Lymph-migrating, tissue-derived dendritic cells are minor constituents within steady-state lymph nodes

Journal of Experimental Medicine

Volumn 205, Issue 12, 2008, Pages 2839-2850

  Jakubzick, Claudia ^a   Bogunovic, Milena ^a   Bonito, Anthony J ^a   Kuan, Emma L ^a   Merad, Miriam ^a   Randolph, Gwendalyn J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOZYME; GREEN FLUORESCENT PROTEIN; LYSOZYME M, MOUSE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL POPULATION; CELL STIMULATION; CONTROLLED STUDY; DENDRITIC CELL; HOMEOSTASIS; LYMPH NODE CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEADY STATE; ANIMAL; C57BL MOUSE; CELL MOTION; CYTOLOGY; GENETICS; IMMUNOLOGY; INFLAMMATION; LUNG; LYMPH NODE; LYMPH VESSEL; MACROPHAGE; METABOLISM; REPORTER GENE; SPLEEN; TRANSGENIC MOUSE;

ANIMALS; CELL MOVEMENT; DENDRITIC CELLS; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HOMEOSTASIS; INFLAMMATION; LUNG; LYMPH NODES; LYMPHATIC VESSELS; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MURAMIDASE; SPLEEN;

EID: 58149280443     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20081430     Document Type: Article

References (60)

1. Pugh, C.W., G.G. MacPherson, and H.W. Steer. 1983. Characterization of nonlymphoid cells derived from rat peripheral lymph. J. Exp. Med. 157:1758-1779.
2. Mackay, C.R., W.L. Marston, and L. Dudler. 1990. Naive and memory T cells show distinct pathways of lymphocyte recirculation. J. Exp. Med. 171:801-817.
3. Randolph, G.J., V. Angeli, and M.A. Swartz. 2005. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 5:617-628.
4. Steinman, R.M. 1991. The dendritic cell system and its role in immuno- genicity. Annu. Rev. Immunol. 9:271-296.
5. MacPherson, G.G., C.D. Jenkins, M.J. Stein, and C. Edwards. 1995. Endotoxin-mediated dendritic cell release from the intestine. Characterization of released dendritic cells and TNF dependence. J. Immunol. 154:1317-1322.
6. Kupiec-Weglinski, J.W., J.M. Austyn, and P.J. Morris. 1988. Migration patterns of dendritic cells in the mouse. Traffic from the blood, and T cell-dependent and-independent entry to lymphoid tissues. J. Exp. Med. 167:632-645.
7. 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.
8. Huang, F.P., N. Platt, M. Wykes, J.R. Major, T.J. Powell, C.D. Jenkins, and G.G. MacPherson. 2000. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J. Exp. Med. 191:435-444.
9. Hemmi, H., M. Yoshino, H. Yamazaki, M. Naito, T. Iyoda, Y. Omatsu, S. Shimoyama, J.J. Letterio, T. Nakabayashi, H. Tagaya, et al. 2001. Skin antigens in the steady state are trafficked to regional lymph nodes by transforming growth factor-beta1-dependent cells. Int. Immunol. 13:695-704.
10. Scheinecker, C., R. McHugh, E.M. Shevach, and R.N. Germain. 2002. Constitutive presentation of a natural tissue autoantigen exclusively by dendritic cells in the draining lymph node. J. Exp. Med. 196:1079-1090.
11. Kurts, C., H. Kosaka, F.R. Carbone, J.F. Miller, and W.R. Heath. 1997. Class I-restricted cross-presentation of exogenous self-antigens leads to deletion of autoreactive CD8+ T cells. J. Exp. Med. 186:239-245.
12. Lee, J.W., M. Epardaud, J. Sun, J.E. Becker, A.C. Cheng, A.R. Yonekura, J.K. Heath, and S.J. Turley. 2007. Peripheral antigen display by lymph node stroma promotes T cell tolerance to intestinal self. Nat. Immunol. 8:181-190.
13. Cella, M., D. J arrossay, F. Facchetti, O. Alebardi, H. Nakajima, A. Lanzavecchia, and M. Colonna. 1999. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I inter-feron. Nat. Med. 5:919-923.
14. Diacovo, T.G., A.L. Blasius, T.W. Mak, M. Cella, and M. Colonna. 2005. Adhesive mechanisms governing interferon-producing cell recruitment into lymph nodes. J. Exp. Med. 202:687-696.
15. 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.
16. Randolph, G.J., J. Ochando, and S. Partida-Sanchez. 2008. Migration of dendritic cells and their precursors. Annu. Rev. Immunol. 26:293-316.
17. Villadangos, J.A., and P. Schnorrer. 2007. Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol. 7:543-555.
18. Ohl, L., M. Mohaupt, N. Czeloth, G. Hintzen, Z. Kiafard, J. Zwirner, T. Blankenstein, G. Henning, and R. Forster. 2004. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity. 21:279-288.
19. Wilson, N.S., L.J. Young, F. Kupresanin, S.H. Naik, D. Vremec, W.R. Heath, S. Akira, K. Shortman, J. Boyle, E. Maraskovsky, et al. 2008. Normal proportion and expression of maturation markers in migratory dendritic cells in the absence of germs or Toll-like receptor signaling. Immunol. Cell Biol. 86:200-205.
20. 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.
21. 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.
22. 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.
23. 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.
24. 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.
25. 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.
26. Onai, N., A. Obata-Onai, M.A. Schmid, T. Ohteki, D. Jarrossay, and M.G. Manz. 2007. Identification of clonogenic common Flt3+M- CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat. Immunol. 8:1207-1216.
27. 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.
28. Landsman, L., C. Varol, and S.Jung. 2007. Distinct differentiation potential of blood monocyte subsets in the lung. J. Immunol. 178:2000-2007.
29. Clausen, B.E., C. Burkhardt, W. Reith, R. Renkawitz, and I. Forster. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8:265-277.
30. Mao, X., Y. Fujiwara, A. Chapdelaine, H. Yang, and S.H. Orkin. 2001. Activation of EGFP expression by Cre-mediated excision in a new ROSA26 reporter mouse strain. Blood. 97:324-326.
31. Ye, M., H. Iwasaki, C.V. Laiosa, M. Stadtfeld, H. Xie, S. Heck, B. Clausen, K. Akashi, and T. Graf. 2003. Hematopoietic stem cells expressing the myeloid lysozyme gene retain long-term, multilineage re- population potential. Immunity. 19:689-699.
32. Geissmann, F., S. Jung, and D.R. Littman. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 19:71-82.
33. 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.
34. Qu, C., E.W. Edwards, F. Tacke, V. Angeli, J. Llodra, G. Sanchez-Schmitz, A. Garin, N.S. Haque, W. Peters, N. van Rooijen, et al. 2004. Role of CCR8 and other chemokine pathways in the migration of monocyte- derived dendritic cells to lymph nodes. J. Exp. Med. 200:1231-1241.
35. Zong, H., J.S. Espinosa, H.H. Su, M.D. Muzumdar, and L. Luo. 2005. Mosaic analysis with double markers in mice. Cell. 121:479-492.
36. Tacke, F., F. Ginhoux, C. Jakubzick, N. van Rooijen, M. Merad, and G.J. Randolph. 2006. Immature monocytes acquire antigens from other cells in the bone marrow and present them to T cells after maturing in the periphery. J. Exp. Med. 203:583-597.
37. 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.
38. Bogunovic, M., F. Ginhoux, A. Wagers, M. Loubeau, L.M. Isola, L. Lubrano, V. Najfeld, R.G. Phelps, C. Grosskreutz, E. Scigliano, et al. 2006. Identification of a radio-resistant and cycling dermal dendritic cell population in mice and men. J. Exp. Med. 203:2627-2638.
39. Sung, S.S., S.M. Fu, C.E. Rose Jr., F. Gaskin, S.T. Ju, and S.R. Beaty. 2006. A major lung CD103 (alphaE)-beta 7 integrin-positive epithelial dendritic cell population expressing langerin and tight junction proteins. J. Immunol. 176:2161-2172.
40. Jakubzick, C., J. Helft, T.J. Kaplan, and G.J. Randolph. 2008. Optimization of methods to study pulmonary dendritic cell migration reveals distinct capacities of DC subsets to acquire soluble versus par- ticulate antigen. J. Immunol. Methods. 337:121-131.
41. Johansson, C., and B.L. Kelsall. 2005. Phenotype and function of intestinal dendritic cells. Semin. Immunol. 17:284-294.
42. Ginhoux, F., M.P. Collin, M. Bogunovic, M. Abel, M. Leboeuf, J. Helft, J. Ochando, A. Kissenpfennig, B. Malissen, M. Grisotto, et al. 2007. Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J. Exp. Med. 204:3133-3146.
43. Henri, S., D. Vremec, A. Kamath, J. Waithman, S. Williams, C. Benoist, K. Burnham, S. Saeland, E. Handman, and K. Shortman. 2001. The dendritic cell populations of mouse lymph nodes. J. Immunol. 167:741-748.
44. Macatonia, S.E., A.J. Edwards, and S.C. Knight. 1986. Dendritic cells and the initiation of contact sensitivity to fluorescein isothiocyanate. Immunology. 59:509-514.
45. Kissenpfennig, A., S. Henri, B. Dubois, C. Laplace-Builhe, P. Perrin, N. Romani, C.H. Tripp, P. Douillard, L. Leserman, D. Kaiserlian, et al. 2005. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity. 22:643-654.
46. + T cells. J. Immunol. 178:6861-6866.
47. Roake, J.A., A.S. Rao, P.J. Morris, C.P. Larsen, D.F. Hankins, and J.M. Austyn. 1995. Dendritic cell loss from nonlymphoid tissues after systemic administration of lipopolysaccharide, tumor necrosis factor, and interleukin 1. J. Exp. Med. 181:2237-2247.
48. Cumberbatch, M., R.J. Dearman, and I. Kimber. 1997. Langerhans cells require signals from both tumour necrosis factor-alpha and interleukin-1 beta for migration. Immunology. 92:388-395.
49. Wang, B., H. Fujisawa, L. Zhuang, S. Kondo, G.M. Shivji, C.S. Kim, T.W. Mak, and D.N. Sauder. 1997. Depressed Langerhans cell migration and reduced contact hypersensitivity response in mice lacking TNF receptor p75. J. Immunol. 159:6148-6155.
50. Mebius, R.E., P.R. Streeter, J. Breve, A.M. Duijvestijn, and G. Kraal. 1991. The influence of afferent lymphatic vessel interruption on vascular addressin expression. J. Cell Biol. 115:85-95.
51. Barker, C.F., and R.E. Billingham. 1968. The role of afferent lymphatics in the rejection of skin homografts. J. Exp. Med. 128:197-221.
52. 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, et al. 2005. CX3CR1- mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science. 307:254-258.
53. Garg, S., A. Oran, J. Wajchman, S. Sasaki, C.H. Maris, J.A. Kapp, and J. J acob. 2003. Genetic tagging shows increased frequency and longevity of antigen-presenting, skin-derived dendritic cells in vivo. Nat. Immunol. 4:907-912.
54. Hon, H., E.B. Rucker III, L. Hennighausen, and J. Jacob. 2004. bcl-xL is critical for dendritic cell survival in vivo. J. Immunol. 173:4425-4432.
55. I naba, K., S. Turley, F. Yamaide, T. Iyoda, K. Mahnke, M. Inaba, M. Pack, M. Subklewe, B. Sauter, D. Sheff, et al. 1998. Efficient presentation of phagocytosed cellular fragments on the major histo- compatibility complex class II products of dendritic cells. J. Exp. Med. 188:2163-2173.
56. Allan, R.S., J. Waithman, S. Bedoui, C.M. J ones, 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.
57. Tacke, F., D. Alvarez, T.J. Kaplan, C. Jakubzick, R. Spanbroek, J. Llodra, A. Garin, J. Liu, M. Mack, N. van Rooijen, et al. 2007. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Invest. 117:185-194.
58. 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 cell-associated antigens. Immunity. 17:211-220.
59. Massberg, S., P. Schaerli, I. Knezevic-Maramica, M. Kollnberger, N. Tubo, E.A. Moseman, I.V. Huff, T. Junt, A.J. Wagers, I.B. Mazo, and U.H. von Andrian. 2007. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell. 131:994-1008.
60. Robbiani, D.F., R.A. Finch, D. J ager, W.A. Muller, A.C. Sartorelli, and G.J. Randolph. 2000. The leukotriene C(4) transporter MRP1 regulates CCL19 (MIP-3beta, ELC)-dependent mobilization of dendritic cells to lymph nodes. Cell. 103:757-768.