Salmonella enterica serovars typhimurium and typhi as model organisms: Revealing paradigm of host-pathogen interactions

Virulence

Volumn 3, Issue 4, 2012, Pages 377-388

  Garai, Preeti ^a   Gnanadhas, Divya Prakash ^a   Chakravortty, Dipshikha ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Model systems; Pathogenicity islands; Salmonella; Virulence

Indexed keywords

INFLAMMASOME; VIRULENCE FACTOR;

ARTICLE; BACTERIAL VIRULENCE; HOST CELL; HOST PATHOGEN INTERACTION; IMMUNE SYSTEM; LYSOSOME; MYCOBACTERIUM; NONHUMAN; PATHOGENESIS; PATHOGENICITY ISLAND; SALMONELLA ENTERICA; SALMONELLA TYPHI; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; TUBERCULOSIS; TYPHOID FEVER;

MYCOBACTERIUM; SALMONELLA; SALMONELLA ENTERICA;

EID: 84866494365     PISSN: 21505594     EISSN: 21505608     Source Type: Journal    
DOI: 10.4161/viru.21087     Document Type: Article

References (115)

1. Porwollik S, McClelland M. Lateral gene transfer in Salmonella. Microbes Infect 2003; 5:977-89; PMID: 12941390; http://dx.doi.org/10.1016/S1286-4579 (03)00186-2.
2. Kumar Y, Valdivia RH. Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 2009; 5:593-601; PMID:19527886; http://dx.doi.org/10.1016/j.chom. 2009.05.014.
3. Deiwick J, Salcedo SP, Boucrot E, Gilliland SM, Henry T, Petermann N, et al. The translocated Salmonella effector proteins SseF and SseG interact and are required to establish an intracellular replication niche. Infect Immun 2006; 74:6965-72; PMID: 17015457; http://dx.doi.org/10.1128/IAI.00648-06.
4. Ray K, Marteyn B, Sansonetti PJ, Tang CM. Life on the inside: the intracellular lifestyle of cytosolic bacteria. Nat Rev Microbiol 2009; 7:333-40; PMID: 19369949; http://dx.doi.org/10.1038/nrmicro2112.
5. Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, Bäumler AJ. Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect 2001; 3:1335-44; PMID:11755423; http://dx.doi.org/ 10.1016/S1286-4579(01)01495-2.
6. Tenor JL, McCormick BA, Ausubel FM, Aballay A. Caenorhabditis elegans-based screen identifies Salmonella virulence factors required for conserved host-pathogen interactions. Curr Biol 2004; 14:1018- 24; PMID:15182677; http://dx.doi.org/10.1016/j. cub.2004.05.050.
7. Geddes K, Cruz F, Heffron F. Analysis of cells targeted by Salmonella type III secretion in vivo. PLoS Pathog 2007; 3:e196; PMID:18159943; http://dx.doi.org/10. 1371/journal.ppat.0030196.
8. Groisman EA, Ochman H. Pathogenicity islands: bacterial evolution in quantum leaps. Cell 1996; 87: 791-4; PMID:8945505; http://dx.doi.org/10.1016/ S0092-8674(00)81985-6.
9. Eswarappa SM, Karnam G, Nagarajan AG, Chakraborty S, Chakravortty D. lac repressor is an antivirulence factor of Salmonella enterica: its role in the evolution of virulence in Salmonella. PLoS One 2009; 4:e5789; PMID:19495420; http://dx.doi.org/ 10.1371/journal.pone.0005789.
10. Lucas RL, Lostroh CP, DiRusso CC, Spector MP, Wanner BL, Lee CA. Multiple factors independently regulate hilA and invasion gene expression in Salmonella enterica serovar typhimurium. J Bacteriol 2000; 182:1872-82; PMID:10714991; http://dx.doi. org/10.1128/JB.182.7.1872-1882.2000.
11. Bijlsma JJ, Groisman EA. The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica. Mol Microbiol 2005; 57:85-96; PMID:15948951; http://dx.doi.org/10. 1111/j.1365-2958.2005.04668.x
12. Bajaj V, Hwang C, Lee CA. hilA is a novel ompR/ toxR family member that activates the expression of Salmonella typhimurium invasion genes. Mol Microbiol 1995; 18:715-27; PMID:8817493; http://dx.doi. org/10.1111/j.1365-2958.1995.mmi_18040715.x
13. Kim CC, Falkow S. Delineation of upstream signaling events in the salmonella pathogenicity island 2 transcriptional activation pathway. J Bacteriol 2004; 186:4694-704; PMID:15231802; http://dx.doi.org/ 10.1128/JB.186.14.4694-4704.2004.
14. Beuzón CR, Méresse S, Unsworth KE, Ruíz-Albert J, Garvis S, Waterman SR, et al. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 2000; 19:3235-49; PMID: 10880437; http://dx.doi.org/10.1093/emboj/19.13. 3235.
15. Merighi M, Carroll-Portillo A, Septer AN, Bhatiya A, Gunn JS. Role of Salmonella enterica serovar Typhimurium two-component system PreA/PreB in modulating PmrA-regulated gene transcription. J Bacteriol 2006; 188:141-9; PMID:16352830; http:// dx.doi.org/10.1128/JB.188.1.141-149.2006.
16. Teplitski M, Al-Agely A, Ahmer BM. Contribution of the SirA regulon to biofilm formation in Salmonella enterica serovar Typhimurium. Microbiology 2006; 152:3411-24; PMID:17074910; http://dx.doi.org/10. 1099/mic.0.29118-0.
17. Johnston C, Pegues DA, Hueck CJ, Lee A, Miller SI. Transcriptional activation of Salmonella typhimurium invasion genes by a member of the phosphorylated response-regulator superfamily. Mol Microbiol 1996; 22:715-27; PMID:8951818; http://dx.doi.org/10. 1046/j.1365-2958.1996.d01-1719.x
18. Garmendia J, Beuzón CR, Ruiz-Albert J, Holden DW. The roles of SsrA-SsrB and OmpR-EnvZ in the regulation of genes encoding the Salmonella typhimurium SPI-2 type III secretion system. Microbiology 2003; 149:2385-96; PMID:12949164; http://dx.doi. org/10.1099/mic.0.26397-0.
19. Hensel M, Hinsley AP, Nikolaus T, Sawers G, Berks BC. The genetic basis of tetrathionate respiration in Salmonella typhimurium. Mol Microbiol 1999; 32: 275-87; PMID:10231485; http://dx.doi.org/10.1046/ j.1365-2958.1999.01345.x
20. Ahmer BM, van Reeuwijk J, Watson PR, Wallis TS, Heffron F. Salmonella SirA is a global regulator of genes mediating enteropathogenesis. Mol Microbiol 1999; 31:971-82; PMID:10048039; http://dx.doi.org/ 10.1046/j.1365-2958.1999.01244.x
21. Lawhon SD, Frye JG, Suyemoto M, Porwollik S, McClelland M, Altier C. Global regulation by CsrA in Salmonella typhimurium. Mol Microbiol 2003; 48: 1633-45; PMID:12791144; http://dx.doi.org/10. 1046/j.1365-2958.2003.03535.x
22. Fink RC, Evans MR, Porwollik S, Vazquez-Torres A, Jones-Carson J, Troxell B, et al. FNR is a global regulator of virulence and anaerobic metabolism in Salmonella enterica serovar Typhimurium (ATCC 14028s). J Bacteriol 2007; 189:2262-73; PMID: 17220229; http://dx.doi.org/10.1128/JB.00726-06.
23. Hansen-Wester I, Hensel M. Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect 2001; 3:549-59; PMID:11418329; http://dx. doi.org/10.1016/S1286-4579(01)01411-3.
24. Chen LM, Kaniga K, Galán JE. Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 1996; 21:1101-15; PMID:8885278; http://dx.doi.org/ 10.1046/j.1365-2958.1996.471410.x
25. Galán JE. Interaction of Salmonella with host cells through the centisome 63 type III secretion system. Curr Opin Microbiol 1999; 2:46-50; PMID: 10047557; http://dx.doi.org/10.1016/S1369-5274 (99)80008-3.
26. Galyov EE, Wood MW, Rosqvist R, Mullan PB, Watson PR, Hedges S, et al. A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa. Mol Microbiol 1997; 25:903- 12; PMID:9364916; http://dx.doi.org/10.1111/j. 1365-2958.1997.mmi525.x
27. Hobbie S, Chen LM, Davis RJ, Galán JE. Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J Immunol 1997; 159:5550-9; PMID: 9548496.
28. Galán JE. Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol 2001; 17:53-86; PMID:11687484; http://dx.doi.org/10. 1146/annurev.cellbio.17.1.53.
29. Knodler LA, Finlay BB, Steele-Mortimer O. The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J Biol Chem 2005; 280:9058-64; PMID:15642738; http://dx.doi.org/10.1074/jbc.M412588200.
30. Haraga A, Ohlson MB, Miller SI. Salmonellae interplay with host cells. Nat Rev Microbiol 2008; 6: 53-66; PMID:18026123; http://dx.doi.org/10.1038/ nrmicro1788.
31. Janssen R, van der Straaten T, van Diepen A, van Dissel JT. Responses to reactive oxygen intermediates and virulence of Salmonella typhimurium. Microbes Infect 2003; 5:527-34; PMID:12758282; http://dx. doi.org/10.1016/S1286-4579(03)00069-8.
32. Chakravortty D, Hansen-Wester I, Hensel M. Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J Exp Med 2002; 195:1155-66; PMID: 11994420; http://dx.doi.org/10.1084/jem.20011547.
33. Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 2010; 467:426-9; PMID:20864996; http://dx. doi.org/10.1038/nature09415.
34. Müller AJ, Kaiser P, Dittmar KE, Weber TC, Haueter S, Endt K, et al. Salmonella gut invasion involves TTSS-2-dependent epithelial traversal, basolateral exit, and uptake by epithelium-sampling lamina propria phagocytes. Cell Host Microbe 2012; 11:19-32; PMID:22264510; http://dx.doi.org/10.1016/j.chom. 2011.11.013.
35. Brown NF, Vallance BA, Coombes BK, Valdez Y, Coburn BA, Finlay BB. Salmonella pathogenicity island 2 is expressed prior to penetrating the intestine. PLoS Pathog 2005; 1:e32; PMID:16304611; http:// dx.doi.org/10.1371/journal.ppat.0010032.
36. Pavlova B, Volf J, Ondrackova P, Matiasovic J, Stepanova H, Crhanova M, et al. SPI-1-encoded type III secretion system of Salmonella enterica is required for the suppression of porcine alveolar macrophage cytokine expression. Vet Res 2011; 42:16; PMID: 21314975; http://dx.doi.org/10.1186/1297-9716-42-16.
37. Blanc-Potard AB, Solomon F, Kayser J, Groisman EA. The SPI-3 pathogenicity island of Salmonella enterica. J Bacteriol 1999; 181:998-1004; PMID:9922266.
38. Seth-Smith HM. SPI-7: Salmonella's Vi-encoding Pathogenicity Island. J Infect Dev Ctries 2008; 2: 267-71; PMID:19741287; http://dx.doi.org/10.3855/ jidc.220.
39. Townsend SM, Kramer NE, Edwards R, Baker S, Hamlin N, Simmonds M, et al. Salmonella enterica serovar Typhi possesses a unique repertoire of fimbrial gene sequences. Infect Immun 2001; 69:2894-901; PMID:11292704; http://dx.doi.org/10.1128/IAI.69. 5.2894-2901.2001.
40. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 2001; 413:848-52; PMID: 11677608; http://dx.doi.org/10.1038/35101607.
41. Lockman HA, Curtiss R, 3rd. Isolation and characterization of conditional adherent and non-type 1 fimbriated Salmonella typhimurium mutants. Mol Microbiol 1992; 6:933-45; PMID:1351241; http:// dx.doi.org/10.1111/j.1365-2958.1992.tb01543.x
42. Bäumler AJ, Tsolis RM, Bowe FA, Kusters JG, Hoffmann S, Heffron F. 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 1996; 64:61-8; PMID:8557375.
43. Bäumler AJ, Heffron F. Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella typhimurium. J Bacteriol 1995; 177:2087- 97; PMID:7721701.
44. Grund S, Weber A. A new type of fimbriae on Salmonella typhimurium. Zentralbl Veterinarmed B 1988; 35:779-82; PMID:2905857.
45. Dorsey CW, Laarakker MC, Humphries AD, Weening EH, Bäumler AJ. Salmonella enterica serotype Typhimurium MisL is an intestinal colonization factor that binds fibronectin. Mol Microbiol 2005; 57: 196-211; PMID:15948960; http://dx.doi.org/10. 1111/j.1365-2958.2005.04666.x
46. Kingsley RA, Santos RL, Keestra AM, Adams LG, Bäumler AJ. Salmonella enterica serotype Typhimurium ShdA is an outer membrane fibronectin-binding protein that is expressed in the intestine. Mol Microbiol 2002; 43:895-905; PMID:11929540; http://dx.doi.org/10. 1046/j.1365-2958.2002.02805.x
47. Gerlach RG, Jäckel D, Stecher B, Wagner C, Lupas A, Hardt WD, et al. Salmonella Pathogenicity Island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell Microbiol 2007; 9:1834- 50; PMID:17388786; http://dx.doi.org/10.1111/j. 1462-5822.2007.00919.x
48. Misselwitz B, Kreibich SK, Rout S, Stecher B, Periaswamy B, Hardt WD. Salmonella enterica serovar Typhimurium binds to HeLa cells via Fim-mediated reversible adhesion and irreversible type three secretion system 1-mediated docking. Infect Immun 2011; 79: 330-41; PMID:20974826; http://dx.doi.org/10.1128/ IAI.00581-10.
49. Guo A, Lasaro MA, Sirard JC, Kraehenbühl JP, Schifferli DM. Adhesin-dependent binding and uptake of Salmonella enterica serovar Typhimurium by dendritic cells. Microbiology 2007; 153:1059-69; PMID:17379714; http://dx.doi.org/10.1099/mic.0. 2006/000331-0.
50. Dibb-Fuller MP, Allen-Vercoe E, Thorns CJ, Woodward MJ. Fimbriae- and flagella-mediated association with and invasion of cultured epithelial cells by Salmonella enteritidis. Microbiology 1999; 145:1023- 31; PMID:10376817; http://dx.doi.org/10.1099/ 13500872-145-5-1023.
51. Browne SH, Hasegawa P, Okamoto S, Fierer J, Guiney DG. Identification of Salmonella SPI-2 secretion system components required for SpvB-mediated cytotoxicity in macrophages and virulence in mice. FEMS Immunol Med Microbiol 2008; 52:194-201; PMID:18248436; http://dx.doi.org/10.1111/j.1574- 695X.2007.00364.x
52. Bearson BL, Wilson L, Foster JW. A low pHinducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J Bacteriol 1998; 180:2409-17; PMID: 9573193.
53. Baik HS, Bearson S, Dunbar S, Foster JW. The acid tolerance response of Salmonella typhimurium provides protection against organic acids. Microbiology 1996; 142:3195-200; PMID:8969516; http://dx.doi. org/10.1099/13500872-142-11-3195.
54. Allam AS, Krishna MG, Sen M, Thomas R, Lahiri A, Gnanadhas DP, et al. Acidic pH induced STM1485 gene is essential for intracellular replication of Salmonella. Virulence 2012; 3:122-35; PMID: 22286698; http://dx.doi.org/10.4161/viru.19029.
55. Paesold G, Guiney DG, Eckmann L, Kagnoff MF. Genes in the Salmonella pathogenicity island 2 and the Salmonella virulence plasmid are essential for Salmonella-induced apoptosis in intestinal epithelial cells. Cell Microbiol 2002; 4:771-81; PMID:12427099; http://dx.doi.org/10.1046/j.1462-5822.2002.00233.x
56. Vazquez-Torres A, Jones-Carson J, Bäumler AJ, Falkow S, Valdivia R, Brown W, et al. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 1999; 401:804-8; PMID: 10548107; http://dx.doi.org/10.1038/44593.
57. Eswarappa SM, Panguluri KK, Hensel M, Chakravortty D. The yejABEF operon of Salmonella confers resistance to antimicrobial peptides and contributes to its virulence. Microbiology 2008; 154:666- 78; PMID:18227269; http://dx.doi.org/10.1099/mic. 0.2007/011114-0.
58. Nizet V. Antimicrobial peptide resistance mechanisms of human bacterial pathogens. Curr Issues Mol Biol 2006; 8:11-26; PMID:16450883.
59. Eswarappa SM, Negi VD, Chakraborty S, Chandrasekhar Sagar BK, Chakravortty D. Division of the Salmonella-containing vacuole and depletion of acidic lysosomes in Salmonella-infected host cells are novel strategies of Salmonella enterica to avoid lysosomes. Infect Immun 2010; 78:68-79; PMID: 19858305; http://dx.doi.org/10.1128/IAI.00668-09.
60. Lahiri A, Lahiri A, Iyer N, Das P, Chakravortty D. Visiting the cell biology of Salmonella infection. Microbes Infect 2010; 12:809-18; PMID:20538070; http://dx.doi.org/10.1016/j.micinf.2010.05.010.
61. Das P, Lahiri A, Lahiri A, Chakravortty D. Modulation of the arginase pathway in the context of microbial pathogenesis: a metabolic enzyme moonlighting as an immune modulator. PLoS Pathog 2010; 6:e1000899; PMID:20585552; http://dx.doi.org/10.1371/journal. ppat.1000899.
62. Das P, Lahiri A, Lahiri A, Sen M, Iyer N, Kapoor N, et al. Cationic amino acid transporters and Salmonella Typhimurium ArgT collectively regulate arginine availability towards intracellular Salmonella growth. PLoS One 2010; 5:e15466; PMID:21151933; http:// dx.doi.org/10.1371/journal.pone.0015466.
63. Spector MP, Cubitt CL. Starvation-inducible loci of Salmonella typhimurium: regulation and roles in starvation-survival. Mol Microbiol 1992; 6:1467-76; PMID:1320726; http://dx.doi.org/10.1111/j.1365- 2958.1992.tb00867.x
64. Jepson MA, Clark MA. The role of M cells in Salmonella infection. Microbes Infect 2001; 3:1183- 90; PMID:11755406; http://dx.doi.org/10.1016/ S1286-4579(01)01478-2.
65. Martinez-Argudo I, Jepson MA. Salmonella translocates across an in vitro M cell model independently of SPI-1 and SPI-2. Microbiology 2008; 154:3887-94; PMID:19047755; http://dx.doi.org/10.1099/mic.0. 2008/021162-0.
66. Gullberg E, Leonard M, Karlsson J, Hopkins AM, Brayden D, Baird AW, et al. Expression of specific markers and particle transport in a new human intestinal M-cell model. Biochem Biophys Res Commun 2000; 279:808-13; PMID:11162433; http://dx.doi.org/10.1006/bbrc.2000.4038.
67. Lim JS, Na HS, Lee HC, Choy HE, Park SC, Han JM, et al. Caveolae-mediated entry of Salmonella typhimurium in a human M-cell model. Biochem Biophys Res Commun 2009; 390:1322-7; PMID: 19879241; http://dx.doi.org/10.1016/j.bbrc.2009.10. 145.
68. Mehta A, Singh S, Ganguly NK. Role of reactive oxygen species in Salmonella typhimurium-induced enterocyte damage. Scand J Gastroenterol 1998; 33: 406-14; PMID:9605263; http://dx.doi.org/10.1080/ 00365529850171044.
69. van der Velden AW, Velasquez M, Starnbach MN. Salmonella rapidly kill dendritic cells via a caspase-1- dependent mechanism. J Immunol 2003; 171:6742-9; PMID:14662878.
70. Bonneau M, Epardaud M, Payot F, Niborski V, Thoulouze MI, Bernex F, et al. Migratory monocytes and granulocytes are major lymphatic carriers of Salmonella from tissue to draining lymph node. J Leukoc Biol 2006; 79:268-76; PMID:16330534; http://dx.doi.org/10.1189/jlb.0605288.
71. Cunnington AJ, de Souza JB, Walther M, Riley EM. Malaria impairs resistance to Salmonella through heme- and heme oxygenase-dependent dysfunctional granulocyte mobilization. Nat Med 2012; 18:120-7; PMID:22179318; http://dx.doi.org/10.1038/nm.2601.
72. Hölzer SU, Hensel M. Divergent roles of Salmonella pathogenicity island 2 and metabolic traits during interaction of S. enterica serovar typhimurium with host cells. PLoSOne 2012; 7:e33220; PMID:22427996; http://dx.doi.org/10.1371/journal.pone.0033220.
73. O'Brien AD. Innate resistance of mice to Salmonella typhi infection. Infect Immun 1982; 38:948-52; PMID:7152679.
74. Mian MF, Pek EA, Chenoweth MJ, Coombes BK, Ashkar AA. Humanized mice for Salmonella typhi infection: new tools for an old problem. Virulence 2011; 2:248-52; PMID:21623167; http://dx.doi.org/ 10.4161/viru.2.3.16133.
75. Aballay A, Yorgey P, Ausubel FM. Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr Biol 2000; 10:1539-42; PMID:11114525; http://dx.doi.org/10.1016/S0960-9822(00)00830-7.
76. Menendez A, Arena ET, Guttman JA, Thorson L, Vallance BA, Vogl W, et al. Salmonella infection of gallbladder epithelial cells drives local inflammation and injury in a model of acute typhoid fever. J Infect Dis 2009; 200:1703-13; PMID:19852670; http://dx. doi.org/10.1086/646608.
77. Griffin AJ, Li LX, Voedisch S, Pabst O, McSorley SJ. Dissemination of persistent intestinal bacteria via the mesenteric lymph nodes causes typhoid relapse. Infect Immun 2011; 79:1479-88; PMID:21263018; http:// dx.doi.org/10.1128/IAI.01033-10.
78. Prouty AM, Schwesinger WH, Gunn JS. Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect Immun 2002; 70:2640-9; PMID:11953406; http://dx.doi.org/10. 1128/IAI.70.5.2640-2649.2002.
79. Srifuengfung S, Chokephaibulkit K, Yungyuen T, Tribuddharat C. Salmonella meningitis and antimicrobial susceptibilities. Southeast Asian J Trop Med Public Health 2005; 36:312-6; PMID:15916035.
80. Ryan RM, Green J, Lewis CE. Use of bacteria in anticancer therapies. Bioessays 2006; 28:84-94; PMID: 16369949; http://dx.doi.org/10.1002/bies.20336.
81. Pawelek JM, Low KB, Bermudes D. Tumor-targeted Salmonella as a novel anticancer vector. Cancer Res 1997; 57:4537-44; PMID:9377566.
82. Bermudes D, Low B, Pawelek J. Tumor-targeted Salmonella. Highly selective delivery vectors. Adv Exp Med Biol 2000; 465:57-63; PMID:10810615; http:// dx.doi.org/10.1007/0-306-46817-4_6.
83. Avogadri F, Martinoli C, Petrovska L, Chiodoni C, Transidico P, Bronte V, et al. Cancer immunotherapy based on killing of Salmonella-infected tumor cells. Cancer Res 2005; 65:3920-7; PMID:15867392; http://dx.doi.org/10.1158/0008-5472.CAN-04-3002.
84. Weyel D, Sedlacek HH, Müller R, Brüsselbach S. Secreted human beta-glucuronidase: a novel tool for gene-directed enzyme prodrug therapy. Gene Ther 2000; 7:224-31; PMID:10694799; http://dx.doi.org/ 10.1038/sj.gt.3301072.
85. Low KB, Ittensohn M, Le T, Platt J, Sodi S, Amoss M, et al. Lipid A mutant Salmonella with suppressed virulence and TNFalpha induction retain tumortargeting in vivo. Nat Biotechnol 1999; 17:37-41; PMID:9920266; http://dx.doi.org/10.1038/5205.
86. Rosenberg SA, Spiess PJ, Kleiner DE. Antitumor effects in mice of the intravenous injection of attenuated Salmonella typhimurium. J Immunother 2002; 25:218-25; PMID:12000863; http://dx.doi.org/ 10.1097/00002371-200205000-00004.
87. Jia LJ, Wei DP, Sun QM, Huang Y, Wu Q, Hua ZC. Oral delivery of tumor-targeting Salmonella for cancer therapy in murine tumor models. Cancer Sci 2007; 98: 1107-12; PMID:17498202; http://dx.doi.org/10. 1111/j.1349-7006.2007.00503.x
88. Lee CH, Wu CL, Shiau AL. Toll-like receptor 4 mediates an antitumor host response induced by Salmonella choleraesuis. Clin Cancer Res 2008; 14: 1905-12; PMID:18347194; http://dx.doi.org/10. 1158/1078-0432.CCR-07-2050.
89. Hayashi K, Zhao M, Yamauchi K, Yamamoto N, Tsuchiya H, Tomita K, et al. Cancer metastasis directly eradicated by targeted therapy with a modified Salmonella typhimurium. J Cell Biochem 2009; 106: 992-8; PMID:19199339; http://dx.doi.org/10.1002/ jcb.22078.
90. Hoffman RM. Tumor-targeting amino acid auxotrophic Salmonella typhimurium. Amino Acids 2009; 37:509-21; PMID:19291366; http://dx.doi.org/10. 1007/s00726-009-0261-8.
91. Toso JF, Gill VJ, Hwu P, Marincola FM, Restifo NP, Schwartzentruber DJ, et al. Phase I study of the intravenous administration of attenuated Salmonella typhimurium to patients with metastatic melanoma. J Clin Oncol 2002; 20:142-52; PMID:11773163; http://dx.doi.org/10.1200/JCO.20.1.142.
92. Panthel K, Meinel KM, Sevil Domènech VE, Geginat G, Linkemann K, Busch DH, et al. Prophylactic anti-tumor immunity against a murine fibrosarcoma triggered by the Salmonella type III secretion system. Microbes Infect 2006; 8:2539-46; PMID:16919987; http://dx.doi.org/10.1016/j.micinf.2006.07.004.
93. Liu F, Zhang L, Hoffman RM, Zhao M. Vessel destruction by tumor-targeting Salmonella typhimurium A1-R is enhanced by high tumor vascularity. Cell Cycle 2010; 9:4518-24; PMID:21135579; http:// dx.doi.org/10.4161/cc.9.22.13744.
94. Arrach N, Zhao M, Porwollik S, Hoffman RM, McClelland M. Salmonella promoters preferentially activated inside tumors. Cancer Res 2008; 68:4827- 32; PMID:18559530; http://dx.doi.org/10.1158/ 0008-5472.CAN-08-0552.
95. Arrach N, Cheng P, Zhao M, Santiviago CA, Hoffman RM, McClelland M. High-throughput screening for salmonella avirulent mutants that retain targeting of solid tumors. Cancer Res 2010; 70:2165-70; PMID: 20231149; http://dx.doi.org/10.1158/0008-5472. CAN-09-4005.
96. Leschner S, Deyneko IV, Lienenklaus S, Wolf K, Bloecker H, Bumann D, et al. Identification of tumorspecific Salmonella Typhimurium promoters and their regulatory logic. Nucleic Acids Res 2012; 40:2984- 94; PMID:22140114; http://dx.doi.org/10.1093/nar/ gkr1041.
97. Xiang R, Luo Y, Niethammer AG, Reisfeld RA. Oral DNA vaccines target the tumor vasculature and microenvironment and suppress tumor growth and metastasis. Immunol Rev 2008; 222:117-28; PMID: 18363997; http://dx.doi.org/10.1111/j.1600-065X. 2008.00613.x
98. Roider E, Jellbauer S, Köhn B, Berchtold C, Partilla M, Busch DH, et al. Invasion and destruction of a murine fibrosarcoma by Salmonella-induced effector CD8 T cells as a therapeutic intervention against cancer. Cancer Immunol Immunother 2011; 60:371- 80; PMID:21132428; http://dx.doi.org/10.1007/ s00262-010-0950-x
99. Panthel K, Meinel KM, Sevil Domènech VE, Trülzsch K, Rüssmann H. Salmonella type III-mediated heterologous antigen delivery: a versatile oral vaccination strategy to induce cellular immunity against infectious agents and tumors. Int J Med Microbiol 2008; 298:99- 103; PMID:17719275; http://dx.doi.org/10.1016/j. ijmm.2007.07.002.
100. Xiong G, Husseiny MI, Song L, Erdreich-Epstein A, Shackleford GM, Seeger RC, et al. Novel cancer vaccine based on genes of Salmonella pathogenicity island 2. Int J Cancer 2010; 126:2622-34; PMID: 19824039.
101. Kang HY, Srinivasan J, Curtiss R, 3rd. Immune responses to recombinant pneumococcal PspA antigen delivered by live attenuated Salmonella enterica serovar typhimurium vaccine. Infect Immun 2002; 70:1739- 49; PMID:11895935; http://dx.doi.org/10.1128/IAI. 70.4.1739-1749.2002.
102. Corthésy-Theulaz IE, Hopkins S, Bachmann D, Saldinger PF, Porta N, Haas R, et al. Mice are protected from Helicobacter pylori infection by nasal immunization with attenuated Salmonella typhimurium phoPc expressing urease A and B subunits. Infect Immun 1998; 66:581-6; PMID:9453612.
103. Grant AJ, Restif O, McKinley TJ, Sheppard M, Maskell DJ, Mastroeni P. Modelling within-host spatiotemporal dynamics of invasive bacterial disease. PLoS Biol 2008; 6:e74; PMID:18399718; http://dx. doi.org/10.1371/journal.pbio.0060074.
104. Mastroeni P, Grant A, Restif O, Maskell D. A dynamic view of the spread and intracellular distribution of Salmonella enterica. Nat Rev Microbiol 2009; 7:73- 80; PMID:19079353; http://dx.doi.org/10.1038/ nrmicro2034.
105. Gog JR, Murcia A, Osterman N, Restif O, McKinley TJ, Sheppard M, et al. Dynamics of Salmonella infection of macrophages at the single cell level. J R Soc Interface 2012; In press; PMID:22552918; http:// dx.doi.org/10.1098/rsif.2012.0163.
106. Ganesh AB, Rajasingh H, Mande SS. Mathematical modeling of regulation of type III secretion system in Salmonella enterica serovar Typhimurium by SirA. In Silico Biol 2009; 9:S57-72; PMID:19537165.
107. Bonhoeffer S, May RM, Shaw GM, Nowak MA. Virus dynamics and drug therapy. Proc Natl Acad Sci U S A 1997; 94:6971-6; PMID:9192676; http://dx.doi.org/ 10.1073/pnas.94.13.6971.
108. Wodarz D, Nowak MA. HIV therapy: managing resistance. Proc Natl Acad Sci U S A 2000; 97:8193-5; PMID:10899988; http://dx.doi.org/10.1073/pnas.97. 15.8193.
109. Sheppard M, Webb C, Heath F, Mallows V, Emilianus R, Maskell D, et al. Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell Microbiol 2003; 5:593-600; PMID:12925129; http://dx.doi.org/10.1046/j. 1462-5822.2003.00296.x
110. Chapagain PP, van Kessel JS, Karns JS, Wolfgang DR, Hovingh E, Nelen KA, et al. A mathematical model of the dynamics of Salmonella Cerro infection in a US dairy herd. Epidemiol Infect 2008; 136:263-72; PMID:17445313; http://dx.doi.org/10.1017/ S0950268807008400.
111. Setta A, Barrow PA, Kaiser P, Jones MA. Immune dynamics following infection of avian macrophages and epithelial cells with typhoidal and non-typhoidal Salmonella enterica serovars; bacterial invasion and persistence, nitric oxide and oxygen production, differential host gene expression, NF-kB signalling and cell cytotoxicity. Vet Immunol Immunopathol 2012; 146: 212-24; PMID:22475571; http://dx.doi.org/10.1016/ j.vetimm.2012.03.008.
112. Setta AM, Barrow PA, Kaiser P, Jones MA. Early immune dynamics following infection with Salmonella enterica serovars Enteritidis, Infantis, Pullorum and Gallinarum: Cytokine and chemokine gene expression profile and cellular changes of chicken cecal tonsils. Comp Immunol Microbiol Infect Dis 2012; 35:397- 410; PMID:22512820; http://dx.doi.org/10.1016/j. cimid.2012.03.004.
113. Ruan J, St John G, Ehrt S, Riley L, Nathan C. noxR3, a novel gene from Mycobacterium tuberculosis, protects Salmonella typhimurium from nitrosative and oxidative stress. Infect Immun 1999; 67:3276-83; PMID:10377101.
114. Madan R, Rastogi R, Parashuraman S, Mukhopadhyay A. Salmonella acquires lysosome-associated membrane protein 1 (LAMP1) on phagosomes from Golgi via SipC protein-mediated recruitment of host Syntaxin6. J Biol Chem 2012; 287:5574-87; PMID:22190682; http://dx.doi.org/10.1074/jbc.M111.286120.
115. Payton M, Auty R, Delgoda R, Everett M, Sim E. Cloning and characterization of arylamine N-acetyltransferase genes from Mycobacterium smegmatis and Mycobacterium tuberculosis: increased expression results in isoniazid resistance. J Bacteriol 1999; 181: 1343-7; PMID:9973365