Zhang Jinwei, Shen Yang, Yang Guitao, Sun Jing, Tang Chuang, Liang Hao, Ma Jideng, Wu Xiaoqian, Cao Haoran, Wu Meng, Ding Yuchun, Li Mingzhou, Liu Zuohua, Ge Liangpeng
Chongqing Academy of Animal Sciences, Chongqing, China.
Key Laboratory of Pig Industry Sciences, Ministry of Agriculture, Chongqing, China.
Front Physiol. 2023 Mar 22;14:1084332. doi: 10.3389/fphys.2023.1084332. eCollection 2023.
The gastrointestinal tract contains a complex microbial community. Peyer's patches (PPs) play an important role in inducing mucosal immune responses in the gastrointestinal tract. However, little is known about the effect of commensal microbiota on the host's PPs. Here, we analyzed the phenotypic-to-transcriptome changes in the intestine PPs of specific pathogen-free (SPF) and germ-free (GF) piglets (fed in an environment with and without commensal microbiota, respectively) to elucidate the role of commensal microbiota in host intestine mucosal immunity. Analyses of anatomical and histological characteristics showed that commensal microbiota deficiency led to PP hypoplasia, especially regarding B and T cells. A total of 12,444 mRNAs were expressed in 12 libraries; 2,156 and 425 differentially expressed (DE) mRNAs were detected in the jejunal PP (JPP) and ileal PP (IPP), respectively (SPF vs. GF). The shared DE mRNAs of the JPP and IPP were mainly involved in basic physiological and metabolic processes, while the specific DE mRNAs were enriched in regulating immune cells in the JPP and microbial responses and cellular immunity in the IPP. Commensal microbiota significantly modulated the expression of genes related to B-cell functions, including activation, proliferation, differentiation, apoptosis, receptor signaling, germinal center formation, and IgA isotype class switching, particularly in the JPP. TLR4 pathway-related genes were induced in response to microbial colonization and in LPS/SCFA-treated B cells. We also detected 69 and 21 DE lncRNAs in the JPP and IPP, respectively, and four one-to-one lncRNA-mRNA pairs were identified. These findings might represent key regulatory axes for host intestine mucosal immunity development during microbial colonization. Overall, the findings of this study revealed that commensal microbiota modulated phenotypic characteristics and gene expression in the piglet intestine PPs and underscored the importance of early microbial colonization for host mucosal immunity development.
胃肠道含有一个复杂的微生物群落。派尔集合淋巴结（PPs）在诱导胃肠道黏膜免疫反应中发挥着重要作用。然而，关于共生微生物群对宿主派尔集合淋巴结的影响却知之甚少。在此，我们分析了无特定病原体（SPF）仔猪和无菌（GF）仔猪（分别在有和没有共生微生物群的环境中饲养）肠道派尔集合淋巴结的表型至转录组变化，以阐明共生微生物群在宿主肠道黏膜免疫中的作用。解剖学和组织学特征分析表明，共生微生物群缺乏导致派尔集合淋巴结发育不全，尤其是B细胞和T细胞方面。12个文库中共表达了12444条mRNA；在空肠派尔集合淋巴结（JPP）和回肠派尔集合淋巴结（IPP）中分别检测到2156条和425条差异表达（DE）mRNA（SPF组与GF组）。JPP和IPP的共享DE mRNA主要参与基本的生理和代谢过程，而特定的DE mRNA在JPP中富集于调节免疫细胞，在IPP中富集于微生物反应和细胞免疫。共生微生物群显著调节了与B细胞功能相关基因的表达，包括激活、增殖、分化、凋亡、受体信号传导、生发中心形成和IgA同种型转换，特别是在JPP中。TLR4通路相关基因在微生物定植以及LPS/短链脂肪酸处理的B细胞中被诱导表达。我们还分别在JPP和IPP中检测到69条和21条DE lncRNA，并鉴定出4对一对一的lncRNA-mRNA对。这些发现可能代表了微生物定植期间宿主肠道黏膜免疫发育的关键调控轴。总体而言，本研究结果表明共生微生物群调节了仔猪肠道派尔集合淋巴结的表型特征和基因表达，并强调了早期微生物定植对宿主黏膜免疫发育的重要性。
