Schistosomes induce regulatory features in human and mouse CD1d hi B cells: Inhibition of allergic inflammation by IL-10 and regulatory T cells

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  van der Vlugt, Luciën E P M ^a   Labuda, Lucja A ^a   Ozir Fazalalikhan, Arifa ^a   Lievers, Ellen ^a   Gloudemans, Anouk K ^a,b   Liu, Kit Yeng ^a   Barr, Tom A ^c   Sparwasser, Tim ^d   Boon, Louis ^e   Ngoa, Ulysse Ateba ^f   Feugap, Eliane Ngoune ^f   Adegnika, Ayola A ^a,f,g   Kremsner, Peter G ^f,g   Gray, David ^c   Yazdanbakhsh, Maria ^a   Smits, Hermelijn H ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^e BIOCEROS   (Netherlands)

^f ALBERT SCHWEITZER HOSPITAL   (Gabon)

^g UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALBENDAZOLE; ARTEMISININ; CD1D ANTIGEN; INTERLEUKIN 10; PRAZIQUANTEL; TRANSCRIPTION FACTOR FOXP3; IL10 PROTEIN, HUMAN; IL10 PROTEIN, MOUSE;

ADOLESCENT; ALLERGY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HELMINTHIASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LUNG; MALARIA; MALE; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; SCHISTOSOMA HEMATOBIUM; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS HAEMATOBIA; SCHISTOSOMIASIS MANSONI; SCHOOL CHILD; SINGLE DRUG DOSE; SPLEEN; ANIMAL; GABON; HELMINTH; HYPERSENSITIVITY; IMMUNOLOGY; MOUSE MUTANT; PARASITOLOGY; PATHOLOGY; SCHISTOSOMA;

MUS; SCHISTOSOMA; SCHISTOSOMA HAEMATOBIUM; SCHISTOSOMA MANSONI; VERMES;

ANIMALS; ANTIGENS, CD1D; B-LYMPHOCYTES; CHILD; GABON; HELMINTHS; HUMANS; HYPERSENSITIVITY; INFLAMMATION; INTERLEUKIN-10; MICE; MICE, KNOCKOUT; SCHISTOSOMA; T-LYMPHOCYTES, REGULATORY;

EID: 84856712791     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030883     Document Type: Article

References (33)

1. Yazdanbakhsh M, Kremsner PG, van RR, (2002) Allergy, parasites, and the hygiene hypothesis. Science 296: 490-494 10.1126/science.296.5567.490 [doi];296/5567/490 [pii].
2. van den Biggelaar AH, van RR, Rodrigues LC, Lell B, Deelder AM, et al. (2000) Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356: 1723-1727 S0140-6736(00)03206-2 [pii];10.1016/S0140-6736(00)03206-2 [doi].
3. Fleming JO, (2011) Helminths and multiple sclerosis: will old friends give us new treatments for MS? J Neuroimmunol 233: 3-5 S0165-5728(11)00006-3 [pii];10.1016/j.jneuroim.2011.01.003 [doi].
4. Croese J, O'neil J, Masson J, Cooke S, Melrose W, et al. (2006) A proof of concept study establishing Necator americanus in Crohn's patients and reservoir donors. Gut 55: 136-137 55/1/136 [pii];10.1136/gut.2005.079129 [doi].
5. Park HK, Cho MK, Choi SH, Kim YS, Yu HS, (2011) Trichinella spiralis: infection reduces airway allergic inflammation in mice. Exp Parasitol 127: 539-544 S0014-4894(10)00323-1 [pii];10.1016/j.exppara.2010.10.004 [doi].
6. Wilson MS, Taylor MD, Balic A, Finney CA, Lamb JR, et al. (2005) Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J Exp Med 202: 1199-1212 jem.20042572 [pii];10.1084/jem.20042572 [doi].
7. Amu S, Saunders SP, Kronenberg M, Mangan NE, Atzberger A, et al. (2010) Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J Allergy Clin Immunol 125: 1114-1124 S0091-6749(10)00045-X [pii];10.1016/j.jaci.2010.01.018 [doi].
8. Smits HH, Hammad H, van NM, Soullie T, Willart MA, et al. (2007) Protective effect of Schistosoma mansoni infection on allergic airway inflammation depends on the intensity and chronicity of infection. J Allergy Clin Immunol 120: 932-940 S0091-6749(07)01051-2 [pii];10.1016/j.jaci.2007.06.009 [doi].
9. Maizels RM, Yazdanbakhsh M, (2008) T-cell regulation in helminth parasite infections: implications for inflammatory diseases. Chem Immunol Allergy 94: 112-123 154944 [pii];10.1159/000154944 [doi].
10. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM, (2002) B cells regulate autoimmunity by provision of IL-10. Nat Immunol 3: 944-950 10.1038/ni833 [doi];ni833 [pii].
11. Mizoguchi A, Bhan AK, (2006) A case for regulatory B cells. J Immunol 176: 705-710 176/2/705 [pii].
12. Ronet C, Hauyon-La TY, Revaz-Breton M, Mastelic B, Tacchini-Cottier F, et al. (2010) Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production. J Immunol 184: 886-894 jimmunol.0901114 [pii];10.4049/jimmunol.0901114 [doi].
13. Jankovic D, Cheever AW, Kullberg MC, Wynn TA, Yap G, et al. (1998) CD4+ T cell-mediated granulomatous pathology in schistosomiasis is downregulated by a B cell-dependent mechanism requiring Fc receptor signaling. J Exp Med 187: 619-629.
14. Mangan NE, Fallon RE, Smith P, van RN, McKenzie AN, et al. (2004) Helminth infection protects mice from anaphylaxis via IL-10-producing B cells. J Immunol 173: 6346-6356 173/10/6346 [pii].
15. Dilillo DJ, Matsushita T, Tedder TF, (2010) B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann N Y Acad Sci 1183: 38-57 NYAS5137 [pii];10.1111/j.1749-6632.2009.05137.x [doi].
16. Blair PA, Norena LY, Flores-Borja F, Rawlings DJ, Isenberg DA, et al. (2010) CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 32: 129-140 S1074-7613(09)00547-0 [pii];10.1016/j.immuni.2009.11.009 [doi].
17. Iwata Y, Matsushita T, Horikawa M, Dilillo DJ, Yanaba K, et al. (2011) Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 117: 530-541 blood-2010-07-294249 [pii];10.1182/blood-2010-07-294249 [doi].
18. Correale J, Farez M, Razzitte G, (2008) Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann Neurol 64: 187-199 10.1002/ana.21438 [doi].
19. Lahl K, Sparwasser T, (2011) In vivo depletion of FoxP3+ Tregs using the DEREG mouse model. Methods Mol Biol 707: 157-172 10.1007/978-1-61737-979-6_10 [doi].
20. Katz N, Chaves A, Pellegrino J, (1972) A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14: 397-400.
21. Adegnika AA, Verweij JJ, Agnandji ST, Chai SK, Breitling LP, et al. (2006) Microscopic and sub-microscopic Plasmodium falciparum infection, but not inflammation caused by infection, is associated with low birth weight. Am J Trop Med Hyg 75: 798-803 75/5/798 [pii].
22. Carter NA, Vasconcellos R, Rosser EC, Tulone C, Munoz-Suano A, et al. (2011) Mice lacking endogenous IL-10-producing regulatory B cells develop exacerbated disease and present with an increased frequency of Th1/Th17 but a decrease in regulatory T cells. J Immunol 186: 5569-5579 jimmunol.1100284 [pii];10.4049/jimmunol.1100284 [doi].
23. Madan R, Demircik F, Surianarayanan S, Allen JL, Divanovic S, et al. (2009) Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J Immunol 183: 2312-2320 jimmunol.0900185 [pii];10.4049/jimmunol.0900185 [doi].
24. Hussaarts L, van der Vlugt LE, Yazdanbakhsh M, Smits HH, (2011) Regulatory B-cell induction by helminths: Implications for allergic disease. J Allergy Clin Immunol 128: 733-739 S0091-6749(11)00767-6 [pii];10.1016/j.jaci.2011.05.012 [doi].
25. Mauri C, Ehrenstein MR, (2008) The 'short' history of regulatory B cells. Trends Immunol 29: 34-40 S1471-4906(07)00287-6 [pii];10.1016/j.it.2007.10.004 [doi].
26. Wilson MS, Taylor MD, O'Gorman MT, Balic A, Barr TA, et al. (2010) Helminth-induced CD19+CD23hi B cells modulate experimental allergic and autoimmune inflammation. Eur J Immunol 40: 1682-1696 10.1002/eji.200939721 [doi].
27. Watanabe R, Fujimoto M, Ishiura N, Kuwano Y, Nakashima H, et al. (2007) CD19 expression in B cells is important for suppression of contact hypersensitivity. Am J Pathol 171: 560-570 S0002-9440(10)61989-X [pii];10.2353/ajpath.2007.061279 [doi].
28. Blair PA, Chavez-Rueda KA, Evans JG, Shlomchik MJ, Eddaoudi A, et al. (2009) Selective targeting of B cells with agonistic anti-CD40 is an efficacious strategy for the generation of induced regulatory T2-like B cells and for the suppression of lupus in MRL/lpr mice. J Immunol 182: 3492-3502 182/6/3492 [pii];10.4049/jimmunol.0803052 [doi].
29. Lloyd CM, Hawrylowicz CM, (2009) Regulatory T cells in asthma. Immunity 31: 438-449 S1074-7613(09)00363-X [pii];10.1016/j.immuni.2009.08.007 [doi].
30. Hartl D, Koller B, Mehlhorn AT, Reinhardt D, Nicolai T, et al. (2007) Quantitative and functional impairment of pulmonary CD4+CD25hi regulatory T cells in pediatric asthma. J Allergy Clin Immunol 119: 1258-1266 S0091-6749(07)00421-6 [pii];10.1016/j.jaci.2007.02.023 [doi].
31. Karlsson MR, Rugtveit J, Brandtzaeg P, (2004) Allergen-responsive CD4+CD25+ regulatory T cells in children who have outgrown cow's milk allergy. J Exp Med 199: 1679-1688 10.1084/jem.20032121 [doi];jem.20032121 [pii].
32. Shreffler WG, Wanich N, Moloney M, Nowak-Wegrzyn A, Sampson HA, (2009) Association of allergen-specific regulatory T cells with the onset of clinical tolerance to milk protein. J Allergy Clin Immunol 123: 43-52 S0091-6749(08)01868-X [pii];10.1016/j.jaci.2008.09.051 [doi].
33. Velupillai P, Secor WE, Horauf AM, Harn DA, (1997) B-1 cell (CD5+B220+) outgrowth in murine schistosomiasis is genetically restricted and is largely due to activation by polylactosamine sugars. J Immunol 158: 338-344.