Pedersen Gitte A, Jensen Helene H, Schelde Anne-Sofie B, Toft Charlotte, Pedersen Hans N, Ulrichsen Maj, Login Frédéric H, Amieva Manuel R, Nejsum Lene N
Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.
Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark.
PLoS One. 2017 Jun 21;12(6):e0179122. doi: 10.1371/journal.pone.0179122. eCollection 2017.
Foodborne Enteropathogenic Escherichia coli (EPEC) infections of the small intestine cause diarrhea especially in children and are a major cause of childhood death in developing countries. EPEC infects the apical membrane of the epithelium of the small intestine by attaching, effacing the microvilli under the bacteria and then forming microcolonies on the cell surface. We first asked the question where on epithelial cells EPEC attaches and grows. Using models of polarized epithelial monolayers, we evaluated the sites of initial EPEC attachment to the apical membrane and found that EPEC preferentially attached over the cell-cell junctions and formed microcolonies preferentially where three cells come together at tricellular tight junctions. The ability of EPEC to adhere increased when host cell polarity was compromised yielding EPEC access to basolateral proteins. EPEC pedestals contain basolateral cytoskeletal proteins. Thus, we asked if attached EPEC causes reorganization the protein composition of the host cell plasma membrane at sites of microcolony formation. We found that EPEC microcolony growth at the apical membrane resulted in a local accumulation of basolateral plasma membrane proteins surrounding the microcolony. Basolateral marker protein aquaporin-3 localized to forming EPEC microcolonies. Components of the basolateral vesicle targeting machinery were re-routed. The Exocyst (Exo70) was recruited to individual EPEC as was the basolateral vesicle SNARE VAMP-3. Moreover, several Rab variants were also recruited to the infection site, and their dominant-negative equivalents were not. To quantitatively study the recruitment of basolateral proteins, we created a pulse of the temperature sensitive basolateral VSVG, VSVG3-SP-GFP, from the trans-Golgi Network. We found that after release from the TGN, significantly more VSVG3-SP-GFP accumulated at the site of microcolony growth than on equivalent membrane regions of uninfected cells. This suggests that trafficking of vesicles destined for the basolateral membrane are redirected to the apical site of microcolony growth. Thus, in addition to disrupting host cell fence function, local host cell plasma membrane protein composition is changed by altered protein trafficking and recruitment of basolateral proteins to the apical microcolony. This may aid EPEC attachment and subsequent microcolony growth.
食源性肠道致病性大肠杆菌(EPEC)感染小肠会引发腹泻,尤其在儿童中较为常见,并且是发展中国家儿童死亡的主要原因。EPEC通过附着在小肠上皮细胞的顶端膜上,使细菌下方的微绒毛消失,然后在细胞表面形成微菌落,从而感染小肠上皮细胞。我们首先提出了EPEC在上皮细胞的何处附着和生长的问题。利用极化上皮单层模型,我们评估了EPEC最初附着在顶端膜上的位点,发现EPEC优先附着在细胞间连接处,并优先在三个细胞在三细胞紧密连接处聚集的地方形成微菌落。当宿主细胞极性受损,使EPEC能够接触到基底外侧蛋白时,EPEC的黏附能力增强。EPEC菌毛包含基底外侧细胞骨架蛋白。因此,我们询问附着的EPEC是否会导致宿主细胞质膜在微菌落形成位点的蛋白质组成发生重组。我们发现,EPEC在顶端膜上的微菌落生长导致微菌落周围基底外侧质膜蛋白的局部积累。基底外侧标记蛋白水通道蛋白-3定位于正在形成的EPEC微菌落。基底外侧囊泡靶向机制的成分被重新定向。外排复合体(Exo70)以及基底外侧囊泡SNARE蛋白VAMP-3被招募到单个EPEC处。此外,几种Rab变体也被招募到感染位点,而它们的显性负性等效物则没有。为了定量研究基底外侧蛋白的招募情况,我们从反式高尔基体网络产生了温度敏感型基底外侧VSVG(VSVG3-SP-GFP)的脉冲。我们发现,从反式高尔基体网络释放后,在微菌落生长位点积累的VSVG3-SP-GFP明显多于未感染细胞的等效膜区域。这表明,运往基底外侧膜的囊泡运输被重新定向到微菌落生长的顶端位点。因此,除了破坏宿主细胞的屏障功能外,局部宿主细胞质膜蛋白组成通过改变蛋白运输以及将基底外侧蛋白招募到顶端微菌落而发生变化。这可能有助于EPEC的附着以及随后的微菌落生长。