Preconceptional allergen immunization can induce offspring IL-17 secreting B cells (B17): do they share similarities with regulatory B10 cells?
Main Article Content
Keywords
Allergy, OVA, Maternal-fetal interface, IL-17, B cells
Abstract
Background: IL-17-producing B cells can be identified in both mice and human and were named B17 cells. The role of B17 cells still needs to be elucidated and its inflammatory or regulatory functions remain controversial.
Objective: We evaluate the effect of maternal immunization with OVA on offspring B cells that produces IL-17 and can show a regulatory potential by IL-10 production.
Methods: C57BL/6 WT, IL-10−/− or CD28−/− female mice were immunized or not with OVA in Alum, and immunized females were boosted after 10 and 20 days. Immunized and nonimmunized females were mated, and pups from both groups were evaluated at 3 or 20 days old (d.o.). Some offspring from the aforementioned two groups were immunized with OVA at 3 d.o., boosted after 10 days and evaluated at 20 d.o.
Results: Maternal immunization with OVA-induced offspring B cells to produce IL-17 at higher intensity compared to the control group of offspring at 3 d.o. This effect was maintained until 20 d.o. and even after neonatal immunization with OVA. The co-production of IL-10 on offspring IL-17 + B cells is up-regulated in response to maternal immunization with OVA. Maternal immunization with OVA on IL-10−/− mice reveals reduced percentage and mean of fluorescence intensity of IL-17 on B cells of offspring.
Conclusion: Preconception OVA immunization can induce offspring B cells that produce IL-17 at higher intensity and co-produce mainly IL-10. This could be the reason why B17 cells had been described in the literature with controversial roles upon their regulatory function.
References
2. Victor J, Fusaro A, Duarte A, Sato M. Preconception maternal immunization to dust mite inhibits the type I hypersensitivity response of offspring. J Allerg Clin Immunol. 2003;111:269-77.
3. Rigato PO, Fusaro AE, Victor JR, Sato MN. Maternal immunization to modulate the development of allergic response and pathogen infections. Immunotherapy. 2009;1:141-56.
4. Muniz BP, Victor JR, Oliveira LD, de Lima Lira M, Perini AA, Olivo A, et al. Tolerogenic microenvironment in neonatal period induced by maternal immunization with ovalbumin. Immunobiology. 2014;219:377-84.
5. Fusaro AE, de Brito CA, Taniguchi EF, Muniz BP, Victor JR, Orii NM, et al. Balance between early life tolerance and sensitization in allergy: dependence on the timing and intensity of prenatal and postnatal allergen exposure of the mother. Immunology. 2009;128:e541-50.
6. Fusaro AE, Brito CA, Victor JR, Rigato PO, Goldoni AL, Duarte AJS, et al. Maternal-fetal interaction: preconception immunization in mice prevents neonatal sensitization induced by allergen exposure during pregnancy and breastfeeding. Immunology. 2007;122:107-15.
7. Fusaro A, Maciel M, Victor J, Oliveira C, Duarte A, Sato M. Influence of maternal murine immunization with Dermatophagoides pteronyssinus extract on the type I hypersensitivity response in offspring. Int Arch Allerg Immunol. 2002;127:208-16.
8. de Lima Lira AA, de Oliveira MG, de Oliveira LM, da Silva Duarte AJ, Sato MN, Victor JR. Maternal immunization with ovalbumin
or Dermatophagoides pteronyssinus has opposing effects on Fc gamma RIIb expression on offspring B cells. Allerg Asthma Clin Immunol. 2014;10:47.
9. Oliveira C, Taniguchi E, Fusaro A, Victor J, Brito C, Duarte A, et al. Bystander effect in synergy to anergy in oral tolerance of Blomia tropicalis/ovalbumin murine co-immunization model. J. Clin. Immunol. 2005;25:153-61.
10. Futata E, de Brito C, Victor J, Fusaro A, Oliveira C, Maciel M, et al. Long-term anergy in orally tolerized mice is linked to decreased B7.2 expression on B cells. Immunobiology. 2006;211:157-66.
11. Bento-de-Souza L, Victor JR, Bento-de-Souza LC, Arrais-Santos M, Rangel-Santos AC, Pereira-Costa É, et al. Constitutive expression of genes encoding notch receptors and ligands in developing lymphocytes, nTreg cells and dendritic cells in the human thymus. Results Immunol. 2016;6:15-20.
12. Victor JR. Influence of maternal immunization with allergens on the thymic maturation of lymphocytes with regulatory potential in children: a broad field for further exploration. J Immunol Res. 2014;2014. Article id: 780386.
13. Sgnotto FDR, Oliveira MG, Lira AAL, Bento-de-Souza L, Duarte AJDS, Victor JR. Low doses of IgG from atopic individuals can modulate in vitro IFN- production by human intra-thymic TCD4 and TCD8 cells: an IVIg comparative approach. Hum Vaccin Immunother. 2017;13(7).
14. de Oliveira MG, Oliveira LM, Lira AAL, Sgnotto FDR, Duarte AJDS, Sato MN, et al. Preconception allergen sensitization can induce B10 cells in offspring: a potential main role for maternal IgG. Allerg Asthma Clin Immunol. 2017;13(22):1563-72.
15. Victor JR. Allergen-specific IgG as a mediator of allergy inhibition: lessons from mother to child. Hum Vaccin Immunother. 2017;13:507-13.
16. Noh J, Noh G. Allergen-specific responses of CD19(high) and CD19(low) B cells in non-IgE-mediated food allergy of late eczematous reactions in atopic dermatitis: presence of IL-17- and IL-32-producing regulatory B cells (Br17 & Br32). Inflamm Allerg Drug Targets. 2012;11:320-9.
17. Bermejo DA, Jackson SW, Gorosito-Serran M, Acosta-Rodriguez EV, Amezcua-Vesely MC, Sather BD, et al. Trypanosoma cruzi trans-sialidase initiates a program independent of the transcription factors RORt and Ahr that leads to IL-17 production by activated B cells. Nat. Immunol. 2013;14:514-22.
18. Schlegel PM, Steiert I, Kötter I, Müller CA. B cells contribute to heterogeneity of IL-17 producing cells in rheumatoid arthritis and healthy controls. PLoS ONE. 2013;8:e82580.
19. Pan W, Hao WT, Shen YJ, Li XY, Wang YJ, Sun FF, et al. The excretory-secretory products of Echinococcus granulosus protoscoleces directly regulate the differentiation of B10 B17 and Th17 cells. Parasit Vectors. 2017;10:348.
20. Freer G, Rindi L. Intracellular cytokine detection by fluorescence-activated flow cytometry: basic principles and recent advances. Methods. 2013;61:30-8.
21. Carter NA, Rosser EC, Mauri C. Interleukin-10 produced by B cells is crucial for the suppression of Th17/Th1 responses, induction of T regulatory type 1 cells and reduction of collagen-induced arthritis. Arthritis Res. Ther. 2012;14:R32.
22. Carter NA, Vasconcellos R, Rosser EC, Tulone C, Munoz- ˜Suano A, Kamanaka M, et al. 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. 2011;186: 5569-79.
23. Mavropoulos A, Varna A, Zafiriou E, Liaskos C, Alexiou I, Roussaki-Schulze A, et al. IL-10 producing Bregs are impaired in psoriatic arthritis and psoriasis and inversely correlate with IL-17- and IFN-producing T cells. Clin. Immunol. 2017;184: 33-41.
24. Mavropoulos A, Liaskos C, Simopoulou T, Bogdanos DP, Sakkas LI. IL-10-producing regulatory B cells (B10 cells) IL-17 + T cells and autoantibodies in systemic sclerosis. Clin. Immunol. 2017;184:26-32.
Article Sidebar
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.