Epithelial microvilli establish an electrostatic barrier to microbial adhesion

Infection and Immunity

Volumn 82, Issue 7, 2014, Pages 2860-2871

  Bennett, Kaila M ^a,b   Walker, Sharon L ^b   Lo, David D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California Riverside   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; TIR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CACO 2 CELL LINE; CELL ADHESION; CELL GROWTH; CELL POLARITY; CELL TRANSPORT; CONTROLLED STUDY; ENTEROHEMORRHAGIC ESCHERICHIA COLI; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; MICROORGANISM; MICROVILLUS; MOLECULAR DYNAMICS; NUCLEOTIDE SEQUENCE; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STATIC ELECTRICITY; SURFACE CHARGE; SUSPENSION; TIGHT JUNCTION; ZETA POTENTIAL;

BACTERIAL ADHESION; CELL LINE, TUMOR; CLONING, MOLECULAR; ENTEROHEMORRHAGIC ESCHERICHIA COLI; EPITHELIAL CELLS; ESCHERICHIA COLI PROTEINS; HUMANS; MICROVILLI; STATIC ELECTRICITY; SURFACE PROPERTIES;

EID: 84903134109     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01681-14     Document Type: Article

References (41)

1. Rostgaard J, Thuneberg L. 1972. Electron microscopical observations on the brush border of proximal tubule cells of mammalian kidney. Z. Zellforsch. Mikrosk. Anat. 132:473-496. http://dx.doi.org/10.1007/BF00306637.
2. Perez de la Cruz Moreno M, Oth M, Deferme S, Lammert F, Tack J, Dressman J, Augustijns P. 2006. Characterization of fasted-state human intestinal fluids collected from duodenum and jejunum. J. Pharm. Pharmacol. 58:1079-1089. http://dx.doi.org/10.1211/jpp.58.8.0009.
3. Jantratid E, Janssen N, Reppas C, Dressman JB. 2008. Dissolution media simulating conditions in the proximal human gastrointestinal tract: an update. Pharm. Res. 25:1663-1676. http://dx.doi.org/10.1007/s11095-008-9569-4.
4. Fallingborg J. 1999. Intraluminal pH of the human gastrointestinal tract. Dan. Med. Bull. 46:183-196.
5. Lange K. 2000. Microvillar ion channels: cytoskeletal modulation of ion fluxes. J. Theor. Biol. 206:561-584. http://dx.doi.org/10.1006/jtbi.2000.2146.
6. Lange K. 2000. Regulation of cell volume via microvillar ion channels. J. Cell. Physiol. 185:21-35. http://dx.doi.org/10.1002/1097-4652(200010) 185:1<21::AID-JCP2>3.0.CO;2-D.
7. Kraehenbuhl JP, Neutra MR. 1992. Molecular and cellular basis of immune protection of mucosal surfaces. Physiol. Rev. 72:853-879.
8. Neutra MR, Kraehenbuhl JP. 1992 Transepithelial transport and mucosal defence I: the role ofMcells. Trends Cell Biol. 2:134-138. http://dx.doi.org/10.1016/0962-8924(92)90099-9.
9. Rajapaksa TE, Bennett KM, Hamer M, Lytle C, Rodgers VG, Lo DD. 2010. Intranasal M cell uptake of nanoparticles is independently influenced by targeting ligands and buffer ionic strength. J. Biol. Chem. 285: 23739-23746. http://dx.doi.org/10.1074/jbc.M110.126359.
10. Jones T, Yeaman MR, Sakoulas G, Yang SJ, Proctor RA, Sahl HG, Schrenzel J, Xiong YQ, Bayer AS. 2008. Failures in clinical treatment of Staphylococcus aureus infection with daptomycin are associated with alterations in surface charge, membrane phospholipid asymmetry, and drug binding. Antimicrob. Agents Chemother. 52:269-278. http://dx.doi.org/10.1128/AAC.00719-07.
11. Boks NP, Norde W, van der Mei HC, Busscher HJ. 2008. Forces involved in bacterial adhesion to hydrophilic and hydrophobic surfaces. Microbiology 154:3122-3133. http://dx.doi.org/10.1099/mic.0.2008/018622-0.
12. Hermansson M. 1999. The DLVO theory in microbial adhesion. Colloids Surf. B Interfaces 14:105-119.
13. Mutsaers SE, Whitaker D, Papadimitriou JM. 1996. Changes in the concentration of microvilli on the free surface of healing mesothelium are associated with alterations in surface membrane charge. J. Pathol. 180: 333-339.
14. Ito S. 1974. Form and function of the glycocalyx on free cell surface. Philos. Trans. R. Soc. Lond. B Biol. Sci. 891:55-66.
15. des Rieux A, Ragnarsson EG, Gullberg E, Preat V, Schneider YJ, Artursson P. 2005. Transport of nanoparticles across an in vitro model of the human intestinal follicle associated epithelium. Eur. J. Pharm. Sci. 25:455-465. http://dx.doi.org/10.1016/j.ejps.2005.04.015.
16. Wang J, Lopez-Fraga M, Rynko A, Lo DD. 2009. TNFR and LT beta R agonists induce follicle-associated epithelium andMcell specific genes in rat and human intestinal epithelial cells. Cytokine 47:69-76. http://dx.doi.org/10.1016/j.cyto.2009.05.001.
17. Rosenberg M, Gutnick D, Rosenberg E. 1980. Adherence of bacteria to hydrocarbons simple method for measuring cell-surface hydrophobicity. FEMS Microbiol. Lett. 9:29-33. http://dx.doi.org/10.1111/j.1574-6968.1980.tb05599.x.
18. Marcus IM, Herzberg M, Walker SL, Freger V. 2012. Pseudomonas aeruginosa attachment on QCM-D sensors: the role of cell and surface hydrophobicities. Langmuir 28:6396-6402. http://dx.doi.org/10.1021/la300333c.
19. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal. Biochem. 72:248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3.
20. Crotty Alexander LE, Maisey HC, Timmer AM, Rooijakkers SH, Gallo RL, von Kockritz-Blickwede M, Nizet V. 2010. M1T1 group A streptococcal pili promote epithelial colonization but diminish systemic virulence through neutrophil extracellular entrapment. J. Mol. Med. 88:371-381. http://dx.doi.org/10.1007/s00109-009-0566-9.
21. Mooseker MS, Howe CL. 1982. The brush border of intestinal epithelium: a model system for analysis of cell-surface architecture and motility. Methods Cell Biol. 25(Part B):143-174.
22. Hanono A, Garbett D, Reczek D, Chambers DN, Bretscher A. 2006. EPI64 regulates microvillar subdomains and structure. J. Cell Biol. 175: 803-813. http://dx.doi.org/10.1083/jcb.200604046.
23. Yonemura S, Tsukita S. 1999. Direct involvement of ezrin/radixin/moesin (ERM)-binding membrane proteins in the organization of microvilli in collaboration with activated ERM proteins. J. Cell Biol. 145: 1497-1509.
24. Berryman M, Franck Z, Bretscher A. 1993. Ezrin is concentrated in the apical microvilli of a wide variety of epithelial cells whereas moesin is found primarily in endothelial cells. J. Cell Sci. 105:1025-1043.
25. Garbett D, Bretscher A. 2012. PDZ interactions regulate rapid turnover of the scaffolding protein EBP50 in microvilli. J. Cell Biol. 198:195-203. http://dx.doi.org/10.1083/jcb.201204008.
26. Hase K, Kawano K, Nochi T, Pontes GS, Fukuda S, Ebisawa M, Kadokura K, Tobe T, Fujimura Y, Kawano S, Yabashi A, Waguri S, Nakato G, Kimura S, Murakami T, Iimura M, Hamura K, Fukuoka SI, Lowe AW, Itoh K, Kiyono H, Ohno H. 2009. Uptake through glycoprotein 2 of FimH(+) bacteria byMcells initiates mucosal immune response. Nature 462:226-230. http://dx.doi.org/10.1038/nature08529.
27. Hsieh EH, Fernandez X, Wang J, Hamer M, Calvillo S, Croft M, Kwon BS, Lo DD. 2010. CD137 is required forMcell functional maturation but not lineage commitment. Am. J. Pathol. 177:666-676. http://dx.doi.org/10.2353/ajpath.2010.090811.
28. Dersch P, Isberg RR. 1999. A region of the Yersinia pseudotuberculosis invasin protein enhances integrin-mediated uptake into mammalian cells and promotes self-association. EMBO J. 18:1199-1213. http://dx.doi.org/10.1093/emboj/18.5.1199.
29. Ottewill RH, Shaw JN. 1966. Stability of monodisperse polystyrene latex dispersions of various sizes. Discuss. Faraday Soc. 42:154-163.
30. Patel JC, Galan JE. 2005. Manipulation of the host actin cytoskeleton by Salmonella-all in the name of entry. Curr. Opin. Microbiol. 8:10-15. http://dx.doi.org/10.1016/j.mib.2004.09.001.
31. Guttman JA, Li YL, Wickham ME, Deng WY, Vogl AW, Finlay B. 2006. Attaching and effacing pathogen-induced tight junction disruption in vivo. Cell. Microbiol. 8:634-645. http://dx.doi.org/10.1111/j.1462-5822.2005.00656.x.
32. Tahoun A, Mahajan S, Paxton E, Malterer G, Donaldson DS, Wang D, Tan A, Gillespie TL, O'Shea M, Roe AJ, Shaw DJ, Gally DL, Lengeling A, Mabbott NA, Haas J, Mahajan A. 2012. Salmonella transforms follicle-associated epithelial cells into M cells to promote intestinal invasion. Cell Host Microbe 12:645-656. http://dx.doi.org/10.1016/j.chom.2012.10.009.
33. Chowdhury I, Walker SL. 2012. Deposition mechanisms of TiO2 nanoparticles in a parallel plate system. J. Colloid. Interface Sci. 369:16-22. http://dx.doi.org/10.1016/j.jcis.2011.12.019.
34. Jarvis KG, Giron JA, Jerse AE, McDaniel TK, Donnenberg MS, Kaper JB. 1995. Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc. Natl. Acad. Sci. U. S. A. 92:7996-8000. http://dx.doi.org/10.1073/pnas.92.17.7996.
35. Gruenheid S, DeVinney R, Bladt F, Goosney D, Gelkop S, Gish GD, Pawson T, Finlay BB. 2001. Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat. Cell Biol. 3:856-859. http://dx.doi.org/10.1038/ncb0901-856.
36. Finlay BB, Rosenshine I, Donnenberg MS, Kaper JB. 1992. Cytoskeletal composition of attaching and effacing lesions associated with enteropathogenic Escherichia coli adherence to HeLa cells. Infect. Immun. 60: 2541-2543.
37. Wolff C, Nisan I, Hanski E, Frankel G, Rosenshine I. 1998. Protein translocation into host epithelial cells by infecting enteropathogenic Escherichia coli. Mol. Microbiol. 28:143-155.
38. Croxen MA, Finlay BB. 2010. Molecular mechanisms of Escherichia coli pathogenicity. Nat. Rev. Microbiol. 8:26-38. http://dx.doi.org/10.1038/nrmicro2265.
39. Bouma G, Strober W. 2003. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 3:521-533. http://dx.doi.org/10.1038/nri1132.
40. Seiderer J, Elben I, Diegelmann J, Glas J, Stallhofer J, Tillack C, Pfennig S, Jurgens M, Schmechel S, Konrad A, Goke B, Ochsenkuhn T, Muller-Myhsok B, Lohse P, Brand S. 2008. Role of the novel th17 cytokine IL-17F in inflammatory bowel disease (IBD): upregulated colonic IL-17F expression in active Crohn's disease and analysis of the IL17F p.Hisl6lArg polymorphism in IBD. Inflamm. Bowel. Dis. 14:437-445. http://dx.doi.org/10.1002/ibd.20339.
41. Woodrow K, Bennett KM, Lo DD. 2012. Mucosal vaccine design and delivery. Annu. Rev. Biomed. Eng. 14:17-46. http://dx.doi.org/10.1146/annurev-bioeng-071811-150054.