Interleukin-33 Produced by M2 Macrophages and Other Immune Cells Contributes to Th2 Immune Reaction of IgG4-related Disease

Overview

Journal Sci Rep

Specialty Science

Date 2017 Feb 17

PMID 28205524

Citations 55

Authors

Sachiko Furukawa

Masafumi Moriyama

Kensuke Miyake

Hitoshi Nakashima

Akihiko Tanaka

Takashi Maehara

Mana Iizuka-Koga

Hiroto Tsuboi

Jun-Nosuke Hayashida

Noriko Ishiguro

Masaki Yamauchi

Takayuki Sumida

Seiji Nakamura

Affiliations

Soon will be listed here.

Abstract

IgG4-related disease (IgG4-RD) is characterized by elevated serum IgG4 and marked infiltration of IgG4-positive cells in multiple organs. Interleukin-33 (IL-33) is a recently described cytokine that is secreted by damaged epithelial cells, macrophages, and dendritic cells, and potently activates helper T type 2 (Th2) immune responses, which have been suggested to play a major role in IgG4 production of IgG4-RD. Here, we assessed the expression of IL-33 and related molecules in the salivary glands (SGs) of patients with IgG4-RD versus that in patients with Sjögren's syndrome (SS) and controls. Expression of IL-33 and its receptor (ST2) was strongly detected around ectopic germinal centers (GCs) in the SGs from patients with IgG4-RD, whereas IL-33 was expressed only in epithelial cells in patients with SS and controls. Moreover, IL-33 and CD68/CD163 macrophages were mainly distributed around ectopic GCs in patients with IgG4-RD. Double immunofluorescence staining showed that IL-33 expression co-localized with CD68/CD163 macrophages. Finally, mRNA expression levels of IL-33 showed a positive correlation to those of Th2 cytokines (IL-4 and IL-13) in patients with IgG4-RD. Our data suggest that IL-33 produced by M2 macrophages might contribute to the pathogenesis of IgG4-RD via aberrant activation of Th2 immune responses.

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References

Awada A, Nicaise C, Ena S, Schandene L, Rasschaert J, Popescu I . Potential involvement of the IL-33-ST2 axis in the pathogenesis of primary Sjogren's syndrome. Ann Rheum Dis. 2014; 73(6):1259-63. DOI: 10.1136/annrheumdis-2012-203187. View

Martinez F, Gordon S . The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 2014; 6:13. PMC: 3944738. DOI: 10.12703/P6-13. View

Maria N, Steenwijk E, IJpma A, van Helden-Meeuwsen C, Vogelsang P, Beumer W . Contrasting expression pattern of RNA-sensing receptors TLR7, RIG-I and MDA5 in interferon-positive and interferon-negative patients with primary Sjögren's syndrome. Ann Rheum Dis. 2016; 76(4):721-730. DOI: 10.1136/annrheumdis-2016-209589. View

Louten J, Rankin A, Li Y, Murphy E, Beaumont M, Moon C . Endogenous IL-33 enhances Th2 cytokine production and T-cell responses during allergic airway inflammation. Int Immunol. 2011; 23(5):307-15. DOI: 10.1093/intimm/dxr006. View

Tsuboi H, Nakai Y, Iizuka M, Asashima H, Hagiya C, Tsuzuki S . DNA microarray analysis of labial salivary glands in IgG4-related disease: comparison with Sjögren's syndrome. Arthritis Rheumatol. 2014; 66(10):2892-9. DOI: 10.1002/art.38748. View

Moriyama M, Hayashida J, Toyoshima T, Ohyama Y, Shinozaki S, Tanaka A . Cytokine/chemokine profiles contribute to understanding the pathogenesis and diagnosis of primary Sjögren's syndrome. Clin Exp Immunol. 2012; 169(1):17-26. PMC: 3390469. DOI: 10.1111/j.1365-2249.2012.04587.x. View

Zen Y, Fujii T, Harada K, Kawano M, Yamada K, Takahira M . Th2 and regulatory immune reactions are increased in immunoglobin G4-related sclerosing pancreatitis and cholangitis. Hepatology. 2007; 45(6):1538-46. DOI: 10.1002/hep.21697. View

Yamamoto M, Takahashi H, Sugai S, Imai K . Clinical and pathological characteristics of Mikulicz's disease (IgG4-related plasmacytic exocrinopathy). Autoimmun Rev. 2005; 4(4):195-200. DOI: 10.1016/j.autrev.2004.10.005. View

Jing J, Yang I, Hui L, Patel J, Evans C, Prikeris R . Role of macrophage receptor with collagenous structure in innate immune tolerance. J Immunol. 2013; 190(12):6360-7. PMC: 3679202. DOI: 10.4049/jimmunol.1202942. View

10.

Maehara T, Moriyama M, Nakashima H, Miyake K, Hayashida J, Tanaka A . Interleukin-21 contributes to germinal centre formation and immunoglobulin G4 production in IgG4-related dacryoadenitis and sialoadenitis, so-called Mikulicz's disease. Ann Rheum Dis. 2012; 71(12):2011-19. DOI: 10.1136/annrheumdis-2012-201477. View

11.

Kamekura R, Kojima T, Takano K, Go M, Sawada N, Himi T . The role of IL-33 and its receptor ST2 in human nasal epithelium with allergic rhinitis. Clin Exp Allergy. 2012; 42(2):218-28. DOI: 10.1111/j.1365-2222.2011.03867.x. View

12.

Stone J, Chan J, Deshpande V, Okazaki K, Umehara H, Zen Y . IgG4-Related Disease. Int J Rheumatol. 2013; 2013:532612. PMC: 3562585. DOI: 10.1155/2013/532612. View

13.

Mattoo H, Mahajan V, Maehara T, Deshpande V, Della-Torre E, Wallace Z . Clonal expansion of CD4(+) cytotoxic T lymphocytes in patients with IgG4-related disease. J Allergy Clin Immunol. 2016; 138(3):825-838. PMC: 5014627. DOI: 10.1016/j.jaci.2015.12.1330. View

14.

Vitali C, Bombardieri S, Jonsson R, Moutsopoulos H, Alexander E, Carsons S . Classification criteria for Sjögren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis. 2002; 61(6):554-8. PMC: 1754137. DOI: 10.1136/ard.61.6.554. View

15.

Miyake K, Moriyama M, Aizawa K, Nagano S, Inoue Y, Sadanaga A . Peripheral CD4+ T cells showing a Th2 phenotype in a patient with Mikulicz's disease associated with lymphadenopathy and pleural effusion. Mod Rheumatol. 2007; 18(1):86-90. DOI: 10.1007/s10165-007-0010-3. View

16.

Zhao J, Kubo S, Nakayamada S, Shimajiri S, Zhang X, Yamaoka K . Association of plasmacytoid dendritic cells with B cell infiltration in minor salivary glands in patients with Sjögren's syndrome. Mod Rheumatol. 2015; 26(5):716-24. DOI: 10.3109/14397595.2015.1129694. View

17.

Murthy S, Larson-Casey J, Ryan A, He C, Kobzik L, Carter A . Alternative activation of macrophages and pulmonary fibrosis are modulated by scavenger receptor, macrophage receptor with collagenous structure. FASEB J. 2015; 29(8):3527-36. PMC: 4511206. DOI: 10.1096/fj.15-271304. View

18.

Maehara T, Mattoo H, Ohta M, Mahajan V, Moriyama M, Yamauchi M . Lesional CD4+ IFN-γ+ cytotoxic T lymphocytes in IgG4-related dacryoadenitis and sialoadenitis. Ann Rheum Dis. 2016; 76(2):377-385. PMC: 5435236. DOI: 10.1136/annrheumdis-2016-209139. View

19.

Fukui Y, Uchida K, Sakaguchi Y, Fukui T, Nishio A, Shikata N . Possible involvement of Toll-like receptor 7 in the development of type 1 autoimmune pancreatitis. J Gastroenterol. 2014; 50(4):435-44. DOI: 10.1007/s00535-014-0977-4. View

20.

Maehara T, Moriyama M, Hayashida J, Tanaka A, Shinozaki S, Kubo Y . Selective localization of T helper subsets in labial salivary glands from primary Sjögren's syndrome patients. Clin Exp Immunol. 2012; 169(2):89-99. PMC: 3406368. DOI: 10.1111/j.1365-2249.2012.04606.x. View