Production of IL-12, IL-23 and IL-27p28 by bone marrow-derived conventional dendritic cells rather than macrophages after LPS/TLR4-dependent induction by Salmonella Enteritidis

Immunobiology

Volumn 212, Issue 9-10, 2008, Pages 739-750

  Siegemund, Sabine ^a   Schütze, Nicole ^a   Freudenberg, Marina A ^b   Lutz, Manfred B ^c   Straubinger, Reinhard K ^a,d   Alber, Gottfried ^a  

^a College of Veterinary Medicine   (Germany)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Antigen presenting cell; Cytokine; Intracellular bacteria; Mouse; Pattern recognition receptor

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; COLONY STIMULATING FACTOR 1; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 23; INTERLEUKIN 27; INTERLEUKIN 27P28; PATTERN RECOGNITION RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; BACTERIAL IMMUNITY; BACTERIAL INFECTION; BONE MARROW; CELL CULTURE; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; FEMALE; IN VITRO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; SALMONELLA ENTERITIDIS; SUPERNATANT; WILD TYPE;

EID: 37049032843     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2007.09.004     Document Type: Article

References (84)

1. Aggarwal S., Ghilardi N., Xie M.H., de Sauvage F.J., and Gurney A.L. Interleukin-23 promotes a distinct CD4T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278 (2003) 1910-1914
2. Alber, G., Al-Robaiy, S., Kleinschek, M., Knauer, J., Krumbholz, P., Richter, J., Schoeneberger, S., Schuetze, N., Schulz, S., Toepfer, K., Voigtlaender, R., Lehmann, J., Mueller, U., 2006. Induction of immunity and inflammation by interleukin-12 family members. Ernst Schering Research Foundation Workshop, pp. 107-127.
3. Albrecht I., Tapmeier T., Zimmermann S., Frey M., Heeg K., and Dalpke A. Toll-like receptors differentially induce nucleosome remodelling at the IL-12p40 promoter. EMBO Rep. 5 (2004) 172-177
4. Altare F., Lammas D., Revy P., Jouanguy E., Doffinger R., Lamhamedi S., Drysdale P., Scheel-Toellner D., Girdlestone J., Darbyshire P., Wadhwa M., Dockrell H., Salmon M., Fischer A., Durandy A., Casanova J.L., and Kumararatne D.S. Inherited interleukin 12 deficiency in a child with bacille Calmette-Guerin and Salmonella Enteritidis disseminated infection. J. Clin. Invest. 102 (1998) 2035-2040
5. Batten M., Li J., Yi S., Kljavin N.M., Danilenko D.M., Lucas S., Lee J., de Sauvage F.J., and Ghilardi N. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 7 (2006) 929-936
6. Bernheiden M., Heinrich J.M., Minigo G., Schutt C., Stelter F., Freeman M., Golenbock D., and Jack R.S. LBP, CD14, TLR4 and the murine innate immune response to a peritoneal Salmonella infection. J. Endotoxin Res. 7 (2001) 447-450
7. Beutler B., Du X., and Poltorak A. Identification of Toll-like receptor 4 (Tlr4) as the sole conduit for LPS signal transduction: genetic and evolutionary studies. J. Endotoxin Res. 7 (2001) 277-280
8. Bihl F., Salez L., Beaubier M., Torres D., Lariviere L., Laroche L., Benedetto A., Martel D., Lapointe J.M., Ryffel B., and Malo D. Overexpression of Toll-like receptor 4 amplifies the host response to lipopolysaccharide and provides a survival advantage in transgenic mice. J. Immunol. 170 (2003) 6141-6150
9. Boonstra A., Asselin-Paturel C., Gilliet M., Crain C., Trinchieri G., Liu Y.J., and O'Garra A. Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential toll-like receptor ligation. J. Exp. Med. 197 (2003) 101-109
10. Bost K.L., and Clements J.D. Intracellular Salmonella dublin induces substantial secretion of the 40-kilodalton subunit of interleukin-12 (IL-12) but minimal secretion of IL-12 as a 70-kilodalton protein in murine macrophages. Infect. Immun. 65 (1997) 3186-3192
11. Brombacher F., Kastelein R.A., and Alber G. Novel IL-12 family members shed light on the orchestration of Th1 responses. Trends Immunol. 24 (2003) 207-212
12. Burgess A.W., Metcalf D., Kozka I.J., Simpson R.J., Vairo G., Hamilton J.A., and Nice E.C. Purification of two forms of colony-stimulating factor from mouse L-cell-conditioned medium. J. Biol. Chem. 260 (1985) 16004-16011
13. Chen Q., Ghilardi N., Wang H., Baker T., Xie M.H., Gurney A., Grewal I.S., and de Sauvage F.J. Development of Th1-type immune responses requires the type I cytokine receptor TCCR. Nature 407 (2000) 916-920
14. Chong C., Bost K.L., and Clements J.D. Differential production of interleukin-12 mRNA by murine macrophages in response to viable or killed Salmonella spp. Infect. Immun. 64 (1996) 1154-1160
15. Clemons-Miller A.R., Cox G.W., Suttles J., and Stout R.D. LPS stimulation of TNF-receptor deficient macrophages: a differential role for TNF-alpha autocrine signaling in the induction of cytokine and nitric oxide production. Immunobiology 202 (2000) 477-492
16. D'Andrea A., Rengaraju M., Valiante N.M., Chehimi J., Kubin M., Aste M., Chan S.H., Kobayashi M., Young D., and Nickbarg E. Production of natural killer cell stimulatory factor (interleukin 12) by peripheral blood mononuclear cells. J. Exp. Med. 176 (1992) 1387-1398
17. D'Andrea A., ste-Amezaga M., Valiante N.M., Ma X., Kubin M., and Trinchieri G. Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J. Exp. Med. 178 (1993) 1041-1048
18. Freudenberg M.A., Keppler D., and Galanos C. Requirement for lipopolysaccharide-responsive macrophages in galactosamine-induced sensitization to endotoxin. Infect. Immun. 51 (1986) 891-895
19. Galanos C., Gumenscheimer M., Muhlradt P., Jirillo E., and Freudenberg M. MALP-2, a Mycoplasma lipopeptide with classical endotoxic properties: end of an era of LPS monopoly?. J. Endotoxin Res. 6 (2000) 471-476
20. Hamano S., Himeno K., Miyazaki Y., Ishii K., Yamanaka A., Takeda A., Zhang M., Hisaeda H., Mak T.W., Yoshimura A., and Yoshida H. WSX-1 is required for resistance to Trypanosoma cruzi infection by regulation of proinflammatory cytokine production. Immunity 19 (2003) 657-667
21. Happel K.I., Dubin P.J., Zheng M., Ghilardi N., Lockhart C., Quinton L.J., Odden A.R., Shellito J.E., Bagby G.J., Nelson S., and Kolls J.K. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202 (2005) 761-769
22. Harrington L.E., Mangan P.R., and Weaver C.T. Expanding the effector CD4 T-cell repertoire: the Th17 lineage. Curr. Opin. Immunol. 18 (2006) 349-356
23. Hochrein H., and Wagner H. Toll-like Receptors. In: Lutz M.B., Romani N., and Steinkasserer A. (Eds). Handbook of Dendritic Cells (2006), Wiley-VCH, Weinheim 119-127
24. Hopkins S.A., Niedergang F., Corthesy-Theulaz I.E., and Kraehenbuhl J.P. A recombinant Salmonella Typhimurium vaccine strain is taken up and survives within murine Peyer's patch dendritic cells. Cell. Microbiol. 2 (2000) 59-68
25. Johansson C., and Wick M.J. Liver dendritic cells present bacterial antigens and produce cytokines upon Salmonella encounter. J. Immunol. 172 (2004) 2496-2503
26. Kawai T., and Akira S. Pathogen recognition with Toll-like receptors. Curr. Opin. Immunol. 17 (2005) 338-344
27. Kawashima T., Murata K., Akira S., Tonozuka Y., Minoshima Y., Feng S., Kumagai H., Tsuruga H., Ikeda Y., Asano S., Nosaka T., and Kitamura T. STAT5 induces macrophage differentiation of M1 leukemia cells through activation of IL-6 production mediated by NF-kappaB p65. J. Immunol. 167 (2001) 3652-3660
28. Khader S.A., Pearl J.E., Sakamoto K., Gilmartin L., Bell G.K., Jelley-Gibbs D.M., Ghilardi N., Desauvage F., and Cooper A.M. IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-gamma responses if IL-12p70 is available. J. Immunol. 175 (2005) 788-795
29. Kincy-Cain T., Clements J.D., and Bost K.L. Endogenous and exogenous interleukin-12 augment the protective immune response in mice orally challenged with Salmonella Dublin. Infect. Immun. 64 (1996) 1437-1440
30. Kirby A.C., Yrlid U., Svensson M., and Wick M.J. Differential involvement of dendritic cell subsets during acute Salmonella infection. J. Immunol. 166 (2001) 6802-6811
31. Lehmann J., Bellmann S., Werner C., Schroder R., Schutze N., and Alber G. IL-12p40-dependent agonistic effects on the development of protective innate and adaptive immunity against Salmonella Enteritidis. J. Immunol. 167 (2001) 5304-5315
32. Lembo A., Kalis C., Kirschning C.J., Mitolo V., Jirillo E., Wagner H., Galanos C., and Freudenberg M.A. Differential contribution of Toll-like receptors 4 and 2 to the cytokine response to Salmonella enterica serovar Typhimurium and Staphylococcus aureus in mice. Infect. Immun. 71 (2003) 6058-6062
33. Li Q., and Cherayil B.J. Role of Toll-like receptor 4 in macrophage activation and tolerance during Salmonella enterica serovar Typhimurium infection. Infect. Immun. 71 (2003) 4873-4882
34. Liu C.H., Fan Y.T., Dias A., Esper L., Corn R.A., Bafica A., Machado F.S., and Aliberti J. Cutting edge: dendritic cells are essential for in vivo IL-12 production and development of resistance against Toxoplasma gondii infection in mice. J. Immunol. 177 (2006) 31-35
35. Lucas S., Ghilardi N., Li J., and de Sauvage F.J. IL-27 regulates IL-12 responsiveness of naive CD4+ T cells through Stat1-dependent and -independent mechanisms. Proc. Natl. Acad. Sci. USA 100 (2003) 15047-15052
36. Lutz M.B. IL-3 in dendritic cell development and function: a comparison with GM-CSF and IL-4. Immunobiology 209 (2004) 79-87
37. Lutz M.B., Kukutsch N., Ogilvie A.L., Rossner S., Koch F., Romani N., and Schuler G. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223 (1999) 77-92
38. Maclennan C., Fieschi C., Lammas D.A., Picard C., Dorman S.E., Sanal O., Maclennan J.M., Holland S.M., Ottenhoff T.H., Casanova J.L., and Kumararatne D.S. Interleukin (IL)-12 and IL-23 are key cytokines for immunity against Salmonella in humans. J. Infect. Dis. 190 (2004) 1755-1757
39. MacVittie T.J., O'Brien A.D., Walker R.I., and Weinberg S.R. Inflammatory response of LPS-hyporesponsive and LPS-responsive mice to challenge with Gram-negative bacteria Salmonella Typhimurium and Klebsiella pneumoniae. Adv. Exp. Med. Biol. 155 (1982) 325-334
40. Magram J., Connaughton S.E., Warrier R.R., Carvajal D.M., Wu C.Y., Ferrante J., Stewart C., Sarmiento U., Faherty D.A., and Gately M.K. IL-12-deficient mice are defective in IFN gamma production and type 1 cytokine responses. Immunity 4 (1996) 471-481
41. Mangan P.R., Harrington L.E., O'Quinn D.B., Helms W.S., Bullard D.C., Elson C.O., Hatton R.D., Wahl S.M., Schoeb T.R., and Weaver C.T. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441 (2006) 231-234
42. Marriott I., Hammond T., Thomas E., and Bost K. Salmonella efficiently enter and survive within cultured CD11c+ dendritic cells initiating cytokine expression. Eur. J. Immunol. 29 (1999) 1107-1115
43. Martin G., Hanel I., Helmuth R., Schroeter A., Erler W., and Meyer H. Immunization with potential Salmonella Enteritidis mutants-1. Production and in vitro characterization. Berl. Muench. Tieraerztl. Wochenschr. 109 (1996) 325-329
44. Mastroeni P., Harrison J.A., Chabalgoity J.A., and Hormaeche C.E. Effect of interleukin 12 neutralization on host resistance and gamma interferon production in mouse typhoid. Infect. Immun. 64 (1996) 189-196
45. Mattner F., Magram J., Ferrante J., Launois P., Di P.K., Behin R., Gately M.K., Louis J.A., and Alber G. Genetically resistant mice lacking interleukin-12 are susceptible to infection with Leishmania major and mount a polarized Th2 cell response. Eur. J. Immunol. 26 (1996) 1553-1559
46. Morelli A.E., Zahorchak A.F., Larregina A.T., Colvin B.L., Logar A.J., Takayama T., Falo L.D., and Thomson A.W. Cytokine production by mouse myeloid dendritic cells in relation to differentiation and terminal maturation induced by lipopolysaccharide or CD40 ligation. Blood 98 (2001) 1512-1523
47. Norimatsu M., Harris J., Chance V., Dougan G., Howard C.J., and Villarreal-Ramos B. Differential response of bovine monocyte-derived macrophages and dendritic cells to infection with Salmonella Typhimurium in a low-dose model in vitro. Immunology 108 (2003) 55-61
48. Oppmann B., Lesley R., Blom B., Timans J.C., Xu Y., Hunte B., Vega F., Yu N., Wang J., Singh K., Zonin F., Vaisberg E., Churakova T., Liu M., Gorman D., Wagner J., Zurawski S., Liu Y., Abrams J.S., Moore K.W., Rennick D., de Waal-Malefyt R., Hannum C., Bazan J.F., and Kastelein R.A. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13 (2000) 715-725
49. Park S.J., Nakagawa T., Kitamura H., Atsumi T., Kamon H., Sawa S., Kamimura D., Ueda N., Iwakura Y., Ishihara K., Murakami M., and Hirano T. IL-6 regulates in vivo dendritic cell differentiation through STAT3 activation. J. Immunol. 173 (2004) 3844-3854
50. Pflanz S., Timans J.C., Cheung J., Rosales R., Kanzler H., Gilbert J., Hibbert L., Churakova T., Travis M., Vaisberg E., Blumenschein W.M., Mattson J.D., Wagner J.L., To W., Zurawski S., McClanahan T.K., Gorman D.M., Bazan J.F., de Waal M.R., Rennick D., and Kastelein R.A. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 16 (2002) 779-790
51. Pietila T.E., Veckman V., Kyllonen P., Lahteenmaki K., Korhonen T.K., and Julkunen I. Activation, cytokine production, and intracellular survival of bacteria in Salmonella-infected human monocyte-derived macrophages and dendritic cells. J. Leukoc. Biol. 78 (2005) 909-920
52. Poltorak A., He X., Smirnova I., Liu M.Y., Van H.C., Du X., Birdwell D., Alejos E., Silva M., Galanos C., Freudenberg M., Ricciardi-Castagnoli P., Layton B., and Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282 (1998) 2085-2088
53. Rescigno M., Urbano M., Valzasina B., Francolini M., Rotta G., Bonasio R., Granucci F., Kraehenbuhl J.P., and Ricciardi-Castagnoli P. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2 (2001) 361-367
54. Rescigno M., Urbano M., Rimoldi M., Valzasina B., Rotta G., Granucci F., and Ricciardi-Castagnoli P. Toll-like receptor 4 is not required for the full maturation of dendritic cells or for the degradation of Gram-negative bacteria. Eur. J. Immunol. 32 (2002) 2800-2806
55. Royle M.C., Totemeyer S., Alldridge L.C., Maskell D.J., and Bryant C.E. Stimulation of Toll-like receptor 4 by lipopolysaccharide during cellular invasion by live Salmonella Typhimurium is a critical but not exclusive event leading to macrophage responses. J. Immunol. 170 (2003) 5445-5454
56. Salazar-Gonzalez R.M., and McSorley S.J. Salmonella flagellin, a microbial target of the innate and adaptive immune system. Immunol. Lett. 101 (2005) 117-122
57. Salcedo S.P., Noursadeghi M., Cohen J., and Holden D.W. Intracellular replication of Salmonella Typhimurium strains in specific subsets of splenic macrophages in vivo. Cell Microbiol. 3 (2001) 587-597
58. Schnurr M., Toy T., Shin A., Wagner M., Cebon J., and Maraskovsky E. Extracellular nucleotide signalling via P2 receptors inhibits IL-12 and enhances IL-23 expression in human dendritic cells: a novel role for the cAMP pathway. Blood 105 (2004) 1582-1589
59. Schuetze N., Schoeneberger S., Mueller U., Freudenberg M.A., Alber G., and Straubinger R.K. IL-12 family members: differential kinetics of their TLR4-mediated induction by Salmonella Enteritidis and the impact of IL-10 in bone marrow-derived macrophages. Int. Immunol. 17 (2005) 649-659
60. Schwandner R., Dziarski R., Wesche H., Rothe M., and Kirschning C.J. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2. J. Biol. Chem. 274 (1999) 17406-17409
61. Shortman K., and Liu Y.J. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2 (2002) 151-161
62. Silva J.S., Vespa G.N., Cardoso M.A., Aliberti J.C., and Cunha F.Q. Tumor necrosis factor alpha mediates resistance to Trypanosoma cruzi infection in mice by inducing nitric oxide production in infected gamma interferon-activated macrophages. Infect. Immun. 63 (1995) 4862-4867
63. Sing A., Merlin T., Knopf H.P., Nielsen P.J., Loppnow H., Galanos C., and Freudenberg M.A. Bacterial induction of beta interferon in mice is a function of the lipopolysaccharide component. Infect. Immun. 68 (2000) 1600-1607
64. Smits H.H., Van Beelen A.J., Hessle C., Westland R., De Jong E., Soeteman E., Wold A., Wierenga E.A., and Kapsenberg M.L. Commensal Gram-negative bacteria prime human dendritic cells for enhanced IL-23 and IL-27 expression and enhanced Th1 development. Eur. J. Immunol. 34 (2004) 1371-1380
65. Springer S., Lehmann J., Lindner T., Thielebein J., Alber G., and Selbitz H.J. A new live Salmonella Enteritidis vaccine for chickens-experimental evidence of its safety and efficacy. Berl. Muench. Tieraerztl. Wochenschr. 113 (2000) 246-252
66. Stumhofer J.S., Laurence A., Wilson E.H., Huang E., Tato C.M., Johnson L.M., Villarino A.V., Huang Q., Yoshimura A., Sehy D., Saris C.J., O'Shea J.J., Hennighausen L., Ernst M., and Hunter C.A. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 7 (2006) 937-945
67. Sundquist M., and Wick M.J. TNF-alpha-dependent and -independent maturation of dendritic cells and recruited CD11c(int)CD11b+ Cells during oral Salmonella infection. J. Immunol. 175 (2005) 3287-3298
68. Svensson M., Johansson C., and Wick M.J. Salmonella enterica serovar Typhimurium-induced maturation of bone marrow-derived dendritic cells. Infect. Immun. 68 (2000) 6311-6320
69. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3 (2003) 133-146
70. Trinchieri G., Pflanz S., and Kastelein R.A. The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 19 (2003) 641-644
71. Vanden E.S., Goriely S., De W.D., Goldman M., and Willems F. Preferential production of the IL-12(p40)/IL-23(p19) heterodimer by dendritic cells from human newborns. Eur. J. Immunol. 36 (2006) 21-26
72. Vazquez-Torres A., Vallance B.A., Bergman M.A., Finlay B.B., Cookson B.T., Jones-Carson J., and Fang F.C. Toll-like receptor 4 dependence of innate and adaptive immunity to Salmonella: importance of the Kupffer cell network. J. Immunol. 172 (2004) 6202-6208
73. Veldhoen M., Hocking R.J., Atkins C.J., Locksley R.M., and Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24 (2006) 179-189
74. Villarino A., Hibbert L., Lieberman L., Wilson E., Mak T., Yoshida H., Kastelein R.A., Saris C., and Hunter C.A. The IL-27R (WSX-1) is required to suppress T cell hyperactivity during infection. Immunity 19 (2003) 645-655
75. von Jeney N., Gunther E., and Jann K. Mitogenic stimulation of murine spleen cells: relation to susceptibility to Salmonella infection. Infect. Immun. 15 (1977) 26-33
76. Wijburg O.L., Simmons C.P., van Rooijen N., and Strugnell R.A. Dual role for macrophages in vivo in pathogenesis and control of murine Salmonella enterica var. Typhimurium infections. Eur. J. Immunol. 30 (2000) 944-953
77. Wirtz S., Becker C., Fantini M.C., Nieuwenhuis E.E., Tubbe I., Galle P.R., Schild H.J., Birkenbach M., Blumberg R.S., and Neurath M.F. EBV-induced gene 3 transcription is induced by TLR signaling in primary dendritic cells via NF-kappa B activation. J. Immunol. 174 (2005) 2814-2824
78. Wirtz S., Tubbe I., Galle P.R., Schild H.J., Birkenbach M., Blumberg R.S., and Neurath M.F. Protection from lethal septic peritonitis by neutralizing the biological function of interleukin 27. J. Exp. Med. 203 (2006) 1875-1881
79. Yamanaka A., Hamano S., Miyazaki Y., Ishii K., Takeda A., Mak T.W., Himeno K., Yoshimura A., and Yoshida H. Hyperproduction of proinflammatory cytokines by WSX-1-deficient NKT cells in concanavalin A-induced hepatitis. J. Immunol. 172 (2004) 3590-3596
80. Yoshida H., Hamano S., Senaldi G., Covey T., Faggioni R., Mu S., Xia M., Wakeham A.C., Nishina H., Potter J., Saris C.J., and Mak T.W. WSX-1 is required for the initiation of Th1 responses and resistance to L. major infection. Immunity 15 (2001) 569-578
81. Yrlid U., Svensson M., Johansson C., and Wick M.J. Salmonella infection of bone marrow-derived macrophages and dendritic cells: influence on antigen presentation and initiating an immune response. FEMS Immunol. Med. Microbiol. 27 (2000) 313-320
82. Yu R.Y., Wang X., Pixley F.J., Yu J.J., Dent A.L., Broxmeyer H.E., Stanley E.R., and Ye B.H. BCL-6 negatively regulates macrophage proliferation by suppressing autocrine IL-6 production. Blood 105 (2005) 1777-1784
83. Zal T., Volkmann A., and Stockinger B. Mechanisms of tolerance induction in major histocompatibility complex class II-restricted T cells specific for a blood-borne self-antigen. J. Exp. Med. 180 (1994) 2089-2099
84. Zhao C., Wood M.W., Galyov E.E., Hopken U.E., Lipp M., Bodmer H.C., Tough D.F., and Carter R.W. Salmonella Typhimurium infection triggers dendritic cells and macrophages to adopt distinct migration patterns in vivo. Eur. J. Immunol. 36 (2006) 2939-2950