Immunoendocrine dysbalance during uncontrolled T. cruzi infection is associated with the acquisition of a Th-1-like phenotype by Foxp3+ T cells

Brain, Behavior, and Immunity

Volumn 45, Issue , 2015, Pages 219-232

  González, Florencia B ^a   Villar, Silvina R ^a   Fernández Bussy, Rodrigo ^a   Martin, Gaëlle H ^b   Pérol, Louis ^c,d   Manarin, Romina ^a   Spinelli, Silvana V ^a   Pilon, Caroline ^e   Cohen, José Laurent ^b,e,f   Bottasso, Oscar A ^a   Piaggio, Eliane ^c,d,g   Pérez, Ana R ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^b INSERM U955   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d INSTITUT CURIE   (France)

^e UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^f HENRI MONDOR HOSPITAL   (France)

^g INSERM   (France)

Author keywords

Chagas disease; Glucocorticoids; IFN ; IL 2; Regulatory T cells

Indexed keywords

ALDESLEUKIN; CORTICOSTERONE; DEXAMETHASONE; GAMMA INTERFERON; GLUCOCORTICOID; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 23; INTERLEUKIN 27; INTERLEUKIN 4; INTERLEUKIN 6; PROTEIN P28; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSFORMING GROWTH FACTOR BETA; GATA3 PROTEIN, MOUSE; IL10 PROTEIN, MOUSE;

ADOPTIVE TRANSFER; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL FRACTIONATION; CELL FUNCTION; CELL PROLIFERATION; CHAGAS DISEASE; CONTROLLED STUDY; CORTICOSTEROID RELEASE; CORTICOSTEROID THERAPY; CORTICOSTERONE BLOOD LEVEL; CYTOKINE PRODUCTION; EFFECTOR CELL; HORMONE DETERMINATION; IMMUNE RESPONSE; LOW DRUG DOSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SURVIVAL TIME; T CELL DEPLETION; TH1 CELL; TH1 TH2 BALANCE; ADRENALECTOMY; ANIMAL; BLOOD; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; HEART MUSCLE; IMMUNOLOGY; PATHOLOGY; PHENOTYPE; SKELETAL MUSCLE; TRYPANOSOMA CRUZI;

ADRENALECTOMY; ANIMALS; CHAGAS CARDIOMYOPATHY; CHAGAS DISEASE; CORTICOSTERONE; DEXAMETHASONE; DISEASE MODELS, ANIMAL; GATA3 TRANSCRIPTION FACTOR; GLUCOCORTICOIDS; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-2; INTERLEUKIN-4; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; MYOCARDIUM; PHENOTYPE; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TRYPANOSOMA CRUZI;

EID: 84924020611     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.11.016     Document Type: Article

References (65)

1. + regulatory T cells (TREG) in systemic lupus erythematosus (SLE) patients: the possible influence of treatment with corticosteroids. Clin. Immunol. 2008, 127:151-157.
2. + T cell responses in acute and chronic viral infections. Eur. J. Immunol. 2007, 37:1502-1512.
3. (+) T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2-inducing cytokines. J. Exp. Med. 2002, 195:603-616.
4. Baeyens A., Pérol L., Fourcade G., Cagnard N., Carpentier W., Woytschak J., Boyman O., Hartemann A., Piaggio E. Limitations of IL-2 and rapamycin in immunotherapy of type 1 diabetes. Diabetes 2013, 62(9):3120-3131.
5. Caretto D., Katzman S.D., Villarino A.V., Gallo E., Abbas A.K. Cutting edge: the Th1 response inhibits the generation of peripheral regulatory T cells. J. Immunol. 2010, 184:30-34.
6. Coura J.R., Borges-Pereira J. Chagas disease: 100 years after its discovery. A systemic review. Acta Trop. 2010, 115:5-13.
7. (+) T regulatory cells in vivo and enhances their capacity to suppress EAE. Eur. J. Immunol. 2006, 36:2139-2149.
8. de Araujo F.F., Vitelli-Avelar D.M., Teixeira-Carvalho A., Antas P.R., Assis Silva Gomes J., Sathler-Avelar R., Otavio Costa Rocha M., Eloi-Santos S.M., Pinho R.T., Correa-Oliveira R., Martins-Filho O.A. Regulatory T cells phenotype in different clinical forms of Chagas' disease. PLoS Negl. Trop. Dis. 2011, 5:e992.
9. + regulatory T cells and attenuates development and progression of atherosclerosis. Circulation 2012, 126:1256-1266.
10. Dutra W.O., Menezes C.A., Magalhaes L.M., Gollob K.J. Immunoregulatory networks in human Chagas disease. Parasite Immunol. 2014, 36(8):377-387.
11. Dutt S., Tseng D., Ermann J., George T.I., Liu Y.P., Davis C.R., Fathman C.G., Strober S. Naive and memory T cells induce different types of graft-versus-host disease. J. Immunol. 2007, 179:6547-6554.
12. Fehervari Z., Yamaguchi T., Sakaguchi S. The dichotomous role of IL-2: tolerance versus immunity. Trends Immunol. 2006, 27:109-111.
13. Fontenot J.D., Dooley J.L., Farr A.G., Rudensky A.Y. Developmental regulation of Foxp3 expression during ontogeny. J. Exp. Med. 2005, 202:901-906.
14. Fontenot J.D., Rasmussen J.P., Gavin M.A., Rudensky A.Y. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 2005, 6:1142-1151.
15. Grinberg-Bleyer Y., Baeyens A., You S., Elhage R., Fourcade G., Gregoire S., Cagnard N., Carpentier W., Tang Q., Bluestone J., Chatenoud L., Klatzmann D., Salomon B.L., Piaggio E. IL-2 reverses established type 1 diabetes in NOD mice by a local effect on pancreatic regulatory T cells. J. Exp. Med. 2010, 207:1871-1878.
16. Hall A.O., Beiting D.P., Tato C., John B., Oldenhove G., Lombana C.G., Pritchard G.H., Silver J.S., Bouladoux N., Stumhofer J.S., Harris T.H., Grainger J., Wojno E.D., Wagage S., Roos D.S., Scott P., Turka L.A., Cherry S., Reiner S.L., Cua D., Belkaid Y., Elloso M.M., Hunter C.A. The cytokines interleukin 27 and interferon-gamma promote distinct Treg cell populations required to limit infection-induced pathology. Immunity 2012, 37:511-523.
17. Hall A.O., Silver J.S., Hunter C.A. The immunobiology of IL-27. Adv. Immunol. 2012, 115:1-44.
18. Hall B.M., Tran G.T., Verma N.D., Plain K.M., Robinson C.M., Nomura M., Hodgkinson S.J. Do natural T regulatory cells become activated to antigen specific T regulatory cells in transplantation and in autoimmunity?. Front. Immunol. 2013, 4:208.
19. Hernandez-Pando R., Streber M., Orozco H., Arriaga K., Pavon L., Al-Nakhli S.A., Rook G.A. The effects of androstenediol and dehydroepiandrosterone on the course and cytokine profile of tuberculosis in BALB/c mice. Immunology 1998, 95:234-241.
20. + regulatory T cells. J. Exp. Med. 2004, 199:303-313.
21. Karagiannidis C., Akdis M., Holopainen P., Woolley N.J., Hense G., Rückert B., Mantel P.Y., Menz G., Akdis C.A., Blaser K., Schmidt-Weber C.B. Glucocorticoids upregulate FOXP3 expression and regulatory T cells in asthma. J. Allergy Clin. Immunol. 2004, 114(6):1425-1433.
22. Koch M.A., Tucker-Heard G., Perdue N.R., Killebrew J.R., Urdahl K.B., Campbell D.J. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 2009, 10:595-602.
23. Koreth J., Matsuoka K., Kim H.T., McDonough S.M., Bindra B., Alyea E.P., Armand P., Cutler C., Ho V.T., Treister N.S., Bienfang D.C., Prasad S., Tzachanis D., Joyce R.M., Avigan D.E., Antin J.H., Ritz J., Soiffer R.J. Interleukin-2 and regulatory T cells in graft-versus-host disease. N. Engl. J. Med. 2011, 365:2055-2066.
24. (+) regulatory T cells have a limited role in the control of Trypanosoma cruzi infection in mice. Infect. Immun. 2007, 75:861-869.
25. La Cava A. Tregs are regulated by cytokines: implications for autoimmunity. Autoimmun. Rev. 2008, 8:83-87.
26. Malek T.R. The main function of IL-2 is to promote the development of T regulatory cells. J. Leukoc. Biol. 2003, 74:961-965.
27. Malek T.R., Bayer A.L. Tolerance, not immunity, crucially depends on IL-2. Nat. Rev. Immunol. 2004, 4:665-674.
28. + T cells in the acute phase of Trypanosoma cruzi infection. Microbes Infect. 2008, 10:825-833.
29. Matsuoka K., Koreth J., Kim H.T., Bascug G., McDonough S., Kawano Y., Murase K., Cutler C., Ho V.T., Alyea E.P., Armand P., Blazar B.R., Antin J.H., Soiffer R.J., Ritz J. Low-dose interleukin-2 therapy restores regulatory T cell homeostasis in patients with chronic graft-versus-host disease. Sci. Transl. Med. 2013, 5:179ra143.
30. Matta Guedes P.M., Gutierrez F.R., Nascimento M.S., Do-Valle-Matta M.A., Silva J.S. Antiparasitical chemotherapy in Chagas' disease cardiomyopathy: current evidence. Trop. Med. Int. Health 2012, 17:1057-1065.
31. Nunes M.C., Dones W., Morillo C.A., Encina J.J., Ribeiro A.L., Ribeiro A.L., Council on Chagas Disease of the Interamerican Society of Cardiology Chagas disease: an overview of clinical and epidemiological aspects. J. Am. Coll. Cardiol. 2013, 62:767-776.
32. + effector T cells. J. Immunol. 2006, 176:7278-7287.
33. + Treg cell number and acquisition of effector cell phenotype during lethal infection. Immunity 2009, 31:772-786.
34. Pandolfi J., Baz P., Fernández P., Discianni Lupi A., Payaslián F., Billordo L.A., Fainboim L., Arruvito L. Regulatory and effector T-cells are differentially modulated by Dexamethasone. Clin. Immunol. 2013, 149(3):400-410.
35. Perez A.R., Roggero E., Nicora A., Palazzi J., Besedovsky H.O., Del Rey A., Bottasso O.A. Thymus atrophy during Trypanosoma cruzi infection is caused by an immuno-endocrine imbalance. Brain Behav. Immun. 2007, 21:890-900.
36. Piaggio E., Sanceau J., Revelli S., Bottasso O., Wietzerbin J., Serra E. Trypanocidal drug benznidazole impairs lipopolysaccharide induction of macrophage nitric oxide synthase gene transcription through inhibition of NF-kappaB activation. J. Immunol. 2001, 167:3422-3426.
37. Ramirez J.D., Montilla M., Cucunuba Z.M., Florez A.C., Zambrano P., Guhl F. Molecular epidemiology of human oral Chagas disease outbreaks in Colombia. PLoS Negl. Trop. Dis. 2013, 7:e2041.
38. Ratman D., Vanden Berghe W., Dejager L., Libert C., Tavernier J., Beck I.M., de Bosscher K. How glucocorticoid receptors modulate the activity of other transcription factors: a scope beyond tethering. Mol. Cell. Endocrinol. 2013, 380(1-2):41-54.
39. Roggero E., Perez A., Tamae-Kakazu M., Piazzon I., Nepomnaschy I., Wietzerbin J., Serra E., Revelli S., Bottasso O. Differential susceptibility to acute Trypanosoma cruzi infection in BALB/c and C57BL/6 mice is not associated with a distinct parasite load but cytokine abnormalities. Clin. Exp. Immunol. 2002, 128:421-428.
40. Roggero E., Perez A.R., Bottasso O.A., Besedovsky H.O., Del Rey A. Neuroendocrine-immunology of experimental Chagas' disease. Ann. N. Y. Acad. Sci. 2009, 1153:264-271.
41. Roggero E., Perez A.R., Tamae-Kakazu M., Piazzon I., Nepomnaschy I., Besedovsky H.O., Bottasso O.A., del Rey A. Endogenous glucocorticoids cause thymus atrophy but are protective during acute Trypanosoma cruzi infection. J. Endocrinol. 2006, 190:495-503.
42. Ronco M.T., Manarin R., Frances D., Serra E., Revelli S., Carnovale C. Benznidazole treatment attenuates liver NF-kappaB activity and MAPK in a cecal ligation and puncture model of sepsis. Mol. Immunol. 2011, 48:867-873.
43. Saadoun D., Rosenzwajg M., Joly F., Six A., Carrat F., Thibault V., Sene D., Cacoub P., Klatzmann D. Regulatory T-cell responses to low-dose interleukin-2 in HCV-induced vasculitis. N. Engl. J. Med. 2011, 365:2067-2077.
44. Sakaguchi S., Vignali D.A., Rudensky A.Y., Niec R.E., Waldmann H. The plasticity and stability of regulatory T cells. Nat. Rev. Immunol. 2013, 13:461-467.
45. + T cells have a limited role on pathogenesis of infection with Trypanosoma cruzi. Microbes Infect. 2008, 10:680-688.
46. 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, 401:708-712.
47. Sathler-Avelar R., Vitelli-Avelar D.M., Teixeira-Carvalho A., Martins-Filho O.A. Innate immunity and regulatory T-cells in human Chagas disease: what must be understood?. Mem. Inst. Oswaldo Cruz 2009, 104(Suppl. 1):246-251.
48. Savino W., Villa-Verde D.M., Mendes-da-Cruz D.A., Silva-Monteiro E., Perez A.R., Aoki Mdel P., Bottasso O., Guinazu N., Silva-Barbosa S.D., Gea S. Cytokines and cell adhesion receptors in the regulation of immunity to Trypanosoma cruzi. Cytokine Growth Factor Rev. 2007, 18:107-124.
49. Sbiera S., Dexneit T., Reichardt S.D., Michel K.D., van den Brandt J., Schmull S., Kraus L., Beyer M., Mlynski R., Wortmann S., Allolio B., Reichardt H.M., Fassnacht M. Influence of short-term glucocorticoid therapy on regulatory T cells in vivo. PLoS ONE 2011, 6(9):e24345.
50. Silverio J.C., Pereira I.R., Cipitelli Mda C., Vinagre N.F., Rodrigues M.M., Gazzinelli R.T., Lannes-Vieira J. CD8+ T-cells expressing interferon gamma or perforin play antagonistic roles in heart injury in experimental Trypanosoma cruzi-elicited cardiomyopathy. PLoS Pathog. 2012, 8:e1002645.
51. Smigiel K.S., Richards E., Srivastava S., Thomas K.R., Dudda J.C., Klonowski K.D., Campbell D.J. CCR7 provides localized access to IL-2 and defines homeostatically distinct regulatory T cell subsets. J. Exp. Med. 2014, 211:121-136.
52. Tang Q., Adams J.Y., Penaranda C., Melli K., Piaggio E., Sgouroudis E., Piccirillo C.A., Salomon B.L., Bluestone J.A. Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity 2008, 28:687-697.
53. Unger W.W., Laban S., Kleijwegt F.S., van der Slik A.R., Roep B.O. Induction of Treg by monocyte-derived DC modulated by vitamin D3 or dexamethasone: differential role for PD-L1. Eur. J. Immunol. 2009, 39:3147-3159.
54. hi T-regulatory cells. Blood 2006, 108:253-261.
55. Vandevyver S., Dejager L., Tuckermann J., Libert C. New insights into the anti-inflammatory mechanisms of glucocorticoids: an emerging role for glucocorticoid-receptor-mediated transactivation. Endocrinology 2013, 154(3):993-1007.
56. Wan S., Xia C., Morel L. IL-6 produced by dendritic cells from lupus-prone mice inhibits CD4+CD25+ T cell regulatory functions. J. Immunol. 2007, 178:271-279.
57. Webster K.E., Walters S., Kohler R.E., Mrkvan T., Boyman O., Surh C.D., Grey S.T., Sprent J. In vivo expansion of T reg cells with IL-2-mAb complexes: induction of resistance to EAE and long-term acceptance of islet allografts without immunosuppression. J. Exp. Med. 2009, 206:751-760.
58. Wilson M.S., Pesce J.T., Ramalingam T.R., Thompson R.W., Cheever A., Wynn T.A. Suppression of murine allergic airway disease by IL-2:anti-IL-2 monoclonal antibody-induced regulatory T cells. J. Immunol. 2008, 181:6942-6954.
59. (+) regulatory T cell fate during inflammation in mice. J. Clin. Investig. 2011, 121:4503-4515.
60. Wüst S., van den Brandt J., Tischner D., Kleiman A., Tuckermann J.P., Gold R., Lühder F., Reichardt H.M. Peripheral T cells are the therapeutic targets of glucocorticoids in experimental autoimmune encephalomyelitis. J. Immunol. 2008, 180(12):8434-8443.
61. (+) regulatory T cells in vivo and suppresses graft-versus-host disease after allogeneic lymphocyte transplantation. Acta Biochim. Biophys. Sin. 2009, 41:781-791.
62. Yoshimoto T., Yoshimoto T., Yasuda K., Mizuguchi J., Nakanishi K. IL-27 suppresses Th2 cell development and Th2 cytokines production from polarized Th2 cells: a novel therapeutic way for Th2-mediated allergic inflammation. J. Immunol. 2007, 179:4415-4423.
63. Yu A., Zhu L., Altman N.H., Malek T.R. A low interleukin-2 receptor signaling threshold supports the development and homeostasis of T regulatory cells. Immunity 2009, 30:204-217.
64. (+) T reg cells in the central nervous system during encephalomyelitis. J. Exp. Med. 2011, 208:1571-1577.
65. Zhou X., Bailey-Bucktrout S.L., Jeker L.T., Penaranda C., Martinez-Llordella M., Ashby M., Nakayama M., Rosenthal W., Bluestone J.A. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat. Immunol. 2009, 10:1000-1007.