Intestinal monocytes and macrophages are required for T cell polarization in response to Citrobacter rodentium

Journal of Experimental Medicine

Volumn 210, Issue 10, 2013, Pages 2025-2039

  Schreiber, Heidi A ^a   Loschko, Jakob ^a   Karssemeijer, Roos A ^a   Escolano, Amelia ^a   Meredith, Matthew M ^a   Mucida, Daniel ^a   Guermonprez, Pierre ^a,b   Nussenzweig, Michel C ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR 1; DIPHTHERIA TOXIN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR RECEPTOR; INTERLEUKIN 12; LYSOZYME;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL POLARITY; CELL TYPE; CITROBACTER RODENTIUM; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; INFLAMMATION; INTESTINE; INTESTINE INFECTION; KUPFFER CELL; LAMINA PROPRIA; LYMPHOID CELL; MACROPHAGE; MESENTERY LYMPH NODE; MONOCYTE; MOUSE; MOUTH INFECTION; NONHUMAN; PATHOGENESIS; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH1 CELL;

EID: 84885464048     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20130903     Document Type: Article

References (89)

1. Athie-Morales, V., H.H. Smits, D.A. Cantrell, and C.M. Hilkens. 2004. Sustained IL-12 signaling is required for Th1 development. J. Immunol. 172:61-69.
2. + common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J. Exp. Med. 206:595-606. http://dx.doi.org/10.1084/jem.20081385
3. Basu, R., D.B. O'Quinn, D.J. Silberger, T.R. Schoeb, L. Fouser, W. Ouyang, R.D. Hatton, and C.T. Weaver. 2012. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity. 37:1061-1075. http://dx.doi.org/10.1016/j.immuni.2012.08.024
4. Bennett, C.L., and B.E. Clausen. 2007. DC ablation in mice: promises, pitfalls, and challenges. Trends Immunol. 28:525-531. http://dx.doi.org/10.1016/j.it.2007.08.011
5. Bogunovic, M., F. Ginhoux, J. Helft, L. Shang, D. Hashimoto, M. Greter, K. Liu, C. Jakubzick, M.A. Ingersoll, M. Leboeuf, et al. 2009. Origin of the lamina propria dendritic cell network. Immunity. 31:513-525. http://dx.doi.org/10.1016/j.immuni.2009.08.010
6. Bogunovic, M., A. Mortha, P.A. Muller, and M. Merad. 2012. Mononuclear phagocyte diversity in the intestine. Immunol. Res. 54:37-49. http://dx.doi.org/10.1007/s12026-012-8323-5
7. Boring, L., J. Gosling, S.W. Chensue, S.L. Kunkel, R.V. Farese Jr., H.E. Broxmeyer, and I.F. Charo. 1997. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J. Clin. Invest. 100:2552-2561. http://dx.doi.org/10.1172/JCI119798
8. Bry, L., and M.B. Brenner. 2004. Critical role of T cell-dependent serum antibody, but not the gut-associated lymphoid tissue, for surviving acute mucosal infection with Citrobacter rodentium, an attaching and effacing pathogen. J. Immunol. 172:433-441.
9. +-T-cell effector functions and costimulatory requirements essential for surviving mucosal infection with Citrobacter rodentium. Infect. Immun. 74:673-681. http://dx.doi.org/10.1128/IAI.74.1.673-681.2006
10. Cerovic, V., S.A. Houston, C.L. Scott, A. Aumeunier, U. Yrlid, A.M. Mowat, and S.W. Milling. 2013. Intestinal CD103(-) dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol. 6:104-113. http://dx.doi.org/10.1038/mi.2012.53
11. Chow, A., B.D. Brown, and M. Merad. 2011. Studying the mononuclear phagocyte system in the molecular age. Nat. Rev. Immunol. 11:788-798. http://dx.doi.org/10.1038/nri3087
12. Clausen, B.E., C. Burkhardt, W. Reith, R. Renkawitz, and I. Förster. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8:265-277. http://dx.doi.org/10.1023/A:1008942828960
13. 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. http://dx.doi.org/10.1182/blood.V99.1.111
14. Denning, T.L., Y.C. Wang, S.R. Patel, I.R. Williams, and B. Pulendran. 2007. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8:1086-1094. http://dx.doi.org/10.1038/ni1511
15. Denning, T.L., B.A. Norris, O. Medina-Contreras, S. Manicassamy, D. Geem, R. Madan, C.L. Karp, and B. Pulendran. 2011. Functional specializations of intestinal dendritic cell and macrophage subsets that control Th17 and regulatory T cell responses are dependent on the T cell/APC ratio, source of mouse strain, and regional localization. J. Immunol. 187:733-747. http://dx.doi.org/10.4049/jimmunol.1002701
16. Diehl, G.E., R.S. Longman, J.X. Zhang, B. Breart, C. Galan, A. Cuesta, S.R. Schwab, and D.R. Littman. 2013. Microbiota restricts trafficking of bacteria to mesenteric lymph nodes by CX(3)CR1(hi) cells. Nature. 494:116-120. http://dx.doi.org/10.1038/nature11809
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. http://dx.doi.org/10.1016/j.immuni.2008.05.019
18. Egan, C.E., M.D. Craven, J. Leng, M. Mack, K.W. Simpson, and E.Y. Denkers. 2009. CCR2-dependent intraepithelial lymphocytes mediate inflammatory gut pathology during Toxoplasma gondii infection. Mucosal Immunol. 2:527-535. http://dx.doi.org/10.1038/mi.2009.105
19. Farache, J., I. Koren, I. Milo, I. Gurevich, K.W. Kim, E. Zigmond, G.C. Furtado, S.A. Lira, and G. Shakhar. 2013. Luminal bacteria recruit CD103(+) dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity. 38:581-595.
20. 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. http://dx.doi.org/10.1126/science.1117729
21. Gautier, E.L., T. Shay, J. Miller, M. Greter, C. Jakubzick, S. Ivanov, J. Helft, A. Chow, K.G. Elpek, S. Gordonov, et al; Immunological Genome Consortium. 2012. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13:1118-1128. http://dx.doi.org/10.1038/ni.2419
22. Geissmann, F., C. Auffray, R. Palframan, C. Wirrig, A. Ciocca, L. Campisi, E. Narni-Mancinelli, and G. Lauvau. 2008. Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol. Cell Biol. 86:398-408. http://dx.doi.org/10.1038/icb.2008.19
23. Geissmann, F., S. Gordon, D.A. Hume, A.M. Mowat, and G.J. Randolph. 2010a. Unravelling mononuclear phagocyte heterogeneity. Nat. Rev. Immunol. 10:453-460. http://dx.doi.org/10.1038/nri2784
24. Geissmann, F., M.G. Manz, S. Jung, M.H. Sieweke, M. Merad, and K. Ley. 2010b. Development of monocytes, macrophages, and dendritic cells. Science. 327:656-661. http://dx.doi.org/10.1126/science.1178331
25. Ginhoux, F., K. Liu, J. Helft, M. Bogunovic, M. Greter, D. Hashimoto, J. Price, N. Yin, J. Bromberg, S.A. Lira, et al. 2009. The origin and development of nonlymphoid tissue CD103+ DCs. J. Exp. Med. 206:3115-3130. http://dx.doi.org/10.1084/jem.20091756
26. Goldszmid, R.S., P. Caspar, A. Rivollier, S. White, A. Dzutsev, S. Hieny, B. Kelsall, G. Trinchieri, and A. Sher. 2012. NK cell-derived interferon-γ orchestrates cellular dynamics and the differentiation of monocytes into dendritic cells at the site of infection. Immunity. 36:1047-1059. http://dx.doi.org/10.1016/j.immuni.2012.03.026
27. Gorak, P.M., C.R. Engwerda, and P.M. Kaye. 1998. Dendritic cells, but not macrophages, produce IL-12 immediately following Leishmania donovani infection. Eur. J. Immunol. 28:687-695. http://dx.doi.org/10.1002/(SICI)1521-4141(199802)28:023.0.CO;2-N
28. Gordon, S., and P.R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5:953-964. http://dx.doi.org/10.1038/nri1733
29. Hadis, U., B. Wahl, O. Schulz, M. Hardtke-Wolenski, A. Schippers, N. Wagner, W. Müller, T. Sparwasser, R. Förster, and O. Pabst. 2011. Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria. Immunity. 34:237-246. http://dx.doi.org/10.1016/j.immuni.2011.01.016
30. Hashimoto, D., J. Miller, and M. Merad. 2011. Dendritic cell and macrophage heterogeneity in vivo. Immunity. 35:323-335. http://dx.doi.org/10.1016/j.immuni.2011.09.007
31. Heufler, C., F. Koch, U. Stanzl, G. Topar, M. Wysocka, G. Trinchieri, A. Enk, R.M. Steinman, N. Romani, and G. Schuler. 1996. Interleukin-12 is produced by dendritic cells and mediates T helper 1 development as well as interferon-gamma production by T helper 1 cells. Eur. J. Immunol. 26:659-668. http://dx.doi.org/10.1002/eji.1830260323
32. Higgins, L.M., G. Frankel, G. Douce, G. Dougan, and T.T. MacDonald. 1999. Citrobacter rodentium infection in mice elicits a mucosal Th1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect. Immun. 67:3031-3039.
33. Hirata, Y., L. Egea, S.M. Dann, L. Eckmann, and M.F. Kagnoff. 2010. GMCSF- facilitated dendritic cell recruitment and survival govern the intestinal mucosal response to a mouse enteric bacterial pathogen. Cell Host Microbe. 7:151-163. http://dx.doi.org/10.1016/j.chom.2010.01.006
34. 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. http://dx.doi.org/10.1016/j.chom.2009.10.007
35. + T cells through IL-12 produced by Listeria-induced macrophages. Science. 260:547-549. http://dx.doi.org/10.1126/science.8097338
36. + dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 205:2139-2149. http://dx.doi.org/10.1084/jem.20080414
37. + dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202:1063-1073. http://dx.doi.org/10.1084/jem.20051100
38. Jönsson, J.I., Z. Xiang, M. Pettersson, M. Lardelli, and G. Nilsson. 2001. Distinct and regulated expression of Notch receptors in hematopoietic lineages and during myeloid differentiation. Eur. J. Immunol. 31:3240-3247. http://dx.doi.org/10.1002/1521-4141(200111)31:113.0.CO;2-E
39. Jung, S., J. Aliberti, P. Graemmel, M.J. Sunshine, G.W. Kreutzberg, A. Sher, and D.R. Littman. 2000. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20:4106-4114. http://dx.doi.org/10.1128/MCB.20.11.4106-4114.2000
40. Jung, S., D. Unutmaz, P. Wong, G. Sano, K. De los Santos, T. Sparwasser, S. Wu, S. Vuthoori, K. Ko, F. Zavala, et al. 2002. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cellassociated antigens. Immunity. 17:211-220. http://dx.doi.org/10.1016/S1074-7613(02)00365-5
41. Kim, C.H., L. Rott, E.J. Kunkel, M.C. Genovese, D.P. Andrew, L. Wu, and E.C. Butcher. 2001. Rules of chemokine receptor association with T cell polarization in vivo. J. Clin. Invest. 108:1331-1339.
42. Kim, Y.G., N. Kamada, M.H. Shaw, N. Warner, G.Y. Chen, L. Franchi, and G. Núñez. 2011. The Nod2 sensor promotes intestinal pathogen eradication via the chemokine CCL2-dependent recruitment of inflammatory monocytes. Immunity. 34:769-780. http://dx.doi.org/10.1016/j.immuni.2011.04.013
43. Kuziel, W.A., S.J. Morgan, T.C. Dawson, S. Griffin, O. Smithies, K. Ley, and N. Maeda. 1997. Severe reduction in leukocyte adhesion and monocyte extravasation in mice deficient in CC chemokine receptor 2. Proc. Natl. Acad. Sci. USA. 94:12053-12058. http://dx.doi.org/10.1073/pnas.94.22.12053
44. Langlet, C., S. Tamoutounour, S. Henri, H. Luche, L. Ardouin, C. Grégoire, B. Malissen, and M. Guilliams. 2012. CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J. Immunol. 188:1751-1760. http://dx.doi.org/10.4049/jimmunol.1102744
45. Lee, S.H., P.M. Starkey, and S. Gordon. 1985. Quantitative analysis of total macrophage content in adult mouse tissues. Immunochemical studies with monoclonal antibody F4/80. J. Exp. Med. 161:475-489. http://dx.doi.org/10.1084/jem.161.3.475
46. León, B., M. López-Bravo, and C. Ardavín. 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. http://dx.doi.org/10.1016/j.immuni.2007.01.017
47. Lewis, K.L., M.L. Caton, M. Bogunovic, M. Greter, L.T. Grajkowska, D. Ng, A. Klinakis, I.F. Charo, S. Jung, J.L. Gommerman, et al. 2011. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity. 35:780-791. http://dx.doi.org/10.1016/j.immuni.2011.08.013
48. Liu, K., and M.C. Nussenzweig. 2010. Origin and development of dendritic cells. Immunol. Rev. 234:45-54. http://dx.doi.org/10.1111/j.0105-2896.2009.00879.x
49. 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. http://dx.doi.org/10.1126/science.1171243
50. MacDonald, K.P., J.S. Palmer, S. Cronau, E. Seppanen, S. Olver, N.C. Raffelt, R. Kuns, A.R. Pettit, A. Clouston, B. Wainwright, et al. 2010. An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue- and tumor-associated macrophages but does not inhibit inflammation. Blood. 116:3955-3963. http://dx.doi.org/10.1182/blood-2010-02-266296
51. α- subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 189:587-592. http://dx.doi.org/10.1084/jem.189.3.587
52. Mangan, P.R., L.E. Harrington, D.B. O'Quinn, W.S. Helms, D.C. Bullard, C.O. Elson, R.D. Hatton, S.M. Wahl, T.R. Schoeb, and C.T. Weaver. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature. 441:231-234. http://dx.doi.org/10.1038/nature04754
53. 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, et al. 2000. Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood. 95:3489-3497.
54. Meredith, M.M., K. Liu, G. Darrasse-Jeze, A.O. Kamphorst, H.A. Schreiber, P. Guermonprez, J. Idoyaga, C. Cheong, K.H. Yao, R.E. Niec, and M.C. Nussenzweig. 2012. Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J. Exp. Med. 209:1153-1165. http://dx.doi.org/10.1084/jem.20112675
55. Miller, J.C., B.D. Brown, T. Shay, E.L. Gautier, V. Jojic, A. Cohain, G. Pandey, M. Leboeuf, K.G. Elpek, J. Helft, et al; Immunological Genome Consortium. 2012. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13:888-899. http://dx.doi.org/10.1038/ni.2370
56. Mundy, R., T.T. MacDonald, G. Dougan, G. Frankel, and S. Wiles. 2005. Citrobacter rodentium of mice and man. Cell. Microbiol. 7:1697-1706. http://dx.doi.org/10.1111/j.1462-5822.2005.00625.x
57. Murphy, K.M., W. Ouyang, J.D. Farrar, J. Yang, S. Ranganath, H. Asnagli, M. Afkarian, and T.L. Murphy. 2000. Signaling and transcription in T helper development. Annu. Rev. Immunol. 18:451-494. http://dx.doi.org/10.1146/annurev.immunol.18.1.451
58. 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. http://dx.doi.org/10.1038/ni.1707
59. Ota, N., K. Wong, P.A. Valdez, Y. Zheng, N.K. Crellin, L. Diehl, and W. Ouyang. 2011. IL-22 bridges the lymphotoxin pathway with the maintenance of colonic lymphoid structures during infection with Citrobacter rodentium. Nat. Immunol. 12:941-948. http://dx.doi.org/10.1038/ni.2089
60. Peters, W., J.G. Cyster, M. Mack, D. Schlöndorff, A.J. Wolf, J.D. Ernst, and I.F. Charo. 2004. CCR2-dependent trafficking of F4/80dim macrophages and CD11cdim/intermediate dendritic cells is crucial for T cell recruitment to lungs infected with Mycobacterium tuberculosis. J. Immunol. 172:7647-7653.
61. Reinhardt, R.L., S. Hong, S.J. Kang, Z.E. Wang, and R.M. Locksley. 2006. Visualization of IL-12/23p40 in vivo reveals immunostimulatory dendritic cell migrants that promote Th1 differentiation. J. Immunol. 177:1618-1627.
62. Reis e Sousa, C., S. Hieny, T. Scharton-Kersten, D. Jankovic, H. Charest, R.N. Germain, and A. Sher. 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. 186:1819-1829. http://dx.doi.org/10.1084/jem.186.11.1819
63. Rivollier, A., J. He, A. Kole, V. Valatas, and B.L. Kelsall. 2012. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J. Exp. Med. 209:139-155. http://dx.doi.org/10.1084/jem.20101387
64. Satoh-Takayama, N., C.A. Vosshenrich, S. Lesjean-Pottier, S. Sawa, M. Lochner, F. Rattis, J.J. Mention, K. Thiam, N. Cerf-Bensussan, O. Mandelboim, et al. 2008. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity. 29:958-970. http://dx.doi.org/10.1016/j.immuni.2008.11.001
65. +, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J. Exp. Med. 206:3101-3114. http://dx.doi.org/10.1084/jem.20091925
66. Schulz, C., E. Gomez Perdiguero, L. Chorro, H. Szabo-Rogers, N. Cagnard, K. Kierdorf, M. Prinz, B. Wu, S.E. Jacobsen, J.W. Pollard, et al. 2012. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science. 336:86-90. http://dx.doi.org/10.1126/science.1219179
67. 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. http://dx.doi.org/10.1038/ni1309
68. Serbina, N.V., T.P. Salazar-Mather, C.A. Biron, W.A. Kuziel, and E.G. Pamer. 2003. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity. 19:59-70. http://dx.doi.org/10.1016/S1074-7613(03)00171-7
69. 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. http://dx.doi.org/10.1146/annurev.immunol.26.021607.090326
70. Shortman, K., and S.H. Naik. 2007. Steady-state and inflammatory dendriticcell development. Nat. Rev. Immunol. 7:19-30. http://dx.doi.org/10.1038/nri1996
71. Simmons, C.P., N.S. Goncalves, M. Ghaem-Maghami, M. Bajaj-Elliott, S. Clare, B. Neves, G. Frankel, G. Dougan, and T.T. MacDonald. 2002. Impaired resistance and enhanced pathology during infection with a noninvasive, attaching-effacing enteric bacterial pathogen, Citrobacter rodentium, in mice lacking IL-12 or IFN-γ. J. Immunol. 168:1804-1812.
72. Sonnenberg, G.F., L.A. Monticelli, M.M. Elloso, L.A. Fouser, and D. Artis. 2011. CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity. 34:122-134. http://dx.doi.org/10.1016/j.immuni.2010.12.009
73. Steinman, R.M., D. Hawiger, and M.C. Nussenzweig. 2003. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21:685-711. http://dx.doi.org/10.1146/annurev.immunol.21.120601.141040
74. Tamoutounour, S., S. Henri, H. Lelouard, B. de Bovis, C. de Haar, C.J. van der Woude, A.M. Woltman, Y. Reyal, D. Bonnet, D. Sichien, et al. 2012. CD64 distinguishes macrophages from dendritic cells in the gut and reveals the Th1-inducing role of mesenteric lymph node macrophages during colitis. Eur. J. Immunol. 42:3150-3166. http://dx.doi.org/10.1002/eji.201242847
75. 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. http://dx.doi.org/10.1172/JCI29919
76. Tumanov, A.V., E.P. Koroleva, X. Guo, Y. Wang, A. Kruglov, S. Nedospasov, and Y.X. Fu. 2011. Lymphotoxin controls the IL-22 protection pathway in gut innate lymphoid cells during mucosal pathogen challenge. Cell Host Microbe. 10:44-53. http://dx.doi.org/10.1016/j.chom.2011.06.002
77. Uematsu, S., K. Fujimoto, M.H. Jang, B.G. Yang, Y.J. Jung, M. Nishiyama, S. Sato, T. Tsujimura, M. Yamamoto, Y. Yokota, et al. 2008. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9:769-776. http://dx.doi.org/10.1038/ni.1622
78. 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. http://dx.doi.org/10.1084/jem.20061011
79. Varol, C., A. Vallon-Eberhard, E. Elinav, T. Aychek, Y. Shapira, H. Luche, H.J. Fehling, W.D. Hardt, G. Shakhar, and S. Jung. 2009. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity. 31:502-512. http://dx.doi.org/10.1016/j.immuni.2009.06.025
80. Varol, C., E. Zigmond, and S. Jung. 2010. Securing the immune tightrope: mononuclear phagocytes in the intestinal lamina propria. Nat. Rev. Immunol. 10:415-426. http://dx.doi.org/10.1038/nri2778
81. Waskow, C., K. Liu, G. Darrasse-Jèze, 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. http://dx.doi.org/10.1038/ni.1615
82. Wiktor-Jedrzejczak, W., A. Bartocci, A.W. Ferrante Jr., A. Ahmed-Ansari, K.W. Sell, J.W. Pollard, and E.R. Stanley. 1990. Total absence of colonystimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc. Natl. Acad. Sci. USA. 87:4828-4832. http://dx.doi.org/10.1073/pnas.87.12.4828
83. Witmer-Pack, M.D., D.A. Hughes, G. Schuler, L. Lawson, A. McWilliam, K. Inaba, R.M. Steinman, and S. Gordon. 1993. Identification of macrophages and dendritic cells in the osteopetrotic (op/op) mouse. J. Cell Sci. 104:1021-1029.
84. Worbs, T., U. Bode, S. Yan, M.W. Hoffmann, G. Hintzen, G. Bernhardt, R. Förster, and O. Pabst. 2006. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J. Exp. Med. 203:519-527. http://dx.doi.org/10.1084/jem.20052016
85. Yona, S., and S. Jung. 2010. Monocytes: subsets, origins, fates and functions. Curr. Opin. Hematol. 17:53-59. http://dx.doi.org/10.1097/MOH.0b013e3283324f80
86. Yona, S., K.W. Kim, Y. Wolf, A. Mildner, D. Varol, M. Breker, D. Strauss-Ayali, S. Viukov, M. Guilliams, A. Misharin, et al. 2013. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity. 38:79-91. http://dx.doi.org/10.1016/j.immuni.2012.12.001
87. + T cells equipped for rapid recall response. J. Immunol. 185:6646-6663. http://dx.doi.org/10.4049/jimmunol.0904156
88. Zheng, Y., P.A. Valdez, D.M. Danilenko, Y. Hu, S.M. Sa, Q. Gong, A.R. Abbas, Z. Modrusan, N. Ghilardi, F.J. de Sauvage, and W. Ouyang. 2008. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14:282-289. http://dx.doi.org/10.1038/nm1720
89. Zigmond, E., C. Varol, J. Farache, E. Elmaliah, A.T. Satpathy, G. Friedlander, M. Mack, N. Shpigel, I.G. Boneca, K.M. Murphy, et al. 2012. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity. 37:1076-1090. http://dx.doi.org/10.1016/j.immuni.2012.08.026