Lipoxin A4 and 15-Epi-Lipoxin A4 Protect against Experimental Cerebral Malaria by Inhibiting IL-12/IFN-γ in the Brain

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Shryock, Nathaniel ^a   McBerry, Cortez ^a   Salazar Gonzalez, Rosa Maria ^a   Janes, Steven ^a   Costa, Fabio T M ^b   Aliberti, Julio ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

15 EPI LIPOXIN A4; ARACHIDONATE 5 LIPOXYGENASE; CD8 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 12P35; INTERLEUKIN 12P40; INTERLEUKIN 12P70; LEUKOTRIENE B4; LIPOXIN; LIPOXIN A; MESSENGER RNA; RNA 18S; SUPPRESSOR OF CYTOKINE SIGNALING 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN MALARIA; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DRUG MECHANISM; ENCEPHALITIS; EPIMER; EXPERIMENTAL INFECTION; FATTY ACID SYNTHESIS; GENE EXPRESSION; IN VIVO STUDY; LYMPHOCYTIC INFILTRATION; MORTALITY; MOUSE; NEUROPROTECTION; NONHUMAN; PLASMODIUM BERGHEI INFECTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SURVIVAL RATE; SURVIVAL TIME;

ANIMALS; ARACHIDONATE 5-LIPOXYGENASE; BRAIN; INTERFERON-GAMMA; INTERLEUKIN-12; LIPOXINS; MALARIA, CEREBRAL; MICE; PLASMODIUM BERGHEI;

ANIMALIA; PLASMODIUM FALCIPARUM;

EID: 84876424943     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061882     Document Type: Article

References (60)

1. Idro R, Jenkins NE, Newton CR, (2005) Pathogenesis, clinical features, and neurological outcome of cerebral malaria. Lancet Neurol 4: 827-840.
2. Dondorp A, Nosten F, Stepniewska K, Day N, White N, et al. (2005) Artesunate versus quinine for treatment of severe falciparum malaria: a randomised trial. Lancet 366: 717-725.
3. John CC, Bangirana P, Byarugaba J, Opoka RO, Idro R, et al. (2008) Cerebral malaria in children is associated with long-term cognitive impairment. Pediatrics 122: e92-99.
4. John CC, Panoskaltsis-Mortari A, Opoka RO, Park GS, Orchard PJ, et al. (2008) Cerebrospinal fluid cytokine levels and cognitive impairment in cerebral malaria. Am J Trop Med Hyg 78: 198-205.
5. Dondorp AM, Fanello CI, Hendriksen IC, Gomes E, Seni A, et al. (2010) Artesunate versus quinine in the treatment of severe falciparum malaria in African children (AQUAMAT): an open-label, randomised trial. Lancet 376: 1647-1657.
6. Villegas-Mendez A, Greig R, Shaw TN, de Souza JB, Gwyer Findlay E, et al. (2012) IFN-gamma-producing CD4+ T cells promote experimental cerebral malaria by modulating CD8+ T cell accumulation within the brain. J Immunol 189: 968-979.
7. Fauconnier M, Palomo J, Bourigault ML, Meme S, Szeremeta F, et al. (2012) IL-12Rbeta2 is essential for the development of experimental cerebral malaria. J Immunol 188: 1905-1914.
8. Lau LS, Fernandez Ruiz D, Davey GM, de Koning-Ward TF, Papenfuss AT, et al. (2011) Blood-stage Plasmodium berghei infection generates a potent, specific CD8+ T-cell response despite residence largely in cells lacking MHC I processing machinery. J Infect Dis 204: 1989-1996.
9. Villegas-Mendez A, de Souza JB, Murungi L, Hafalla JC, Shaw TN, et al. (2011) Heterogeneous and tissue-specific regulation of effector T cell responses by IFN-gamma during Plasmodium berghei ANKA infection. J Immunol 187: 2885-2897.
10. Claser C, Malleret B, Gun SY, Wong AY, Chang ZW, et al. (2011) CD8+ T cells and IFN-gamma mediate the time-dependent accumulation of infected red blood cells in deep organs during experimental cerebral malaria. PLoS One 6: e18720.
11. Nie CQ, Bernard NJ, Norman MU, Amante FH, Lundie RJ, et al. (2009) IP-10-mediated T cell homing promotes cerebral inflammation over splenic immunity to malaria infection. PLoS Pathog 5: e1000369.
12. Belnoue E, Potter SM, Rosa DS, Mauduit M, Gruner AC, et al. (2008) Control of pathogenic CD8+ T cell migration to the brain by IFN-gamma during experimental cerebral malaria. Parasite Immunol 30: 544-553.
13. Amani V, Vigario AM, Belnoue E, Marussig M, Fonseca L, et al. (2000) Involvement of IFN-gamma receptor-medicated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. Eur J Immunol 30: 1646-1655.
14. Rudin W, Favre N, Bordmann G, Ryffel B, (1997) Interferon-gamma is essential for the development of cerebral malaria. Eur J Immunol 27: 810-815.
15. Rudin W, Eugster HP, Bordmann G, Bonato J, Muller M, et al. (1997) Resistance to cerebral malaria in tumor necrosis factor-alpha/beta-deficient mice is associated with a reduction of intercellular adhesion molecule-1 up-regulation and T helper type 1 response. Am J Pathol 150: 257-266.
16. Grau GE, Heremans H, Piguet PF, Pointaire P, Lambert PH, et al. (1989) Monoclonal antibody against interferon gamma can prevent experimental cerebral malaria and its associated overproduction of tumor necrosis factor. Proc Natl Acad Sci U S A 86: 5572-5574.
17. de Miranda AS, Lacerda-Queiroz N, de Carvalho Vilela M, Rodrigues DH, Rachid MA, et al. (2011) Anxiety-like behavior and proinflammatory cytokine levels in the brain of C57BL/6 mice infected with Plasmodium berghei (strain ANKA). Neurosci Lett 491: 202-206.
18. Togbe D, de Sousa PL, Fauconnier M, Boissay V, Fick L, et al. (2008) Both functional LTbeta receptor and TNF receptor 2 are required for the development of experimental cerebral malaria. PLoS One 3: e2608.
19. Engwerda CR, Mynott TL, Sawhney S, De Souza JB, Bickle QD, et al. (2002) Locally up-regulated lymphotoxin alpha, not systemic tumor necrosis factor alpha, is the principle mediator of murine cerebral malaria. J Exp Med 195: 1371-1377.
20. Grau GE, Lou JN, (1995) Experimental cerebral malaria: possible new mechanisms in the TNF-induced microvascular pathology. Soz Praventivmed 40: 50-57.
21. de Kossodo S, Grau GE, (1993) Profiles of cytokine production in relation with susceptibility to cerebral malaria. J Immunol 151: 4811-4820.
22. Grau GE, Fajardo LF, Piguet PF, Allet B, Lambert PH, et al. (1987) Tumor necrosis factor (cachectin) as an essential mediator in murine cerebral malaria. Science 237: 1210-1212.
23. Achtman AH, Pilat S, Law CW, Lynn DJ, Janot L, et al. (2012) Effective adjunctive therapy by an innate defense regulatory peptide in a preclinical model of severe malaria. Sci Transl Med 4: 135ra164.
24. Serghides L, Kim H, Lu Z, Kain DC, Miller C, et al. (2011) Inhaled nitric oxide reduces endothelial activation and parasite accumulation in the brain, and enhances survival in experimental cerebral malaria. PLoS One 6: e27714.
25. Serghides L, (2012) The Case for the Use of PPARgamma Agonists as an Adjunctive Therapy for Cerebral Malaria. PPAR Res 2012: 513865.
26. John CC, Kutamba E, Mugarura K, Opoka RO, (2010) Adjunctive therapy for cerebral malaria and other severe forms of Plasmodium falciparum malaria. Expert Rev Anti Infect Ther 8: 997-1008.
27. Charunwatthana P, Abul Faiz M, Ruangveerayut R, Maude RJ, Rahman MR, et al. (2009) N-acetylcysteine as adjunctive treatment in severe malaria: a randomized, double-blinded placebo-controlled clinical trial. Crit Care Med 37: 516-522.
28. Bienvenu AL, Ferrandiz J, Kaiser K, Latour C, Picot S, (2008) Artesunate-erythropoietin combination for murine cerebral malaria treatment. Acta Trop 106: 104-108.
29. Day N, Dondorp AM, (2007) The management of patients with severe malaria. Am J Trop Med Hyg 77: 29-35.
30. Penet MF, Abou-Hamdan M, Coltel N, Cornille E, Grau GE, et al. (2008) Protection against cerebral malaria by the low-molecular-weight thiol pantethine. Proc Natl Acad Sci U S A 105: 1321-1326.
31. Planche T, Krishna S, (2005) The relevance of malaria pathophysiology to strategies of clinical management. Curr Opin Infect Dis 18: 369-375.
32. Craig AG, Grau GE, Janse C, Kazura JW, Milner D, et al. (2012) The role of animal models for research on severe malaria. PLoS Pathog 8: e1002401.
33. Renia L, Potter SM, Mauduit M, Rosa DS, Kayibanda M, et al. (2006) Pathogenic T cells in cerebral malaria. Int J Parasitol 36: 547-554.
34. Hunt NH, Grau GE, Engwerda C, Barnum SR, van der Heyde H, et al. (2010) Murine cerebral malaria: the whole story. Trends Parasitol 26: 272-274.
35. Hunt NH, Grau GE, (2003) Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol 24: 491-499.
36. Serhan CN, Krishnamoorthy S, Recchiuti A, Chiang N, (2011) Novel anti-inflammatory--pro-resolving mediators and their receptors. Curr Top Med Chem 11: 629-647.
37. Serhan CN, (2007) Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. Annu Rev Immunol 25: 101-137.
38. Aliberti J, Hieny S, Reis e Sousa C, Serhan CN, Sher A, (2002) Lipoxin-mediated inhibition of IL-12 production by DCs: a mechanism for regulation of microbial immunity. Nat Immunol 3: 76-82.
39. Aliberti J, Serhan C, Sher A, (2002) Parasite-induced lipoxin A4 is an endogenous regulator of IL-12 production and immunopathology in Toxoplasma gondii infection. J Exp Med 196: 1253-1262.
40. Bafica A, Scanga CA, Serhan C, Machado F, White S, et al. (2005) Host control of Mycobacterium tuberculosis is regulated by 5-lipoxygenase-dependent lipoxin production. J Clin Invest 115: 1601-1606.
41. Herb F, Thye T, Niemann S, Browne EN, Chinbuah MA, et al. (2008) ALOX5 variants associated with susceptibility to human pulmonary tuberculosis. Hum Mol Genet 17: 1052-1060.
42. Birnbaum Y, Ye Y, Lin Y, Freeberg SY, Huang MH, et al. (2007) Aspirin augments 15-epi-lipoxin A4 production by lipopolysaccharide, but blocks the pioglitazone and atorvastatin induction of 15-epi-lipoxin A4 in the rat heart. Prostaglandins Other Lipid Mediat 83: 89-98.
43. Birnbaum Y, Ye Y, Lin Y, Freeberg SY, Nishi SP, et al. (2006) Augmentation of myocardial production of 15-epi-lipoxin-a4 by pioglitazone and atorvastatin in the rat. Circulation 114: 929-935.
44. Serhan CN, Maddox JF, Petasis NA, Akritopoulou-Zanze I, Papayianni A, et al. (1995) Design of lipoxin A4 stable analogs that block transmigration and adhesion of human neutrophils. Biochemistry 34: 14609-14615.
45. Palmer CD, Guinan EC, Levy O, (2011) Deficient expression of bactericidal/permeability-increasing protein in immunocompromised hosts: translational potential of replacement therapy. Biochem Soc Trans 39: 994-999.
46. Walker J, Dichter E, Lacorte G, Kerner D, Spur B, et al. (2011) Lipoxin a4 increases survival by decreasing systemic inflammation and bacterial load in sepsis. Shock 36: 410-416.
47. Aliberti J, (2005) Host persistence: exploitation of anti-inflammatory pathways by Toxoplasma gondii. Nat Rev Immunol 5: 162-170.
48. McBerry C, Gonzalez RM, Shryock N, Dias A, Aliberti J, (2012) SOCS2-induced proteasome-dependent TRAF6 degradation: a common anti-inflammatory pathway for control of innate immune responses. PLoS One 7: e38384.
49. Schwab JM, Chiang N, Arita M, Serhan CN, (2007) Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 447: 869-874.
50. Takano T, Clish CB, Gronert K, Petasis N, Serhan CN, (1998) Neutrophil-mediated changes in vascular permeability are inhibited by topical application of aspirin-triggered 15-epi-lipoxin A4 and novel lipoxin B4 stable analogues. J Clin Invest 101: 819-826.
51. Maddox JF, Hachicha M, Takano T, Petasis NA, Fokin VV, et al. (1997) Lipoxin A4 stable analogs are potent mimetics that stimulate human monocytes and THP-1 cells via a G-protein-linked lipoxin A4 receptor. J Biol Chem 272: 6972-6978.
52. Higgins SJ, Kain KC, Liles WC, (2011) Immunopathogenesis of falciparum malaria: implications for adjunctive therapy in the management of severe and cerebral malaria. Expert Rev Anti Infect Ther 9: 803-819.
53. Van den Steen PE, Geurts N, Deroost K, Van Aelst I, Verhenne S, et al. (2010) Immunopathology and dexamethasone therapy in a new model for malaria-associated acute respiratory distress syndrome. Am J Respir Crit Care Med 181: 957-968.
54. Prasad K, Garner P, (2000) Steroids for treating cerebral malaria. Cochrane Database Syst Rev CD000972.
55. Rampengan TH, (1991) Cerebral malaria in children. Comparative study between heparin, dexamethasone and placebo. Paediatr Indones 31: 59-66.
56. Hoffman SL, Rustama D, Punjabi NH, Surampaet B, Sanjaya B, et al. (1988) High-dose dexamethasone in quinine-treated patients with cerebral malaria: a double-blind, placebo-controlled trial. J Infect Dis 158: 325-331.
57. Wyler DJ, (1988) Steroids are out in the treatment of cerebral malaria: what's next? J Infect Dis 158: 320-324.
58. Willcox ML, (2001) Salicylates, nitric oxide, malaria, and Reye's syndrome. Lancet 357: 1881-1882.
59. Keri JE, Thomas K, Berman B, Falabella A, (2000) Purpura fulminans in a patient with malaria. Eur J Dermatol 10: 617-619.
60. Morris T, Stables M, Hobbs A, de Souza P, Colville-Nash P, et al. (2009) Effects of low-dose aspirin on acute inflammatory responses in humans. J Immunol 183: 2089-2096.