Helminth-induced impairment of humoral immunity differently contribute to their anti-arthritic effects in mice: Comparison of Schistosoma mansoni and Trichinella spiralis

Yoshio Osada; Shoichi Shimizu; Kentaro Morita; Eman M Gaballah; Zhiliang Wu; Yoichi Maekawa

doi:10.1016/j.exppara.2024.108752

Helminth-induced impairment of humoral immunity differently contribute to their anti-arthritic effects in mice: Comparison of Schistosoma mansoni and Trichinella spiralis

Exp Parasitol. 2024 Apr 9:261:108752. doi: 10.1016/j.exppara.2024.108752. Online ahead of print.

Authors

Yoshio Osada¹, Shoichi Shimizu², Kentaro Morita², Eman M Gaballah³, Zhiliang Wu⁴, Yoichi Maekawa⁵

Affiliations

¹ Department of Immunology and Parasitology, University of Occupational and Environmental Health, Japan, 1-1, Iseigaoka, Yahatanishi-ku, Kitakyushu, 807-8555, Japan. Electronic address: yosada@med.uoeh-u.ac.jp.
² Department of Immunology and Parasitology, University of Occupational and Environmental Health, Japan, 1-1, Iseigaoka, Yahatanishi-ku, Kitakyushu, 807-8555, Japan.
³ Department of Immunology and Parasitology, University of Occupational and Environmental Health, Japan, 1-1, Iseigaoka, Yahatanishi-ku, Kitakyushu, 807-8555, Japan; Department of Medical Parasitology, Faculty of Medicine, Damietta University, Damietta, Egypt.
⁴ Department of Parasitology and Infectious Diseases, Gifu University Graduate School of Medicine, 1-1, Yanagito, Gifu, 501-1194, Japan.
⁵ Department of Parasitology and Infectious Diseases, Gifu University Graduate School of Medicine, 1-1, Yanagito, Gifu, 501-1194, Japan; Division of Preemptive Food Research, Preemptive Food Research Center (PFRC), Gifu University Institute for Advanced Study (GUiAS), 1-1 Yanagido, Gifu, 501-1193, Japan; Division of Animal Medical Science, Center for One Medicine Innovative Translational Research (COMIT), Gifu University Institute for Advanced Study (GUiAS), 1-1 Yanagido, Gifu, 501-1193, Japan.

PMID: 38604301
DOI: 10.1016/j.exppara.2024.108752

Abstract

Aims: We have previously reported reduction of anti-type II collagen (IIC) IgG levels in collagen-induced arthritis (CIA) by Schistosoma mansoni (Sm) and Trichinella spiralis (Ts). To clarify the contribution of the impairment of humoral immunity to their anti-arthritic activities, we herein investigated the relationship between anti-IIC IgG levels and arthritic swelling in Sm- or Ts-infected mice.

Methods and results: Male DBA/1J mice were infected with Sm cercariae or Ts muscle larvae prior to the IIC immunization. In the Sm-infected mice, paw swelling and anti-IIC IgG levels were continuously lower than those of non-infected control group. In contrast, arthritic swelling in the Ts-infected mice only decreased in the early phase of CIA progression, despite the continued impairment of anti-IIC IgG production throughout the experimental period. Correlation coefficients between residual paw swelling and anti-IIC IgG titers were similar or higher in the Sm group than in the control group, but were similar or lower in the Ts group than in the control group.

Conclusion: The down-modulations of anti-IIC IgG levels by the two parasitic infections and the correlation analyses suggest that the anti-arthritic activity of Sm was primarily attributed to the modulation of IgG-independent arthritogenic mechanisms and secondarily to the impairment of anti-IIC IgG production. In contrast, Ts could alleviate CIA mainly via the impairment of antibody production.

Keywords: Collagen-induced arthritis; Humoral immunity; IgG; Schistosoma mansoni; Trichinella spiralis.