Monocyte-derived inflammatory dendritic cells in the granuloma during mycobacterial infection

Advances in Experimental Medicine and Biology

Volumn 946, Issue , 2012, Pages 277-293

  Schreiber, Heidi A ^b   Sandor, Matyas ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b NONE

Author keywords

Acute and chronic infection; BCG; CD4 + T cells; Dendritic cells; Granuloma; Mycobacteria

Indexed keywords

ARTICLE; CD4+ T LYMPHOCYTE; DENDRITIC CELL; GRANULOMA; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; MONOCYTE; MYCOBACTERIOSIS; MYCOBACTERIUM; MYCOSIS; NONHUMAN; PRIORITY JOURNAL; PROTOZOAL INFECTION; VIRUS INFECTION;

ANIMALS; DENDRITIC CELLS; GRANULOMA; HUMANS; INFLAMMATION; MONOCYTES; MYCOBACTERIUM; MYCOBACTERIUM INFECTIONS;

CORYNEBACTERINEAE; MYCOBACTERIUM;

EID: 80555154754     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-0106-3_16     Document Type: Article

References (93)

1. Aldridge, J. R., Jr., C. E. Moseley, D. A. Boltz, N. J. Negovetich, C. Reynolds, J. Franks, S. A. Brown, P. C. Doherty, R. G. Webster and P. G. Thomas.2009) TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc Natl Acad Sci U S A. 106, 5306-5311
2. Allan, R. S., J. Waithman, S. Bedoui, C. M. Jones, J. A. Villadangos, Y. Zhan, A. M. Lew, K. Shortman, W. R. Heath and F. R. Carbone.2006) Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity. 25, 153-162
3. Arnold, L., A. Henry, F. Poron, Y. Baba-Amer, N. van Rooijen, A. Plonquet, R. K. Gherardi and B. Chazaud.2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med. 204, 1057-1069
4. Auffray, C., D. Fogg, M. Garfa, G. Elain, O. Join-Lambert, S. Kayal, S. Sarnacki, A. Cumano, G. Lauvau and F. Geissmann.2007) Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science. 317, 666-670
5. Auffray, C., D. K. Fogg, E. Narni-Mancinelli, B. Senechal, C. Trouillet, N. Saederup, J. Leemput, K. Bigot, L. Campisi, M. Abitbol, T. Molina, I. Charo, D. A. Hume, A. Cumano, G. Lauvau and F. Geissmann.2009) CX3CR1+ CD115+ CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J Exp Med. 206, 595-606
6. Auffray, C., M. H. Sieweke and F. Geissmann.2009) Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu Rev Immunol. 27, 669-692
7. Badewa, A. P., L. J. Quinton, J. E. Shellito and C. M. Mason.2005) Chemokine receptor 5 and its ligands in the immune response to murine tuberculosis. Tuberculosis (Edinb). 85, 185-195
8. Bakri, Y., S. Sarrazin, U. P. Mayer, S. Tillmanns, C. Nerlov, A. Boned and M. H. Sieweke.2005) Balance of MafB and PU.1 specifies alternative macrophage or dendritic cell fate. Blood. 105, 2707-2716
9. Belz, G. T., C. M. Smith, L. Kleinert, P. Reading, A. Brooks, K. Shortman, F. R. Carbone and W. R. Heath.2004) Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc Natl Acad Sci U S A. 101, 8670-8675
10. Blease, K., B. Mehrad, N. W. Lukacs, S. L. Kunkel, T. J. Standiford and C. M. Hogaboam.2001) Antifungal and airway remodeling roles for murine monocyte chemoattractant protein-1/CCL2 during pulmonary exposure to Asperigillus fumigatus conidia. J Immunol. 166, 1832-1842
11. Blease, K., B. Mehrad, T. J. Standiford, N. W. Lukacs, J. Gosling, L. Boring, I. F. Charo, S. L. Kunkel and C. M. Hogaboam.2000) Enhanced pulmonary allergic responses to Aspergillus in CCR2-/- mice. J Immunol. 165, 2603-2611
12. Cheong, C., I. Matos, J. H. Choi, D. B. Dandamudi, E. Shrestha, M. P. Longhi, K. L. Jeffrey, R. M. Anthony, C. Kluger, G. Nchinda, H. Koh, A. Rodriguez, J. Idoyaga, M. Pack, K. Velinzon, C. G. Park and R. M. Steinman.2010) Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell. 143, 416-429
13. Combadiere, C., S. Potteaux, M. Rodero, T. Simon, A. Pezard, B. Esposito, R. Merval, A. Proudfoot, A. Tedgui and Z. Mallat.2008) Combined inhibition of CCL2, CX3CR1, and CCR5 abrogates Ly6C(hi) and Ly6C(lo) monocytosis and almost abolishes atherosclerosis in hypercholesterolemic mice. Circulation. 117, 1649-1657
14. Czuprynski, C. J., J. F. Brown, N. Maroushek, R. D. Wagner and H. Steinberg.1994) Administration of anti-granulocyte mAb RB6-8C5 impairs the resistance of mice to Listeria monocytogenes infection. J Immunol. 152, 1836-1846
15. Dahl, R., J. C. Walsh, D. Lancki, P. Laslo, S. R. Iyer, H. Singh and M. C. Simon.2003) Regulation of macrophage and neutrophil cell fates by the PU. 1:C/EBPalpha ratio and granulocyte colony-stimulating factor. Nat Immunol. 4, 1029-1036
16. Dai, X. M., G. R. Ryan, A. J. Hapel, M. G. Dominguez, R. G. Russell, S. Kapp, V. Sylvestre and E. R. Stanley.2002) Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood. 99, 111-120
17. Dunay, I. R., R. A. Damatta, B. Fux, R. Presti, S. Greco, M. Colonna and L. D. Sibley.2008) Gr1(+) inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity. 29, 306-317
18. Egen, J. G., A. G. Rothfuchs, C. G. Feng, N. Winter, A. Sher and R. N. Germain.2008) Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity. 28, 271-284
19. Eidsmo, L., R. Allan, I. Caminschi, N. van Rooijen, W. R. Heath and F. R. Carbone.2009) Differential migration of epidermal and dermal dendritic cells during skin infection. J Immunol. 182, 3165-3172
20. Ersland, K., M. Wuthrich and B. S. Klein.2010) Dynamic interplay among monocyte-derived, dermal, and resident lymph node dendritic cells during the generation of vaccine immunity to fungi. Cell Host Microbe. 7, 474-487
21. Fleming, T. J., M. L. Fleming and T. R. Malek.1993) Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow. RB6-8C5 mAb to granulocyte-differentiation antigen (Gr- 1) detects members of the Ly-6 family. J Immunol. 151, 2399-2408
22. Flores-Villanueva, P. O., J. A. Ruiz-Morales, C. H. Song, L. M. Flores, E. K. Jo, M. Montano, P. F. Barnes, M. Selman and J. Granados.2005) A functional promoter polymorphism in monocyte chemoattractant protein-1 is associated with increased susceptibility to pulmonary tuberculosis. J Exp Med. 202, 1649-1658
23. Fogg, D. K., C. Sibon, C. Miled, S. Jung, P. Aucouturier, D. R. Littman, A. Cumano and F. Geissmann.2006) A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science. 311, 83-87
24. Geissmann, F., S. Jung and D. R. Littman.2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 19, 71-82
25. Ginhoux, F., F. Tacke, V. Angeli, M. Bogunovic, M. Loubeau, X. M. Dai, E. R. Stanley, G. J. Randolph and M. Merad.2006) Langerhans cells arise from monocytes in vivo. Nat Immunol. 7, 265-273
26. Gonzalez-Mejia, M. E. and A. I. Doseff.2009) Regulation of monocytes and macrophages cell fate. Front Biosci. 14, 2413-2431
27. Hall, J. D., S. L. Kurtz, N. W. Rigel, B. M. Gunn, S. Taft-Benz, J. P. Morrison, A. M. Fong, D. D. Patel, M. Braunstein and T. H. Kawula.2009) The impact of chemokine receptor CX3CR1 deficiency during respiratory infections with Mycobacterium tuberculosis or Francisella tularensis. Clin Exp Immunol. 156, 278-284
28. Hohl, T. M., A. Rivera, L. Lipuma, A. Gallegos, C. Shi, M. Mack and E. G. Pamer.2009) Inflammatory monocytes facilitate adaptive CD4 T cell responses during respiratory fungal infection. Cell Host Microbe. 6, 470-481
29. Holt, P. G., S. Haining, D. J. Nelson and J. D. Sedgwick.1994) Origin and steady-state turnover of class II MHC-bearing dendritic cells in the epithelium of the conducting airways. J Immunol. 153, 256-261
30. Humphreys, I. R., G. R. Stewart, D. J. Turner, J. Patel, D. Karamanou, R. J. Snelgrove and D. B. Young.2006) A role for dendritic cells in the dissemination of mycobacterial infection. Microbes Infect. 8, 1339-1346
31. Iijima, N., M. M. Linehan, S. Saeland and A. Iwasaki.2007) Vaginal epithelial dendritic cells renew from bone marrow precursors. Proc Natl Acad Sci U S A. 104, 19061-19066
32. Inaba, K., M. Inaba, N. Romani, H. Aya, M. Deguchi, S. Ikehara, S. Muramatsu and R. M. Steinman.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
33. Jakubzick, C., F. Tacke, F. Ginhoux, A. J. Wagers, N. van Rooijen, M. Mack, M. Merad and G. J. Randolph.2008) Blood monocyte subsets differentially give rise to CD103+ and CD103- pulmonary dendritic cell populations. J Immunol. 180, 3019-3027
34. Jiao, X., R. Lo-Man, P. Guermonprez, L. Fiette, E. Deriaud, S. Burgaud, B. Gicquel, N. Winter and C. Leclerc.2002) Dendritic cells are host cells for mycobacteria in vivo that trigger innate and acquired immunity. J Immunol. 168, 1294-1301
35. Kahnert, A., U. E. Hopken, M. Stein, S. Bandermann, M. Lipp and S. H. Kaufmann.2007) Mycobacterium tuberculosis triggers formation of lymphoid structure in murine lungs. J Infect Dis. 195, 46-54
36. Kamath, A. T., S. Henri, F. Battye, D. F. Tough and K. Shortman.2002) Developmental kinetics and lifespan of dendritic cells in mouse lymphoid organs. Blood. 100, 1734-1741
37. Kamphorst, A. O., P. Guermonprez, D. Dudziak and M. C. Nussenzweig.2010) Route of antigen uptake differentially impacts presentation by dendritic cells and activated monocytes. J Immunol. 185, 3426-3435
38. Kang, S. J., H. E. Liang, B. Reizis and R. M. Locksley.2008) Regulation of hierarchical clustering and activation of innate immune cells by dendritic cells. Immunity. 29, 819-833
39. Khader, S. A., J. Rangel-Moreno, J. J. Fountain, C. A. Martino, W. W. Reiley, J. E. Pearl, G. M. Winslow, D. L. Woodland, T. D. Randall and A. M. Cooper.2009) In a murine tuberculosis model, the absence of homeostatic chemokines delays granuloma formation and protective immunity. J Immunol. 183, 8004-8014
40. Kurihara, T., G. Warr, J. Loy and R. Bravo.1997) Defects in macrophage recruitment and host defense in mice lacking the CCR2 chemokine receptor. J Exp Med. 186, 1757-1762
41. Laouar, Y., T. Welte, X. Y. Fu and R. A. Flavell.2003) STAT3 is required for Flt3L-dependent dendritic cell differentiation. Immunity. 19, 903-912
42. Leon, B. and C. Ardavin.2008) Monocyte migration to inflamed skin and lymph nodes is differentially controlled by L-selectin and PSGL-1. Blood. 111, 3126-3130
43. Leon, B., M. Lopez-Bravo and C. Ardavin.2007) Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity. 26, 519-531
44. Lin, Y., J. Gong, M. Zhang, W. Xue and P. F. Barnes.1998) Production of monocyte chemoattractant protein 1 in tuberculosis patients. Infect Immun. 66, 2319-2322
45. Lindquist, R. L., G. Shakhar, D. Dudziak, H. Wardemann, T. Eisenreich, M. L. Dustin and M. C. Nussenzweig.2004) Visualizing dendritic cell networks in vivo. Nat Immunol. 5, 1243-1250
46. Liu, K. and M. C. Nussenzweig.2010) Origin and development of dendritic cells. Immunol Rev. 234, 45-54
47. Liu, K., G. D. Victora, T. A. Schwickert, P. Guermonprez, M. M. Meredith, K. Yao, F. F. Chu, G. J. Randolph, A. Y. Rudensky and M. Nussenzweig.2009) In vivo analysis of dendritic cell development and homeostasis. Science. 324, 392-397
48. Liu, K., C. Waskow, X. Liu, K. Yao, J. Hoh and M. Nussenzweig.2007) Origin of dendritic cells in peripheral lymphoid organs of mice. Nat Immunol. 8, 578-583
49. McCurley, N. and I. Mellman.2010) Monocyte-derived dendritic cells exhibit increased levels of lysosomal proteolysis as compared to other human dendritic cell populations. PLoS One. 5, e11949
50. McKenna, H. J., K. L. Stocking, R. E. Miller, K. Brasel, T. De Smedt, E. Maraskovsky, C. R. Maliszewski, D. H. Lynch, J. Smith, B. Pulendran, E. R. Roux, M. Teepe, S. D. Lyman and J. J. Peschon.2000) Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood. 95, 3489-3497
51. Mohrs, K., A. E. Wakil, N. Killeen, R. M. Locksley and M. Mohrs.2005) A two-step process for cytokine production revealed by IL-4 dual-reporter mice. Immunity. 23, 419-429
52. Murray, E., R. Webb and M. Swann.1926) A disease of rabbits characterized by a large mononuclear monocytosis, caused by a hitherto undescribed bacillus Bacterium monocytogenes. J Pathol Bacteriol. 29, 407-439
53. Nahrendorf, M., F. K. Swirski, E. Aikawa, L. Stangenberg, T. Wurdinger, J. L. Figueiredo, P. Libby, R. Weissleder and M. J. Pittet.2007) The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med. 204, 3037-3047
54. Naik, S. H., D. Metcalf, A. van Nieuwenhuijze, I. Wicks, L. Wu, M. O'Keeffe and K. Shortman.2006) Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat Immunol. 7, 663-671
55. Nakano, H., K. L. Lin, M. Yanagita, C. Charbonneau, D. N. Cook, T. Kakiuchi and M. D. Gunn.2009) Blood-derived inflammatory dendritic cells in lymph nodes stimulate acute T helper type 1 immune responses. Nat Immunol. 10, 394-402
56. Niess, J. H., S. Brand, X. Gu, L. Landsman, S. Jung, B. A. McCormick, J. M. Vyas, M. Boes, H. L. Ploegh, J. G. Fox, D. R. Littman and H. C. Reinecker.2005) CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science. 307, 254-258
57. Park, S. J., M. D. Burdick, W. K. Brix, M. H. Stoler, D. S. Askew, R. M. Strieter and B. Mehrad.2010) Neutropenia Enhances Lung Dendritic Cell Recruitment in Response to Aspergillus via a Cytokine-to-Chemokine Amplification Loop. J Immunol.
58. Peters, W., H. M. Scott, H. F. Chambers, J. L. Flynn, I. F. Charo and J. D. Ernst.2001) Chemokine receptor 2 serves an early and essential role in resistance to Mycobacterium tuberculosis. Proc Natl Acad Sci U S A. 98, 7958-7963
59. Randolph, G. J.2006) Migratory dendritic cells: sometimes simply ferries? Immunity. 25, 15-18
60. Randolph, G. J., S. Beaulieu, S. Lebecque, R. M. Steinman and W. A. Muller.1998) Differentiation of monocytes into dendritic cells in a model of transendothelial trafficking. Science. 282, 480-483
61. Randolph, G. J., K. Inaba, D. F. Robbiani, R. M. Steinman and W. A. Muller.1999) Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity. 11, 753-761
62. Randolph, G. J., C. Jakubzick and C. Qu.2008) Antigen presentation by monocytes and monocyte- derived cells. Curr Opin Immunol. 20, 52-60
63. Ravindran, R., L. Rusch, A. Itano, M. K. Jenkins and S. J. McSorley.2007) CCR6-dependent recruitment of blood phagocytes is necessary for rapid CD4 T cell responses to local bacterial infection. Proc Natl Acad Sci U S A. 104, 12075-12080
64. Reljic, R., C. Di Sano, C. Crawford, F. Dieli, S. Challacombe and J. Ivanyi.2005) Time course of mycobacterial infection of dendritic cells in the lungs of intranasally infected mice. Tuberculosis (Edinb). 85, 81-88
65. Robben, P. M., M. LaRegina, W. A. Kuziel and L. D. Sibley.2005) Recruitment of Gr-1+ monocytes is essential for control of acute toxoplasmosis. J Exp Med. 201, 1761-1769
66. Russell, D. G.2007) Who puts the tubercle in tuberculosis? Nat Rev Microbiol. 5, 39-47
67. Rydstrom, A. and M. J. Wick.2007) Monocyte recruitment, activation, and function in the gutassociated lymphoid tissue during oral Salmonella infection. J Immunol. 178, 5789-5801
68. Sallusto, F. and A. Lanzavecchia.1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/ macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med. 179, 1109-1118
69. Schreiber, H. A. and M. Sandor.2010) The role of dendritic cells in mycobacterium-induced granulomas. Immunol Lett. 130, 26-31
70. Schreiber, H. A., P. D. Hulseberg, J. Lee, J. Prechl, P. Barta, N. Szlavik, J. S. Harding, Z. Fabry and M. Sandor.2010) Dendritic cells in chronic mycobacterial granulomas restrict local antibacterial T cell response in a murine model. PLoS One. 5, e11453
71. Schreiber, O., K. Steinwede, N. Ding, M. Srivastava, R. Maus, F. Langer, J. Prokein, S. Ehlers, T. Welte, M. D. Gunn and U. A. Maus.2008) Mice that overexpress CC chemokine ligand 2 in their lungs show increased protective immunity to infection with Mycobacterium bovis bacilli Calmette-Guerin. J Infect Dis. 198, 1044-1054
72. Scott, H. M. and J. L. Flynn.2002) Mycobacterium tuberculosis in chemokine receptor 2-deficient mice: influence of dose on disease progression. Infect Immun. 70, 5946-5954
73. Serbina, N. V. and E. G. Pamer.2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol. 7, 311-317
74. Serbina, N. V., T. Jia, T. M. Hohl and E. G. Pamer.2008) Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol. 26, 421-452
75. Serbina, N. V., W. Kuziel, R. Flavell, S. Akira, B. Rollins and E. G. Pamer.2003a) Sequential MyD88-independent and -dependent activation of innate immune responses to intracellular bacterial infection. Immunity. 19, 891-901
76. Serbina, N. V., T. P. Salazar-Mather, C. A. Biron, W. A. Kuziel and E. G. Pamer.2003b) TNF/ iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity. 19, 59-70
77. Steinman, R. M. and Z. A. Cohn.1973) Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med. 137, 1142-1162
78. Steinman, R. M. and Z. A. Cohn.1974a) Identification of a novel cell type in peripheral lymphoid organs of mice. II. Functional properties in vitro. J Exp Med. 139, 380-397
79. Steinman, R. M., D. S. Lustig and Z. A. Cohn.1974b) Identification of a novel cell type in peripheral lymphoid organs of mice. 3. Functional properties in vivo. J Exp Med. 139, 1431-1445
80. Sunderkotter, C., T. Nikolic, M. J. Dillon, N. Van Rooijen, M. Stehling, D. A. Drevets and P. J. Leenen.2004) Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol. 172, 4410-4417
81. Tacke, F., D. Alvarez, T. J. Kaplan, C. Jakubzick, R. Spanbroek, J. Llodra, A. Garin, J. Liu, M. Mack, N. van Rooijen, S. A. Lira, A. J. Habenicht and G. J. Randolph.2007) Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest. 117, 185-194
82. Tacke, F. and G. J. Randolph.2006) Migratory fate and differentiation of blood monocyte subsets. Immunobiology. 211, 609-618
83. Tian, T., J. Woodworth, M. Skold and S. M. Behar.2005) In vivo depletion of CD11c+ cells delays the CD4 +T cell response to Mycobacterium tuberculosis and exacerbates the outcome of infection. J Immunol. 175, 3268-3272
84. Tsou, C. L., W. Peters, Y. Si, S. Slaymaker, A. M. Aslanian, S. P. Weisberg, M. Mack and I. F. Charo.2007) Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest. 117, 902-909
85. Ulrichs, T. and S. H. Kaufmann.2006) New insights into the function of granulomas in human tuberculosis. J Pathol. 208, 261-269
86. Varol, C., L. Landsman, D. K. Fogg, L. Greenshtein, B. Gildor, R. Margalit, V. Kalchenko, F. Geissmann and S. Jung.2007) Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med. 204, 171-180
87. Volkman, H. E., H. Clay, D. Beery, J. C. Chang, D. R. Sherman and L. Ramakrishnan.2004) Tuberculous granuloma formation is enhanced by a mycobacterium virulence determinant. PLoS Biol. 2, e367
88. Wakim, L. M., J. Waithman, N. van Rooijen, W. R. Heath and F. R. Carbone.2008) Dendritic cellinduced memory T cell activation in nonlymphoid tissues. Science. 319, 198-202
89. Waskow, C., K. Liu, G. Darrasse-Jeze, P. Guermonprez, F. Ginhoux, M. Merad, T. Shengelia, K. Yao and M. Nussenzweig.2008) The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat Immunol. 9, 676-683
90. Whitelaw, D. M.1966) The intravascular lifespan of monocytes. Blood. 28, 455-464
91. Wolf, A. J., L. Desvignes, B. Linas, N. Banaiee, T. Tamura, K. Takatsu and J. D. Ernst.2007a) Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J Exp Med.
92. Wolf, A. J., B. Linas, G. J. Trevejo-Nunez, E. Kincaid, T. Tamura, K. Takatsu and J. D. Ernst.2007b) Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J Immunol. 179, 2509-2519
93. Zhan, Y., Y. Xu, S. Seah, J. L. Brady, E. M. Carrington, C. Cheers, B. A. Croker, L. Wu, J. A. Villadangos and A. M. Lew.2010) Resident and monocyte-derived dendritic cells become dominant IL-12 producers under different conditions and signaling pathways. J Immunol. 185, 2125-2133