Differential phenotypic diversity among epidemic-spanning salmonella enterica serovar enteritidis isolates from humans or animals

Applied and Environmental Microbiology

Volumn 76, Issue 20, 2010, Pages 6812-6820

  Yim, Lucía ^a   Betancor, Laura ^a   Martinez, Arací ^a   Giossa, Gerardo ^b   Bryant, Clare ^c   Maskell, Duncan ^c   Chabalgoity, Jose A ^a  

^a DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^b UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CACO-2 CELLS; COMPARATIVE GENOMICS; EGG ALBUMEN; FOOD BORNE DISEASE; INVASIVENESS; PATHOGENIC POTENTIAL; PHENOTYPIC DIVERSITY; REFERENCE STRAINS; SALMONELLA ENTERICA; SEROVAR; URUGUAY; VIRULENT STRAINS;

ANIMALS; ASSAYS; EPIDEMIOLOGY; HEALTH; SALMONELLA;

PATHOLOGY;

BACTERIUM; BIOASSAY; DISEASE INCIDENCE; EPIDEMIC; FITNESS; GASTROENTERITIS; GENOMICS; PATHOGEN; PHENOTYPIC PLASTICITY; PROTEIN; SURVIVAL; VIRULENCE;

ANIMAL; ANIMAL SALMONELLOSIS; ARTICLE; BIRD DISEASE; CELL STRAIN CACO 2; CHICKEN; CLASSIFICATION; DISEASE MODEL; EGG; EPITHELIUM CELL; GENETICS; HUMAN; ISOLATION AND PURIFICATION; LOCOMOTION; MICROBIAL VIABILITY; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; SALMONELLA ENTERITIDIS; SALMONELLOSIS; URUGUAY; VIRULENCE;

ANIMALS; CACO-2 CELLS; CHICKENS; DISEASE MODELS, ANIMAL; EGGS; EPITHELIAL CELLS; HUMANS; LOCOMOTION; MICROBIAL VIABILITY; POULTRY DISEASES; SALMONELLA ENTERITIDIS; SALMONELLA INFECTIONS; SALMONELLA INFECTIONS, ANIMAL; URUGUAY; VIRULENCE;

ANIMALIA; GALLUS GALLUS; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS;

EID: 77958582905     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00497-10     Document Type: Article

References (53)

1. Anderle, P., M. Rumbo, F. Sierro, R. Mansourian, P. Michetti, M. A. Roberts, and J. P. Kraehenbuhl. 2005. Novel markers of the human follicleassociated epithelium identified by genomic profiling and microdissection. Gastroenterology 129:321-327.
2. Barrow, P. A. 1991. Experimental infection of chickens with Salmonella enteritidis. Avian Pathol. 20:145-153.
3. Bäumler, A. J., B. M. Hargis, and R. M. Tsolis. 2000. Tracing the origins of Salmonella outbreaks. Science 287:50-52.
4. Betancor, L., F. Schelotto, A. Martínez, M. Pereira, G. Algorta, M. A. Rodríguez, R. Vignoli, and J. A. Chabalgoity. 2004. Random amplified polymorphic DNA and phenotyping analysis of Salmonella enterica serovar Enteritidis isolates collected from humans and poultry in Uruguay from 1995 to 2002. J. Clin. Microbiol. 42:1155-1162.
5. Betancor, L., L. Yim, M. Fookes, A. Martinez, N. R. Thomson, A. Ivens, S. Peters, C. Bryant, G. Algorta, S. Kariuki, F. Schelotto, D. Maskell, G. Dougan, and J. A. Chabalgoity. 2009. Genomic and phenotypic variation in epidemic-spanning Salmonella enterica serovar Enteritidis isolates. BMC Microbiol. 9:237.
6. Betancor, L., M. Pereira, A. Martinez, G. Giossa, M. Fookes, K. Flores, P. Barrios, V. Repiso, R. Vignoli, N. Cordeiro, G. Algorta, N. Thomson, D. Maskell, F. Schelotto, and J. A. Chabalgoity. 2010. Prevalence of Salmonella enterica in poultry and eggs in Uruguay during an epidemic due to Salmonella enterica serovar Enteritidis. J. Clin. Microbiol. 48:2413-2423.
7. Bolton, A. J., M. P. Osborne, and J. Stephen. 2000. Comparative study of the invasiveness of Salmonella serotypes Typhimurium, Choleraesuis and Dublin for Caco-2 cells, HEp-2 cells and rabbit ileal epithelia. J. Med. Microbiol. 49:503-511.
8. Clavijo, R. I., C. Loui, G. L. Andersen, L. W. Riley, and S. Lu. 2006. Identification of genes associated with survival of Salmonella enterica serovar Enteritidis in chicken egg albumen. Appl. Environ. Microbiol. 72:1055-1064. (Pubitemid 43271210)
9. Cogan, T. A., and T. J. Humphrey. 2003. The rise and fall of Salmonella Enteritidis in the UK. J. Appl. Microbiol. 94:114S-119S.
10. Danyluk, M. D., M. Nozawa-Inoue, K. R. Hristova, K. M. Scow, B. Lampinen, and L. J. Harris. 2008. Survival and growth of Salmonella Enteritidis PT 30 in almond orchard soils. J. Appl. Microbiol. 104:1391-1399.
11. Das, E., G. C. Gurakan, and A. Bayindirli. 2006. Effect of controlled atmosphere storage, modified atmosphere packaging and gaseous ozone treatment on the survival of Salmonella Enteritidis on cherry tomatoes. Food Microbiol. 23:430-438.
12. Dibb-Fuller, M. P., E. Allen-Vercoe, C. J. Thorns, and M. J. Woodward. 1999. Fimbriae- and flagella-mediated association with and invasion of cultured epithelial cells by Salmonella enteritidis. Microbiology 145(Pt. 5):1023-1031.
13. Eckmann, L., M. F. Kagnoff, and J. Fierer. 1993. Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect. Immun. 61: 4569-4574.
14. Eichelberg, K., C. C. Ginocchio, and J. E. Galan. 1994. Molecular and functional characterization of the Salmonella typhimurium invasion genes invB and invC: homology of InvC to the F0F1 ATPase family of proteins. J. Bacteriol. 176:4501-4510.
15. Ellermeier, J. R., and J. M. Slauch. 2007. Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr. Opin. Microbiol. 10:24-29.
16. Finlay, B. B., and J. H. Brumell. 2000. Salmonella interactions with host cells: in vitro to in vivo. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355:623-631.
17. Galán, J. E., and R. Curtiss III. 1989. Cloning and molecular characteriza-tion of genes whose products allow Salmonella Typhimurium to penetrate tissue culture cells. Proc. Natl. Acad. Sci. U. S. A. 86:6383-6387.
18. Galanis, E., D. M. Lo Fo Wong, M. E. Patrick, N. Binsztein, A. Cieslik, T. Chalermchikit, A. Aidara-Kane, A. Ellis, F. J. Angulo, H. C. Wegener, and World Health Organization Global Salm-Surv. 2006. Web-based surveillance and global Salmonella distribution, 2000-2002. Emerg. Infect. Dis. 12:381-388.
19. Gantois, I., R. Ducatelle, F. Pasmans, F. Haesebrouck, and F. Van Immerseel. 2008. Salmonella enterica serovar Enteritidis genes induced during oviduct colonization and egg contamination in laying hens. Appl. Environ. Microbiol. 74:6616-6622.
20. Gewirtz, A. T., P. O. Simon, Jr., C. K. Schmitt, L. J. Taylor, C. H. Hagedorn, A. D. O'Brien, A. S. Neish, and J. L. Madara. 2001. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J. Clin. Invest. 107:99-109.
21. Guard-Petter, J. 2001. The chicken, the egg and Salmonella enteritidis. Environ. Microbiol. 3:421-430.
22. Hald, T., D. Vose, H. C. Wegener, and T. Koupeev. 2004. A Bayesian approach to quantify the contribution of animal-food sources to human salmonelosis. Risk Anal. 24:255-269.
23. Humphrey, T. J. 1994. Contamination of egg shell and contents with Salmonella enteritidis: a review. Int. J. Food Microbiol. 21:31-40.
24. Jones, B. D., C. A. Lee, and S. Falkow. 1992. Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect. Immun. 60:2475-2480.
25. Kang, H., C. Loui, R. I. Clavijo, L. W. Riley, and S. Lu. 2006. Survival characteristics of Salmonella enterica serovar Enteritidis in chicken egg albumen. Epidemiol. Infect. 134:967-976.
26. Keller, L. H., C. E. Benson, K. Krotec, and R. J. Eckroade. 1995. Salmonella enteritidis colonization of the reproductive tract and forming and freshly laid eggs of chickens. Infect. Immun. 63:2443-2449.
27. Keller, L. H., D. M. Schifferli, C. E. Benson, S. Aslam, and R. J. Eckroade. 1997. Invasion of chicken reproductive tissues and forming eggs is not unique to Salmonella enteritidis. Avian Dis. 41:535-539.
28. Kim, S. H., and C. I. Wei. 2007. Invasiveness and intracellular growth of multidrug-resistant Salmonella and other pathogens in Caco-2 cells. J. Food Sci. 72:M72-M78.
29. Langridge, G. C., J. Wain, and S. Nair. 18 August 2008, posting date. Chapter 8.6.2.2, Invasive salmonellosis in humans. In A. Bock et al. (ed.), EcoSal-Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, DC. doi:10:1128/ecosal.8.6.2.2.
30. La Ragione, R. M., W. A. Cooley, P. Velge, M. A. Jepson, and M. J. Woodward. 2003. Membrane ruffling and invasion of human and avian cell lines is reduced for aflagellate mutants of Salmonella enterica serotype Enteritidis. Int. J. Med. Microbiol. 293:261-272.
31. Lu, S., P. B. Killoran, and L. W. Riley. 2003. Association of Salmonella enterica serovar enteritidis yafD with resistance to chicken egg albumen. Infect. Immun. 71:6734-6741.
32. Lu, S., A. R. Manges, Y. Xu, F. C. Fang, and L. W. Riley. 1999. Analysis of virulence of clinical isolates of Salmonella enteritidis in vivo and in vitro. Infect. Immun. 67:5651-5657.
33. Maurelli, A. T., R. E. Fernandez, C. A. Bloch, C. K. Rode, and A. Fasano. 1998. "Black holes" and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 95:3943-3948.
34. McCormick, B. A., S. I. Miller, D. Carnes, and J. L. Madara. 1995. Transepithelial signaling to neutrophils by salmonellae: a novel virulence mechanism for gastroenteritis. Infect. Immun. 63:2302-2309.
35. Mohle-Boetani, J. C., J. Farrar, P. Bradley, J. D. Barak, M. Miller, R. Mandrell, P. Mead, W. E. Keene, K. Cummings, S. Abbott, and S. B. Werner. 2009. Salmonella infections associated with mung bean sprouts: epidemiological and environmental investigations. Epidemiol. Infect. 137:357-366.
36. Penheiter, K. L., N. Mathur, D. Giles, T. Fahlen, and B. D. Jones. 1997. Non-invasive Salmonella typhimurium mutants are avirulent because of an inability to enter and destroyMcells of ileal Peyer's patches. Mol. Microbiol. 24:697-709.
37. Rabsch, W., H. Tschäpe, and A. J. Bäumler. 2001. Non-typhoidal salmonellosis: emerging problems. Microbes Infect. 3:237-247.
38. Raffatellu, M., R. P. Wilson, D. Chessa, H. Andrews-Polymenis, Q. T. Tran, S. Lawhon, S. Khare, L. G. Adams, and A. J. Bäumler. 2005. SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype Typhimurium invasion of epithelial cells. Infect. Immun. 73:146-154.
39. Saeed, A. M., S. T. Walk, M. Arshad, and T. S. Whittam. 2006. Clonal structure and variation in virulence of Salmonella Enteritidis isolated from mice, chickens, and humans. J. AOAC Int. 89:504-511.
40. Schmitt, C. K., J. S. Ikeda, S. C. Darnell, P. R. Watson, J. Bispham, T. S. Wallis, D. L. Weinstein, E. S. Metcalf, and A. D. O'Brien. 2001. Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect. Immun. 69:5619-5625.
41. Sierro, F., B. Dubois, A. Coste, D. Kaiserlian, J. P. Kraehenbuhl, and J. C. Sirard. 2001. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 98:13722-13727.
42. Stecher, B., A. J. Macpherson, S. Hapfelmeier, M. Kremer, T. Stallmach, and W. D. Hardt. 2005. Comparison of Salmonella enterica serovar Typhimurium colitis in germfree mice and mice pretreated with streptomycin. Infect. Immun. 73:3228-3241.
43. Stecher, B., M. Barthel, M. C. Schlumberger, L. Haberli, W. Rabsch, M. Kremer, and W. D. Hardt. 2008. Motility allows S. Typhimurium to benefit from the mucosal defence. Cell. Microbiol. 10:1166-1180.
44. Tallant, T., A. Deb, N. Kar, J. Lupica, M. J. de Veer, and J. A. DiDonato. 2004. Flagellin acting via TLR5 is the major activator of key signaling pathways leading to NF-kappa B and proinflammatory gene program activation in intestinal epithelial cells. BMC Microbiol. 4:33.
45. Thorns, C. 2000. Bacterial food-borne zoonoses. Rev. Sci. Tech. 19:226-239.
46. van Asten, F. J., H. G. Hendriks, J. F. Koninkx, and J. E. van Dijk. 2004. Flagella-mediated bacterial motility accelerates but is not required for Salmonella serotype Enteritidis invasion of differentiated Caco-2 cells. Int. J. Med. Microbiol. 294:395-399.
47. Van Asten, F. J., H. G. Hendriks, J. F. Koninkx, B. A. Van der Zeijst, and W. Gaastra. 2000. Inactivation of the flagellin gene of Salmonella enterica serotype Enteritidis strongly reduces invasion into differentiated Caco-2 cells. FEMS Microbiol. Lett. 185:175-179.
48. Velge, P., A. Cloeckaert, and P. Barrow. 2005. Emergence of Salmonella epidemics: the problems related to Salmonella enterica serotype Enteritidis and multiple antibiotic resistance in other major serotypes. Vet. Res. 36: 267-288.
49. Wallis, T. S., and E. E. Galyov. 2000. Molecular basis of Salmonella-induced enteritis. Mol. Microbiol. 36:997-1005.
50. Winter, S. E., P. Thiennimitr, S. P. Nuccio, T. Haneda, M. G. Winter, R. P. Wilson, J. M. Russell, T. Henry, Q. T. Tran, S. D. Lawhon, G. Gomez, C. L. Bevins, H. Russmann, D. M. Monack, L. G. Adams, and A. J. Baumler. 2009. Contribution of flagellin pattern recognition to intestinal inflammation during Salmonella enterica serotype Typhimurium infection. Infect. Immun. 77:1904-1916.
51. Yang, S. K., L. Eckmann, A. Panja, and M. F. Kagnoff. 1997. Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells. Gastroenterology 113:1214-1223.
52. Zeng, H., A. Q. Carlson, Y. Guo, Y. Yu, L. S. Collier-Hyams, J. L. Madara, A. T. Gewirtz, and A. S. Neish. 2003. Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J. Immunol. 171:3668-3674.
53. Zhang, S., R. L. Santos, R. M. Tsolis, S. Stender, W. D. Hardt, A. J. Bäumler, and L. G. Adams. 2002. The Salmonella enterica serotype Typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect. Immun. 70:3843-3855.