Interleukin-13 partly induced by the NLRP3 inflammasome promotes Trichinella spiralis encapsulation in infected mice

Xuanrui Liu; Bo Zhang; Zhiyuan Zhang; Xueting Wang; Tongxuan Zhang; Haibin Huang; Chunwei Shi; Wentao Yang; Yanlong Jiang; Xin Cao; Jianzhong Wang; Yan Zeng; Chunfeng Wang; Nan Wang; Guilian Yang

doi:10.1016/j.vetpar.2024.110386

Interleukin-13 partly induced by the NLRP3 inflammasome promotes Trichinella spiralis encapsulation in infected mice

Vet Parasitol. 2024 Dec 25:334:110386. doi: 10.1016/j.vetpar.2024.110386. Online ahead of print.

Authors

Xuanrui Liu¹, Bo Zhang², Zhiyuan Zhang³, Xueting Wang⁴, Tongxuan Zhang⁵, Haibin Huang⁶, Chunwei Shi⁷, Wentao Yang⁸, Yanlong Jiang⁹, Xin Cao¹⁰, Jianzhong Wang¹¹, Yan Zeng¹², Chunfeng Wang¹³, Nan Wang¹⁴, Guilian Yang¹⁵

Affiliations

¹ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
² College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
³ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
⁴ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
⁵ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
⁶ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
⁷ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
⁸ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
⁹ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
¹⁰ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
¹¹ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
¹² College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
¹³ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
¹⁴ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].
¹⁵ College of Veterinary Medicine, Jilin Agricultural University, Changchun 130118, China; Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun 130118, China; Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun 130118, China. Electronic address: [email protected].

PMID: 39732108
DOI: 10.1016/j.vetpar.2024.110386

Abstract

Trichinella spiralis infection is a serious parasitic zoonosis in which a collagenous capsule surrounding the larva is developed in the striated muscle cells. However, the mechanism of T. spiralis encapsulation is currently poorly understood. It has been reported that T. spiralis infection can induce the production of IL-13 via the NLRP3 inflammasome, and it has also been suggested IL-13 thus produced may be involved in T. spiralis encapsulation. This research aimed to clarify the involvement of NLRP3 and IL-13 in the T. spiralis capsule formation process. IL-13 and NLRP3 inhibitors were used in a T. spiralis infected mouse model and in C₂C₁₂ cells to analyze the role of IL-13 and NLRP3 in encapsulation. The results showed that T. spiralis infection significantly increased the expression levels of IL-13 and collagen IV and VI. The production of collagen around the T. spiralis encapsulation zone was significantly inhibited when an IL-13 inhibitor was applied. Moreover, the expression levels of IL-13 and collagen IV and VI were significantly decreased by the NLRP3 inhibitor in vitro and in vivo. The above results indicated that NLRP3 can participate in the development of T. spiralis encapsulation by regulating IL-13 expression and stimulating collagen IV and VI synthesis during T. spiralis infection.

Keywords: Collagen; Encapsulation; IL-13; NLRP3; Trichinella spiralis.