Deficiency of leukotriene B4 receptor type 1 ameliorates ovalbumin-induced allergic enteritis in mice.
BLT1
allergic enteritis
dendritic cells
eosinophils
food allergy LTB4
neutrophils
ovalbumin
Journal
Clinical and experimental pharmacology & physiology
ISSN: 1440-1681
Titre abrégé: Clin Exp Pharmacol Physiol
Pays: Australia
ID NLM: 0425076
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
revised:
30
05
2023
received:
21
02
2023
accepted:
24
06
2023
medline:
3
8
2023
pubmed:
6
7
2023
entrez:
5
7
2023
Statut:
ppublish
Résumé
Leukotriene B4 receptor type 1 (BLT1), a high-affinity receptor for leukotriene B4 (LTB4), plays an important role in inflammatory responses, including allergic airway inflammation. In this study, we examined the effect of genetic BLT1 deletion (BLT1KO) on ovalbumin (OVA)-induced allergic enteritis in mice to determine the pathogenic role of LTB4/BLT1 in allergic enteritis, a gastrointestinal form of food allergy. Repeated oral OVA challenges after sensitization with OVA and aluminium potassium sulphate induced allergic enteritis, characterized by systemic allergic symptoms (scratching, immobility and swelling), diarrhoea, colonic oedema and colonic goblet cell hyperplasia, accompanied by increased colonic peroxidase activity, colonic inflammatory cytokine expression and increased serum OVA-specific IgE levels. The severity of enteritis was significantly attenuated in BLT1KO mice compared with wild-type (WT) mice, without an increase in serum OVA-specific IgE levels. The accumulation of neutrophils, eosinophils, M2-macrophages, dendritic cells, CD4+ T cells and mast cells was observed in the colonic mucosa of allergic enteritis, and such accumulation was significantly lower in BLT1KO mice than in WT mice. BLT1 expression was upregulated and colocalized mostly in neutrophils and partly in eosinophils and dendritic cells in the colonic mucosa of allergic enteritis. These findings indicate that BLT1 deficiency ameliorates OVA-induced allergic enteritis in mice and that LTB4/BLT1 contributes to neutrophil and eosinophil accumulation in the allergic colonic mucosa. Therefore, BLT1 is a promising drug target for treating food allergies.
Identifiants
pubmed: 37406678
doi: 10.1111/1440-1681.13808
doi:
Substances chimiques
Ovalbumin
9006-59-1
Receptors, Leukotriene B4
0
Leukotriene B4
1HGW4DR56D
Immunoglobulin E
37341-29-0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
766-775Informations de copyright
© 2023 John Wiley & Sons Australia, Ltd.
Références
Loh W, Tang MLK. The epidemiology of food allergy in the global context. Int J Environ Res Public Health. 2018;15(9):2043.
Warren CM, Jiang J, Gupta RS. Epidemiology and burden of food allergy. Curr Allergy Asthma Rep. 2020;20(2):6.
Nowak-Wegrzyn A. Food protein-induced enterocolitis syndrome and allergic proctocolitis. Allergy Asthma Proc. 2015;36(3):172-184.
Bischoff SC, Mayer JH, Manns MP. Allergy and the gut. Int Arch Allergy Immunol. 2000;121(4):270-283.
Sicherer SH, Sampson HA. Food allergy: epidemiology, pathogenesis, diagnosis, and treatment. J Allergy Clin Immunol. 2014;133(2):291-307.
Kidd P. Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease. Altern Med Rev. 2003;8(3):223-246.
Coviello C, Rodriquez DC, Cecchi S, et al. Different clinical manifestation of cow's milk allergy in two preterm twins newborns. J Matern Fetal Neonatal Med. 2012;25(Suppl 1):132-133.
Molnar K, Pinter P, Gyorffy H, et al. Characteristics of allergic colitis in breast-fed infants in the absence of cow's milk allergy. World J Gastroenterol. 2013;19(24):3824-3830.
Yokomizo T. Leukotriene B4 receptors: novel roles in immunological regulations. Adv Enzyme Regul. 2011;51(1):59-64.
Yokomizo T. Two distinct leukotriene B4 receptors, BLT1 and BLT2. J Biochem. 2015;157(2):65-71.
Yokomizo T, Nakamura M, Shimizu T. Leukotriene receptors as potential therapeutic targets. J Clin Invest. 2018;128(7):2691-2701.
Saeki K, Yokomizo T. Identification, signaling, and functions of LTB4 receptors. Semin Immunol. 2017;33:30-36.
Terawaki K, Yokomizo T, Nagase T, et al. Absence of leukotriene B4 receptor 1 confers resistance to airway hyperresponsiveness and Th2-type immune responses. J Immunol. 2005;175(7):4217-4225.
Toda A, Terawaki K, Yamazaki S, Saeki K, Shimizu T, Yokomizo T. Attenuated Th1 induction by dendritic cells from mice deficient in the leukotriene B4 receptor 1. Biochimie. 2010;92(6):682-691.
Kihara Y, Yokomizo T, Kunita A, et al. The leukotriene B4 receptor, BLT1, is required for the induction of experimental autoimmune encephalomyelitis. Biochem Biophys Res Commun. 2010;394(3):673-678.
Miyahara N, Ohnishi H, Matsuda H, et al. Leukotriene B4 receptor 1 expression on dendritic cells is required for the development of Th2 responses and allergen-induced airway hyperresponsiveness. J Immunol. 2008;181(2):1170-1178.
Park D, Kwak DW, Kim JH. Leukotriene B4 receptors contribute to house dust mite-induced eosinophilic airway inflammation via TH2 cytokine production. BMB Rep. 2021;54(3):182-187.
Nakamura M, Shimizu T. Recent advances in function and structure of two leukotriene B(4) receptors: BLT1 and BLT2. Biochem Pharmacol. 2022;203:115178.
Zhou J, Lai W, Yang W, et al. BLT1 in dendritic cells promotes Th1/Th17 differentiation and its deficiency ameliorates TNBS-induced colitis. Cell Mol Immunol. 2018;15(12):1047-1056.
Henderson WR Jr, Lewis DB, Albert RK, et al. The importance of leukotrienes in airway inflammation in a mouse model of asthma. J Exp Med. 1996;184(4):1483-1494.
El Gazzar M, El Mezayen R, Nicolls MR, Marecki JC, Dreskin SC. Downregulation of leukotriene biosynthesis by thymoquinone attenuates airway inflammation in a mouse model of allergic asthma. Biochim Biophys Acta. 2006;1760(7):1088-1095.
Shin HS, Eom JE, Shin DU, Yeon SH, Lim SI, Lee SY. Preventive effects of a probiotic mixture in an ovalbumin-induced food allergy model. J Microbiol Biotechnol. 2018;28(1):65-76.
Yamaki K, Yoshino S. Preventive and therapeutic effects of rapamycin, a mammalian target of rapamycin inhibitor, on food allergy in mice. Allergy. 2012;67(10):1259-1270.
Taube C, Miyahara N, Ott V, et al. The leukotriene B4 receptor (BLT1) is required for effector CD8+ T cell-mediated, mast cell-dependent airway hyperresponsiveness. J Immunol. 2006;176(5):3157-3164.
Martinez FO, Helming L, Milde R, et al. Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood. 2013;121(9):e57-e69.
Melgert BN, ten Hacken NH, Rutgers B, Timens W, Postma DS, Hylkema MN. More alternative activation of macrophages in lungs of asthmatic patients. J Allergy Clin Immunol. 2011;127(3):831-833.
Goodarzi K, Goodarzi M, Tager AM, Luster AD, von Andrian UH. Leukotriene B4 and BLT1 control cytotoxic effector T cell recruitment to inflamed tissues. Nat Immunol. 2003;4(10):965-973.
Ott VL, Cambier JC, Kappler J, Marrack P, Swanson BJ. Mast cell-dependent migration of effector CD8+ T cells through production of leukotriene B4. Nat Immunol. 2003;4(10):974-981.
Huang WW, Garcia-Zepeda EA, Sauty A, Oettgen HC, Rothenberg ME, Luster AD. Molecular and biological characterization of the murine leukotriene B4 receptor expressed on eosinophils. J Exp Med. 1998;188(6):1063-1074.
Tager AM, Dufour JH, Goodarzi K, Bercury SD, von Andrian UH, Luster AD. BLTR mediates leukotriene B(4)-induced chemotaxis and adhesion and plays a dominant role in eosinophil accumulation in a murine model of peritonitis. J Exp Med. 2000;192(3):439-446.
Macauley MS, Crocker PR, Paulson JC. Siglec-mediated regulation of immune cell function in disease. Nat Rev Immunol. 2014;14(10):653-666.
Wang H, Xu GB, Chen H, Pan YX. Maternal high-fat diet activates hepatic interleukin-4 in rat male offspring accompanied by increased eosinophil infiltration. Am J Physiol Gastrointest Liver Physiol. 2021;320(1):G81-G92.
Ryu S, Shin JW, Kwon S, et al. Siglec-F-expressing neutrophils are essential for creating a profibrotic microenvironment in renal fibrosis. J Clin Invest. 2022;132(12):e156876.
Pani G, Siminovitch KA. Protein tyrosine phosphatase roles in the regulation of lymphocyte signaling. Clin Immunol Immunopathol. 1997;84(1):1-16.
Natsuaki Y, Egawa G, Nakamizo S, et al. Perivascular leukocyte clusters are essential for efficient activation of effector T cells in the skin. Nat Immunol. 2014;15(11):1064-1069.
Kuroda E, Ozasa K, Temizoz B, et al. Inhaled fine particles induce alveolar macrophage death and interleukin-1alpha release to promote inducible bronchus-associated lymphoid tissue formation. Immunity. 2016;45(6):1299-1310.
Koga T, Sasaki F, Saeki K, et al. Expression of leukotriene B(4) receptor 1 defines functionally distinct DCs that control allergic skin inflammation. Cell Mol Immunol. 2021;18(6):1437-1449.
Waseda K, Miyahara N, Kanehiro A, et al. Blocking the leukotriene B4 receptor 1 inhibits late-phase airway responses in established disease. Am J Respir Cell Mol Biol. 2011;45(4):851-857.
Yokomizo T, Kato K, Terawaki K, Izumi T, Shimizu T. A second leukotriene B(4) receptor, BLT2. A new therapeutic target in inflammation and immunological disorders. J Exp Med. 2000;192(3):421-432.
Matsunaga Y, Fukuyama S, Okuno T, et al. Leukotriene B4 receptor BLT2 negatively regulates allergic airway eosinophilia. FASEB J. 2013;27(8):3306-3314.
Wang J, Guo X, Chen C, et al. Gender differences in food allergy depend on the PPAR gamma/NF-kappaB in the intestines of mice. Life Sci. 2021;278:119606.
McGrath JC, Drummond GB, McLachlan EM, Kilkenny C, Wainwright CL. Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol. 2010;160(7):1573-1576.
Brandt EB, Strait RT, Hershko D, et al. Mast cells are required for experimental oral allergen-induced diarrhea. J Clin Invest. 2003;112(11):1666-1677.
Nakamura T, Maeda S, Horiguchi K, et al. PGD2 deficiency exacerbates food antigen-induced mast cell hyperplasia. Nat Commun. 2015;6:7514.
Yasuda M, Kawahara R, Hashimura H, et al. Dopamine D2-receptor antagonists ameliorate indomethacin-induced small intestinal ulceration in mice by activating α7 nicotinic acetylcholine receptors. J Pharmacol Sci. 2011;116(3):274-282.
Utsumi D, Matsumoto K, Amagase K, Horie S, Kato S. 5-HT3 receptors promote colonic inflammation via activation of substance P/neurokinin-1 receptors in dextran sulphate sodium-induced murine colitis. Br J Pharmacol. 2016;173(11):1835-1849.
Matsumoto K, Lo MW, Hosoya T, et al. Experimental colitis alters expression of 5-HT receptors and transient receptor potential vanilloid 1 leading to visceral hypersensitivity in mice. Lab Invest. 2012;92(5):769-782.
Sasaki F, Koga T, Saeki K, et al. Biochemical and immunological characterization of a novel monoclonal antibody against mouse leukotriene B4 receptor 1. PLoS One. 2017;12(9):e0185133.