PD-1-dependent therapeutic effect of Trichinella spiralis cystatin on myocardial infarction in a mice model

Abstract Background Ischemia-induced inflammation is the primary pathological mechanism underlying cardiac tissue injury caused by myocardial infarction (MI). Trichinella spiralis cystatin (Ts-Cys) has been shown to regulate macrophage polarization and alleviate various inflammatory and immune-relat...

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Main Authors: Weixiao Zhang, Wenhui Yin, Hongtao Wang, Lingqin Wu, Chang Li, Xinyu Peng, Xiang Li, Kaibo Jiang, Huiqi Yang, Chenyue Dang, Erhe Gao, Qiwang Jin, Xiaodi Yang
Format: Article
Language:English
Published: BMC 2025-06-01
Series:Parasites & Vectors
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Online Access:https://doi.org/10.1186/s13071-025-06854-4
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Summary:Abstract Background Ischemia-induced inflammation is the primary pathological mechanism underlying cardiac tissue injury caused by myocardial infarction (MI). Trichinella spiralis cystatin (Ts-Cys) has been shown to regulate macrophage polarization and alleviate various inflammatory and immune-related diseases. Programmed cell death-1 (PD-1) is a crucial checkpoint receptor molecule and highly involved in maintaining immune tolerance. In this study, our aims were to investigate whether recombinant Ts-Cys protein (rTs-Cys) could be used to treat MI with recruited macrophage-dominant myocardial inflammation and whether PD-1 is involved in the immunomodulation of Ts-Cys in inflammatory diseases. Methods MI models were established in wild-type (WT) and PD-1 knockout (PD-1−/−) mice, followed by the intraperitoneal injection of rTs-Cys. The survival rates of mice were observed for 28 days post-surgery and treatment. Cardiac function was assessed by echocardiography. Histopathological evaluation of heart tissue affected by infarction was conducted to examine local inflammatory cell infiltration and cardiac tissue damage. Real-time quantitative PCR was used to detect messenger RNA expression levels of vascular endothelial growth factor (VEGF) and the macrophage surface markers inducible nitric oxide synthase and arginase-1 in the MI area. Serological levels of cytokines, including tumor necrosis factor-alpha (TNF-α), interleukin-6 (IL-6), interleukin-10 (IL-10) and transforming growth factor-beta (TGF-β), were measured using an enzyme-linked immunosorbent assay. Bone marrow-derived macrophages from WT and PD-1−/− mice were used to assess the effects of rTs-Cys on macrophage polarization in vitro. Results In WT mice, rTs-Cys treatment significantly improved the 28-day survival rate and cardiac function, reduced local inflammatory cell infiltration and cardiac pathological damage and increased VEGF expression levels of MI mice. The therapeutic effect of rTs-Cys was associated with macrophage polarization from the pro-inflammatory M1 phenotype to the regulatory M2 phenotype with reduced levels of inflammatory cytokines (TNF-α and IL-6) and increased levels of regulatory cytokines (IL-10 and TGF-β), as determined by both in vivo and in vitro tests. However, this therapeutic effect of rTs-Cys on MI was significantly reduced in PD-1−/− mice, as reflected by the higher level of M1 macrophages, elevated levels of inflammatory cytokines and decreased levels of regulatory cytokines. Conclusions rTs-Cys promotes M2-type polarization of macrophages through the PD-1 pathway to alleviate MI in mice and is, therefore, a potential drug for the treatment of MI and other inflammation-related diseases with involvement of the PD-1 checkpoint molecule. Graphical Abstract
ISSN:1756-3305