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Type I Interferon Increases Inflammasomes Associated Pyroptosis in the Salivary Glands of Patients with Primary Sjögren's Syndrome

  • Seung-Min Hong (Rheumatism Research Center, Catholic Research Institute of Medical Science, College of Medicine, The Catholic University of Korea) ;
  • Jaeseon Lee (Rheumatism Research Center, Catholic Research Institute of Medical Science, College of Medicine, The Catholic University of Korea) ;
  • Se Gwang Jang (Rheumatism Research Center, Catholic Research Institute of Medical Science, College of Medicine, The Catholic University of Korea) ;
  • Jennifer Lee (Rheumatism Research Center, Catholic Research Institute of Medical Science, College of Medicine, The Catholic University of Korea) ;
  • Mi-La Cho (Rheumatism Research Center, Catholic Research Institute of Medical Science, College of Medicine, The Catholic University of Korea) ;
  • Seung-Ki Kwok (Rheumatism Research Center, Catholic Research Institute of Medical Science, College of Medicine, The Catholic University of Korea) ;
  • Sung-Hwan Park (Rheumatism Research Center, Catholic Research Institute of Medical Science, College of Medicine, The Catholic University of Korea)
  • Received : 2020.04.03
  • Accepted : 2020.08.21
  • Published : 2020.10.31
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Abstract

Sjögren's syndrome (SS) is a chronic and systemic autoimmune disease characterized by lymphocytic infiltration in the exocrine glands. In SS, type I IFN has a pathogenic role, and recently, inflammasome activation has been observed in both immune and non-immune cells. However, the relationship between type I IFN and inflammasome-associated pyroptosis in SS has not been studied. We measured IL-18, caspase-1, and IFN-stimulated gene 15 (ISG15) in saliva and serum, and compared whether the expression levels of inflammasome and pyroptosis components, including absent in melanoma 2 (AIM2), NLR family pyrin domain containing 3 (NLRP3), apoptosis-associated speck-like protein (ASC), caspase-1, gasdermin D (GSDMD), and gasdermin E (GSDME), in minor salivary gland (MSG) are related to the expression levels of type I IFN signature genes. Expression of type I IFN signature genes was correlated with mRNA levels of caspase-1 and GSDMD in MSG. In confocal analysis, the expression of caspase-1 and GSDMD was higher in salivary gland epithelial cells (SGECs) from SS patients. In the type I IFN-treated human salivary gland epithelial cell line, the expression of caspase-1 and GSDMD was increased, and pyroptosis was accelerated in a caspase-dependent manner upon inflammasome activation. In conclusion, we demonstrate that type I IFN may contribute to inflammasome-associated pyroptosis of the SGECs of SS patients, suggesting another pathogenic role of type I IFN in SS in terms of target tissue -SGECs destruction.

Keywords

Acknowledgement

We thank Edanz Group China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript. This study was supported by a grant from the Korean Health Technology R&D Project of the Ministry of Health & Welfare, Republic of Korea (HI13C0016), and the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (HI15C1062).

References

  1. Li H, Ice JA, Lessard CJ, Sivils KL. Interferons in Sjogren's syndrome: genes, mechanisms, and effects. Front Immunol 2013;4:290.
  2. Crow MK, Olferiev M, Kirou KA. Type I interferons in autoimmune disease. Annu Rev Pathol 2019;14:369-393. https://doi.org/10.1146/annurev-pathol-020117-043952
  3. Furumoto Y, Smith CK, Blanco L, Zhao W, Brooks SR, Thacker SG, Abdalrahman Z, Sciume G, Tsai WL, Trier AM, et al. Tofacitinib ameliorates murine lupus and its associated vascular dysfunction. Arthritis Rheumatol 2017;69:148-160. https://doi.org/10.1002/art.39818
  4. Lee J, Lee J, Kwok SK, Baek S, Jang SG, Hong SM, Min JW, Choi SS, Lee J, Cho ML, et al. JAK-1 inhibition suppresses interferon-induced BAFF production in human salivary gland: potential therapeutic strategy for primary Sjogren's syndrome. Arthritis Rheumatol 2018;70:2057-2066. https://doi.org/10.1002/art.40589
  5. Fragoulis GE, McInnes IB, Siebert S. JAK-inhibitors. New players in the field of immune-mediated diseases, beyond rheumatoid arthritis. Rheumatology (Oxford) 2019;58 :i43-i54. https://doi.org/10.1093/rheumatology/key276
  6. Kolb JP, Oguin TH 3rd, Oberst A, Martinez J. Programmed cell death and inflammation: winter is coming. Trends Immunol 2017;38:705-718. https://doi.org/10.1016/j.it.2017.06.009
  7. Deuteraiou K, Kitas G, Garyfallos A, Dimitroulas T. Novel insights into the role of inflammasomes in autoimmune and metabolic rheumatic diseases. Rheumatol Int 2018;38:1345-1354. https://doi.org/10.1007/s00296-018-4074-5
  8. Baldini C, Rossi C, Ferro F, Santini E, Seccia V, Donati V, Solini A. The P2X7 receptor-inflammasome complex has a role in modulating the inflammatory response in primary Sjogren's syndrome. J Intern Med 2013;274:480-489. https://doi.org/10.1111/joim.12115
  9. Niu L, Zhang S, Wu J, Chen L, Wang Y. Upregulation of nlrp3 inflammasome in the tears and ocular surface of dry eye patients. PLoS One 2015;10:e0126277.
  10. Baldini C, Santini E, Rossi C, Donati V, Solini A. The P2X7 receptor-NLRP3 inflammasome complex predicts the development of non-Hodgkin's lymphoma in Sjogren's syndrome: a prospective, observational, single-centre study. J Intern Med 2017;282:175-186. https://doi.org/10.1111/joim.12631
  11. Vakrakou AG, Boiu S, Ziakas PD, Xingi E, Boleti H, Manoussakis MN. Systemic activation of NLRP3 inflammasome in patients with severe primary Sjogren's syndrome fueled by inflammagenic DNA accumulations. J Autoimmun 2018;91:23-33. https://doi.org/10.1016/j.jaut.2018.02.010
  12. Vakrakou AG, Svolaki IP, Evangelou K, Gorgoulis VG, Manoussakis MN. Cell-autonomous epithelial activation of AIM2 (absent in melanoma-2) inflammasome by cytoplasmic DNA accumulations in primary Sjogren's syndrome. J Autoimmun 2020;108:102381.
  13. Liu J, Berthier CC, Kahlenberg JM. Enhanced inflammasome activity in systemic lupus erythematosus is mediated via type i interferon-induced up-regulation of interferon regulatory factor 1. Arthritis Rheumatol 2017;69:1840-1849. https://doi.org/10.1002/art.40166
  14. Kopitar-Jerala N. The role of interferons in inflammation and inflammasome activation. Front Immunol 2017;8:873.
  15. Man SM, Karki R, Malireddi RK, Neale G, Vogel P, Yamamoto M, Lamkanfi M, Kanneganti TD. The transcription factor IRF1 and guanylate-binding proteins target activation of the AIM2 inflammasome by Francisella infection. Nat Immunol 2015;16:467-475. https://doi.org/10.1038/ni.3118
  16. Guarda G, Braun M, Staehli F, Tardivel A, Mattmann C, Forster I, Farlik M, Decker T, Du Pasquier RA, Romero P, et al. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 2011;34:213-223. https://doi.org/10.1016/j.immuni.2011.02.006
  17. Vitali C, Bombardieri S, Jonsson R, Moutsopoulos HM, Alexander EL, Carsons SE, Daniels TE, Fox PC, Fox RI, Kassan SS, et al. Classification criteria for Sjogren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis 2002;61:554-558. https://doi.org/10.1136/ard.61.6.554
  18. Shiboski SC, Shiboski CH, Criswell L, Baer A, Challacombe S, Lanfranchi H, Schiodt M, Umehara H, Vivino F, Zhao Y, et al. American College of Rheumatology classification criteria for Sjogren's syndrome: a data-driven, expert consensus approach in the Sjogren's International Collaborative Clinical Alliance cohort. Arthritis Care Res (Hoboken) 2012;64:475-487. https://doi.org/10.1002/acr.21591
  19. D'Cunha J, Ramanujam S, Wagner RJ, Witt PL, Knight E Jr, Borden EC. In vitro and in vivo secretion of human ISG15, an IFN-induced immunomodulatory cytokine. J Immunol 1996;157:4100-4108. https://doi.org/10.4049/jimmunol.157.9.4100
  20. Lin LC, Elkashty O, Ramamoorthi M, Trinh N, Liu Y, Sunavala-Dossabhoy G, Pranzatelli T, Michael DG, Chivasso C, Perret J, et al. Cross-contamination of the human salivary gland HSG cell line with HeLa cells: a STR analysis study. Oral Dis 2018;24:1477-1483. https://doi.org/10.1111/odi.12920
  21. Liu T, Tang Q, Liu K, Xie W, Liu X, Wang H, Wang RF, Cui J. TRIM11 suppresses AIM2 inflammasome by degrading AIM2 via p62-dependent selective autophagy. Cell Reports 2016;16:1988-2002. https://doi.org/10.1016/j.celrep.2016.07.019
  22. Yang F, Lou G, Zhou X, Zheng M, He J, Chen Z. MicroRNA-223 acts as an important regulator to Kupffer cells activation at the early stage of Con A-induced acute liver failure via AIM2 signaling pathway. Cell Physiol Biochem 2014;34:2137-2152. https://doi.org/10.1159/000369658
  23. Chen L, Song Y, He L, Wan X, Lai L, Dai F, Liu Y, Wang Q. MicroRNA-223 promotes type I interferon production in antiviral innate immunity by targeting forkhead box protein O3 (FOXO3). J Biol Chem 2016;291:14706-14716. https://doi.org/10.1074/jbc.M115.700252
  24. Gurung P, Kanneganti TD. Novel roles for caspase-8 in IL-1β and inflammasome regulation. Am J Pathol 2015;185:17-25. https://doi.org/10.1016/j.ajpath.2014.08.025
  25. Yu J, Li S, Qi J, Chen Z, Wu Y, Guo J, Wang K, Sun X, Zheng J. Cleavage of GSDME by caspase-3 determines lobaplatin-induced pyroptosis in colon cancer cells. Cell Death Dis 2019;10:193.
  26. Sarhan J, Liu BC, Muendlein HI, Li P, Nilson R, Tang AY, Rongvaux A, Bunnell SC, Shao F, Green DR, et al. Caspase-8 induces cleavage of gasdermin D to elicit pyroptosis during Yersinia infection. Proc Natl Acad Sci U S A 2018;115:E10888-E10897. https://doi.org/10.1073/pnas.1809548115
  27. Taabazuing CY, Okondo MC, Bachovchin DA. Pyroptosis and apoptosis pathways engage in bidirectional crosstalk in monocytes and macrophages. Cell Chem Biol 2017;24:507-514.e4.  https://doi.org/10.1016/j.chembiol.2017.03.009
  28. Li Y, Guo X, Hu C, Du Y, Guo C, Di Wang , Zhao W, Huang G, Li C, Lu Q, et al. Type I IFN operates pyroptosis and necroptosis during multidrug-resistant A. baumannii infection. Cell Death Differ 2018;25:1304-1318. https://doi.org/10.1038/s41418-017-0041-z
  29. Kayagaki N, Lee BL, Stowe IB, Kornfeld OS, O'Rourke K, Mirrashidi KM, Haley B, Watanabe C, RooseGirma M, Modrusan Z, et al. IRF2 transcriptionally induces GSDMD expression for pyroptosis. Sci Signal 2019;12:eaax4917.
  30. Duan X, Ponomareva L, Veeranki S, Panchanathan R, Dickerson E, Choubey D. Differential roles for the interferon-inducible IFI16 and AIM2 innate immune sensors for cytosolic DNA in cellular senescence of human fibroblasts. Mol Cancer Res 2011;9:589-602. https://doi.org/10.1158/1541-7786.MCR-10-0565
  31. Man SM, Karki R, Kanneganti TD. Molecular mechanisms and functions of pyroptosis, inflammatory caspases and inflammasomes in infectious diseases. Immunol Rev 2017;277:61-75. https://doi.org/10.1111/imr.12534
  32. Ma Y, Jiang J, Gao Y, Shi T, Zhu X, Zhang K, Lu K, Xue B. Research progress of the relationship between pyroptosis and disease. Am J Transl Res 2018;10:2213-2219.
  33. Li Y, Shen Y, Jin K, Wen Z, Cao W, Wu B, Wen R, Tian L, Berry GJ, Goronzy JJ, et al. The DNA repair nuclease MRE11A functions as a mitochondrial protector and prevents T cell pyroptosis and tissue inflammation. Cell Metab 2019;30:477-492.e6. https://doi.org/10.1016/j.cmet.2019.06.016
  34. Faliti CE, Gualtierotti R, Rottoli E, Gerosa M, Perruzza L, Romagnani A, Pellegrini G, De Ponte Conti B, Rossi RL, Idzko M, et al. P2X7 receptor restrains pathogenic Tfh cell generation in systemic lupus erythematosus. J Exp Med 2019;216:317-336.  https://doi.org/10.1084/jem.20171976