Interleukin 1β Mediates the Pathogenesis of Nasal Mucosal Epithelial Barrier Dysfunction in Allergic Rhinitis

Hanrui Wang; Xiaoyu Song; Yao Wang; Ting Yang; Wanchen Liu; Yakui Mou; Chao Ren; Xicheng Song

doi:10.2147/JIR.S488340

Interleukin 1β Mediates the Pathogenesis of Nasal Mucosal Epithelial Barrier Dysfunction in Allergic Rhinitis

J Inflamm Res. 2024 Nov 19:17:9071-9085. doi: 10.2147/JIR.S488340. eCollection 2024.

Authors

Hanrui Wang^#^{1

2

3

4}, Xiaoyu Song^#^{1

2

3

4}, Yao Wang^{1

2

3

4}, Ting Yang^{1

2

3

4}, Wanchen Liu^{1

2

3

4}, Yakui Mou^#^{1

2

3

4}, Chao Ren^{1

2

3

4

5}, Xicheng Song^{1

2

3

4}

Affiliations

¹ Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao University, Yantai, People's Republic of China.
² Shandong Provincial Key Laboratory of Neuroimmune Interaction and Regulation, Yantai Yuhuangding Hospital, Yantai, People's Republic of China.
³ Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, People's Republic of China.
⁴ Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Qingdao University, Yantai, People's Republic of China.
⁵ Department of Neurology, Yantai Yuhuangding Hospital, Qingdao University, Yantai, People's Republic of China.

^# Contributed equally.

Abstract

Background: The nasal mucosal epithelial barrier is the primary site of allergic rhinitis (AR). Interleukin-1β (IL-1β), as a crucial factor in immune inflammation, not only plays a crucial role in hypersensitivity reactions but also affects the digestive mucosa and skin epithelial barrier. However, the role of IL-1β in the nasal mucosal epithelial barrier in AR has not been reported, and this study aimed to investigate the effect and possible mechanisms involved.

Methods: Dermatophagoides pteronyssinus 1 was used as an allergen to construct an AR mouse model and stimulate human nasal mucosal epithelial cells (HNEpCs) and observe the expression changes of IL-1β and epithelial barrier indicators CLDN1 and OCLN in mouse nasal mucosa and HNEpCs. Then, the possible mechanisms of action were explored via exogenous IL-1β stimulation and pharmacological inhibition of IL-1β or its receptor interleukin-1 receptor type 1 (IL-1R1).

Results: The results showed that Dermatophagoides pteronyssinus 1-primed mouse nasal mucosa or human HENpCs had increased expression of IL-1β and decreased CLDN1 and OCLN, and IL-1β could directly lead to reduced expression of epithelial barrier indexes in HNEpCs. In addition, inhibition of IL-1β or IL-1R1 can effectively alleviate the damage to the epithelial barrier.

Conclusion: IL-1β has a destructive effect on the nasal mucosal epithelial barrier in AR, and inhibition of IL-1β or its receptor IL-1R1 can effectively protect the nasal mucosal barrier. IL-1β is a potential target for the treatment of AR.

Keywords: DerP1; allergic rhinitis; epithelial barrier; interleukin-1β; nasal mucous membrane.

Grants and funding

This work was supported by the National Natural Science Foundation of China (82371119, 82271146, 82071021); the Natural Science Foundation of Shandong Province (ZR2024MH034); the Key Research and Development Program of Shandong Province (Major Science and Technology Innovation Project: 2022CXGC020506; Competitive Innovation Platform Project: no. 2024CXPT091); the Taishan Scholar Project (NO. tsqn202312392); Shandong Provincial Postdoctoral Foundation Project (Innovation Project; SDCX-ZG-202203077); Science and Technology Innovation development plan of Yantai (2023ZDCX033); the Outstanding Young Talents Project in Health of Qilu and the youth talent training program from Qingdao medical college of Qingdao University (No. RZ2300002690).