Mercado-Evans Vicki, Branthoover Holly, Chew Claude, Serchejian Camille, Saltzman Alexander B, Mejia Marlyd E, Zulk Jacob J, Cornax Ingrid, Nizet Victor, Patras Kathryn A
Department of Molecular Virology and Microbiology.
Medical Scientist Training Program.
JCI Insight. 2025 Jan 9;10(1):e180024. doi: 10.1172/jci.insight.180024.
Urinary neutrophils are a hallmark of urinary tract infection (UTI), yet the mechanisms governing their activation, function, and efficacy in controlling infection remain incompletely understood. Tamm-Horsfall glycoprotein (THP), the most abundant protein in urine, uses terminal sialic acids to bind an inhibitory receptor and dampen neutrophil inflammatory responses. We hypothesized that neutrophil modulation is an integral part of THP-mediated host protection. In a UTI model, THP-deficient mice showed elevated urinary tract bacterial burdens, increased neutrophil recruitment, and more severe tissue histopathological changes compared with WT mice. Furthermore, THP-deficient mice displayed impaired urinary NETosis during UTI. To investigate the effect of THP on NETosis, we coupled in vitro fluorescence-based NET assays, proteomic analyses, and standard and imaging flow cytometry with peripheral human neutrophils. We found that THP increases proteins involved in respiratory chain, neutrophil granules, and chromatin remodeling pathways; enhances NETosis in an ROS-dependent manner; and drives NET-associated morphologic features including nuclear decondensation. These effects were observed only in the presence of a NETosis stimulus and could not be solely replicated with equivalent levels of sialic acid alone. We conclude that THP is a critical regulator of NETosis in the urinary tract, playing a key role in host defense against UTI.
尿中性粒细胞是尿路感染(UTI)的一个标志,但关于其激活、功能以及控制感染的效力的调控机制仍未完全明确。Tamm-Horsfall糖蛋白(THP)是尿液中最丰富的蛋白质,它利用末端唾液酸结合一种抑制性受体并减弱中性粒细胞的炎症反应。我们推测中性粒细胞调节是THP介导的宿主保护的一个重要组成部分。在一个UTI模型中,与野生型小鼠相比,THP缺陷型小鼠的尿路细菌负荷增加、中性粒细胞募集增多且组织组织病理学变化更严重。此外,THP缺陷型小鼠在UTI期间表现出尿中中性粒细胞胞外诱捕网形成受损。为了研究THP对中性粒细胞胞外诱捕网形成的影响,我们将基于体外荧光的中性粒细胞胞外诱捕网检测、蛋白质组学分析以及标准和成像流式细胞术与外周血人中性粒细胞相结合。我们发现THP增加了参与呼吸链、中性粒细胞颗粒和染色质重塑途径的蛋白质;以活性氧依赖的方式增强中性粒细胞胞外诱捕网形成;并驱动包括核解聚在内的与中性粒细胞胞外诱捕网相关的形态学特征。这些效应仅在存在中性粒细胞胞外诱捕网形成刺激的情况下观察到,并且不能仅用同等水平的唾液酸单独复制。我们得出结论,THP是尿路中中性粒细胞胞外诱捕网形成的关键调节因子,在宿主抵御UTI的防御中起关键作用。