Su Kim, Jokl Elliot, Costain Alice, Simpson Kara, Cheeseman Antonn, Phythian-Adams Alexander, Couper Kevin N, MacDonald Andrew S, Piper Hanley Karen
Faculty of Biology, Medicine & Health, Manchester Academic Health Science Centre, University of Manchester, Oxford, Manchester, United Kingdom.
Lydia Becker Institute of Immunology and Inflammation, University of Manchester, Oxford, Manchester, United Kingdom.
PLoS Pathog. 2025 Jun 9;21(6):e1012928. doi: 10.1371/journal.ppat.1012928. eCollection 2025 Jun.
Schistosomiasis is a neglected, and potentially lethal, parasitic disease that affects hundreds of millions of people worldwide. As part of the schistosome lifecycle, parasite eggs accumulate within the liver where they evoke intense granulomatous pathology, typified by a dense extracellular matrix (ECM) barrier, which serves to contain toxic egg secretions. In severe cases, this progressive and irreversible egg-evoked ECM deposition can lead to pathological scarring, impaired liver function and lethality. Thus, identifying the core regulators that govern ECM deposition may aid discovery of new therapeutic targets for schistosomiasis. The transcription factor Sex determining region Y-box 9 (Sox9) is a known regulator of pathological scaring. We found that, following Schistosoma mansoni infection, SOX9 was ectopically expressed in myofibroblasts within the granuloma and in surrounding hepatocytes. In the absence of SOX9, granuloma size was significantly diminished, and mice failed to produce a robust ECM barrier around eggs, resulting in more diffuse liver injury and scattered distribution of immune cells. Immunologically, SOX9 loss in both naïve and infected mice led to an increase in hepatic neutrophil and monocyte proportions, with the expansion of Ly6clo monocyte populations in infected SOX9 deficient mice only. Infected SOX9-deficient mice also displayed exaggerated Type 2 inflammation, including pronounced eosinophilia. These data highlight the importance of SOX9 for intact hepatic granuloma formation during schistosomiasis and suggest SOX9 or its related factors may provide attractive future targets for meeting the clinical need to limit and/or reverse fibrotic disease.
血吸虫病是一种被忽视的、具有潜在致命性的寄生虫病,全球数亿人受其影响。作为血吸虫生命周期的一部分,寄生虫卵在肝脏中积聚,在那里引发强烈的肉芽肿性病理变化,其典型特征是致密的细胞外基质(ECM)屏障,该屏障用于容纳有毒的虫卵分泌物。在严重情况下,这种渐进性且不可逆的虫卵诱发的ECM沉积可导致病理性瘢痕形成、肝功能受损和死亡。因此,确定控制ECM沉积的核心调节因子可能有助于发现血吸虫病的新治疗靶点。转录因子性别决定区Y盒9(Sox9)是已知的病理性瘢痕形成调节因子。我们发现,感染曼氏血吸虫后,SOX9在肉芽肿内的肌成纤维细胞和周围肝细胞中异位表达。在缺乏SOX9的情况下,肉芽肿大小显著减小,并且小鼠未能在虫卵周围形成强大的ECM屏障,导致更弥漫性的肝损伤和免疫细胞的散在分布。在免疫学方面,未感染和感染小鼠中SOX9的缺失均导致肝脏中性粒细胞和单核细胞比例增加,仅在感染的SOX9缺陷小鼠中Ly6clo单核细胞群体有所扩大。感染SOX9缺陷的小鼠还表现出2型炎症反应加剧,包括明显的嗜酸性粒细胞增多。这些数据突出了SOX9在血吸虫病期间完整肝肉芽肿形成中的重要性,并表明SOX9或其相关因子可能为满足限制和/或逆转纤维化疾病的临床需求提供有吸引力的未来靶点。