Shigella targets epithelial tricellular junctions and uses a noncanonical clathrin-dependent endocytic pathway to spread between cells

Cell Host and Microbe

Volumn 11, Issue 4, 2012, Pages 325-336

  Fukumatsu, Makoto ^a   Ogawa, Michinaga ^a   Arakawa, Satoko ^b   Suzuki, Masato ^a   Nakayama, Kazuhisa ^c   Shimizu, Shigeomi ^b   Kim, Minsoo ^a   Mimuro, Hitomi ^a   Sasakawa, Chihiro ^a,d  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d NIPPON INSTITUTE FOR BIOLOGICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; DYNAMIN II; EPSIN; EPSIN 1; OCCLUDIN; PHOSPHATIDYLINOSITOL 3 KINASE; TRICELLULIN; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; BACTERIAL TRANSLOCATION; CELL CONTACT; CELL JUNCTION; CELL MEMBRANE; CELL MOTION; CELL SPREADING; ENDOCYTOSIS; ENZYME ACTIVITY; EPITHELIUM CELL; LISTERIA MONOCYTOGENES; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOPODIUM; SHIGELLA FLEXNERI;

ANIMALS; CELL LINE; CLATHRIN; DYSENTERY, BACILLARY; ENDOCYTOSIS; EPITHELIAL CELLS; HUMANS; MARVEL DOMAIN CONTAINING 2 PROTEIN; MEMBRANE PROTEINS; SHIGELLA; TIGHT JUNCTIONS;

EID: 84859938186     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2012.03.001     Document Type: Article

References (50)

1. Chen, C., and Zhuang, X. (2008). Epsin 1 is a cargo-specific adaptor for the clathrin-mediated endocytosis of the influenza virus. Proc. Natl. Acad. Sci. USA 105, 11790-11795.
2. Chen, H., Fre, S., Slepnev, V.I., Capua, M.R., Takei, K., Butler, M.H., Di Fiore, P.P., and De Camilli, P. (1998). Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 394, 793-797. (Pubitemid 28391645)
3. Collins, A., Warrington, A., Taylor, K.A., and Svitkina, T. (2011). Structural organization of the actin cytoskeleton at sites of clathrin-mediated endocytosis. Curr. Biol. 21, 1167-1175.
4. Conibear, E. (2010). Converging views of endocytosis in yeast and mammals. Curr. Opin. Cell Biol. 22, 513-518.
5. Conner, S.D., Schröter, T., and Schmid, S.L. (2003). AAK1-mediated micro2 phosphorylation is stimulated by assembled clathrin. Traffic 4, 885-890. (Pubitemid 37540590)
6. Cossart, P., and Sansonetti, P.J. (2004). Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304, 242-248. (Pubitemid 38452169)
7. Cureton, D.K., Massol, R.H., Whelan, S.P., and Kirchhausen, T. (2010). The length of vesicular stomatitis virus particles dictates a need for actin assembly during clathrin-dependent endocytosis. PLoS Pathog. 6, e1001127.
8. de Beco, S., Gueudry, C., Amblard, F., and Coscoy, S. (2009). Endocytosis is required for E-cadherin redistribution at mature adherens junctions. Proc. Natl. Acad. Sci. USA 106, 7010-7015.
9. Drake, M.T., Downs, M.A., and Traub, L.M. (2000). Epsin binds to clathrin by associating directly with the clathrin-terminal domain. Evidence for cooperative binding through two discrete sites. J. Biol. Chem. 275, 6479-6489. (Pubitemid 30129946)
10. Edelblum, K.L., and Turner, J.R. (2009). The tight junction in inflammatory disease: communication breakdown. Curr. Opin. Pharmacol. 9, 715-720.
11. Ferguson, S.M., Raimondi, A., Paradise, S., Shen, H., Mesaki, K., Ferguson, A., Destaing, O., Ko, G., Takasaki, J., Cremona, O., et al. (2009). Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev. Cell 17, 811-822.
12. Ford, M.G., Mills, I.G., Peter, B.J., Vallis, Y., Praefcke, G.J., Evans, P.R., and McMahon, H.T. (2002). Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366.
13. Ikenouchi, J., Furuse, M., Furuse, K., Sasaki, H., Tsukita, S., and Tsukita, S. (2005). Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J. Cell Biol. 171, 939-945. (Pubitemid 41815826)
14. Ikenouchi, J., Sasaki, H., Tsukita, S., Furuse, M., and Tsukita, S. (2008). Loss of occludin affects tricellular localization of tricellulin. Mol. Biol. Cell 19, 4687-4693.
15. Itoh, T., Koshiba, S., Kigawa, T., Kikuchi, A., Yokoyama, S., and Takenawa, T. (2001). Role of the ENTH domain in phosphatidylinositol-4,5- bisphosphate binding and endocytosis. Science 291, 1047-1051. (Pubitemid 32157414)
16. Ivanov, A.I., Nusrat, A., and Parkos, C.A. (2005). Endocytosis of the apical junctional complex: mechanisms and possible roles in regulation of epithelial barriers. Bioessays 27, 356-365. (Pubitemid 40592592)
17. Keyel, P.A., Mishra, S.K., Roth, R., Heuser, J.E., Watkins, S.C., and Traub, L.M. (2006). A single common portal for clathrin-mediated endocytosis of distinct cargo governed by cargo-selective adaptors. Mol. Biol. Cell 17, 4300-4317. (Pubitemid 44522050)
18. Koch, S., and Nusrat, A. (2009). Dynamic regulation of epithelial cell fate and barrier function by intercellular junctions. Ann. N Y Acad. Sci. 1165, 220-227.
19. Krug, S.M., Amasheh, S., Richter, J.F., Milatz, S., Günzel, D., Westphal, J.K., Huber, O., Schulzke, J.D., and Fromm, M. (2009). Tricellulin forms a barrier to macromolecules in tricellular tight junctions without affecting ion permeability. Mol. Biol. Cell 20, 3713-3724.
20. Le, T.L., Yap, A.S., and Stow, J.L. (1999). Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J. Cell Biol. 146, 219-232. (Pubitemid 29349976)
21. Lindmo, K., and Stenmark, H. (2006). Regulation of membrane traffic by phosphoinositide 3-kinases. J. Cell Sci. 119, 605-614.
22. Madara, J.L. (1990). Maintenance of the macromolecular barrier at cell extrusion sites in intestinal epithelium: physiological rearrangement of tight junctions. J. Membr. Biol. 116, 177-184.
23. McMahon, H.T., and Boucrot, E. (2011). Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517-533.
24. Merrifield, C.J., Perrais, D., and Zenisek, D. (2005). Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121, 593-606. (Pubitemid 40720012)
25. Motley, A., Bright, N.A., Seaman, M.N., and Robinson, M.S. (2003). Clathrin-mediated endocytosis in AP-2-depleted cells. J. Cell Biol. 162, 909-918. (Pubitemid 37087730)
26. Nishida, Y., Arakawa, S., Fujitani, K., Yamaguchi, H., Mizuta, T., Kanaseki, T., Komatsu, M., Otsu, K., Tsujimoto, Y., and Shimizu, S. (2009). Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461, 654-658.
27. Ogawa, M., Suzuki, T., Tatsuno, I., Abe, H., and Sasakawa, C. (2003). IcsB, secreted via the type III secretion system, is chaperoned by IpgA and required at the post-invasion stage of Shigella pathogenicity. Mol. Microbiol. 48, 913-931. (Pubitemid 36628259)
28. Ogawa, M., Handa, Y., Ashida, H., Suzuki, M., and Sasakawa, C. (2008). The versatility of Shigella effectors. Nat. Rev. Microbiol. 6, 11-16. (Pubitemid 350286216)
29. Otani, T., Ichii, T., Aono, S., and Takeichi, M. (2006). Cdc42 GEF Tuba regulates the junctional configuration of simple epithelial cells. J. Cell Biol. 175, 135-146. (Pubitemid 44537205)
30. Pentecost, M., Otto, G., Theriot, J.A., and Amieva, M.R. (2006). Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. PLoS Pathog. 2, e3.
31. Pentecost, M., Kumaran, J., Ghosh, P., and Amieva, M.R. (2010). Listeria monocytogenes internalin B activates junctional endocytosis to accelerate intestinal invasion. PLoS Pathog. 6, e1000900.
32. Pizarro-Cerdá, J., Bonazzi, M., and Cossart, P. (2010). Clathrin-mediated endocytosis: what works for small, also works for big. Bioessays 32, 496-504.
33. Polo, S., Sigismund, S., Faretta, M., Guidi, M., Capua, M.R., Bossi, G., Chen, H., De Camilli, P., and Di Fiore, P.P. (2002). A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416, 451-455. (Pubitemid 34272882)
34. Rajabian, T., Gavicherla, B., Heisig, M., Müller-Altrock, S., Goebel, W., Gray-Owen, S.D., and Ireton, K. (2009). The bacterial virulence factor InlC perturbs apical cell junctions and promotes cell-to-cell spread of Listeria. Nat. Cell Biol. 11, 1212-1218.
35. Rathman, M., de Lanerolle, P., Ohayon, H., Gounon, P., and Sansonetti, P. (2000). Myosin light chain kinase plays an essential role in S. flexneri dissemination. J. Cell Sci. 113, 3375-3386.
36. Rong, S.B., Hu, Y., Enyedy, I., Powis, G., Meuillet, E.J., Wu, X., Wang, R., Wang, S., and Kozikowski, A.P. (2001). Molecular modeling studies of the Akt PH domain and its interaction with phosphoinositides. J. Med. Chem. 44, 898-908. (Pubitemid 32861614)
37. Sansonetti, P.J., Mounier, J., Prévost, M.C., and Mè ge, R.M. (1994). Cadherin expression is required for the spread of Shigella flexneri between epithelial cells. Cell 76, 829-839. (Pubitemid 24085321)
38. Shen, L., Weber, C.R., and Turner, J.R. (2008). The tight junction protein complex undergoes rapid and continuous molecular remodeling at steady state. J. Cell Biol. 181, 683-695. (Pubitemid 351717514)
39. Shen, A., Zhou, D., Shen, Q., Liu, H.O., Sun, L., Liu, Y., Chen, J., Yang, J., Ji, Y., and Cheng, C. (2009). The expression of tumor necrosis factor-alpha (TNF-alpha) by the intrathecal injection of lipopolysaccharide in the rat spinal cord. Neurochem. Res. 34, 333-341.
40. Shen, L., Weber, C.R., Raleigh, D.R., Yu, D., and Turner, J.R. (2011). Tight junction pore and leak pathways: a dynamic duo. Annu. Rev. Physiol. 73, 283-309.
41. Shih, S.C., Katzmann, D.J., Schnell, J.D., Sutanto, M., Emr, S.D., and Hicke, L. (2002). Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat. Cell Biol. 4, 389-393. (Pubitemid 34521036)
42. Steed, E., Balda, M.S., and Matter, K. (2010). Dynamics and functions of tight junctions. Trends Cell Biol. 20, 142-149.
43. Tilney, L.G., and Portnoy, D.A. (1989). Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109, 1597-1608.
44. Tran Van Nhieu, G., Clair, C., Bruzzone, R., Mesnil, M., Sansonetti, P., and Combettes, L. (2003). Connexin-dependent inter-cellular communication increases invasion and dissemination of Shigella in epithelial cells. Nat. Cell Biol. 5, 720-726. (Pubitemid 36986779)
45. Troyanovsky, R.B., Sokolov, E.P., and Troyanovsky, S.M. (2006). Endocytosis of cadherin from intracellular junctions is the driving force for cadherin adhesive dimer disassembly. Mol. Biol. Cell 17, 3484-3493. (Pubitemid 44156442)
46. Utech, M., Mennigen, R., and Bruewer, M. (2010). Endocytosis and recycling of tight junction proteins in inflammation. J. Biomed. Biotechnol. 2010, 484987.
47. Vanden Broeck, D., and De Wolf, M.J. (2006). Selective blocking of clathrin-mediated endocytosis by RNA interference: epsin as target protein. Biotechniques 41, 475-484.
48. Veiga, E., and Cossart, P. (2005). Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells. Nat. Cell Biol. 7, 894-900. (Pubitemid 41486290)
49. Vieira, O.V., Botelho, R.J., Rameh, L., Brachmann, S.M., Matsuo, T., Davidson, H.W., Schreiber, A., Backer, J.M., Cantley, L.C., and Grinstein, S. (2001). Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation. J. Cell Biol. 155, 19-25. (Pubitemid 34286204)
50. Westphal, J.K., Dörfel, M.J., Krug, S.M., Cording, J.D., Piontek, J., Blasig, I.E., Tauber, R., Fromm, M., and Huber, O. (2010). Tricellulin forms homomeric and heteromeric tight junctional complexes. Cell. Mol. Life Sci. 67, 2057-2068.