Virulence traits in cronobacter species isolated from different sources

Canadian Journal of Microbiology

Volumn 57, Issue 9, 2011, Pages 735-744

  Cruz, Ariadnna ^a   Xicohtencatl Cortes, Juan ^b   González Pedrajo, Bertha ^c   Bobadilla, Miriam ^d   Eslava, Carlos ^a   Rosas, Irma ^c  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b HOSPITAL INFANTIL DE MÉXICO FEDERICO GÓMEZ   (Mexico)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^d INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

Author keywords

Adherence; Biofilm; Cronobacter spp.; Invasion; Putative virulence genes

Indexed keywords

ADHERENCE; BIOINFORMATIC ANALYSIS; CRONOBACTER SPP.; ENTEROBACTER; FOOD-BORNE PATHOGENS; INVASION; PATHOGENIC MECHANISMS; PLASMINOGEN ACTIVATORS; PULSED FIELD GEL ELECTROPHORESIS; VIRULENCE GENE;

BIOFILMS; BIOINFORMATICS; ELECTROPHORESIS; INTERNET PROTOCOLS; POLYMERASE CHAIN REACTION;

GENES;

BACTERIAL DNA; BACTERIAL PROTEIN; BACTERIAL RNA; HEMOLYSIN TYPE 3; PLASMINOGEN ACTIVATOR; RNA 16S; SIDEPHORE INTERACTING PROTEIN; UNCLASSIFIED DRUG;

ADAPTIVE RADIATION; BACTERIUM; BIOFILM; BIOLOGICAL INVASION; CELL ORGANELLE; CLUSTER ANALYSIS; ELECTROKINESIS; GEL; GENETIC ANALYSIS; IDENTIFICATION METHOD; INFECTIVITY; NEONATE; PATHOGENICITY; PATHOTYPE; POLYMERASE CHAIN REACTION; VIRULENCE;

ARTICLE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; BIOFILM; BIOINFORMATICS; CONTROLLED STUDY; CRONOBACTER DUBLINENSIS; CRONOBACTER MALONATICUS; CRONOBACTER MUYTJENSII; CRONOBACTER TURICENSIS; ENTEROBACTER; ENTEROBACTER SAKAZAKII; GENE CLUSTER; GENETIC ANALYSIS; GENOTYPE; HEP 2 CELL; HUMAN; HUMAN CELL; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; RNA SEQUENCE;

BIOFILMS; CRONOBACTER; ELECTROPHORESIS, GEL, PULSED-FIELD; ENTEROBACTERIACEAE INFECTIONS; GENES, BACTERIAL; HUMANS; PHENOTYPE; PHYLOGENY; POLYMERASE CHAIN REACTION; SIDEROPHORES; VIRULENCE; VIRULENCE FACTORS;

ENTEROBACTER SAKAZAKII; NEGIBACTERIA;

EID: 80052944630     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/w11-063     Document Type: Article

References (42)

1. Baida, G.E., and Kuzmin, N.P. 1996. Mechanism of action of hemolysin III from Bacillus cereus. Biochim. Biophys. Acta, 1284(2): 122-124. doi:10.1016/S0005-2736(96)00168-X. PMID:8962879.
2. Baldwin, A., Loughlin, M., Caubilla-Barron, J., Kucerova, E., Manning, G., Dowson, C., and Forsythe, S. 2009. Multilocus sequence typing of Cronobacter sakazakii and Cronobacter malonaticus reveals stable clonal structures with clinical significance which do not correlate with biotypes. BMC Microbiol. 9(1): 223. doi:10.1186/1471-2180-9-223. PMID:19852808.
3. Beuchat, L.R., Kim, H., Gurtler, J.B., Lin, L.C., Ryu, J.H., and Richards, G.M. 2009. Cronobacter sakazakii in foods and factors affecting its survival, growth, and inactivation. Int. J. Food Microbiol. 136(2): 204-213. doi:10.1016/j.ijfoodmicro.2009.02.029. PMID:19346021.
4. Bowen, A.B., and Braden, C.R. 2006. Invasive Enterobacter sakazakii disease in infants. Emerg. Infect. Dis. 12(8): 1185-1189. PMID:16965695.
5. Caubilla-Barron, J., Hurrell, E., Townsend, S., Cheetham, P., Loc-Carrillo, C., Fayet, O., et al. 2007. Genotypic and phenotypic analysis of Enterobacter sakazakii strains from an outbreak resulting in fatalities in a neonatal intensive care unit in France. J. Clin. Microbiol. 45(12): 3979-3985. doi:10.1128/JCM.01075-07. PMID:17928419É.
6. Chen, Y.C., Chang, M.C., Chuang, Y.C., and Jeang, C.L. 2004. Characterization and virulence of hemolysin III from Vibrio vulnificus. Curr. Microbiol. 49(3): 175-179. doi:10.1007/s00284-004-4288-5. PMID:15386100.
7. Donlan, R.M., and Costerton, J.W. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15(2): 167-193. doi:10.1128/CMR.15.2.167-193.2002. PMID:11932229.
8. Franco, A.A., Kothary, M.H., Gopinath, G., Jarvis, K.G., Grim, C.J., Hu, L., et al. 2011. Cpa, the outer membrane protease of Cronobacter sakazakii, activates plasminogen and mediates resistance to serum bactericidal activity. Infect. Immun. 79(4): 1578-1587. doi:10.1128/IAI.01165-10. PMID:21245266.
9. Gorvel, J.P., and Moreno, E. 2002. Brucella intracellular life: from invasion to intracellular replication. Vet. Microbiol. 90(1-4): 281-297. doi:10.1016/S0378-1135(02)00214-6. PMID:12414149.
10. Hartmann, I., Carranza, P., Lehner, A., Stephan, R., Eberl, L., and Riedel, K. 2010. Genes involved in Cronobacter sakazakii biofilm formation. Appl. Environ. Microbiol. 76(7): 2251-2261. doi:10.1128/AEM.00930-09. PMID:20118366.
11. Healy, B., Huynh, S., Mullane, N., O'Brien, S., Iversen, C., Lehner, A., et al. 2009. Microarray-based comparative genomic indexing of the Cronobacter genus (Enterobacter sakazakii). Int. J. Food Microbiol. 136(2): 159-164. doi:10.1016/j.ijfoodmicro.2009.07.008. PMID:19664834.
12. Healy, B., Cooney, S., O'Brien, S., Iversen, C., Whyte, P., Nally, J., et al. 2010. Cronobacter (Enterobacter sakazakii): an opportunistic foodborne pathogen. Foodborne Pathog. Dis. 7(4): 339-350. doi:10.1089/fpd.2009.0379. PMID:19958103.
13. Hunter, C.J., Singamsetty, V.K., Chokshi, N.K., Boyle, P., Camerini, V., Grishin, A.V., et al. 2008. Enterobacter sakazakii enhances epithelial cell injury by inducing apoptosis in a rat model of necrotizing enterocolitis. J. Infect. Dis. 198(4): 586-593. doi:10.1086/590186. PMID:18588483.
14. Hurrell, E., Kucerova, E., Loughlin, M., Caubilla-Barron, J., and Forsythe, S.J. 2009a. Biofilm formation on enteral feeding tubes by Cronobacter sakazakii, Salmonella serovars and other Enterobacteriaceae. Int. J. Food Microbiol. 136(2): 227-231. doi:10.1016/j.ijfoodmicro.2009.08.007. PMID:19720416.
15. Hurrell, E., Kucerova, E., Loughlin, M., Caubilla-Barron, J., Hilton, A., Armstrong, R., et al. 2009b. Neonatal enteral feeding tubes as loci for colonization by members of the Enterobacteriaceae. BMC Infect. Dis. 9(1): 146. doi:10.1186/1471-2334-9-146. PMID: 19723318.
16. Iversen, C., Waddington, M., Farmer, J.J., 3rd, and Forsythe, S.J. 2006. The biochemical differentiation of Enterobacter sakazakii genotypes. BMC Microbiol. 6(1): 94. doi:10.1186/1471-2180-6-94. PMID:17067387.
17. Iversen, C., Lehner, A., Mullane, N., Bidlas, E., Cleenwerck, I., Marugg, J., et al. 2007. The taxonomy of Enterobacter sakazakii: proposal of a new genus Cronobacter gen. nov., and descriptions of Cronobacter sakazakii comb. nov. Cronobacter sakazakii subsp. sakazakii, comb. nov., Cronobacter sakazakii subsp. malonaticus subsp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov., and Cronobacter genomospecies 1. BMC Evol. Biol. 7(1): 64. doi:10.1186/1471-2148-7-64. PMID:17439656.
18. Iversen, C., Mullane, N., McCardell, B., Tall, B.D., Lehner, A., Fanning, S., et al. 2008. Cronobacter gen. nov., a new genus to accommodate the biogroups of Enterobacter sakazakii, and proposal of Cronobacter sakazakii gen. nov., comb. nov., Cronobacter malonaticus sp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov., Cronobacter genomospecies 1, and of three subspecies, Cronobacter dublinensis subsp. dublinensis subsp. nov., Cronobacter dublinensis subsp. lausannensis subsp. nov., and Cronobacter dublinensis subsp. lactaridi subsp. nov. Int. J. Syst. Evol. Microbiol. 58(6): 1442-1447. doi:10.1099/ijs.0.65577-0. PMID: 18523192.
19. Jaradat, Z.W., Ababneh, Q.O., Saadoun, I.M., Samara, N.A., and Rashdan, A.M. 2009. Isolation of Cronobacter spp. (formerly Enterobacter sakazakii) from infant food, herbs and environmental samples and the subsequent identification and confirmation of the isolates using biochemical, chromogenic assays, PCR and 16S rRNA sequencing. BMC Microbiol. 9(1): 225. doi:10.1186/1471-2180-9-225. PMID:19860874.
20. Kim, K., Kim, K.P., Choi, J., Lim, J.A., Lee, J., Hwang, S., and Ryu, S. 2010. Outer membrane proteins A (OmpA) and X (OmpX) are essential for basolateral invasion of Cronobacter sakazakii. Appl. Environ. Microbiol. 76(15): 5188-5198. doi:10.1128/AEM.02498-09. PMID:20543055.
21. Kucerova, E., Clifton, S.W., Xia, X.Q., Long, F., Porwollik, S., Fulton, L., et al. 2010. Genome sequence of Cronobacter sakazakii BAA-894 and comparative genomic hybridization analysis with other Cronobacter species. PLoS ONE, 5(3): e9556. doi:10.1371/journal.pone.0009556. PMID:20221447.
22. Mange, J.P., Stephan, R., Borel, N., Wild, P., Kim, K.S., Pospischil, A., and Lehner, A. 2006. Adhesive properties of Enterobacter sakazakii to human epithelial and brain microvascular endothelial cells. BMC Microbiol. 6(1): 58. doi:10.1186/1471-2180-6-58. PMID:16800879.
23. Miethke, M., and Marahiel, M.A. 2007. Siderophore-based iron acquisition and pathogen control. Microbiol. Mol. Biol. Rev. 71(3): 413-451. doi:10.1128/MMBR.00012-07. PMID:17804665.
24. Miled-Bennour, R., Ells, T.C., Pagotto, F.J., Farber, J.M., Kerouanton, A., Meheut, T., et al. 2010. Genotypic and phenotypic characterisation of a collection of Cronobacter (Enterobacter sakazakii) isolates. Int. J. Food Microbiol. 139(1-2): 116-125. doi:10.1016/j.ijfoodmicro.2010.01.045. PMID:20181403.
25. Mittal, R., Wang, Y., Hunter, C.J., Gonzalez-Gomez, I., and Prasadarao, N.V. 2009. Brain damage in newborn rat model of meningitis by Enterobacter sakazakii: a role for outer membrane protein A. Lab. Invest. 89(3): 263-277. doi:10.1038/labinvest.2008.164. PMID:19139724.
26. Mohan Nair, M.K., and Venkitanarayanan, K.S. 2007. Role of bacterial OmpA and host citoskeleton in the invasion of human intestinal epithelial cells by Enterobacter sakazakii. Pediatr. Res. 62(6): 664-669. doi:10.1203/PDR.0b013e3181587864. PMID: 17957161.
27. Molloy, C., Cagney, C., O'Brien, S., Iversen, C., Fanning, S., and Duffy, G. 2009. Surveillance and characterisation by pulsed-field gel electrophoresis of Cronobacter spp. in farming and domestic environments, food production animals and retail foods. Int. J. Food Microbiol. 136(2): 198-203. doi:10.1016/j.ijfoodmicro.2009.07.007. PMID:19683357.
28. Mullane, N.R., Whyte, P., Wall, P.G., Quinn, T., and Fanning, S. 2007. Application of pulsed-field gel electrophoresis to characterize and trace the prevalence of Enterobacter sakazakii in an infant formula processing facility. Int. J. Food Microbiol. 116(1): 73-81. doi:10.1016/j.ijfoodmicro.2006.12.036. PMID:17307267.
29. Nazarowec-White, M., and Farber, J.M. 1999. Phenotypic and genotypic typing of food and clinical isolates of Enterobacter sakazakii. J. Med. Microbiol. 48(6): 559-567. doi:10.1099/00222615-48-6-559. PMID:10359305.
30. Nicholson, T.F., Watts, K.M., and Hunstad, D.A. 2009. OmpA of uropathogenic Escherichia coli promotes postinvasion pathogenesis of cystitis. Infect. Immun. 77(12): 5245-5251. doi:10.1128/IAI.00670-09. PMID:19797074.
31. Pagotto, F.J., Nazarowec-White, M., Bidawid, S., and Farber, J.M. 2003. Enterobacter sakazakii: infectivity and enterotoxin production in vitro and in vivo. J. Food Prot. 66(3): 370-375. PMID: 12636287.
32. Pizarro-Cerdá, J., and Cossart, P. 2006. Bacterial adhesion and entry into host cells. Cell, 124(4): 715-727. doi:10.1016/j.cell.2006.02.012. PMID:16497583.
33. Proudy, I., Bougle, D., Coton, E., Coton, M., Leclercq, R., and Vergnaud, M. 2008. Genotypic characterization of Enterobacter sakazakii isolates by PFGE, BOX-PCR and sequencing of the fliC gene. J. Appl. Microbiol. 104(1): 26-34. PMID:17850301.
34. Schmid, M., Iversen, C., Gontia, I., Stephan, R., Hofmann, A., Hartmann, A., et al. 2009. Evidence for a plant-associated natural habitat for Cronobacter spp. Res. Microbiol. 160(8): 608-614. doi:10.1016/j.resmic.2009.08.013. PMID:19748571.
35. Singamsetty, V.K., Wang, Y., Shimada, H., and Prasadarao, N.V. 2008. Outer membrane protein A expression in Enterobacter sakazakii is required to induce microtubule condensation in human brain microvascular endothelial cells for invasion. Microb. Pathog. 45(3): 181-191. doi:10.1016/j.micpath.2008.05.006. PMID: 18606523.
36. Tenover, F.C., Arbeit, R.D., Goering, R.V., Mickelsen, P.A., Murray, B.E., Persing, D.H., and Swaminathan, B. 1995. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 33(9): 2233-2239. PMID:7494007.
37. Townsend, S.M., Hurrell, E., Gonzalez-Gomez, I., Lowe, J., Frye, J.G., Forsythe, S., and Badger, J.L. 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(10): 3538-3547. doi:10.1099/mic.0.2007/009316-0. PMID:17906151.
38. Townsend, S., Hurrell, E., and Forsythe, S. 2008. Virulence studies of Enterobacter sakazakii isolates associated with a neonatal intensive care unit outbreak. BMC Microbiol. 8(1): 64. doi:10.1186/1471-2180-8-64. PMID:18423002.
39. Wu, H.J., Wang, A.H., and Jennings, M.P. 2008. Discovery of virulence factors of pathogenic bacteria. Curr. Opin. Chem. Biol. 12(1): 93-101. doi:10.1016/j.cbpa.2008.01.023. PMID:18284925.
40. Xicohtencatl-Cortes, J., Monteiro-Neto, V., Ledesma, M.A., Jordan, D.M., Francetic, O., Kaper, J.B., et al. 2007. Intestinal adherence associated with type IV pili of enterohemorrhagic Escherichia coli O157:H7. J. Clin. Invest. 117(11): 3519-3529. doi:10.1172/JCI30727. PMID:17948128.
41. Xicohtencatl-Cortes, J., Monteiro-Neto, V., Saldana, Z., Ledesma, M.A., Puente, J.L., and Giron, J.A. 2009. The type 4 pili of enterohemorrhagic Escherichia coli O157:H7 are multipurpose structures with pathogenic attributes. J. Bacteriol. 191(1): 411-421. doi:10.1128/JB.01306-08. PMID:18952791.
42. Yang, J., Chen, L., Sun, L., Yu, J., and Jin, Q. 2008. VFDB 2008 release: an enhanced web-based resource for comparative pathogenomics. Nucleic Acids Res. 36(Suppl 1): D539-D542. doi:10.1093/nar/gkm951. PMID:17984080.