Review on the polarity disruption of intestinal epithelial cells by enteropathogenic Escherichia coli
WANG Yu-bo1, XU Qian-qian2, 3, GUO Shi-jin2, 3, WANG Yan-ping2, 3, ZHANG Ying2, 3, YANG Li-mei2, 3, SHEN Zhi-qiang2, 3
1. Department of Thoracic Surgery, Binzhou Medical College Hospital, Binzhou 256600, China; 2. Shandong Binzhou Animal Science and Veterinary Medicine Academy, Shandong Binzhou Research, Development and Promotion Center for Livestock and Poultry Propolis Vaccine, Binzhou 256600, China; 3. Shandong Lvdu Ante veterinary drug Industry Co., Ltd, Binzhou 256600, China
Abstract：Epithelial cells constitute a physical barrier which protects the host from microbial pathogens. Polarized epithelial cells contain distinct apical and basolateral membrane domains separated by intercellular junctions, and the most important were tight junctions, which contribute to the maintenance of apical-basal polarity. Polarity complexes also contribute to the establishment of tight junction(TJ) formation. Enteropathogenic Escherichia coli through dysregulation of multiple factors, including disruption of the intestinal barrier, redistribution of adhesion and polarity proteins, and recruitment of polarity complexes to infection sites, all of which lead to impaired apical-basal polarity and perturbed epithelial TJ barrier function and structure. Here, we review the important role played in intestinal epithelial cells polarity maintenance of tight junctions, impact of enteropathogenic Escherichia coli on the disruption of cell-cell junctions and epithelial polarity, which provide references for the study of enteropathogenic Escherichia coli action mechanism and the corresponding defense methods.
[1] Lai Y, Rosenshine I, Leong JM, et al.Intimate host attachment: enteropathogenic and enterohaemorrhagic Escherichia coli[J]. Cell Microbiol, 2013, 15(11): 1796-1808. DOI: 10.1111/cmi.12179 [2] Rodriguez-Boulan E, Macara IG.Organization and execution of the epithelial polarity programme[J]. Nat Rev Mol Cell Biol, 2014, 15(4): 225-42. DOI: 10.1038/nrm3775 [3] Tepass U.The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival[J]. Annu Rev Cell Dev Biol, 2012, 28: 655-85. DOI: 10.1146/annurev-cellbio-092910-154033 [4] Farquhar M, Palade G.Junctional complexes in various epithelia[J]. J Cell Biol, 1963, 17: 375-412. DOI: 10.1083/jcb.17.2.375 [5] Van Itallie C, Anderson J.Architecture of tight junctions and principles of molecular composition[J]. Semin Cell Dev Biol, 2014, 36: 157-165. DOI: 10.1016/j.semcdb.2014.08.011 [6] Suzuki A, Yamanaka T, Hirose T, et al.Atypical protein kinase C is involved in the evolutionarily conserved par protein complex and plays a critical role in establishing epithelia-specific junctional structures[J]. J Cell Biol, 2001, 152(6): 1183-1196. DOI: 10.1083/jcb.152.6.1183 [7] Wei Z, Li Y, Iye F, et al.Structural basis for the phosphorylation-regulated interaction between the cyto- plasmic tail of cell polarity protein crumbs and the actin-binding protein moesin[J]. J Biol Chem, 2015, 290(18): 11384-11392. DOI:10.1074/jbc.M115.643791 [8] Yamanaka T, Horikoshi Y, Sugiyama Y, et al.Mammalian Lgl forms a protein complex with PAR-6 and aPKC independently of PAR-3 to regulate epithelial cell polarity[J]. Curr Biol, 2003, 13(9): 734-743. DOI: 10.1016/S0960-9822(03)00244-6 [9] Mcnamara BP, Koutsouris A, O’connell CB, et al.Translocated EspF protein from enteropathogenic Escherichia coli disrupts host intestinal barrier function[J]. J Clin Invest, 2001, 107(5): 621-629. DOI:10.1172/JCI11138 [10] Dean P, Kenny B.Intestinal barrier dysfunction by enteropathogenic Escherichia coli is mediated by two effector molecules and a bacterial surface protein[J]. Mol Microbiol, 2004, 54(3): 665-675. DOI: 10.1111/j.1365-2958.2004.04308.x [11] Guttman JA, Li Y, Wickham ME, et al.Attaching and effacing pathogen-induced tight junction disruption in vivo[J]. Cell Microbiol, 2006, 8(4): 634-645. DOI:10.1111/j.1462-5822.2005.00656.x [12] Tomson FL, Viswanathan VK, Kanack KJ, et al.Enteropathogenic Escherichia coli EspG disrupts microtubules and in conjunction with Orf3 enhances perturbation of the tight junction barrier[J]. Mol Microbiol, 2005, 56(2): 447-464. DOI: 10.1111/j.1365-2958.2005.04571.x [13] Matsuzawa T, Kuwae A, Abe A.Enteropathogenic Escherichia coli type III effectors EspG and EspG2 alter epithelial paracellular permeability[J]. Infect Immun, 2005, 73(10): 6283-6289. DOI: 10.1128/IAI.73.10.6283-6289.2005 [14] Muza-Moons MM, Schneeberger EE, Hecht GA.Enteropathogenic Escherichia coli infection leads to appearance of aberrant tight junctions strands in the lateral membrane of intestinal epithelial cells[J]. Cell Microbiol, 2004, 6(8): 783-793. DOI:10.1111/j.1462-5822.2004.00404.x [15] Tapia R, Kralicek SE, Hecht GA.EPEC effector EspF promotes Crumbs3 endocytosis and disrupts epithelial cell polarity[J]. Cell Microbiol, 2017, 19(11). DOI:10.1111/cmi.12757 [16] Martinez E, Schroeder GN, Berger CN, et al.Binding to Na(+) /H(+) exchanger regulatory factor 2 (NHERF2) affects trafficking and function of the enteropathogenic Escherichia coli type III secretion system effectors Map, EspI and NleH[J]. Cell Microbiol, 2010, 12(12): 1718-1731. DOI:10.1111/j.1462-5822.2010.01503.x [17] Singh AP, Aijaz S.Generation of a MDCK cell line with constitutive expression of the Enteropathogenic E. coli effector protein Map as an in vitro model of pathogenesis[J]. Bioengineered, 2015, 6(6): 335-341. DOI:10.1080/21655979.2015.1096456 [18] Kim J, Thanabalasuriar A, Chaworth-Musters T, et al.The bacterial virulence factor NleA inhibits cellular protein secretion by disrupting mammalian COPII function[J]. Cell Host Microbe, 2007, 2(3): 160-171. DOI:10.1016/j.chom.2007.07.010 [19] Thanabalasuriar A, Kim J, Gruenheid S.The inhibition of COPII trafficking is important for intestinal epithelial tight junction disruption during enteropathogenic Escherichia coli and Citrobacter rodentium infection[J]. Microbes Infect, 2013, 15(10-11): 738-744. DOI:10.1016/j.micinf.2013.05.001 [20] Glotfelty LG, Zahs A, Iancu C, et al.Microtubules are required for efficient epithelial tight junction homeostasis and restoration[J]. Am J Physiol Cell Physiol, 2014, 307(3): C245-254. DOI:10.1152/ajpcell.00336.2013 [21] Muza-Moons MM, Koutsouris A, Hecht G.Disruption of cell polarity by enteropathogenic Escherichia coli enables basolateral membrane proteins to migrate apically and to potentiate physiological consequences[J]. Infect Immun, 2003, 71(12): 7069-7078. DOI:10.1128/IAI.71.12.7069-7078.2003 [22] Charney AN, Kinsey MD, Myers L, et al.Na+-K+-activated adenosine triphosphatase and intestinal electrolyte transport. Effect of adrenal steroids[J]. J Clin Invest, 1975, 56(3): 653-660. DOI: 10.1172/JCI108135 [23] Gill RK, Borthakur A, Hodges K, et al.Mechanism underlying inhibition of intestinal apical Cl/OH exchange following infection with enteropathogenic E. coli[J]. J Clin Invest, 2007, 117(2): 428-437. DOI:10.1172/JCI29625 [24] Savkovic SD, Koutsouris A, Hecht G.PKC zeta participates in activation of inflammatory response induced by enteropathogenic E. coli[J]. Am J Physiol Cell Physiol, 2003, 285(3): C512-521. DOI:10.1152/ajpcell.00444.2002 [25] Huang Z, Sutton SE, Wallenfang AJ, et al.Structural insights into host GTPase isoform selection by a family of bacterial GEF mimics[J]. Nat Struct Mol Biol, 2009, 16(8): 853-860. DOI:10.1038/nsmb.1647 [26] Izaki T, Kamakura S, Kohjima M, et al.Phosphorylation-dependent binding of 14-3-3 to Par3beta, a human Par3-related cell polarity protein[J]. Biochem Biophys Res Commun, 2005, 329(1): 211-218. DOI:10.1016/j.bbrc.2005.01.115 [27] Viswanathan VK, Lukic S, Koutsouris A, et al.Cytokeratin 18 interacts with the enteropathogenic Escherichia coli secreted protein F (EspF) and is redistributed after infection[J]. Cell Microbiol, 2004, 6(10): 987-997. DOI:10.1111/j.1462-5822.2004.00416.x [28] Germane KL, Spiller BW.Structural and functional studies indicate that the EPEC effector, EspG, directly binds p21-activated kinase[J]. Biochemistry, 2011, 50(6): 917-919. DOI:10.1021/bi1020138 [29] Goosney DL, De Grado M, Finlay BB.Putting E. coli on a pedestal: a unique system to study signal transduction and the actin cytoskeleton[J]. Trends Cell Biol, 1999, 9(1): 11-14.DOI: 10.1016/S0962-8924(98)01418-4 [30] Mashukova A, Oriolo AS, Wald FA, et al.Rescue of atypical protein kinase C in epithelia by the cytoskeleton and Hsp70 family chaperones[J]. J Cell Sci, 2009, 122(Pt 14): 2491-2503. DOI:10.1242/jcs.046979 [31] Liao J, Omary MB.14-3-3 proteins associate with phosphorylated simple epithelial keratins during cell cycle progression and act as a solubility cofactor[J]. J Cell Biol, 1996, 133(2): 345-357. DOI:10.1083/jcb.133.2.345 [32] Ku NO, Michie S, Resurreccion EZ, et al.Keratin binding to 14-3-3 proteins modulates keratin filaments and hepatocyte mitotic progression[J]. Proc Natl Acad Sci U S A, 2002, 99(7): 4373-4378. DOI:10.1073/pnas.072624299
2019, Vol. 35 
