Skip to main content
Top
Published in: Inflammation 1/2017

01-02-2017 | ORIGINAL ARTICLE

Immunomodulatory Effects of Adjuvants CPG, MPLA, and BCG on the Derp2-Induced Acute Asthma at Early Life in an Animal Model of BALB/c Mice

Authors: V. Mohammadi-Shahrokhi, A. Rezaei, A. Andalib, A. Rahnama, A. Jafarzadeh, N. Eskandari

Published in: Inflammation | Issue 1/2017

Login to get access

Abstract

The Th1- and Treg cell-related immune responses play key roles in the modulation of Th2 cell-related allergic disorders. The aim was to evaluate the effects of CPG, MPLA, and BCG on the number of Th1-, Th2-, and Treg cell-related parameters in an animal model of asthma. BALB/c mice were divided into five groups and immunized subcutaneously (SC) on days 1, 15, and 22 with allergen Derp2. Three groups of mice were pretreated SC on days 0, 14, and 21 with CPG, CPG + MPLA, or CPG + BCG. All mice were then challenged intranasally with Derp2 on days 28–37. Blood samples were collected from the retro-orbital sinus, on days 0, 23, and 40. The serum levels of IL-4, IFN-γ, IgE, and IgG2a were measured using ELISA technique. The blood number of Th1 and Treg cells was determined using flow cytometry. At the sensitization phase, the number of Th1 and the serum levels of IFN-γ and IgG2a were significantly increased in the Derp2-sensitized group pretreated with CPG plus MPLA, and the number of Treg cells was significantly elevated in Derp2-sensitized mice pretreated with CPG or CPG plus MPLA as compared with that in Derp2-sensitized control mice. At the challenge phase, the number of Th1 was significantly elevated in Derp2-sensitized mice pretreated with CPG plus MPLA, CPG plus BCG, or CPG; the count of Treg cells was significantly increased in Derp2-sensitized mice pretreated with CPG plus BCG group; and the levels of IFN-γ and IgG2a were significantly enhanced in the Derp2-sensitized group pretreated with CPG plus MPLA in comparison with those in Derp2-sensitized control mice. The scores of inflammation and mucus secretion in the lung were significantly decreased in the Derp2-sensitized group pretreated with CPG, BCG, and CPG plus MPLA in comparison with those in the Derp2-sensitized control group. These results showed that BCG, MPLA, and CPG modulate Th1-, Th2-, and Treg-related parameters and ameliorate lung inflammatory parameters in a mouse model of asthma.
Literature
1.
go back to reference Larche, M., C.A. Akdis, and R. Valenta. 2006. Immunological mechanisms of allergen-specific immunotherapy. Nature Reviews. Immunology 6: 761–771.CrossRefPubMed Larche, M., C.A. Akdis, and R. Valenta. 2006. Immunological mechanisms of allergen-specific immunotherapy. Nature Reviews. Immunology 6: 761–771.CrossRefPubMed
2.
go back to reference Zhang, L., L. He, J. Gong, and C. Liu. 2016. Risk factors associated with irreversible airway obstruction in asthma: a systematic review and meta-analysis. BioMed Research International 2016: 9868704.PubMedPubMedCentral Zhang, L., L. He, J. Gong, and C. Liu. 2016. Risk factors associated with irreversible airway obstruction in asthma: a systematic review and meta-analysis. BioMed Research International 2016: 9868704.PubMedPubMedCentral
3.
go back to reference Lee, J.U., J.D. Kim, and C.S. Park. 2015. Gene-environment interactions in asthma: genetic and epigenetic effects. Yonsei Medical Journal 56: 877–886.CrossRefPubMedPubMedCentral Lee, J.U., J.D. Kim, and C.S. Park. 2015. Gene-environment interactions in asthma: genetic and epigenetic effects. Yonsei Medical Journal 56: 877–886.CrossRefPubMedPubMedCentral
4.
go back to reference Wang, X., Q. Yang, P. Wang, et al. 2010. Derp2-mutant gene vaccine inhibits airway inflammation and up-regulates Toll-like receptor 9 in an allergic asthmatic mouse model. Asian Pacific Journal of Allergy and Immunology/Launched by the Allergy and Immunology Society of Thailand 28: 287–293. Wang, X., Q. Yang, P. Wang, et al. 2010. Derp2-mutant gene vaccine inhibits airway inflammation and up-regulates Toll-like receptor 9 in an allergic asthmatic mouse model. Asian Pacific Journal of Allergy and Immunology/Launched by the Allergy and Immunology Society of Thailand 28: 287–293.
5.
go back to reference Genc, S., H. Eroglu, U.C. Kucuksezer, et al. 2012. The decreased CD4+CD25+ FoxP3+ T cells in nonstimulated allergic rhinitis patients sensitized to house dust mites. The Journal of Asthma: Official Journal of the Association for the Care of Asthma 49: 569–574.CrossRef Genc, S., H. Eroglu, U.C. Kucuksezer, et al. 2012. The decreased CD4+CD25+ FoxP3+ T cells in nonstimulated allergic rhinitis patients sensitized to house dust mites. The Journal of Asthma: Official Journal of the Association for the Care of Asthma 49: 569–574.CrossRef
6.
go back to reference Tong P, Wesemann DR. 2015. Molecular mechanisms of IgE class switch recombination. In IgE antibodies: generation and function. Berlin: Springer, pp 21–37. Tong P, Wesemann DR. 2015. Molecular mechanisms of IgE class switch recombination. In IgE antibodies: generation and function. Berlin: Springer, pp 21–37.
7.
go back to reference Bienvenu, J., C. Doche, M.C. Gutowski, et al. 1995. Production of proinflammatory cytokines and cytokines involved in the TH1/TH2 balance is modulated by pentoxifylline. Journal of Cardiovascular Pharmacology 25: S80–S84.CrossRefPubMed Bienvenu, J., C. Doche, M.C. Gutowski, et al. 1995. Production of proinflammatory cytokines and cytokines involved in the TH1/TH2 balance is modulated by pentoxifylline. Journal of Cardiovascular Pharmacology 25: S80–S84.CrossRefPubMed
8.
go back to reference Bisseye, C., M. van der Sande, W.D. Morgan, et al. 2009. Plasmodium falciparum infection of the placenta impacts on the T helper type 1 (Th1)/Th2 balance of neonatal T cells through CD4(+)CD25(+) forkhead box P3(+) regulatory T cells and interleukin-10. Clinical and Experimental Immunology 158: 287–293.CrossRefPubMedPubMedCentral Bisseye, C., M. van der Sande, W.D. Morgan, et al. 2009. Plasmodium falciparum infection of the placenta impacts on the T helper type 1 (Th1)/Th2 balance of neonatal T cells through CD4(+)CD25(+) forkhead box P3(+) regulatory T cells and interleukin-10. Clinical and Experimental Immunology 158: 287–293.CrossRefPubMedPubMedCentral
9.
go back to reference Shahrakyvahed, A., J. Sanchooli, N. Sanadgol, M.K. Arababadi, and D. Kennedy. 2014. TLR9: an important molecule in the fight against hepatitis B virus. Postgraduate Medical Journal 90: 396–401.CrossRefPubMed Shahrakyvahed, A., J. Sanchooli, N. Sanadgol, M.K. Arababadi, and D. Kennedy. 2014. TLR9: an important molecule in the fight against hepatitis B virus. Postgraduate Medical Journal 90: 396–401.CrossRefPubMed
10.
go back to reference Kim, D.-H., J.-H. Sohn, H.-J. Park, et al. 2016. CpG oligodeoxynucleotide inhibits cockroach-induced asthma via induction of IFN-γ+ Th1 cells or Foxp3+ regulatory T cells in the lung. Allergy, Asthma & Immunology Research 8: 264–275.CrossRef Kim, D.-H., J.-H. Sohn, H.-J. Park, et al. 2016. CpG oligodeoxynucleotide inhibits cockroach-induced asthma via induction of IFN-γ+ Th1 cells or Foxp3+ regulatory T cells in the lung. Allergy, Asthma & Immunology Research 8: 264–275.CrossRef
11.
go back to reference Santeliz, J.V., G. Van Nest, P. Traquina, E. Larsen, and M. Wills-Karp. 2002. Amb a 1-linked CpG oligodeoxynucleotides reverse established airway hyperresponsiveness in a murine model of asthma. Journal of Allergy and Clinical Immunology 109: 455–462.CrossRefPubMed Santeliz, J.V., G. Van Nest, P. Traquina, E. Larsen, and M. Wills-Karp. 2002. Amb a 1-linked CpG oligodeoxynucleotides reverse established airway hyperresponsiveness in a murine model of asthma. Journal of Allergy and Clinical Immunology 109: 455–462.CrossRefPubMed
12.
go back to reference Dubensky, T.W., and S.G. Reed. 2010. Adjuvants for cancer vaccines. Seminars in Immunology. 22(3): 155–161.CrossRefPubMed Dubensky, T.W., and S.G. Reed. 2010. Adjuvants for cancer vaccines. Seminars in Immunology. 22(3): 155–161.CrossRefPubMed
13.
go back to reference Joshi, J., and S. Kaur. 2014. To investigate the therapeutic potential of immunochemotherapy with cisplatin + 78 kDa + MPL-A against Leishmania donovani in BALB/c mice. Parasite Immunology 36: 3–12.CrossRefPubMed Joshi, J., and S. Kaur. 2014. To investigate the therapeutic potential of immunochemotherapy with cisplatin + 78 kDa + MPL-A against Leishmania donovani in BALB/c mice. Parasite Immunology 36: 3–12.CrossRefPubMed
14.
go back to reference Habibi, M., M.R. Asadi Karam, and S. Bouzari. 2015. Evaluation of the effect of MPL and delivery route on immunogenicity and protectivity of different formulations of FimH and MrpH from uropathogenic Escherichia coli and Proteus mirabilis in a UTI mouse model. International Immunopharmacology 28: 70–78.CrossRefPubMed Habibi, M., M.R. Asadi Karam, and S. Bouzari. 2015. Evaluation of the effect of MPL and delivery route on immunogenicity and protectivity of different formulations of FimH and MrpH from uropathogenic Escherichia coli and Proteus mirabilis in a UTI mouse model. International Immunopharmacology 28: 70–78.CrossRefPubMed
15.
go back to reference Heldwein, K.A., M.D. Liang, T.K. Andresen, et al. 2003. TLR2 and TLR4 serve distinct roles in the host immune response against Mycobacterium bovis BCG. Journal of Leukocyte Biology 74: 277–286.CrossRefPubMed Heldwein, K.A., M.D. Liang, T.K. Andresen, et al. 2003. TLR2 and TLR4 serve distinct roles in the host immune response against Mycobacterium bovis BCG. Journal of Leukocyte Biology 74: 277–286.CrossRefPubMed
16.
go back to reference Akkoc, T., M. Aydogan, A. Yildiz, et al. 2010. Neonatal BCG vaccination induces IL-10 production by CD4+ CD25+ T cells. Pediatric Allergy and Immunology 21: 1059–1063.CrossRefPubMed Akkoc, T., M. Aydogan, A. Yildiz, et al. 2010. Neonatal BCG vaccination induces IL-10 production by CD4+ CD25+ T cells. Pediatric Allergy and Immunology 21: 1059–1063.CrossRefPubMed
17.
go back to reference Boer, M.C., C. Prins, K.E. van Meijgaarden, et al. 2015. Mycobacterium bovis BCG vaccination induces divergent proinflammatory or regulatory T cell responses in adults. Clinical and Vaccine Immunology: CVI 22: 778–788.CrossRefPubMedPubMedCentral Boer, M.C., C. Prins, K.E. van Meijgaarden, et al. 2015. Mycobacterium bovis BCG vaccination induces divergent proinflammatory or regulatory T cell responses in adults. Clinical and Vaccine Immunology: CVI 22: 778–788.CrossRefPubMedPubMedCentral
18.
go back to reference Verwaerde, C., A.S. Debrie, C. Dombu, et al. 2014. HBHA vaccination may require both Th1 and Th17 immune responses to protect mice against tuberculosis. Vaccine 32: 6240–6250.CrossRefPubMed Verwaerde, C., A.S. Debrie, C. Dombu, et al. 2014. HBHA vaccination may require both Th1 and Th17 immune responses to protect mice against tuberculosis. Vaccine 32: 6240–6250.CrossRefPubMed
19.
go back to reference Gu, D., W. Chen, Y. Mi, et al. 2016. The Mycobacterium bovis BCG prime-Rv0577 DNA boost vaccination induces a durable Th1 immune response in mice. Acta Biochimica et Biophysica Sinica 48: 385–390.CrossRefPubMed Gu, D., W. Chen, Y. Mi, et al. 2016. The Mycobacterium bovis BCG prime-Rv0577 DNA boost vaccination induces a durable Th1 immune response in mice. Acta Biochimica et Biophysica Sinica 48: 385–390.CrossRefPubMed
20.
go back to reference Ballester, M., L. Jeanbart, A. de Titta, et al. 2015. Nanoparticle conjugation enhances the immunomodulatory effects of intranasally delivered CpG in house dust mite-allergic mice. Scientific Reports 5: 14274.CrossRefPubMedPubMedCentral Ballester, M., L. Jeanbart, A. de Titta, et al. 2015. Nanoparticle conjugation enhances the immunomodulatory effects of intranasally delivered CpG in house dust mite-allergic mice. Scientific Reports 5: 14274.CrossRefPubMedPubMedCentral
21.
go back to reference Ou, J., W. Shi, Y. Xu, and Z. Tao. 2014. Intranasal immunization with DNA vaccine coexpressing Der p 1 and ubiquitin in an allergic rhinitis mouse model. Annals of Allergy, Asthma & Immunology: Official Publication of the American College of Allergy, Asthma, & Immunology 113: 658–665. e651.CrossRef Ou, J., W. Shi, Y. Xu, and Z. Tao. 2014. Intranasal immunization with DNA vaccine coexpressing Der p 1 and ubiquitin in an allergic rhinitis mouse model. Annals of Allergy, Asthma & Immunology: Official Publication of the American College of Allergy, Asthma, & Immunology 113: 658–665. e651.CrossRef
22.
go back to reference Lagranderie, M., M.A. Nahori, A.M. Balazuc, et al. 2003. Dendritic cells recruited to the lung shortly after intranasal delivery of Mycobacterium bovis BCG drive the primary immune response towards a type 1 cytokine production. Immunology 108: 352–364.CrossRefPubMedPubMedCentral Lagranderie, M., M.A. Nahori, A.M. Balazuc, et al. 2003. Dendritic cells recruited to the lung shortly after intranasal delivery of Mycobacterium bovis BCG drive the primary immune response towards a type 1 cytokine production. Immunology 108: 352–364.CrossRefPubMedPubMedCentral
23.
24.
go back to reference Li, H.-B., J.-Y. Zhang, Y.-F. He, et al. 2012. Systemic immunization with an epitope-based vaccine elicits a Th1-biased response and provides protection against Helicobacter pylori in mice. Vaccine 31: 120–126.CrossRefPubMed Li, H.-B., J.-Y. Zhang, Y.-F. He, et al. 2012. Systemic immunization with an epitope-based vaccine elicits a Th1-biased response and provides protection against Helicobacter pylori in mice. Vaccine 31: 120–126.CrossRefPubMed
25.
go back to reference Ito, T., T. Takii, M. Maruyama, et al. 2010. Effectiveness of BCG vaccination to aged mice. Immunity & Ageing 7: 1.CrossRef Ito, T., T. Takii, M. Maruyama, et al. 2010. Effectiveness of BCG vaccination to aged mice. Immunity & Ageing 7: 1.CrossRef
26.
go back to reference Fernández, I., A. Peña, N. Del Teso, V. Pérez, and J. Rodríguez-Cuesta. 2010. Clinical biochemistry parameters in C57BL/6J mice after blood collection from the submandibular vein and retroorbital plexus. Journal of the American Association for Laboratory Animal Science 49: 202–206.PubMedPubMedCentral Fernández, I., A. Peña, N. Del Teso, V. Pérez, and J. Rodríguez-Cuesta. 2010. Clinical biochemistry parameters in C57BL/6J mice after blood collection from the submandibular vein and retroorbital plexus. Journal of the American Association for Laboratory Animal Science 49: 202–206.PubMedPubMedCentral
27.
go back to reference Duechs, M.J., J.E. Brunt, F. Gantner, and K.J. Erb. 2012. Adjuvant effects of different TLR agonists on the induction of allergen-specific Th2 responses. Open Journal of Immunology 2: 17.CrossRef Duechs, M.J., J.E. Brunt, F. Gantner, and K.J. Erb. 2012. Adjuvant effects of different TLR agonists on the induction of allergen-specific Th2 responses. Open Journal of Immunology 2: 17.CrossRef
28.
go back to reference Mackenzie, K.J., D.J. Nowakowska, M.D. Leech, et al. 2014. Effector and central memory T helper 2 cells respond differently to peptide immunotherapy. Proceedings of the National Academy of Sciences 111: E784–E793.CrossRef Mackenzie, K.J., D.J. Nowakowska, M.D. Leech, et al. 2014. Effector and central memory T helper 2 cells respond differently to peptide immunotherapy. Proceedings of the National Academy of Sciences 111: E784–E793.CrossRef
29.
go back to reference Düchs M, der Promotionskommission M. 2011. Effects of Toll-like receptor agonists on the pathogenesis of atopic asthma in mice. Universitätsbibliothek der Universität Würzburg. Düchs M, der Promotionskommission M. 2011. Effects of Toll-like receptor agonists on the pathogenesis of atopic asthma in mice. Universitätsbibliothek der Universität Würzburg.
30.
go back to reference Coleman, M.M., J. Keane, and K.H. Mills. 2010. Editorial: Tregs and BCG—dangerous liaisons in TB. Journal of Leukocyte Biology 88: 1067–1069.CrossRefPubMed Coleman, M.M., J. Keane, and K.H. Mills. 2010. Editorial: Tregs and BCG—dangerous liaisons in TB. Journal of Leukocyte Biology 88: 1067–1069.CrossRefPubMed
32.
go back to reference Soleimani, M., and J. Rafinejad. 2008. House dust mite contamination in hotels and inns in Bandar Abbas, south of Iran. Journal of Environmental Health Science & Engineering 5: 207–210. Soleimani, M., and J. Rafinejad. 2008. House dust mite contamination in hotels and inns in Bandar Abbas, south of Iran. Journal of Environmental Health Science & Engineering 5: 207–210.
33.
go back to reference Kleinnijenhuis, J., J. Quintin, F. Preijers, et al. 2013. Long-lasting effects of BCG vaccination on both heterologous Th1/Th17 responses and innate trained immunity. Journal of Innate Immunity 6: 152–158.CrossRefPubMedPubMedCentral Kleinnijenhuis, J., J. Quintin, F. Preijers, et al. 2013. Long-lasting effects of BCG vaccination on both heterologous Th1/Th17 responses and innate trained immunity. Journal of Innate Immunity 6: 152–158.CrossRefPubMedPubMedCentral
34.
go back to reference Thomas, W.R., B.J. Hales, and W.-A. Smith. 2010. House dust mite allergens in asthma and allergy. Trends in Molecular Medicine 16: 321–328.CrossRefPubMed Thomas, W.R., B.J. Hales, and W.-A. Smith. 2010. House dust mite allergens in asthma and allergy. Trends in Molecular Medicine 16: 321–328.CrossRefPubMed
35.
go back to reference Moingeon, P., T. Batard, R. Fadel, et al. 2006. Immune mechanisms of allergen-specific sublingual immunotherapy. Allergy 61: 151–165.CrossRefPubMed Moingeon, P., T. Batard, R. Fadel, et al. 2006. Immune mechanisms of allergen-specific sublingual immunotherapy. Allergy 61: 151–165.CrossRefPubMed
36.
go back to reference Tversky, J.R., A.P. Bieneman, K.L. Chichester, R.G. Hamilton, and J.T. Schroeder. 2010. Subcutaneous allergen immunotherapy restores human dendritic cell innate immune function. Clinical & Experimental Allergy 40: 94–102. Tversky, J.R., A.P. Bieneman, K.L. Chichester, R.G. Hamilton, and J.T. Schroeder. 2010. Subcutaneous allergen immunotherapy restores human dendritic cell innate immune function. Clinical & Experimental Allergy 40: 94–102.
37.
go back to reference Peat, J.K., E. Tovey, B.G. Toelle, et al. 1996. House dust mite allergens. A major risk factor for childhood asthma in Australia. American Journal of Respiratory and Critical Care Medicine 153: 141–146.CrossRefPubMed Peat, J.K., E. Tovey, B.G. Toelle, et al. 1996. House dust mite allergens. A major risk factor for childhood asthma in Australia. American Journal of Respiratory and Critical Care Medicine 153: 141–146.CrossRefPubMed
38.
go back to reference Ballester M, Jeanbart L, De Titta A et al. 2015. Nanoparticle conjugation enhances the immunomodulatory effects of intranasally delivered CpG in house dust mite-allergic mice. Scientific Reports 5. Ballester M, Jeanbart L, De Titta A et al. 2015. Nanoparticle conjugation enhances the immunomodulatory effects of intranasally delivered CpG in house dust mite-allergic mice. Scientific Reports 5.
39.
go back to reference VanCott, J.L., A.E. Prada, M.M. McNeal, et al. 2006. Mice develop effective but delayed protective immune responses when immunized as neonates either intranasally with nonliving VP6/LT (R192G) or orally with live rhesus rotavirus vaccine candidates. Journal of Virology 80: 4949–4961.CrossRefPubMedPubMedCentral VanCott, J.L., A.E. Prada, M.M. McNeal, et al. 2006. Mice develop effective but delayed protective immune responses when immunized as neonates either intranasally with nonliving VP6/LT (R192G) or orally with live rhesus rotavirus vaccine candidates. Journal of Virology 80: 4949–4961.CrossRefPubMedPubMedCentral
40.
go back to reference Abbas AK, Lichtman AH, Pillai S. 2011. Cellular and molecular immunology. Elsevier Health Sciences. Abbas AK, Lichtman AH, Pillai S. 2011. Cellular and molecular immunology. Elsevier Health Sciences.
41.
go back to reference Gong, P., Y. Li, Y.P. Tan, and H. Li. 2016. Pretreatment with inactivated Bacillus Calmette-Guerin increases CD4+CD25+ regulatory T cell function and decreases functional and structural effects of asthma induction in a rat asthma model. Artificial Organs 40: 360–367.CrossRefPubMed Gong, P., Y. Li, Y.P. Tan, and H. Li. 2016. Pretreatment with inactivated Bacillus Calmette-Guerin increases CD4+CD25+ regulatory T cell function and decreases functional and structural effects of asthma induction in a rat asthma model. Artificial Organs 40: 360–367.CrossRefPubMed
42.
go back to reference Kaveh, D.A., M. Carmen Garcia-Pelayo, and P.J. Hogarth. 2014. Persistent BCG bacilli perpetuate CD4 T effector memory and optimal protection against tuberculosis. Vaccine 32: 6911–6918.CrossRefPubMed Kaveh, D.A., M. Carmen Garcia-Pelayo, and P.J. Hogarth. 2014. Persistent BCG bacilli perpetuate CD4 T effector memory and optimal protection against tuberculosis. Vaccine 32: 6911–6918.CrossRefPubMed
43.
go back to reference Shi, Y., M.A. Felder, P.M. Sondel, and A.L. Rakhmilevich. 2015. Synergy of anti-CD40, CpG and MPL in activation of mouse macrophages. Molecular Immunology 66: 208–215.CrossRefPubMedPubMedCentral Shi, Y., M.A. Felder, P.M. Sondel, and A.L. Rakhmilevich. 2015. Synergy of anti-CD40, CpG and MPL in activation of mouse macrophages. Molecular Immunology 66: 208–215.CrossRefPubMedPubMedCentral
44.
go back to reference Gouveia, A.C., A.S. Brugiolo, C.C. Alves, et al. 2013. Th2 responses in OVA-sensitized BALB/c mice are down-modulated by Mycobacterium bovis BCG treatment. Journal of Clinical Immunology 33: 235–245.CrossRefPubMed Gouveia, A.C., A.S. Brugiolo, C.C. Alves, et al. 2013. Th2 responses in OVA-sensitized BALB/c mice are down-modulated by Mycobacterium bovis BCG treatment. Journal of Clinical Immunology 33: 235–245.CrossRefPubMed
45.
go back to reference Noack, M., and P. Miossec. 2014. Th17 and regulatory T cell balance in autoimmune and inflammatory diseases. Autoimmunity Reviews 13: 668–677.CrossRefPubMed Noack, M., and P. Miossec. 2014. Th17 and regulatory T cell balance in autoimmune and inflammatory diseases. Autoimmunity Reviews 13: 668–677.CrossRefPubMed
47.
go back to reference Xu, P., X. Zhang, X. Wang, et al. 2014. Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nature Genetics 46: 1212–1219.CrossRefPubMed Xu, P., X. Zhang, X. Wang, et al. 2014. Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nature Genetics 46: 1212–1219.CrossRefPubMed
48.
go back to reference Sallusto, F., and A. Lanzavecchia. 2000. Understanding dendritic cell and T-lymphocyte traffic through the analysis of chemokine receptor expression. Immunological Reviews 177: 134–140.CrossRefPubMed Sallusto, F., and A. Lanzavecchia. 2000. Understanding dendritic cell and T-lymphocyte traffic through the analysis of chemokine receptor expression. Immunological Reviews 177: 134–140.CrossRefPubMed
49.
go back to reference Salehi S. 2013. The role of Syk in airway hyperresponsiveness and remodeling in house dust mite induced murine models of allergic airways inflammation. Toronto University. Salehi S. 2013. The role of Syk in airway hyperresponsiveness and remodeling in house dust mite induced murine models of allergic airways inflammation. Toronto University.
50.
go back to reference Tao, K., M. Fujii, Tsukumo S-i, et al. 2007. Genetic variations of Toll-like receptor 9 predispose to systemic lupus erythematosus in Japanese population. Annals of the Rheumatic Diseases 66: 905–909.CrossRefPubMedPubMedCentral Tao, K., M. Fujii, Tsukumo S-i, et al. 2007. Genetic variations of Toll-like receptor 9 predispose to systemic lupus erythematosus in Japanese population. Annals of the Rheumatic Diseases 66: 905–909.CrossRefPubMedPubMedCentral
51.
go back to reference Boer MC, Joosten SA, Ottenhoff TH. 2015. Regulatory T-cells at the interface between human host and pathogens in infectious diseases and vaccination. Frontiers in Immunology 6. Boer MC, Joosten SA, Ottenhoff TH. 2015. Regulatory T-cells at the interface between human host and pathogens in infectious diseases and vaccination. Frontiers in Immunology 6.
Metadata
Title
Immunomodulatory Effects of Adjuvants CPG, MPLA, and BCG on the Derp2-Induced Acute Asthma at Early Life in an Animal Model of BALB/c Mice
Authors
V. Mohammadi-Shahrokhi
A. Rezaei
A. Andalib
A. Rahnama
A. Jafarzadeh
N. Eskandari
Publication date
01-02-2017
Publisher
Springer US
Published in
Inflammation / Issue 1/2017
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-016-0476-2

Other articles of this Issue 1/2017

Inflammation 1/2017 Go to the issue