The H1 Histamine Receptor Regulates Allergic Lung Responses

Overview

Journal J Clin Invest

Specialty General Medicine

Date 2006 May 9

PMID 16680192

Citations 52

Authors

Paul J Bryce

Clinton B Mathias

Krista L Harrison

Takeshi Watanabe

Raif S Geha

Hans C Oettgen

Affiliations

Soon will be listed here.

Abstract

Histamine, signaling via the type 1 receptor (H1R), has been shown to suppress Th2 cytokine production by in vitro cultured T cells. We examined the role of H1R in allergic inflammation in vivo using a murine asthma model. Allergen-stimulated splenic T cells from sensitized H1R-/- mice exhibited enhanced Th2 cytokine production. Despite this Th2 bias, allergen-challenged H1R-/- mice exhibited diminished lung Th2 cytokine mRNA levels, airway inflammation, goblet cell metaplasia, and airway hyperresponsiveness (AHR). Restoration of pulmonary Th2 cytokines in H1R-/- mice by intranasal IL-4 or IL-13 restored inflammatory lung responses and AHR. Further investigation revealed that histamine acts as a T cell chemotactic factor and defective T cell trafficking was responsible for the absence of lung inflammation. Cultured T cells migrated in response to histamine in vitro, but this was ablated by blockade of H1R but not H2R. In vivo, allergen-specific WT but not H1R-/- CD4+ T cells were recruited to the lungs of naive recipients following inhaled allergen challenge. H1R-/- T cells failed to confer airway inflammation or AHR observed after transfer of WT T cells. Our data establish a role for histamine and H1R in promoting the migration of Th2 cells into sites of allergen exposure.

Citing Articles

CD226 implicated in Akt-dependent apoptosis of CD4 T cell contributes to asthmatic pathogenesis.

Zhang Y, Xie Y, Zhang X, Duan C, Ma J, Wang Y Cell Death Dis. 2024; 15(9):705.

PMID: 39349422 PMC: 11442704. DOI: 10.1038/s41419-024-07080-z.

The histamine receptor H1 acts as an alternative receptor for SARS-CoV-2.

Yu F, Liu X, Ou H, Li X, Liu R, Lv X mBio. 2024; 15(8):e0108824.

PMID: 38953634 PMC: 11324024. DOI: 10.1128/mbio.01088-24.

Gut-lung axis and asthma: A historical review on mechanism and future perspective.

Song X, Liang J, Lin S, Xie Y, Ke C, Ao D Clin Transl Allergy. 2024; 14(5):e12356.

PMID: 38687096 PMC: 11060082. DOI: 10.1002/clt2.12356.

Intestinal Helminth Infection Impairs Oral and Parenteral Vaccine Efficacy.

Zhang Y, Hardy L, Kapita C, Hall J, Arbeeva L, Campbell E J Immunol. 2023; 211(3):389-402.

PMID: 37272847 PMC: 10524302. DOI: 10.4049/jimmunol.2300084.

Relationship between antidepressants and severity of SARS-CoV-2 Omicron infection: a retrospective cohort study using real-world data.

Wang H, Wei Y, Hung C, Jiang X, Li C, Jia K Lancet Reg Health West Pac. 2023; 34:100716.

PMID: 37256206 PMC: 9970034. DOI: 10.1016/j.lanwpc.2023.100716.

References

Broide D, Gleich G, Cuomo A, Coburn D, Federman E, Schwartz L . Evidence of ongoing mast cell and eosinophil degranulation in symptomatic asthma airway. J Allergy Clin Immunol. 1991; 88(4):637-48. DOI: 10.1016/0091-6749(91)90158-k. View

Banu Y, Watanabe T . Augmentation of antigen receptor-mediated responses by histamine H1 receptor signaling. J Exp Med. 1999; 189(4):673-82. PMC: 2192933. DOI: 10.1084/jem.189.4.673. View

Hofstra C, Desai P, Thurmond R, Fung-Leung W . Histamine H4 receptor mediates chemotaxis and calcium mobilization of mast cells. J Pharmacol Exp Ther. 2003; 305(3):1212-21. DOI: 10.1124/jpet.102.046581. View

Wills-Karp M, Luyimbazi J, Xu X, Schofield B, Neben T, Karp C . Interleukin-13: central mediator of allergic asthma. Science. 1998; 282(5397):2258-61. DOI: 10.1126/science.282.5397.2258. View

Krouwels F, Hol B, Lutter R, Bruinier B, Bast A, Jansen H . Histamine affects interleukin-4, interleukin-5, and interferon-gamma production by human T cell clones from the airways and blood. Am J Respir Cell Mol Biol. 1998; 18(5):721-30. DOI: 10.1165/ajrcmb.18.5.2909. View

Schroeder J, Schleimer R, Lichtenstein L, Kreutner W . Inhibition of cytokine generation and mediator release by human basophils treated with desloratadine. Clin Exp Allergy. 2001; 31(9):1369-77. DOI: 10.1046/j.1365-2222.2001.01130.x. View

Yang M, Hogan S, Henry P, Matthaei K, McKenzie A, Young I . Interleukin-13 mediates airways hyperreactivity through the IL-4 receptor-alpha chain and STAT-6 independently of IL-5 and eotaxin. Am J Respir Cell Mol Biol. 2001; 25(4):522-30. DOI: 10.1165/ajrcmb.25.4.4620. View

Robinson D, Hamid Q, Bentley A, Ying S, Kay A, Durham S . Activation of CD4+ T cells, increased TH2-type cytokine mRNA expression, and eosinophil recruitment in bronchoalveolar lavage after allergen inhalation challenge in patients with atopic asthma. J Allergy Clin Immunol. 1993; 92(2):313-24. DOI: 10.1016/0091-6749(93)90175-f. View

Okada C, Eda R, Miyagawa H, Sugiyama H, Hopp R, Bewtra A . Effect of cetirizine on human eosinophil superoxide generation, eosinophil chemotaxis and eosinophil peroxidase in vitro. Int Arch Allergy Immunol. 1994; 103(4):384-90. DOI: 10.1159/000236658. View

10.

Robinson D, Hamid Q, Ying S, Tsicopoulos A, Barkans J, Bentley A . Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N Engl J Med. 1992; 326(5):298-304. DOI: 10.1056/NEJM199201303260504. View

11.

Finkelman F, Katona I, Urban Jr J, Holmes J, OHara J, Tung A . IL-4 is required to generate and sustain in vivo IgE responses. J Immunol. 1988; 141(7):2335-41. View

12.

Sirois J, Menard G, Moses A, Bissonnette E . Importance of histamine in the cytokine network in the lung through H2 and H3 receptors: stimulation of IL-10 production. J Immunol. 2000; 164(6):2964-70. DOI: 10.4049/jimmunol.164.6.2964. View

13.

Carlsson R, Dohlsten M, Sjogren H . Histamine modulates the production of interferon-gamma and interleukin-2 by mitogen-activated human mononuclear blood cells. Cell Immunol. 1985; 96(1):104-12. DOI: 10.1016/0008-8749(85)90343-0. View

14.

Dy M, Schneider E . Histamine-cytokine connection in immunity and hematopoiesis. Cytokine Growth Factor Rev. 2004; 15(5):393-410. DOI: 10.1016/j.cytogfr.2004.06.003. View

15.

Miyahara N, Swanson B, Takeda K, Taube C, Miyahara S, Kodama T . Effector CD8+ T cells mediate inflammation and airway hyper-responsiveness. Nat Med. 2004; 10(8):865-9. DOI: 10.1038/nm1081. View

16.

Venkayya R, Lam M, Willkom M, Grunig G, Corry D, Erle D . The Th2 lymphocyte products IL-4 and IL-13 rapidly induce airway hyperresponsiveness through direct effects on resident airway cells. Am J Respir Cell Mol Biol. 2002; 26(2):202-8. DOI: 10.1165/ajrcmb.26.2.4600. View

17.

Inoue I, Yanai K, Kitamura D, Taniuchi I, Kobayashi T, Niimura K . Impaired locomotor activity and exploratory behavior in mice lacking histamine H1 receptors. Proc Natl Acad Sci U S A. 1996; 93(23):13316-20. PMC: 24090. DOI: 10.1073/pnas.93.23.13316. View

18.

Ma R, Gao J, Meeker N, Fillmore P, Tung K, Watanabe T . Identification of Bphs, an autoimmune disease locus, as histamine receptor H1. Science. 2002; 297(5581):620-3. DOI: 10.1126/science.1072810. View

19.

Temann U, Ray P, Flavell R . Pulmonary overexpression of IL-9 induces Th2 cytokine expression, leading to immune pathology. J Clin Invest. 2002; 109(1):29-39. PMC: 150821. DOI: 10.1172/JCI13696. View

20.

Seto Y, Nakajima H, Suto A, Shimoda K, Saito Y, Nakayama K . Enhanced Th2 cell-mediated allergic inflammation in Tyk2-deficient mice. J Immunol. 2003; 170(2):1077-83. DOI: 10.4049/jimmunol.170.2.1077. View