Inhibitory receptors are expressed by Trypanosoma cruzi-specific effector T cells and in hearts of subjects with chronic chagas disease

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Argüello, Rafael J ^a   Albareda, María C ^a   Alvarez, María G ^b   Bertocchi, Graciela ^b   Armenti, Alejandro H ^b   Vigliano, Carlos ^c   Meckert, Patricia C ^c   Tarleton, Rick L ^d   Laucella, Susana A ^a,b  

^a Instituto Nacional de Diagnostico e Investigacion de la Enfermedad de Chagas Dr Mario Fatala Chaben   (Argentina)

^b Hospital Interzonal General de Agudos Eva Peronquot   (Argentina)

^c HOSPITAL UNIVERSITARIO FUNDACIÓN FAVALORO   (Argentina)

^d UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZNIDAZOLE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; LEUKOCYTE IMMUNOGLOBULIN LIKE RECEPTOR 1; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CD4+ T LYMPHOCYTE; CHAGAS DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; EFFECTOR CELL; ELECTROCARDIOGRAPHY; FLOW CYTOMETRY; HUMAN; HUMAN TISSUE; LYMPHOCYTIC INFILTRATION; MAJOR CLINICAL STUDY; MYOCARDITIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; TRYPANOSOMA CRUZI; UPREGULATION;

TRYPANOSOMA CRUZI;

EID: 84871349098     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035966     Document Type: Article

References (70)

1. World Health Organization (2002) Control of Chagas disease. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser 905: 1-109.
2. Higuchi MD, Ries MM, Aiello VD, Benvenuti LA, Gutierrez PS, et al. (1997) Association of an increase in CD8+ T cells with the presence of Trypanosoma cruzi antigens in chronic, human, chagasic myocarditis. Am J Trop Med Hyg 56: 485-489.
3. Laguens RP, Cabeza Meckert PM, Vigliano CA, (1999) [Pathogenesis of human chronic chagasic myocarditis]. Medicina (B Aires) 59 (Suppl 2): 63-68.
4. Kaech SM, Wherry EJ, Ahmed R, (2002) Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol 2: 251-262.
5. Wherry EJ, Barber DL, Kaech SM, Blattman JN, Ahmed R, (2004) Antigen-independent memory CD8 T cells do not develop during chronic viral infection. Proc Natl Acad Sci U S A 101: 16004-16009.
6. Blackburn SD, Wherry EJ, (2007) IL-10, T cell exhaustion and viral persistence. Trends Microbiol 15: 143-146.
7. Shin H, Wherry EJ, (2007) CD8 T cell dysfunction during chronic viral infection. Curr Opin Immunol 19: 408-415.
8. Zammit DJ, Lefrancois L, (2006) Dendritic cell-T cell interactions in the generation and maintenance of CD8 T cell memory. Microbes Infect 8: 1108-1115.
9. Vezys V, Masopust D, Kemball CC, Barber DL, O'Mara LA, et al. (2006) Continuous recruitment of naive T cells contributes to heterogeneity of antiviral CD8 T cells during persistent infection. J Exp Med 203: 2263-2269.
10. Akbar AN, Henson SM, (2011) Are senescence and exhaustion intertwined or unrelated processes that compromise immunity? Nat Rev Immunol 11: 289-295.
11. Harari A, Dutoit V, Cellerai C, Bart PA, Du Pasquier RA, et al. (2006) Functional signatures of protective antiviral T-cell immunity in human virus infections. Immunol Rev 211: 236-254.
12. Appay V, van Lier RA, Sallusto F, Roederer M, (2008) Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 73: 975-983.
13. Wherry EJ, Blattman JN, Murali-Krishna K, van der Most R, Ahmed R, (2003) Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol 77: 4911-4927.
14. Ince MN, Harnisch B, Xu Z, Lee SK, Lange C, et al. (2004) Increased expression of the natural killer cell inhibitory receptor CD85j/ILT2 on antigen-specific effector CD8 T cells and its impact on CD8 T-cell function. Immunology 112: 531-542.
15. Antrobus RD, Khan N, Hislop AD, Montamat-Sicotte D, Garner LI, et al. (2005) Virus-specific cytotoxic T lymphocytes differentially express cell-surface leukocyte immunoglobulin-like receptor-1, an inhibitory receptor for class I major histocompatibility complex molecules. J Infect Dis 191: 1842-1853.
16. Zaunders JJ, Ip S, Munier ML, Kaufmann DE, Suzuki K, et al. (2006) Infection of CD127+ (interleukin-7 receptor+) CD4+ cells and overexpression of CTLA-4 are linked to loss of antigen-specific CD4 T cells during primary human immunodeficiency virus type 1 infection. J Virol 80: 10162-10172.
17. Kaufmann DE, Kavanagh DG, Pereyra F, Zaunders JJ, Mackey EW, et al. (2007) Upregulation of CTLA-4 by HIV-specific CD4+ T cells correlates with disease progression and defines a reversible immune dysfunction. Nat Immunol 8: 1246-1254.
18. Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, et al. (2006) Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439: 682-687.
19. Read S, Greenwald R, Izcue A, Robinson N, Mandelbrot D, et al. (2006) Blockade of CTLA-4 on CD4+CD25+ regulatory T cells abrogates their function in vivo. J Immunol 177: 4376-4383.
20. Ise W, Kohyama M, Nutsch KM, Lee HM, Suri A, et al. (2010) CTLA-4 suppresses the pathogenicity of self antigen-specific T cells by cell-intrinsic and cell-extrinsic mechanisms. Nat Immunol 11: 129-135.
21. Chen YQ, Shi HZ, (2006) CD28/CTLA-4-CD80/CD86 and ICOS-B7RP-1 costimulatory pathway in bronchial asthma. Allergy 61: 15-26.
22. Greenwald RJ, Oosterwegel MA, van der Woude D, Kubal A, Mandelbrot DA, et al. (2002) CTLA-4 regulates cell cycle progression during a primary immune response. Eur J Immunol 32: 366-373.
23. Walker LSK, Sansom DM, (2011) The emerging role of CTLA4 as a cellextrinsic regulator of T cell responses. Nat Rev Immunol 11: 854-863.
24. Borges L, Cosman D, (2000) LIRs/ILTs/MIRs, inhibitory and stimulatory Ig-superfamily receptors expressed in myeloid and lymphoid cells. Cytokine Growth Factor Rev 11: 209-217.
25. Cella M, Nakajima H, Facchetti F, Hoffmann T, Colonna M, (2000) ILT receptors at the interface between lymphoid and myeloid cells. Curr Top Microbiol Immunol 251: 161-166.
26. Cosman D, Fanger N, Borges L, Kubin M, Chin W, et al. (1997) A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7: 273-282.
27. Chapman TL, Heikeman AP, Bjorkman PJ, (1999) The inhibitory receptor LIR-1 uses a common binding interaction to recognize class I MHC molecules and the viral homolog UL18. Immunity 11: 603-613.
28. Laucella SA, Postan M, Martin D, Hubby Fralish B, Albareda MC, et al. (2004) Frequency of interferon- gamma-producing T cells specific for Trypanosoma cruzi inversely correlates with disease severity in chronic human Chagas disease. J Infect Dis 189: 909-918.
29. Albareda MC, Olivera GC, Laucella SA, Alvarez MG, Fernandez ER, et al. (2009) Chronic human infection with Trypanosoma cruzi drives CD4+ T cells to immune senescence. J Immunol 183: 4103-4108.
30. Albareda MC, Laucella SA, Alvarez MG, Armenti AH, Bertochi G, et al. (2006) Trypanosoma cruzi modulates the profile of memory CD8+ T cells in chronic Chagas' disease patients. Int Immunol 18: 465-471.
31. Alvarez MG, Postan M, Weatherly DB, Albareda MC, Sidney J, et al. (2008) HLA Class I-T Cell Epitopes from trans-Sialidase Proteins Reveal Functionally Distinct Subsets of CD8 T Cells in Chronic Chagas Disease. PLoS Negl Trop Dis 2: e288.
32. Bank/WHO, UW, UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases (1995) Twelfth Programme Report of the UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases (TDR). World Health Organization Geneva pp. 125-134.
33. Kuschnir E, Sgammini H, Castro R, Evequoz C, Ledesma R, et al. (1985) Evaluation of cardiac function by radioisotopic angiography, in patients with chronic Chagas cardiopathy. Arq Bras Cardiol 45: 249-256.
34. Viotti R, Vigliano C, Lococo B, Bertocchi G, Petti M, et al. (2006) Long-term cardiac outcomes of treating chronic Chagas disease with benznidazole versus no treatment: a nonrandomized trial. Ann Intern Med 144: 724-734.
35. Vandenborre K, Delabie J, Boogaerts MA, De Vos R, Lorre K, et al. (1998) Human CTLA-4 is expressed in situ on T lymphocytes in germinal centers, in cutaneous graft-versus-host disease, and in Hodgkin's disease. Am J Pathol 152: 963-973.
36. Marinova E, Han S, Zheng B, (2007) Germinal center helper T cells are dual functional regulatory cells with suppressive activity to conventional CD4+ T cells. J Immunol 178: 5010-5017.
37. Edwards WD, Tajik AJ, Seward JB, (1981) Standardized nomenclature and anatomic basis for regional tomographic analysis of the heart. Mayo Clin Proc 56: 479-497.
38. Aretz HT, Billingham ME, Edwards WD, Factor SM, Fallon JT, et al. (1987) Myocarditis. A histopathologic definition and classification. Am J Cardiovasc Pathol 1: 3-14.
39. Teft WA, Kirchhof MG, Madrenas J, (2006) A molecular perspective of CTLA-4 function. Annu Rev Immunol 24: 65-97.
40. Olivera GC, Albareda MC, Alvarez MG, De Rissio AM, Fichera LE, et al. (2010) Trypanosoma cruzi-specific immune responses in subjects from endemic areas of Chagas disease of Argentina. Microbes Infect 12: 359-363.
41. Laucella SA, Mazliah DP, Bertocchi G, Alvarez MG, Cooley G, et al. (2009) Changes in Trypanosoma cruzi-specific immune responses after treatment: surrogate markers of treatment efficacy. Clin Infect Dis 49: 1675-1684.
42. Merlo A, Saverino D, Tenca C, Grossi CE, Bruno S, et al. (2001) CD85/LIR-1/ILT2 and CD152 (cytotoxic T lymphocyte antigen 4) inhibitory molecules down-regulate the cytolytic activity of human CD4+ T-cell clones specific for Mycobacterium tuberculosis. Infect Immun 69: 6022-6029.
43. Northfield J, Lucas M, Jones H, Young NT, Klenerman P, (2005) Does memory improve with age? CD85j (ILT-2/LIR-1) expression on CD8 T cells correlates with 'memory inflation' in human cytomegalovirus infection. Immunol Cell Biol 83: 182-188.
44. Ibegbu CC, Xu YX, Harris W, Maggio D, Miller JD, et al. (2005) Expression of killer cell lectin-like receptor G1 on antigen-specific human CD8+ T lymphocytes during active, latent, and resolved infection and its relation with CD57. J Immunol 174: 6088-6094.
45. Blackburn SD, Crawford A, Shin H, Polley A, Freeman GJ, et al. (2010) Tissue-specific differences in PD-1 and PD-L1 expression during chronic viral infection: implications for CD8 T-cell exhaustion. J Virol 84: 2078-2089.
46. Nakamoto N, Cho H, Shaked A, Olthoff K, Valiga ME, et al. (2009) Synergistic reversal of intrahepatic HCV-specific CD8 T cell exhaustion by combined PD-1/CTLA-4 blockade. PLoS Pathog 5: e1000313.
47. Schlotmann T, Waase I, Julch C, Klauenberg U, Muller-Myhsok B, et al. (2000) CD4 alphabeta T lymphocytes express high levels of the T lymphocyte antigen CTLA-4 (CD152) in acute malaria. J Infect Dis 182: 367-370.
48. Souza PE, Rocha MO, Menezes CA, Coelho JS, Chaves AC, et al. (2007) Trypanosoma cruzi infection induces differential modulation of costimulatory molecules and cytokines by monocytes and T cells from patients with indeterminate and cardiac Chagas' disease. Infect Immun 75: 1886-1894.
49. de Araújo FF, Vitelli-Avelar DM, Teixeira-Carvalho A, Antas PR, Assis Silva Gomes J, et al. (2011) Regulatory T cells phenotype in different clinical forms of Chagas' disease. PLoS Negl Trop Dis 5: e992.
50. Hermann E, Berthe A, Truyens C, Alonso-Vega C, Parrado R, et al. (2010) Killer cell immunoglobulin-like receptor expression induction on neonatal CD8+ T cells in vitro and following congenital infection with Trypanosoma cruzi. Immunology 129: 418-426.
51. Martins GA, Tadokoro CE, Silva RB, Silva JS, Rizzo LV, (2004) CTLA-4 blockage increases resistance to infection with the intracellular protozoan Trypanosoma cruzi. J Immunol 172: 4893-4901.
52. Graefe SE, Jacobs T, Wachter U, Broker BM, Fleischer B, (2004) CTLA-4 regulates the murine immune response to Trypanosoma cruzi infection. Parasite Immunol 26: 19-28.
53. Gutierrez FR, Mariano FS, Oliveira CJ, Pavanelli WR, Guedes PM, et al. (2011) Regulation of Trypanosoma cruzi-induced myocarditis by programmed death cell receptor 1. Infect Immun 79: 1873-1881.
54. Raziorrouh B, Ulsenheimer A, Schraut W, Heeg M, Kurktschiev P, et al. (2011) Inhibitory molecules that regulate expansion and restoration of HCV-specific CD4+ T cells in patients with chronic infection. Gastroenterology 141: 1422-1431, 1431 e1421-1426.
55. Sauce D, Almeida JR, Larsen M, Haro L, Autran B, et al. (2007) PD-1 expression on human CD8 T cells depends on both state of differentiation and activation status. AIDS 21: 2005-2013.
56. Alegre ML, Frauwirth KA, Thompson CB, (2001) T-cell regulation by CD28 and CTLA-4. Nat Rev Immunol 1: 220-228.
57. Tarleton RL, Koller BH, Latour A, Postan M, (1992) Susceptibility of beta 2-microglobulin deficient mice to Trypanosoma cruzi infection. Nature 356: 338-340.
58. Tarleton RL, Sun J, Zhang L, Postan M, (1994) Depletion of T-cell subpopulations results in exacerbation of myocarditis and parasitism in experimentalChagas' disease. Infect Immun 62: 1820-1829.
59. Wizel B, Palmieri M, Mendoza C, Arana B, Sidney J, et al. (1998) Human infection with Try panosoma cruzi induces antigen-specific cytotoxic T lymphocyte responses. J Clin Invest 102: 1062-1071.
60. Wagner CS, Riise GC, Bergström T, Kärre K, Carbone E, et al. (2007) Increased expression of leukocyte Ig-like receptor-1 and activating role of UL18 in the response to cytomegalovirus infection. J Immunol 178: 3536-3543.
61. Saverino D, Ghiotto F, Merlo A, Bruno S, Battini L, et al. (2004) Specific recognition of the viral protein UL18 by CD85j/LIR-1/ILT2 on CD8+ T cells mediates the non-MHC-restricted lysis of human cytomegalovirus-infected cells. J Immunol 172: 5629-5637.
62. Kumar S, Tarleton RL, (2001) Antigen-specific Th1 but not Th2 cells provide protection from lethal Trypanosoma cruzi infection in mice. J Immunol 166: 4596-4603.
63. Schijman AG, Vigliano CA, Viotti RJ, Burgos JM, Brandariz S, et al. (2004) Trypanosoma cruzi DNA in cardiac lesions of Argentinean patients with end-stage chronic chagas heart disease. Am J Trop Med Hyg 70: 210-220.
64. Jimenez-Martinez MC, Linares M, Baez R, Montano LF, Martinez-Cairo S, et al. (2004) Intracellular expression of interleukin-4 and interferon-gamma by a Mycobacterium tuberculosis antigen-stimulated CD4+ CD57+ T-cell subpopulation with memory phenotype in tuberculosis patients. Immunology 111: 100-106.
65. Bengsch B, Spangenberg HC, Kersting N, Neumann-Haefelin C, Panther E, et al. (2007) Analysis of CD127 and KLRG1 expression on hepatitis C virus-specific CD8+ T cells reveals the existence of different memory T-cell subsets in the peripheral blood and liver. J Virol 81: 945-953.
66. Vezys V, Masopust D, Kemball CC, Barber DL, O'Mara LA, et al. (2006) Continuous recruitment of naive T cells contributes to heterogeneity of antiviral CD8 T cells during persistent infection. J Exp Med 203: 2263-2269.
67. Radziewicz H, Uebelhoer L, Bengsch B, Grakoui A, (2007) Memory CD8+ T cell differentiation in viral infection: a cell for all seasons. World J Gastroenterol 13: 4848-4857.
68. Blackburn SD, Shin H, Haining WN, Zou T, Workman CJ, et al. (2009) Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol 10: 29-37.
69. Kassu A, Marcus RA, D'Souza MB, Kelly-McKnight EA, Golden-Mason L, et al. (2010) Regulation of virus-specific CD4+ T cell function by multiple costimulatory receptors during chronic HIV infection. J Immunol 185: 3007-3018.
70. Yi JS, Cox MA, Zajac AJ, (2010) T-cell exhaustion: characteristics, causes and conversion. Immunology 129: 474-481.