Skip to main content Accessibility help
×
Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-29T17:22:38.602Z Has data issue: false hasContentIssue false

10 - Interactions between Salmonella and dendritic cells: what happens along the way?

Published online by Cambridge University Press:  04 December 2009

Duncan Maskell
Affiliation:
University of Cambridge
Cecilia Johansson
Affiliation:
Department of Clinical Immunology, University of Goteborg, Guldhedsgatan 10A, Goteborg SE-413 46, Sweden
Malin Sundquist
Affiliation:
Department of Clinical Immunology, University of Goteborg, Guldhedsgatan 10A, Goteborg SE-413 46, Sweden
Mary Jo Wick
Affiliation:
Department of Clinical Immunology, University of Goteborg, Guldhedsgatan 10A, Goteborg SE-413 46, Sweden
Pietro Mastroeni
Affiliation:
University of Cambridge
Get access

Summary

INTRODUCTION

Dendritic cells (DC) are efficient antigen-presenting cells and are likely to be involved in the initiation of T-cell responses to Salmonella. However, it is not known what type of DC initiate immune responses to Salmonella or where this initiation takes place. Studies on interactions between Salmonella and DC are emerging and are shedding light on this topic. This chapter will review how Salmonella interacts with DC, following the course the bacteria take after oral infection. One of the earliest sites of Salmonella replication is within the Peyer's patches of the gut. Thereafter, Salmonella can be found in the gut-draining mesenteric lymph nodes. After systemic release of bacteria or bacteria-containing cells, Salmonella spread to the spleen and liver and replicate further. The relevance of the interactions between Salmonella and DC in these organs for initiating antibacterial T-cell responses is discussed. This is preceded by a brief overview of the biology of DC.

DENDRITIC CELLS

DC originate from precursors in the bone marrow and were named because of their morphology having long, branched dendrites (Steinman and Cohn, 1973; Steinman et al., 1974). DC are widely distributed in lymphoid as well as non-lymphoid tissues (Steptoe et al., 2000; Vremec and Shortman, 1997; Steiniger et al., 1984).

Type
Chapter
Information
Salmonella Infections
Clinical, Immunological and Molecular Aspects
, pp. 279 - 298
Publisher: Cambridge University Press
Print publication year: 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ardavin, C. (2003). Origin, precursors and differentiation of mouse dendritic cells. Nat Rev Immunol, 3, 582–90.CrossRefGoogle ScholarPubMed
Asselin-Paturel, C., Boonstra, A., Dalod, M.et al. (2001). Mouse type I IFNproducing cells are immature APCs with plasmacytoid morphology. Nat Immunol, 2, 1144–50.CrossRefGoogle ScholarPubMed
Banchereau, J. and Steinman, R. M. (1998). Dendritic cells and the control of immunity. Nature, 392, 245–52.CrossRefGoogle ScholarPubMed
Björck, P. (2001). Isolation and characterization of plasmacytoid dendritic cells from Flt3 ligand and granulocyte–macrophage colony-stimulating factor-treated mice. Blood, 98, 3520–26.CrossRefGoogle ScholarPubMed
Cella, M., Scheidegger, D., Palmer-Lehmann, K.et al. (1996). Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T-cell stimulatory capacity: T-T help via APC activation. J Exp Med, 184, 747–52.CrossRefGoogle ScholarPubMed
Crowley, M. T., Reilly, C. R. and Lo, D. (1999). Influence of lymphocytes on the presence and organization of dendritic cell subsets in the spleen. J Immunol, 163, 4894–900.Google ScholarPubMed
Smedt, T., Pajak, B., Muraille, E.et al. (1996). Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo. J Exp Med, 184, 1413–24.CrossRefGoogle ScholarPubMed
George, A. (1996). Generation of gamma interferon responses in murine Peyer's patches following oral immunization. Infect Immun, 64, 4606–11.Google ScholarPubMed
Henri, S., Vremec, D., Kamath, A.et al. (2001). The dendritic cell populations of mouse lymph nodes. J Immunol, 167, 741–8.CrossRefGoogle ScholarPubMed
Hopkins, S. A., Niedergang, F., Corthesy-Theulaz, I. E. and Kraehenbuhl, J. P. (2000). A recombinant Salmonella typhimurium vaccine strain is taken up and survives within murine Peyer's patch dendritic cells. Cell Microbiol, 2, 59–68.CrossRefGoogle ScholarPubMed
Inaba, K., Inaba, M., Deguchi, M.et al. (1993). Granulocytes, macrophages, and dendritic cells arise from a common major histocompatibility complex class II-negative progenitor in mouse bone marrow. Proc Natl Acad Sci USA, 90, 3038–42.CrossRefGoogle ScholarPubMed
Iwasaki, A. and Kelsall, B. L. (1999). Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T-helper type 2 cells. J Exp Med, 190, 229–39.CrossRefGoogle Scholar
Iwasaki, A. and Kelsall, B. L. (2000). Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3α, MIP-3β, and secondary lymphoid organ chemokine. J Exp Med, 191, 1381–94.CrossRefGoogle ScholarPubMed
Iwasaki, A. and Kelsall, B. L. (2001). Unique functions of CD11b+, CD8α+, and double-negative Peyer's patch dendritic cells. J Immunol, 166, 4884–90.CrossRefGoogle ScholarPubMed
Jensen, V. B., Harty, J. T. and Jones, B. D. (1998). Interactions of the invasive pathogens Salmonella typhimurium, Listeria monocytogenes, and Shigella flexneri with M cells and murine Peyer's patches. Infect Immun, 66, 3758–66.Google Scholar
Jepson, M. A. and Clark, M. A. (2001). The role of M cells in Salmonella infection. Microbes Infect, 3, 1183–90.CrossRefGoogle ScholarPubMed
Johansson, C. and Wick, M. (2004). Liver dendritic cells present bacterial antigens and produce cytokines upon Salmonella encounter. J Immunol, 172, 2496–503.CrossRefGoogle ScholarPubMed
Johansson-Lindbom, B., Svensson, M., Wurbel, M. A.et al. (2003). Selective generation of gut tropic T-cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J Exp Med, 198, 963–9.CrossRefGoogle ScholarPubMed
Jones, B. D., Ghori, N. and Falkow, S. (1994). Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med, 180, 15–23.CrossRefGoogle ScholarPubMed
Jung, S., Unutmaz, D., Wong, P.et al. (2002). In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T-cells by exogenous cell-associated antigens. Immunity, 17, 211–20.CrossRefGoogle ScholarPubMed
Kamath, A. T., Pooley, J., Keeffe, M. A.et al. (2000). The development, maturation, and turnover rate of mouse spleen dendritic cell populations. J Immunol, 165, 6762–70.CrossRefGoogle ScholarPubMed
Karem, K. L., Kanangat, S. and Rouse, B. T. (1996). Cytokine expression in the gut associated lymphoid tissue after oral administration of attenuated Salmonella vaccine strains. Vaccine, 14, 1495–502.CrossRefGoogle ScholarPubMed
Kelsall, B. L. and Strober, W. (1996). Distinct populations of dendritic cells are present in the subepithelial dome and T-cell regions of the murine Peyer's patch. J Exp Med, 183, 237–47.CrossRefGoogle ScholarPubMed
Kirby, A. C., Yrlid, U., Svensson, M. and Wick, M. J. (2001). Differential involvement of dendritic cell subsets during acute Salmonella infection. J Immunol, 166, 6802–11.CrossRefGoogle ScholarPubMed
Koch, F., Stanzl, U., Jennewein, P.et al. (1996). High level IL12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL4 and IL10. J Exp Med, 184, 741–6.CrossRefGoogle Scholar
Kudo, S., Matsuno, K., Ezaki, T. and Ogawa, M. (1997). A novel migration pathway for rat dendritic cells from the blood: hepatic sinusoids-lymph translocation. J Exp Med, 185, 777–84.CrossRefGoogle ScholarPubMed
Kursar, M., Bonhagen, K., Kohler, A.et al. (2002). Organ-specific CD4+ T-cell response during Listeria monocytogenes infection. J Immunol, 168, 6382–7.CrossRefGoogle ScholarPubMed
Leenen, P. J., Radosevic, K., Voerman, J. S.et al. (1998). Heterogeneity of mouse spleen dendritic cells: in vivo phagocytic activity, expression of macrophage markers, and subpopulation turnover. J Immunol, 160, 2166–73.Google ScholarPubMed
Lian, Z. X., Okada, T., He, X. S.et al. (2003). Heterogeneity of dendritic cells in the mouse liver: identification and characterization of four distinct populations. J Immunol, 170, 2323–30.CrossRefGoogle ScholarPubMed
MacPherson, G. G., Jenkins, C. D., Stein, M. J. and Edwards, C. (1995). Endotoxin-mediated dendritic cell release from the intestine. Characterization of released dendritic cells and TNFα dependence. J Immunol, 154, 1317–22.Google ScholarPubMed
Maldonado-Lopez, R., Maliszewski, C., Urbain, J. and Moser, M. (2001). Cytokines regulate the capacity of CD8α+ and CD8α− dendritic cells to prime Th1/Th2 cells in vivo. J Immunol, 167, 4345–50.CrossRefGoogle ScholarPubMed
Maric, I., Holt, P. G., Perdue, M. H. and Bienenstock, J. (1996). Class II MHC antigen (Ia)-bearing dendritic cells in the epithelium of the rat intestine. J Immunol, 156, 1408–14.Google ScholarPubMed
Marriott, I., Hammond, T. G., Thomas, E. K. and Bost, K. L. (1999). Salmonella efficiently enter and survive within cultured CD11c+ dendritic cells initiating cytokine expression. Eur J Immunol, 29, 1107–15.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Matsuno, K., Ezaki, T., Kudo, S. and Uehara, Y. (1996). A life stage of particle-laden rat dendritic cells in vivo: their terminal division, active phagocytosis, and translocation from the liver to the draining lymph. J Exp Med, 183, 1865–78.CrossRefGoogle ScholarPubMed
McSorley, S. J., Cookson, B. T. and Jenkins, M. K. (2000). Characterization of CD4+ T-cell responses during natural infection with Salmonella typhimurium. J Immunol, 164, 986–93.CrossRefGoogle ScholarPubMed
McSorley, S. J., Asch, S., Costalonga, M., Reinhardt, R. L. and Jenkins, M. K. (2002a). Tracking Salmonella-specific CD4 T-cells in vivo reveals a local mucosal response to a disseminated infection. Immunity, 16, 365–77.CrossRefGoogle Scholar
McSorley, S. J., Ehst, B. D., Yu, Y. and Gewirtz, A. T. (2002b). Bacterial flagellin is an effective adjuvant for CD4+ T-cells in vivo. J Immunol, 169, 3914–19.CrossRefGoogle Scholar
Morelli, A. E., Connell, P. J., Khanna, A.et al. (2000). Preferential induction of Th1 responses by functionally mature hepatic (CD8α− and CD8α+) dendritic cells: association with conversion from liver transplant tolerance to acute rejection. Transplantation, 69, 2647–57.CrossRefGoogle ScholarPubMed
Moser, M. and Murphy, K. M. (2000). Dendritic cell regulation of TH1–TH2 development. Nat Immunol, 1, 199–205.CrossRefGoogle ScholarPubMed
Nagler-Anderson, C. (2001). Man the barrier! Strategic defences in the intestinal mucosa. Nat Rev Immunol, 1, 59–67.CrossRefGoogle ScholarPubMed
Nakano, H., Yanagita, M. and Gunn, M. D. (2001). CD11c+B220+Gr-1+ cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J Exp Med, 194, 1171–8.CrossRefGoogle ScholarPubMed
Neutra, M. R., Frey, A. and Kraehenbuhl, J. P. (1996). Epithelial M cells: gateways for mucosal infection and immunization. Cell, 86, 345–8.CrossRefGoogle ScholarPubMed
Niess, J. H.,Brand, S.,Gu, X.et al. (2005). CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science, 307, 254–8.CrossRefGoogle ScholarPubMed
O'Connell, P. J., Morelli, A. E., Logar, A. J. and Thomson, A. W. (2000). Phenotypic and functional characterization of mouse hepatic CD8γ+ lymphoid-related dendritic cells. J Immunol, 165, 795–803.CrossRefGoogle ScholarPubMed
Okahashi, N., Yamamoto, M., Vancott, J. L.et al. (1996). Oral immunization of interleukin-4 (IL4) knockout mice with a recombinant Salmonella strain or cholera toxin reveals that CD4+ Th2 cells producing IL6 and IL10 are associated with mucosal immunoglobulin A responses. Infect Immun, 64, 1516–25.Google Scholar
Pavli, P., Woodhams, C. E., Doe, W. F. and Hume, D. A. (1990). Isolation and characterization of antigen-presenting dendritic cells from the mouse intestinal lamina propria. Immunology, 70, 40–7.Google ScholarPubMed
Pope, C., Kim, S. K., Marzo, A.et al. (2001). Organ-specific regulation of the CD8 T-cell response to Listeria monocytogenes infection. J Immunol, 166, 3402–9.CrossRefGoogle ScholarPubMed
Regnault, A., Lankar, D., Lacabanne, V.et al. (1999). Fcγ receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J Exp Med, 189, 371–80.CrossRefGoogle ScholarPubMed
Reis e Sousa, C. R., Hieny, S., Scharton-Kersten, T.et al. (1997). In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T-cell areas. J Exp Med, 186, 1819–29.CrossRefGoogle ScholarPubMed
Rescigno, M., Urbano, M., Valzasina, B.et al. (2001). Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol, 2, 361–7.CrossRefGoogle ScholarPubMed
Richter-Dahlfors, A., Buchan, A. M. J. and Finlay, B. B. (1997). Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med, 186, 569–80.CrossRefGoogle ScholarPubMed
Sallusto, F., Cella, M., Danieli, C. and Lanzavecchia, A. (1995). Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med, 182, 389–400.CrossRefGoogle ScholarPubMed
Sato, A., Hashiguchi, M., Toda, E.et al. (2003). CD11b+ Peyer's patch dendritic cells secrete IL6 and induce IgA secretion from naive B cells. J Immunol, 171, 3684–90.CrossRefGoogle Scholar
Sato, T., Yamamoto, H., Sasaki, C. and Wake, K. (1998). Maturation of rat dendritic cells during intrahepatic translocation evaluated using monoclonal antibodies and electron microscopy. Cell Tissue Res, 294, 503–14.CrossRefGoogle ScholarPubMed
Schulz, O., Edwards, D. A., Schito, M.et al. (2000). CD40 triggering of heterodimeric IL12 p70 production by dendritic cells in vivo requires a microbial priming signal. Immunity, 13, 453–62.CrossRefGoogle ScholarPubMed
Sheppard, M., Webb, C., Heath, F.et al. (2003). Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell Microbiol, 5, 593–600.CrossRefGoogle ScholarPubMed
Shortman, K. and Liu, Y. J. (2002). Mouse and human dendritic cell subtypes. Nature Rev Immunol, 2, 151–61.CrossRefGoogle ScholarPubMed
Shreedhar, V. K., Kelsall, B. L. and Neutra, M. R. (2003). Cholera toxin induces migration of dendritic cells from the subepithelial dome region to T- and B-cell areas of Peyer's patches. Infect Immun, 71, 504–9.CrossRefGoogle Scholar
Shurin, M. R., Pandharipande, P. P., Zorina, T. D.et al. (1997). FLT3 ligand induces the generation of functionally active dendritic cells in mice. Cell Immunol, 179, 174–84.CrossRefGoogle ScholarPubMed
Sparwasser, T., Koch, E. S., Vabulas, R. M.et al. (1998). Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur J Immunol, 28, 2045–54.3.0.CO;2-8>CrossRefGoogle ScholarPubMed
Steiniger, B., Klempnauer, J. and Wonigeit, K. (1984). Phenotype and histological distribution of interstitial dendritic cells in the rat pancreas, liver, heart, and kidney. Transplantation, 38, 169–74.CrossRefGoogle Scholar
Steinman, R. M. and Cohn, Z. A. (1973). Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med, 137, 1142–62.CrossRefGoogle ScholarPubMed
Steinman, R. M., Lustig, D. S. and Cohn, Z. A. (1974). Identification of a novel cell type in peripheral lymphoid organs of mice. 3. Functional properties in vivo. J Exp Med, 139, 1431–45.CrossRefGoogle ScholarPubMed
Steinman, R. M., Pack, M. and Inaba, K. (1997). Dendritic cells in the T-cell areas of lymphoid organs. Immunol Rev, 156, 25–37.CrossRefGoogle ScholarPubMed
Steptoe, R. J., Patel, R. K., Subbotin, V. M. and Thomson, A. W. (2000). Comparative analysis of dendritic cell density and total number in commonly transplanted organs: morphometric estimation in normal mice. Transpl Immunol, 8, 49–56.CrossRefGoogle ScholarPubMed
Sundquist, M., Johansson, C. and Wick, M. J. (2003). Dendritic cells as inducers of antimicrobial immunity in vivo. Apmis, 111, 715–24.CrossRefGoogle ScholarPubMed
Svensson, M. and Wick, M. J. (1999). Classical MHC class I peptide presentation of a bacterial fusion protein by bone marrow-derived dendritic cells. Eur J Immunol, 29, 180–8.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Svensson, M., Johansson, C. and Wick, M. J. (2000). Salmonella enterica serovar Typhimurium-induced maturation of bone marrow-derived dendritic cells. Infect Immun, 68, 6311–20.CrossRefGoogle ScholarPubMed
VanCott, J. L., Chatfield, S. N., Roberts, M.et al. (1998). Regulation of host immune responses by modification of Salmonella virulence genes. Nat Med, 4, 1247–52.CrossRefGoogle ScholarPubMed
Vazquez-Torres, A. and Fang, F. C. (2000). Cellular routes of invasion by enteropathogens. Curr Opin Microbiol, 3, 54–9.CrossRefGoogle ScholarPubMed
Vazquez-Torres, A., Jones-Carson, J., Baumler, A. J.et al. (1999). Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature, 401, 804–8.Google ScholarPubMed
Vermaelen, K. Y., Carro-Muino, I., Lambrecht, B. N. and Pauwels, R. A. (2001). Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J Exp Med, 193, 51–60.CrossRefGoogle ScholarPubMed
Vremec, D. and Shortman, K. (1997). Dendritic cell subtypes in mouse lymphoid organs: cross-correlation of surface markers, changes with incubation, and differences among thymus, spleen, and lymph nodes. J Immunol, 159, 565–73.Google ScholarPubMed
Vremec, D., Pooley, J., Hochrein, H., Wu, L. and Shortman, K. (2000). CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J Immunol 164, 2978–86.CrossRefGoogle ScholarPubMed
Wick, M. J. (2002). The role of dendritic cells during Salmonella infection. Curr Opin Immunol, 14, 437–43.CrossRefGoogle ScholarPubMed
Wick, M. J.,Leithäuser, F. and Reimann, J. (2002). The hepatic immune system. Crit Rev Immunol, 22, 47–103.CrossRefGoogle ScholarPubMed
Wilson, N. S., El-Sukkari, D., Belz, G. T.et al. (2003). Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood, 102, 2187–94.CrossRefGoogle ScholarPubMed
Winzler, C., Rovere, P., Rescigno, M.et al. (1997) Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J Exp Med, 185, 317–28.CrossRefGoogle ScholarPubMed
Woo, J., Lu, L., Rao, A. S., Li, Y.et al. (1994). Isolation, phenotype, and allostimulatory activity of mouse liver dendritic cells. Transplantation, 58, 484–91.CrossRefGoogle ScholarPubMed
Wu, L., Li, C. L. and Shortman, K. (1996). Thymic dendritic cell precursors: relationship to the T lymphocyte lineage and phenotype of the dendritic cell progeny. J Exp Med, 184, 903–11.CrossRefGoogle Scholar
Yrlid, U. and Wick, M. J. (2002). Antigen presentation capacity and cytokine production by murine splenic dendritic cell subsets upon Salmonella encounter. J Immunol, 169, 108–16.CrossRefGoogle ScholarPubMed
Yrlid, U., Svensson, M., Hakansson, A.et al. (2001). In vivo activation of dendritic cells and T-cells during Salmonella enterica serovar Typhimurium infection. Infect Immun, 69, 5726–35.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×