Peanuts can contribute to anaphylactic shock by activating complement

Journal of Allergy and Clinical Immunology

Volumn 123, Issue 2, 2009, Pages 342-351

  Khodoun, Marat ^a,b   Strait, Richard ^c   Orekov, Tatyana ^a,b   Hogan, Simon ^c   Karasuyama, Hajime ^d   Herbert, De'Broski R ^a,b   Köhl, Jörg ^c,e   Finkelman, Fred D ^a,b,c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^e UNIVERSITY OF LÜBECK   (Germany)

Author keywords

anaphylaxis; basophils; C3a; complement; histamine; macrophages; mast cells; Peanut; platelet activating factor; shock

Indexed keywords

ALLERGEN; COMPLEMENT COMPONENT C3A; FC RECEPTOR; HISTAMINE; IMMUNOGLOBULIN E; IMMUNOGLOBULIN RECEPTOR; INTERLEUKIN 4; PROPRANOLOL; THROMBOCYTE ACTIVATING FACTOR;

ADAPTIVE IMMUNITY; ANAPHYLACTIC SHOCK; ANIMAL MODEL; ARTICLE; BASOPHIL; CELL TYPE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MACROPHAGE; MAST CELL; MAST CELL DEGRANULATION; MOUSE; NONHUMAN; NUT; PATHOGENESIS; PEANUT; PRIORITY JOURNAL; RECTAL THERMOMETER;

ADRENERGIC BETA-ANTAGONISTS; ALLERGENS; ANAPHYLAXIS; ANIMALS; ARACHIS HYPOGAEA; BASOPHILS; CELL DEGRANULATION; CHYMASES; COMPLEMENT ACTIVATION; COMPLEMENT C3A; HISTAMINE; HUMANS; IMMUNOGLOBULIN E; INTERLEUKIN-4; MACROPHAGES; MAST CELLS; MICE; MICE, INBRED BALB C; PEANUT HYPERSENSITIVITY; PLATELET ACTIVATING FACTOR; PROPRANOLOL; RECEPTORS, IGG; TOLL-LIKE RECEPTORS;

EID: 59449108818     PISSN: 00916749     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jaci.2008.11.004     Document Type: Article

References (63)

1. Sicherer S.H., Munoz-Furlong A., and Sampson H.A. Prevalence of peanut and tree nut allergy in the United States determined by means of a random digit dial telephone survey: a 5-year follow-up study. J Allergy Clin Immunol 112 (2003) 1203-1207
2. Bock S.A., Munoz-Furlong A., and Sampson H.A. Fatalities due to anaphylactic reactions to foods. J Allergy Clin Immunol 107 (2001) 191-193
3. Bock S.A., Munoz-Furlong A., and Sampson H.A. Further fatalities caused by anaphylactic reactions to food, 2001-2006. J Allergy Clin Immunol 119 (2007) 1016-1018
4. Skolnick H.S., Conover-Walker M.K., Koerner C.B., Sampson H.A., Burks W., and Wood R.A. The natural history of peanut allergy. J Allergy Clin Immunol 107 (2001) 367-374
5. Palmer K., and Burks W. Current developments in peanut allergy. Curr Opin Allergy Clin Immunol 6 (2006) 202-206
6. Beyer K., Morrow E., Li X.M., Bardina L., Bannon G.A., Burks A.W., et al. Effects of cooking methods on peanut allergenicity. J Allergy Clin Immunol 107 (2001) 1077-1081
7. Maleki S.J., Kopper R.A., Shin D.S., Park C.W., Compadre C.M., Sampson H., et al. Structure of the major peanut allergen Ara h 1 may protect IgE-binding epitopes from degradation. J Immunol 164 (2000) 5844-5849
8. Sen M., Kopper R., Pons L., Abraham E.C., Burks A.W., and Bannon G.A. Protein structure plays a critical role in peanut allergen stability and may determine immunodominant IgE-binding epitopes. J Immunol 169 (2002) 882-887
9. Shreffler W.G., Castro R.R., Kucuk Z.Y., Charlop-Powers Z., Grishina G., Yoo S., et al. The major glycoprotein allergen from Arachis hypogaea, Ara h 1, is a ligand of dendritic cell-specific ICAM-grabbing nonintegrin and acts as a Th2 adjuvant in vitro. J Immunol 177 (2006) 3677-3685
10. van Wijk F., Nierkens S., Hassing I., Feijen M., Koppelman S.J., de Jong G.A., et al. The effect of the food matrix on in vivo immune responses to purified peanut allergens. Toxicol Sci 86 (2005) 333-341
11. Takai T., Li M., Sylvestre D., Clynes R., and Ravetch J.V. FcR γ chain deletion results in pleiotrophic effector cell defects. Cell 76 (1994) 519-529
12. Luther S.A., Lopez T., Bai W., Hanahan D., and Cyster J.G. BLC expression in pancreatic islets causes B cell recruitment and lymphotoxin-dependent lymphoid neogenesis. Immunity 12 (2000) 471-481
13. Wessels M.R., Butko P., Ma M., Warren H.B., Lage A.L., and Carroll M.C. Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc Natl Acad Sci U S A 92 (1995) 11490-11494
14. Hopken U.E., Lu B., Gerard N.P., and Gerard C. Impaired inflammatory responses in the reverse arthus reaction through genetic deletion of the C5a receptor. J Exp Med 186 (1997) 749-756
15. Humbles A.A., Lu B., Nilsson C.A., Lilly C., Israel E., Fujiwara Y., et al. A role for the C3a anaphylatoxin receptor in the effector phase of asthma. Nature 406 (2000) 998-1001
16. Mombaerts P., Iacomini J., Johnson R.S., Herrup K., Tonegawa S., and Papaioannou V.E. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68 (1992) 869-877
17. Godfrey P., Rahal J.O., Beamer W.G., Copeland N.G., Jenkins N.A., and Mayo K.E. GHRH receptor of little mice contains a missense mutation in the extracellular domain that disrupts receptor function. Nat Genet 4 (1993) 227-232
18. Hoshino K., Takeuchi O., Kawai T., Sanjo H., Ogawa T., Takeda Y., et al. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 162 (1999) 3749-3752
19. Takeuchi O., Hoshino K., Kawai T., Sanjo H., Takada H., Ogawa T., et al. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11 (1999) 443-451
20. Adachi O., Kawai T., Takeda K., Matsumoto M., Tsutsui H., Sakagami M., et al. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9 (1998) 143-150
21. Forbes E.E., Groschwitz K., Abonia J.P., Brandt E.B., Cohen E., Blanchard C., et al. IL-9- and mast cell-mediated intestinal permeability predisposes to oral antigen hypersensitivity. J Exp Med 205 (2008) 897-913
22. Strait R.T., Morris S.C., Yang M., Qu X.W., and Finkelman F.D. Pathways of anaphylaxis in the mouse. J Allergy Clin Immunol 109 (2002) 658-668
23. Mizgerd J.P., Molina R.M., Stearns R.C., Brain J.D., and Warner A.E. Gadolinium induces macrophage apoptosis. J Leukoc Biol 59 (1996) 189-195
24. Van Rooijen N., and Sanders A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 174 (1994) 83-93
25. Otto M., Hawlisch H., Monk P.N., Muller M., Klos A., Karp C.L., et al. C5a mutants are potent antagonists of the C5a receptor (CD88) and of C5L2: position 69 is the locus that determines agonism or antagonism. J Biol Chem 279 (2004) 142-151
26. Ames R.S., Lee D., Foley J.J., Jurewicz A.J., Tornetta M.A., Bautsch W., et al. Identification of a selective nonpeptide antagonist of the anaphylatoxin C3a receptor that demonstrates antiinflammatory activity in animal models. J Immunol 166 (2001) 6341-6348
27. Grencis R.K., Else K.J., Huntley J.F., and Nishikawa S.I. The in vivo role of stem cell factor (c-kit ligand) on mastocytosis and host protective immunity to the intestinal nematode. Trichinella spiralis in mice. Parasite Immunol 15 (1993) 55-59
28. Baniyash M., and Eshhar Z. Inhibition of IgE binding to mast cells and basophils by monoclonal antibodies to murine IgE. Eur J Immunol 14 (1984) 799-807
29. Strait R.T., Morris S.C., Smiley K., and Urban Jr. J.F. Finkelman FD. IL-4 exacerbates anaphylaxis. J Immunol 170 (2003) 3835-3842
30. Finkelman F.D., Madden K.B., Morris S.C., Holmes J.M., Boiani N., Katona I.M., et al. Anti-cytokine antibodies as carrier proteins. Prolongation of in vivo effects of exogenous cytokines by injection of cytokine-anti-cytokine antibody complexes. J Immunol 151 (1993) 1235-1244
31. Kojima T., Obata K., Mukai K., Sato S., Takai T., Minegishi Y., et al. Mast cells and basophils are selectively activated in vitro and in vivo through CD200R3 in an IgE-independent manner. J Immunol 179 (2007) 7093-7100
32. Tsujimura Y., Obata K., Mukai K., Shindou H., Yoshida M., Nishikado H., et al. Basophils play a pivotal role in immunoglobulin-G-mediated but not immunoglobulin-E-mediated systemic anaphylaxis. Immunity 28 (2008) 581-589
33. Khodoun M.V., Orekhova T., Potter C., Morris S., and Finkelman F.D. Basophils initiate IL-4 production during a memory T-dependent response. J Exp Med 200 (2004) 857-870
34. Urban Jr. J.F., Noben-Trauth N., Schopf L., Madden K.B., and Finkelman F.D. Cutting edge: IL-4 receptor expression by non-bone marrow-derived cells is required to expel gastrointestinal nematode parasites. J Immunol 167 (2001) 6078-6081
35. Peitzman A.B., Billiar T.R., Harbrecht B.G., Kelly E., Udekwu A.O., and Simmons R.L. Hemorrhagic shock. Curr Probl Surg 32 (1995) 925-1002
36. Lang D.M. Anaphylactoid and anaphylactic reactions. Hazards of β-blockers. Drug Saf 12 (1995) 299-304
37. Madden K.B., Yeung K.A., Zhao A., Gause W.C., Finkelman F.D., Katona I.M., et al. Enteric nematodes induce stereotypic STAT6-dependent alterations in intestinal epithelial cell function. J Immunol 172 (2004) 5616-5621
38. Takeuchi O., Takeda K., Hoshino K., Adachi O., Ogawa T., and Akira S. Cellular responses to bacterial cell wall components are mediated through MyD88-dependent signaling cascades. Int Immunol 12 (2000) 113-117
39. Mencia-Huerta J.M., and Benveniste J. Platelet-activation factor and macrophages. I. Evidence for the release from rate and mouse peritoneal macrophages and not from mastocytes. Eur J Immunol 9 (1979) 409-415
40. Cavaillon J.M., Fitting C., and Haeffner-Cavaillon N. Recombinant C5a enhances interleukin 1 and tumor necrosis factor release by lipopolysaccharide-stimulated monocytes and macrophages. Eur J Immunol 20 (1990) 253-257
41. Johnson A.R., Hugli T.E., and Muller-Eberhard H.J. Release of histamine from rat mast cells by complement peptides C3a and C5a. Immunology 28 (1975) 1067-1080
42. Abbas A.K., and Lichtman A.H. Cellular and molecular immunology. 5th ed. (2003), Elsevier Science, Philadelphia
43. Thurman J.M., and Holers V.M. The central role of the alternative complement pathway in human disease. J Immunol 176 (2006) 1305-1310
44. Proust B., Astier C., Jacquenet S., Ogier V., Magueur E., Roitel O., et al. A single oral sensitization to peanut without adjuvant leads to anaphylaxis in mice. Int Arch Allergy Immunol 146 (2008) 212-218
45. Trendelenburg M., Fossati-Jimack L., Cortes-Hernandez J., Turnberg D., Lewis M., Izui S., et al. The role of complement in cryoglobulin-induced immune complex glomerulonephritis. J Immunol 175 (2005) 6909-6914
46. Hawlisch H., Wills-Karp M., Karp C.L., and Kohl J. The anaphylatoxins bridge innate and adaptive immune responses in allergic asthma. Mol Immunol 41 (2004) 123-131
47. Nakano Y., Morita S., Kawamoto A., Suda T., Chida K., and Nakamura H. Elevated complement C3a in plasma from patients with severe acute asthma. J Allergy Clin Immunol 112 (2003) 525-530
48. Ali H., and Panettieri Jr. R.A. Anaphylatoxin C3a receptors in asthma. Respir Res 6 (2005) 19
49. Rittirsch D., Flierl M.A., Nadeau B.A., Day D.E., Huber-Lang M., Mackay C.R., et al. Functional roles for C5a receptors in sepsis. Nat Med 14 (2008) 551-557
50. Baelder R., Fuchs B., Bautsch W., Zwirner J., Köhl J., Hoymann H.G., et al. Pharmacological targeting of anaphylatoxin receptors during the effector phase of allergic asthma suppresses airway hyperresponsiveness and airway inflammation. J Immunol 174 (2005) 783-789
51. Kildsgaard J., Hollmann T.J., Matthews K.W., Bian K., Murad F., and Wetsel R.A. Cutting edge: targeted disruption of the C3a receptor gene demonstrates a novel protective anti-inflammatory role for C3a in endotoxin-shock. J Immunol 165 (2000) 5406-5409
52. Becker E.L., Mota I., and Wong D. Inhibition by antihistamines of the vascular permeability increase induced by bradykinin. Br J Pharmacol 34 (1968) 330-336
53. Nakajima K., Murakami M., Yanoshita R., Samejima Y., Karasawa K., Setaka M., et al. Activated mast cells release extracellular type platelet-activating factor acetylhydrolase that contributes to autocrine inactivation of platelet-activating factor. J Biol Chem 272 (1997) 19708-19713
54. Mondino B.J., and Sumner H.L. Generation of complement-derived anaphylatoxins in normal human donor corneas. Invest Ophthalmol Vis Sci 31 (1990) 1945-1949
55. Cauwels A., Janssen B., Buys E., Sips P., and Brouckaert P. Anaphylactic shock depends on PI3K and eNOS-derived NO. J Clin Invest 116 (2006) 2244-2251
56. TenBrook Jr. J.A., Wolf M.P., Hoffman S.N., Rosenwasser L.J., Konstam M.A., Salem D.N., et al. Should β-blockers be given to patients with heart disease and peanut-induced anaphylaxis? A decision analysis. J Allergy Clin Immunol 113 (2004) 977-982
57. Perry T.T., Matsui E.C., Kay Conover-Walker M., and Wood R.A. The relationship of allergen-specific IgE levels and oral food challenge outcome. J Allergy Clin Immunol 114 (2004) 144-149
58. De Carolis C., Perricone R., De Sanctis G., and Fontana L. Complement activation by Hymenoptera venom allergenic extracts. J Allergy Clin Immunol 70 (1982) 219-220
59. Reisman R.E. Stinging insect allergy. Med Clin North Am 76 (1992) 883-894
60. von Zabern I., Przyklenk H., Nolte R., and Vogt W. Effect of different penicillin derivatives on complement components in human serum. Int Arch Allergy Appl Immunol 75 (1984) 164-172
61. Leone R., Conforti A., Venegoni M., Motola D., Moretti U., Meneghelli I., et al. Drug-induced anaphylaxis: case/non-case study based on an Italian pharmacovigilance database. Drug Saf 28 (2005) 547-556
62. Dempsey P.W., Allison M.E., Akkaraju S., Goodnow C.C., and Fearon D.T. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 271 (1996) 348-350
63. Stager S., Alexander J., Kirby A.C., Botto M., Rooijen N.V., Smith D.F., et al. Natural antibodies and complement are endogenous adjuvants for vaccine-induced CD8+ T-cell responses. Nat Med 9 (2003) 1287-1292