Differential susceptibility of bone marrow-derived dendritic cells and macrophages to productive infection with Listeria monocytogenes

Cellular Microbiology

Volumn 9, Issue 6, 2007, Pages 1397-1411

  Westcott, Marlena M ^a   Henry, Curtis J ^a   Cook, Anne S ^a   Grant, Kenneth W ^a   Hiltbold, Elizabeth M ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GREEN FLUORESCENT PROTEIN;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; BACTERIAL CELL; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL STRAIN; BONE MARROW CELL; CELL CULTURE; CELL FATE; CELL FUNCTION; CELL MATURATION; CELL SPREADING; CELL SUBPOPULATION; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; DENDRITIC CELL; IMMUNOFLUORESCENCE; LISTERIA MONOCYTOGENES; LISTERIOSIS; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; TRANSMISSION ELECTRON MICROSCOPY;

ACTINS; ANIMALS; BONE MARROW CELLS; CYTOSOL; DENDRITIC CELLS; LISTERIA INFECTIONS; LISTERIA MONOCYTOGENES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; T-LYMPHOCYTES; TOLL-LIKE RECEPTORS;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; MURINAE;

EID: 34248671404     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00880.x     Document Type: Article

References (55)

1. Aichele, P., Zinke, J., Grode, L., Schwendener, R.A., Kaufmann, S.H., and Seiler, P. (2003) Macrophages of the splenic marginal zone are essential for trapping of blood-borne particulate antigen but dispensable for induction of specific T cell responses. J Immunol 171: 1148-1155.
2. Akira, S., Takeda, K., and Kaisho, T. (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2: 675-680.
3. Belz, G.T., Shortman, K., Bevan, M.J., and Heath, W.R. (2005) CD8alpha+ dendritic cells selectively present MHC class I-restricted noncytolytic viral and intracellular bacterial antigens in vivo. J Immunol 175: 196-200.
4. Bouwer, H.G., Alberti-Segui, C., Montfort, M.J., Berkowitz, N.D., and Higgins, D.E. (2006) Directed antigen delivery as a vaccine strategy for an intracellular bacterial pathogen. Proc Natl Acad Sci USA 103: 5102-5107.
5. Brundage, R.A., Smith, G.A., Camilli, A., Theriot, J.A., and Portnoy, D.A. (1993) Expression and phosphorylation of the Listeria monocytogenes ActA protein in mammalian cells. Proc Natl Acad Sci USA 90: 11890-11894.
6. Brzoza, K.L., Rockel, A.B., and Hiltbold, E.M. (2004) Cytoplasmic entry of Listeria monocytogenes enhances dendritic cell maturation and T cell differentiation and function. J Immunol 173: 2641-2651.
7. Cella, M., Engering, A., Pinet, V., Pieters, J., and Lanzavecchia, A. (1997) Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 388: 782-787.
8. Chow, A.Y., and Mellman, I. (2005) Old lysosomes, new tricks: MHC II dynamics in DCs. Trends Immunol 26: 72-78.
9. Chow, A., Toomre, D., Garrett, W., and Mellman, I. (2002) Dendritic cell maturation triggers retrograde MHC class II transport from lysosomes to the plasma membrane. Nature 418: 988-994.
10. Conlan, J.W. (1996) Early pathogenesis of Listeria monocytogenes infection in the mouse spleen. J Med Microbiol 44: 295-302.
11. Cormack, B.P., Valdivia, R.H., and Falkow, S. (1996) FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173: 33-38.
12. Datta, S.K., Redecke, V., Prilliman, K.R., Takabayashi, K., Corr, M., Tallant, T., et al. (2003) A subset of Toll-like receptor ligands induces cross-presentation by bone marrow-derived dendritic cells. J Immunol 170: 4102-4110.
13. Decatur, A.L., and Portnoy, D.A. (2000) A PEST-like sequence in listeriolysin O essential for Listeria monocytogenes pathogenicity. Science 290: 992-995.
14. Feng, H., Zhang, D., Palliser, D., Zhu, P., Cai, S., Schlesinger, A., et al. (2005) Listeria -infected myeloid dendritic cells produce IFN-beta, priming T cell activation. J Immunol 175: 421-432.
15. Freitag, N.E., and Jacobs, K.E. (1999) Examination of Listeria monocytogenes intracellular gene expression by using the green fluorescent protein of Aequorea victoria. Infect Immun 67: 1844-1852.
16. Gautier, G., Humbert, M., Deauvieau, F., Scuiller, M., Hiscott, J., Bates, E.E., et al. (2005) A type I interferon autocrine-paracrine loop is involved in Toll-like receptor-induced interleukin-12p70 secretion by dendritic cells. J Exp Med 201: 1435-1446.
17. Gedde, M.M., Higgins, D.E., Tilney, L.G., and Portnoy, D.A. (2000) Role of listeriolysin O in cell-to-cell spread of Listeria monocytogenes. Infect Immun 68: 999-1003.
18. Gordon, S. (2002) Pattern recognition receptors: Doubling up for the innate immune response. Cell 111: 927-930.
19. Grundling, A., Burrack, L.S., Bouwer, H.G., and Higgins, D.E. (2004) Listeria monocytogenes regulates flagellar motility gene expression through MogR, a transcriptional repressor required for virulence. Proc Natl Acad Sci USA 101: 12318-12323.
20. Guzman, C.A., Domann, E., Rohde, M., Bruder, D., Darji, A., Weiss, S., et al. (1996) Apoptosis of mouse dendritic cells is triggered by listeriolysin, the major virulence determinant of Listeria monocytogenes. Mol Microbiol 20: 119-126.
21. den Haan, J.M., Lehar, S.M., and Bevan, M.J. (2000) CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med 192: 1685-1696.
22. Heath, W.R., Belz, G.T., Behrens, G.M., Smith, C.M., Forehan, S.P., Parish, I.A., et al. (2004) Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol Rev 199: 9-26.
23. Henry, R., Shaughnessy, L., Loessner, M.J., Alberti-Segui, C., Higgins, D.E., and Swanson, J.A. (2006) Cytolysin-dependent delay of vacuole maturation in macrophages infected with Listeria monocytogenes. Cell Microbiol 8: 107-119.
24. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., et al. (1992) Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 176: 1693-1702.
25. Janda, J., Schoneberger, P., Skoberne, M., Messerle, M., Russmann, H., and Geginat, G. (2004) Cross-presentation of Listeria-derived CD8 T cell epitopes requires unstable bacterial translation products. J Immunol 173: 5644-5651.
26. Jung, S., Unutmaz, D., Wong, P., Sano, G., De los Santos, K., Sparwasser, T., et al. (2002) In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity 17: 211-220.
27. Kamath, A.T., Pooley, J., O'Keeffe, M.A., Vremec, D., Zhan, Y., Lew, A.M., et al. (2000) The development, maturation, and turnover rate of mouse spleen dendritic cell populations. J Immunol 165: 6762-6770.
28. Ladel, C.H., Flesch, I.E., Arnoldi, J., and Kaufmann, S.H. (1994) Studies with MHC-deficient knock-out mice reveal impact of both MHC I- and MHC II-dependent T cell responses on Listeria monocytogenes infection. J Immunol 153: 3116-3122.
29. Lutz, M.B., Kukutsch, N., Ogilvie, A.L., Rossner, S., Koch, F., Romani, N., and Schuler, G. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223: 77-92.
30. McCaffrey, R.L., Fawcett, P., O'Riordan, M., Lee, K.D., Havell, E.A., Brown, P.O., and Portnoy, D.A. (2004) A specific gene expression program triggered by Gram-positive bacteria in the cytosol. Proc Natl Acad Sci USA 101: 11386-11391.
31. Medzhitov, R., and Janeway, C.A., Jr (2002) Decoding the patterns of self and nonself by the innate immune system. Science 296: 298-300.
32. Michelsen, K.S., Aicher, A., Mohaupt, M., Hartung, T., Dimmeler, S., Kirschning, C.J., and Schumann, R.R. (2001) 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 276: 25680-25686.
33. Moors, M.A., Levitt, B., Youngman, P., and Portnoy, D.A. (1999) Expression of listeriolysin O and ActA by intracellular and extracellular Listeria monocytogenes. Infect Immun 67: 131-139.
34. Muraille, E., Giannino, R., Guirnalda, P., Leiner, I., Jung, S., Pamer, E.G., and Lauvau, G. (2005) Distinct in vivo dendritic cell activation by live versus killed Listeria monocytogenes. Eur J Immunol 35: 1463-1471.
35. Pamer, E.G. (2004) Immune responses to Listeria monocytogenes. Nat Rev Immunol 4: 812-823.
36. Pierre, P., Turley, S.J., Gatti, E., Hull, M., Meltzer, J., Mirza, A., et al. (1997) Developmental regulation of MHC class II transport in mouse dendritic cells. Nature 388: 787-792.
37. Portnoy, D.A., Jacks, P.S., and Hinrichs, D.J. (1988) Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167: 1459-1471.
38. Portnoy, D.A., Schreiber, R.D., Connelly, P., and Tilney, L.G. (1989) Gamma interferon limits access of Listeria monocytogenes to the macrophage cytoplasm. J Exp Med 170: 2141-2146.
39. Portnoy, D.A., Auerbuch, V., and Glomski, I.J. (2002) The cell biology of Listeria monocytogenes infection: The intersection of bacterial pathogenesis and cell-mediated immunity. J Cell Biol 158: 409-414.
40. Pron, B., Boumaila, C., Jaubert, F., Berche, P., Milon, G., Geissmann, F., and Gaillard, J.L. (2001) Dendritic cells are early cellular targets of Listeria monocytogenes after intestinal delivery and are involved in bacterial spread in the host. Cell Microbiol 3: 331-340.
41. Racoosin, E.L., and Swanson, J.A. (1989) Macrophage colony-stimulating factor (rM-CSF) stimulates pinocytosis in bone marrow-derived macrophages. J Exp Med 170: 1635-1648.
42. 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.
43. Serbina, N.V., Salazar-Mather, T.P., Biron, C.A., Kuziel, W.A., and Pamer, E.G. (2003) TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19: 59-70.
44. Shen, H., Miller, J.F., Fan, X., Kolwyck, D., Ahmed, R., and Harty, J.T. (1998) Compartmentalization of bacterial antigens: Differential effects on priming of CD8 T cells and protective immunity. Cell 92: 535-545.
45. Shetron-Rama, L.M., Marquis, H., Bouwer, H.G., and Freitag, N.E. (2002) Intracellular induction of Listeria monocytogenes actA expression. Infect Immun 70: 1087-1096.
46. Shortman, K., and Liu, Y.J. (2002) Mouse and human dendritic cell subtypes. Nat Rev Immunol 2: 151-161.
47. Spisek, R., Brazova, J., Rozkova, D., Zapletalova, K., Sediva, A., and Bartunkova, J. (2004) Maturation of dendritic cells by bacterial immunomodulators. Vaccine 22: 2761-2768.
48. Steinman, R.M. (1991) The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 9: 271-296.
49. Steinman, R.M., Bonifaz, L., Fujii, S., Liu, K., Bonnyay, D., Yamazaki, S., et al. (2005) The innate functions of dendritic cells in peripheral lymphoid tissues. Adv Exp Med Biol 560: 83-97.
50. Stier, E.M., Mandal, M., and Lee, K.D. (2005) Differential cytosolic delivery and presentation of antigen by listeriolysin O-liposomes to macrophages and dendritic cells. Mol Pharm 2: 74-82.
51. Tailor, P., Tamura, T., and Ozato, K. (2006) IRF family proteins and type I interferon induction in dendritic cells. Cell Res 16: 134-140.
52. Trombetta, E.S., and Mellman, I. (2005) Cell biology of antigen processing in vitro and in vivo. Annu Rev Immunol 23: 975-1028.
53. Trombetta, E.S., Ebersold, M., Garrett, W., Pypaert, M., and Mellman, I. (2003) Activation of lysosomal function during dendritic cell maturation. Science 299: 1400-1403.
54. Winzler, C., Rovere, P., Rescigno, M., Granucci, F., Penna, G., Adorini, L., et al. (1997) Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J Exp Med 185: 317-328.
55. Zammit, D.J., Cauley, L.S., Pham, Q.M., and Lefrancois, L. (2005) Dendritic cells maximize the memory CD8 T cell response to infection. Immunity 22: 561-570.