Journal Article
. 2011 Dec; 6(12):e28917.
doi: 10.1371/journal.pone.0028917.

Contribution of classic and alternative effector pathways in peanut-induced anaphylactic responses

Joost J Smit 1 Karina Willemsen  Ine Hassing  Danielle Fiechter  Gert Storm  Louis van Bloois  Jeanette H W Leusen  Maarten Pennings  Dietmar Zaiss  Raymond H H Pieters  
Affiliations
  • PMID: 22194949
  •     34 References
  •     28 citations

Abstract

Food allergy affects approximately 5% of children and is the leading cause of hospitalization for anaphylactic reactions in westernized countries. However, the pathways of anaphylaxis in food allergy are still relatively unknown. We investigated the effector pathways of allergic and anaphylactic responses of different strains of mice in a clinical relevant model of peanut allergy. C3H/HeOuJ, C57BL/6 and BALB/c mice were sensitized by intragastric peanut extract and challenged by intragastric or intraperitoneal injection of peanut. Peanut-specific T cell responses, IgE, IgG1 and IgG2a and mucosal mast cell degranulation were induced to different extent in C3H/HeOuJ, C57BL/6 and BALB/c mice. Interestingly, anaphylactic symptoms after systemic challenge were highest in C3H/HeOuJ followed by C57BL/6 but were absent in BALB/c mice. Mechanistic studies showed that the food allergic systemic anaphylaxis was dependent on platelets, FcRγ and mast cells, and partially dependent on platelet activating factor and monocytes/macrophages, depending on mouse strain. These data demonstrate that in three mouse strains, components of the classic and alternative anaphylactic cascade are differently expressed, leading to differential outcomes in parameters of allergic disease and food induced systemic anaphylaxis.

PAF, a putative mediator of oral inflammation.
L M McManus, R N Pinckard.
Crit Rev Oral Biol Med, 2002 May 11; 11(2). PMID: 12002818
Review.
Impact of CD40 ligand, B cells, and mast cells in peanut-induced anaphylactic responses.
Jiangfeng Sun, Katherine Arias, +8 authors, Manel Jordana.
J Immunol, 2007 Nov 06; 179(10). PMID: 17982059
Concurrent blockade of platelet-activating factor and histamine prevents life-threatening peanut-induced anaphylactic reactions.
Katherine Arias, Moiz Baig, +7 authors, Manel Jordana.
J Allergy Clin Immunol, 2009 May 05; 124(2). PMID: 19409603
Pathways of anaphylaxis in the mouse.
Richard T Strait, Suzanne C Morris, +2 authors, Fred D Finkelman.
J Allergy Clin Immunol, 2002 Apr 10; 109(4). PMID: 11941316
Distinct immune effector pathways contribute to the full expression of peanut-induced anaphylactic reactions in mice.
Katherine Arias, Derek K Chu, +10 authors, Manel Jordana.
J Allergy Clin Immunol, 2011 Jun 01; 127(6). PMID: 21624619
Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice.
Jean M Daley, Alan A Thomay, +2 authors, Jorge E Albina.
J Leukoc Biol, 2007 Sep 22; 83(1). PMID: 17884993
Highly Cited.
Platelet activating factor as a mediator and therapeutic approach in bronchial asthma.
A Kasperska-Zajac, Z Brzoza, B Rogala.
Inflammation, 2008 Jan 15; 31(2). PMID: 18193345
Review.
Analysis of food-allergic and anaphylactic events in the National Electronic Injury Surveillance System.
Marianne Phelan Ross, Martine Ferguson, +3 authors, Stefano Luccioli.
J Allergy Clin Immunol, 2008 Jan 22; 121(1). PMID: 18206508
IL-9 promotes but is not necessary for systemic anaphylaxis.
Laurent Knoops, Jamila Louahed, Jacques Van Snick, Jean-Christophe Renauld.
J Immunol, 2005 Jun 24; 175(1). PMID: 15972666
Ingested allergens must be absorbed systemically to induce systemic anaphylaxis.
Richard T Strait, Ashley Mahler, +3 authors, Fred D Finkelman.
J Allergy Clin Immunol, 2011 Mar 01; 127(4). PMID: 21354602    Free PMC article.
Avirulant Salmonella typhimurium strains prevent food allergy in mice.
P A Eigenmann, K E Asigbetse, C P Frossard.
Clin Exp Immunol, 2008 Jan 15; 151(3). PMID: 18190606    Free PMC article.
Idiopathic anaphylaxis.
Johannes Ring, Ulf Darsow.
Curr Allergy Asthma Rep, 2002 Mar 16; 2(1). PMID: 11895624
Review.
Basophils are essential initiators of a novel type of chronic allergic inflammation.
Kazushige Obata, Kaori Mukai, +5 authors, Hajime Karasuyama.
Blood, 2007 Apr 06; 110(3). PMID: 17409268
Granule proteinases define mast cell heterogeneity in the serosa and the gastrointestinal mucosa of the mouse.
H R Miller, J F Huntley, +3 authors, D Wakelin.
Immunology, 1988 Dec 01; 65(4). PMID: 3065218    Free PMC article.
CTLA-4 signaling regulates the intensity of hypersensitivity responses to food antigens, but is not decisive in the induction of sensitization.
Femke van Wijk, Sanne Hoeks, +5 authors, Raymond Pieters.
J Immunol, 2004 Dec 22; 174(1). PMID: 15611239
Mast cells are required for experimental oral allergen-induced diarrhea.
Eric B Brandt, Richard T Strait, +6 authors, Marc E Rothenberg.
J Clin Invest, 2003 Dec 09; 112(11). PMID: 14660743    Free PMC article.
Highly Cited.
Epidemiology of food allergy.
Scott H Sicherer.
J Allergy Clin Immunol, 2011 Jan 18; 127(3). PMID: 21236480
Highly Cited. Review.
Nonredundant roles of basophils in immunity.
Hajime Karasuyama, Kaori Mukai, +2 authors, Takeshi Wada.
Annu Rev Immunol, 2010 Dec 21; 29. PMID: 21166539
Review.
Platelet-activating factor, PAF acetylhydrolase, and severe anaphylaxis.
Peter Vadas, Milton Gold, +7 authors, Jupiter Yeung.
N Engl J Med, 2008 Jan 04; 358(1). PMID: 18172172
Highly Cited.
Immunophysiology of experimental food allergy.
M C Berin, L Mayer.
Mucosal Immunol, 2008 Dec 17; 2(1). PMID: 19079331
Review.
Genetic susceptibility to food allergy is linked to differential TH2-TH1 responses in C3H/HeJ and BALB/c mice.
Vivian Morafo, Kamal Srivastava, +4 authors, AndXiu-Min Li.
J Allergy Clin Immunol, 2003 May 14; 111(5). PMID: 12743580
Mast cells: emerging sentinel innate immune cells with diverse role in immunity.
V Kumar, A Sharma.
Mol Immunol, 2010 Aug 04; 48(1-3). PMID: 20678798
Review.
Regulation by intestinal γδ T cells during establishment of food allergic sensitization in mice.
M Bol-Schoenmakers, M Marcondes Rezende, +6 authors, J J Smit.
Allergy, 2010 Oct 01; 66(3). PMID: 20880210
Food Allergy Herbal Formula-2 silences peanut-induced anaphylaxis for a prolonged posttreatment period via IFN-gamma-producing CD8+ T cells.
Kamal D Srivastava, Chunfeng Qu, +3 authors, Xiu-Min Li.
J Allergy Clin Immunol, 2009 Feb 11; 123(2). PMID: 19203662
Peanuts can contribute to anaphylactic shock by activating complement.
Marat Khodoun, Richard Strait, +5 authors, Fred D Finkelman.
J Allergy Clin Immunol, 2009 Jan 06; 123(2). PMID: 19121857    Free PMC article.
Platelet depletion in mice increases mortality after thermal injury.
Satoshi Fujimi, Malcolm P MacConmara, +4 authors, Peter H Lapchak.
Blood, 2006 Feb 10; 107(11). PMID: 16467203    Free PMC article.
IgG-blocking antibodies inhibit IgE-mediated anaphylaxis in vivo through both antigen interception and Fc gamma RIIb cross-linking.
Richard T Strait, Suzanne C Morris, Fred D Finkelman.
J Clin Invest, 2006 Feb 25; 116(3). PMID: 16498503    Free PMC article.
Peanut allergy.
A Wesley Burks.
Lancet, 2008 May 06; 371(9623). PMID: 18456104
Review.
Short-term anaphylactic IgG antibodies in human sera.
W E Parish.
Lancet, 1970 Sep 19; 2(7673). PMID: 4195549
Enhanced engraftment of human cells in RAG2/gammac double-knockout mice after treatment with CL2MDP liposomes.
Henk Rozemuller, Shosh Knaän-Shanzer, +3 authors, Anton C M Martens.
Exp Hematol, 2004 Nov 13; 32(11). PMID: 15539091
Acute allergic skin reactions and intestinal contractility changes in mice orally sensitized against casein or whey.
Bastiaan Schouten, Betty C A M van Esch, +3 authors, Johan Garssen.
Int Arch Allergy Immunol, 2008 Jun 04; 147(2). PMID: 18520157
Mouse and human neutrophils induce anaphylaxis.
Friederike Jönsson, David A Mancardi, +6 authors, Pierre Bruhns.
J Clin Invest, 2011 Mar 26; 121(4). PMID: 21436586    Free PMC article.
Highly Cited.
Anaphylaxis: lessons from mouse models.
Fred D Finkelman.
J Allergy Clin Immunol, 2007 Sep 04; 120(3). PMID: 17765751
Highly Cited. Review.
Role of TLR4 in allergic sensitization to food proteins in mice.
M C Berin, Y Zheng, +2 authors, H A Sampson.
Allergy, 2005 Dec 21; 61(1). PMID: 16364158
Mucosal immunology of food allergy.
M Cecilia Berin, Hugh A Sampson.
Curr Biol, 2013 May 11; 23(9). PMID: 23660362    Free PMC article.
Review.
Use of animal models to investigate major allergens associated with food allergy.
Jenna L Van Gramberg, Michael J de Veer, +2 authors, Robert J Bischof.
J Allergy (Cairo), 2013 May 22; 2013. PMID: 23690797    Free PMC article.
Selective ablation of mast cells or basophils reduces peanut-induced anaphylaxis in mice.
Laurent L Reber, Thomas Marichal, +8 authors, Stephen J Galli.
J Allergy Clin Immunol, 2013 Aug 07; 132(4). PMID: 23915716    Free PMC article.
The immunology of food allergy.
Laura K Johnston, Karen B Chien, Paul J Bryce.
J Immunol, 2014 Mar 13; 192(6). PMID: 24610821    Free PMC article.
Review.
Food allergy: Insights into etiology, prevention, and treatment provided by murine models.
Michiko K Oyoshi, Hans C Oettgen, +2 authors, Paul J Bryce.
J Allergy Clin Immunol, 2014 Mar 19; 133(2). PMID: 24636470    Free PMC article.
Review.
Allergic sensitization: screening methods.
Gregory S Ladics, Jeremy Fry, +8 authors, Jean-Michel Wal.
Clin Transl Allergy, 2014 Apr 18; 4(1). PMID: 24739743    Free PMC article.
Future Therapies for IgE-Mediated Food Allergy.
M Cecilia Berin.
Curr Pediatr Rep, 2014 Jun 03; 2(2). PMID: 24883237    Free PMC article.
Potential effector and immunoregulatory functions of mast cells in mucosal immunity.
L L Reber, R Sibilano, K Mukai, S J Galli.
Mucosal Immunol, 2015 Feb 12; 8(3). PMID: 25669149    Free PMC article.
Review.
Approaches for analyzing the roles of mast cells and their proteases in vivo.
Stephen J Galli, Mindy Tsai, +3 authors, Gunnar Pejler.
Adv Immunol, 2015 Mar 03; 126. PMID: 25727288    Free PMC article.
Review.
Heterogeneous responses and cross reactivity between the major peanut allergens Ara h 1, 2,3 and 6 in a mouse model for peanut allergy.
Joost J Smit, Maarten T Pennings, +3 authors, Raymond H Pieters.
Clin Transl Allergy, 2015 Mar 25; 5. PMID: 25802736    Free PMC article.
Induction of Interleukin-9-Producing Mucosal Mast Cells Promotes Susceptibility to IgE-Mediated Experimental Food Allergy.
Chun-Yu Chen, Jee-Boong Lee, +11 authors, Yui-Hsi Wang.
Immunity, 2015 Sep 28; 43(4). PMID: 26410628    Free PMC article.
Highly Cited.
IL-25 and CD4(+) TH2 cells enhance type 2 innate lymphoid cell-derived IL-13 production, which promotes IgE-mediated experimental food allergy.
Jee-Boong Lee, Chun-Yu Chen, +9 authors, Yui-Hsi Wang.
J Allergy Clin Immunol, 2015 Nov 13; 137(4). PMID: 26560039    Free PMC article.
Antibody Production, Anaphylactic Signs, and T-Cell Responses Induced by Oral Sensitization With Ovalbumin in BALB/c and C3H/HeOuJ Mice.
Alba Pablos-Tanarro, Ivan López-Expósito, +2 authors, Elena Molina.
Allergy Asthma Immunol Res, 2016 Mar 01; 8(3). PMID: 26922934    Free PMC article.
B cells establish, but do not maintain, long-lived murine anti-peanut IgE(a).
D M Moutsoglou, S C Dreskin.
Clin Exp Allergy, 2016 Mar 30; 46(4). PMID: 27021119    Free PMC article.
Current challenges facing the assessment of the allergenic capacity of food allergens in animal models.
Katrine Lindholm Bøgh, Jolanda van Bilsen, +17 authors, Liam O'Mahony.
Clin Transl Allergy, 2016 Jun 18; 6. PMID: 27313841    Free PMC article.
Review.
Epidemiology of severe anaphylaxis: can we use population-based data to understand anaphylaxis?
Paul J Turner, Dianne E Campbell.
Curr Opin Allergy Clin Immunol, 2016 Aug 05; 16(5). PMID: 27490124    Free PMC article.
Review.
Mass cytometry profiling the response of basophils and the complete peripheral blood compartment to peanut.
Leticia Tordesillas, Adeeb H Rahman, +2 authors, M Cecilia Berin.
J Allergy Clin Immunol, 2016 Aug 18; 138(6). PMID: 27531074    Free PMC article.
Pathways of immediate hypothermia and leukocyte infiltration in an adjuvant-free mouse model of anaphylaxis.
Bianca Balbino, Riccardo Sibilano, +7 authors, Stephen J Galli.
J Allergy Clin Immunol, 2016 Aug 25; 139(2). PMID: 27555460    Free PMC article.
The pathophysiology of anaphylaxis.
Laurent L Reber, Joseph D Hernandez, Stephen J Galli.
J Allergy Clin Immunol, 2017 Aug 07; 140(2). PMID: 28780941    Free PMC article.
Highly Cited. Review.
Human CD22 Inhibits Murine B Cell Receptor Activation in a Human CD22 Transgenic Mouse Model.
Kyle J Bednar, Elena Shanina, +10 authors, Matthew S Macauley.
J Immunol, 2017 Oct 04; 199(9). PMID: 28972089    Free PMC article.
The efficacy of oral and subcutaneous antigen-specific immunotherapy in murine cow's milk- and peanut allergy models.
Marlotte M Vonk, Laura Wagenaar, +5 authors, Johan Garssen.
Clin Transl Allergy, 2017 Oct 13; 7. PMID: 29021893    Free PMC article.
Oral sensitization to whey proteins induces age- and sex-dependent behavioral abnormality and neuroinflammatory responses in a mouse model of food allergy: a potential role of mast cells.
Danielle L Germundson, Nicholas A Smith, +3 authors, Kumi Nagamoto-Combs.
J Neuroinflammation, 2018 Apr 25; 15(1). PMID: 29685134    Free PMC article.
Reuse of public, genome-wide, murine eosinophil expression data for hypotheses development.
Jillian O Grace, Astha Malik, +3 authors, Patricia C Fulkerson.
J Leukoc Biol, 2018 May 15; 104(1). PMID: 29758095    Free PMC article.
FcεRI-HDAC3-MCP1 Signaling Axis Promotes Passive Anaphylaxis Mediated by Cellular Interactions.
Misun Kim, Yoojung Kwon, +2 authors, Dooil Jeoung.
Int J Mol Sci, 2019 Oct 11; 20(19). PMID: 31597362    Free PMC article.
Review.
Mouse strain differences in response to oral immunotherapy for peanut allergy.
Laura Wagenaar, Marianne W H C Bol-Schoenmakers, +3 authors, Raymond H H Pieters.
Immun Inflamm Dis, 2019 Mar 07; 7(1). PMID: 30838819    Free PMC article.
Administration of Extensive Hydrolysates From Caseins and Lactobacillus rhamnosus GG Probiotic Does Not Prevent Cow's Milk Proteins Allergy in a Mouse Model.
Karine Adel-Patient, Marine Guinot, +4 authors, Christophe Junot.
Front Immunol, 2020 Oct 13; 11. PMID: 33042105    Free PMC article.
A network-based approach for identifying suitable biomarkers for oral immunotherapy of food allergy.
Jolanda H M van Bilsen, Lars Verschuren, +7 authors, Tim J van den Broek.
BMC Bioinformatics, 2019 Apr 25; 20(1). PMID: 31014233    Free PMC article.
Oral anaphylaxis to peanut in a mouse model is associated with gut permeability but not with Tlr4 or Dock8 mutations.
Jake A Gertie, Biyan Zhang, +8 authors, Stephanie C Eisenbarth.
J Allergy Clin Immunol, 2021 May 30;. PMID: 34051223    Free PMC article.