Regulatory T cells and tolerogenic dendritic cells: from basic biology to clinical applications
Abstract
The induction of antigen (Ag)-specific tolerance is critical for the prevention of autoimmunity and maintenance of immune homeostasis. Recently, attention has been focused on induction of active suppression by regulatory T cells (Treg cells). Also, a role for dendritic cells (DCs) in the promotion of peripheral tolerance has been demonstrated by several studies and is the subject of intensive investigation. It is currently believed that the maturation/activation state of DCs might be a control point for the induction of peripheral tolerance through modifications of the activation state of T cells. Several lines of experimental evidence suggest that unique DC subsets or discrete functional states of the DCs might be devoted to the promotion of Treg cell differentiation. The present review summarizes the emerging literature on the developmental origin and function of human Treg cells and tolerogenic/regulatory DCs. Furthermore, clinical implications of these studies for cellular therapy of immune-mediated pathologies are discussed.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Glucocorticoids can convert dendritic cells to tolerogenic cells that promote regulatory T cell production, and this effect relies on glucocorticoid-mediated expression of GILZ.
“GCs can also convert DCs to tolerogenic cells, which promote the production of regulatory T cells (38, 39). This immunosuppressive effect critically relies on the GC-mediated expression of glucocorticoid-induce leucine zipper (GILZ), since this transcription factor appears as both necessary and sufficient for the induction of a tolerogenic state (40, 41).”
From The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [39]
Cites
Sallusto, F., & Lanzavecchia, A. (1994) · The Journal of Experimental Medicine · doi:10.1084/jem.179.4.1109 · Cited by 5,129 · see citing works
Chen, W., Jin, W., Hardegen, N. J., Lei, K.-J., Li, L., Marinos, N. J., McGrady, G., & Wahl, S. M. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20030152 · Cited by 4,678 · see citing works
A CD4+T-cell subset inhibits antigen-specific T-cell responses and prevents colitis
Groux, H., O’Garra, A., Bigler, M., Rouleau, M., Antonenko, S. V., de Vries, J. E., & Roncarolo, M. G. (1997) · Nature · doi:10.1038/39614 · Cited by 3,588 · see citing works
Steinman, R. M., Hawiger, D., & Nussenzweig, M. C. (2003) · Annual Review of Immunology · doi:10.1146/annurev.immunol.21.120601.141040 · Cited by 3,124 · see citing works
Brunkow, M. E., Jeffery, E. W., Hjerrild, K. A., Paeper, B. W., Clark, L. B., Yasayko, S.-A., Wilkinson, J. E., Galas, D. J., Ziegler, S. F., & Ramsdell, F. (2001) · Nature Genetics · doi:10.1038/83784 · Cited by 2,628 · see citing works
The Nature of the Principal Type 1 Interferon-Producing Cells in Human Blood
Siegal, F. P., Kadowaki, N., Shodell, M., Fitzgerald-Bocarsly, P. A., Shah, K., Ho, S., Antonenko, S., & Liu, Y.-J. (1999) · Science · doi:10.1126/science.284.5421.1835 · Cited by 2,293 · see citing works
CD4+CD25+ suppressor T cells: more questions than answers
Shevach, E. M. (2002) · Nature reviews. Immunology · doi:10.1038/nri821 · Cited by 2,097 · see citing works
Kadowaki, N., Ho, S., Antonenko, S., de Waal Malefyt, R., Kastelein, R. A., Bazan, F., & Liu, Y.-J. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.194.6.863 · Cited by 1,964 · see citing works
Loss of Functional Suppression by CD4+CD25+ Regulatory T Cells in Patients with Multiple Sclerosis
Viglietta, V., Baecher‐Allan, C., Weiner, H. L., & Hafler, D. A. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20031579 · Cited by 1,858 · see citing works
Reciprocal Control of T Helper Cell and Dendritic Cell Differentiation
Rissoan, M., Soumelis, V., Kadowaki, N., Grouard, G., Brière, F., Malefyt, R. D. W., & Liu, Y.-J. (1999) · Science · doi:10.1126/science.283.5405.1183 · Cited by 1,835 · see citing works
Sakaguchi, S. (2000) · Cell · doi:10.1016/s0092-8674(00)80856-9 · Cited by 1,812 · see citing works
Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance
Shimizu, J., Yamazaki, S., Takahashi, T., Ishida, Y., & Sakaguchi, S. (2002) · Nature Immunology · doi:10.1038/ni759 · Cited by 1,729 · see citing works
Regulatory T cells mediate maternal tolerance to the fetus
Aluvihare, V. R., Kallikourdis, M., & Betz, A. G. (2004) · Nature Immunology · doi:10.1038/ni1037 · Cited by 1,661 · see citing works
Nakamura, K., Kitani, A., & Strober, W. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.194.5.629 · Cited by 1,596 · see citing works
GM-CSF and TNF-α cooperate in the generation of dendritic Langerhans cells
Caux, C., Dezutter‐Dambuyant, C., Schmitt, D., & Banchereau, J. (1992) · Nature · doi:10.1038/360258a0 · Cited by 1,551 · see citing works
Jonuleit, H., Schmitt, E., Schuler, G., Knop, J., & Enk, A. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.9.1213 · Cited by 1,538 · see citing works
Dendritic Cells: Unique Leukocyte Populations Which Control the Primary Immune Response
Hart, D. N. J. (1997) · Blood · doi:10.1182/blood.v90.9.3245 · Cited by 1,513 · see citing works
Shimizu, J., Yamazaki, S., & Sakaguchi, S. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.10.5211 · Cited by 1,491 · see citing works
Liyanage, U. K., Moore, T. T., Joo, H., Tanaka, Y., Herrmann, V. M., Doherty, G. M., Drebin, J. A., Strasberg, S. M., Eberlein, T. J., Goedegebuure, P. S., et al. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.5.2756 · Cited by 1,466 · see citing works
Dzionek, A., Fuchs, A., Schmidt, P., Cremer, S., Zysk, M., Miltenyi, S., Buck, D., & Schmitz, J. (2000) · Journal of Immunology · doi:10.4049/jimmunol.165.11.6037 · Cited by 1,433 · see citing works
Modulation of tryptophan catabolism by regulatory T cells
Fallarino, F., Grohmann, U., Hwang, K. W., Orabona, C., Vacca, C., Bianchi, R., Belladonna, M. L., Fioretti, M. C., Alegre, M., & Puccetti, P. (2003) · Nature Immunology · doi:10.1038/ni1003 · Cited by 1,375 · see citing works
Dhodapkar, M. V., Steinman, R. M., Krasovsky, J., Münz, C., & Bhardwaj, N. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.2.233 · Cited by 1,359 · see citing works
Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity?
Lutz, M. B., & Schuler, G. (2002) · Trends in Immunology · doi:10.1016/s1471-4906(02)02281-0 · Cited by 1,349 · see citing works
Regulatory T cells in transplantation tolerance
Wood, K. J., & Sakaguchi, S. (2003) · Nature reviews. Immunology · doi:10.1038/nri1027 · Cited by 1,318 · see citing works
Bonifaz, L. C., Bonnyay, D., Mahnke, K., Rivera, M. N., Nussenzweig, M. C., & Steinman, R. M. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20021598 · Cited by 1,306 · see citing works
Edinger, M., Hoffmann, P., Ermann, J., Drago, K., Fathman, C. G., Strober, S., & Negrin, R. S. (2003) · Nature Medicine · doi:10.1038/nm915 · Cited by 1,286 · see citing works
Jonuleit, H., Schmitt, E., Stassen, M., Tuettenberg, A., Knop, J., & Enk, A. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.11.1285 · Cited by 1,255 · see citing works
Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25– T cells
Walker, M., Kasprowicz, D. J., Gersuk, V. H., Bénard, A., Landeghen, M. V., Buckner, J. H., & Ziegler, S. F. (2003) · Journal of Clinical Investigation · doi:10.1172/jci19441 · Cited by 1,242 · see citing works
Akbari, O., DeKruyff, R. H., & Umetsu, D. T. (2001) · Nature Immunology · doi:10.1038/90667 · Cited by 1,196 · see citing works
Grouard, G., Rissoan, M., Filgueira, L., Durand, I., Banchereau, J., & Liu, Y.-J. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.185.6.1101 · Cited by 1,187 · see citing works
Regulatory T cells in the control of immune pathology
Maloy, K. J., & Powrie, F. M. (2001) · Nature Immunology · doi:10.1038/ni0901-816 · Cited by 1,177 · see citing works
Barrat, F. J., Cua, D. J., Boonstra, A., Richards, D. F., Crain, C., Savelkoul, H. F. J., Malefyt, R. D. W., Coffman, R. L., Hawrylowicz, C. M., & O’Garra, A. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20011629 · Cited by 1,161 · see citing works
Dieckmann, D., Ploettner, H., Berchtold, S., Berger, T. G., & Schuler, G. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.11.1303 · Cited by 1,140 · see citing works
Woo, E. Y., Chu, C., Goletz, T. J., Schlienger, K., Yeh, H., Coukos, G., Rubin, S. C., Kaiser, L. R., & June, C. H. (2001) · PubMed · Cited by 1,113 · see citing works
Hoffmann, P., Ermann, J., Edinger, M., Fathman, C. G., & Strober, S. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20020399 · Cited by 1,096 · see citing works
Taylor, P. A., Lees, C. J., & Blazar, B. R. (2002) · Blood · doi:10.1182/blood.v99.10.3493 · Cited by 1,039 · see citing works
Potential Regulatory Function of Human Dendritic Cells Expressing Indoleamine 2,3-Dioxygenase
Munn, D. H., Sharma, M. D., Lee, J. R., Jhaver, K. G., Johnson, T. S., Keskin, D. B., Marshall, B., Chandler, P., Antonia, S. J., Burgess, R. E., et al. (2002) · Science · doi:10.1126/science.1073514 · Cited by 1,028 · see citing works
Levings, M. K., Sangregorio, R., & Roncarolo, M. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.11.1295 · Cited by 966 · see citing works
Terness, P., Bauer, T. M., Röse, L., Dufter, C., Watzlik, A., Simon, H., & Opelz, G. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20020052 · Cited by 939 · see citing works
Cutting Edge: Cure of Colitis by CD4+CD25+ Regulatory T Cells
Mottet, C., Uhlig, H. H., & Powrie, F. M. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.8.3939 · Cited by 928 · see citing works
Iellem, A., Mariani, M., Lang, R., Recalde, H. R., Panina‐Bordignon, P., Sinigaglia, F., & D’Ambrosio, D. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.194.6.847 · Cited by 915 · see citing works
Huang, F., Platt, N., Wykes, M., Major, J. R., Powell, T. J., Jenkins, C. D., & MacPherson, G. G. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.191.3.435 · Cited by 902 · see citing works
Ghiringhelli, F., Larmonier, N., Schmitt, E., Parcellier, A., Cathelin, D., Garrido, C., Chauffert, B., Solary, É., Bonnotte, B., & Martin, F. (2004) · European Journal of Immunology · doi:10.1002/eji.200324181 · Cited by 878 · see citing works
Direct Expansion of Functional CD25+ CD4+ Regulatory T Cells by Antigen-processing Dendritic Cells
Yamazaki, S., Iyoda, T., Tarbell, K. V., Olson, K., Velinzon, K., Inaba, K., & Steinman, R. M. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20030422 · Cited by 856 · see citing works
Induction and mechanism of action of transforming growth factor‐β‐secreting Th3 regulatory cells
Weiner, H. L. (2001) · Immunological Reviews · doi:10.1034/j.1600-065x.2001.1820117.x · Cited by 850 · see citing works
Roncarolo, M. G., Bacchetta, R., Bordignon, C., Narula, S. K., & Levings, M. K. (2001) · Immunological Reviews · doi:10.1034/j.1600-065x.2001.1820105.x · Cited by 814 · see citing works
Tolerization of dendritic cells by TS cells: the crucial role of inhibitory receptors ILT3 and ILT4
Chang, C.-C., Ciubotariu, R., Manavalan, J. S., Yuan, J., Colovai, A. I., Piazza, F., Lederman, S. M., Colonna, M., Cortesini, R., Dalla‐Favera, R., et al. (2002) · Nature Immunology · doi:10.1038/ni760 · Cited by 803 · see citing works
Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 polarization
Cella, M., Facchetti, F., Lanzavecchia, A., & Colonna, M. (2000) · Nature Immunology · doi:10.1038/79747 · Cited by 790 · see citing works
Wakkach, A., Fournier, N., Brun, V., Breittmayer, J., Cottrez, F., & Groux, H. (2003) · Immunity · doi:10.1016/s1074-7613(03)00113-4 · Cited by 788 · see citing works
Kohm, A. P., Carpentier, P. A., Anger, H. A., & Miller, S. D. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.9.4712 · Cited by 782 · see citing works
Ling, E. M., Smith, T. R. F., Nguyen, X. D., Pridgeon, C., Dallman, M. J., Arbery, J., Carr, V. A., & Robinson, D. S. (2004) · The Lancet · doi:10.1016/s0140-6736(04)15592-x · Cited by 744 · see citing works
CD4+CD25+ Immunoregulatory T Cells
Cohen, J. L., Trenado, A., Vasey, D., Klatzmann, D., & Salomon, B. L. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20020090 · Cited by 686 · see citing works
Increase of regulatory T cells in the peripheral blood of cancer patients.
Wolf, A. M., Wolf, D. G. F., Steurer, M., Gastl, G., Gunsilius, E., & Grubeck-Loebenstein, B. (2003) · PubMed · Cited by 655 · see citing works
Dendritic cell lineage, plasticity and cross-regulation
Liu, Y.-J., Kanzler, H., Soumelis, V., & Gilliet, M. F. (2001) · Nature Immunology · doi:10.1038/89726 · Cited by 608 · see citing works
Jonuleit, H., Schmitt, E., Kakirman, H., Stassen, M., Knop, J., & Enk, A. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20020394 · Cited by 605 · see citing works
Griffin, M. D., Lutz, W. H., Phan, V., Bachman, L. A., McKEAN, D. J., & Kumar, R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.121172198 · Cited by 600 · see citing works
IFN-α and IL-10 Induce the Differentiation of Human Type 1 T Regulatory Cells
Levings, M. K., Sangregorio, R., Galbiati, F., Squadrone, S., Malefyt, R. D. W., & Roncarolo, M. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.9.5530 · Cited by 595 · see citing works
Granulocyte-colony stimulating factor mobilizes T helper 2-inducing dendritic cells
Arpinati, M., Green, C. L., Heimfeld, S., Heuser, J. E., & Anasetti, C. (2000) · Blood · doi:10.1182/blood.v95.8.2484.008k01_2484_2490 · Cited by 570 · see citing works
IL-2, Regulatory T Cells, and Tolerance
Nelson, B. H. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.7.3983 · Cited by 558 · see citing works
Menges, M., Rößner, S., Voigtländer, C., Schindler, H., Kukutsch, N. A., Bogdan, C., Erb, K. J., Schuler, G., & Lutz, M. B. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.20011341 · Cited by 556 · see citing works
Dendritic cells: emerging pharmacological targets of immunosuppressive drugs
Hackstein, H., & Thomson, A. W. (2004) · Nature reviews. Immunology · doi:10.1038/nri1256 · Cited by 546 · see citing works
Yamagiwa, S., Gray, J. D., Hashimoto, S., & Horwitz, D. A. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.12.7282 · Cited by 537 · see citing works
Trenado, A., Charlotte, F., Fisson, S., Yagello, M., Klatzmann, D., Salomon, B. L., & Cohen, J. L. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17702 · Cited by 493 · see citing works
Differentiation of T Regulatory Cells by Immature Dendritic Cells
Roncarolo, M., Levings, M. K., & Traversari, C. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.2.f5 · Cited by 484 · see citing works
Misra, N., Bayry, J., Lacroix‐Desmazes, S., Kazatchkine, M. D., & Kaveri, S. V. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.8.4676 · Cited by 477 · see citing works
Frontline: Neuropilin‐1: a surface marker of regulatory T cells
Bruder, D., Probst-Kepper, M., Westendorf, A., Geffers, R., Beissert, S., Loser, K., von Boehmer, H., Buer, J., & Hansen, W. (2004) · European Journal of Immunology · doi:10.1002/eji.200324799 · Cited by 475 · see citing works
Munn, D. H., Sharma, M. D., & Mellor, A. L. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.7.4100 · Cited by 453 · see citing works
The Regulatory T Cell Family: Distinct Subsets and their Interrelations
Jonuleit, H., & Schmitt, E. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.12.6323 · Cited by 436 · see citing works
Levings, M. K., Sangregorio, R., Sartirana, C., Moschin, A. L., Battaglia, M., Orban, P. C., & Roncarolo, M. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20021139 · Cited by 429 · see citing works
The Role of IL-10 and TGF-β in the Differentiation and Effector Function of T Regulatory Cells
Levings, M. K., Bacchetta, R., Schulz, U., & Roncarolo, M. G. (2002) · International Archives of Allergy and Immunology · doi:10.1159/000067596 · Cited by 423 · see citing works
Regulatory T cells under scrutiny
Bach, J. F. (2003) · Nature reviews. Immunology · doi:10.1038/nri1026 · Cited by 414 · see citing works
Induction of CD4+/CD25+ regulatory T cells by targeting of antigens to immature dendritic cells
Mahnke, K., Qian, Y., Knop, J., & Enk, A. (2003) · Blood · doi:10.1182/blood-2002-10-3229 · Cited by 388 · see citing works
Phenotype, Localization, and Mechanism of Suppression of CD4+CD25+ Human Thymocytes
Annunziato, F., Cosmi, L., Liotta, F., Lazzeri, E., Manetti, R., Vanini, V., Romagnani, P., Maggi, E., & Romagnani, S. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20020110 · Cited by 379 · see citing works
Fu, F., Li, Y., Qian, S., et al. (1996) · Transplantation · doi:10.1097/00007890-199609150-00021 · Cited by 366 · see citing works
Kriegel, M. A., Lohmann, T., Gabler, C., Blank, N., Kalden, J. R., & Lorenz, H. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20032158 · Cited by 351 · see citing works
High expression of ILT3 and ILT4 is a general feature of tolerogenic dendritic cells
Manavalan, J. S., Rossi, P. C., Vlad, G., Piazza, F., Yarilina, A., Cortesini, R., MANCINI, D. M., & Suciu‐Foca, N. (2003) · Transplant Immunology · doi:10.1016/s0966-3274(03)00058-3 · Cited by 319 · see citing works
Sato, K., Yamashita, N., Yamashita, N., Baba, M., & Matsuyama, T. (2003) · Immunity · doi:10.1016/s1074-7613(03)00055-4 · Cited by 313 · see citing works
Dendritic cells in transplantation--friend or foe?
Lechler, R., Ng, W.-F., & Steinman, R. M. (2001) · Immunity · doi:10.1016/s1074-7613(01)00116-9 · Cited by 312 · see citing works
Antigen-induced regulatory T cells in autoimmunity
von Herrath, M. G., & Harrison, L. C. (2003) · Nature reviews. Immunology · doi:10.1038/nri1029 · Cited by 310 · see citing works
Contributions of Direct and Indirect T Cell Alloreactivity During Allograft Rejection in Mice
Bénichou, G., Valujskikh, A., & Heeger, P. S. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.1.352 · Cited by 309 · see citing works
Origin and differentiation of dendritic cells
Ardavı́n, C., del Hoyo, G. M., Martı́n, P., Anjuère, F., Fernández-Arias, C., Marı́n, A. R., Ruiz, S., Parrillas, V., & Hernández‐Vargas, H. (2001) · Trends in Immunology · doi:10.1016/s1471-4906(01)02059-2 · Cited by 289 · see citing works
Dendritic cells: On the move from bench to bedside
Nestle, F. O., Banchereau, J., & Hart, D. N. J. (2001) · Nature Medicine · doi:10.1038/89863 · Cited by 288 · see citing works
Dendritic cells: regulators of alloimmunity and opportunities for tolerance induction
Morelli, A. E., & Thomson, A. W. (2003) · Immunological Reviews · doi:10.1046/j.1600-065x.2003.00079.x · Cited by 283 · see citing works
CD86 and CD80 Differentially Modulate the Suppressive Function of Human Regulatory T Cells
Zheng, Y., Manzotti, C. N., Liu, M., Burke, F., Mead, K. I., & Sansom, D. M. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.5.2778 · Cited by 277 · see citing works
Modulating the immune response with dendritic cells and their growth factors
Pulendran, B., Banchereau, J., Maraskovsky, E., & Maliszewski, C. R. (2001) · Trends in Immunology · doi:10.1016/s1471-4906(00)01794-4 · Cited by 263 · see citing works
Martin, E., O’Sullivan, B., Low, P., & Thomas, R. (2003) · Immunity · doi:10.1016/s1074-7613(02)00503-4 · Cited by 254 · see citing works
Sato, K., Yamashita, N., Baba, M., & Matsuyama, T. (2003) · Blood · doi:10.1182/blood-2002-09-2712 · Cited by 247 · see citing works
Controlling the Toll road to dendritic cell polarization
Mazzoni, A., & Segal, D. M. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.1003482 · Cited by 226 · see citing works
Franzke, A., Piao, W., Lauber, J., Gatzlaff, P., Koenecke, C., Hansen, W., Schmitt‐Thomssen, A., Hertenstein, B., Buer, J., & Ganser, A. (2003) · Blood · doi:10.1182/blood-2002-04-1200 · Cited by 213 · see citing works
Baker, R. J., Hernández-Fuentes, M. P., Brookes, P., Chaudhry, A., Cook, H. T., & Lechler, R. I. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.12.7199 · Cited by 211 · see citing works
Clark, F. J., Gregg, R. E., Piper, K., Dunnion, D., Freeman, L., Griffiths, M., Begum, G., Mahendra, P., Craddock, C., Moss, P. A. H., et al. (2003) · Blood · doi:10.1182/blood-2003-06-2073 · Cited by 211 · see citing works
Lü, L., Li, W., Fu, F., Chambers, F. G., Qian, S., Fung, J. J., & Thomson, A. W. (1997) · Transplantation · doi:10.1097/00007890-199712270-00031 · Cited by 207 · see citing works
Hoyne, G. F., Roux, I., Corsin-Jimenez, M., et al. (2000) · International Immunology · doi:10.1093/intimm/12.2.177 · Cited by 205 · see citing works
Antov, A., Yang, L., Vig, M., Baltimore, D., & Parijs, L. V. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.7.3435 · Cited by 204 · see citing works
Rastellini, C., Lü, L., Ricordi, C., Starzl, T. E., Rao, A. S., & Thomson, A. W. (1995) · PubMed · Cited by 201 · see citing works
IL-10 and TGF- induce alloreactive CD4+CD25- T cells to acquire regulatory cell function
Chen, Z.-M. (2003) · Blood · doi:10.1182/blood-2002-09-2798 · Cited by 184 · see citing works
Somasundaram, R., Jacob, L., Swoboda, R., Caputo, L., Song, H., Basak, S. K., Monos, D. S., Peritt, D., Marincola, F. M., Cai, D., et al. (2002) · PubMed · Cited by 181 · see citing works
Volpi, I., Perruccio, K., Tosti, A., Capanni, M., Ruggeri, L., Posati, S., Aversa, F., Tabilio, A., Romani, L. R., Martelli, M. F., et al. (2001) · Blood · doi:10.1182/blood.v97.8.2514 · Cited by 178 · see citing works
Regulatory T Cells Overexpress a Subset of Th2 Gene Transcripts
Zélénika, D., Adams, E., Humm, S., Graça, L., Thompson, S. A. J., Cobbold, S. P., & Waldmann, H. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.3.1069 · Cited by 173 · see citing works
Cutting Edge: Self-Peptides Drive the Peripheral Expansion of CD4+CD25+ Regulatory T Cells
Cozzo, C., Larkin, J., & Caton, A. J. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.11.5678 · Cited by 170 · see citing works
Sayegh, M. H., Khoury, S. J., Hancock, W. W., et al. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.16.7762 · Cited by 160 · see citing works
Overexpression of the Notch ligand, Jagged-1, induces alloantigen-specific human regulatory T cells
Yvon, E. S., Vigouroux, S., Rousseau, R. F., et al. (2003) · Blood · doi:10.1182/blood-2002-12-3826 · Cited by 157 · see citing works
Role for granulocyte colony–stimulating factor in the generation of human T regulatory type 1 cells
Rutella, S., Pierelli, L., Bonanno, G., Sica, S., Ameglio, F., Capoluongo, E., Mariotti, A., Scambia, G., d’Onofrio, G., & Leone, G. G. M. (2002) · Blood · doi:10.1182/blood-2001-12-0291 · Cited by 154 · see citing works
Self-citationMorris, E. S., MacDonald, K. P. A., Rowe, V., Johnson, D., Banovic, T., Clouston, A. D., & Hill, G. R. (2004) · Blood · doi:10.1182/blood-2003-08-2864 · Cited by 134 · see citing works
Cobbold, S. P., Nolan, K. F., Graça, L., Castejón, R., Moine, A. L., Frewin, M. R., Humm, S., Adams, E., Thompson, S. A. J., Zélénika, D., et al. (2003) · Immunological Reviews · doi:10.1046/j.1600-065x.2003.00078.x · Cited by 133 · see citing works
On the Role of Dendritic Cells in Peripheral T Cell Tolerance and Modulation of Autoimmunity
Legge, K. L., Gregg, R. K., Maldonado-López, R., Li, L., Caprio, J. C., Moser, M., & Zaghouani, H. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20011061 · Cited by 133 · see citing works
Induction of FOXP3‐expressing regulatory CD4pos T cells by human mature autologous dendritic cells
Verhasselt, V., Vosters, O., Beuneu, C., Nicaise, C., Stordeur, P., & Goldman, M. (2004) · European Journal of Immunology · doi:10.1002/eji.200324552 · Cited by 128 · see citing works
Impaired Development of CD4+ CD25+ Regulatory T Cells in the Absence of STAT1
Nishibori, T., Tanabe, Y., Su, L., & David, M. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20020509 · Cited by 128 · see citing works
Rutella, S., Bonanno, G., Pierelli, L., Mariotti, A., Capoluongo, E., Contemi, A. M., Ameglio, F., Curti, A., Ritis, D. G. D., Voso, M. T., et al. (2004) · European Journal of Immunology · doi:10.1002/eji.200324651 · Cited by 125 · see citing works
Self-citationHeavy chain ferritin activates regulatory T cells by induction of changes in dendritic cells
Gray, C. P., Arosio, P., & Hersey, P. (2002) · Blood · doi:10.1182/blood.v99.9.3326 · Cited by 118 · see citing works
Zavala, F., Abad, S., Ezine, S., Taupin, V., Masson, A., & Bach, J. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.4.2011 · Cited by 112 · see citing works
Faunce, D. E., Terajewicz, A., & Stein‐Streilein, J. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.4.1991 · Cited by 110 · see citing works
Induction of tolerogenic DCs: ‘you are what you eat’
Mahnke, K., KNOP, J., & Enk, A. (2003) · Trends in Immunology · doi:10.1016/j.it.2003.09.012 · Cited by 87 · see citing works
Potential of tolerogenic dendritic cells for transplantation
Morelli, A. E., Hackstein, H., & Thomson, A. W. (2001) · Seminars in Immunology · doi:10.1006/smim.2001.0328 · Cited by 75 · see citing works
Human CD4+CD25+ regulatory T cells and infectious tolerance.
Stassen, M., Schmitt, E., & Jonuleit, H. (2004) · Transplantation · doi:10.1097/00007890-200401151-00009 · Cited by 70 · see citing works
Nouri-Shirazi, M. A., & Guinet, E. (2002) · Transplantation · doi:10.1097/00007890-200210150-00024 · Cited by 64 · see citing works
Functional modulation of dendritic cells to suppress adaptive immune responses
Woltman, A. M., & van Kooten, C. (2003) · Journal of Leukocyte Biology · doi:10.1189/jlb.0902431 · Cited by 56 · see citing works
Rutella, S., Rumi, C., Lucia, M. B., Sica, S., Cauda, R., & Leone, G. G. M. (1998) · PubMed · Cited by 48 · see citing works
Self-citationMotta, M. R., Castellani, S., Rizzi, S., et al. (2003) · British Journal of Haematology · doi:10.1046/j.1365-2141.2003.04270.x · Cited by 45 · see citing works
Vučković, S., Kim, M., Khalil, D., et al. (2003) · Blood · doi:10.1182/blood-2002-03-0973 · Cited by 45 · see citing works
Cross-priming versus cross-tolerance: are two signals enough?
Blankenstein, T. J. F. (2002) · Trends in Immunology · doi:10.1016/s1471-4906(02)02185-3 · Cited by 29 · see citing works
Rutella, S., Rumi, C., Sica, S., & Leone, G. G. M. (1999) · Journal of Interferon & Cytokine Research · doi:10.1089/107999099313181 · Cited by 27 · see citing works
Self-citationRutella, S., Pierelli, L., Rumi, C., et al. (2001) · Experimental Hematology · doi:10.1016/s0301-472x(01)00617-8 · Cited by 18 · see citing works
Self-citationRadcliff, F. J., Caruso, D. A., Koina, C., et al. (2002) · British Journal of Haematology · doi:10.1046/j.1365-2141.2002.03717.x · Cited by 11 · see citing works
Tsuchihashi (2000) · doi:10.1002/1521-4141(200006)30:6
Flagged first, then by citations
Cited by
Sorted by citations
Coutinho, A. E., & Chapman, K. E. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.04.005 · Cited by 1,815 · see citing works
The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain
Bellavance, M.-A., & Rivest, S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00136 · Cited by 419 · see citing works
Jantsch, J., Chakravortty, D., Turza, N., Prechtel, A. T., Buchholz, B., Gerlach, R. G., Volke, M., Gläsner, J., Warnecke, C., Wiesener, M. S., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.7.4697 · Cited by 414 · see citing works
Candida albicans mannoprotein influences the biological function of dendritic cells
Pietrella, D., Bistoni, G., Corbucci, C., Perito, S., & Vecchiarelli, A. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2005.00651.x · Cited by 75 · see citing works
- Authors
- Rutella, S., & Lemoli, R. M.
- Affiliations
- Università Cattolica del Sacro Cuore (IT)
- University of Bologna (IT)
- Corresponding author
- Rutella, Sergio
- Venue
- Immunology Letters
- Publisher
- Elsevier BV
- Published
- 2004-06
- Volume
- 94
- Issue
- 1-2
- Pages
- 11-26
- ISSN
- 0165-2478 (ISSN-L)
- OpenAlex
- W2005981263
- Cited by
- 147
- References
- 127
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2023: 3 · 2022: 1 · 2021: 2 · 2020: 3 · 2019: 3 · 2018: 3 · 2017: 4 · 2016: 2 · 2015: 6 · 2014: 1 · 2013: 8 · 2012: 3
- FWCI
- 1.69
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Immunology Letters (publishedVersion)
- PubMed (publishedVersion)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
- Nottingham Trent University's Institutional Repository (Nottingham Trent Repository) (submittedVersion)
- CINECA IRIS Institutial Research Information System (University of Genoa) (submittedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- regulatory T cells, tolerogenic dendritic cells, peripheral tolerance, antigen-specific tolerance, autoimmunity, immune homeostasis, dendritic cell maturation, Treg differentiation, dendritic cell subsets, cell therapy, immune-mediated diseases
- MeSH terms
- Autoimmune Diseases, Dendritic Cells, Humans, Immune Tolerance, Antigen Presentation, T-Lymphocytes, Regulatory
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review