Unique roles of Schistosoma japonicum protein Sj16 to induce IFN-γ and IL-10 producing CD4+CD25+ regulatory T cells in vitro and in vivo

Parasite Immunology

Volumn 34, Issue 8-9, 2012, Pages 430-439

  Sun, X J ^a   Li, R ^a   Sun, X ^b   Zhou, Y ^a   Wang, Y ^a   Liu, X J ^a   Lu, Q ^a   Zhou, C L ^a   Wu, Z D ^b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

BMDCs; CD4+CD25+ regulatory T cells; IFN ; Schistosoma japonicum; Sj16

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; RECOMBINANT PROTEIN; SCHISTOSOMA JAPONICUM PROTEIN 16; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CD4+ CD25+ T LYMPHOCYTE; CELL POPULATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; GENE REPRESSION; IN VITRO STUDY; IN VIVO STUDY; MICROENVIRONMENT; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SCHISTOSOMA JAPONICUM; SCHISTOSOMIASIS JAPONICA; SPLEEN CELL;

ANIMALS; ANTIGENS, CD4; ANTIGENS, HELMINTH; CELL PROLIFERATION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HELMINTH PROTEINS; IMMUNE TOLERANCE; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; SCHISTOSOMA JAPONICUM; SPLEEN; T-LYMPHOCYTES, REGULATORY;

MUS; SCHISTOSOMA; SCHISTOSOMA JAPONICUM; VERMES; VERTEBRATA;

EID: 84864762979     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2012.01377.x     Document Type: Article

References (50)

1. Li SZ, Luz A, Wang XH, et al. Schistosomiasis in China: acute infections during 2005-2008. Chin Med J (Engl) 2009; 122: 1009-1014.
2. Ramaswamy K, Salafsky B, Potluri S, He YX, Li JW & Shibuya T. Secretion of an anti-inflammatory, immunomodulatory factor by Schistosomulae of Schistosoma mansoni. J Inflamm 1995; 46: 13-22.
3. Ramaswamy K, He YX & Salafsky B. ICAM-1 and iNOS expression increased in the skin of mice after vaccination with gamma-irradiated cercariae of Schistosoma mansoni. Exp Parasitol 1997; 86: 118-132.
4. Hewitson JP, Grainger JR & Maizels RM. Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol 2009; 167: 1-11.
5. Curwen RS, Ashton PD, Sundaralingam S & Wilson RA. Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Mol Cell Proteomics 2006; 5: 835-844.
6. Rao KV & Ramaswamy K. Cloning and expression of a gene encoding Sm16, an anti-inflammatory protein from Schistosoma mansoni. Mol Biochem Parasitol 2000; 108: 101-108.
7. Gobert GN, Moertel L, Brindley PJ & McManus DP. Developmental gene expression profiles of the human pathogen Schistosoma japonicum. BMC Genomics 2009; 10: 128.
8. Hu S, Wu Z, Yang L & Fung MC. Molecular cloning and expression of a functional anti-inflammatory protein, Sj16, of Schistosoma japonicum. Int J Parasitol 2009; 39: 191-200.
9. Sun X, Liu YH, Lv ZY, et al. rSj16, a recombinant protein of Schistosoma japonicum-derived molecule, reduces severity of the complete Freund's adjuvant-induced adjuvant arthritis in rats' model. Parasite Immunol 2010; 32: 739-748.
10. Taylor JJ, Mohrs M & Pearce EJ. Regulatory T cell responses develop in parallel to Th responses and control the magnitude and phenotype of the Th effector population. J Immunol 2006; 176: 5839-5847.
11. Layland LE, Rad R, Wagner H & da Costa CU. Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2. Eur J Immunol 2007; 37: 2174-2184.
12. McKee AS & Pearce EJ. CD25+CD4+ cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development. J Immunol 2004; 173: 1224-1231.
13. Mahnke K & Enk AH. Dendritic cells: key cells for the induction of regulatory T cells? Curr Top Microbiol Immunol 2005; 293: 133-150.
14. Quintana FJ & Cohen IR. Regulatory T cells and immune computation. Eur J Immunol 2008; 38: 903-907.
15. McGuirk P & Mills KH. Pathogen-specific regulatory T cells provoke a shift in the Th1/Th2 paradigm in immunity to infectious diseases. Trends Immunol 2002; 23: 450-455.
16. Doetze A, Satoguina J, Burchard G, et al. Antigen-specific cellular hyporesponsiveness in a chronic human helminth infection is mediated by T(h)3/T(r)1-type cytokines IL-10 and transforming growth factor-beta but not by a T(h)1 to T(h)2 shift. Int Immunol 2000; 12: 623-630.
17. Hauet-Broere F, Wieten L, Guichelaar T, Berlo S, van der Zee R & Van Eden W. Heat shock proteins induce T cell regulation of chronic inflammation. Ann Rheum Dis 2006; 65(Suppl 3): iii65-iii68.
18. Yang J, Zhao J, Yang Y, et al. Schistosoma japonicum egg antigens stimulate CD4 CD25 T cells and modulate airway inflammation in a murine model of asthma. Immunology 2007; 120: 8-18.
19. Mountford AP & Trottein F. Schistosomes in the skin: a balance between immune priming and regulation. Trends Parasitol 2004; 20: 221-226.
20. Smith P, Mangan NE & Fallon PG. Generation of parasite antigens for use in Toll-like receptor research. Methods Mol Biol 2009; 517: 401-413.
21. Qureshi MH, Empey KM & Garvy BA. Modulation of proinflammatory responses to Pneumocystis carinii f. sp. muris in neonatal mice by granulocyte-macrophage colony-stimulating factor and IL-4: role of APCs. J Immunol 2005; 174: 441-448.
22. Li A, Ojogho O, Franco E, Baron P, Iwaki Y & Escher A. Pro-apoptotic DNA vaccination ameliorates new onset of autoimmune diabetes in NOD mice and induces foxp3+ regulatory T cells in vitro. Vaccine 2006; 24: 5036-5046.
23. Sornasse T, Larenas PV, Davis KA, de Vries JE & Yssel H. Differentiation and stability of T helper 1 and 2 cells derived from naive human neonatal CD4+ T cells, analyzed at the single-cell level. J Exp Med 1996; 184: 473-483.
24. Fontenot JD, Gavin MA & Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003; 4: 330-336.
25. Takahashi T, Kuniyasu Y, Toda M, et al. Immunologic self-tolerance maintained by CD25+CD4+ naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state. Int Immunol 1998; 10: 1969-1980.
26. Thornton AM & Shevach EM. CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 1998; 188: 287-296.
27. Vlad G, Cortesini R & Suciu-Foca N. License to heal: bidirectional interaction of antigen-specific regulatory T cells and tolerogenic APC. J Immunol 2005; 174: 5907-5914.
28. Szabo SJ, Sullivan BM, Stemmann C, Satoskar AR, Sleckman BP & Glimcher LH. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 2002; 295: 338-342.
29. Pearce EJ. Priming of the immune response by schistosome eggs. Parasite Immunol 2005; 27: 265-270.
30. Mills KH. Regulatory T cells: friend or foe in immunity to infection? Nat Rev Immunol 2004; 4: 841-855.
31. Sakaguchi S, Ono M, Setoguchi R, et al. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 2006; 212: 8-27.
32. Belkaid Y & Rouse BT. Natural regulatory T cells in infectious disease. Nat Immunol 2005; 6: 353-360.
33. Hong J, Li N, Zhang X, Zheng B & Zhang JZ. Induction of CD4+CD25+ regulatory T cells by copolymer-I through activation of transcription factor Foxp3. Proc Natl Acad Sci U S A 2005; 102: 6449-6454.
34. Jonuleit H, Schmitt E, Schuler G, Knop J & Enk AH. Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med 2000; 192: 1213-1222.
35. Vignali DA, Collison LW & Workman CJ. How regulatory T cells work. Nat Rev Immunol 2008; 8: 523-532.
36. Enk AH. DCs and cytokines cooperate for the induction of tregs. Ernst Schering Res Found Workshop 2006; 56: 97-106.
37. Hogg KG, Kumkate S, Anderson S & Mountford AP. Interleukin-12 p40 secretion by cutaneous CD11c+ and F4/80+ cells is a major feature of the innate immune response in mice that develop Th1-mediated protective immunity to Schistosoma mansoni. Infect Immun 2003; 71: 3563-3571.
38. Hogg KG, Kumkate S & Mountford AP. IL-10 regulates early IL-12-mediated immune responses induced by the radiation-attenuated schistosome vaccine. Int Immunol 2003; 15: 1451-1459.
39. Angeli V, Faveeuw C, Roye O, et al. Role of the parasite-derived prostaglandin D2 in the inhibition of epidermal Langerhans cell migration during schistosomiasis infection. J Exp Med 2001; 193: 1135-1147.
40. Iannone F, De Bari C, Dell'Accio F, et al. Interleukin-10 and interleukin-10 receptor in human osteoarthritic and healthy chondrocytes. Clin Exp Rheumatol 2001; 19: 139-145.
41. Abbas AK, Murphy KM & Sher A. Functional diversity of helper T lymphocytes. Nature 1996; 383: 787-793.
42. Romagnani S. Lymphokine production by human T cells in disease states. Annu Rev Immunol 1994; 12: 227-257.
43. Zhao J, Fett C, Trandem K, Fleming E & Perlman S. IFN-{gamma}- and IL-10-expressing virus epitope-specific Foxp3+ T reg cells in the central nervous system during encephalomyelitis. J Exp Med 2011; 208: 1571-1577.
44. Hu X & Ivashkiv LB. Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity 2009; 31: 539-550.
45. Barnes MJ & Powrie F. Hybrid Treg cells: steel frames and plastic exteriors. Nat Immunol 2009; 10: 563-564.
46. Hewitson JP, Hamblin PA & Mountford AP. Immunity induced by the radiation-attenuated schistosome vaccine. Parasite Immunol 2005; 27: 271-280.
47. Tao FF, Yang YF, Wang H, et al. Th1-type epitopes-based cocktail PDDV attenuates hepatic fibrosis in C57BL/6 mice with chronic Schistosoma japonicum infection. Vaccine 2009; 27: 4110-4117.
48. El Ridi R, Salem R, Wagih A, Mahana N, El Demellawy M & Tallima H. Influence of interleukin-2 and interferon-gamma in murine schistosomiasis. Cytokine 2006; 33: 281-288.
49. Wang Z, Hong J, Sun W, et al. Role of IFN-gamma in induction of Foxp3 and conversion of CD4+ CD25- T cells to CD4+ Tregs. J Clin Invest 2006; 116: 2434-2441.
50. Koch MA, Tucker-Heard G, Perdue NR, Killebrew JR, Urdahl KB & Campbell DJ. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat Immunol 2009; 10: 595-602.