Abstract
Abstract The existence of dendritic cell (DC) subsets is firmly established, but their trafficking properties are virtually unknown. In this study, we show that myeloid (M-DCs) and plasmacytoid (P-DCs) DCs isolated from human blood differ widely in the capacity to migrate to chemotactic stimuli. The pattern of chemokine receptors expressed by blood M-DCs and P-DCs, with the exception of CCR7, is similar. However, most chemokine receptors of P-DCs, in particular those specific for inflammatory chemokines and classical chemotactic agonists, are not functional in circulating cells. Following maturation induced by CD40 ligation, the receptors for inflammatory chemokines are down-regulated, and CCR7 on P-DCs becomes coupled to migration. The drastically impaired capacity of blood P-DCs to migrate in response to inflammatory chemotactic signals contrasts with the response to lymph node-homing chemokines, indicating a propensity to migrate to secondary lymphoid organs rather than to sites of inflammation.
References
35
Referenced
247
-
Banchereau, J., R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245
(
10.1038/32588
) -
Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18: 767
(
10.1146/annurev.immunol.18.1.767
) -
Reid, S. D., G. Penna, L. Adorini. 2000. The control of T cell responses by dendritic cell subsets. Curr. Opin. Immunol. 12: 114
(
10.1016/S0952-7915(99)00059-X
) -
Vremec, D., M. Zorbas, R. Scollay, D. J. Saunders, C. F. Ardavin, L. Wu, K. Shortman. 1992. The surface phenotype of dendritic cells purified from mouse thymus and spleen: investigation of the CD8 expression by a subpopulation of dendritic cells. J. Exp. Med. 176: 47
(
10.1084/jem.176.1.47
) -
Shortman, K., L. Wu. 1996. Early T lymphocyte progenitors. Annu. Rev. Immunol. 14: 29
(
10.1146/annurev.immunol.14.1.29
) - O’Doherty, U., M. Peng, S. Gezelter, W. J. Swiggard, M. Betjes, N. Bhardwaj, R. M. Steinman. 1994. Human blood contains two subsets of dendritic cells, one immunologically mature and the other immature. Immunology 82: 487
-
Banchereau, J., B. Pulendran, R. Steinman, K. Palucka. 2000. Will the making of plasmacytoid dendritic cells in vitro help unravel their mysteries?. J. Exp. Med. 192: 39
(
10.1084/jem.192.12.F39
) -
Olweus, J., A. BitMansour, R. Warnke, P. A. Thompson, J. Carballido, L. J. Picker, F. Lund-Johansen. 1997. Dendritic cell ontogeny: a human dendritic cell lineage of myeloid origin. Proc. Natl. Acad. Sci. USA 94: 12551
(
10.1073/pnas.94.23.12551
) -
Grouard, G., M. C. Rissoan, L. Filgueira, I. Durand, J. Banchereau, Y. J. Liu. 1997. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J. Exp. Med. 185: 1101
(
10.1084/jem.185.6.1101
) -
Cella, M., D. Jarrossay, F. Facchetti, O. Alebardi, H. Nakajima, A. Lanzavecchia, M. Colonna. 1999. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat. Med. 5: 919
(
10.1038/11360
) -
Rissoan, M. C., V. Soumelis, N. Kadowaki, G. Grouard, F. Briere, R. de Waal Malefyt, Y. J. Liu. 1999. Reciprocal control of T helper cell and dendritic cell differentiation. Science 283: 1183
(
10.1126/science.283.5405.1183
) -
Siegal, F. P., N. Kadowaki, M. Shodell, P. A. Fitzgerald-Bocarsly, K. Shah, S. Ho, S. Antonenko, Y. J. Liu. 1999. The nature of the principal type 1 interferon-producing cells in human blood. Science 284: 1835
(
10.1126/science.284.5421.1835
) -
Facchetti, F., C. De Wolf-Peeters, J. J. van den Oord, R. De vos, V. J. Desmet. 1988. Plasmacytoid T cells: a cell population normally present in the reactive lymph node. An immunohistochemical and electron microscopic study. Hum. Pathol. 19: 1085
(
10.1016/S0046-8177(88)80091-1
) -
Dzionek, A., A. Fuchs, P. Schmidt, S. Cremer, M. Zysk, S. Miltenyi, D. W. Buck, J. Schmitz. 2000. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J. Immunol. 165: 6037
(
10.4049/jimmunol.165.11.6037
) -
Penna, G., L. Adorini. 2000. 1α,25-dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J. Immunol. 164: 2405
(
10.4049/jimmunol.164.5.2405
) -
Nakajima, H., J. Samaridis, L. Angman, M. Colonna. 1999. Human myeloid cells express an activating ILT receptor (ILT1) that associates with Fc receptor γ-chain. J. Immunol. 162: 5
(
10.4049/jimmunol.162.1.5
) -
Zlotnik, A., O. Yoshie. 2000. Chemokines: a new classification system and their role in immunity. Immunity 12: 121
(
10.1016/S1074-7613(00)80165-X
) -
Dieu-Nosjean, M. C., C. Massacrier, B. Homey, B. Vanbervliet, J. J. Pin, A. Vicari, S. Lebecque, C. Dezutter-Dambuyant, D. Schmitt, A. Zlotnik, C. Caux. 2000. Macrophage inflammatory protein 3α is expressed at inflamed epithelial surfaces and is the most potent chemokine known in attracting Langerhans cell precursors. J. Exp. Med. 192: 705
(
10.1084/jem.192.5.705
) -
Sozzani, S., P. Allavena, G. D’Amico, W. Luini, G. Bianchi, M. Kataura, T. Imai, O. Yoshie, R. Bonecchi, A. Mantovani. 1998. Differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties. J. Immunol. 161: 1083
(
10.4049/jimmunol.161.3.1083
) -
Dieu, M. C., B. Vanbervliet, A. Vicari, J. M. Bridon, E. Oldham, S. Ait-Yahia, F. Briere, A. Zlotnik, S. Lebecque, C. Caux. 1998. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J. Exp. Med. 188: 373
(
10.1084/jem.188.2.373
) -
Lin, C. L., R. M. Suri, R. A. Rahdon, J. M. Austyn, J. A. Roake. 1998. Dendritic cell chemotaxis and transendothelial migration are induced by distinct chemokines and are regulated on maturation. Eur. J. Immunol. 28: 4114
(
10.1002/(SICI)1521-4141(199812)28:12<4114::AID-IMMU4114>3.0.CO;2-C
) -
Muller, A., B. Homey, H. Soto, N. Ge, D. Catron, M. E. Buchanan, T. McClanahan, E. Murphy, W. Yuan, S. N. Wagner, et al 2001. Involvement of chemokine receptors in breast cancer metastasis. Nature 410: 50
(
10.1038/35065016
) -
Gretz, J. E., C. C. Norbury, A. O. Anderson, A. E. Proudfoot, S. Shaw. 2000. Lymph-borne chemokines and other low molecular weight molecules reach high endothelial venules via specialized conduits while a functional barrier limits access to the lymphocyte microenvironments in lymph node cortex. J. Exp. Med. 192: 1425
(
10.1084/jem.192.10.1425
) -
Randolph, G. J., K. Inaba, D. F. Robbiani, R. M. Steinman, W. A. Muller. 1999. Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 11: 753
(
10.1016/S1074-7613(00)80149-1
) -
Bleul, C. C., J. L. Schultze, T. A. Springer. 1998. B lymphocyte chemotaxis regulated in association with microanatomic localization, differentiation state, and B cell receptor engagement. J. Exp. Med. 187: 753
(
10.1084/jem.187.5.753
) -
Liao, F., R. L. Rabin, C. S. Smith, G. Sharma, T. B. Nutman, J. M. Farber. 1999. CC-chemokine receptor 6 is expressed on diverse memory subsets of T cells and determines responsiveness to macrophage inflammatory protein 3α. J. Immunol. 162: 186
(
10.4049/jimmunol.162.1.186
) -
Bonecchi, R., F. Facchetti, S. Dusi, W. Luini, D. Lissandrini, M. Simmelink, M. Locati, S. Bernasconi, P. Allavena, E. Brandt, et al 2000. Induction of functional IL-8 receptors by IL-4 and IL-13 in human monocytes. J. Immunol. 164: 3862
(
10.4049/jimmunol.164.7.3862
) -
Sozzani, S., W. Luini, A. Borsatti, N. Polentarutti, D. Zhou, L. Piemonti, G. D’Amico, C. A. Power, T. N. Wells, M. Gobbi, et al 1997. Receptor expression and responsiveness of human dendritic cells to a defined set of CC and CXC chemokines. J. Immunol. 159: 1993
(
10.4049/jimmunol.159.4.1993
) -
D’Amico, G., G. Frascaroli, G. Bianchi, P. Transidico, A. Doni, A. Vecchi, S. Sozzani, P. Allavena, A. Mantovani. 2000. Uncoupling of inflammatory chemokine receptors by IL-10: generation of functional decoys. Nat. Immunol. 1: 387
(
10.1038/80819
) -
Sallusto, F., P. Schaerli, P. Loetscher, C. Schaniel, D. Lenig, C. R. Mackay, S. Qin, A. Lanzavecchia. 1998. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur. J. Immunol. 28: 2760
(
10.1002/(SICI)1521-4141(199809)28:09<2760::AID-IMMU2760>3.0.CO;2-N
) -
Thoma-Uszynski, S., S. M. Kiertscher, M. T. Ochoa, D. A. Bouis, M. V. Norgard, K. Miyake, P. J. Godowski, M. D. Roth, R. L. Modlin. 2000. Activation of Toll-like receptor 2 on human dendritic cells triggers induction of IL-12, but not IL-10. J. Immunol. 165: 3804
(
10.4049/jimmunol.165.7.3804
) -
Kadowaki, N., S. Antonenko, J. Y. Lau, Y. J. Liu. 2000. Natural interferon α/β-producing cells link innate and adaptive immunity. J. Exp. Med. 192: 219
(
10.1084/jem.192.2.219
) -
Jahnsen, F. L., F. Lund-Johansen, J. F. Dunne, L. Farkas, R. Haye, P. Brandtzaeg. 2000. Experimentally induced recruitment of plasmacytoid (CD123high) dendritic cells in human nasal allergy. J. Immunol. 165: 4062
(
10.4049/jimmunol.165.7.4062
) -
Cella, M., M. Salio, Y. Sakakibara, H. Langen, I. Julkunen, A. Lanzavecchia. 1999. Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J. Exp. Med. 189: 821
(
10.1084/jem.189.5.821
) -
Roncarolo, M. G., M. K. Levings, C. Traversari. 2001. Differentiation of T regulatory cells by immature dendritic cells. J. Exp. Med. 193: F5
(
10.1084/jem.193.2.F5
)
@article{Penna_2001, title={Cutting Edge: Selective Usage of Chemokine Receptors by Plasmacytoid Dendritic Cells}, volume={167}, ISSN={1550-6606}, url={http://dx.doi.org/10.4049/jimmunol.167.4.1862}, DOI={10.4049/jimmunol.167.4.1862}, number={4}, journal={The Journal of Immunology}, publisher={Oxford University Press (OUP)}, author={Penna, Giuseppe and Sozzani, Silvano and Adorini, Luciano}, year={2001}, month=aug, pages={1862–1866} }