Myocardial Chemokine Expression and Intensity of Myocarditis in Chagas Cardiomyopathy Are Controlled by Polymorphisms in CXCL9 and CXCL10

PLoS Neglected Tropical Diseases

Volumn 6, Issue 10, 2012, Pages

  Nogueira, Luciana Gabriel ^a,b   Santos, Ronaldo Honorato Barros ^a   Ianni, Barbara Maria ^a   Fiorelli, Alfredo Inácio ^a   Mairena, Eliane Conti ^a,b   Benvenuti, Luiz Alberto ^a   Frade, Amanda ^a,b   Donadi, Eduardo ^a   Dias, Fabrício ^a   Saba, Bruno ^c   Wang, Hui Tzu Lin ^c   Fragata, Abilio ^c   Sampaio, Marcelo ^c   Hirata, Mario Hiroyuki ^c   Buck, Paula ^a   Mady, Charles ^a   Bocchi, Edimar Alcides ^a   Stolf, Noedir Antonio ^a   Kalil, Jorge ^a,b   Cunha Neto, Edecio ^a,b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Institute of Investigation in Immunology iii   (Brazil)

^c INSTITUTO DANTE PAZZANESE DE CARDIOLOGIA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN NATRIURETIC PEPTIDE; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CCR8; CHEMOKINE RECEPTOR CXCR3; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MESSENGER RNA; THYMUS AND ACTIVATION REGULATED CHEMOKINE;

ADOLESCENT; ADULT; ARTICLE; CHAGAS DISEASE; CLINICAL ARTICLE/MAJOR CLINICAL??; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAPHY; FEMALE; GENE EXPRESSION; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC RISK; GENOTYPE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE FAILURE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; MALE; POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM;

ADOLESCENT; ADULT; CHAGAS CARDIOMYOPATHY; CHEMOKINE CXCL10; CHEMOKINE CXCL9; DISEASE RESISTANCE; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MALE; MIDDLE AGED; POLYMORPHISM, GENETIC; TRYPANOSOMA CRUZI; YOUNG ADULT;

EID: 84869001878     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001867     Document Type: Article

References (69)

1. Schofield CJ, Jannin J, Salvatella R, (2006) The future of Chagas disease control. Trends Parasitol 22: 583-588.
2. Kirchhoff LV, Weiss LM, Wittner M, Tanowitz HB, (2004) Parasitic diseases of the heart. Front Biosci 9: 706-723.
3. Martin UO, Afchain D, de Marteleur A, Ledesma O, Capron A, (1987) [Circulating immune complexes in different developmental stages of Chagas' disease]. Medicina (B Aires) 47: 159-162.
4. Coura JR, (2007) Chagas disease: what is known and what is needed-a background article. Mem Inst Oswaldo Cruz 102 Suppl 1: 113-122.
5. Higuchi ML, De Morais CF, Pereira Barreto AC, Lopes EA, Stolf N, et al. (1987) The role of active myocarditis in the development of heart failure in chronic Chagas' disease: a study based on endomyocardial biopsies. Clin Cardiol 10: 665-670.
6. Barbosa AP, Cardinalli Neto A, Otaviano AP, Rocha BF, Bestetti RB, (2011) Comparison of outcome between Chagas cardiomyopathy and idiopathic dilated cardiomyopathy. Arq Bras Cardiol 97: 517-525.
7. Bestetti RB, Muccillo G, (1997) Clinical course of Chagas' heart disease: a comparison with dilated cardiomyopathy. Int J Cardiol 60: 187-193.
8. Marin-Neto JA, Rassi A Jr, Morillo CA, Avezum A, Connolly SJ, et al. (2008) Rationale and design of a randomized placebo-controlled trial assessing the effects of etiologic treatment in Chagas' cardiomyopathy: the BENznidazole Evaluation For Interrupting Trypanosomiasis (BENEFIT). Am Heart J 156: 37-43.
9. Milei J, Storino R, Fernandez Alonso G, Beigelman R, Vanzulli S, et al. (1992) Endomyocardial biopsies in chronic chagasic cardiomyopathy. Immunohistochemical and ultrastructural findings. Cardiology 80: 424-437.
10. Cunha-Neto E, Nogueira LG, Teixeira PC, Ramasawmy R, Drigo SA, et al. (2009) Immunological and non-immunological effects of cytokines and chemokines in the pathogenesis of chronic Chagas disease cardiomyopathy. Mem Inst Oswaldo Cruz 104 Suppl 1: 252-258.
11. Higuchi Mde L, Gutierrez PS, Aiello VD, Palomino S, Bocchi E, et al. (1993) Immunohistochemical characterization of infiltrating cells in human chronic chagasic myocarditis: comparison with myocardial rejection process. Virchows Arch A Pathol Anat Histopathol 423: 157-160.
12. Reis DD, Jones EM, Tostes S Jr, Lopes ER, Gazzinelli G, et al. (1993) Characterization of inflammatory infiltrates in chronic chagasic myocardial lesions: presence of tumor necrosis factor-alpha+ cells and dominance of granzyme A+, CD8+ lymphocytes. Am J Trop Med Hyg 48: 637-644.
13. Reis MM, Higuchi Mde L, Benvenuti LA, Aiello VD, Gutierrez PS, et al. (1997) 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 83: 165-172.
14. Abel LC, Rizzo LV, Ianni B, Albuquerque F, Bacal F, et al. (2001) Chronic Chagas' disease cardiomyopathy patients display an increased IFN-gamma response to Trypanosoma cruzi infection. J Autoimmun 17: 99-107.
15. Morato MJ, Colley DG, Powell MR, (1998) Cytokine profiles during experimental Chagas' disease. Braz J Med Biol Res 31: 123-125.
16. Talvani A, Ribeiro CS, Aliberti JC, Michailowsky V, Santos PV, et al. (2000) Kinetics of cytokine gene expression in experimental chagasic cardiomyopathy: tissue parasitism and endogenous IFN-gamma as important determinants of chemokine mRNA expression during infection with Trypanosoma cruzi. Microbes Infect 2: 851-866.
17. Gomes JA, Bahia-Oliveira LM, Rocha MO, Martins-Filho OA, Gazzinelli G, et al. (2003) Evidence that development of severe cardiomyopathy in human Chagas' disease is due to a Th1-specific immune response. Infect Immun 71: 1185-1193.
18. Cunha-Neto E, Kalil J, (2001) Heart-infiltrating and peripheral T cells in the pathogenesis of human Chagas' disease cardiomyopathy. Autoimmunity 34: 187-192.
19. Anez N, Carrasco H, Parada H, Crisante G, Rojas A, et al. (1999) Myocardial parasite persistence in chronic chagasic patients. Am J Trop Med Hyg 60: 726-732.
20. Olivares-Villagomez D, McCurley TL, Vnencak-Jones CL, Correa-Oliveira R, Colley DG, et al. (1998) Polymerase chain reaction amplification of three different Trypanosoma cruzi DNA sequences from human chagasic cardiac tissue. Am J Trop Med Hyg 59: 563-570.
21. Fonseca SG, Moins-Teisserenc H, Clave E, Ianni B, Nunes VL, et al. (2005) Identification of multiple HLA-A*0201-restricted cruzipain and FL-160 CD8+ epitopes recognized by T cells from chronically Trypanosoma cruzi-infected patients. Microbes Infect 7: 688-697.
22. Cunha-Neto E, Coelho V, Guilherme L, Fiorelli A, Stolf N, et al. (1996) Autoimmunity in Chagas' disease. Identification of cardiac myosin-B13 Trypanosoma cruzi protein crossreactive T cell clones in heart lesions of a chronic Chagas' cardiomyopathy patient. J Clin Invest 98: 1709-1712.
23. Turner JE, Steinmetz OM, Stahl RA, Panzer U, (2007) Targeting of Th1-associated chemokine receptors CXCR3 and CCR5 as therapeutic strategy for inflammatory diseases. Mini Rev Med Chem 7: 1089-1096.
24. Teixeira MM, Gazzinelli RT, Silva JS, (2002) Chemokines, inflammation and Trypanosoma cruzi infection. Trends Parasitol 18: 262-265.
25. Marino AP, Silva AA, Santos PV, Pinto LM, Gazinelli RT, et al. (2005) CC-chemokine receptors: a potential therapeutic target for Trypanosoma cruzi-elicited myocarditis. Mem Inst Oswaldo Cruz 100 Suppl 1: 93-96.
26. Gomes JA, Bahia-Oliveira LM, Rocha MO, Busek SC, Teixeira MM, et al. (2005) Type 1 chemokine receptor expression in Chagas' disease correlates with morbidity in cardiac patients. Infect Immun 73: 7960-7966.
27. Cunha-Neto E, Dzau VJ, Allen PD, Stamatiou D, Benvenutti L, et al. (2005) Cardiac gene expression profiling provides evidence for cytokinopathy as a molecular mechanism in Chagas' disease cardiomyopathy. Am J Pathol 167: 305-313.
28. Groom JR, Luster AD, (2011) CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol Cell Biol 89: 207-215.
29. Calzada JE, Nieto A, Beraun Y, Martin J, (2001) Chemokine receptor CCR5 polymorphisms and Chagas' disease cardiomyopathy. Tissue Antigens 58: 154-158.
30. Nickel RG, Casolaro V, Wahn U, Beyer K, Barnes KC, et al. (2000) Atopic dermatitis is associated with a functional mutation in the promoter of the C-C chemokine RANTES. J Immunol 164: 1612-1616.
31. Sekiya T, Tsunemi Y, Miyamasu M, Ohta K, Morita A, et al. (2003) Variations in the human Th2-specific chemokine TARC gene. Immunogenetics 54: 742-745.
32. Jorge MT, Macedo TA, Janones RS, Carizzi DP, Heredia RA, et al. (2003) Types of arrhythmia among cases of American trypanosomiasis, compared with those in other cardiology patients. Ann Trop Med Parasitol 97: 139-148.
33. Fonseca SG, Reis MM, Coelho V, Nogueira LG, Monteiro SM, et al. (2007) Locally produced survival cytokines IL-15 and IL-7 may be associated to the predominance of CD8+ T cells at heart lesions of human chronic Chagas disease cardiomyopathy. Scand J Immunol 66: 362-371.
34. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, et al. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-622.
35. Bruck P, Bartsch W, Penna-Martinez M, Kahles H, Seidl C, et al. (2009) Polymorphisms of CXCR3-binding chemokines in type 1 diabetes. Hum Immunol 70: 552-555.
36. Soto-Sanchez J, Santos-Juanes J, Coto-Segura P, Coto E, Diaz M, et al. (2010) Genetic variation at the CCR5/CCR2 gene cluster and risk of psoriasis and psoriatic arthritis. Cytokine 50: 114-116.
37. Zhernakova A, Alizadeh BZ, Eerligh P, Hanifi-Moghaddam P, Schloot NC, et al. (2006) Genetic variants of RANTES are associated with serum RANTES level and protection for type 1 diabetes. Genes Immun 7: 544-549.
38. Reis DD, Jones EM, Tostes S, Lopes ER, Chapadeiro E, et al. (1993) Expression of major histocompatibility complex antigens and adhesion molecules in hearts of patients with chronic Chagas' disease. Am J Trop Med Hyg 49: 192-200.
39. Sallusto F, Mackay CR, Lanzavecchia A, (2000) The role of chemokine receptors in primary, effector, and memory immune responses. Annu Rev Immunol 18: 593-620.
40. Yates CC, Whaley D, Kulasekeran P, Hancock WW, Lu B, et al. (2007) Delayed and deficient dermal maturation in mice lacking the CXCR3 ELR-negative CXC chemokine receptor. Am J Pathol 171: 484-495.
41. Sallusto F, Lanzavecchia A, Mackay CR, (1998) Chemokines and chemokine receptors in T-cell priming and Th1/Th2-mediated responses. Immunol Today 19: 568-574.
42. Bonecchi R, Bianchi G, Bordignon PP, D'Ambrosio D, Lang R, et al. (1998) Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J Exp Med 187: 129-134.
43. D'Ambrosio D, Iellem A, Bonecchi R, Mazzeo D, Sozzani S, et al. (1998) Selective up-regulation of chemokine receptors CCR4 and CCR8 upon activation of polarized human type 2 Th cells. J Immunol 161: 5111-5115.
44. Forster R, Davalos-Misslitz AC, Rot A, (2008) CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol 8: 362-371.
45. Abe R, Donnelly SC, Peng T, Bucala R, Metz CN, (2001) Peripheral blood fibrocytes: differentiation pathway and migration to wound sites. J Immunol 166: 7556-7562.
46. Riol-Blanco L, Sanchez-Sanchez N, Torres A, Tejedor A, Narumiya S, et al. (2005) The chemokine receptor CCR7 activates in dendritic cells two signaling modules that independently regulate chemotaxis and migratory speed. J Immunol 174: 4070-4080.
47. Farber JM, (1997) Mig and IP-10: CXC chemokines that target lymphocytes. J Leukoc Biol 61: 246-257.
48. Bujak M, Dobaczewski M, Gonzalez-Quesada C, Xia Y, Leucker T, et al. (2009) Induction of the CXC chemokine interferon-gamma-inducible protein 10 regulates the reparative response following myocardial infarction. Circ Res 105: 973-983.
49. Appay V, Rowland-Jones SL, (2001) RANTES: a versatile and controversial chemokine. Trends Immunol 22: 83-87.
50. Baggiolini M, Dewald B, Moser B, (1994) Interleukin-8 and related chemotactic cytokines-CXC and CC chemokines. Adv Immunol 55: 97-179.
51. Machado FS, Martins GA, Aliberti JC, Mestriner FL, Cunha FQ, et al. (2000) Trypanosoma cruzi-infected cardiomyocytes produce chemokines and cytokines that trigger potent nitric oxide-dependent trypanocidal activity. Circulation 102: 3003-3008.
52. Marino AP, da Silva A, dos Santos P, Pinto LM, Gazzinelli RT, et al. (2004) Regulated on activation, normal T cell expressed and secreted (RANTES) antagonist (Met-RANTES) controls the early phase of Trypanosoma cruzi-elicited myocarditis. Circulation 110: 1443-1449.
53. Guedes PM, Veloso VM, Talvani A, Diniz LF, Caldas IS, et al. (2010) Increased type 1 chemokine expression in experimental Chagas disease correlates with cardiac pathology in beagle dogs. Vet Immunol Immunopathol 138: 106-113.
54. Soares MB, de Lima RS, Rocha LL, Vasconcelos JF, Rogatto SR, et al. (2010) Gene expression changes associated with myocarditis and fibrosis in hearts of mice with chronic chagasic cardiomyopathy. J Infect Dis 202: 416-426.
55. Manque PA, Probst CM, Pereira MC, Rampazzo RC, Ozaki LS, et al. (2011) Trypanosoma cruzi infection induces a global host cell response in cardiomyocytes. Infect Immun 79: 1855-1862.
56. Gong JH, Nicholls EF, Elliott MR, Brown KL, Hokamp K, et al. (2012) G-protein-coupled receptor independent, immunomodulatory properties of chemokine CXCL9. Cell Immunol 261: 105-113.
57. Ramasawmy R, Cunha-Neto E, Fae KC, Martello FG, Muller NG, et al. (2006) The monocyte chemoattractant protein-1 gene polymorphism is associated with cardiomyopathy in human chagas disease. Clin Infect Dis 43: 305-311.
58. Florez O, Martin J, Gonzalez CI, (2012) Genetic variants in the chemokines and chemokine receptors in Chagas disease. Hum Immunol.
59. Bilate AM, Cunha-Neto E, (2008) Chagas disease cardiomyopathy: current concepts of an old disease. Rev Inst Med Trop Sao Paulo 50: 67-74.
60. Drigo SA, Cunha-Neto E, Ianni B, Cardoso MR, Braga PE, et al. (2006) TNF gene polymorphisms are associated with reduced survival in severe Chagas' disease cardiomyopathy patients. Microbes Infect 8: 598-603.
61. Lee HH, Farber JM, (1996) Localization of the gene for the human MIG cytokine on chromosome 4q21 adjacent to INP10 reveals a chemokine "mini-cluster". Cytogenet Cell Genet 74: 255-258.
62. McDermott DH, Zimmerman PA, Guignard F, Kleeberger CA, Leitman SF, et al. (1998) CCR5 promoter polymorphism and HIV-1 disease progression. Multicenter AIDS Cohort Study (MACS). Lancet 352: 866-870.
63. Lacher M, Kappler R, Berkholz S, Baurecht H, von Schweinitz D, et al. (2007) Association of a CXCL9 polymorphism with pediatric Crohn's disease. Biochem Biophys Res Commun 363: 701-707.
64. Deng G, Zhou G, Zhang R, Zhai Y, Zhao W, et al. (2008) Regulatory polymorphisms in the promoter of CXCL10 gene and disease progression in male hepatitis B virus carriers. Gastroenterology 134: 716-726.
65. Klich I, Fendler W, Wyka K, Mlynarski W, (2011) Effect of the IP10 (CXCL10) and HLA genotype on the risk of type 1 diabetes in children. Pediatr Endocrinol Diabetes Metab 17: 10-13.
66. Erdel M, Theurl M, Meyer M, Duba HC, Utermann G, et al. (2001) High-resolution mapping of the human 4q21 and the mouse 5E3 SCYB chemokine cluster by fiber-fluorescence in situ hybridization. Immunogenetics 53: 611-615.
67. Troia-Cancio P, Asmuth DM, (2011) Lessons from maraviroc clinical trials. Expert Rev Anti Infect Ther 9: 649-651.
68. Hart AL, Ng SC, Mann E, Al-Hassi HO, Bernardo D, et al. (2010) Homing of immune cells: role in homeostasis and intestinal inflammation. Inflamm Bowel Dis 16: 1969-1977.
69. Kakuta Y, Okumi M, Miyagawa S, Tsutahara K, Abe T, et al. (2012) Blocking of CCR5 and CXCR3 suppresses the infiltration of macrophages in acute renal allograft rejection. Transplantation 93: 24-31.