Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse

PLoS Pathogens

Volumn 2, Issue 2, 2006, Pages 0087-0100

  Lawley, Trevor D ^a   Chan, Kaman ^a   Thompson, Lucinda J ^a   Kim, Charles C ^a   Govoni, Gregory R ^a   Monack, Denise M ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; LIPOPOLYSACCHARIDE; PHOP PROTEIN; MEMBRANE PROTEIN; SPI 2 PROTEIN, SALMONELLA; SPI-2 PROTEIN, SALMONELLA; SPI1 PROTEIN, SALMONELLA; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENOME; BACTERIAL OUTER MEMBRANE; BACTERIAL VIRULENCE; BACTERIUM IDENTIFICATION; BACTERIUM MUTANT; CONTROLLED STUDY; DNA LIBRARY; DNA MICROARRAY; FEMALE; FIMBRIA; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GENE MUTATION; GENETIC SCREENING; MOUSE; MUTAGENESIS; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PROPHAGE; PROTEIN SECRETION; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SPLEEN; TRANSPOSON; WILD TYPE; ANIMAL; ANIMAL SALMONELLOSIS; BACTERIAL GENE; GENETICS; GENOMIC ISLAND; MICROBIOLOGY; MUTATION; PHYSIOLOGY;

ANIMALIA; BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

ANIMALS; BACTERIAL PROTEINS; FIMBRIAE, BACTERIAL; GENES, BACTERIAL; GENOME, BACTERIAL; GENOMIC ISLANDS; MEMBRANE PROTEINS; MICE; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; VIRULENCE FACTORS;

EID: 33645777008     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0020011     Document Type: Article

References (79)

1. Beltran P, Musser JM, Helmuth R, Farmer JJ 3rd, Frerichs WM, et al. (1988) Toward a population genetic analysis of Salmonella: genetic diversity and relationships among strains of serotypes S. choleraesuis, S. derby, S. dublin, S. enteritidis, S. heidelberg, S. infantis, S. newport, and S. typhimurium. Proc Natl Acad Sci U S A 85: 7753-7757.
2. Kingsley RA, Baumler AJ (2000) Host adaptation and the emergence of infectious disease: The Salmonella paradigm. Mol Microbiol 36: 1006-1014.
3. Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, et al. (2001) Animal models of Salmonella infections: Enteritis versus typhoid fever. Microbes Infect 3: 1335-1344.
4. Tsolis RM, Kingsley RA, Townsend SM, Ficht TA, Adams LG, et al. (1999) Of mice, calves, and men. Comparison of the mouse typhoid model with other Salmonella infections. Adv Exp Med Biol 473: 261-274.
5. Wigley P (2004) Genetic resistance to Salmonella infection in domestic animals. Res Vet Sci 76: 165-169.
6. Monack DM, Mueller A, Falkow S (2004) Persistent bacterial infections: The interface of the pathogen and the host immune system. Nat Rev Microbiol 2: 747-765.
7. Levine MM, Black RE, Lanata C (1982) Precise estimation of the numbers of chronic carriers of Salmonella typhi in Santiago, Chile, an endemic area. J Infect Dis 146: 724-726.
8. +/+ mice and can be reactivated by IFNgamma neutralization. J Exp Med 199: 231-241.
9. Wigley P, Berchieri A Jr, Page KL, Smith AL, Barrow PA (2001) Salmonella enterica serovar Pullorum persists in splenic macrophages and in the reproductive tract during persistent, disease-free carriage in chickens. Infect Immun 69: 7873-7879.
10. Groisman EA, Ochman H (1997) How Salmonella became a pathogen. Trends Microbiol 5: 343-349.
11. Galan JE (2001) Salmonella interactions with host cells: Type III secretion at work. Annu Rev Cell Dev Biol 17: 53-86.
12. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, et al. (1999) The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci U S A 96: 2396-2401.
13. Monack DM, Hersh D, Ghori N, Bouley D, Zychlinsky A, et al. (2000) Salmonella exploits caspase-1 to colonize Peyer's patches in a murine typhoid model. J Exp Med 192: 249-258.
14. Cirillo DM, Valdivia RH, Monack DM, Falkow S (1998) Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol 30: 175-188.
15. Hensel M, Shea JE, Waterman SR, Mundy R, Nikolaus T, et al. (1998) Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol Microbiol 30: 163-174.
16. Jones BD, Falkow S (1996) Salmonellosis: Host immune responses and bacterial virulence determinants. Annu Rev Immunol 14: 533-561.
17. Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, et al. (1995) Simultaneous identification of bacterial virulence genes by negative selection. Science 269: 400-403.
18. Richter-Dahlfors A, Buchan AM, Finlay BB (1997) Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med 186: 569-580.
19. Sheppard M, Webb C, Heath F, Mallows V, Emilianus R, et al. (2003) Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell Microbiol 5: 593-600.
20. Vidal SM, Malo D, Vogan K, Skamene E, Gros P (1993) Natural resistance to infection with intracellular parasites: Isolation of a candidate for Bcg. Cell 73: 469-485.
21. Govoni G, Canonne-Hergaux F, Pfeifer CG, Marcus SL, Mills SD, et al. (1999) Functional expression of Nramp1 in vitro in the murine macrophage line RAW264.7. Infect Immun 67: 2225-2232.
22. Tierrez A, Garcia-Del Portillo F (2005) New concepts in Salmonella virulence: The importance of reducing the intracellular growth rate in the host. Cell Microbiol 7: 901-909.
23. Brodsky IE, Ghori N, Falkow S, Monack D (2005) Mig-14 is an inner membrane-associated protein that promotes Salmonella typhimurium resistance to CRAMP, survival within activated macrophages and persistent infection. Mol Microbiol 55: 954-972.
24. Detweiler CS, Monack DM, Brodsky IE, Mathew H, Falkow S (2003) virK, somA and rcsC are important for systemic Salmonella enterica serovar Typhimurium infection and cationic peptide resistance. Mol Microbiol 48: 385-400.
25. Fang FC, Libby SJ, Castor ME, Fung AM (2005) Isocitrate lyase (AceA) is required for Salmonella persistence but not for acute lethal infection in mice. Infect Immun 73: 2547-2549.
26. Chan K, Kim CC, Falkow S (2005) Microarray-based detection of Salmonella enterica serovar Typhimurium transposon mutants that cannot survive in macrophages and mice. Infect Immun 73: 5438-5449.
27. Sassetti CM, Boyd DH, Rubin EJ (2001) Comprehensive identification of conditionally essential genes in mycobacteria. Proc Natl Acad Sci U S A 98: 12712-12717.
28. Badarinarayana V, Estep PW 3rd, Shendure J, Edwards J, Tavazoie S, et al. (2001) Selection analyses of insertional mutants using subgenic-resolution arrays. Nat Biotechnol 19: 1060-1065.
29. Unsworth KE, Holden DW (2000) Identification and analysis of bacterial virulence genes in vivo. Philos Trans R Soc Lond B Biol Sci 355: 613-622.
30. Carter PB, Collins FM (1974) The route of enteric infection in normal mice. J Exp Med 139: 1189-1203.
31. Meynell GG (1957) The applicability of the hypothesis of independent action to fatal infections in mice given Salmonella typhimurium by mouth. J Gen Microbiol 16: 396-404.
32. Meynell GG, Stocker BA (1957) Some hypotheses on the aetiology of fatal infections in partially resistant hosts and their application to mice challenged with Salmonella paratyphi-B or Salmonella typhimurium by intraperitoneal injection. J Gen Microbiol 16: 38-58.
33. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
34. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, et al. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852-856.
35. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, et al. (2003) The COG database: An updated version includes eukaryotes. BMC Bioinformatics 4: 41.
36. Sassetti CM, Rubin EJ (2003) Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci U S A 100: 12989-12994.
37. Ohlson MB, Fluhr K, Birmingham CL, Brumell JH, Miller SI (2005) SseJ deacylase activity by Salmonella enterica serovar Typhimurium promotes virulence in mice. Infect Immun 73: 6249-6259.
38. Ruiz-Albert J, Yu XJ, Beuzon CR, Blakey AN, Galyov EE, et al. (2002) Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol Microbiol 44: 645-661.
39. Kujat Choy SL, Boyle EC, Gal-Mor O, Goode DL, Valdez Y, et al. (2004) SseK1 and SseK2 are novel translocated proteins of Salmonella enterica serovar typhimurium. Infect Immun 72: 5115-5125.
40. Geddes K, Worley M, Niemann G, Heffron F (2005) Identification of new secreted effectors in Salmonella enterica serovar Typhimurium. Infect Immun 73: 6260-6271.
41. Jiang X, Rossanese OW, Brown NF, Kujat-Choy S, Galan JE, et al. (2004) The related effector proteins SopD and SopD2 from Salmonella enterica serovar Typhimurium contribute to virulence during systemic infection of mice. Mol Microbiol 54: 1186-1198.
42. Blanc-Potard AB, Groisman EA (1997) The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J 16: 5376-5385.
43. Waldor MK, Mekalanos JJ (1994) ToxR regulates virulence gene expression in non-O1 strains of Vibrio cholerae that cause epidemic cholera. Infect Immun 62: 72-78.
44. Morgan E, Campbell JD, Rowe SC, Bispham J, Stevens MP, et al. (2004) Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol Microbiol 54: 994-1010.
45. Folkesson A, Lofdahl S, Normark S (2002) The Salmonella enterica subspecies I specific centisome 7 genomic island encodes novel protein families present in bacteria living in close contact with eukaryotic cells. Res Microbiol 153: 537-545.
46. Wood MW, Jones MA, Watson PR, Hedges S, Wallis TS, et al. (1998) Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol Microbiol 29: 883-891.
47. Sauer FG, Mulvey MA, Schilling JD, Martinez JJ, Hultgren SJ (2000) Bacterial pili: molecular mechanisms of pathogenesis. Curr Opin Microbiol 3: 65-72.
48. Baumler AJ, Tsolis RM, Bowe FA, Kusters JG, Hoffmann S, et al. (1996) The pef fimbrial operon of Salmonella typhimurium mediates adhesion to murine small intestine and is necessary for fluid accumulation in the infant mouse. Infect Immun 64: 61-68.
49. Weening EH, Barker JD, Laarakker MC, Humphries AD, Tsolis RM, et al. (2005) The Salmonella enterica serotype Typhimurium lpf, bcf, stb, stc, std, and sth fimbrial operons are required for intestinal persistence in mice. Infect Immun 73: 3358-3366.
50. Stein MA, Leung KY, Zwick M, Garcia-del Portillo F, Finlay BB (1996) Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol Microbiol 20: 151-164.
51. Caron J, Loredo-Osti JC, Laroche L, Skamene E, Morgan K, et al. (2002) Identification of genetic loci controlling bacterial clearance in experimental Salmonella enteritidis infection: An unexpected role of Nramp1 (Slc11a1) in the persistence of infection in mice. Genes Immun 3: 196-204.
52. Zaharik ML, Vallance BA, Puente JL, Gros P, Finlay BB (2002) Host-pathogen interactions: Host resistance factor Nramp1 up-regulates the expression of Salmonella pathogenicity island-2 virulence genes. Proc Natl Acad Sci U S A 99: 15705-15710.
53. Glickman MS, Jacobs WR Jr (2001) Microbial pathogenesis of Mycobacterium tuberculosis: dawn of a discipline. Cell 104: 477-485.
54. Jones BD, Falkow S (1994) Identification and characterization of a Salmonella typhimurium oxygen-regulated gene required for bacterial internalization. Infect Immun 62: 3745-3752.
55. Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, et al. (2003) Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 71: 2839-2858.
56. Murray RA, Lee CA (2000) Invasion genes are not required for Salmonella enterica serovar typhimurium to breach the intestinal epithelium: Evidence that salmonella pathogenicity island 1 has alternative functions during infection. Infect Immun 68: 5050-5055.
57. Coburn B, Li Y, Owen D, Vallance BA, Finlay BB (2005) Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect Immun 73: 3219-3227.
58. Brumell JH, Steele-Mortimer O, Finlay BB (1999) Bacterial invasion: Force feeding by Salmonella. Curr Biol 9: R277-R280.
59. Deiwick J, Nikolaus T, Shea JE, Gleeson C, Holden DW, et al. (1998) Mutations in Salmonella pathogenicity island 2 (SPI2) genes affecting transcription of SPI1 genes and resistance to antimicrobial agents. J Bacteriol 180: 4775-4780.
60. Hensel M, Shea JE, Raupach B, Monack D, Falkow S, et al. (1997) Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella Pathogenicity Island 2. Mol Microbiol 24: 155-167.
61. Hernandez LD, Hueffer K, Wenk MR, Galan JE (2004) Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304: 1805-1807.
62. Steele-Mortimer O, Brumell JH, Knodler LA, Meresse S, Lopez A, 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.
63. Drecktrah D, Knodler LA, Galbraith K, Steele-Mortimer O (2005) The Salmonella SPI1 effector SopB stimulates nitric oxide production long after invasion. Cell Microbiol 7: 105-113.
64. Kubori T, Galan JE (2003) Temporal regulation of salmonella virulence effector function by proteasome-dependent protein degradation. Cell 115: 333-342.
65. Guiney DG (2005) The role of host cell death in Salmonella infections. Curr Top Microbiol Immunol 289: 131-150.
66. Monack DM, Raupach B, Hromockyj AE, Falkow S (1996) Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci U S A 93: 9833-9838.
67. Mastroeni P, Sheppard M (2004) Salmonella infections in the mouse model: host resistance factors and in vivo dynamics of bacterial spread and distribution in the tissues. Microbes Infect 6: 398-405.
68. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47: 103-118.
69. Smith BP, Reina-Guerra M, Hoiseth SK, Stocker BA, Habasha F, et al. (1984) Aromatic-dependent Salmonella typhimurium as modified live vaccines for calves. Am J Vet Res 45: 59-66.
70. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
71. Wang Y, Taylor DE (1990) Chloramphenicol resistance in Campylobacter coli: Nucleotide sequence, expression, and cloning vector construction. Gene 94: 23-28.
72. Salama NR, Shepherd B, Falkow S (2004) Global transposon mutagenesis and essential gene analysis of Helicobacter pylori. J Bacteriol 186: 7926-7935.
73. Chan K, Baker S, Kim CC, Detweiler CS, Dougan G, et al. (2003) Genomic comparison of Salmonella enterica serovars and Salmonella bongori by use of an S. enterica serovar typhimurium DNA microarray. J Bacteriol 185: 553-563.
74. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, et al. (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413: 848-852.
75. Deng W, Liou SR, Plunkett G 3rd, Mayhew GF, Rose DJ, et al. (2003) Comparative genomics of Salmonella enterica serovar Typhi strains Ty2 and CT18. J Bacteriol 185: 2330-2337.
76. Cummings CA, Brinig MM, Lepp PW, van de Pas S, Relman DA (2004) Bordetella species are distinguished by patterns of substantial gene loss and host adaptation. J Bacteriol 186: 1484-1492.
77. Gollub J, Ball CA, Binkley G, Demeter J, Finkelstein DB, et al. (2003) The Stanford Microarray Database: Data access and quality assessment tools. Nucleic Acids Res 31: 94-96.
78. Kim CC, Falkow S (2003) Significance analysis of lexical bias in microarray data. BMC Bioinformatics 4: 12.
79. Brandt SM, Dionne MS, Khush RS, Pham LN, Vigdal TJ, et al. (2004) Secreted bacterial effectors and host-produced Eiger/TNF drive death in a Salmonella-infected fruit fly. PLoS Biol 2: e418. DOI: 10.1371/journal.pbio. 0020418