Trypanosoma cruzi evades the protective role of interferon-gamma-signaling in parasite-infected cells

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Stahl, Philipp ^a   Ruppert, Volker ^a   Schwarz, Ralph T ^a,c   Meyer, Thomas ^b  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; STAT1 PROTEIN; PHOSPHOSERINE; STAT1 PROTEIN, HUMAN;

AMASTIGOTE; ARTICLE; BINDING AFFINITY; CHAGAS DISEASE; CONTROLLED STUDY; DNA BINDING; DOSE RESPONSE; GENE IDENTIFICATION; HUMAN; HUMAN CELL; IDO GENE; IN VITRO STUDY; NONHUMAN; PARASITE CLEARANCE; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE; ANIMAL; BIOLOGICAL MODEL; CELL LINE; DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; PARASITE; PARASITOLOGY; PHOSPHORYLATION;

TRYPANOSOMA CRUZI;

ANIMALS; CELL LINE; CHAGAS DISEASE; GENE EXPRESSION REGULATION; HUMANS; IMMUNE EVASION; INTERFERON-GAMMA; MODELS, BIOLOGICAL; PARASITES; PHOSPHORYLATION; PHOSPHOSERINE; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TRYPANOSOMA CRUZI;

EID: 84908439918     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110512     Document Type: Article

References (53)

1. Boscardin SB, Torrecilhas AC, Manarin R, Revelli S., Rey EG, et al. (2010) Chagas' disease: an update on immune mechanisms and therapeutic strategies. J Cell Mol Med 14: 1373-1384.
2. Lescure FX, Le Loup G, Freilij H, Develoux M., Paris L, et al. (2010) Chagas disease: changes in knowledge and management. Lancet Infect Dis 10: 556-570.
3. Nagajyothi F, Machado FS, Burleigh B.A., Jelicks LA, Scherer PE, et al. (2012) Mechanisms of Trypanosoma cruzi persistence in Chagas disease. Cell Microbiol 14: 634-643.
4. Epting CL, Coates BM, Engman DM (2010) Molecular mechanisms of host cell invasion by Trypanosoma cruzi. Exp Parasitol 126: 283-291.
5. Sánchez LV, Ramírez JD (2013) Congenital and oral transmission of American trypanosomiasis: an overview of physiopathogenic aspects. Parasitol 140: 147-159.
6. Machado FS, Dutra WO, Esper L, Gollob K.J., Teixeira MM, et al. (2012) Current understanding of immunity to Trypanosoma cruzi infection and pathogenesis of Chagas disease. Semin Immunopathol 34: 753-770.
7. Gonçalves VM, Matteucci KC, Buzzo C.L., Miollo BH, Ferrante D, et al. (2013) NLRP3 controls Trypanosoma cruzi infection through a caspase-1-dependent IL-1R-independent NO production. PLoS Negl Trop Dis 7: e2469.
8. Truyens C, Angelo-Barrios A, Torrico F., van Damme J, Heremans H, et al. (1994) Interleukin-6 (IL-6) production in mice infected with Trypanosoma cruzi: effect of its paradoxical increase by anti-IL-6 monoclonal antibody treatment on infection and acute-phase and humoral immune responses. Infect Immun 62: 692-696.
9. Aliberti JC, Cardoso MA, Martins G.A., Gazzinelli RT, Vieira LQ, et al. (1996) Interleukin-12 mediates resistance to Trypanosoma cruzi in mice and is produced by murine macrophages in response to live trypomastigotes. Infect Immun 64: 1961-1967.
10. Camargo MM, Almeida IC, Pereira M.E., Ferguson MA, Travassos LR, et al. (1997) Glycosylphosphatidylinositol-anchored mucin-like glycoproteins isolated from Trypanosoma cruzi trypomastigotes initiate the synthesis of proinflamma-tory cytokines by macrophages. J Immunol 158: 5890-5901.
11. Almeida IC, Camargo MM, Procópio DO, Silva L.S., Mehlert A., et al. (2000) Highly purified glycosylphosphatidylinositols from Trypanosoma cruzi are potent proinflammatory agents. EMBO J. 19: 1476-1485.
12. Antúnez MI, Cardoni RL (2000) IL-12 and IFNγ production, and NK cell activity, in acute and chronic experimental Trypanosoma cruzi infections. Immunol Lett 71: 103-109.
13. Michailowsky V, Silva NM, Rocha C.D., Vieira LQ, Lannes-Vieira J, et al. (2001) Pivotal role of interleukin-12 and interferon-γ axis in controlling tissue parasitism and inflammation in the heart and central nervous system during Trypanosoma cruzi infection. Am J Pathol 159: 1723-1733.
14. Bastos KR, Barboza R, Sardinha L., Russo M, Alvarez JM, et al. (2007) Role of endogenous IFNγ in macrophage programming induced by IL-12 and IL-18. J Interferon Cytokine Res 27: 399-410.
15. Kierszenbaum F, Sonnenfeld G (1984) Beta-interferon inhibits cell infection by Trypanosoma cruzi. J Immunol 132: 905-908.
16. Plata F, Wietzerbin J, Pons F.G., Falcoff E., Eisen H (1984) Synergistic protection by specific antibodies and interferon against infection by Trypanosoma cruzi in vitro. Eur J Immunol 14: 930-935.
17. Koga R, Hamano S, Kuwata H., Atarashi K, Ogawa M, et al. (2006) TLR-dependent induction of IFNβ mediates host defense against Trypanosoma cruzi. J Immunol 177: 7059-7066.
18. Chessler AD, Ferreira LR, Chang T.H., Fitzgerald KA, Burleigh BA (2008) A novel IFN regulatory factor 3-dependent pathway activated by trypanosomes triggers IFNβ in macrophages and fibroblasts. J Immunol 181: 7917-7924.
19. Wirth JJ, Kierszenbaum F, Sonnenfeld G., Zlotnik A (1985) Enhancing effects of gamma interferon on phagocytic cell association with and killing of Trypanosoma cruzi. Infect Immun 49: 61-66.
20. Rodrigues AA, Saosa JS, da Silva GK, Martins FA, da Silva AA, et al. (2012) IFNγ plays a unique role in protection against low virulent Trypanosoma cruzi strain. PLoS Negl Trop Dis 6: e1598.
21. Campos MA, Closel M, Valente E.P., Cardoso JE, Akira S, et al. (2004) Impaired production of proinflammatory cytokines and host resistance to acute infection with Trypanosoma cruzi in mice lacking functional myeloid differentiation factor 88. J Immunol 172: 1711-1718.
22. Huang H, Calderon TM, Berman J.W., Braunstein VL, Weiss LM, et al. (1999) Infection of endothelial cells with Trypanosoma cruzi activates NF-κB and induces vascular adhesion molecule expression. Infect Immun 67: 5434-5440.
23. Hall BS, Tam W, Sen R., Pereira ME (2000) Cell-specific activation of nuclear factor-κB by the parasite Trypanosoma cruzi promotes resistance to intracellular infection. Mol Biol Cell 11: 153-160.
24. Hovsepian E, Penas F, Siffo S., Mirkin GA, Goren NB (2013) IL-10 inhibits the NF-κB and ERK/MAPK-mediated production of pro-inflammatory mediators by up-regulation of SOCS-3 in Trypanosoma cruzi-infected cardiomyocytes. PLoS One 8: e79445.
25. Hölscher C, Köhler G, Müller U, Mossmann H., Schaub GA, et al. (1998) Defective nitric oxide effector functions lead to extreme susceptibility of Trypanosoma cruzi-infected mice deficient in gamma interferon receptor or inducible nitric oxide synthase. Infect Immun 66: 1208-1215.
26. Vaena de Avalos S, Blader IJ, Fisher M, Boothroyd JC, Burleigh BA (2002) Immediate/early response to Trypanosoma cruzi infection involves minimal modulation of host cell transcription. J Biol Chem 277: 639-644.
27. Bergeron M, Olivier M (2006) Trypanosoma cruzi-mediated IFNγ-inducible nitric oxide output in macrophages is regulated by iNOS mRNA stability. J Immunol 177: 6271-6280.
28. Poncini CV, Giménez G, Pontillo C.A., Alba-Soto CD, de Isola EL, et al. (2010) Central role of extracellular signal-regulated kinase and Toll-like receptor 4 in IL-10 production in regulatory dendritic cells induced by Trypanosoma cruzi. Mol Immunol 47: 1981-1988.
29. Cerávolo IP, Chaves AC, Bonjardim C.A., Sibley D., Romanha AJ, et al. (1999) Replication of Toxoplasma gondii, but not Trypanosoma cruzi, is regulated in human fibroblasts activated with gamma interferon: requirement of a functional JAK/STAT pathway. Infect Immun 67: 2233-2240.
30. Stahl P, Ruppert V, Meyer T., Schmidt J, Campos MA, et al. (2013) Trypomastigotes and amastigotes of Trypanosoma cruzi induce apoptosis and STAT3 activation in cardiomyocytes in vitro. Apoptosis 18: 653-663.
31. Darnell JE Jr, Kerr IM, Stark GR (1994) Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264: 1415-1421.
32. Vinkemeier U (2004) Getting the message across, STAT! Design principles of a molecular signaling circuit. J Cell Biol 167, 197-201.
33. Sehgal PB (2008) Paradigm shifts in the cell biology of STAT signaling. Semin Cell Dev Biol 19: 329-340.
34. Lödige I, Marg A, Wiesner B., Malecová B, Oelgeschläger T, et al. (2005) Nuclear export determines the cytokine sensitivity of STAT transcription factors. J Biol Chem 280: 43087-43099.
35. Wen Z, Zhong Z, Darnell JE Jr (1995) Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82: 241-250.
36. Kovarik P, Mangold M, Ramsauer K., Heidari H, Steinborn R, et al. (2001) Specificity of signaling by STAT1 depends on SH2 and C-terminal domains that regulate Ser727 phosphorylation, differentially affecting specific target gene expression. EMBO J 20: 91-100.
37. Varinou L, Ramsauer K, Karaghiosoff M., Kolbe T, Pfeffer K, et al. (2003) Phosphorylation of the Stat1 transactivation domain is required for full-fledged IFNγ-dependent innate immunity. Immunity 19: 793-802.
38. Müller M, Laxton C, Briscoe J., Schindler C, Improta T, et al. (1993) Complementation of a mutant cell line: central role of the 91 kDa polypeptide of ISGF3 in the interferon-α and -γ signal transduction pathways. EMBO J 12: 4221-4228.
39. Begitt A, Meyer T, van Rossum M, Vinkemeier U (2000) Nucleocytoplasmic translocation of Stat1 is regulated by a leucine-rich export signal in the coiled-coil domain. Proc Natl Acad Sci USA 97: 10418-10423.
40. Däubener W, Wanagat N, Pilz K., Seghrouchni S, Fischer HG, et al. (1994) A new, simple, bioassay for human IFNγ. J Immunol Methods 168: 39-47.
41. Pfaffl MW (2001) A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res 29: e45.
42. Cheon H, Yang J, Stark GR (2011) The functions of signal transducers and activators of transcriptions 1 and 3 as cytokine-inducible proteins. J Interferon Cytokine Res 31: 33-40.
43. Schneider AG, Abi Abdallah DS, Butcher BA, Denkers EY (2013) Toxoplasma gondii triggers phosphorylation and nuclear translocation of dendritic cell STAT1 while simultaneously blocking IFNγ-induced STAT1 transcriptional activity. PLoS One 8: e60215.
44. Martens S, Parvanova I, Zerrahn J., Griffiths G, Schell G, et al. (2005) Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathog 1: e24.
45. Machado FS, Martins GA, Aliberti J.C., 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.
46. Chatterjee-Kishore M, Wright KL, Ting J.P., Stark GR (2000) How Stat1 mediates constitutive gene expression: a complex of non-phosphorylated Stat1 and IRF1 supports transcription of the LMP2 gene. EMBO J 19, 4111-4122.
47. Kumar A, Commane M, Flickinger T.W., Horvath CM, Stark GR (1997) Defective TNF-a-induced apoptosis in STAT1-null cells due to low constitutive levels of caspases. Science 278: 1630-1632.
48. Stephanou A, Scarabelli TM, Brar B.K., Nakanishi Y., Matsumura M, et al. (2001) Induction of apoptosis and Fas receptor/Fas ligand expression by ischemia/reperfusion in cardiac myocytes requires serine 727 of the STAT-1 transcription factor but not tyrosine 701. J Biol Chem 276: 28340-28347.
49. Forget G, Gregory DJ, Olivier M (2005) Proteasome-mediated degradation of STAT1a following infection of macrophages with Leishmania donovani. J Biol Chem 280: 30542-30549.
50. Olivier M, Gregory DJ, Forget G (2005) Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin Microbiol Rev 18: 293-305.
51. Andrejeva J, Young DF, Goodbourn S, Randall RE (2002) Degradation of STAT1 and STAT2 by the V proteins of simian virus 5 and human parainfluenza virus type 2, respectively: consequences for virus replication in the presence of alpha/beta and gamma interferons. J Virol 76: 2159-2167.
52. Parisien JP, Lau JF, Rodriguez J.J., Ulane CM, Horvath CM (2002) Selective STAT protein degradation induced by paramyxoviruses requires both STAT1 and STAT2 but is independent of a/b interferon signal transduction. J Virol 76, 4190-4198.
53. Ramachandran A, Horvath CM (2009) Paramyxovirus disruption of interferon signal transduction: STATus report. J Interferon Cytokine Res 29: 531-537.