Ran Maoshuang, Bao Jialing, Li Boning, Shi Yulian, Yang Wenxin, Meng Xianzhi, Chen Jie, Wei Junhong, Long Mengxian, Li Tian, Li Chunfeng, Pan Guoqing, Zhou Zeyang
State Key Laboratory of Resource Insects, Southwest University, Chongqing, China.
Chongqing Key Laboratory of Microsporidia Infection and Control, Southwest University, Chongqing, China.
PLoS Pathog. 2025 Jan 7;21(1):e1012373. doi: 10.1371/journal.ppat.1012373. eCollection 2025 Jan.
Microsporidia are a group of intracellular pathogens that actively manipulate host cell biological processes to facilitate their intracellular niche. Apoptosis is an important defense mechanism by which host cell control intracellular pathogens. Microsporidia modulating host cell apoptosis has been reported previously, however the molecular mechanism is not yet clear. In this report, we describe that the microsporidia Nosema bombycis inhibits apoptosis of Bombyx mori cells through a secreted protein NbSPN14, which is a serine protease inhibitor (Serpin). An immunofluorescent assay demonstrated that upon infection with N. bombycis, NbSPN14 was initially found in the B. mori cell cytoplasm and then became enriched in the host cell nucleus. Overexpression and RNA-interference (RNAi) of NbSPN14 in B. mori' embryo cell confirmed that NbSPN14 inhibited host cells apoptosis. Immunofluorescent and Co-IP assays verified the co-localization and interaction of NbSPN14 with the BmICE, the Caspase 3 homolog in B. mori. Knocking out of BmICE or mutating the BmICE-interacting P1 site of NbSPN14, eliminated the localization of NbSPN14 into the host nucleus and prevented the apoptosis-inhibiting effect of NbSPN14, which also proved that the interaction between BmICE and NbSPN14 occurred in host cytoplasm and the NbSPN14 translocation into host cell nucleus depends on BmICE. These data elucidate that N. bombycis secretory protein NbSPN14 inhibits host cell apoptosis by directly inhibiting the Caspase protease BmICE, which provides an important insight for understanding pathogen-host interactions and a potential therapeutic target for N. bombycis proliferation.
微孢子虫是一类细胞内病原体,它们会主动操控宿主细胞的生物学过程,以利于自身在细胞内生存。细胞凋亡是宿主细胞控制细胞内病原体的一种重要防御机制。此前已有报道称微孢子虫可调节宿主细胞凋亡,但其分子机制尚不清楚。在本报告中,我们描述了家蚕微孢子虫通过一种分泌蛋白NbSPN14抑制家蚕细胞凋亡,该蛋白是一种丝氨酸蛋白酶抑制剂(Serpin)。免疫荧光分析表明,感染家蚕微孢子虫后,NbSPN14最初在家蚕细胞胞质中被发现,随后在宿主细胞核中富集。在家蚕胚胎细胞中对NbSPN14进行过表达和RNA干扰(RNAi)实验,证实NbSPN14可抑制宿主细胞凋亡。免疫荧光和免疫共沉淀实验验证了NbSPN14与家蚕中Caspase 3同源物BmICE的共定位及相互作用。敲除BmICE或突变NbSPN14与BmICE相互作用的P1位点,可消除NbSPN14在宿主细胞核中的定位,并阻止NbSPN14的凋亡抑制作用,这也证明BmICE与NbSPN14的相互作用发生在宿主细胞质中,且NbSPN14向宿主细胞核的转运依赖于BmICE。这些数据表明,家蚕微孢子虫分泌蛋白NbSPN14通过直接抑制Caspase蛋白酶BmICE来抑制宿主细胞凋亡,这为理解病原体与宿主的相互作用提供了重要见解,并为家蚕微孢子虫增殖提供了潜在的治疗靶点。