Zamanian Mostafa, Fraser Lisa M, Agbedanu Prince N, Harischandra Hiruni, Moorhead Andrew R, Day Tim A, Bartholomay Lyric C, Kimber Michael J
Department of Biomedical Sciences, Iowa State University, Ames, Iowa, United States of America; Department of Molecular Biosciences, Northwestern University, Evanston, Illinois, United States of America.
Department of Biomedical Sciences, Iowa State University, Ames, Iowa, United States of America.
PLoS Negl Trop Dis. 2015 Sep 24;9(9):e0004069. doi: 10.1371/journal.pntd.0004069. eCollection 2015.
Lymphatic filariasis (LF) is a socio-economically devastating mosquito-borne Neglected Tropical Disease caused by parasitic filarial nematodes. The interaction between the parasite and host, both mosquito and human, during infection, development and persistence is dynamic and delicately balanced. Manipulation of this interface to the detriment of the parasite is a promising potential avenue to develop disease therapies but is prevented by our very limited understanding of the host-parasite relationship. Exosomes are bioactive small vesicles (30-120 nm) secreted by a wide range of cell types and involved in a wide range of physiological processes. Here, we report the identification and partial characterization of exosome-like vesicles (ELVs) released from the infective L3 stage of the human filarial parasite Brugia malayi. Exosome-like vesicles were isolated from parasites in culture media and electron microscopy and nanoparticle tracking analysis were used to confirm that vesicles produced by juvenile B. malayi are exosome-like based on size and morphology. We show that loss of parasite viability correlates with a time-dependent decay in vesicle size specificity and rate of release. The protein cargo of these vesicles is shown to include common exosomal protein markers and putative effector proteins. These Brugia-derived vesicles contain small RNA species that include microRNAs with host homology, suggesting a potential role in host manipulation. Confocal microscopy shows J774A.1, a murine macrophage cell line, internalize purified ELVs, and we demonstrate that these ELVs effectively stimulate a classically activated macrophage phenotype in J774A.1. To our knowledge, this is the first report of exosome-like vesicle release by a human parasitic nematode and our data suggest a novel mechanism by which human parasitic nematodes may actively direct the host responses to infection. Further interrogation of the makeup and function of these bioactive vesicles could seed new therapeutic strategies and unearth stage-specific diagnostic biomarkers.
淋巴丝虫病(LF)是一种由寄生丝虫线虫引起的、具有社会经济破坏性的蚊媒传播被忽视热带病。在感染、发育和持续存在过程中,寄生虫与宿主(包括蚊子和人类)之间的相互作用是动态且微妙平衡的。操纵这个对寄生虫不利的界面是开发疾病疗法的一个有前景的潜在途径,但由于我们对宿主 - 寄生虫关系的了解非常有限,这一途径受到了阻碍。外泌体是由多种细胞类型分泌的具有生物活性的小囊泡(30 - 120纳米),参与多种生理过程。在此,我们报告了从人类丝虫寄生虫马来布鲁线虫感染性L3期释放的类外泌体囊泡(ELV)的鉴定和部分特征。从培养基中的寄生虫分离出类外泌体囊泡,并使用电子显微镜和纳米颗粒跟踪分析来确认,基于大小和形态,马来布鲁线虫幼虫产生的囊泡是类外泌体。我们表明,寄生虫活力的丧失与囊泡大小特异性和释放速率随时间的衰减相关。这些囊泡的蛋白质货物显示包括常见的外泌体蛋白质标志物和假定的效应蛋白。这些源自布鲁线虫的囊泡含有小RNA种类,包括与宿主具有同源性的微小RNA,表明其在操纵宿主方面可能发挥作用。共聚焦显微镜显示,小鼠巨噬细胞系J774A.1可内化纯化的ELV,并且我们证明这些ELV可有效刺激J774A.1中经典活化的巨噬细胞表型。据我们所知,这是人类寄生线虫释放类外泌体囊泡的首次报告,我们的数据表明了一种新机制,人类寄生线虫可能通过该机制积极引导宿主对感染的反应。对这些生物活性囊泡的组成和功能进行进一步研究,可能会催生新的治疗策略并发现阶段特异性诊断生物标志物。