Rezaee Fariba, Harford Terri J, Linfield Debra T, Altawallbeh Ghaith, Midura Ronald J, Ivanov Andrei I, Piedimonte Giovanni
Pediatric Research Center and Pediatric Institute, Cleveland Clinic Children's, Cleveland, Ohio, United States of America.
Pathobiology Department, Lerner Research Institute, Cleveland, Ohio, United States of America.
PLoS One. 2017 Jul 31;12(7):e0181876. doi: 10.1371/journal.pone.0181876. eCollection 2017.
Airway epithelium forms a barrier to the outside world and has a crucial role in susceptibility to viral infections. Cyclic adenosine monophosphate (cAMP) is an important second messenger acting via two intracellular signaling molecules: protein kinase A (PKA) and the guanidine nucleotide exchange factor, Epac. We sought to investigate effects of increased cAMP level on the disruption of model airway epithelial barrier caused by RSV infection and the molecular mechanisms underlying cAMP actions. Human bronchial epithelial cells were infected with RSV-A2 and treated with either cAMP releasing agent, forskolin, or cAMP analogs. Structure and functions of the Apical Junctional Complex (AJC) were evaluated by measuring transepithelial electrical resistance and permeability to FITC-dextran, and determining localization of AJC proteins by confocal microscopy. Increased intracellular cAMP level significantly attenuated RSV-induced disassembly of AJC. These barrier-protective effects of cAMP were due to the activation of PKA signaling and did not involve Epac activity. Increased cAMP level reduced RSV-induced reorganization of the actin cytoskeleton, including apical accumulation of an essential actin-binding protein, cortactin, and inhibited expression of the RSV F protein. These barrier-protective and antiviral-function of cAMP signaling were evident even when cAMP level was increased after the onset of RSV infection. Taken together, our study demonstrates that cAMP/PKA signaling attenuated RSV-induced disruption of structure and functions of the model airway epithelial barrier by mechanisms involving the stabilization of epithelial junctions and inhibition of viral biogenesis. Improving our understanding of the mechanisms involved in RSV-induced epithelial dysfunction and viral pathogenesis will help to develop novel anti-viral therapeutic approaches.
气道上皮细胞构成了与外界的屏障,在病毒感染易感性方面起着关键作用。环磷酸腺苷(cAMP)是一种重要的第二信使,通过两种细胞内信号分子发挥作用:蛋白激酶A(PKA)和鸟苷酸交换因子Epac。我们试图研究cAMP水平升高对呼吸道合胞病毒(RSV)感染所致模型气道上皮屏障破坏的影响以及cAMP作用的分子机制。人支气管上皮细胞用RSV-A2感染,并分别用cAMP释放剂福斯可林或cAMP类似物处理。通过测量跨上皮电阻和对异硫氰酸荧光素标记葡聚糖的通透性,并通过共聚焦显微镜确定顶端连接复合体(AJC)蛋白的定位,来评估AJC的结构和功能。细胞内cAMP水平升高显著减弱了RSV诱导的AJC解体。cAMP的这些屏障保护作用归因于PKA信号的激活,且不涉及Epac活性。cAMP水平升高减少了RSV诱导的肌动蛋白细胞骨架重排,包括一种重要的肌动蛋白结合蛋白皮质肌动蛋白的顶端积累,并抑制了RSV F蛋白的表达。即使在RSV感染开始后cAMP水平升高,cAMP信号的这些屏障保护和抗病毒功能仍然明显。综上所述,我们的研究表明,cAMP/PKA信号通过涉及稳定上皮连接和抑制病毒生物合成的机制减弱了RSV诱导的模型气道上皮屏障结构和功能的破坏。增进我们对RSV诱导的上皮功能障碍和病毒发病机制的理解将有助于开发新的抗病毒治疗方法。