Salmonella-host interactions - modulation of the host innate immune system

Frontiers in Immunology

Volumn 5, Issue OCT, 2014, Pages

  Hurley, Daniel ^a   McCusker, Matthew P ^a   Fanning, Séamus ^a   Martins, Marta ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Gastroenteritis; Host innate immunity; Macrophages; NTS; Pathogenicity islands; Salmonellosis

Indexed keywords

LIPOPOLYSACCHARIDE;

BACTERIAL TRANSMISSION; CYTOKINE RESPONSE; EVOLUTIONARY ADAPTATION; GASTROENTERITIS; GRAM NEGATIVE BACTERIUM; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE DEFICIENCY; IMMUNE RESPONSE; INNATE IMMUNITY; MACROPHAGE; MODULATION; NONHUMAN; PATHOGENICITY; PATHOGENICITY ISLAND; PHAGOCYTOSIS; REVIEW; SALMONELLA ENTERICA; SYSTEMIC DISEASE; TYPHOID FEVER;

EID: 84916640846     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00481     Document Type: Review

References (98)

1. Gunn JS, Marshall JM, Baker S, Dongol S, Charles RC, Ryan ET. Salmonella chronic carriage: epidemiology, diagnosis, and gallbladder persistence. Trends Microbiol (2014). doi: 10.1016/j.tim.2014.06.007
2. Gal-Mor O, Boyle EC, Grassl GA. Same species, different diseases: how and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Front Microbiol (2014) 5:391. doi:10.3389/fmicb.2014.00391
3. Batz MB, Henke E, Kowalcyk B. Long-term consequences of foodborne infections. Infect Dis Clin North Am (2013) 27(3):599-616. doi:10.1016/j.idc.2013.05.003
4. Chen HM, Wang Y, Su LH, Chiu CH. Nontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatr Neonatol (2013) 54(3):147-52. doi:10.1016/j.pedneo.2013.01.010
5. Fàbrega A, Vila J. Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev (2013) 26(2):308-41. doi:10.1128/CMR.00066-12
6. Santos RL. Pathobiology of salmonella, intestinal microbiota, and the host innate immune response. Front Immunol (2014) 26(5):252. doi:10.3389/fimmu.2014.00252
7. Ruby T, McLaughlin L, Gopinath S, Monack D. Salmonella's long-term relationship with its host. FEMS Microbiol Rev (2012) 36(3):600-15. doi:10.1111/j.1574-6976.2012.00332.x
8. Croswell A, Amir E, Teggatz P, Barman M, Salzman NH. Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric Salmonella infection. Infect Immun (2009) 77(7):2741-53. doi:10.1128/IAI.00006-09
9. Gopinath S, Carden S, Monack D. Shedding light on Salmonella carriers. Trends Microbiol (2012) 20(7):320-7. doi:10.1016/j.tim.2012.04.004
10. Thiennimitr P, Winter SE, Bäumler AJ. Salmonella, the host and its microbiota. Curr Opin Microbiol (2012) 15(1):108-14. doi:10.1016/j.mib.2011.10.002
11. Raffatellu M, Wilson RP, Winter SE, Bäumler AJ. Clinical pathogenesis of typhoid fever. J Infect Dev Ctries (2008) 2(4):260-6. doi:10.3855/jidc.219
12. Crump JA, Mintz ED. Global trends in typhoid and paratyphoid fever. Clin Infect Dis (2010) 50(2):241-6. doi:10.1086/649541
13. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis (2010) 50(6):882-9. doi:10.1086/650733
14. Coburn B, Grassl GA, Finlay BB. Salmonella, the host and disease: a brief review. Immunol Cell Biol (2006) 85(2):112-8. doi:10.1038/sj.icb.7100007
15. de Jong HK, Parry CM, van der Poll T, Wiersinga WJ. Host-pathogen interaction in invasive Salmonellosis. PLoS Pathog (2012) 8(10):e1002933. doi:10.1371/journal.ppat.1002933
16. Fierer J, Guiney DG. Diverse virulence traits underlying different clinical outcomes of Salmonella infection. J Clin Invest (2001) 107(7):775-80. doi:10.1172/JCI12561
17. Bäumler AJ, Tsolis RM, Ficht TA, Adams LG. Evolution of host adaptation in Salmonella enterica. Infect Immun (1998) 66(10):4579-87.
18. Stecher B, Macpherson AJ, Hapfelmeier S, Kremer M, Stallmach T, Hardt W-D. Comparison of Salmonella enterica serovar Typhimurium colitis in germfree mice and mice pretreated with streptomycin. Infect Immun (2005) 73(6):3228-41. doi:10.1128/IAI.73.6.3228-3241.2005
19. Gordon MA. Salmonella infections in immunocompromised adults. J Infect (2008) 56(6):413-22. doi:10.1016/j.jinf.2008.03.012
20. Dhanoa A, Fatt QK. Non-typhoidal Salmonella bacteraemia: epidemiology, clinical characteristics and its' association with severe immunosuppression. Ann Clin Microbiol Antimicrob (2009) 8:15. doi:10.1186/1476-0711-8-15
21. Richter-Dahlfors A, Buchan AMJ, Finlay BB. Murine Salmonellosis studied by confocal microscopy: Salmonella Typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med (1997) 186(4):569-80. doi:10.1084/jem.186.4.569
22. Yrlid U, Svensson M, Håkansson A, Chambers BJ, Ljunggren HG, Wick MJ. In vivo activation of dendritic cells and T cells during Salmonella enterica serovar Typhimurium infection. Infect Immun (2001) 69(9):5726-35. doi:10.1128/IAI.69.9.5726-5735.2001
23. 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(10):9058-64. doi:10.1074/jbc.M412588200
24. Ibarra JA, Steele-Mortimer O. Salmonella - the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol (2009) 11(11):1579-86. doi:10.1111/j.1462-5822.2009.01368.x
25. Sabbagh SC, Forest CG, Lepage C, Leclerc J-M, Daigle F. So similar, yet so different: uncovering distinctive features in the genomes of Salmonella enterica serovars Typhimurium and Typhi. FEMS Microbiol Lett (2010) 305(1):1-13. doi:10.1111/j.1574-6968.2010.01904.x
26. Hayward MR, Jansen VAA, Woodward MJ. Comparative genomics of Salmonella enterica serovars Derby and Mbandaka, two prevalent serovars associated with different livestock species in the UK. BMC Genomics (2013) 14(1):365. doi:10.1186/1471-2164-14-365
27. Galán JE. Interaction of Salmonella with host cells through the centisome 63 Type III secretion system. Curr Opin Microbiol (1999) 2(1):46-50. doi:10.1016/S1369-5274(99)80008-3
28. Hensel M, Shea JE, Waterman SR, Mundy R, Nikolaus T, Banks G, et al. 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 (1998) 30(1):163-74. doi:10.1046/j.1365-2958.1998.01047.x
29. Ehrbar K, Friebel A, Miller SI, Hardt WD. 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 (2003) 185(23):6950-67. doi:10.1128/JB.185.23.6950-6967.2003
30. Hapfelmeier S, Stecher B, Barthel M, Kremer M, Müller AJ, Heikenwalder M, et al. The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J Immunol (2005) 174(3):1675-85. doi:10.4049/jimmunol.174.3.1675
31. Ibarra JA, Knodler LA, Sturdevant DE, Virtaneva K, Carmody AB, Fischer ER, et al. Induction of Salmonella pathogenicity island 1 under different growth conditions can affect Salmonella-host cell interactions in vitro. Microbiology (2010) 156(Pt 4):1120-33. doi:10.1099/mic.0.032896-0
32. Waterman SR, Holden DW. Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol (2003) 5:501-11. doi:10.1046/j.1462-5822.2003.00294.x
33. Figueira R, Watson KG, Holden DW, Helaine S. Identification of Salmonella pathogenicity island-2 type III secretion system effectors involved in intramacrophage replication of S. enterica serovar Typhimurium: implications for rational vaccine design. MBio (2013) 4(2):e00065-13. doi:10.1128/mBio.00065-13
34. Blanc-Potard AB, Solomon F, Kayser J, Groisman EA. The SPI-3 pathogenicity island of Salmonella enterica. J Bacteriol (1999) 181(3):998-1004.
35. Rychlik I, Karasova D, Sebkova A. Virulence potential of five major pathogenicity islands (SPI-1 to SPI-5) of Salmonella enterica serovar enteritidis for chickens. BMC Microbiol (2009) 9:268. doi:10.1186/1471-2180-9-268
36. Kiss T, Morgan E, Nagy G. Contribution of SPI-4 genes to the virulence of Salmonella enterica. FEMS Microbiol Lett (2007) 275(1):153-9. doi:10.1111/j.1574-6968.2007.00871.x
37. Gerlach RG, Jäckel D, Stecher B. Salmonella pathogenicity island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell Microbiol (2007) 9(7):1834-50. doi:10.1111/j.1462-5822.2007.00919.x
38. Zhang S, Santos RL, Tsolis RM, Stender S, Hardt W-D, Bäumler AJ, et al. The Salmonella enterica serotype Typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 Act in concert to induce diarrhea in calves. Infect Immun (2002) 70(7):3843-55. doi:10.1128/IAI.70.7.3843-3855.2002
39. Marcus SL, Brumell JH, Pfeifer CG, Finlay BB. Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect (2000) 2(2):145-56. doi:10.1016/S1286-4579(00)00273-2
40. McCormick BA, Colgan SP, Delp-Archer C, Miller SI, Madara JL. Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol (1993) 123(4):895-907. doi:10.1083/jcb.123.4.895
41. Gewirtz AT, Siber AM, Madara JL, McCormick BA. Orchestration of neutrophil movement by intestinal epithelial cells in response to Salmonella Typhimurium can be uncoupled from bacterial internalization. Infect Immun (1999) 67(2):608-17.
42. Lee CA, Silva M, Siber AM, Kelly AJ, Galyov E, McCormick BA. A secreted Salmonella protein induces a proinflammatory response in epithelial cells, which promotes neutrophil migration. Proc Natl Acad Sci USA (2000) 97(22):12283-8. doi:10.1073/pnas.97.22.12283
43. 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(11):5550-9.
44. Hernandez LD, Pypaert M, Flavell RA, Galán JE. A Salmonella protein causes macrophage cell death by inducing autophagy. J Cell Biol (2003) 163(5):1123-31. doi:10.1083/jcb.200309161
45. Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun (2005) 73(4):1907-16. doi:10.1128/IAI.73.4.1907-1916.2005
46. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA (1999) 96(5):2396-401. doi:10.1073/pnas.96.5.2396
47. Lara-Tejero M, Sutterwala FS, Ogura Y, Grant EP, Bertin J, Coyle AJ, et al. Role of the caspase-1 inflammasome in Salmonella Typhimurium pathogenesis. J Exp Med (2006) 203(6):1407-12. doi:10.1084/jem.20060206
48. Coburn B, Li Y, Owen D, Vallance BA, Finlay BB. Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect Immun (2005) 73(6):3219-27. doi:10.1128/IAI.73.6.3219-3227.2005
49. Figueira R, Holden DW. Functions of the Salmonella pathogenicity island 2 (SPI-2) type III secretion system effectors. Microbiology (2012) 158(Pt 5):1147-61. doi:10.1099/mic.0.058115-0
50. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat Immunol (2010) 11(5):373-84. doi:10.1038/ni.1863
51. Schroder K, Tschopp J. The inflammasomes. Cell (2010) 140(6):821-32. doi:10.1016/j.cell.2010.01.040
52. Vazquez-Torres A, Vallance BA, Bergman MA, Finlay BB, Cookson BT, Jones-Carson J, et al. Toll-like receptor 4 dependence of innate and adaptive immunity to Salmonella: importance of the Kupffer cell network. J Immunol (2004) 172(10):6202-8. doi:10.4049/jimmunol.172.10.6202
53. Wilson RP, Raffatellu M, Chessa D, Winter SE, Tükel C, Bäumler AJ. The Vi-capsule prevents toll-like receptor 4 recognition of Salmonella. Cell Microbiol (2008) 10(4):876-90. doi:10.1111/j.1462-5822.2007.01090.x
54. O'Brien GC, Wang JH, Redmond HP. Bacterial lipoprotein induces resistance to Gram-negative sepsis in TLR4-deficient mice via enhanced bacterial clearance. J Immunol (2005) 174(2):1020-6. doi:10.4049/jimmunol.174.2.1020
55. Janeway CA Jr., Travers P, Walport M, Shlomchik MJ. Immunobiology. New York: Garland Science (2001).
56. Delves PJ, Martin SJ, Burton DR, Roitt IM. Essential Immunology. New Jersey: Wiley-Blackwell (2011).
57. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol (2001) 2(4):361-7. doi:10.1038/86373
58. Jones BD, Ghori N, Falkow S. Salmonella Typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med (1994) 180(1):15-23. doi:10.1084/jem.180.1.15
59. Crawford RW, Rosales-Reyes R, Ramírez-Aguilar Mde L, Chapa-Azuela O, Alpuche-Aranda C, Gunn JS. Gallstones play a significant role in Salmonella spp. gall bladder colonization and carriage. Proc Natl Acad Sci USA (2010) 107(9):4353-8. doi:10.1073/pnas.1000862107
60. Gonzalez-Escobedo G, Marshall JM, Gunn JS. Chronic and acute infection of the gall bladder by Salmonella Typhi: understanding the carrier state. Nat Rev Microbiol (2011) 9(1):9-14. doi:10.1038/nrmicro2490
61. Gorvel JP, Méresse S. Maturation steps of the Salmonella-containing vacuole. Microbes Infect (2001) 3(14-15):1299-303. doi:10.1016/S1286-4579(01)01490-3
62. Coombes BK, Coburn BA, Potter AA, Gomis S, Mirakhur K, Li Y, et al. Analysis of the contribution of Salmonella pathogenicity islands 1 and 2 to enteric disease progression using a novel bovine ileal loop model and a murine model of infectious enterocolitis. Infect Immun (2005) 73(11):7161-9. doi:10.1128/IAI.73.11.7161-7169.2005
63. Pullinger GD, Paulin SM, Charleston B, Watson PR, Bowen AJ, Dziva F, et al. Systemic translocation of Salmonella enterica serovar Dublin in cattle occurs predominantly via efferent lymphatics in a cell-free niche and requires type III secretion system 1 (T3SS-1) but not T3SS-2. Infect Immun (2007) 75(11):5191-9. doi:10.1128/IAI.00784-07
64. Butler T, Ho M, Acharya G, Tiwari M, Gallati H. Interleukin-6, gamma interferon, and tumor necrosis factor receptors in typhoid fever related to outcome of antimicrobial therapy. Antimicrob Agents Chemother (1993) 37(11):2418-21. doi:10.1128/AAC.37.11.2418
65. Monack DM, Bouley DM, Falkow S. Salmonella typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp1+/+ Mice and can be reactivated by IFNgamma neutralization. J Exp Med (2004) 199(2):231-41. doi:10.1084/jem.20031319
66. Thompson LJ, Dunstan SJ, Dolecek C, Perkins T, House D, Dougan G, et al. Transcriptional response in the peripheral blood of patients infected with Salmonella enterica serovar typhi. Proc Natl Acad Sci USA (2009) 106(52):22433-8. doi:10.1073/pnas.0912386106
67. Gal-Mor O, Suez J, Elhadad D, Porwollik S, Leshem E, Valinsky L, et al. Molecular and cellular characterization of a Salmonella enterica serovar Paratyphi A outbreak strain and the human immune response to infection. Clin Vaccine Immunol (2012) 19(2):146-56. doi:10.1128/CVI.05468-11
68. Mastroeni P, Clare S, Khan S, Harrison JA, Hormaeche CE, Okamura H, et al. Interleukin 18 contributes to host resistance and gamma interferon production in mice infected with virulent Salmonella Typhimurium. Infect Immun (1999) 67(2):478-83.
69. Svensson M, Johansson C, Wick MJ. Salmonella Typhimurium-induced cytokine production and surface molecule expression by murine macrophages. Microb Pathog (2001) 31(2):91-102. doi:10.1006/mpat.2001.0448
70. Rosenberger CM, Pollard AJ, Finlay BB. Gene array technology to determine host responses to Salmonella. Microbes Infect (2001) 3(14-15):1353-60. doi:10.1016/S1286-4579(01)01497-6
71. Jung HC, Eckmann L, Yang SK, Panja A, Fierer J, Morzycka-Wroblewska E, et al. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest (1995) 95(1):55-65. doi:10.1172/JCI117676
72. Pietilä TE, Veckman V, Kyllönen P, Lähteenmäki K, Korhonen TK, Julkunen I. Activation, cytokine production, and intracellular survival of bacteria in Salmonella-infected human monocyte-derived macrophages and dendritic cells. J Leukoc Biol (2005) 78(4):909-20. doi:10.1189/jlb.1204721
73. Depaolo RW, Lathan R, Rollins BJ, Karpus WJ. The chemokine CCL2 is required for control of murine gastric Salmonella enterica infection. Infect Immun (2005) 73(10):6514-22. doi:10.1128/IAI.73.10.6514-6522.2005
74. Uchiya K-I, Groisman EA, Nikai T. Involvement of Salmonella pathogenicity island 2 in the up-regulation of interleukin-10 expression in macrophages: role of protein kinase A signal pathway. Infect Immun (2004) 72(4):1964-73. doi:10.1128/IAI.72.4.1964-1973.2004
75. Kröger C, Dillon SC, Cameron AD, Papenfort K, Sivasankaran SK, Hokamp K, et al. The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci USA (2012) 109(20):E1277-86. doi:10.1073/pnas.1201061109
76. Kröger C, Colgan A, Srikumar S, Händler K, Sivasankaran SK, Hammarlöf DL, et al. An infection-relevant transcriptomic compendium for Salmonella enterica serovar Typhimurium. Cell Host Microbe (2013) 14(6):683-95. doi:10.1016/j.chom.2013.11.010
77. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol (2003) 47(1):103-18. doi:10.1046/j.1365-2958.2003.03313.x
78. Bowden SD, Rowley G, Hinton JC, Thompson A. Glucose and glycolysis are required for the successful infection of macrophages and mice by Salmonella enterica serovar Typhimurium. Infect Immun (2009) 77(7):3117-26. doi:10.1128/IAI.00093-09
79. Hernández SB, Cota I, Ducret A, Aussel L, Casadesús J. Adaptation and preadaptation of Salmonella enterica to bile. PLoS Genet (2012) 8(1):e1002459. doi:10.1371/journal.pgen.1002459
80. Shah J, Desai PT, Chen D, Stevens JR, Weimer BC. Preadaptation to cold stress in Salmonella enterica serovar Typhimurium increases survival during subsequent acid stress exposure. Appl Environ Microbiol (2013) 79(23):7281-9. doi:10.1128/AEM.02621-13
81. Van der Poll T, Opal SM. Host-pathogen interactions in sepsis. Lancet Infect Dis (2008) 8(1):32-43. doi:10.1016/S1473-3099(07)70265-7
82. de Jong HK, van der Poll T, Wiersinga WJ. The systemic pro-inflammatory response in sepsis. J Innate Immun (2010) 2(5):422-30. doi:10.1159/000316286
83. Raffatellu M, Chessa D, Wilson RP, Tükel C, Akçelik M, Bäumler AJ. Capsule-mediated immune evasion: a new hypothesis explaining aspects of typhoid fever pathogenesis. Infect Immun (2006) 74(1):19-27. doi:10.1128/IAI.74.1.19-27.2006
84. Näsström E, Vu Thieu NT, Dongol S, Karkey A, Voong Vinh P, Ha Thanh T, et al. Salmonella Typhi and Salmonella Paratyphi A elaborate distinct systemic metabolite signatures during enteric fever. ELife (2014) 5:3. doi:10.7554/eLife.03100
85. Raffatellu M, Santos RL, Verhoeven DE, George MD, Wilson RP, Winter SE, et al. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med (2008) 14(4):421-8. doi:10.1038/nm1743
86. Gordon MA, Kankwatira AM, Mwafulirwa G, Walsh AL, Hopkins MJ, Parry CM, et al. Invasive non-typhoid Salmonellae establish systemic intracellular infection in HIV-infected adults: an emerging disease pathogenesis. Clin Infect Dis (2010) 50(7):953-62. doi:10.1086/651080
87. 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(14-15):1335-44. doi:10.1016/S1286-4579(01)01495-2
88. Kaiser P, Diard M, Stecher B, Hardt WD. The streptomycin mouse model for Salmonella diarrhea: functional analysis of the microbiota, the pathogen's virulence factors, and the host's mucosal immune response. Immunol Rev (2012) 245(1):56-83. doi:10.1111/j.1600-065X.2011.01070.x
89. Barthel M, Hapfelmeier S, Quintanilla-Martínez L, Kremer M, Rohde M, Hogardt M, et al. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun (2003) 71(5):2839-58. doi:10.1128/IAI.71.5.2839-2858.2003
90. Que JU, Hentges DJ. Effect of streptomycin administration on colonization resistance to Salmonella typhimurium in mice. Infect Immun (1985) 48(1):169-74.
91. Song J, Willinger T, Rongvaux A, Eynon EE, Stevens S, Manz MG, et al. A mouse model for the human pathogen Salmonella Typhi. Cell Host Microbe (2010) 8(4):369-76. doi:10.1016/j.chom.2010.09.003
92. Mathur R, Oh H, Zhang D, Park S-G, Seo J, Koblansky A, et al. A mouse model of Salmonella Typhi infection. Cell (2012) 151(3):590-602. doi:10.1016/j.cell.2012.08.042
93. Libby SJ, Brehm MA, Greiner DL, Shultz LD, McClelland M, Smith KD, et al. Humanized nonobese diabetic-SCID IL2rgammanull mice are susceptible to lethal Salmonella Typhi infection. Proc Natl Acad Sci USA (2010) 107(35):15589-94. doi:10.1073/pnas.1005566107
94. Bender JK, Wille T, Blank K, Lange A, Gerlach RG. LPS structure and PhoQ activity are important for Salmonella Typhimurium virulence in the Galleria mellonella infection model. PLoS One (2013) 8(10):e73287. doi:10.1371/journal.pone.0073287
95. Viegas SC, Mil-Homens D, Fialho AM, Arraiano CM. The virulence of Salmonella enterica serovar Typhimurium in the insect model Galleria mellonella is impaired by mutations in RNase E and RNase III. Appl Environ Microbiol (2013) 79(19):6124-33. doi:10.1128/AEM.02044-13
96. Torraca V, Masud S, Spaink HP, Meijer AH. Macrophage-pathogen interactions in infectious diseases: new therapeutic insights from the zebrafish host model. Dis Model Mech (2014) 7(7):785-97. doi:10.1242/dmm.015594
97. Van der Sar AM, Musters RJP, van Eeden FJM, Appelmelk BJ, Vandenbroucke-Grauls CMJE, Bitter W. Zebrafish embryos as a model host for the real time analysis of Salmonella typhimurium infections. Cell Microbiol (2003) 5(9):601-11. doi:10.1046/j.1462-5822.2003.00303.x
98. WHO. Antimicrobial Resistance: Global Report on Surveillance. Geneva: World Health Organization (2014).