Clostridium difficile toxins facilitate bacterial colonization by modulating the fence and gate function of colonic epithelium

Journal of Infectious Diseases

Volumn 209, Issue 7, 2014, Pages 1095-1104

  Kasendra, Magdalena ^a   Barrile, Riccardo ^a   Leuzzi, Rosanna ^a   Soriani, Marco ^a  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

Author keywords

adhesion; C. difficile; cell polarity; toxins

Indexed keywords

CLOSTRIDIUM DIFFICILE TOXIN A; CLOSTRIDIUM DIFFICILE TOXIN B; EGTAZIC ACID;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL TRANSLOCATION; BACTERIUM ADHERENCE; CELL MEMBRANE; CELL POLARITY; CELL STRAIN CACO 2; CELL SURFACE; CELLULAR DISTRIBUTION; COLON MUCOSA; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL;

ADHESION; C. DIFFICILE; CELL POLARITY; TOXINS;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL CULTURE TECHNIQUES; CLOSTRIDIUM DIFFICILE; COLON; ENTEROTOXINS; HUMANS; INTESTINAL MUCOSA; ORGAN CULTURE TECHNIQUES;

EID: 84898978251     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jit617     Document Type: Article

References (40)

1. Bryant DM, Mostov KE. From cells to organs: Building polarized tissue. Nat Rev Mol Cell Biol 2008; 9:887-901
2. Wang Q, Margolis B. Apical junctional complexes and cell polarity. Kidney Int 2007; 72:1448-58. (Pubitemid 350197955
3. Bonazzi M, Cossart P. Impenetrable barriers or entry portals? The role of cell-cell adhesion during infection. J Cell Biol 2011; 195: 349-58
4. Guttman JA, Finlay BB. Tight junctions as targets of infectious agents. Biochim Biophys Acta 2009; 1788:832-41
5. Bergelson JM. Intercellular junctional proteins as receptors and barriers to virus infection and spread. Cell Host Microbe 2009; 5:517-21
6. Engel J, Eran Y. Subversion of mucosal barrier polarity by pseudomonas aeruginosa. Front Microbiol 2011; 2:114
7. 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. Infect Immun 2003; 71:7069-78. (Pubitemid 37475339
8. Tan S, Tompkins LS, Amieva MR. Helicobacter pylori usurps cell polarity to turn the cell surface into a replicative niche. PLoS Pathog 2009; 5: E1000407
9. Carter GP, Rood JI, Lyras D. The role of toxin A and toxin B in Clostridium difficile-Associated disease: Past and present perspectives. Gut Microbes 2010; 1:58-64
10. Lyras D, O'Connor JR, Howarth PM, et al. Toxin B is essential for virulence of Clostridium difficile. Nature 2009; 458:1176-9
11. Kuehne SA, Cartman ST, Minton NP. Both, toxin A and toxin B, are important in Clostridium difficile infection. Gut Microbes 2011; 2: 252-5
12. Just I, Selzer J, Wilm M, von Eichel-Streiber C, Mann M, Aktories K. Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 1995; 375:500-3
13. Just I, Selzer J, von Eichel-Streiber C, Aktories K. The low molecular mass GTP-binding protein Rho is affected by toxin A from Clostridium difficile. J Clin Invest 1995; 95:1026-31
14. Popoff MR, Geny B. Rho/Ras-GTPase-dependent and-independent activity of clostridial glucosylating toxins. J Med Microbiol 2011; 60: 1057-69
15. Davies AH, Roberts AK, Shone CC, Acharya KR. Super toxins from a super bug: Structure and function of Clostridium difficile toxins. Biochem J 2011; 436:517-26
16. Viswanathan VK, Mallozzi MJ, Vedantam G. Clostridium difficile infection: An overview of the disease and its pathogenesis, epidemiology and interventions. Gut Microbes 2010; 1:234-42
17. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature 2002; 420:629-35. (Pubitemid 36764489
18. Volberg T, Geiger B, Kartenbeck J, Franke WW. Changes in membrane-microfilament interaction in intercellular adherens junctions upon removal of extracellular Ca2+ ions. J Cell Biol 1986; 102: 1832-42. (Pubitemid 16078767
19. Vllasaliu D, Fowler R, Garnett M, Eaton M, Stolnik S. Barrier characteristics of epithelial cultures modelling the airway and intestinal mucosa: A comparison. Biochem Biophys Res Commun 2011; 415: 579-85
20. Jaffe AB, Kaji N, Durgan J, Hall A. Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J Cell Biol 2008; 183:625-33
21. Matter K, Balda MS. Functional analysis of tight junctions. Methods 2003; 30:228-34. (Pubitemid 36677557
22. Artursson P, Karlsson J. Correlation between oral drug absorption in humans and apparent drug permeability coefficients in human intestinal epithelial (Caco-2) cells. Biochem Biophys Res Commun 1991; 175:880-5
23. Delie F, Rubas W. A human colonic cell line sharing similarities with enterocytes as a model to examine oral absorption: Advantages and limitations of the Caco-2 model. Crit Rev Ther Drug Carrier Syst 1997; 14:221-86. (Pubitemid 27355917
24. Natoli M, Leoni BD, D'Agnano I, et al. Cell growing density affects the structural and functional properties of Caco-2 differentiated monolayer. J Cell Physiol 2011; 226:1531-43
25. Hecht G, Pothoulakis C, LaMont JT, Madara JL. Clostridium difficile toxin A perturbs cytoskeletal structure and tight junction permeability of cultured human intestinal epithelial monolayers. J Clin Invest 1988; 82:1516-24. (Pubitemid 19007753
26. Lima AA, Lyerly DM, Wilkins TD, Innes DJ, Guerrant RL. Effects of Clostridium difficile toxins A and B in rabbit small and large intestine in vivo and on cultured cells in vitro. Infect Immun 1988; 56:582-8. (Pubitemid 18058786
27. Moore R, Pothoulakis C, LaMont JT, Carlson S, Madara JL. C. difficile toxin A increases intestinal permeability and induces Cl-secretion. Am J Physiol 1990; 259:G165-72
28. Riegler M, Sedivy R, Pothoulakis C, et al. Clostridium difficile toxin B is more potent than toxin A in damaging human colonic epithelium in vitro. J Clin Invest 1995; 95:2004-11
29. Bhavsar AP, Guttman JA, Finlay BB. Manipulation of host-cell pathways by bacterial pathogens. Nature 2007; 449:827-34. (Pubitemid 47598623
30. Cerquetti M, Serafino A, Sebastianelli A, Mastrantonio P. Binding of Clostridium difficile to Caco-2 epithelial cell line and to extracellular matrix proteins. FEMS Immunol Med Microbiol 2002; 32:211-8. (Pubitemid 34270512
31. Nusrat A, von Eichel-Streiber C, Turner JR, Verkade P, Madara JL, Parkos CA. Clostridium difficile toxins disrupt epithelial barrier function by altering membrane microdomain localization of tight junction proteins. Infect Immun 2001; 69:1329-36. (Pubitemid 32187577
32. Chen ML, Pothoulakis C, LaMont JT. Protein kinase C signaling regulates ZO-1 translocation and increased paracellular flux of T84 colonocytes exposed to Clostridium difficile toxin A. J Biol Chem 2002; 277: 4247-54. (Pubitemid 34968688
33. Chumbler NM, Farrow MA, Lapierre LA, et al. Clostridium difficile toxin B causes epithelial cell necrosis through an autoprocessing-independent mechanism. PLoS Pathog 2012; 8:e1003072
34. Vohra P, Poxton IR. Comparison of toxin and spore production in clinically relevant strains of Clostridium difficile. Microbiol 2011; 157: 1343-53
35. Borriello SP,Welch AR, Barclay FE, Davies HA. Mucosal association by Clostridium difficile in the hamster gastrointestinal tract. J Med Microbiol 1988; 25:191-6. (Pubitemid 18077701
36. Ozaki E, Kato H, Kita H, et al. Clostridium difficile colonization in healthy adults: Transient colonization and correlation with enterococcal colonization. J Med Microbiol 2004; 53:167-72. (Pubitemid 38223698
37. Jangi S, Lamont JT. Asymptomatic colonization by Clostridium difficile in infants: Implications for disease in later life. J Pediatr Gastroenterol Nutr 2010; 51:2-7
38. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: How bacterial recognition shapes intestinal function. Nat Rev Immunol 2010; 10:131-44
39. Ryan A, Lynch M, Smith SM, et al. A role for TLR4 in Clostridium difficile infection and the recognition of surface layer proteins. PLoS Pathog 2011; 7:e1002076
40. Yoshino YT, Kitazawa T, Ikeda M, et al. Clostridium difficile flagellin stimulates toll-like receptor 5, and toxin B promotes flagellin-induced chemokine production via TLR5. Life Sci 2013; 92:211-7