Department of Physiology, Temerty Faculty of Medicine, University of Toronto, Toronto, ON, Canada; Keenan Research Centre for Biomedical Science, St. Michael's Hospital, Toronto, ON, Canada.
Department of Chemistry and Environmental Science, New Jersey Institute of Technology, Newark, NJ, USA.
Mol Ther. 2023 Sep 6;31(9):2681-2701. doi: 10.1016/j.ymthe.2023.06.011. Epub 2023 Jun 19.
Virus-induced lung injury is associated with loss of pulmonary epithelial-endothelial tight junction integrity. While the alveolar-capillary membrane may be an indirect target of injury, viruses may interact directly and/or indirectly with miRs to augment their replication potential and evade the host antiviral defense system. Here, we expose how the influenza virus (H1N1) capitalizes on host-derived interferon-induced, microRNA (miR)-193b-5p to target occludin and compromise antiviral defenses. Lung biopsies from patients infected with H1N1 revealed increased miR-193b-5p levels, marked reduction in occludin protein, and disruption of the alveolar-capillary barrier. In C57BL/6 mice, the expression of miR-193b-5p increased, and occludin decreased, 5-6 days post-infection with influenza (PR8). Inhibition of miR-193b-5p in primary human bronchial, pulmonary microvascular, and nasal epithelial cells enhanced antiviral responses. miR-193b-deficient mice were resistant to PR8. Knockdown of occludin, both in vitro and in vivo, and overexpression of miR-193b-5p reconstituted susceptibility to viral infection. miR-193b-5p inhibitor mitigated loss of occludin, improved viral clearance, reduced lung edema, and augmented survival in infected mice. Our results elucidate how the innate immune system may be exploited by the influenza virus and how strategies that prevent loss of occludin and preserve tight junction function may limit susceptibility to virus-induced lung injury.
病毒诱导的肺损伤与肺上皮-内皮紧密连接完整性的丧失有关。虽然肺泡-毛细血管膜可能是损伤的间接靶点,但病毒可能直接和/或间接地与 microRNA(miR)相互作用,以增强其复制潜力并逃避宿主抗病毒防御系统。在这里,我们揭示了流感病毒(H1N1)如何利用宿主衍生的干扰素诱导的 microRNA(miR)-193b-5p 来靶向紧密连接蛋白 occludin 并破坏抗病毒防御。感染 H1N1 的患者的肺活检显示 miR-193b-5p 水平升高,occludin 蛋白明显减少,肺泡-毛细血管屏障破坏。在 C57BL/6 小鼠中,流感(PR8)感染后 5-6 天,miR-193b-5p 的表达增加,occludin 减少。在原代人支气管、肺微血管和鼻上皮细胞中抑制 miR-193b-5p 可增强抗病毒反应。miR-193b 缺陷型小鼠对 PR8 具有抗性。体外和体内敲低 occludin 以及过表达 miR-193b-5p 均可重建对病毒感染的易感性。miR-193b-5p 抑制剂减轻了 occludin 的丢失,改善了病毒清除,减少了肺水肿,并提高了感染小鼠的存活率。我们的研究结果阐明了流感病毒如何利用先天免疫系统,以及预防 occludin 丢失和保持紧密连接功能的策略如何限制病毒诱导的肺损伤易感性。