Combined blockade of the histamine H1 and H4 receptor suppresses peanut-induced intestinal anaphylaxis by regulating dendritic cell function

Allergy: European Journal of Allergy and Clinical Immunology

Volumn 71, Issue 11, 2016, Pages 1561-1574

  Wang, M ^a   Han, J ^a   Domenico, J ^a   Shin, Y S ^a   Jia, Y ^a   Gelfand, E W ^a  

^a DEPARTMENT OF MEDICINE   (United States)

Author keywords

CD4+ T cells; dendritic cells; H1R; H4R; peanut allergy

Indexed keywords

1 (5 CHLORO 2 INDOLYLCARBONYL) 4 METHYLPIPERAZINE; HISTAMINE H1 RECEPTOR; HISTAMINE H4 RECEPTOR; LORATADINE; ALLERGEN; ANTIHISTAMINIC AGENT; CALCIUM; CYTOKINE; HISTAMINE H1 RECEPTOR ANTAGONIST; HRH4 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ADOPTIVE TRANSFER; ANAPHYLAXIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CALCIUM MOBILIZATION; CELL FUNCTION; CHEMOTAXIS; CONTROLLED STUDY; DENDRITIC CELL; DIARRHEA; ENTERITIS; FEMALE; HELPER CELL; INTESTINAL ANAPHYLAXIS; INTESTINE MUCOSA; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PEANUT ALLERGY; PRIORITY JOURNAL; SYMPTOMATOLOGY; ANIMAL; ANTAGONISTS AND INHIBITORS; ARACHIS; CD4+ T LYMPHOCYTE; CELL LINEAGE; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; TH17 CELL; TH2 CELL;

ADOPTIVE TRANSFER; ALLERGENS; ANAPHYLAXIS; ANIMALS; ANTIGEN-PRESENTING CELLS; ARACHIS; CALCIUM; CD4-POSITIVE T-LYMPHOCYTES; CELL LINEAGE; CHEMOTAXIS; CYTOKINES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; HISTAMINE ANTAGONISTS; HISTAMINE H1 ANTAGONISTS; INTESTINAL MUCOSA; MICE; PEANUT HYPERSENSITIVITY; RECEPTORS, HISTAMINE H4; TH17 CELLS; TH2 CELLS; TRANSCRIPTION FACTORS;

EID: 84980348266     PISSN: 01054538     EISSN: 13989995     Source Type: Journal    
DOI: 10.1111/all.12904     Document Type: Article

References (52)

1. Sicherer SH, Munoz-Furlong A, Sampson HA. 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 2003;112:1203–1207.
2. Mullins RJ, Dear KB, Tang ML. Characteristics of childhood peanut allergy in the Australian Capital Territory, 1995 to 2007. J Allergy Clin Immunol 2009;123:689–693.
3. Du TG, Roberts G, Sayre PH, Bahnson HT, Radulovic S, Santos AF et al. Randomized trial of peanut consumption in infants at risk for peanut allergy. N Engl J Med 2015;372:803–813.
4. Wang M, Takeda K, Shiraishi Y, Okamoto M, Dakhama A, Joetham A et al. Peanut-induced intestinal allergy is mediated through a mast cell-IgE-FcepsilonRI-IL-13 pathway. J Allergy Clin Immunol 2010;126:306–316.
5. Brandt EB, Strait RT, Hershko D, Wang Q, Muntel EE, Scribner TA et al. Mast cells are required for experimental oral allergen-induced diarrhea. J Clin Invest 2003;112:1666–1677.
6. Smit JJ, Bol-Schoenmakers M, Hassing I, Fiechter D, Boon L, Bleumink R et al. The role of intestinal dendritic cells subsets in the establishment of food allergy. Clin Exp Allergy 2011;41:890–898.
7. Thurmond RL, Gelfand EW, Dunford PJ. The role of histamine H1 and H4 receptors in allergic inflammation: the search for new antihistamines. Nat Rev Drug Discov 2008;7:41–53.
8. Jutel M, Blaser K, Akdis CA. Histamine in chronic allergic responses. J Invest Allergol Clin Immunol 2005;15:1–8.
9. Dunford PJ, O'Donnell N, Riley JP, Williams KN, Karlsson L, Thurmond RL. The histamine H4 receptor mediates allergic airway inflammation by regulating the activation of CD4 + T cells. J Immunol 2006;176:7062–7070.
10. Town GI, Holgate ST. Comparison of the effect of loratadine on the airway and skin responses to histamine, methacholine, and allergen in subjects with asthma. J Allergy Clin Immunol 1990;86:886–893.
11. Nguyen T, Shapiro DA, George SR, Setola V, Lee DK, Cheng R et al. Discovery of a novel member of the histamine receptor family. Mol Pharmacol 2001;59:427–433.
12. Shiraishi Y, Jia Y, Domenico J, Joetham A, Karasuyama H, Takeda K et al. Sequential engagement of FcεRI on mast cells and basophil histamine H(4) receptor and FcεRI in allergic rhinitis. J Immunol 2013;190:539–548.
13. Dunford PJ, Williams KN, Desai PJ, Karlsson L, McQueen D, Thurmond RL. Histamine H4 receptor antagonists are superior to traditional antihistamines in the attenuation of experimental pruritus. J Allergy Clin Immunol 2007;119:176–183.
14. del Rio R, Noubade R, Saligrama N, Wall EH, Krementsov DN, Poynter ME et al. Histamine H4 receptor optimizes T regulatory cell frequency and facilitates anti-inflammatory responses within the central nervous system. J Immunol 2012;188:541–547.
15. Ruiter B, Shreffler WG. The role of dendritic cells in food allergy. J Allergy Clin Immunol 2012;129:921–928.
16. Lambrecht BN, Hammad H. The immunology of asthma. Nat Immunol 2015;16:45–56.
17. Frischmeyer-Guerrerio PA, Guerrerio AL, Chichester KL, Bieneman AP, Hamilton RA, Wood RA et al. Dendritic cell and T cell responses in children with food allergy. Clin Exp Allergy 2011;41:61–71.
18. Idzko M, la Sala A, Ferrari D, Panther E, Herouy Y, Dichmann S et al. Expression and function of histamine receptors in human monocyte-derived dendritic cells. J Allergy Clin Immunol 2002;109:839–846.
19. Jutel M, Watanabe T, Klunker S, Akdis M, Thomet OA, Malolepszy J et al. Histamine regulates T-cell and antibody responses by differential expression of H1 and H2 receptors. Nature 2001;413:420–425.
20. Caron G, Delneste Y, Roelandts E, Duez C, Bonnefoy JY, Pestel J et al. Histamine polarizes human dendritic cells into Th2 cell-promoting effector dendritic cells. J Immunol 2001;167:3682–3686.
21. Gutzmer R, Diestel C, Mommert S, Köther B, Stark H, Wittmann M et al. Histamine H4 receptor stimulation suppresses IL-12p70 production and mediates chemotaxis in human monocyte-derived dendritic cells. J Immunol 2005;174:5224–5232.
22. Wang M, Ramirez J, Han J, Jia Y, Domenico J, Seibold MA et al. The steroidogenic enzyme Cyp11a1 is essential for development of peanut-induced intestinal anaphylaxis. J Allergy Clin Immunol 2013;132:1174–1183.
23. Cowden JM, Zhang M, Dunford PJ, Thurmond RL. The histamine H4 receptor mediates inflammation and pruritus in Th2-dependent dermal inflammation. J Invest Dermatol 2010;130:1023–1033.
24. Li XM, Serebrisky D, Lee SY, Huang CK, Bardina L, Schofield BH 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 2000;106:150–158.
25. Okamoto M, Matsuda H, Joetham A, Lucas JJ, Domenico J, Yasutomo K et al. Jagged1 on dendritic cells and Notch on CD4 + T cells initiate lung allergic responsiveness by inducing IL-4 production. J Immunol 2009;183:2995–3003.
26. Ohnishi H, Miyahara N, Dakhama A, Takeda K, Mathis S, Haribabu B et al. Corticosteroids enhance CD8 + T cell-mediated airway hyperresponsiveness and allergic inflammation by upregulating leukotriene B4 receptor 1. J Allergy Clin Immunol 2008;121:864–871.
27. González-Navajas JM, Fine S, Law J, Datta SK, Nguyen KP, Yu M et al. TLR4 signaling in effector CD4 + T cells regulates TCR activation and experimental colitis in mice. J Clin Invest 2010;120:570–581.
28. Chirdo FG, Millington OR, Beacock-Sharp H, Mowat AM. Immunomodulatory dendritic cells in intestinal lamina propria. Eur J Immunol 2005;35:1831–1840.
29. Hammad H, Lambrecht BN. Recent progress in the biology of airway dendritic cells and implications for understanding the regulation of asthmatic inflammation. J Allergy Clin Immunol 2006;118:331–336.
30. Smolinska S, Jutel M, Crameri R, O'Mahony L. Histamine and gut mucosal immune regulation. Allergy 2014;69:273–281.
31. Alcañiz L, Vega A, Chacón P, El Bekay R, Ventura I, Aroca R et al. Histamine production by human neutrophils. FASEB J 2013;27:2902–2910.
32. Kelly MT, Martin RR, White A. Mediators of histamine release from human platelets, lymphocytes, and granulocytes. J Clin Invest 1971;50:1044–1049.
33. Bryce PJ, Geha R, Oettgen HC. Desloratadine inhibits allergen-induced airway inflammation and bronchial hyperresponsiveness and alters T-cell responses in murine models of asthma. J Allergy Clin Immunol 2003;112:149–158.
34. Gelfand EW, Cui ZH, Takeda K, Kanehiro A, Joetham A. Fexofenadine modulates T cell function, preventing allergen-induced airway inflammation and hyperresponsiveness. J Allergy Clin Immunol 2002;110:85–95.
35. Dirksen A, Engel T, Frølund L, Heinig JH, Svendsen UG, Weeke B. Effect of a non-sedative antihistaminic (loratadine) in moderate asthma. A double-blind controlled clinical crossover-trial. Allergy 1989;44:566–571.
36. Thurmond RL, Desai PJ, Dunford PJ, Fung-Leung WP, Hofstra CL, Jiang W et al. A potent and selective histamine H4 receptor antagonist with anti-inflammatory properties. J Pharmacol Exp Ther 2004;309:404–413.
37. Cowden JM, Riley JP, Ma JY, Thurmond RL, Dunford PJ. Histamine H4 receptor antagonism diminishes existing airway inflammation and dysfunction via modulation of Th2 cytokines. Respir Res 2010;11:86–98.
38. Lin XP, Magnusson J, Ahlstedt S, Dahlman-Höglund A, LA Hanson L, Magnusson O et al. Local allergic reaction in food-hypersensitive adults despite a lack of systemic food-specific IgE. J Allergy Clin Immunol 2002;109:879–887.
39. Mazzoni A, Young HA, Spitzer JH, Visintin A, Segal DM. Histamine regulates cytokine production in maturing dendritic cells, resulting in altered T cell polarization. J Clin Invest 2001;108:1865–1873.
40. Rescigno M, Di Sabatino A. Dendritic cells in intestinal homeostasis and disease. J Clin Invest 2009;119:2441–2450.
41. Mowat AM. Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev Immunol 2003;3:331–341.
42. Coombes JL, Powrie F. Dendritic cells in intestinal immune regulation. Nat Rev Immunol 2008;8:435–446.
43. Sander LE, Lorentz A, Sellge G, Coëffier M, Neipp M, Veres T et al. Selective expression of histamine receptors H1R, H2R, and H4R, but not H3R, in the human intestinal tract. Gut 2006;55:498–504.
44. Frei R, Ferstl R, Konieczna P, Ziegler M, Simon T, Rugeles TM et al. Histamine receptor 2 modifies dendritic cell responses to microbial ligands. J Allergy Clin Immunol 2013;132:194–204.
45. Beermann S, Bernhardt G, Seifert R, Buschauer A, Neumann D. Histamine H(1)- and H(4)-receptor signaling cooperatively regulate MAPK activation. Biochem Pharmacol 2015;98:432–439.
46. Ramanathan R, Alvarez N, Su AD, Chowdhury S, Alton K, Stauber K et al. Metabolism and excretion of loratadine in male and female mice, rats and monkeys. Xenobiotica 2005;35:155–189.
47. Department of Chemical Engineering, Indian Institute of Technology Madras, Chennai, India
48. Zhang YF, Chen XY, Zhong DF, Dong YM. Pharmacokinetics of loratadine and its active metabolite descarboethoxyloratadine in healthy Chinese subjects. Acta Pharmacol Sin 2003;24:715–718.
49. Bäumer W, Wendorff S, Gutzmer R, Werfel T, Dijkstra D, Chazot P et al. Histamine H4 receptors modulate dendritic cell migration through skin–immunomodulatory role of histamine. Allergy 2008;63:1387–1394.
50. Wang M, Okamoto M, Domenico J, Han J, Ashino S, Shin YS et al. Inhibition of Pim1 kinase prevents peanut allergy by enhancing Runx3 expression and suppressing T(H)2 and T(H)17 T-cell differentiation. J Allergy Clin Immunol 2012;130:932–944.
51. Knight AK, Blázquez AB, Zhang S, Mayer L, Sampson HA, Berin MC. CD4 T cells activated in the mesenteric lymph node mediate gastrointestinal food allergy in mice. Am J Physiol Gastrointest Liver Physiol 2007;293:G1234–G1243.
52. Islam SA, Luster AD. T cell homing to epithelial barriers in allergic disease. Nat Med 2012;18:705–715.