Genetic susceptibility to Chagas disease cardiomyopathy: Involvement of several genes of the innate immunity and chemokine-dependent migration pathways

BMC Infectious Diseases

Volumn 13, Issue 1, 2013, Pages

  Frade, Amanda F ^a,b,e   Pissetti, Cristina W ^c   Ianni, Barbara M ^a   Saba, Bruno ^d   Lin Wang, Hui T ^d   Nogueira, Luciana G ^a,b   De Melo Borges, Ariana ^c   Buck, Paula ^a   Dias, Fabrício ^a   Baron, Monique ^a   Ferreira, Ludmila Rodrigues P ^a   Schmidt, Andre ^a   Marin Neto, José A ^a   Hirata, Mario ^d   Sampaio, Marcelo ^d   Fragata, Abílio ^d   Pereira, Alexandre C ^a   Donadi, Eduardo ^a   Kalil, Jorge ^a,b   Rodrigues, Virmondes ^c   Cunha Neto, Edecio ^a,b   Chevillard, Christophe ^e   more..

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Institute of Investigation in Immunology iii   (Brazil)

^c FEDERAL UNIVERSITY OF TRIÂNGULO MINEIRO   (Brazil)

^d Instituto de Cardiologia Dante Pazzanese   (Brazil)

^e AIX MARSEILLE UNIVERSITY   (France)

Author keywords

CCL2; CCR5; Chagas disease; Susceptibility; TIRAP

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CCR5; MONOCYTE CHEMOTACTIC PROTEIN 1;

ADULT; ARTICLE; BRAZIL; CCL2 GENE; CCR5 GENE; CHAGAS DISEASE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC SUSCEPTIBILITY; GENOTYPE; HEART LEFT VENTRICLE EJECTION FRACTION; HUMAN; INNATE IMMUNITY; LYMPHOCYTE MIGRATION; MAJOR CLINICAL STUDY; MAL TIRAP GENE; MALE; MIDDLE AGED; MONOCYTE; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE;

ADULT; AGED; BRAZIL; CHAGAS CARDIOMYOPATHY; CHEMOKINE CCL2; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HUMANS; IMMUNITY, INNATE; MALE; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, CCR5; RECEPTORS, INTERLEUKIN-1; TRYPANOSOMA CRUZI;

EID: 84889972716     PISSN: None     EISSN: 14712334     Source Type: Journal    
DOI: 10.1186/1471-2334-13-587     Document Type: Article

References (64)

1. Schofield CJ, Jannin J, Salvatella R. The future of Chagas disease control. Trends Parasitol 2006, 22(12):583-588. 10.1016/j.pt.2006.09.011, 17049308.
2. Coura JR. Chagas disease: what is known and what is needed-a background article. Mem Inst Oswaldo Cruz 2007, 102(Suppl 1):113-122.
3. Kirchhoff LV, Weiss LM, Wittner M, Tanowitz HB. Parasitic diseases of the heart. Front Biosci 2004, 9:706-723. 10.2741/1255, 14766402.
4. Barbosa AP, Cardinalli Neto A, Otaviano AP, Rocha BF, Bestetti RB. Comparison of outcome between Chagas cardiomyopathy and idiopathic dilated cardiomyopathy. Arq Bras Cardiol 2011, 97(6):517-525. 10.1590/S0066-782X2011005000112, 22030565.
5. Bestetti RB, Muccillo G. Clinical course of Chagas' heart disease: a comparison with dilated cardiomyopathy. Int J Cardiol 1997, 60(2):187-193. 10.1016/S0167-5273(97)00083-1, 9226290.
6. Bafica A, Santiago HC, Goldszmid R, Ropert C, Gazzinelli RT, Sher A. Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection. J Immunol 2006, 177(6):3515-3519.
7. Reis MM, Higuchi Mde L, Benvenuti LA, Aiello VD, Gutierrez PS, Bellotti G, Pileggi F. An in situ quantitative immunohistochemical study of cytokines and IL-2R + in chronic human chagasic myocarditis: correlation with the presence of myocardial Trypanosoma cruzi antigens. Clin Immunol Immunopathol 1997, 83(2):165-172. 10.1006/clin.1997.4335, 9143377.
8. Bilate AM, Cunha-Neto E. Chagas disease cardiomyopathy: current concepts of an old disease. Rev Inst Med Trop Sao Paulo 2008, 50(2):67-74. 10.1590/S0036-46652008007500001, 18488083.
9. Muller U, Kohler G, Mossmann H, Schaub GA, Alber G, Di Santo JP, Brombacher F, Holscher C. IL-12-independent IFN-gamma production by T cells in experimental Chagas' disease is mediated by IL-18. J Immunol 2001, 167(6):3346-3353.
10. Rocha Rodrigues DB, dos Reis MA, Romano A, Pereira SA, Teixeira Vde P, Tostes S, Rodrigues V. In situ expression of regulatory cytokines by heart inflammatory cells in Chagas' disease patients with heart failure. Clin Dev Immunol 2013, 2012:361730.
11. Ribeirao M, Pereira-Chioccola VL, Renia L, Augusto Fragata Filho A, Schenkman S, Rodrigues MM. Chagasic patients develop a type 1 immune response to Trypanosoma cruzi trans-sialidase. Parasite Immunol 2000, 22(1):49-53. 10.1046/j.1365-3024.2000.00260.x, 10607290.
12. Cunha-Neto E, Dzau VJ, Allen PD, Stamatiou D, Benvenutti L, Higuchi ML, Koyama NS, Silva JS, Kalil J, Liew CC. Cardiac gene expression profiling provides evidence for cytokinopathy as a molecular mechanism in Chagas' disease cardiomyopathy. Am J Pathol 2005, 167(2):305-313. 10.1016/S0002-9440(10)62976-8, 1603558, 16049318.
13. Cunha-Neto E, Kalil J. Heart-infiltrating and peripheral T cells in the pathogenesis of human Chagas' disease cardiomyopathy. Autoimmunity 2001, 34(3):187-192. 10.3109/08916930109007383, 11908776.
14. Talvani A, Rocha MO, Barcelos LS, Gomes YM, Ribeiro AL, Teixeira MM. Elevated concentrations of CCL2 and tumor necrosis factor-alpha in chagasic cardiomyopathy. Clin Infect Dis 2004, 38(7):943-950. 10.1086/381892, 15034825.
15. Gomes JA, Bahia-Oliveira LM, Rocha MO, Martins-Filho OA, Gazzinelli G, Correa-Oliveira R. Evidence that development of severe cardiomyopathy in human Chagas' disease is due to a Th1-specific immune response. Infect Immun 2003, 71(3):1185-1193. 10.1128/IAI.71.3.1185-1193.2003, 148818, 12595431.
16. Talvani A, Rocha MO, Ribeiro AL, Correa-Oliveira R, Teixeira MM. Chemokine receptor expression on the surface of peripheral blood mononuclear cells in Chagas disease. J Infect Dis 2004, 189(2):214-220. 10.1086/380803, 14722885.
17. Araujo FF, Gomes JA, Rocha MO, Williams-Blangero S, Pinheiro VM, Morato MJ, Correa-Oliveira R. Potential role of CD4 + CD25HIGH regulatory T cells in morbidity in Chagas disease. Front Biosci 2007, 12:2797-2806. 10.2741/2273, 17485260.
18. Guedes PM, Gutierrez FR, Silva GK, Dellalibera-Joviliano R, Rodrigues GJ, Bendhack LM, Rassi A, Rassi A, Schmidt A, Maciel BC, et al. Deficient regulatory T cell activity and low frequency of IL-17-producing T cells correlate with the extent of cardiomyopathy in human Chagas' disease. PLoS Negl Trop Dis 2012, 6(4):e1630. 10.1371/journal.pntd.0001630, 3335880, 22545173.
19. Magalhaes LM, Villani FN, Nunes Mdo C, Gollob KJ, Rocha MO, Dutra WO. High interleukin 17 expression is correlated with better cardiac function in human Chagas disease. J Infect Dis 2013, 207(4):661-665. 10.1093/infdis/jis724, 23204182.
20. Abel LC, Rizzo LV, Ianni B, Albuquerque F, Bacal F, Carrara D, Bocchi EA, Teixeira HC, Mady C, Kalil J, et al. Chronic Chagas' disease cardiomyopathy patients display an increased IFN-gamma response to Trypanosoma cruzi infection. J Autoimmun 2001, 17(1):99-107. 10.1006/jaut.2001.0523, 11488642.
21. Reis DD, Jones EM, Tostes S, Lopes ER, Chapadeiro E, Gazzinelli G, Colley DG, McCurley TL. Expression of major histocompatibility complex antigens and adhesion molecules in hearts of patients with chronic Chagas' disease. Am J Trop Med Hyg 1993, 49(2):192-200.
22. Nogueira LG, Santos RH, Ianni BM, Fiorelli AI, Mairena EC, Benvenuti LA, Frade A, Donadi E, Dias F, Saba B, et al. Myocardial Chemokine expression and intensity of myocarditis in Chagas cardiomyopathy Are controlled by polymorphisms in CXCL9 and CXCL10. PLoS Negl Trop Dis 2012, 6(10):e1867. 10.1371/journal.pntd.0001867, 3493616, 23150742.
23. Gomes JA, Bahia-Oliveira LM, Rocha MO, Busek SC, Teixeira MM, Silva JS, Correa-Oliveira R. Type 1 chemokine receptor expression in Chagas' disease correlates with morbidity in cardiac patients. Infect Immun 2005, 73(12):7960-7966. 10.1128/IAI.73.12.7960-7966.2005, 1307097, 16299288.
24. Zicker F, Smith PG, Netto JC, Oliveira RM, Zicker EM. Physical activity, opportunity for reinfection, and sibling history of heart disease as risk factors for Chagas' cardiopathy. Am J Trop Med Hyg 1990, 43(5):498-505.
25. Llop E, Rothhammer F, Acuna M, Apt W. HLA antigens in cardiomyopathic Chilean chagasics. Am J Hum Genet 1988, 43(5):770-773. 1715553, 3189340.
26. Llop E, Rothhammer F, Acuna M, Apt W, Arribada A. HLA antigens in Chagas cardiomyopathy: new evidence based on a case-control study. Rev Med Chil 1991, 119(6):633-636.
27. Fernandez-Mestre MT, Layrisse Z, Montagnani S, Acquatella H, Catalioti F, Matos M, Balbas O, Makhatadze N, Dominguez E, Herrera F, et al. Influence of the HLA class II polymorphism in chronic Chagas' disease. Parasite Immunol 1998, 20(4):197-203.
28. Layrisse Z, Fernandez MT, Montagnani S, Matos M, Balbas O, Herrera F, Colorado IA, Catalioti F, Acquatella H. HLA-C(*)03 is a risk factor for cardiomyopathy in Chagas disease. Hum Immunol 2000, 61(9):925-929. 10.1016/S0198-8859(00)00161-0, 11053636.
29. Deghaide NH, Dantas RO, Donadi EA. HLA class I and II profiles of patients presenting with Chagas' disease. Dig Dis Sci 1998, 43(2):246-252. 10.1023/A:1018829600200, 9512114.
30. Colorado IA, Acquatella H, Catalioti F, Fernandez MT, Layrisse Z. HLA class II DRB1, DQB1, DPB1 polymorphism and cardiomyopathy due to Trypanosoma cruzi chronic infection. Hum Immunol 2000, 61(3):320-325. 10.1016/S0198-8859(99)00177-9, 10689123.
31. Rodriguez-Perez JM, Cruz-Robles D, Hernandez-Pacheco G, Perez-Hernandez N, Murguia LE, Granados J, Reyes PA, Vargas-Alarcon G. Tumor necrosis factor-alpha promoter polymorphism in Mexican patients with Chagas' disease. Immunol Lett 2005, 98(1):97-102. 10.1016/j.imlet.2004.10.017, 15790514.
32. Campelo V, Dantas RO, Simoes RT, Mendes-Junior CT, Sousa SM, Simoes AL, Donadi EA. TNF microsatellite alleles in Brazilian Chagasic patients. Dig Dis Sci 2007, 52(12):3334-3339. 10.1007/s10620-006-9699-7, 17712635.
33. Drigo SA, Cunha-Neto E, Ianni B, Mady C, Fae KC, Buck P, Kalil J, Goldberg AC. Lack of association of tumor necrosis factor-alpha polymorphisms with Chagas disease in Brazilian patients. Immunol Lett 2007, 108(1):109-111. 10.1016/j.imlet.2006.10.008, 17141882.
34. Beraun Y, Nieto A, Collado MD, Gonzalez A, Martin J. Polymorphisms at tumor necrosis factor (TNF) loci are not associated with Chagas' disease. Tissue Antigens 1998, 52(1):81-83. 10.1111/j.1399-0039.1998.tb03028.x, 9714479.
35. Drigo SA, Cunha-Neto E, Ianni B, Cardoso MR, Braga PE, Fae KC, Nunes VL, Buck P, Mady C, Kalil J, et al. TNF gene polymorphisms are associated with reduced survival in severe Chagas' disease cardiomyopathy patients. Microbes Infect 2006, 8(3):598-603. 10.1016/j.micinf.2005.08.009, 16427798.
36. Florez O, Martin J, Gonzalez CI. Interleukin 4, interleukin 4 receptor-alpha and interleukin 10 gene polymorphisms in Chagas disease. Parasite Immunol 2011, 33(9):506-511. 10.1111/j.1365-3024.2011.01314.x, 21729106.
37. Cruz-Robles D, Chavez-Gonzalez JP, Cavazos-Quero MM, Perez-Mendez O, Reyes PA, Vargas-Alarcon G. Association between IL-1B and IL-1RN gene polymorphisms and Chagas' disease development susceptibility. Immunol Invest 2009, 38(3-4):231-239.
38. Costa GC, da Costa Rocha MO, Moreira PR, Menezes CA, Silva MR, Gollob KJ, Dutra WO. Functional IL-10 gene polymorphism is associated with Chagas disease cardiomyopathy. J Infect Dis 2009, 199(3):451-454. 10.1086/596061, 19099482.
39. Moreno M, Silva EL, Ramirez LE, Palacio LG, Rivera D, Arcos-Burgos M. Chagas' disease susceptibility/resistance: linkage disequilibrium analysis suggests epistasis between major histocompatibility complex and interleukin-10. Tissue Antigens 2004, 64(1):18-24. 10.1111/j.1399-0039.2004.00260.x, 15191519.
40. Zafra G, Morillo C, Martin J, Gonzalez A, Gonzalez CI. Polymorphism in the 3′ UTR of the IL12B gene is associated with Chagas' disease cardiomyopathy. Microbes Infect 2007, 9(9):1049-1052. 10.1016/j.micinf.2007.04.010, 17644387.
41. Ramasawmy R, Cunha-Neto E, Fae KC, Borba SC, Teixeira PC, Ferreira SC, Goldberg AC, Ianni B, Mady C, Kalil J. Heterozygosity for the S180L variant of MAL/TIRAP, a gene expressing an adaptor protein in the Toll-like receptor pathway, is associated with lower risk of developing chronic Chagas cardiomyopathy. J Infect Dis 2009, 199(12):1838-1845. 10.1086/599212, 19456234.
42. Ramasawmy R, Cunha-Neto E, Fae KC, Martello FG, Muller NG, Cavalcanti VL, Ianni B, Mady C, Kalil J, Goldberg AC. The monocyte chemoattractant protein-1 gene polymorphism is associated with cardiomyopathy in human chagas disease. Clin Infect Dis 2006, 43(3):305-311. 10.1086/505395, 16804844.
43. Ramasawmy R, Cunha-Neto E, Fae KC, Muller NG, Cavalcanti VL, Drigo SA, Ianni B, Mady C, Kalil J, Goldberg AC. BAT1, a putative anti-inflammatory gene, is associated with chronic Chagas cardiomyopathy. J Infect Dis 2006, 193(10):1394-1399. 10.1086/503368, 16619187.
44. Ramasawmy R, Fae KC, Cunha-Neto E, Muller NG, Cavalcanti VL, Ferreira RC, Drigo SA, Ianni B, Mady C, Goldberg AC, et al. Polymorphisms in the gene for lymphotoxin-alpha predispose to chronic Chagas cardiomyopathy. J Infect Dis 2007, 196(12):1836-1843. 10.1086/523653, 18190265.
45. Pissetti CW, de Oliveira RF, Correia D, Nascentes GA, Llaguno MM, Rodrigues V. Association between the lymphotoxin-alpha gene polymorphism and chagasic cardiopathy. J Interferon Cytokine Res 2013, 33(3):130-135. 10.1089/jir.2012.0024, 23289732.
46. Ramasawmy R, Fae KC, Cunha-Neto E, Borba SC, Ianni B, Mady C, Goldberg AC, Kalil J. Variants in the promoter region of IKBL/NFKBIL1 gene may mark susceptibility to the development of chronic Chagas' cardiomyopathy among Trypanosoma cruzi-infected individuals. Mol Immunol 2008, 45(1):283-288. 10.1016/j.molimm.2007.04.015, 17544510.
47. Calzada JE, Nieto A, Beraun Y, Martin J. Chemokine receptor CCR5 polymorphisms and Chagas' disease cardiomyopathy. Tissue Antigens 2001, 58(3):154-158. 10.1034/j.1399-0039.2001.580302.x, 11703822.
48. Fernandez-Mestre MT, Montagnani S, Layrisse Z. Is the CCR5-59029-G/G genotype a protective factor for cardiomyopathy in Chagas disease?. Hum Immunol 2004, 65(7):725-728. 10.1016/j.humimm.2004.05.002, 15301862.
49. Torres OA, Calzada JE, Beraun Y, Morillo CA, Gonzalez CI, Gonzalez A, Martin J. Association of the macrophage migration inhibitory factor -173G/C polymorphism with Chagas disease. Hum Immunol 2009, 70(7):543-546. 10.1016/j.humimm.2009.04.022, 19376177.
50. Torres OA, Calzada JE, Beraun Y, Morillo CA, Gonzalez A, Gonzalez CI, Martin J. Role of the IFNG +874 T/A polymorphism in Chagas disease in a Colombian population. Infect Genet Evol 2010, 10(5):682-685. 10.1016/j.meegid.2010.03.009, 20359550.
51. Cunha-Neto E, Kalil J. Autoimmunity in Chagas' heart disease. Sao Paulo Med J 1995, 113(2):757-766.
52. Teixeira PC, Frade AF, Nogueira LG, Kalil J, Chevillard C, Cunha-Neto E. Pathogenesis of Chagas disease cardiomyopathy. World J Clin Infect Dis 2012, 2(3):39-53.
53. Vasconcelos RH, Montenegro SM, Azevedo EA, Gomes YM, Morais CN. Genetic susceptibility to chronic Chagas disease: an overview of single nucleotide polymorphisms of cytokine genes. Cytokine 2012, 59(2):203-208. 10.1016/j.cyto.2012.04.035, 22595647.
54. Fae KC, Drigo SA, Cunha-Neto E, Ianni B, Mady C, Kalil J, Goldberg AC. HLA and beta-myosin heavy chain do not influence susceptibility to Chagas disease cardiomyopathy. Microbes Infect 2000, 2(7):745-751. 10.1016/S1286-4579(00)00501-3, 10955954.
55. Weitzel T, Zulantay I, Danquah I, Hamann L, Schumann RR, Apt W, Mockenhaupt FP. Mannose-binding lectin and Toll-like receptor polymorphisms and Chagas disease in Chile. Am J Trop Med Hyg 2012, 86(2):229-232. 10.4269/ajtmh.2012.11-0539, 3269271, 22302853.
56. Jorge MT, Macedo TA, Janones RS, Carizzi DP, Heredia RA, Acha RE. Types of arrhythmia among cases of American trypanosomiasis, compared with those in other cardiology patients. Ann Trop Med Parasitol 2003, 97(2):139-148. 10.1179/000349803235001561, 12803869.
57. van Veldhuisen DJ, Linssen GC, Jaarsma T, van Gilst WH, Hoes AW, Tijssen JG, Paulus WJ, Voors AA, Hillege HL. B-type natriuretic peptide and prognosis in heart failure patients with preserved and reduced ejection fraction. J Am Coll Cardiol 2013, 61(14):1498-1506. 10.1016/j.jacc.2012.12.044, 23500300.
58. Januzzi JL. Natriuretic peptides, ejection fraction, and prognosis: parsing the phenotypes of heart failure. J Am Coll Cardiol 2013, 61(14):1507-1509. 10.1016/j.jacc.2013.01.039, 23500284.
59. Barretto AC, Arteaga E, Mady C, Ianni BM, Bellotti G, Pileggi F. Male sex. Prognostic factor in Chagas' disease. Arq Bras Cardiol 1993, 60(4):225-227.
60. Basquiera AL, Sembaj A, Aguerri AM, Omelianiuk M, Guzman S, Moreno Barral J, Caeiro TF, Madoery RJ, Salomone OA. Risk progression to chronic Chagas cardiomyopathy: influence of male sex and of parasitaemia detected by polymerase chain reaction. Heart 2003, 89(10):1186-1190. 10.1136/heart.89.10.1186, 1767891, 12975414.
61. Florez O, Martin J, Gonzalez CI. Genetic variants in the chemokines and chemokine receptors in Chagas disease. Hum Immunol 2012, 73(8):852-858. 10.1016/j.humimm.2012.04.005, 22537745.
62. Marino AP, da Silva A, dos Santos P, Pinto LM, Gazzinelli RT, Teixeira MM, Lannes-Vieira J. Regulated on activation, normal T cell expressed and secreted (RANTES) antagonist (Met-RANTES) controls the early phase of Trypanosoma cruzi-elicited myocarditis. Circulation 2004, 110(11):1443-1449. 10.1161/01.CIR.0000141561.15939.EC, 15337689.
63. Medeiros GA, Silverio JC, Marino AP, Roffe E, Vieira V, Kroll-Palhares K, Carvalho CE, Silva AA, Teixeira MM, Lannes-Vieira J. Treatment of chronically Trypanosoma cruzi-infected mice with a CCR1/CCR5 antagonist (Met-RANTES) results in amelioration of cardiac tissue damage. Microbes Infect 2009, 11(2):264-273. 10.1016/j.micinf.2008.11.012, 19100857.
64. Marino AP, Silva AA, Santos PV, Pinto LM, Gazinelli RT, Teixeira MM, Lannes-Vieira J. CC-chemokine receptors: a potential therapeutic target for Trypanosoma cruzi-elicited myocarditis. Mem Inst Oswaldo Cruz 2005, 100(Suppl 1):93-96.