Enteropathogenic Escherichia coli, Shigella flexneri, and Listeria monocytogenes Recruit a Junctional Protein, Zonula Occludens-1, to Actin Tails and Pedestals

• Published in: Infection and Immunity Vol. 75; no. 2; pp. 565 - 573
• Main Authors: Hanajima-Ozawa, Miyuki, Matsuzawa, Takeshi, Fukui, Aya, Kamitani, Shigeki, Ohnishi, Hiroe, Abe, Akio, Horiguchi, Yasuhiko, Miyake, Masami
• Format: Journal Article
• Language: English
• Published: Washington, DC American Society for Microbiology 01.02.2007
• Subjects: Actin-Related Protein 2 - metabolism; Actin-Related Protein 3 - metabolism; Actins - metabolism; Adaptor Proteins, Signal Transducing; Animals; Bacteriology; Biological and medical sciences; Cellular Microbiology: Pathogen-Host Cell Molecular Interactions; Cytoplasm - chemistry; Epithelial Cells - microbiology; Escherichia coli; Escherichia coli - physiology; Fundamental and applied biological sciences. Psychology; HeLa Cells; Humans; Hymenoptera; Immunohistochemistry; Listeria monocytogenes; Listeria monocytogenes - physiology; Membrane Proteins - metabolism; Mice; Microbiology; Microscopy, Fluorescence; Miscellaneous; NIH 3T3 Cells; Oncogene Proteins - physiology; Phosphoproteins - metabolism; Shigella flexneri; Shigella flexneri - physiology; Zonula Occludens-1 Protein; Microbiology; Actin; Escherichia coli; Listeria monocytogenes; Bacteria; Shigella flexneri; Immunity; Protein; Enterobacteriaceae
• ISSN: 0019-9567; 1098-5522
• DOI: 10.1128/IAI.01479-06

Enteropathogenic Escherichia coli, Shigella flexneri, and Listeria monocytogenes induce localized actin polymerization at the cytoplasmic face of the plasma membrane or within the host cytoplasm, creating unique actin-rich structures termed pedestals or actin tails. The process is known to be mediated by the actin-related protein 2 and 3 (Arp2/3) complex, which in these cases acts downstream of neural Wiskott-Aldrich syndrome protein (N-WASP) or of a listerial functional homolog of WASP family proteins. Here, we show that zonula occludens-1 (ZO-1), a protein in the tight junctions of polarized epithelial cells, is recruited to actin tails and pedestals. Immunocytochemical analysis revealed that ZO-1 was stained most in the distal part of the actin-rich structures, and the incorporation was mediated by the proline-rich region of the ZO-1 molecule. The direct clustering of membrane-targeted Nck, which is known to activate the N-WASP-Arp2/3 pathway, triggered the formation of the ZO-1-associated actin tails. The results suggest that the activation of the Arp2/3 complex downstream of N-WASP or a WASP-related molecule is a key to the formation of the particular actin-rich structures that bind with ZO-1. We propose that an analysis of the recruitment on a molecular basis will lead to an understanding of how ZO-1 recognizes a distinctive actin-rich structure under pathophysiological conditions.