Ferritin1-mediated ferroptosis participates in granular acini degeneration of Haemaphysalis longicornis salivary glands

IF 3.1 2区医学 Q2 INFECTIOUS DISEASES Ticks and Tick-borne Diseases Pub Date : 2025-03-01 DOI:10.1016/j.ttbdis.2025.102464

Dongqi Yuan , Songqin Chen , Yongzhi Zhou, Jie Cao, Houshuang Zhang, Yanan Wang, Jinlin Zhou

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Abstract

Ticks (Haemaphysalis longicornis) transmit pathogens to their hosts through their salivary glands during blood-feeding. The salivary glands of adult parthenogenetic H. longicornis undergo degeneration post-engorgement. Clarifying the molecular mechanisms underlying salivary gland degeneration of H. longicornis is conducive to identifying novel targets for preventing and controlling these widespread vectors. In this study, we investigated the salivary glands of adult parthenogenetic H. longicornis to elucidate the relationship between ferroptosis, iron-dependent cell death, H. longicornis ferritin 1 (HlFer1) and salivary gland degeneration post-attachment and post-engorgement. Fluorescence microscopy, revealed increased iron accumulation, reactive oxygen species, lipid peroxidation, and decreased mitochondrial cristae in the granular acini of H. longicornis salivary glands post-engorgement. The results of a qPCR analysis indicated that HlFer1, glutathione peroxidase 4 (GPX4), transferrin (TRF), and high mobility group protein B1 (HMGB1) expression elevated in H. longicornis salivary glands post-attachment and post-engorgement. In vitro culture of H. longicornis salivary glands showed that erastin promotes ferroptosis, while ferrostatin-1 blocks this process. RNA interference (RNAi) targeting HlFer1 promoted ferroptosis in salivary gland granular acini. In conclusion, we demonstrated that HlFer1-induced ferroptosis is a key molecular mechanism underlying the salivary gland granular acini degeneration of H. longicornis. Our findings are important for developing novel preventive measures against H. longicornis as a disease vector.

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蜱（Haemaphysalis longicornis）在吸血过程中通过唾液腺向宿主传播病原体。孤雌生殖的长角蜱成虫的唾液腺在增殖后会发生退化。阐明长角水母唾液腺变性的分子机制有助于确定预防和控制这些广泛传播的病媒的新靶标。在这项研究中，我们研究了孤雌生殖的成年长角虹鳟的唾液腺，以阐明附着后和蜕皮后的长角虹鳟铁蛋白1（HlFer1）与唾液腺变性之间的关系。荧光显微镜检查显示，长角蜥唾液腺增生后颗粒状突起中的铁积累、活性氧、脂质过氧化和线粒体嵴减少。qPCR 分析结果表明，HlFer1、谷胱甘肽过氧化物酶 4 (GPX4)、转铁蛋白 (TRF) 和高迁移率基团蛋白 B1 (HMGB1) 在长角虹鳟唾液腺附着后和峡化后的表达均升高。体外培养长角水母唾液腺的结果表明，麦拉宁能促进铁突变，而铁前列素-1则能阻止这一过程。以 HlFer1 为靶点的 RNA 干扰（RNAi）促进了唾液腺颗粒棘突的铁突变。总之，我们证明了HlFer1诱导的铁蜕变是长角雉唾液腺颗粒状尖头变性的一个关键分子机制。我们的研究结果对于开发新的预防措施以防止长角蝰成为病媒具有重要意义。

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来源期刊

Ticks and Tick-borne Diseases INFECTIOUS DISEASES-MICROBIOLOGY

CiteScore

6.90

自引率

12.50%

发文量

185

审稿时长

6-12 weeks

期刊介绍： Ticks and Tick-borne Diseases is an international, peer-reviewed scientific journal. It publishes original research papers, short communications, state-of-the-art mini-reviews, letters to the editor, clinical-case studies, announcements of pertinent international meetings, and editorials. The journal covers a broad spectrum and brings together various disciplines, for example, zoology, microbiology, molecular biology, genetics, mathematical modelling, veterinary and human medicine. Multidisciplinary approaches and the use of conventional and novel methods/methodologies (in the field and in the laboratory) are crucial for deeper understanding of the natural processes and human behaviour/activities that result in human or animal diseases and in economic effects of ticks and tick-borne pathogens. Such understanding is essential for management of tick populations and tick-borne diseases in an effective and environmentally acceptable manner.