CrossRefPubMed Jiang B, Brecher P. N-acetyl-L-cysteine potentiates interleukin-1ß induction of nitric oxide synthase: role of p44/42 mitogen-activated protein kinases. Hypertension. 2000;35:914–8.CrossRefPubMed
66.
go back to reference Fernhoff NB, Derbyshire ER, Marletta MA. A nitric oxide/cysteine interaction mediates the activation of soluble guanylate cyclase. Proc Natl Acad Sci USA. 2009;106:21602–7.CrossRefPubMedCentralPubMed Fernhoff NB, Derbyshire ER, Marletta MA. A nitric oxide/cysteine interaction mediates the activation of soluble guanylate cyclase. Proc Natl Acad Sci USA. 2009;106:21602–7.CrossRefPubMedCentralPubMed
67.
go back to reference Watt G, Jongsakul K, Ruangvirayuth R. A pilot study of N-acetylcysteine as adjunctive therapy for severe malaria. Q J Med. 2002;295:285–90.CrossRef Watt G, Jongsakul K, Ruangvirayuth R. A pilot study of N-acetylcysteine as adjunctive therapy for severe malaria. Q J Med. 2002;295:285–90.CrossRef
68.
go back to reference Dhangadamajhi G, Mohapatra BN, Kar SK, Ranjit M. Endothelial nitric oxide synthase gene polymorphisms and Plasmodium falciparum infection in Indian adults. Infect Immun. 2009;77:2943–7.CrossRefPubMedCentralPubMed Dhangadamajhi G, Mohapatra BN, Kar SK, Ranjit M. Endothelial nitric oxide synthase gene polymorphisms and Plasmodium falciparum infection in Indian adults. Infect Immun. 2009;77:2943–7.CrossRefPubMedCentralPubMed
69.
go back to reference Zhu J, Krishnegowda G, Gowda DC. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum. J Biol Chem. 2005;280:8617–27.CrossRefPubMed Zhu J, Krishnegowda G, Gowda DC. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum. J Biol Chem. 2005;280:8617–27.CrossRefPubMed
70.
go back to reference Anstey NM, Handojo TH, Pain MC, Kenangalem E, Tjitra E, Price RN, et al. Lung injury in vivax malaria: pathophysiological evidence for pulmonary vascular sequestration and post treatment alveolar-capillary inflammation. J Infect Dis. 2007;195:589–96.CrossRefPubMedCentralPubMed Anstey NM, Handojo TH, Pain MC, Kenangalem E, Tjitra E, Price RN, et al. Lung injury in vivax malaria: pathophysiological evidence for pulmonary vascular sequestration and post treatment alveolar-capillary inflammation. J Infect Dis. 2007;195:589–96.CrossRefPubMedCentralPubMed
71.
go back to reference Dimmeler S, Haendeler J, Nehls M, Zeiher AM. Suppression of apoptosis by nitric oxide via inhibition of interleukin-1β–converting enzyme (ice)-like and cysteine protease protein (cpp)-32–like proteases. J Exp Med. 1997;185:601–8.CrossRefPubMedCentralPubMed Dimmeler S, Haendeler J, Nehls M, Zeiher AM. Suppression of apoptosis by nitric oxide via inhibition of interleukin-1β–converting enzyme (ice)-like and cysteine protease protein (cpp)-32–like proteases. J Exp Med. 1997;185:601–8.CrossRefPubMedCentralPubMed
72.
go back to reference Pino P, Taoufiq Z, Nicheu J, Vouldoukis I, Mazier D. Blood–brain barrier breakdown during cerebral malaria: suicide or murder? Thromb Haemost. 2005;94:336–40.PubMed Pino P, Taoufiq Z, Nicheu J, Vouldoukis I, Mazier D. Blood–brain barrier breakdown during cerebral malaria: suicide or murder? Thromb Haemost. 2005;94:336–40.PubMed
Metadata
Title
N-acetyl cysteine and mushroom Agaricus sylvaticus supplementation decreased parasitaemia and pulmonary oxidative stress in a mice model of malaria
Authors
Bruno A. Quadros Gomes
Lucio F. D. da Silva
Antonio R. Quadros Gomes
Danilo R. Moreira
Maria Fani Dolabela
Rogério S. Santos
Michael D. Green
Eliete P. Carvalho
Sandro Percário
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2015
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-015-0717-0

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