Transposon mutagenesis of Salmonella enterica serovar enteritidis identifies genes that contribute to invasiveness in human and chicken cells and survival in egg albumen

Infection and Immunity

Volumn 80, Issue 12, 2012, Pages 4203-4215

  Shah, Devendra H ^a   Zhou, Xiaohui ^a   Kim, Hye Young ^b   Call, Douglas R ^a   Guard, Jean ^c  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KASUGAMYCIN; OVALBUMIN; POLYMYXIN;

ANIMAL CELL; ARTICLE; ASSAY; BACTERIAL GENE; BACTERIAL VIRULENCE; CELL INVASION; CELL STRAIN CACO 2; CONTROLLED STUDY; CSGB GENE; FLIH GENE; FLJB GENE; GENE IDENTIFICATION; GENE INSERTION; GENE LOCUS; GENE MUTATION; GENOMIC ISLAND; HILA GENE; HUMAN; HUMAN CELL; INVB GENE; INVF GENE; INVG GENE; INVI GENE; KSGA GENE; LIVER CELL; LIVER CELL CARCINOMA; MACROPHAGE; MICROBIAL ATTENUATION; MINIMUM INHIBITORY CONCENTRATION; MUTAGENESIS; NONHUMAN; ORGA GENE; PEGD GENE; PHSA SOPA GENE; PIPA GENE; PRGH GENE; PRIORITY JOURNAL; PROP BASS GENE; RFBM GENE; RFBN GENE; SALMONELLA ENTERICA; SALMONELLA ENTERICA SEROVAR ENTERITIDIS; SALMONELLA ENTERITIDIS; SEN0034 GENE; SEN0803 GENE; SEN1152 GENE; SEN1154 SOPE GENE; SEN1393 GENE; SEN1966 GENE; SEN2278 GENE; SEN3503 GENE; SICA GENE; SIIE GENE; SINH GENE; SIPC GENE; SPAO GENE; SPAP GENE; SPAS GENE; SPVR GENE; SURVIVAL; TRANSPOSON;

ALBUMINS; ANIMALS; CACO-2 CELLS; CHICKENS; DNA TRANSPOSABLE ELEMENTS; EGGS; EPITHELIAL CELLS; GENES, BACTERIAL; GENOMIC ISLANDS; HUMANS; INTESTINES; LIVER; MUTAGENESIS, INSERTIONAL; POULTRY DISEASES; SALMONELLA ENTERITIDIS; SALMONELLA INFECTIONS, ANIMAL; VIRULENCE;

EID: 84870839050     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00790-12     Document Type: Article

References (103)

1. Agron PG, et al. 2001. Identification by subtractive hybridization of sequences specific for Salmonella enterica serovar enteritidis. Appl. Environ. Microbiol. 67:4984-4991.
2. Allen-Vercoe E, Sayers AR, Woodward MJ. 1999. Virulence of Salmonella enterica serotype Enteritidis aflagellate and afimbriate mutants in a day-old chick model. Epidemiol. Infect. 122:395-402.
3. Apel D, Surette MG. 2008. Bringing order to a complex molecular machine: the assembly of the bacterial flagella. Biochim. Biophys. Acta 1778:1851-1858.
4. Barnhart MM, Chapman MR. 2006. Curli biogenesis and function. Annu. Rev. Microbiol. 60:131-147.
5. Beug H, von Kirchbach A, Doderlein G, Conscience JF, Graf T. 1979. Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell 18:375-390.
6. Binet R, Maurelli AT. 2009. The chlamydial functional homolog of KsgA confers kasugamycin sensitivity to Chlamydia trachomatis and impacts bacterial fitness. BMC Microbiol. 9:279.
7. Bispham J, Tripathi BN, Watson PR, Wallis TS. 2001. Salmonella pathogenicity island2 influences both systemic salmonellosis andSalmonella-induced enteritis in calves. Infect. Immun. 69:367-377.
8. Bronstein PA, Miao EA, Miller SI. 2000. InvB is a type III secretion chaperone specific for SspA. J. Bacteriol. 182:6638-6644.
9. Carnell SC, et al. 2007. Role in virulence and protective efficacy in pigs of Salmonella enterica serovar Typhimurium secreted components identified by signature-tagged mutagenesis. Microbiology 153:1940-1952.
10. CDC. 2007. Salmonella serotype Enteritidis infections among workers producing poultry vaccine, Maine, November-December 2006. Morb. Mortal Wkly. Rep. 56:877-879.
11. Clavijo RI, Loui C, Andersen GL, Riley LW, Lu S. 2006. Identification of genes associated with survival of Salmonella enterica serovar Enteriti-dis in chicken egg albumen. Appl. Environ. Microbiol. 72:1055-1064.
12. Clayton DJ, et al. 2008. Analysis of the role of 13 major fimbrial subunits in colonisation of the chicken intestines by Salmonella enterica serovar Enteritidis reveals a role for a novel locus. BMC Microbiol. 8:228.
13. Cogan TA, et al. 2004. Flagella and curli fimbriae are important for the growth of Salmonella enterica serovars in hen eggs. Microbiology 150: 1063-1071.
14. Collazo CM, Zierler MK, Galan JE. 1995. Functional analysis of the Salmonella typhimurium invasion genes invl and invJ and identification of a target of the protein secretion apparatus encoded in the inv locus. Mol. Microbiol. 15:25-38.
15. Darwin KH, Robinson LS, Miller VL. 2001. SigE is a chaperone for the Salmonella enterica serovar Typhimurium invasion protein SigD. J. Bac-teriol. 183:1452-1454.
16. Demirci H, et al. 2010. Modification of 16S ribosomal RNA by the KsgA methyltransferase restructures the 30S subunit to optimize ribosome function. RNA 16:2319-2324.
17. Desin TS, et al. 2009. Salmonella enterica serovar Enteritidis pathoge-nicity island 1 is not essential for but facilitates rapid systemic spread in chickens. Infect. Immun. 77:2866-2875.
18. Dhawi AA, et al. 2011. Adaptation to the chicken intestine in Salmonella Enteritidis PT4 studied by transcriptional analysis. Vet. Microbiol. 153: 198-204.
19. Dibb-Fuller MP, Allen-Vercoe E, Thorns CJ, Woodward MJ. 1999. Fimbriae-and flagella-mediated association with and invasion of cultured epithelial cells by Salmonella enteritidis. Microbiology 145:1023-1031.
20. Dieye Y, Ameiss K, Mellata M, Curtiss R III. 2009. The Salmonella Pathogenicity Island (SPI) 1 contributes more than SPI2 to the colonization of the chicken by Salmonella entericaserovar Typhimurium. BMC Microbiol. 9:3.
21. Dieye Y, Dyszel JL, Kader R, Ahmer BM. 2007. Systematic analysis of the regulation of type three secreted effectors in Salmonella enterica se-rovar Typhimurium. BMC Microbiol. 7:3.
22. Ehrbar K, Friebel A, Miller SI, Hardt WD. 2003. Role of the Salmonella pathogenicity island 1 (SPI-1) protein InvB in type III secretion of SopE and SopE2, two Salmonella effector proteins encoded outside of SPI-1. J. Bacteriol. 185:6950-6967.
23. Eichelberg K, Galan JE. 2000. The flagellar sigma factor FliA (sigma(28)) regulates the expression of Salmonella genes associated with the centi-some 63 type III secretion system. Infect. Immun. 68:2735-2743.
24. Ellermeier JR, Slauch JM. 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.
25. Finlay BB, Falkow S. 1989. Salmonella as an intracellular parasite. Mol. Microbiol. 3:1833-1841.
26. Forbes SJ, Eschmann M, Mantis NJ. 2008. Inhibition of Salmonella entericaserovar Typhimurium motility and entry into epithelial cells bya protective antilipopolysaccharide monoclonal immunoglobulin A antibody. Infect. Immun. 76:4137-4144.
27. Galan JE. 1996. Molecular genetic bases of Salmonella entry into host cells. Mol. Microbiol. 20:263-271.
28. Gantois I, et al. 2009. Mechanisms of egg contamination by Salmonella enteritidis. FEMS Microbiol. Rev. 33:718-738.
29. Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Van Immerseel F. 2008. Salmonella enterica serovar Enteritidis genes induced during oviduct colonization and egg contamination in laying hens. Appl. Environ. Microbiol. 74:6616-6622.
30. Gerlach RG, Jackel D, Geymeier N, Hensel M. 2007. Salmonella patho-genicity island 4-mediated adhesioniscoregulated with invasion genes in Salmonella enterica. Infect. Immun. 75:4697-4709.
31. Gerlach RG, et al. 2007. Salmonella Pathogenicity Island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell Microbiol. 9:1834-1850.
32. Guard-Petter J. 2001. The chicken, the egg and Salmonella enteritidis. Environ. Microbiol. 3:421-430.
33. Guard-Petter J, Keller LH, Rahman MM, Carlson RW, Silvers S. 1996. A novel relationship between O-antigen variation, matrix formation, and invasiveness of Salmonella enteritidis. Epidemiol. Infect. 117:219-231.
34. Guard-Petter J, Lakshmi B, Carlson R, Ingram K. 1995. Characterization of lipopolysaccharide heterogeneity in Salmonella enteritidis by an improved gel electrophoresis method. Appl. Environ. Microbiol. 61: 2845-2851.
35. Gunn JS, et al. 1998. PmrA-PmrB-regulated genes necessary for 4-ami-noarabinose lipidAmodification and polymyxin resistance. Mol. Micro-biol. 27:1171-1182.
36. Hautefort I, et al. 2008. During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcrip-tional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol. 10:958-984.
37. Heinzinger NK, Fujimoto SY, Clark MA, Moreno MS, Barrett EL. 1995. Sequence analysis of the phs operon in Salmonella typhimurium and the contributionof thiosulfate reduction to anaerobic energy metabolism. J. Bacteriol. 177:2813-2820.
38. Hoare A, et al. 2006. The outer core lipopolysaccharide of Salmonella enterica serovar Typhi is required for bacterial entry into epithelial cells. Infect. Immun. 74:1555-1564.
39. Hultgren SJ, Normark S. 1991. Biogenesis of the bacterial pilus. Curr. Opin. Genet. Dev. 1:313-318.
40. Humphrey TJ, et al. 1996. Isolates of Salmonella enterica Enteritidis PT4 with enhanced heat and acid tolerance are more virulent in mice and more invasive in chickens. Epidemiol. Infect. 117:79-88.
41. Ilg K, et al. 2009. O-antigen-negative Salmonella enterica serovar Typhi-murium is attenuated in intestinal colonization but elicits colitis in streptomycin-treated mice. Infect. Immun. 77:2568-2575.
42. Jones BD, Falkow S. 1994. Identification and characterization of a Salmonella typhimurium oxygen-regulated gene required for bacterial inter-nalization. Infect. Immun. 62:3745-3752.
43. Jones GW, Richardson LA, Uhlman D. 1981. The invasion of HeLa cells by Salmonella typhimurium: reversible and irreversible bacterial attachment and the role of bacterial motility. J. Gen. Microbiol. 127:351-360.
44. Jones MA, Hulme SD, Barrow PA, Wigley P. 2007. The Salmonella pathogenicity island 1 and Salmonella pathogenicity island 2 type III secretion systems play a major role in pathogenesis of systemic disease and gastrointestinal tract colonization of Salmonella enterica serovar Ty-phimurium in the chicken. Avian Pathol. 36:199-203.
45. Karasova D, et al. 2010. Influence of 5 major Salmonella pathogenicity islands on NK cell depletion in mice infected with Salmonella enterica serovar Enteritidis. BMC Microbiol. 10:75.
46. Kawaguchi T, Nomura K, Hirayama Y, Kitagawa T. 1987. Establishment and characterization of a chicken hepatocellular carcinoma cell line, LMH. Cancer Res. 47:4460-4464.
47. Keller LH, Benson CE, Krotec K, Eckroade RJ. 1995. Salmonella enter-itidis colonization of the reproductive tract and forming and freshly laid eggs of chickens. Infect. Immun. 63:2443-2449.
48. Kihlstrom E, Edebo L. 1976. Association of viable and inactivated Salmonella typhimurium395MS andMR10with HeLa cells. Infect. Immun. 14:851-857.
49. Kimbrough TG, Miller SI. 2002. Assembly of the type III secretion needle complex of Salmonella typhimurium. Microbes Infect. 4:75-82.
50. Kimbrough TG, Miller SI. 2000. Contribution of Salmonella typhimu-rium type III secretion components to needle complex formation. Proc. Natl. Acad. Sci. U. S. A. 97:11008-11013.
51. Kimura AC, et al. 2004. Chicken consumption is a newly identified risk factor for sporadic Salmonella enterica serotype Enteritidis infections in the United States: a case-control study in FoodNet sites. Clin. Infect. Dis. 38(Suppl. 3):S244-S252.
52. Kingsley RA, et al. 2003. Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype Typhimurium: identification of intestinal colonization and persistence determinants. Infect. Immun. 71: 629-640.
53. Kiss T, Morgan E, Nagy G. 2007. Contribution of SPI-4 genes to the virulence of Salmonella enterica. FEMS Microbiol. Lett. 275:153-159.
54. Klein JR, Fahlen TF, Jones BD. 2000. Transcriptional organization and function of invasion genes within Salmonella enterica serovar Typhimu-rium pathogenicity island 1, including the prgH, prgI, prgJ, prgK, orgA, orgB, and orgC genes. Infect. Immun. 68:3368-3376.
55. Kubori T, et al. 1998. Supramolecular structure of the Salmonella ty-phimurium type III protein secretion system. Science 280:602-605.
56. Lawley TD, et al. 2006. Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog. 2:e11. doi:10.1371/journal.ppat.0020011.
57. Lostroh CP, Lee CA. 2001. The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect. 3:1281-1291.
58. Ly KT, Casanova JE. 2007. Mechanisms of Salmonella entry into host cells. Cell Microbiol. 9:2103-2111.
59. Lyczak JB, et al. 2001. Epithelial cell contact-induced alterations in Salmonella enterica serovar Typhi lipopolysaccharide are critical for bacterial internalization. Cell Microbiol. 3:763-772.
60. Macnab RM. 2004. Type III flagellar protein export and flagellar assembly. Biochim. Biophys. Acta 1694:207-217.
61. Martin GD, et al. 2000. Invasiveness of Salmonella serotypes Typhimu-rium and Enteritidis of human gastro-enteritic origin for rabbit ileum: role of LPS, plasmids and host factors. J. Med. Microbiol. 49:1011-1021.
62. Mecsas J, Bilis I, Falkow S. 2001. Identification of attenuated Yersinia pseudotuberculosis strains and characterization of an orogastric infection in BALB/c mice on day 5 postinfection by signature-tagged mutagenesis. Infect. Immun. 69:2779-2787.
63. Morales CA, et al. 2005. Correlation of phenotype with the genotype of egg-contaminating Salmonella enterica serovar Enteritidis. Appl. Environ. Microbiol. 71:4388-4399.
64. Morgan E, et al. 2004. Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 54:994-1010.
65. Myeni SK, Zhou D. 2010. The C terminus of SipC binds and bundles F-actin to promote Salmonella invasion. J. Biol. Chem. 285:13357-13363.
66. Parker CT, Guard-Petter J. 2001. Contribution of flagella and invasion proteins to pathogenesis of Salmonella enterica serovar enteritidis in chicks. FEMS Microbiol. Lett. 204:287-291.
67. Patrick ME, et al. 2004. Salmonella enteritidis infections, United States, 1985-1999. Emerg. Infect. Dis. 10:1-7.
68. Pegues DA, Hantman MJ, Behlau I, Miller SI. 1995. PhoP/PhoQ transcriptional repression ofSalmonella typhimuriuminvasion genes: evidence for a role in protein secretion. Mol. Microbiol. 17:169-181.
69. Perkins TT, et al. 2009. A strand-specific RNA-Seq analysis of the tran-scriptome of the typhoid bacillus Salmonella typhi. PLoS Genet. 5:e1000569. doi:10.1371/journal.pgen.1000569.
70. Petter JG. 1993. Detection of two smooth colony phenotypes in a Salmonella enteritidis isolate which vary in their ability to contaminate eggs. Appl. Environ. Microbiol. 59:2884-2890.
71. Rodriguez-Escudero I, Ferrer NL, Rotger R, Cid VJ, Molina M. 2011. Interaction of the Salmonella Typhimurium effector protein SopB with host cell Cdc42 is involved in intracellular replication. Mol. Microbiol. 80:1220-1240.
72. Rychlik I, Gregorova D, Hradecka H. 2006. Distribution and function of plasmids in Salmonella enterica. Vet. Microbiol. 112:1-10.
73. Rychlik I, et al. 2009. Virulence potential of five major pathogenicity islands (SPI-1 to SPI-5) of Salmonella enterica serovar Enteritidis for chickens. BMC Microbiol. 9:268.
74. Sabbagh SC, Forest CG, Lepage C, Leclerc JM, Daigle F. 2010. So similar, yetsodifferent: uncovering distinctive featuresinthe genomes of Salmonella enterica serovars Typhimurium and Typhi. FEMS Microbiol. Lett. 305:1-13.
75. Sakai Y, et al. 1987. Properties of the membrane-bound 5=-nucleotidase and utilization of extracellular ATP in Vibrio parahaemolyticus. J. Gen. Microbiol. 133:2751-2757.
76. Santiviago CA, et al. 2010. Spontaneous excision of the Salmonella enterica serovar Enteritidis-specific defective prophage-like element phiSE14. J. Bacteriol. 192:2246-2254.
77. Schmitt CK, et al. 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.
78. Schraidt O, et al. 2010. Topology and organization of the Salmonella typhimurium type III secretion needle complex components. PLoS Pathog. 6:e1000824. doi:10.1371/journal.ppat.1000824.
79. Shah DH, et al. 2012. Salmonella Enteritidis strains from poultry exhibit differential responses to acid stress, oxidative stress, and survival in the egg albumen. Foodborne Pathog. Dis. 9:258-264.
80. Shah DH, et al. 2005. Identification of Salmonella gallinarum virulence genes in a chicken infection model using PCR-based signature-tagged mutagenesis. Microbiology 151:3957-3968.
81. Shah DH, et al. 2005. Control of fowl typhoid using tissue culture medium waste after harvest of Korean wild ginseng (Panax ginseng). J. Appl. Poultry Res. 14:455-462.
82. Shah DH, Zhou X, Addwebi T, Davis MA, Call DR. 2011. In vitro and in vivo pathogenicity of Salmonella enteritidis clinical strains isolated from North America. Arch. Microbiol. 193:811-821.
83. Shah DH, et al. 2011. Cell invasion of poultry-associated Salmonella enterica serovar Enteritidis isolates is associated with pathogenicity, mo-tility and proteins secreted by the type III secretion system. Microbiology 157:1428-1445.
84. Silva CA, et al. 2012. Infection of mice by Salmonella enterica serovar Enteritidis involves additional genes that are absent in the genome of serovar Typhimurium. Infect. Immun. 80:839-849.
85. Soncini FC, Groisman EA. 1996. Two-component regulatory systems can interact to process multiple environmental signals. J. Bacteriol. 178: 6796-6801.
86. Spector MP, et al. 1999. The medium-/long-chain fatty acyl-CoA dehy-drogenase (fadF) gene of Salmonella typhimuriumis a phase 1 starvation-stress response (SSR) locus. Microbiology 145:15-31.
87. Steele-Mortimer O, et al. 2002. The invasion-associated type III secretion system of Salmonella enterica serovar Typhimurium is necessary for intracellular proliferation and vacuole biogenesis in epithelial cells. Cell Microbiol. 4:43-54.
88. Stone BJ, et al. 1992. Identification of novel loci affecting entry of Salmonella enteritidis into eukaryotic cells. J. Bacteriol. 174:3945-3952.
89. Subramoni S, Nguyen DT, Sokol PA. 2011. Burkholderia cenocepacia ShvR-regulated genes that influence colony morphology, biofilm formation, and virulence. Infect. Immun. 79:2984-2997.
90. Sukhan A, Kubori T, Wilson J, Galan JE. 2001. Genetic analysis of assembly of the Salmonella enterica serovar Typhimurium type III secretion-associated needle complex. J. Bacteriol. 183:1159-1167.
91. Sukupolvi S, et al. 1997. Expression of thin aggregative fimbriae promotes interaction of Salmonella typhimurium SR-11 with mouse small intestinal epithelial cells. Infect. Immun. 65:5320-5325.
92. Swigonova Z, Mohsen AW, Vockley J. 2009. Acyl-CoA dehydrogenases: dynamic history of protein family evolution. J. Mol. Evol. 69:176-193.
93. Thomson NR, et al. 2008. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. 18:1624-1637.
94. Toguchi A, Siano M, Burkart M, Harshey RM. 2000. Genetics of swarming motility in Salmonella enterica serovar Typhimurium: critical role for lipopolysaccharide. J. Bacteriol. 182:6308-6321.
95. Tucker SC, Galan JE. 2000. Complex function for SicA, a Salmonella entericaserovar Typhimurium type III secretion-associated chaperone. J. Bacteriol. 182:2262-2268.
96. Van Asten FJ, Hendriks HG, Koninkx JF, Van der Zeijst BA, Gaastra W. 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.
97. van Buul CP, Visser W, van Knippenberg PH. 1984. Increased translational fidelity caused by the antibiotic kasugamycin and ribo-somal ambiguity in mutants harbouring the ksgA gene. FEBS Lett. 177:119-124.
98. van der Velden AW, Baumler AJ, Tsolis RM, Heffron F. 1998. Multiple fimbrial adhesins are required for full virulence of Salmonella typhimu-rium in mice. Infect. Immun. 66:2803-2808.
99. Wagner S, et al. 2010. Organization and coordinated assembly of the type III secretion export apparatus. Proc. Natl. Acad. Sci. U. S. A. 107: 17745-17750.
100. Wiegand I, Hilpert K, Hancock RE. 2008. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3:163-175.
101. Wood MW, et al. 1998. Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol. Microbiol. 29:883-891.
102. Xiang SH, Haase AM, Reeves PR. 1993. Variation of the rfb gene clusters in Salmonella enterica. J. Bacteriol. 175:4877-4884.
103. Zhang Y, Zagnitko O, Rodionova I, Osterman A, Godzik A. 2011. The FGGY carbohydrate kinase family: insights into the evolution of functional specificities. PLoS Comput. Biol. 7:e1002318. doi:10.1371/ journal.pcbi.1002318.