دورية أكاديمية
أعرض في EDS

Anaphylaxis induced by Thalassophryne nattereri venom in mice is an IgE/IgG1-mediated, IL-4-dependent phenomenon.

التفاصيل البيبلوغرافية
العنوان: Anaphylaxis induced by Thalassophryne nattereri venom in mice is an IgE/IgG1-mediated, IL-4-dependent phenomenon.
المؤلفون: Bruni FM; Immunoregulation Unit, Special Laboratory of Applied Toxinology, Butantan Institute, São Paulo, Brazil., Coutinho EMM; Immunoregulation Unit, Special Laboratory of Applied Toxinology, Butantan Institute, São Paulo, Brazil., Andrade-Barros AI; Immunoregulation Unit, Special Laboratory of Applied Toxinology, Butantan Institute, São Paulo, Brazil., Grund LZ; Immunoregulation Unit, Special Laboratory of Applied Toxinology, Butantan Institute, São Paulo, Brazil., Lopes-Ferreira M; Immunoregulation Unit, Special Laboratory of Applied Toxinology, Butantan Institute, São Paulo, Brazil., Lima C; Immunoregulation Unit, Special Laboratory of Applied Toxinology, Butantan Institute, São Paulo, Brazil. carla.lima@butantan.gov.br.
المصدر: Scientific reports [Sci Rep] 2020 Jan 17; Vol. 10 (1), pp. 584. Date of Electronic Publication: 2020 Jan 17.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101563288 Publication Model: Electronic Cited Medium: Internet ISSN: 2045-2322 (Electronic) Linking ISSN: 20452322 NLM ISO Abbreviation: Sci Rep Subsets: MEDLINE
أسماء مطبوعة: Original Publication: London : Nature Publishing Group, copyright 2011-
مواضيع طبية MeSH: Anaphylaxis/*immunology , Batrachoidiformes/*metabolism , Fish Venoms/*adverse effects , Interleukin-4/*genetics , Interleukin-4/*metabolism, Administration, Cutaneous ; Administration, Oral ; Anaphylaxis/chemically induced ; Animals ; Disease Models, Animal ; Female ; Fish Venoms/immunology ; Gene Knockout Techniques ; Humans ; Immunoglobulin E/immunology ; Immunoglobulin G/immunology ; Injections, Intraperitoneal ; Interferon-gamma/metabolism ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Rats
مستخلص: We hypothesized that beyond the Thalassophryne nattereri venoms ability to induce in mice a strong specific-Th2 response with high levels of specific IgE/IgG1, it would be able to trigger anaphylaxis in sensitized individuals. To investigate whether the venom is capable of inducing an allergic reaction in mice and characterize soluble and cellular mediators involved in this process, BALB/c female mice were sensitized intraperitoneally with decreasing-dose of venom at weekly intervals for 4 weeks and challenged by intraperitoneal, oral or epicutaneous routes with venom 2 weeks later. Our data show that sensitized-mice challenged by all routes showed intense symptoms of anaphylaxis, dependent on the anaphylactic IgG1 and IgE antibodies and mast cells. The late-phase reaction developed after initial symptoms was characterized by the influx of eosinophils, dependent on IL-5, IL-17A and eotaxin produced by Th2 cells in inflamed lungs and skin draining lymph-nodes. Using C57BL/6 deficient mice we demonstrated that IL-4 KO mice failed to develop anaphylactic symptoms or local Th2 inflammation, producing low levels of IgG1 and increased levels of IgG2a. Together our results demonstrated that the venom of T. nattereri has allergenic proteins that can trigger an allergic process, a phenomenon IgE-IgG1 dependent, IL-4-mediated and negatively regulated by IFN-γ.
References: Portier, F. & Richet, C. Action anaphylachque dês quelques venins. CR. Soc. Biol. 54, 170–172 (1902).
Ziegman, R. & Alewood, P. Bioactive components in fish venoms. Toxins (Basel). 30(7(5)), 1497–1531 (2015). (PMID: 10.3390/toxins7051497)
Haddad, V. Jr., Lupi, O., Lonza, J. P. & Tyring, S. K. Tropical dermatology: marine and aquatic dermatology. J. Am. Acad. Dermatol. 61(5), 733–750; quiz 751–752 (2009).
Almeida, V. G. & Rocha, C. M. Registros de acidentes com peixes peçonhentos e/ou venenosos. Rev. Soc. Bras. Toxicol. 7, 26–30 (1989).
Auto, H.F. Acidentes por peixes peçonhentos Thalassophryne (Niquim), considerações em torno de 32 casos. Revista da Escola de Ciências Médicas de Alagoas. 34–40 (1992).
Facó, P. E. et al. Epidemiologia dos acidentes por Thalassophryne nattereri (niquim) no Estado do Ceará (1992–2002). Revista da Sociedade Brasileira de Medicina Tropical. 38(6), 479–482 (2005). (PMID: 10.1590/S0037-8682200500060000616410922)
Haddad, V. Jr., Pardal, P. P. O., Cardoso, J. L. & Martins, I. A. The venomous toadfish Thalassophryne nattereri (niquim or miquim): Repor of 43 injuries provoked in fishermen of Salinópolis (Pará State) and Aracaju (Serjipe State). Rev. Inst. Med. Trop. 4, 221–223 (2003). (PMID: 10.1590/S0036-46652003000400009)
Lopes-Ferreira, M., Grund, L. Z. & Lima, C. Thalassophryne nattereri fish venom: from the envenoming to the understanding of the immune system. J. Venom Anim. Toxins Incl. Trop. Dis. 13(20), 35 (2014). (PMID: 10.1186/1678-9199-20-35)
Fonseca, L. A. & Lopes-Ferreira, M. Clinical and experimental studies regarding poisoning caused by a fish T. nattereri (niquim). Ann. Bras. Dermatol. 75, 435–443 (2000).
Piran-Soares, A. A. et al. Neutralizing antibodies obtained in a persistent immune response are effective against deleterious effects induced by the Thalassophryne nattereri fish venom. Toxicon. 49, 920–930 (2007). (PMID: 10.1016/j.toxicon.2007.01.00117391720)
Lopes-Ferreira, M. et al. Hemostatic effects induced by T. nattereri fish venom: a model of endothelium-mediated blood flow impairement. Toxicon. 40, 1141–1147 (2002). (PMID: 10.1016/S0041-0101(02)00114-912165317)
Lopes-Ferreira, M. et al. Skeletal muscle necrosis and regeneration after injection of Thalassophryne nattereri (niquim) fish venom in mice. Int. J. Exp. Pathol. 82, 55–64 (2001). (PMID: 10.1046/j.1365-2613.2001.00181.x114225412517697)
Lima, C. et al. Characterization of local inflammatory response induced by Thalassophryne nattereri fish venom in a mouse model of tissue injury. Toxicon. 42, 499–507 (2003). (PMID: 10.1016/S0041-0101(03)00228-914529731)
Grund, L. Z., Souza, V. M. O., Faquim-Mauro, E. L., Lima, C. & Lopes-Ferreira, M. Experimental immunization with Thalassophryne nattereri fish venom: striking IL-5 production and impaired of B220+ cells. Toxicon. 48(5), 499–508 (2006). (PMID: 10.1016/j.toxicon.2006.06.01416930659)
Grund, L. Z., Komegae, E. N., Lopes-Ferreira, M. & Lima, C. IL-5 and IL-17A are critical for the chronic IgE response and differentiation of long-lived antibody-secreting cells in inflamed tissues. Cytokine. 59(2), 335–351 (2012). (PMID: 10.1016/j.cyto.2012.04.04522633287)
Grund, L. Z., Lopes-Ferreira, M. & Lima, C. The hierarchical process of differentiation of long-lived antibody-secreting cells is dependent on integrated signals derived from antigen and IL-17A. PLoS One. 18(8(9)), e74566 (2013). (PMID: 10.1371/journal.pone.0074566)
Lopes-Ferreira, M. et al. Kininogenase activity of Thalassophryne nattereri fish venom. Biochem. Pharmacol. 68, 2151–2157 (2004). (PMID: 10.1016/j.bcp.2004.07.03715498505)
Magalhães, G. S. et al. Natterins, a new class of protein with kininogenase activity characterized from Thalassophryne nattereri fish venom. Biochimie. 87, 687–699 (2005). (PMID: 10.1016/j.biochi.2005.03.01616054523)
Komegae, E. N., Grund, L. Z., Lopes-Ferreira, M. & Lima, C. The longevity of th2 humoral response induced by proteases natterins requires the participation of long-lasting innate-like B cells and plasma cells in spleen. PLoS One. 28(8(6)), 67135 (2013). (PMID: 10.1371/journal.pone.0067135)
Kweon, M. N., Yamamoto, M., Kajiki, M., Takahashi, I. & Kiyono, H. Systemically derived large intestinal CD4(+) Th2 cells play a central role in STAT6-mediated allergic diarrhea. J. Clin. Invest. 106, 199–206 (2000). (PMID: 10.1172/JCI849010903335314304)
Balbino, B. et al. Pathways of immediate hypothermia and leukocyte infiltration in an adjuvant-free mouse model of anaphylaxis. J. Allergy Clin. Immunol. 139(2), 584–596 (2017). (PMID: 10.1016/j.jaci.2016.05.04727555460)
Li, X. M., Schofield, B. H., Huang, C. K., Kleiner, G. I. & Sampson, H. A. A murine model of IgE-mediated cow’s milk hypersensitivity. J. Allergy Clin. Immunol. 103, 206–214 (1999). (PMID: 10.1016/S0091-6749(99)70492-69949309)
Capobianco, F. et al. Oral sensitization with shrimp tropomyosin induces in mice allergen-specific IgE, T cell response and systemic anaphylactic reactions. Int. Immunol. 20(8), 1077–1086 (2008). (PMID: 10.1093/intimm/dxn06518562336)
Hsieh, K. Y., Tsai, C. C., Wu, C. H. & Lin, R. H. Epicutaneous exposure to protein antigen and food allergy. Clin. Exp. Allergy. 33, 1067–1075 (2003). (PMID: 10.1046/j.1365-2222.2003.01724.x12911780)
Arizmendi, N. G. et al. Mucosal exposure to cockroach extract induces allergic sensitization and allergic airway inflammation. Allergy Asthma Clin. Immunol. 14(7(1)), 22–32 (2011). (PMID: 10.1186/1710-1492-7-22)
Leung, P. S. et al. Induction of shrimp tropomyosin-specific hypersensitivity in mice. Int. Arch. Allergy Immunol. 147(4), 305–314 (2008). (PMID: 10.1159/00014403818617750)
Li, X. M. et al. A murine model of peanut anaphylaxis: T- and B-cell responses to a major peanut allergen mimic human responses. J. Allergy Clin. Immunol. 106(1 Pt 1), 150–158 (2000). (PMID: 10.1067/mai.2000.10739510887318)
Gilfillan, A. M. & Tkaczyk, C. Integrated signalling pathways for mast-cell activation. Nature Rev. Immunol. 6, 218–230 (2006). (PMID: 10.1038/nri1782)
Arias, K. et al. Concurrent blockade of platelet-activating factor and histamine prevents life-threatening peanut-induced anaphylactic reactions. J. Allergy Clin. Immunol. 124(2), 307–314 (2009). (PMID: 10.1016/j.jaci.2009.03.01219409603)
Harada, M. et al. Age-dependent difference in susceptibility to IgE antibody- and IgG1 antibody-mediated passive anaphylactic shock in the mouse. Immunol. Invest. 5-6, 515–523 (1991). (PMID: 10.3109/08820139109082632)
Miyajima, I. et al. Systemic anaphylaxis in the mouse can be mediated largely through IgG1 and FcγRIII. J. Clin. Invest. 99, 901–914 (1997). (PMID: 10.1172/JCI1192559062348507898)
Finkelman, F. D. Anaphylaxis: lessons from mouse models. J. Allergy Clin. Immunol. 3, 506–515 (2007). (PMID: 10.1016/j.jaci.2007.07.033)
Kikuchi, Y. et al. Crucial commitment of proteolytic activity of a purified recombinant major house dust mite allergen Der p1 to sensitization toward IgE and IgG responses. J. Immunol. 177, 1609–1617 (2006). (PMID: 10.4049/jimmunol.177.3.160916849469)
Gough, L., Schulz, O., Sewell, H. F. & Shakib, F. The cysteine protease activity of the major dust mite allergen Der p 1 selectively enhances the immunoglobulin E antibody response. J. Exp. Med. 190, 1897–1902 (1999). (PMID: 10.1084/jem.190.12.1897106013642195724)
Kauffman, H. F., Tomee, J. F., van de Riet, M. A., Timmerman, A. J. & Borger, P. Protease-dependent activation of epithelial cells by fungal allergens leads to morphologic changes and cytokine production. J. Allergy Clin. Immunol. 105, 1185–1193 (2000). (PMID: 10.1067/mai.2000.10621010856154)
Gough, L., Campbell, E., Bayley, D., Van Heeke, G. & Shakib, F. Proteolytic activity of the house dust mite allergen Der p 1 enhances allergenicity in a mouse inhalation model. Clin. Exp. Allergy. 33, 1159–1163 (2003). (PMID: 10.1046/j.1365-2222.2003.01716.x12911793)
Lewkowich, I. P. et al. Protease-activated receptor 2 activation of myeloid dendritic cells regulates allergic airway inflammation. Respir. Res. 21, 12–22 (2011).
Chen, J. C. et al. The protease allergen Pen c 13 induces allergic airway inflammation and changes in epithelial barrier integrity and function in a murine model. J. Biol. Chem. 286(30), 26667–26679 (2011). (PMID: 10.1074/jbc.M110.193987216132163143630)
Galli, S. J., Tsai, M. & Piliponsky, A. M. The development of allergic inflammation. Nature. 24(454(7203)), 445–454 (2008). (PMID: 10.1038/nature07204)
Meijer, M., Rijkers, G. T. & van Overveld, F. J. Neutrophils and emerging targets for treatment in chronic obstructive pulmonary disease. Exp. Rev. Clin. Immunol. 9, 1055–1068 (2013). (PMID: 10.1586/1744666X.2013.851347)
Allinne, J. et al. IL-33 blockade affects mediators of persistence and exacerbation in a model of chronic airway inflammation. J. Allergy Clin. Immunol. 25, pii: S0091-6749(19)31243-6 (2019).
Mould, A. W., Matthaei, K. I., Young, I. G. & Foster, P. S. Relationship between interleukin-5 and eotaxin in regulating blood and tissue eosinophilia in mice. J. Clin. Invest. 99, 1064–1071 (1997). (PMID: 10.1172/JCI1192349062365507915)
Sergejeva, S., Ivanov, S., Lotvall, J. & Linden, A. Interleukin-17 as a recruitment and survival factor for airway macrophages in allergic airway inflammation. Am. J. Respir. Cell Mol. Biol. 33(3), 248–253 (2005). (PMID: 10.1165/rcmb.2004-0213OC15901616)
Wang, Y. H. et al. A novel subset of CD4(+) T(H)2 memory/effector cells that produce inflammatory IL-17 cytokine and promote the exacerbation of chronic allergic asthma. J. Exp. Med. 25(207(11)), 2479–2491 (2010). (PMID: 10.1084/jem.20101376)
Palframan, R. T., Collins, P. D., Willhians, T. J. & Rankin, S. M. Eotaxin induces a rapid release of eosinophils and their progenitors from the bone marrow. Blood. 91, 2240–2248 (1998). (PMID: 10.1182/blood.V91.7.22409516121)
Nieuwenhuizen, N., Herbert, D. R., Brombacher, F. & Lopata, A. L. Differential requirements for interleukin (IL)-4 and IL-13 in protein contact dermatitis induced by Anisakis. Allergy. 64(9), 1309–1318 (2009). (PMID: 10.1111/j.1398-9995.2009.02002.x19254288)
Sicherer, S. H. & Leung, D. Y. 2011. Advances in allergic skin disease, anaphylaxis, and hypersensitivity reactions to foods, drugs, and insects. J. Allergy Clin. Immunol. 127(2), 326–335 (2010). (PMID: 10.1016/j.jaci.2010.11.02421190728)
Bonadonna, P., Zanotti, R. & Müller, U. Mastocytosis and insect venom allergy. Curr. Opin. Allergy Clin. Immunol. 10(4), 347–353 (2010). (PMID: 10.1097/ACI.0b013e32833b280c20485157)
Gupta, K. & Harvima, I. T. Mast cell-neural interactions contribute to pain and itch. Immunol. Rev. 282(1), 168–187 (2018). (PMID: 10.1111/imr.12622294312165812374)
Berton, M. T. & Linehan, L. A. IL-4 activates a latent DNA-binding factor that binds a shared IFN-g and IL-4 response element present in the germ-line g1 Ig promoter. J. Immunol. 154, 4513–4525 (1995). (PMID: 77223067722306)
Zhu, J., Yamane, H., Cote-Sierra, J., Guo, L. & Paul, W. E. GATA-3 promotes Th2 responses through three different mechanisms: induction of Th2 cytokine production, selective growth of Th2 cells and inhibition of Th1 cell-specific factors. Cell Res. 16(1), 3–10 (2006). (PMID: 10.1038/sj.cr.731000216467870)
Szabo, S. J. et al. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell. 100, 655–669 (2000). (PMID: 10.1016/S0092-8674(00)80702-310761931)
Kuipers, H. et al. Dendritic cells retrovirally overexpressing IL-12 induce strong Th1 responses to inhaled antigen in the lung but fail to revert established Th2 sensitization. J. Leuk. Biol. 5, 1028–1038 (2004). (PMID: 10.1189/jlb.0604325)
Meyts, I. et al. IL-12 contributes to allergen-induced airway inflammation in experimental asthma. J. Immunol. 177(9), 6460–6470 (2006). (PMID: 10.4049/jimmunol.177.9.646017056578)
Piancatelli, D., Bellotta, L., Del Beato, T., Duse, M. & Della Penna, M. R. Total IL-12 levels are increased in paediatric atopic dermatitis: correlations with age and disease severity. Int. J. Immunopathol. Pharmacol. 21(2), 359–365 (2008). (PMID: 10.1177/03946320080210021318547480)
Zhang, H. et al. Modulation of mast cell proteinase-activated receptor expression and IL-4 release by IL-12. Immunol. Cell Biol. 7, 558–566 (2007). (PMID: 10.1038/sj.icb.7100085)
Lopes-Ferreira, M., Barbaro, K. C., Cardoso, D. F., Moura-da-Silva, A. M. & Mota, I. Thalassophryne nattereri fish venom: biological and biochemical characterization and serum neutralization of its toxic activities. Toxicon. 36, 405–410 (1998). (PMID: 10.1016/S0041-0101(97)00115-39620588)
المشرفين على المادة: 0 (Fish Venoms)
0 (IFNG protein, mouse)
0 (Il4 protein, mouse)
0 (Immunoglobulin G)
207137-56-2 (Interleukin-4)
37341-29-0 (Immunoglobulin E)
82115-62-6 (Interferon-gamma)
تواريخ الأحداث: Date Created: 20200119 Date Completed: 20201119 Latest Revision: 20210116
رمز التحديث: 20240628
مُعرف محوري في PubMed: PMC6969187
DOI: 10.1038/s41598-019-57231-y
PMID: 31953450
قاعدة البيانات: MEDLINE
الوصف
تدمد:2045-2322
DOI:10.1038/s41598-019-57231-y