Institut Pasteur, Biology of Infection Unit, Paris, France.
PLoS Pathog. 2013;9(5):e1003381. doi: 10.1371/journal.ppat.1003381. Epub 2013 May 30.
Listeria monocytogenes (Lm) is an invasive foodborne pathogen that leads to severe central nervous system and maternal-fetal infections. Lm ability to actively cross the intestinal barrier is one of its key pathogenic properties. Lm crosses the intestinal epithelium upon the interaction of its surface protein internalin (InlA) with its host receptor E-cadherin (Ecad). InlA-Ecad interaction is species-specific, does not occur in wild-type mice, but does in transgenic mice expressing human Ecad and knock-in mice expressing humanized mouse Ecad. To study listeriosis in wild-type mice, InlA has been "murinized" to interact with mouse Ecad. Here, we demonstrate that, unexpectedly, murinized InlA (InlA(m)) mediates not only Ecad-dependent internalization, but also N-cadherin-dependent internalization. Consequently, InlA(m)-expressing Lm targets not only goblet cells expressing luminally-accessible Ecad, as does Lm in humanized mice, but also targets villous M cells, which express luminally-accessible N-cadherin. This aberrant Lm portal of entry results in enhanced innate immune responses and intestinal barrier damage, both of which are not observed in wild-type Lm-infected humanized mice. Murinization of InlA therefore not only extends the host range of Lm, but also broadens its receptor repertoire, providing Lm with artifactual pathogenic properties. These results challenge the relevance of using InlA(m)-expressing Lm to study human listeriosis and in vivo host responses to this human pathogen.
李斯特菌(Lm)是一种侵袭性食源性病原体,可导致严重的中枢神经系统和母婴感染。Lm 主动穿过肠道屏障的能力是其关键致病特性之一。Lm 通过其表面蛋白内毒素(InlA)与宿主受体 E-钙粘蛋白(Ecad)的相互作用穿过肠道上皮细胞。InlA-Ecad 相互作用具有物种特异性,不会在野生型小鼠中发生,但会在表达人 Ecad 的转基因小鼠和表达人源化小鼠 Ecad 的敲入小鼠中发生。为了在野生型小鼠中研究李斯特菌病,已经“鼠源化”了 InlA 以与小鼠 Ecad 相互作用。在这里,我们出乎意料地证明,鼠源化的 InlA(InlA(m))不仅介导 Ecad 依赖性内化,还介导 N-钙粘蛋白依赖性内化。因此,表达 InlA(m)的 Lm 不仅靶向表达腔accessible Ecad 的杯状细胞,就像人源化小鼠中的 Lm 一样,还靶向表达腔accessible N-钙粘蛋白的绒毛 M 细胞。这种异常的 Lm 进入门户导致固有免疫反应增强和肠道屏障损伤,而在野生型 Lm 感染的人源化小鼠中未观察到这些损伤。因此,InlA 的鼠源化不仅扩展了 Lm 的宿主范围,还扩展了其受体库,赋予了 Lm 人为的致病特性。这些结果质疑了使用表达 InlA(m)的 Lm 来研究人类李斯特菌病和体内宿主对这种人类病原体的反应的相关性。