Spatiotemporal transcriptomic profiling reveals the dynamic immunological landscape of alveolar echinococcosis

Author:

Ou ZhihuaORCID,Li Li,Ren Peidi,Zhou Ting-Ting,He Fan,Chen Jialing,Cai Huimin,Han Xiumin,Wu Yao-Dong,Li Jiandong,Li Xiu-Rong,Tan Qiming,Li Wenhui,Chen Qi,Zhang Nian-Zhang,He Xiuju,Chen Wei-Gang,Zhao Yanping,Sun Jiwen,Zhang Qian,Wu Yan-Tao,Liang Yingan,You Jie,Hu Guohai,Tian Xue-Qi,Liao Sha,Fu Bao-Quan,Chen Ao,Cai Xue-Peng,Yang Huanming,Wang Jian,Jin XinORCID,Xu Xun,Jia Wan-Zhong,Li JunhuaORCID,Yan Hong-Bin

Abstract

ABSTRACTAlveolar echinococcosis (AE) is caused by the invasive growth of the metacestodes ofEchinococcus multilocularis(E. multilocularis). The early diagnosis, management, and treatment of AE remains challenging. Herein, we integrated bulk RNA-seq, scRNA-seq, and ST technologies to reveal the immune characteristics both spatially and chronologically inE. multilocularisinfected mouse liver. An unprecedented high-resolution spatial atlas of theE. multilocularisinfection foci was obtained, revealing the pivotal role of neutrophils,Spp1+monocyte-derived macrophages (MoMFs), and fibroblasts in AE progression. We observed continuous recruitment of neutrophils and macrophages into the infected tissues, indicating prolonged immune stimulation by the growing metacestodes. However, their spatial distribution patterns and functions changed during the infection cause. At the early infection stage,Il1bhineutrophils aggregated in the lesion displayed the highest pattern-recognition receptor activity and may kill the metacestodes through NETosis, but their death in the infection foci might also trigger immune suppression. Meanwhile,Spp1+MoMFs attached to the protoscoleces to clear the infection. At the late infection stage, the neutrophils failed to infiltrate into the lesion although their continuous recruitment into the infected liver. Even though theSpp1+MoMFs enclosing the microcysts ofE. multilocularismay retain their pathogen-killing ability, they may also promote fibrosis and angiogenesis through interaction with fibroblasts. The pro- and anti-inflammatory phenotype balance of these immune cells may be associated with the transition of parasite control strategy from “active killing” to “negative segregation” by the host. Our findings identify key molecular traits involved in AE development, which may benefit the treatment of echinococcosis.

Publisher

Cold Spring Harbor Laboratory

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