Trypanosoma cruzi entrance through systemic or mucosal infection sites differentially modulates regional immune response following acute infection in mice

Frontiers in Immunology

Volumn 4, Issue JUL, 2013, Pages

  De Meis, Juliana ^a   De Albuquerque, Juliana Barreto ^a   Dos Santos, Danielle Silva ^a   Farias de Oliveira, Désio Aurélio ^a   Berbert, Luiz Ricardo ^a   Cotta de Almeida, Vinícius ^a   Savino, Wilson ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE;

APOPTOSIS; CHAGAS DISEASE; DISEASE SEVERITY; HUMAN; IMMUNE RESPONSE; IMMUNITY; INFECTION; LYMPH NODE; MORTALITY; MOUSE; NONHUMAN; PARASITE LOAD; PARASITEMIA; REVIEW; TRYPANOSOMA CRUZI;

EID: 84883892764     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00216     Document Type: Review

References (99)

1. Hotez PJ, Molyneux DH, Stillwaggon E, Bentwich Z, Kumaresan J. Neglected tropical diseases and HIV/AIDS. Lancet (2006) 368:1865-6. doi:10.1016/S0140-6736(06)69765-1
2. Savino W, Villa-Verde DM, Mendes-Da-Cruz DA, Silva-Monteiro E, Perez AR, Aoki Mdel P, et al. Cytokines and cell adhesion receptors in the regulation of immunity to Trypanosoma cruzi. Cytokine Growth Factor Rev (2007) 18:107-24. doi:10.1016/j.cytogfr.2007.01.010
3. Dorn P, Buekens P, Hanford E. Whac-a-mole: future trends in Chagas transmission and the importance of a global perspective on disease control. Future Microbiol (2007) 2:365-7. doi:10.2217/17460913.2.4.365
4. Tarleton RL, Reithinger R, Urbina JA, Kitron U, Gurtler RE. The challenges of Chagas disease - grim outlook or glimmer of hope. PLoS Med (2007) 4:e332. doi:10.1371/journal.pmed.0040332
5. Sanchez LV, Ramirez JD. Congenital and oral transmission of American trypanosomiasis: an overview of physiopathogenic aspects. Parasitology (2012) 140:147-59. doi:10.1017/S0031182012001394
6. Bisio M, Seidenstein ME, Burgos JM, Ballering G, Risso M, Pontoriero R, et al. Urbanization of congenital transmission of Trypanosoma cruzi: prospective polymerase chain reaction study in pregnancy. Trans R Soc Trop Med Hyg (2011) 105:543-9. doi:10.1016/j.trstmh.2011.07.003
7. Barbosa-Ferreira JM, Guerra JA, Santana Filho FS, Magalhaes BM, Coelho LI, Barbosa MG. Cardiac involvement in Acute Chagas disease cases in the Amazon region. Arq Bras Cardiol (2010) 94:147-9. doi:10.1590/S0066-782X2010000600023
8. Pinto AY, Harada GS, Valente V, Abud JE, Gomes F, Souza GC, et al. Cardiac attacks in patients with acute Chagas disease in a family micro-outbreak, in Abaetetuba, Brazilian Amazon. Rev Soc Bras Med Trop (2001) 34:413-9.
9. Vinas Albajar P, Laredo SV, Terrazas MB, Coura JR. Dilated cardiomyopathy in patients with chronic Chagasic infection: report of two fatal autochthonous cases from Rio Negro, State of Amazonas, Brazil. Rev Soc Bras Med Trop (2003) 36:401-7.
10. Ianni BM, Mady C. The sugarcane juice was delicious, but. Arq Bras Cardiol (2005) 85:379-81.
11. Moreira OC, Ramirez JD, Velazquez E, Melo MF, Lima-Ferreira C, Guhl F, et al. Towards the establishment of a consensus real-time qPCR to monitor Trypanosoma cruzi parasitemia in patients with chronic Chagas disease cardiomyopathy: a substudy from the BENEFIT trial. Acta Trop (2013) 125:23-31. doi:10.1016/j.actatropica.2012.08.020
12. Jones EM, Colley DG, Tostes S, Lopes ER, Vnencak-Jones CL, McCurley TL. Amplification of a Trypanosoma cruzi DNA sequence from inflammatory lesions in human Chagasic cardiomyopathy. Am J Trop Med Hyg (1993) 48:348-57.
13. Brandariz S, Schijman A, Vigliano C, Arteman P, Viotti R, Beldjord C, et al. Detection of parasite DNA in Chagas' heart disease. Lancet (1995) 346:1370-1. doi:10.1016/S0140-6736(95)92388-8
14. Vago AR, Macedo AM, Adad SJ, Reis DD, Correa-Oliveira R. PCR detection of Trypanosoma cruzi DNA in oesophageal tissues of patients with chronic digestive Chagas' disease. Lancet (1996) 348:891-2. doi:10.1016/S0140-6736(05)64761-7
15. Vago AR, Macedo AM, Oliveira RP, Andrade LO, Chiari E, Galvao LM, et al. Kinetoplast DNA signatures of Trypanosoma cruzi strains obtained directly from infected tissues. Am J Pathol (1996) 149:2153-9.
16. Lane JE, Olivares-Villagomez D, Vnencak-Jones CL, McCurley TL, Carter CE. Detection of Trypanosoma cruzi with the polymerase chain reaction and in situ hybridization in infected murine cardiac tissue. Am J Trop Med Hyg (1997) 56:588-95.
17. Olivares-Villagomez D, McCurley TL, Vnencak-Jones CL, Correa-Oliveira R, Colley DG, Carter CE. Polymerase chain reaction amplification of three different Trypanosoma cruzi DNA sequences from human Chagasic cardiac tissue. Am J Trop Med Hyg (1998) 59:563-70.
18. Zhang L, Tarleton RL. Parasite persistence correlates with disease severity and localization in chronic Chagas' disease. J Infect Dis (1999) 180:480-6. doi:10.1086/314889
19. Mortara RA, Da Silva S, Patricio FR, Higuchi ML, Lopes ER, Gabbai AA, et al. Imaging Trypanosoma cruzi within tissues from Chagasic patients using confocal microscopy with monoclonal antibodies. Parasitol Res (1999) 85:800-8. doi:10.1007/s004360050636
20. Combs TP, Nagajyothi F, Mukherjee S, De Almeida CJ, Jelicks LA, Schubert W, et al. The adipocyte as an important target cell for Trypanosoma cruzi infection. J Biol Chem (2005) 280:24085-94. doi:10.1074/jbc. M412802200
21. Ferreira AV, Segatto M, Menezes Z, Macedo AM, Gelape C, De Oliveira Andrade L, et al. Evidence for Trypanosoma cruzi in adipose tissue in human chronic Chagas disease. Microbes Infect (2011) 13:1002-5. doi:10.1016/j.micinf.2011.06.002
22. Sartori AM, Ibrahim KY, Nunes Westphalen EV, Braz LM, Oliveira OC Jr, Gakiya E, et al. Manifestations of Chagas disease (American trypanosomiasis) in patients with HIV/AIDS. Ann Trop Med Parasitol (2007) 101:31-50. doi:10.1179/136485907X154629
23. Fiorelli AI, Santos RH, Oliveira JL Jr, Lourenco-Filho DD, Dias RR, Oliveira AS, et al. Heart transplantation in 107 cases of Chagas' disease. Transplant Proc (2011) 43:220-4. doi:10.1016/j.transproceed.2010.12.046
24. Ben Younes-ChennoufiA, Hontebeyrie-Joskowicz M, Tricottet V, Eisen H, Reynes M, Said G. Persistence of Trypanosoma cruzi antigens in the inflammatory lesions of chronically infected mice. Trans R Soc Trop Med Hyg (1988) 82:77-83. doi:10.1016/0035-9203(88)90269-6
25. Higuchi M, Brito T, Reis M, Barbosa A, Bellotti G, Pereira-Barreto A, et al. Correlation between Trypanosoma cruzi parasitism and myocardial inflammatory infiltrate in human chronic Chagasic myocarditis: light microscopy and immunohistochemical findings. Cardiovasc Pathol (1993) 2:101-6. doi:10.1016/1054-8807(93)90021-S
26. Bellotti G, Bocchi EA, De Moraes AV, Higuchi ML, Barbero-Marcial M, Sosa E, et al. In vivo detection of Trypanosoma cruzi antigens in hearts of patients with chronic Chagas' heart disease. Am Heart J (1996) 131:301-7. doi:10.1016/S0002-8703(96)90358-0
27. Reis MM, Higuchi Mde L, Benvenuti LA, Aiello VD, Gutierrez PS, Bellotti G, et al. 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) 83:165-72. doi:10.1006/clin.1997.4335
28. Tarleton RL, Zhang L, Downs MO. "Autoimmune rejection" of neonatal heart transplants in experimental Chagas disease is a parasite-specific response to infected host tissue. Proc Natl Acad Sci U S A (1997) 94:3932-7. doi:10.1073/pnas.94.8.3932
29. Marsden PD. Trypanosoma cruzi infections in CFI mice. II. Infections induced by different routes. Ann Trop Med Parasitol (1967) 61:62-7.
30. Camandaroba EL, Pinheiro Lima CM, Andrade SG. Oral transmission of Chagas disease: importance of Trypanosoma cruzi biodeme in the intragastric experimental infection. Rev Inst Med Trop Sao Paulo (2002) 44:97-103. doi:10.1590/S0036-46652002000200008
31. Caradonna K, Pereiraperrin M. Preferential brain homing following intranasal administration of Trypanosoma cruzi. Infect Immun (2009) 77:1349-56. doi:10.1128/IAI.01434-08
32. Minoprio PM, Coutinho A, Joskowicz M, D'Imperio Lima MR, Eisen H. Polyclonal lymphocyte responses to murine Trypanosoma cruzi infection. II. Cytotoxic T lymphocytes. Scand J Immunol (1986) 24:669-79. doi:10.1111/j.1365-3083.1986.tb02186.x
33. de Meis J, Mendes-Da-Cruz DA, Farias-De-Oliveira DA, Correa-De-Santana E, Pinto-Mariz F, Cotta-De-Almeida V, et al. Atrophy of mesenteric lymph nodes in experimental Chagas' disease: differential role of Fas/Fas-L and TNFRI/TNF pathways. Microbes Infect (2006) 8:221-31. doi:10.1016/j.micinf.2005.06.027
34. Bryan MA, Norris KA. Genetic immunization converts the Trypanosoma cruzi B-Cell mitogen proline racemase to an effective immunogen. Infect Immun (2010) 78:810-22. doi:10.1128/IAI.00926-09
35. Reina-San-Martin B, Degrave W, Rougeot C, Cosson A, Chamond N, Cordeiro-Da-Silva A, et al. A B-cell mitogen from a pathogenic trypanosome is a eukaryotic proline racemase. Nat Med (2000) 6:890-7. doi:10.1038/78651
36. Buschiazzo A, Goytia M, Schaeffer F, Degrave W, Shepard W, Gregoire C, et al. Crystal structure, catalytic mechanism, and mitogenic properties of Trypanosoma cruzi proline racemase. Proc Natl Acad Sci U S A (2006) 103:1705-10. doi:10.1073/pnas.0509010103
37. Rodriguez AM, Santoro F, Afchain D, Bazin H, Capron A. Trypanosoma cruzi infection in B-cell-deficient rats. Infect Immun (1981) 31:524-9.
38. Minoprio P, Burlen O, Pereira P, Guilbert B, Andrade L, Hontebeyrie-Joskowicz M, et al. Most B cells in acute Trypanosoma cruzi infection lack parasite specificity. Scand J Immunol (1988) 28:553-61. doi:10.1111/j.1365-3083.1988.tb01487.x
39. Minoprio P, Coutinho A, Spinella S, Hontebeyrie-Joskowicz M. Xid immunodeficiency imparts increased parasite clearance and resistance to pathology in experimental Chagas' disease. Int Immunol (1991) 3:427-33. doi:10.1093/intimm/3.5.427
40. Yoshida N, Araya JE, Da Silveira JF, Giorgio S. Trypanosoma cruzi: antibody production and T cell response induced by stage-specific surface glycoproteins purified from metacyclic trypomastigotes. Exp Parasitol (1993) 77:405-13. doi:10.1006/expr.1993.1100
41. Freire-de-Lima C, Pecanha LM, Dos Reis GA. Chronic experimental Chagas' disease: functional syngeneic T-B-cell cooperation in vitro in the absence of an exogenous stimulus. Infect Immun (1996) 64:2861-6.
42. De Arruda Hinds LB, Alexandre-Moreira MS, Decote-Ricardo D, Nunes MP, Pecanha LM. Increased immunoglobulin secretion by B lymphocytes from Trypanosoma cruzi infected mice after B lymphocytes-natural killer cell interaction. Parasite Immunol (2001) 23:581-6. doi:10.1046/j.1365-3024.2001.00418.x
43. Girones N, Rodriguez CI, Carrasco-Marin E, Hernaez RF, De Rego JL, Fresno M. Dominant T- and B-cell epitopes in an autoantigen linked to Chagas' disease. J Clin Invest (2001) 107:985-93. doi:10.1172/JCI10734
44. Gao W, Wortis HH, Pereira MA. The Trypanosoma cruzi trans-sialidase is a T cell-independent B cell mitogen and an inducer of non-specific Ig secretion. Int Immunol (2002) 14:299-308. doi:10.1093/intimm/14.3.299
45. Acosta Rodriguez EV, Zuniga EI, Montes CL, Merino MC, Bermejo DA, Amezcua Vesely MC, et al. Trypanosoma cruzi infection beats the B-cell compartment favouring parasite establishment: can we strike first? Scand J Immunol (2007) 66:137-42. doi:10.1111/j.1365-3083.2007.01968.x
46. Tarleton RL, Grusby MJ, Postan M, Glimcher LH. Trypanosoma cruzi infection in MHC-deficient mice: further evidence for the role of both class I- and class II -restricted T cells in immune resistance and disease. Int Immunol. (1996), 8: 13-22, doi:10.1093/intimm/8.1.13.
47. Millar AE, Kahn SJ. The SA85-1.1 protein of the Trypanosoma cruzi trans-sialidase superfamily is a dominant T-cell antigen. Infect Immun (2000) 68:3574-80. doi:10.1128/IAI.68.6.3574-3580.2000
48. Silva EM, Guillermo LV, Ribeiro-Gomes FL, De Meis J, Pereira RM, Wu Z, et al. Caspase-8 activity prevents type 2 cytokine responses and is required for protective T cell-mediated immunity against Trypanosoma cruzi infection. J Immunol (2005) 174:6314-21.
49. de Meis J, Ferreira LM, Guillermo LV, Silva EM, Dosreis GA, Lopes MF. Apoptosis differentially regulates mesenteric and subcutaneous lymph node immune responses to Trypanosoma cruzi. Eur J Immunol (2008) 38:139-46. doi:10.1002/eji.200737582
50. Florez O, Esper J, Higuera S, Barraza MF, Cabrera HB, Mantilla JC, et al. Chagasic megacolon associated with Trypanosoma cruzi I in a Colombian patient. Parasitol Res (2010) 107:439-42. doi:10.1007/s00436-010-1874-2
51. Teixeira AR, Nitz N, Guimaro MC, Gomes C, Santos-Buch CA. Chagas disease. Postgrad Med J (2006) 82:788-98. doi:10.1136/pgmj.2006.047357
52. da Silveira AB, Lemos EM, Adad SJ, Correa-Oliveira R, Furness JB, D'Avila Reis D. Megacolon in Chagas disease: a study of inflammatory cells, enteric nerves, glial cells. Hum Pathol (2007) 38:1256-64. doi:10.1016/j.humpath.2007.01.020
53. Antunez MI, Feinstein RE, Cardoni RL, Gronvik KO. Trypanosoma cruzi: T cell subpopulations in the Peyer's patches of BALB/c infected mice. Exp Parasitol (1997) 87:58-64. doi:10.1006/expr.1997.4171
54. de Meis J, Morrot A, Farias-De-Oliveira DA, Villa-Verde DM, Savino W. Differential regional immune response in Chagas disease. PLoS Negl Trop Dis (2009) 3:e417. doi:10.1371/journal.pntd.0000417
55. Guillermo LV, Silva EM, Ribeiro-Gomes FL, De Meis J, Pereira WF, Yagita H, et al. The Fas death pathway controls coordinated expansions of type 1 CD8 and type 2 CD4 T cells in Trypanosoma cruzi infection. J Leukoc Biol (2007) 81:942-51. doi:10.1189/jlb.1006643
56. Zuniga E, Motran CC, Montes CL, Yagita H, Gruppi A. Trypanosoma cruzi infection selectively renders parasite-specific IgG+ B lymphocytes susceptible to Fas/Fas ligand-mediated fratricide. J Immunol (2002) 168:3965-73.
57. Silva EM, Guillermo LV, Ribeiro-Gomes FL, De Meis J, Nunes MP, Senra JF, et al. Caspase inhibition reduces lymphocyte apoptosis and improves host immune responses to Trypanosoma cruzi infection. Eur J Immunol (2007) 37:738-46. doi:10.1002/eji.200636790
58. Lopes MF, Guillermo LV, Silva EM. Decoding caspase signaling in host immunity to the protozoan Trypanosoma cruzi. Trends Immunol (2007) 28:366-72. doi:10.1016/j.it.2007.06.004
59. Pandiyan P, Zheng L, Lenardo MJ. The molecular mechanisms of regulatory T cell immunosuppression. Front Immunol (2011) 2:60. doi:10.3389/fimmu.2011.00060
60. Lenardo M, Chan KM, Hornung F, McFarland H, Siegel R, Wang J, et al. Mature T lymphocyte apoptosis - immune regulation in a dynamic and unpredictable antigenic environment. Annu Rev Immunol (1999) 17:221-53. doi:10.1146/annurev.immunol.17.1.221
61. Zheng L, Trageser CL, Willerford DM, Lenardo MJ. T cell growth cytokines cause the superinduction of molecules mediating antigen-induced T lymphocyte death. J Immunol (1998) 160:763-9.
62. Green DR, Droin N, Pinkoski M. Activation-induced cell death in T cells. Immunol Rev (2003) 193:70-81. doi:10.1034/j.1600-065X.2003.00051.x
63. Zhang J, Xu X, Liu Y. Activation-induced cell death in T cells and autoimmunity. Cell Mol Immunol (2004) 1:186-92.
64. Ke F, Voss A, Kerr JB, O'Reilly LA, Tai L, Echeverry N, et al. BCL-2 family member BOK is widely expressed but its loss has only minimal impact in mice. Cell Death Differ (2012) 19:915-25. doi:10.1038/cdd.2011.210
65. Mason KD, Lin A, Robb L, Josefsson EC, Henley KJ, Gray DH, et al. Proapoptotic Bak and Bax guard against fatal systemic and organ-specific autoimmune disease. Proc Natl Acad Sci U S A (2013) 110:2599-604. doi:10.1073/pnas.1215097110
66. Willis SN, Fletcher JI, Kaufmann T, Van Delft MF, Chen L, Czabotar PE, et al. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science (2007) 315:856-9. doi:10.1126/science.1133289
67. Chipuk JE, Green DR. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol (2008) 18:157-64. doi:10.1016/j.tcb.2008.01.007
68. Pandiyan P, Zheng L, Ishihara S, Reed J, Lenardo MJ. CD4+CD25+Foxp3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells. Nat Immunol (2007) 8:1353-62.doi:10.1038/ni1536.
69. Hoft DF, Farrar PL, Kratz-Owens K, Shaffer D. Gastric invasion by Trypanosoma cruzi and induction of protective mucosal immune responses. Infect Immun (1996) 64:3800-10.
70. Alberti E, Acosta A, Sarmiento ME, Hidalgo C, Vidal T, Fachado A, et al. Specific cellular and humoral immune response in Balb/c mice immunised with an expression genomic library of Trypanosoma cruzi. Vaccine (1998) 16:608-12. doi:10.1016/S0264-410X(97)00228-4
71. Sullivan NL, EickhoffCS, Zhang X, Giddings OK, Lane TE, Hoft DF. Importance of the CCR5-CCL5 axis for mucosal Trypanosoma cruzi protection and B cell activation. J Immunol (2011) 187(3):1358-68. doi:10.4049/jimmunol.1100033
72. Hoft DF, EickhoffCS. Type 1 immunity provides optimal protection against both mucosal and systemic Trypanosoma cruzi challenges. Infect Immun (2002) 70:6715-25. doi:10.1128/IAI.70.12.6715-6725.2002
73. Hoft DF, EickhoffCS. Type 1 immunity provides both optimal mucosal and systemic protection against a mucosally invasive, intracellular pathogen. Infect Immun (2005) 73:4934-40. doi:10.1128/IAI.73.8.4934-4940.2005
74. Giddings OK, EickhoffCS, Smith TJ, Bryant LA, Hoft DF. Anatomical route of invasion and protective mucosal immunity in Trypanosoma cruzi conjunctival infection. Infect Immun (2006) 74:5549-60. doi:10.1128/IAI.00319-06
75. Shikanai-Yasuda MA, Carvalho NB. Oral transmission of Chagas disease. Clin Infect Dis (2012) 54:845-52. doi:10.1093/cid/cir956
76. Andrade ZA, Silva HR. Parasitism of adipocytes by Trypanosoma cruzi. Mem Inst Oswaldo Cruz (1995) 90:521-2. doi:10.1590/S0074-02761995000400018
77. Buckner FS, Wilson AJ, Van Voorhis WC. Detection of live Trypanosoma cruzi in tissues of infected mice by using histochemical stain for beta-galactosidase. Infect Immun (1999) 67:403-9.
78. Guarner J, Bartlett J, Zaki SR, Colley DG, Grijalva MJ, Powell MR. Mouse model for Chagas disease: immunohistochemical distribution of different stages of Trypanosoma cruzi in tissues throughout infection. Am J Trop Med Hyg (2001) 65:152-8.
79. Correa-de-Santana E, Paez-Pereda M, Theodoropoulou M, Kenji Nihei O, Gruebler Y, Bozza M, et al. Hypothalamus-pituitary-adrenal axis during Trypanosoma cruzi acute infection in mice. J Neuroimmunol (2006) 173:12-22. doi:10.1016/j.jneuroim.2005.08.015
80. Qvarnstrom Y, Schijman AG, Veron V, Aznar C, Steurer F, Da Silva AJ. Sensitive and specific detection of Trypanosoma cruzi DNA in clinical specimens using a multi-target real-time PCR approach. PLoS Negl Trop Dis (2012) 6:e1689. doi:10.1371/journal.pntd.0001689
81. Cortez M, Silva MR, Neira I, Ferreira D, Sasso GR, Luquetti AO, et al. (2006). Trypanosoma cruzi surface molecule gp90 downregulates invasion of gastric mucosal epithelium in orally infected mice. Microbes Infect 8:36-44. doi:10.1016/j.micinf.2005.05.016
82. Veloso VM, Guedes PM, Andrade IM, Caldas IS, Martins HR, Carneiro CM, et al. Trypanosoma cruzi: blood parasitism kinetics and their correlation with heart parasitism intensity during long-term infection of Beagle dogs. Mem Inst Oswaldo Cruz (2008)103:528-34. doi:10.1590/S0074-02762008000600003
83. Castro-Sesquen YE, Gilman RH, Yauri V, Cok J, Angulo N, Escalante H, et al. Detection of soluble antigen and DNA of Trypanosoma cruzi in urine is independent of renal injury in the guinea pig model. PLoS ONE (2013) 8:e58480. doi:10.1371/journal.pone.0058480
84. Morocoima A, Rodriguez M, Herrera L, Urdaneta-Morales S. Trypanosoma cruzi: experimental parasitism of bone and cartilage. Parasitol Res (2006) 99:663-8. doi:10.1007/s000436-006-0211-2
85. Baena Teran R, Arancibia A, Basquiera AL, De La Fuente JL, Ricchi B, De Diller AB. Trypanosoma cruzi in the bone marrow. Br J Haematol (2012) 157:1. doi:10.1111/j.1365-2141.2012.09049.x
86. Da Costa SC, Calabrese KS, Bauer PG, Savino W, Lagrange PH. Studies of the thymus in Chagas' disease: III. Colonization of the thymus and other lymphoid organs of adult and newborn mice by Trypanosoma cruzi. Pathol Biol (Paris) (1991) 39:91-7.
87. Andrade LO, Machado CR, Chiari E, Pena SD, Macedo AM. Differential tissue distribution of diverse clones of Trypanosoma cruzi in infected mice. Mol Biochem Parasitol (1999) 100:163-72. doi:10.1016/S0166-6851(99)90035-X
88. Rachid MA, Teixeira AL, Barcelos LS, Machado CR, Chiari E, Tanowitz HB, et al. Role of endothelin receptors in the control of central nervous system parasitism in Trypanosoma cruzi infection in rats. J Neuroimmunol (2010) 220
89. Vago AR, Andrade LO, Leite AA, D'avila Reis D, Macedo AM, Adad SJ, et al. Genetic characterization of Trypanosoma cruzi directly from tissues of patients with chronic Chagas disease: differential distribution of genetic types into diverse organs. Am J Pathol (2000) 156:1805-9.
90. Schijman AG, Vigliano CA, Viotti RJ, Burgos JM, Brandariz S, Lococo BE, et al. Trypanosoma cruzi DNA in cardiac lesions of Argentinean patients with endstage chronic chagas heart disease. Am J Trop Med Hyg (2004) 70:210-20.
91. Vago AR, Silva DM, Adad SJ, Correa-Oliveira R, D'avila Reis D. Chronic Chagas disease: presence of parasite DNA in the oesophagus of patients without megaoesophagus. Trans R Soc Trop Med Hyg (2003) 97:308-9.doi:10.1016/S0035-9203(03)90155-6.
92. Staquicini DI, Martins RM, Macedo S, Sasso GR, Atayde VD, Juliano MA, et al. Role of GP82 in the selective binding to gastric mucin during oral infection with Trypanosoma cruzi. PLoS Negl Trop Dis (2006) 4:e613. doi:10.1371/journal.pntd.0000613
93. Kuhn RE, Vaughn RT, Iannuzzi NP. The in vivo distribution of 51Cr-labeled Trypanosoma cruzi in mice. Int J Parasitol (1974).4:585-8.doi:10.1016/0020-7519(74)90022-8
94. Nogueira N, Gordon S, Cohn Z. Trypanosoma cruzi: modification of macrophage function during infection. J Exp Med (1977) 146:157-71. doi:10.1084/jem.146.1.157
95. Yoshida N. Trypanosoma cruzi infection by oral route: how the interplay between parasite and host components modulates infectivity. Parasitol Int (2008) 57:105-9. doi:10.1016/j.parint.2007.12.008
96. DePaolo RW, Kamdar K, Khakpour S, Sugiura Y, Wang W, Jabri B. A specific role for TLR1 in protective T(H)17 immunity during mucosal infection. J Exp Med (2012) 209:1437-44. doi:10.1084/jem.20112339
97. Pepper M, Linehan JL, Pagan AJ, Zell T, Dileepan T, Cleary PP, et al. Different routes of bacterial infection induce long-lived TH1 memory cells and short-lived TH17 cells. Nat Immunol (2010) 11:83-9. doi:10.1038/ni.1826
98. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature (1999) 401:708-12. doi:10.1038/44385
99. Barbosa-Ferreira JM, Nobre AF, Maldonado JG, Borges-Pereira J, Zauza PL, Coura JR. Stroke in a chronic autochthonous Chagasic patient from the Brazilian Amazon. Rev Soc Bras Med Trop (2010) 43:751-3. doi:10.1590/S0037-86822010000600034