Simvastatin and Benznidazole-Mediated Prevention of Trypanosoma cruzi-Induced Endothelial Activation: Role of 15-epi-lipoxin A4 in the Action of Simvastatin

PLoS Neglected Tropical Diseases

Volumn 9, Issue 5, 2015, Pages

  Campos Estrada, Carolina ^a   Liempi, Ana ^a   González Herrera, Fabiola ^a   Lapier, Michel ^a   Kemmerling, Ulrike ^a   Pesce, Barbara ^a   Ferreira, Jorge ^a   López Muñoz, Rodrigo ^a,b   Maya, Juan D ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

15 EPI LIPOXIN A4; ARACHIDONATE 5 LIPOXYGENASE; BENZNIDAZOLE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOXIN A; SIMVASTATIN; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; ANTITRYPANOSOMAL AGENT; CELL ADHESION MOLECULE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LIPOXIN; NITROIMIDAZOLE DERIVATIVE;

AMASTIGOTE; ARTICLE; CELL MIGRATION; CELL VIABILITY; CHAGAS DISEASE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOTHELIUM; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; LEUKOCYTE ADHERENCE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TIME OF FLIGHT MASS SPECTROMETRY; TRYPANOSOMA CRUZI; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; CELL CULTURE; DRUG EFFECTS; PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULAR ENDOTHELIUM;

CELL ADHESION MOLECULES; CELLS, CULTURED; CHAGAS DISEASE; ENDOTHELIUM, VASCULAR; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; LIPOXINS; NF-KAPPA B; NITROIMIDAZOLES; SIGNAL TRANSDUCTION; SIMVASTATIN; TRYPANOCIDAL AGENTS;

EID: 84930644369     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003770     Document Type: Article

References (46)

1. WHO Working to overcome the global impact of neglected tropical diseases: first WHO report on neglected tropical diseases: update 2011. Geneva: World Health Organization. 2011. viii, 14 p. p.
2. Coura JR, Chagas disease: control, elimination and eradication. Is it possible? Mem Inst Oswaldo Cruz 2013; 108: 962–967. doi: 10.1590/0074-0276130565 24402148
3. Rassi A, Jr.Rassi A, Marcondes de Rezende J, American trypanosomiasis (Chagas disease). Infect Dis Clin North Am 2012; 26: 275–291. doi: 10.1016/j.idc.2012.03.002 22632639
4. Ribeiro AL, Nunes MP, Teixeira MM, Rocha MO, Diagnosis and management of Chagas disease and cardiomyopathy. Nat Rev Cardiol 2012; 9: 576–589. doi: 10.1038/nrcardio.2012.109 22847166
5. Andrade D, Serra R, Svensjo E, Lima AP, Ramos ES, Jr.et al. Trypanosoma cruzi invades host cells through the activation of endothelin and bradykinin receptors: a converging pathway leading to Chagasic vasculopathy. Br J Pharmacol 2012; 165: 1333–1347. doi: 10.1111/j.1476-5381.2011.01609.x 21797847
6. Molina-Berrios A, Campos-Estrada C, Lapier M, Duaso J, Kemmerling U, et al. Benznidazole prevents endothelial damage in an experimental model of Chagas disease. Acta Trop 2013; 127: 6–13. doi: 10.1016/j.actatropica.2013.03.006 23529066
7. Huang H, Petkova SB, Cohen AW, Bouzahzah B, Chan J, et al. Activation of transcription factors AP-1 and NF-kappa B in murine Chagasic myocarditis. Infect Immun 2003; 71: 2859–2867. 12704159
8. Prado CM, Jelicks LA, Weiss LM, Factor SM, Tanowitz HB, et al. The vasculature in Chagas disease. Adv Parasitol 2011; 76: 83–99. doi: 10.1016/B978-0-12-385895-5.00004-9 21884888
9. Rossi MA, Tanowitz HB, Malvestio LM, Celes MR, Campos EC, et al. Coronary microvascular disease in chronic Chagas cardiomyopathy including an overview on history, pathology, and other proposed pathogenic mechanisms. PLoS Negl Trop Dis 2010; 4: e674. doi: 10.1371/journal.pntd.0000674 20824217
10. Molina-Berrios A, Campos-Estrada C, Henriquez N, Faundez M, Torres G, et al. Protective role of acetylsalicylic acid in experimental Trypanosoma cruzi infection: evidence of a 15-epi-lipoxin A(4)-mediated effect. PLoS Negl Trop Dis 2013; 7: e2173. doi: 10.1371/journal.pntd.0002173 23638194
11. Melo L, Caldas IS, Azevedo MA, Goncalves KR, da Silva do Nascimento AF, et al. Low doses of simvastatin therapy ameliorate cardiac inflammatory remodeling in Trypanosoma cruzi-infected dogs. Am J Trop Med Hyg 2011; 84: 325–331. doi: 10.4269/ajtmh.2011.10-0451 21292909
12. Birnbaum Y, Ye Y, Lin Y, Freeberg SY, Huang MH, et al. 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 2007; 83: 89–98. 17259075
13. Aranda E, Owen GI, A semi-quantitative assay to screen for angiogenic compounds and compounds with angiogenic potential using the EA.hy926 endothelial cell line. Biol Res 2009; 42: 377–389. doi: /S0716-97602009000300012 19915746
14. Collins SJ, Gallo RC, Gallagher RE, Continuous growth and differentiation of human myeloid leukaemic cells in suspension culture. Nature 1977; 270: 347–349. 271272
15. Contreras VT, Araujo-Jorge TC, Bonaldo MC, Thomaz N, Barbosa HS, et al. Biological aspects of the Dm 28c clone of Trypanosoma cruzi after metacyclogenesis in chemically defined media. Mem Inst Oswaldo Cruz 1988; 83: 123–133. 3074237
16. Stach K, Nguyen XD, Lang S, Elmas E, Weiss C, et al. Simvastatin and atorvastatin attenuate VCAM-1 and uPAR expression on human endothelial cells and platelet surface expression of CD40 ligand. Cardiol J 2012; 19: 20–28. 22298164
17. Yang JC, Huang F, Wu CJ, Chen YC, Lu TH, et al. Simvastatin reduces VCAM-1 expression in human umbilical vein endothelial cells exposed to lipopolysaccharide. Inflamm Res 2012; 61: 485–491. doi: 10.1007/s00011-012-0435-9 22245985
18. Lopez-Munoz R, Faundez M, Klein S, Escanilla S, Torres G, et al. Trypanosoma cruzi: In vitro effect of aspirin with nifurtimox and benznidazole. Exp Parasitol 2010; 124: 167–171. doi: 10.1016/j.exppara.2009.09.005 19735656
19. Mosmann T, Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65: 55–63. 6606682
20. Chou TC, Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006; 58: 621–681. 16968952
21. Tong S, Neboori HJ, Tran ED, Schmid-Schonbein GW, Constitutive expression and enzymatic cleavage of ICAM-1 in the spontaneously hypertensive rat. J Vasc Res 2011; 48: 386–396. doi: 10.1159/000323474 21464573
22. Copaja M, Venegas D, Aranguiz P, Canales J, Vivar R, et al. Simvastatin disrupts cytoskeleton and decreases cardiac fibroblast adhesion, migration and viability. Toxicology 2012; 294: 42–49. doi: 10.1016/j.tox.2012.01.011 22306966
23. Liang Y, Li X, Zhang X, Li Z, Wang L, et al. Elevated levels of plasma TNF-alpha are associated with microvascular endothelial dysfunction in patients with sepsis through activating the NF-kappaB and p38 mitogen-activated protein kinase in endothelial cells. Shock 2014; 41: 275–281. doi: 10.1097/SHK.0000000000000116 24430552
24. Birnbaum Y, Ye Y, Pleiotropic effects of statins: the role of eicosanoid production. Curr Atheroscler Rep 2012; 14: 135–139. doi: 10.1007/s11883-012-0232-5 22286195
25. Yoshimoto T, Yokoyama C, Ochi K, Yamamoto S, Maki Y, et al. 2,3,5-Trimethyl-6-(12-hydroxy-5,10-dodecadiynyl)-1,4-benzoquinone (AA861), a selective inhibitor of the 5-lipoxygenase reaction and the biosynthesis of slow-reacting substance of anaphylaxis. Biochim Biophys Acta 1982; 713: 470–473. 6817808
26. Lee HM, Ok SH, Sung HJ, Eun SY, Kim HJ, et al. Mepivacaine-induced contraction involves phosphorylation of extracellular signal-regulated kinase through activation of the lipoxygenase pathway in isolated rat aortic smooth muscle. Can J Physiol Pharmacol 2013; 91: 285–294. doi: 10.1139/cjpp-2012-0197 23627840
27. Choi YS, Jeong YS, Ok SH, Shin IW, Lee SH, et al. The direct effect of levobupivacaine in isolated rat aorta involves lipoxygenase pathway activation and endothelial nitric oxide release. Anesth Analg 2010; 110: 341–349. doi: 10.1213/ANE.0b013e3181c76f52 19955508
28. Kim BJ, Kim SY, Lee S, Jeon JH, Matsui H, et al. The role of transient receptor potential channel blockers in human gastric cancer cell viability. Can J Physiol Pharmacol 2012; 90: 175–186. doi: 10.1139/y11-114 22308955
29. Lee S, Felts KA, Parry GC, Armacost LM, Cobb RR, Inhibition of 5-lipoxygenase blocks IL-1 beta-induced vascular adhesion molecule-1 gene expression in human endothelial cells. J Immunol 1997; 158: 3401–3407. 9120300
30. Kempe S, Kestler H, Lasar A, Wirth T, NF-kappaB controls the global pro-inflammatory response in endothelial cells: evidence for the regulation of a pro-atherogenic program. Nucleic Acids Res 2005; 33: 5308–5319. 16177180
31. Norata GD, Tibolla G, Seccomandi PM, Poletti A, Catapano AL, Dihydrotestosterone decreases tumor necrosis factor-alpha and lipopolysaccharide-induced inflammatory response in human endothelial cells. J Clin Endocrinol Metab 2006; 91: 546–554. 16317058
32. Dias WB, Fajardo FD, Graca-Souza AV, Freire-de-Lima L, Vieira F, et al. Endothelial cell signalling induced by trans-sialidase from Trypanosoma cruzi. Cell Microbiol 2008; 10: 88–99. 17672865
33. Cutrullis RA, Moscatelli GF, Moroni S, Volta BJ, Cardoni RL, et al. Benznidazole therapy modulates interferon-gamma and M2 muscarinic receptor autoantibody responses in Trypanosoma cruzi-infected children. PLoS One 2011; 6: e27133. doi: 10.1371/journal.pone.0027133 22066031
34. Manarin R, Pascutti MF, Ruffino JP, De Las Heras B, Bosca L, et al. Benznidazole blocks NF-kappaB activation but not AP-1 through inhibition of IKK. Mol Immunol 2010; 47: 2485–2491. doi: 10.1016/j.molimm.2010.06.002 20598748
35. Ronco MT, Manarin R, Frances D, Serra E, Revelli S, et al. Benznidazole treatment attenuates liver NF-kappaB activity and MAPK in a cecal ligation and puncture model of sepsis. Mol Immunol 2011; 48: 867–873. doi: 10.1016/j.molimm.2010.12.021 21269697
36. Silva RR, Shrestha-Bajracharya D, Almeida-Leite CM, Leite R, Bahia MT, et al. Short-term therapy with simvastatin reduces inflammatory mediators and heart inflammation during the acute phase of experimental Chagas disease. Mem Inst Oswaldo Cruz 2012; 107: 513–521. 22666863
37. Ortego M, Gomez-Hernandez A, Vidal C, Sanchez-Galan E, Blanco-Colio LM, et al. HMG-CoA reductase inhibitors reduce I kappa B kinase activity induced by oxidative stress in monocytes and vascular smooth muscle cells. J Cardiovasc Pharmacol 2005; 45: 468–475. 15821443
38. Berenbaum MC, What Is Synergy. Pharmacological Reviews 1989; 41: 93–141. 2692037
39. Fitzgerald JB, Schoeberl B, Nielsen UB, Sorger PK, Systems biology and combination therapy in the quest for clinical efficacy. Nat Chem Biol 2006; 2: 458–466. 16921358
40. Pavanelli WR, Gutierrez FR, Mariano FS, Prado CM, Ferreira BR, et al. 5-lipoxygenase is a key determinant of acute myocardial inflammation and mortality during Trypanosoma cruzi infection. Microbes Infect 2010; 12: 587–597. doi: 10.1016/j.micinf.2010.03.016 20381637
41. Machado FS, Dutra WO, Esper L, Gollob KJ, Teixeira MM, et al. Current understanding of immunity to Trypanosoma cruzi infection and pathogenesis of Chagas disease. Semin Immunopathol 2012; 34: 753–770. doi: 10.1007/s00281-012-0351-7 23076807
42. Talvani A, Teixeira MM, Inflammation and Chagas disease some mechanisms and relevance. Adv Parasitol 2011; 76: 171–194. doi: 10.1016/B978-0-12-385895-5.00008-6 21884892
43. Buckley CD, Gilroy DW, Serhan CN, Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. Immunity 2014; 40: 315–327. doi: 10.1016/j.immuni.2014.02.009 24656045
44. Chinthamani S, Odusanwo O, Mondal N, Nelson J, Neelamegham S, et al. Lipoxin A4 inhibits immune cell binding to salivary epithelium and vascular endothelium. Am J Physiol Cell Physiol 2012; 302: C968–978. doi: 10.1152/ajpcell.00259.2011 22205391
45. Serhan CN, Lipoxins and aspirin-triggered 15-epi-lipoxins are the first lipid mediators of endogenous anti-inflammation and resolution. Prostaglandins Leukot Essent Fatty Acids 2005; 73: 141–162. 16005201
46. Machado FS, Mukherjee S, Weiss LM, Tanowitz HB, Ashton AW, Bioactive lipids in Trypanosoma cruzi infection. Adv Parasitol 2011; 76: 1–31. doi: 10.1016/B978-0-12-385895-5.00001-3 21884885