Sun Rex, Urban Joseph F, Notari Luigi, Vanuytsel Tim, Madden Kathleen B, Bohl Jennifer A, Ramalingam Thirumalai R, Wynn Thomas A, Zhao Aiping, Shea-Donohue Terez
Departments of Radiation Oncology and Medicine, University of Maryland School of Medicine, Baltimore, Maryland, USA.
U.S. Department of Agriculture, Agricultural Research Service, Beltsville Human Nutrition Research Center, Diet, Genomics, and Immunology Laboratory, Beltsville, Maryland, USA.
Infect Immun. 2016 Mar 24;84(4):1032-1044. doi: 10.1128/IAI.00990-15. Print 2016 Apr.
Nematode infection upregulates interleukin-4 (IL-4) and IL-13 and induces STAT6-dependent changes in gut function that promote worm clearance. IL-4 and IL-13 activate the type 2 IL-4 receptor (IL-4R), which contains the IL-13Rα1 and IL-4Rα chains. We used mice deficient in IL-13Rα1 (IL-13Rα1(-/-)) to examine the contribution of IL-13 acting at the type 2 IL-4R to immune and functional responses to primary (Hb1) and secondary (Hb2) infections with the gastrointestinal nematode parasite Heligmosomoides bakeri There were differences between strains in the IL-4 and IL-13 expression responses to Hb1 but not Hb2 infection. Following Hb2 infection, deficient mice had impaired worm expulsion and higher worm fecundity despite normal production of Th2-derived cytokines. The upregulation of IL-25 and IL-13Rα2 in Hb1- and Hb2-infected wild-type (WT) mice was absent in IL-13Rα1(-/-)mice. Goblet cell numbers and resistin-like molecule beta (RELM-β) expression were attenuated significantly in IL-13Rα1(-/-)mice following Hb2 infections. IL-13Rα1 contributes to the development of alternatively activated macrophages, but the type 1 IL-4R is also important. Hb1 infection had no effects on smooth muscle function or epithelial permeability in either strain, while the enhanced mucosal permeability and changes in smooth muscle function and morphology observed in response to Hb2 infection in WT mice were absent in IL-13Rα1(-/-)mice. Notably, the contribution of claudin-2, which has been linked to IL-13, does not mediate the increased mucosal permeability following Hb2 infection. These results show that activation of IL-13Rα1 is critical for key aspects of the immune and functional responses to Hb2 infection that facilitate expulsion.
线虫感染会上调白细胞介素-4(IL-4)和IL-13,并诱导肠道功能发生依赖于信号转导和转录激活因子6(STAT6)的变化,从而促进蠕虫清除。IL-4和IL-13激活2型IL-4受体(IL-4R),该受体包含IL-13Rα1和IL-4Rα链。我们使用IL-13Rα1缺陷型小鼠(IL-13Rα1(-/-))来研究作用于2型IL-4R的IL-13对胃肠道线虫寄生虫巴氏赫勒线虫原发性(Hb1)和继发性(Hb2)感染的免疫和功能反应的贡献。在对Hb1感染的IL-4和IL-13表达反应中,不同品系之间存在差异,但对Hb2感染则没有差异。在Hb2感染后,尽管Th2衍生细胞因子的产生正常,但缺陷型小鼠的蠕虫排出受损且蠕虫繁殖力更高。在IL-13Rα1(-/-)小鼠中,未观察到在感染Hb1和Hb2的野生型(WT)小鼠中IL-25和IL-13Rα2的上调。在Hb2感染后,IL-13Rα1(-/-)小鼠的杯状细胞数量和抵抗素样分子β(RELM-β)表达显著减弱。IL-13Rα1有助于交替活化巨噬细胞的发育,但1型IL-4R也很重要。Hb1感染对两种品系的平滑肌功能或上皮通透性均无影响,而WT小鼠中对Hb2感染所观察到的黏膜通透性增强以及平滑肌功能和形态变化在IL-13Rα1(-/-)小鼠中未出现。值得注意的是,与IL-13相关的紧密连接蛋白2并不介导Hb2感染后黏膜通透性的增加。这些结果表明,IL-13Rα1的激活对于促进排出的Hb2感染免疫和功能反应的关键方面至关重要。