Molecular interactions between dendritic cells and Salmonella: Escape from adaptive immunity and implications on pathogenesis

Critical Reviews in Immunology

Volumn 25, Issue 5, 2005, Pages 389-403

  Bueno, Susan M ^a   Tobar, Jaime A ^a   Iruretagoyena, Mirentxu I ^a   Kalergis, Alexis M ^a,b,c,d  

^a Facultad de Ciencias Biologicas   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

Adaptive immunity; Dendritic cells; Salmonella enterica serovar Typhimurium; Salmonella pathogenicity island; T cell activation; Type Three Secretion System; Virulence factor

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL PROTEIN; GENE PRODUCT;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; BACTERIAL GENE; BACTERIAL SURVIVAL; BACTERIOLYSIS; DENDRITIC CELL; HUMAN; IMMUNITY; INNATE IMMUNITY; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PATHOGENESIS; PATHOGENICITY ISLAND; PRIORITY JOURNAL; REVIEW; SALMONELLA; SALMONELLA ENTERICA; SPI 2 GENE; T LYMPHOCYTE; TYPHOID FEVER;

ANIMALS; ANTIGEN PRESENTATION; DENDRITIC CELLS; IMMUNITY, NATURAL; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; VIRULENCE FACTORS;

EID: 29144476532     PISSN: 10408401     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevImmunol.v25.i5.40     Document Type: Review

References (109)

1. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392(6673):245-52.
2. Reis e Sousa C. Dendritic cells as sensors of infection. Immunity. 2001;14(5):495-8.
3. Lanzavecchia A, Sallusto F. Regulation of T cell immunity by dendritic cells. Cell. 2001;106(3):263-6.
4. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, Pulendran B, Palucka K. Immunobiology of dendritic cells. Annu Rev Immunol. 2000;18:767-811.
5. Kalergis AM. Modulation of T cell immunity by TCR/pMHC dwell time and activating/inhibitory receptor pairs on the antigen-presenting cell. Curr Pharm Des. 2003;9(3):233-44.
6. Michelsen KS, Aicher A, Mohaupt M, Hartung T, Dimmeler S, Kirschning CJ, Schumann RR. The role of toll-like receptors (TLRs) in bacteria-induced maturation of murine dendritic cells (DCS). Peptidoglycan and lipoteichoic acid are inducers of DC maturation and require TLR2. J Biol Chem. 2001;276(28):25680-6.
7. Inaba K, Inaba M, Deguchi M, Hagi K, Yasumizu R, Ikehara S, Muramatsu S, Steinman RM. Granulocytes, macrophages, and dendritic cells arise from a common major histocompatibility complex class II-negative progenitor in mouse bone marrow. Proc Natl Acad Sci U S A. 1993;90(7):3038-42.
8. Inaba K, Turley S, Yamaide F, Iyoda T, Mahnke K, Inaba M, Pack M, Subklewe M, Sauter B, Sheff D, Albert M, Bhardwaj N, Mellman I, Steinman RM. Efficient presentation of phagocytosed cellular fragments on the major histocompatibility complex class II products of dendritic cells. J Exp Med. 1998;188(11):2163-73.
9. Turley SJ, Inaba K, Garrett WS, Ebersold M, Unternaehrer J, Steinman RM, Mellman I. Transport of peptide-MHC class II complexes in developing dendritic cells. Science. 2000;288(5465):522-7.
10. Huang Q, Liu D, Majewski P, Schulte LC, Korn JM, Young RA, Lander ES, Hacohen N. The plasticity of dendritic cell responses to pathogens and their components. Science. 2001;294(5543):870-5.
11. Jung S, Unutmaz D, Wong P, Sano G, De los Santos K, Sparwasser T, Wu S, Vuthoori S, Ko K, Zavala F, Pamer EG, Littman DR, Lang RA. In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity. 2002;17(2):211-20.
12. Zammit DJ, Cauley LS, Pham QM, Lefrancois L. Dendritic cells maximize the memory CD8 T cell response to infection. Immunity. 2005;22(5):561-70.
13. Dustin ML, Cooper JA. The immunological synapse and the actin cytoskeleton: molecular hardware for T cell signaling. Nat Immunol. 2000;1(1):23-9.
14. Kamath AT, Sheasby CE, Tough DF. Dendritic cells and NK cells stimulate bystander T cell activation in response to TLR agonists through secretion of IFN-alpha beta and IFN-gamma. J Immunol. 2005;174(2):767-76.
15. Resdgno M. Dendritic cells and the complexity of microbial infection. Trends Microbiol. 2002;10(9):425-61.
16. Tobar JA, Gonzalez PA, Kalergis AM. Salmonella escape from antigen presentation can be overcome by targeting bacteria to Fc gamma receptors on dendritic cells. J Immunol. 2004;173(6):4058-65.
17. Pang T, Levine MM, Ivanoff B, Wain J, Finlay BB. Typhoid fever-important issues still remain. Trends Microbiol. 1998;6(4):131-3.
18. House D, Bishop A, Parry C, Dougan G, Wain J. Typhoid fever: pathogenesis and disease. Curr Opin Infect Dis. 2001;14(5):573-8.
19. Marcus SL, Brumell JH, Pfeifer CG, Finlay BB. Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect. 2000;2(2):145-56.
20. Hensel M, Shea JE, Waterman SR, Mundy R, Nikolaus T, Banks G, Vazquez-Torres A, Gleeson C, Fang FC, Holden DW. 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.
21. Hansen-Wester I, Hensel M. Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect. 2001;3(7):549-59.
22. Jones B, 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.
23. Conlan JW, North RJ. Early pathogenesis of infection in the liver with the facultative intracellular bacteria Listeria monocytogenes, Francisella tularensis, and Salmonella typhimurium involves lysis of infected hepatocytes by leukocytes. Infect Immun. 1992;60(12):5164-71.
24. Salcedo SP, Noursadeghi M, Cohen J, Holden DW. Intracellular replication of Salmonella typhimurium strains in specific subsets of splenic macrophages in vivo. Cell Microbiol. 2001;3(9):587-97.
25. Richter-Dahlfors A, Buchan AM, 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.
26. Cossart P, Sansonetti PJ. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science. 2004;304(5668):242-8.
27. Hentschel U, Hacker J. Pathogenicity islands: the tip of the iceberg. Microbes Infect. 2001;3(7):545-8.
28. Hacker J, Kaper JB. Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol. 2000;54:641-79.
29. Cotter PA, DiRita VJ. Bacterial virulence gene regulation: an evolutionary perspective. Annu Rev Microbiol. 2000;54:519-65.
30. 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(7):1872-82.
31. Zhou D, Galan J. Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect. 2001;3(14-15):1293-8.
32. Hensel M. Salmonella pathogenicity island 2. Mol Microbiol. 2000;36(5):1015-23.
33. Waterman SR, Holden DW. Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol. 2003;5(8):501-11.
34. Shotland Y, Kramer H, Groisman EA. The Salmonella SpiC protein targets the mammalian Hook3 protein function to alter cellular trafficking. Mol Microbiol. 2003;49(6):1565-76.
35. Ochman H, Soncini FC, Solomon F, Groisman EA. Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci U S A. 1996;93(15):7800-4.
36. Shea JE, Beuzon CR, Gleeson C, Mundy R, Holden DW. Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infect Immun. 1999;67(1):213-9.
37. Gulig PA, Danbara H, Guiney DG, Lax AJ, Norel F, Rhen M. Molecular analysis of spv virulence genes of the Salmonella virulence plasmids. Mol Microbiol. 1993;7(6):825-30.
38. Libby SJ, Adams LG, Ficht TA, Allen C, Whitford HA, Buchmeier NA, Bossie S, Guiney DG. The spv genes on the Salmonella dublin virulence plasmid are required for severe enteritis and systemic infection in the natural host. Infect Immun. 1997;65(5):1786-92.
39. Blanc-Potard AB, Groisman EA. The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J. 1997;16(17):5376-85.
40. Ho TD, Figueroa-Bossi N, Wang M, Uzzau S, Bossi L, Slauch JM. Identification of GtgE, a novel virulence factor encoded on the Gifsy-2 bacteriophage of Salmonella enterica serovar Typhimurium. J Bacteriol. 2002;184(19):5234-9.
41. Uzzau S, Bossi L, Figueroa-Bossi N. Differential accumulation of Salmonella [Cu, Zn] superoxide dismutases SodCI and SodCII in intracellular bacteria: correlation with their relative contribution to pathogenicity. Mol Microbiol. 2002;46(1):147-56.
42. Figueroa-Bossi N, Bossi L. Inducible prophages contribute to Salmonella virulence in mice. Mol Microbiol. 1999;33(1):167-76.
43. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, Porwollik S, Ali J, Dante M, Du F, Hou S, Layman D, Leonard S, Nguyen C, Scott K, Holmes A, Grewal N, Mulvaney E, Ryan E, Sun H, Florea L, Miller W, Stoneking T, Nhan M, Waterston R, Wilson RK. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 2001;413(6858):852-6.
44. Mirold S, Ehrbar K, Weissmuller A, Prager R, Tschape H, Russmann H, Hardt WD. Salmonella host cell invasion emerged by acquisition of a mosaic of separate genetic elements, including Salmonella pathogenicity island 1 (SPI1), SPI5, and sopE2. J Bacteriol. 2001;183(7):2348-58.
45. Hapfelmeier S, Ehrbar K, Stecher B, Barthel M, Kremer M, Hardt WD. Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun. 2004;72(2):795-809.
46. Hardt WD, Urlaub H, Galan JE. A substrate of the centisome 63 type III protein secretion system of Salmonella typhimurium is encoded by a cryptic bacteriophage. Proc Natl Acad Sci USA. 1998;95(5):2574-9.
47. Porwollik S, McClelland M. Lateral gene transfer in Salmonella. Microbes Infect. 2003;5(11):977-89.
48. McClelland M, Wilson RK. Comparison of sample sequences of the Salmonella typhi genome to the sequence of the complete Escherichia coli K-12 genome. Infect Immun. 1998;66(9):4305-12.
49. Hansen-Wester I, Stecher B, Hensel M. Type III secretion of Salmonella enterica serovar Typhimurium translocated effectors and SseFG. Infect Immun. 2002;70(3):1403-9.
50. Kuhle V, Hensel M. SseF and SseG are translocated effectors of the type III secretion system of Salmonella pathogenicity island 2 that modulate aggregation of endosomal compartments. Cell Microbiol. 2002;4(12):813-24.
51. Nikolaus T, Deiwick J, Rappl C, Freeman JA, Schroder W, Miller SI, Hensel M. SseBCD proteins are secreted by the type III secretion system of Salmonella pathogenicity island 2 and function as a translocon. J Bacteriol. 2001;183(20):6036-45.
52. Jantsch J, Cheminay C, Chakravortty D, Lindig T, Hein J, Hensel M. Intracellular activities of Salmonella enterica in murine dendritic cells. Cell Microbiol. 2003;5(12):933-45.
53. Svensson M, Johansson C, Wick MJ. Salmonella enterica serovar Typhimurium-induced maturation of bone marrow-derived dendritic cells. Infect Immun. 2000;68(11):6311-20.
54. Yrlid U, Svensson M, Hakansson 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.
55. Niedergang F, Sirard JC, Blanc CT, Kraehenbuhl JP. Entry and survival of Salmonella typhimurium in dendritic cells and presentation of recombinant antigens do not require macrophage-specific virulence factors. Proc Natl Acad Sci U S A. 2000;97(26):14650-5.
56. Petrovska L, Aspinall RJ, Barber L, Clare S, Simmons CP, Stratford R, Khan SA, Lemoine NR, Frankel G, Holden DW, Dougan G. Salmonella enterica serovar Typhimurium interaction with dendritic cells: impact of the sifA gene. Cell Microbiol. 2004;6(11):1071-84.
57. Marriott I, Hammond TG, Thomas EK, Bost KL. Salmonella efficiently enter and survive within cultured CD11c+ dendritic cells initiating cytokine expression. Eur J Immunol. 1999;29(4):1107-15.
58. Fu G, Wijburg OL, Cameron PU, Price JD, Strugnell RA. Salmonella enterica serovar Typhimurium infection of dendritic cells leads to functionally increased expression of the macrophage-derived chemokine. Infect Immun. 2005;73(3):1714-22.
59. Hopkins SA, Niedergang F, Corthesy-Theulaz IE, Kraehenbuhl JP. A recombinant Salmonella typhimurium vaccine strain is taken up and survives within murine Peyer's patch dendritic cells. Cell Microbiol. 2000;2(1):59-68.
60. Shreedhar VK, Kelsall BL, Neutra MR. Cholera toxin induces migration of dendritic cells from the subepithelial dome region to T- and B-cell areas of Peyer's patches. Infect Immun. 2003;71(1):504-9.
61. Sierro F, Dubois B, Coste A, Kaiserlian D, Kraehenbuhl JP, Sirard JC. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc Natl Acad Sci U S A. 2001;98(24):13722-7.
62. Sozzani S, Allavena P, Vecchi A, Mantovani A. The role of chemokines in the regulation of dendritic cell trafficking. J Leukoc Biol. 1999;66(1):1-9.
63. Sozzani S, Allavena P, D'Amico G, Luini W, Bianchi G, Kataura M, Imai T, Yoshie O, Bonecchi R, Mantovani A. Differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties. J Immunol. 1998;161(3):1083-6.
64. Sallusto F, Schaerli P, Loetscher P, Schaniel C, Lenig D, Mackay CR, Qin S, Lanzavecchia A. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur J Immunol. 1998;28(9):2760-9.
65. Alaniz RC, Sandall S, Thomas EK, Wilson CB. Increased dendritic cell numbers impair protective immunity to intracellular bacteria despite augmenting antigen-specific CD8+ T lymphocyte responses. J Immunol. 2004;172(6):3725-35.
66. Cheminay C, Schoen M, Hensel M, Wandersee-Steinhauser A, Ritter U, Korner H, Rollinghoff M, Hein J. Migration of Salmonella typhimurium-harboring bone marrow-derived dendritic cells toward the chemokines CCL19 and CCL21. Microb Pathog. 2002;32(5):207-18.
67. Means TK, Hayashi F, Smith KD, Aderem A, Luster AD. The Toll-like receptor 5 stimulus bacterial flagellin induces maturation and chemokine production in human dendritic cells. J Immunol. 2003;170(10):5165-75.
68. Niedergang F, Didierlaurent A, Kraehenbuhl JP, Sirard JC. Dendritic cells: the host Achille's heel for mucosal pathogens? Trends Microbiol. 2004;12(2):79-88.
69. Kaisho T, Akira S. Pleiotropic function of Toll-like receptors. Microbes Infect. 2004;6(15):1388-94.
70. Robbins JD, Robbins JB. Reexamination of the protective role of the capsular polysaccharide (Vi antigen) of Salmonella typhi. J Infect Dis. 1984;150(3):436-49.
71. Jarva H, Janulczyk R, Hellwage J, Zipfel PF, Bjorck L, Meri S. Streptococcus pneumoniae evades complement attack and opsonophagocytosis by expressing the pspC locus-encoded Hie protein that binds to short consensus repeats 8-11 of factor H. J Immunol. 2002;168(4):1886-94.
72. Holden DW. Trafficking of the Salmonella vacuole in macrophages. Traffic. 2002;3(3):161-9.
73. Garcia-Del Portillo F, Jungnitz H, Rohde M, Guzman CA. Interaction of Salmonella enterica serotype Typhimurium with dendritic cells is defined by targeting to compartments lacking lysosomal membrane glycoproteins. Infect Immun. 2000;68(5):2985-91.
74. Hess J, Dietrich G, Gentschev I, Miko D, Goebel W, Kaufmann SH. Protection against murine listeriosis by an attenuated recombinant Salmonella typhimurium vaccine strain that secretes the naturally somatic antigen superoxide dismutase. Infect Immun. 1997;65(4):1286-92.
75. Johansson C, Wick MJ. Liver dendritic cells present bacterial antigens and produce cytokines upon Salmonella encounter. J Immunol. 2004;172(4):2496- 503.
76. Yrlid U, Wick MJ. Antigen presentation capacity and cytokine production by murine splenic dendritic cell subsets upon Salmonella encounter. J Immunol. 2002;169(1):108-16.
77. Cheminay C, Mohlenbrink A, Hensel M. Intracellular Salmonella inhibit antigen presentation by dendritic cells. J Immunol. 2005;174(5):2892-9.
78. Srinivasan A, Foley J, Ravindran R, McSorley SJ. Low-dose Salmonella infection evades activation of flagellin-specific CD4 T cells. J Immunol. 2004;173(6):4091-9.
79. McSorley SJ, Asch S, Costalonga M, Reinhardt RL, Jenkins MK. Tracking Salmonella-specific CD4 T cells in vivo reveals a local mucosal response to a disseminated infection. Immunity. 2002;16(3):365-77.
80. Clarke SR, Barnden M, Kurts C, Carbone FR, Miller JF, Heath WR. Characterization of the ovalbumin-specific TCR transgenic line OT-I: MHC elements for positive and negative selection. Immunol Cell Biol. 2000;78(2):110-7.
81. Robertson JM, Jensen PE, Evavold BD. DO11.10 and OT-II T cells recognize a C-terminal ovalbumin 323-339 epitope. J Immunol. 2000;164(9):4706-12.
82. Svensson M, Wick MJ. Classical MHC class I peptide presentation of a bacterial fusion protein by bone marrow-derived dendritic cells. Eur J Immunol. 1999;29(1):180-8.
83. Fields PI, Groisman EA, Heffron F. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 1989;243(4894 Pt 1):1059-62.
84. Gunn JS, Hohmann EL, Miller SI. Transcriptional regulation of Salmonella virulence: a PhoQ, periplasmic domain mutation results in increased net phosphotransfer to PhoP. J Bacteriol. 1996;178 (21):6369-73.
85. Uchiya K, Barbieri MA, Funato K, Shah AH, Stahl PD, Groisman EA. A Salmonella virulence protein that inhibits cellular trafficking. EMBO J. 1999;18(14):3924-33.
86. Yu XJ, Ruiz-Albert J, Unsworth KE, Garvis S, Liu M, Holden DW. SpiC is required for secretion of Salmonella Pathogenicity Island 2 type III secretion system proteins. Cell Microbiol. 2002;4(8):531-40.
87. Freeman JA, Rappl C, Kuhle V, Hensel M, Miller SI. SpiC is required for translocation of Salmonella pathogenicity island 2 effectors and secretion of translocon proteins SseB and SseC. J Bacteriol. 2002;184(18):4971-80.
88. Kubori T, Galan JE. Temporal regulation of Salmonella virulence effector function by proteasome-dependent protein degradation. Cell. 2003;115(3):333-42.
89. Qimron U, Madar N, Mittrucker HW, Zilka A, Yosef I, Bloushtain N, Kaufmann SH, Rosenshine I, Apte RN, Porgador A. Identification of Salmonella typhimurium genes responsible for interference with peptide presentation on MHC class I molecules: Deltayej Salmonella mutants induce superior CD8+ T-cell responses. Cell Microbiol. 2004;6(11):1057-70.
90. Trulzsch K, Geginat G, Sporleder T, Ruckdeschel K, Hoffmann R, Heesemann J, Russmann H. Yersinia outer protein P inhibits CD8 T cell priming in the mouse infection model. J Immunol. 2005;174(7):4244-51.
91. Erfurth SE, Grobner S, Kramer U, Gunst DS, Soldanova I, Schaller M, Autenrieth IB, Borgmann S. Yersinia enterocolitica induces apoptosis and inhibits surface molecule expression and cytokine production in murine dendritic cells. Infect Immun. 2004;72(12):7045-54.
92. Monack DM, Raupach B, Hromockyj AE, Falkow S. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci U S A. 1996;93(18):9833-8.
93. Knodler LA, Finlay BB. Salmonella and apoptosis: to live or let die? Microbes Infect. 2001;3(14-15):1321-6.
94. Hueffer K, Galan JE. Salmonella-induced macrophage death: multiple mechanisms, different outcomes. Cell Microbiol. 2004;6(11):1019-25.
95. Brennan MA, Cookson BT. Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol. 2000;38(1):31-40.
96. Monack DM, Detweiler CS, Falkow S. Salmonella pathogenicity island 2-dependent macrophage death is mediated in part by the host cysteine protease caspase-1. Cell Microbiol. 2001;3(12):825-37.
97. van der Velden J, de Jong JW, Owen VJ, Burton PB, Stienen GJ. Effect of protein kinase A on calcium sensitivity of force and its sarcomere length dependence in human cardiomyocytes. Cardiovasc Res. 2000;46(3):487-95.
98. van der Velden AWM, Velasquez M, Starnbach MN. Salmonella rapidly kill dendritic cells via a caspase-1-dependent mechanism. J Immunol. 2003;171(12):6742-9.
99. Lundberg U, Vinatzer U, Berdnik D, von Gabain A, Baccarini M. Growth phase-regulated induction of Salmonella-induced macrophage apoptosis correlates with transient expression of SPI-1 genes. J Bacteriol. 1999;181(11):3433-7.
100. 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(11):771-81.
101. 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.
102. Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun. 2005;73(4):1907-16.
103. Fantuzzi G, Dinarello CA. Interleukin-18 and interleukin-1 beta: two cytokine substrates for ICE (caspase-1). J Clin Immunol. 1999;19(1):1-11.
104. Monack DM, Hersh D, Ghori N, Bouley D, Zychlinsky A, Falkow S. Salmonella exploits caspase-1 to colonize Peyer's patches in a murine typhoid model. J Exp Med. 2000;192(2):249-58.
105. van der Velden AW, Velasquez M, Starnbach MN. Salmonella rapidly kill dendritic cells via a caspase-1-dependent mechanism. J Immunol. 2003;171(12):6742-9.
106. Yrlid U, Svensson M, Johansson C, Wick MJ. Salmonella infection of bone marrow-derived macrophages and dendritic cells: influence on antigen presentation and initiating an immune response. FEMS Immunol Med Microbiol. 2000;27(4):313-20.
107. Vindurampulle CJ, Attridge SR. Impact of vector priming on the immunogenicity of recombinant Salmonella vaccines. Infect Immun. 2003;71(1):287-97.
108. Chen H, Schifferli DM. Construction, characterization, and immunogenicity of an attenuated Salmonella enterica serovar typhimurium pgtE vaccine expressing fimbriae with integrated viral epitopes from the spiC promoter. Infect Immun. 2003;71(8):4664-73.
109. Baud D, Ponci F, Bobst M, De Grandi P, Nardelli-Haefliger D. Improved efficiency of a Salmonella-based vaccine against human papillomavirus type 16 virus-like particles achieved by using a codon-optimized version of L1. J Virol. 2004;78(23):12901-9.