Enterobacter sakazakii invasion in human intestinal Caco-2 cells requires the host cell cytoskeleton and is enhanced by disruption of tight junction

Infection and Immunity

Volumn 76, Issue 2, 2008, Pages 562-570

  Kim, Kwang Pyo ^a,b   Loessner, Martin J ^a  

^a ETH ZURICH   (Switzerland)

^b Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

ARTICLE; BACTERIAL STRAIN; CELL POLARITY; CELL STRAIN CACO 2; CONTROLLED STUDY; CYTOSKELETON; DISEASE COURSE; ENTEROBACTER INFECTION; ENTEROBACTER SAKAZAKII; HOST CELL; HUMAN; HUMAN CELL; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; TIGHT JUNCTION;

BACTERIAL TRANSLOCATION; CACO-2 CELLS; COLONY COUNT, MICROBIAL; CYTOSKELETON; CYTOSOL; ENTEROBACTER SAKAZAKII; ENTEROCYTES; HUMANS; TIGHT JUNCTIONS;

EID: 39149141382     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00937-07     Document Type: Article

References (48)

1. Adegbola, R. A., and D. C. Old. 1983. Fimbrial haemagglutinins in Enterobacter species. J. Gen. Microbiol. 129:2175-2180.
2. Biering, G., S. Karlsson, N. C. Clark, K. E. Jonsdottir, P. Ludvigsson, and O. Steingrimsson. 1989. Three cases of neonatal meningitis caused by Enterobacter sakazakii in powdered milk. J. Clin. Microbiol. 27:2054-2056.
3. Breeuwer, P., A. Lardeau, M. Peterz, and H. M. Joosten. 2003. Desiccation and heat tolerance of Enterobacter sakazakii. J. Appl. Microbiol. 95:967-973.
4. Cossart, P., and P. J. Sansonetti. 2004. Bacterial invasion: the paradigms of enteroinvasie pathogens. Science 304:242-248.
5. Criss, A. K., and J. E. Casanova. 2003. Coordinate regulation of Salmonella enterica serovar Typhimurium invasion of epithelial cells by the Arp2/3 complex and Rho GTPases. Infect. Immun. 71:2885-2891.
6. Cruz, N., X. Alvarez, R. D. Berg, and E. A. Deitch. 1994. Bacterial translocation across enterocytes: results of a study of bacterial-enterocyte interactions utilizing Caco-2 cells. Shock 1:67-72.
7. Drudy, D., N. R. Mullane, T. Yuinn, P. G. Wall, and S. Fanning. 2006. Enterobacter sakazakii: an emerging pathogen in powdered infant formula. Clin. Infect. Dis. 42:996-1002.
8. Faix, R. G., and J. T. Adams. 1994. Neonatal necrotizing enterocolitis: current concepts and controversies. Adv. Pediatr. Infect. Dis. 9:1-36.
9. Farmer, J. J., III, M. A. Asbury, F. W. Hickman, D. J. Brenner, and the Enterobacteriaceae Study Group. 1980. Enterobacter sakazakii: a new species of "Enterobacteriaceae" isolated from clinical specimens. Int. J. Syst. Bacteriol. 30:569-584.
10. Finlay, B. B., and S. Falkow. 1989. Common themes in microbial pathogenicity. Microbiol. Rev. 53:210-230.
11. Gahring, L. C., F. Heffron, B. B. Finlay, and S. Falkow. 1990. Invasion and replication of Salmonella typhimurium in animal cells. Infect. Immun. 58: 443-448.
12. Gaillard, J. L., P. Berche, J. Mounier, S. Richard, and P. Sansonetti. 1987. In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect. Immun. 55:2822-2829.
13. Reference deleted.
14. Hamilton, J. V., M. J. Lehane, and H. R. Braig. 2003. Isolation of Enterobacter sakazakii from midgut of Stomoxys calcitrans. Emerg. Infect. Dis. 9:1355-1356.
15. Harmsen, H. J., A. C. Wildeboer-Veloo, G. C. Raangs, A. A. Wagendorp, N. Klijn, J. G. Bindels, and G. W. Wellings. 2000. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J. Pediatr. Gastroenterol. Nutr. 30:61-67.
16. International Commission on Microbiological Specifications for Foods (ICMSF). 2002. Microorganisms in food 7. Microbiological testing in food safety management. Kluwer Academic/Plenum Publishers, New York, NY.
17. Iversen, C., M. Lane, and S. J. Forsythe. 2004. The growth profile, thermotolerance and bilfilm formation of Enterobacter sakazakii grown in infant formula milk. Lett. Appl. Microbiol. 38:378-382.
18. Jones, B. D., H. F. Paterson, A. Hall, and S. Falkow. 1993. Salmonella typhimurium induces membrane ruffling by a growth factor-receptor-independent mechanism. Proc. Natl. Acad. Sci. USA 90:10390-10394.
19. Jumarie, C., and C. Malo. 1991. Caco-2 cells cultured in serum-free medium as a model for the study of enterocytic differentiation in vitro. J. Cell. Physiol. 149:24-33.
20. Kandhai, M. C., M. W. Reij, L. G. Gorris, O. Guillaume-Gentil, and M. van Schothorst. 2004. Occurrence of Enterobacter sakazakii in food production environments and households. Lancet 363:39-40.
21. Kim, K.-P., J. Klumpp, and M. J. Loessner. 2007. Enterobacter sakazakii bacteriophages can prevent bacterial growth in reconstituted infant formula. Int. J. Food Microbiol. 115:195-203.
22. Kleiman, M. B., S. D. Allen, P. Neal, and J. Reynolds. 1981. Meningoencephalitis and compartmentalization of the cerebral ventricles caused by Enterobacter sakazakii. J. Clin. Microbiol. 14:352-354.
23. Kuzina, L. V., J. J. Peloquin, D. C. Vacek, and T. A. Miller. 2001. Isolation and identification of bacteria associated with adult laboratory Mexican fruit flies, Anastrepa ludens (Diptera: Tephritidae). Curr. Microbiol. 42:290-294.
24. Lebner, A., R. Riedel, L. Eberl, P. Breeuwer, B. Diep, and R. Stephan. 2005. Biofilm formation, extracellular polysaccharide production, and cell-to-cell signaling in various Enterobacter sakazakii strains: aspects promoting environmental persistence. J. Food Prot. 68:2287-2294.
25. Loessner, M. J., K. Kramer, F. Ebel, and S. Scherer. 2002. C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates. Mol. Microbiol. 44:335-349.
26. Mange, J. P., R. Stephan, N. Borel, P. Wild, K. S. Kim, A. Pospichil, and A. Lehner. 2006. Adhesive properties of Enterobacter sakazakii to human epithelial and brain endothelial cells. BMC Microbiol. 6:58.
27. Mengaud, J., H. Ohayon, P. Gounon, R.-M. Mege, and P. Cossart. 1996. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84:923-932.
28. Miyoshi, J., and Y. Takai. 2005. Molecular perspective on tight-junction assembly and epithelial polarity. Adv. Drug Deliv. Rev. 57:815-855.
29. Moriez, R., C. Salvador-Cartier, V. Theodorou, J. Fioramonti, H. Eutamene, and L. Bueno. 2005. Myosin light chain kinase is involved in lipopoiysaccharide-induced disruption of colonic epithelial barrier and bacterial translocation in rats. Am. J. Pathol. 267:1071-1079.
30. Muytjens, H. L., H. C. Zanen, H. J. Sonderkamp, L. A. Kollée, I. K. Wachsmuth, and J. J. Farmer III. 1983. Analysis of eight cases of neonatal meningitis and sepsis due to Enterobacter sakazakii. J. Clin. Microbiol. 18: 115-120.
31. Reference deleted.
32. Nazarowec-White, M., and J. M. Farber. 1997. Incidence, survival and growth of Enterobacter sakazakii in infant formula. J. Food Prot. 60:226-230.
33. Nazarowec-White, M., and J. M. Farber. 1997. Thermal resistance of Enterobacter sakazakii in reconstituted dried-infant formula. Lett. Appl. Microbiol. 24:9-13.
34. Oelschlaeger, T. A., P. Guerry, and D. J. Kopecko. 1993. Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii. Proc. Natl. Acad. Sci. USA 90:6884-6888.
35. Pagotto, F. J., M. Nazarowec-White, S. Bidawid, and J. M. Farber. 2003. Enterobacter sakazakii: infectivity and enterotoxin production in vitro and in vivo. J. Food Protect. 66:370-375.
36. Portzehl, H., P. C. Caldwell, and J. C. Rueegg. 1964. The dependence of contraction and relaxation of muscle fibres from the crab Maia squinado on the internal concentration of free calcium ions. Biochim. Biophys. Acta 79:581-591.
37. Postupa, R., and E. Aldova. 1984. Enterobacter sakazakii: a Tween 80 esterase-positive representative of the genus Enterobacter isolated from powdered milk specimens. J. Hyg. Epidemiol. Microbiol. Immunol. 28:435-440.
38. Rousset, M. 1986. The human colon carcinoma cell lines HT-29 and Caco-2: Two in vitro models for the study of intestinal differentiation. Biochimie 68:1035-1040.
39. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Sanders, W. E., Jr., and C. C. Sanders. 1997. Enterobacter spp.: pathogens poised to flourish at the turn of the century. Clin. Microbiol. Rev. 10:220-241.
41. Sreenivasan, P. K., D. H. Meyer, and P. M. Fives-Taylor. 1993. Requirements for invasion of epithelial cells by Actinobacillus actinomycetemcomitans. Infect. Immun. 61:1239-1245.
42. Townsend, S., J. C. Barron, C. Loc-Carrillo, and S. Forsythe. 2007. The presence of endotoxin in powdered infant formula milk and the influence of endotoxin and Enterobacter sakazakii on bacterial translocation in the infant rat. Food Microbiol. 24:67-74.
43. Townsend, S. M., E. Hurrell, I. Gonzlaez-Gomez, J. Lowe, J. G. Frye, S. Forsythe, and J. L. Badger. 2007. Enterobacter sakazakii invades brain capillary endothelial cells, persists in human macrophages influencing cytokine secretion and induces severe brain pathology in the neonatal rat. Microbiology 153:3538-3547.
44. van Acker, J., F. de Smet, G. Muyldermans, A. Bougatef, A. Naessens, and S. Lauwers. 2001. Outbreak of necrotizing enterocolitis associated with Enterobacter sakazakii in powdered milk formula. J. Clin. Microbiol. 39:293-297.
45. Walker-Smith, J. 1972. Variation of small intestinal morphology with age. Arch. Dis. Child. 47:80-83.
46. Weir, E. 2002. Powdered infant formula and fatal infection with Enterobacter sakazakii. CMAJ 166:1570.
47. Willis, J., and J. E. Robinson. 1988. Enterobacter sakazakii meningitis in neonates. Pediatr. Infect. Dis. J. 7:196-199.
48. Wooding, F. B. P., M. W. Smith, and H. Craig. 1978. The ultrastructure of the neonatal pig colon. Am. J. Anat. 152:269-286.