Immunology and Cell Biology (1997) 75, 223–230; doi:10.1038/icb.1997.35
The role of dendritic cells in T cell activation
K Ni1 and HC O'Neill1
1Division of Biochemistry and Molecular Biology, Faculty of Science, Australian National University, Canberra, Australian Capital Territory, Australia
Correspondence: Dr HC O'Neill, Division of Biochemistry and Molecular Biology, Faculty of Science, Australian National University, Canberra, ACT 2601, Australia.
Received 29 October 1996; Accepted 10 February 1997.
Top of pageAbstract
Dendritic cells (DC) are distinguishable from other antigen-presenting cells by their potent antigen-presenting capacity. They are not only efficient at presenting peptide antigen but can also process and present soluble protein antigens to antigen-specific T cells and cloned T cell lines. They are very strong stimulators of both allogeneic and syngeneic mixed lymphocyte reactions and have a unique capacity to stimulate naive T cells. The potent functional capacity of DC is related to a high-level expression of major histocompatibility complex class I/II molecules and constitutive expression of costimulatory molecules, such as CD80/CD86 as well as heat stable antigen. CD40 and the leucocyte function antigen (LFA) family of adhesion molecules. Recent studies have shown that DC are also involved in regulation of the immune response via induction of both central and peripheral tolerance.
Keywords:
antigen presentation capacity, costimulators, dendritic cells, T cell activation, tolerance
Top of pageReferences
- Klinkert WE. Rat bone marrow precursors develop into dendritic accessory cells under the influence of a conditioned medium. Immunobiology 1984; 168: 414–24.
- Austyn JM, Steinman RM, Weinstein DE, Granelli-Pipemo A, Palladino MA. Dendritic cells initiate a two-stage mechanism for T lymphocyte proliferation. J. Exp. Med. 1983; 157: 1101–15. | Article | PubMed | ISI | ChemPort |
- Inaba K, Steinman RM, Van Voorhis WC, Muramatsu S. Dendritic cells are critical accessory cells for thymus-dependent antibody responses in mouse and in man. Proc. Natl Acad. Sci. USA 1983; 80: 6041–5. | Article | PubMed | ChemPort |
- Klinkert WE, Labadie JH, Bowers WE. Accessory and stimulating properties of dendritic cells and macrophages isolated from various rat tissues. J. Exp. Med. 1982; 156: 1–19. | Article | PubMed | ISI | ChemPort |
- Steinman RM, Witmer MD. Lymphoid dendritic cells are potent stimulators of the primary mixed leukocyte reaction in mice. Proc. Natl Acad. Sci. USA 1978; 75: 5132–6. | Article | PubMed | ChemPort |
- Sornasse T, Flamand V, De Becker G et al. Antigen-pulsed dendritic cells can efficiently induce an antibody response in vivo. J. Exp. Med. 1992; 175: 15–21. | Article | PubMed | ISI | ChemPort |
- Lechler RI, Batchelor JR. Restoration of immunogenicity to passenger cell-depleted kidney allografts by the addition of donors train dendritic cells. J. Exp. Med. 1982; 155: 31–41. | Article | PubMed | ISI | ChemPort |
- Inaba K, Steinman RM. Protein-specific helper T-lymphocyte formation initiated by dendritic cells. Science 1985; 229: 475–9. | Article | PubMed | ChemPort |
- Inaba K, Metlay JP, Crowley MT, Steinman RM. Dendritic cells pulsed with protein antigens in vitro can prime antigen-specific, MHC-restricted T cells in situ. J. Exp. Med. 1990; 172: 631–40. | Article | PubMed | ISI | ChemPort |
- Levin D, Constant S, Pasqualini T, Flavell R, Bottomly K. Role of dendritic cells in the priming of CD4+ T lymphocytes to peptide antigen in vivo. J. Immunol. 1993; 151: 6742–50. | PubMed | ISI | ChemPort |
- Lin RH, Mamula MJ, Hardin JA, Janeway CAJ. Induction of autoreactive B cells allows priming of autoreactive T cells. J. Exp. Med. 1991; 173: 1433–9. | Article | PubMed | ISI | ChemPort |
- Fuchs EJ, Matzinger P. B cells turn off virgin but not memory T cells. Science 1992; 258: 1156–9. | Article | PubMed | ISI | ChemPort |
- McCormack JM, Moore SC, Gatewood JW, Walker WS. Mouse splenic macrophage cell lines with different antigen-presenting activities for CD4+ helper T cell subsets and allogeneic CD8+ T cells. Cell. Immunol. 1992; 145: 359–71.
- Wolos JA, Davey FR. Function of lymphocyte subpopulations in chronic lymphocytic leukemia. Cancer 1980; 45: 893–8.
- Tanaka S, Sakai A. Stimulation of allogeneic lymphocytes by skin epidermal cells in the rat. Transplantation 1979; 27: 194–9. | PubMed | ChemPort |
- Lafferty KJ, Woolnough J. The origin and mechanism of the allograft rejection. Immunol. Rev. 1977; 35: 231–62. | Article | PubMed | ISI | ChemPort |
- De Bruijn MLH, Nieland JD, Harding CV, Melief CJM. Processing and presentation of intact hen egg-white lysozyme by dendritic cells. Eur. J. Immunol. 1992; 22: 2347–52.
- Metlay JP, Pure E, Steinman RM. Distinct features of dendritic cells and anti-Ig activated B cells as stimulators of the primary mixed leukocyte reaction. J. Exp. Med. 1989; 169: 239–54. | Article | PubMed | ChemPort |
- Steinman RM, Adams JC, Cohn ZA. Identification of a novel cell type in peripheral lymphoid organs of mice. IV: identification and distribution in mouse spleen. J. Exp. Med. 1975; 141: 804–20. | PubMed | ChemPort |
- Nussenzweig MC, Steinman RM. Contribution of dendritic cells to stimulation of the murine syngeneic mixed leukocyte reaction. J. Exp. Med. 1980; 151: 1196–212. | Article | PubMed | ISI | ChemPort |
- Weksler ME, Kuntz MM, Bimbaum G, Innes JB. Lymphocyte transformation induced by autologous cells. Fed. Proc. 1978; 37: 2370–3.
- Shortman K, Vremec D, Damico A, Batty F, Boyd R. Nature of the thymocytes associated with dendritic cells and macrophages in thymic rosettes. Cell. Immunol. 1989; 119: 85–100.
- Inaba K, Schuler G, Witmer MD, Valinksy J, Atassi B, Steinman RM. Immunologic properties of purified epidermal Langerhans cells: Distinct requirements for stimulation of unprimed and sensitized T lymphocytes. J. Exp. Med. 1986; 164: 605–13. | Article | PubMed | ISI | ChemPort |
- Cumberbatch M, Illingworth I, Kimber I. Antigen-bearing dendritic cells in the draining lymph nodes of contact sensitized mice: cluster formation with lymphocytes. Immunology 1991; 74: 139–45. | PubMed | ISI | ChemPort |
- Sanchez-Madrid F, Simon P, Thompson S, Springer TA. Mapping of antigenic and functional epitopes on the alpha-and beta-subunits of two related mouse glycoproteins involved in cell interactions. LFA-1 and Mac-I. J. Exp. Med. 1983; 158: 586–602. | Article | PubMed | ChemPort |
- Unkeless SL. Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fe receptors. J. Exp. Med. 1979; 150: 586–96.
- Ada G. Antigen-processing revisited: a foreword. Immunol. Rev. 1987; 98: 1–8.
- Ziegler HK, Unanue ER. Decrease in macrophage antigen catabolism caused by ammonia and chloroquine is associated with inhibition of antigen presentation to T cells. Proc. Natl Acad. Sci. USA 1982; 79: 175–8. | Article | PubMed | ChemPort |
- Scheicher C, Mehlig M, Dienes HP, Reske K. Uptake of microparticle-adsorbed protein antigen by bone marrow-derived dendritic cells results in up-regulation of interleukin-1
and interleukin-12 p40/p35 and triggers prolonged, efficient antigen presentation. Eur. J. Immunol. 1995; 25: 1566–72. | PubMed | ISI | ChemPort | - Inaba K, Inaba M, Naito M, Steinman RM. Dendritic cell progenitors phagocytose particulates, including bacillus Calmette-Guerin organisms, and sensitize mice to mycobacterial antigens in vivo. J. Exp. Med. 1993; 178: 479–88. | Article | PubMed | ISI | ChemPort |
- Reis e Sousa C, Stahl PD, Austyn JM. Phagocytosis of antigens by Langerhans cells in vitro. J. Exp. Med. 1993; 178: 509–19. | Article | PubMed | ChemPort |
- Koch F, Trockenbacher B, Kampgen E et al. Antigen processing in populations of mature murine dendritic cells is caused by subsets of incompletely matured cells. J. Immunol. 1995; 155: 93–100. | PubMed | ISI | ChemPort |
- Johnson JG, Jenkins MK. The role of anergy in peripheral T cell unresponsiveness. Life Sci. 1994; 55: 1767–80.
- Galvin F, Freeman GJ, Razi-Wolf Z et al. Murine B7 antigen provides a sufficient costimulatory signal for antigen-specific and MHC-restricted T cell activation. J. Immunol. 1992; 149: 3802–8. | PubMed | ISI | ChemPort |
- Tan P, Anasetti C, Hansen JA et al. Induction of alloantigen-specific hyporesponsiveness in human T lymphocytes by blocking interaction of CD28 with its natural ligand B7/BB1. J. Exp. Med. 1993; 177: 165–73. | Article | PubMed | ISI | ChemPort |
- Azuma M, Cayabyab M, Buck D, Phillips JH, Lanier LL. CD28 interaction with B7 costimulates primary allogeneic proliferative responses and cytotoxicity mediated by small, resting T lymphocytes. J. Exp. Med. 1992; 175: 353–60. | Article | PubMed | ISI | ChemPort |
- Van de Velde H, Lorre K, Bakkus M, Thielemans K, Ceuppens JL, de Boer M. CD45RO+ memory T cells but not CD45RA+ naive T cells can be efficiently activated by remote co-stimulation with B7. Int. Immunol. 1993; 5: 1483–7.
- Ding L, Shevach EM. Activation of CD4+ T cells by delivery of the B7 costimulatory signal on bystander antigen-presenting cells (trans-costimulation). Eur. J. Immunol. 1994; 24: 859–66.
- Kundig TM, Bachmann MF, Dipaolo C et al. Fibroblasts as efficient antigen-presenting cells in lymphoid organs. Science 1995; 268: 1343–7. | Article | PubMed | ISI | ChemPort |
- Katz DR, Feldmann M, Tees R, Schreier MH. Heterogeneity of accessory cells interacting with T-helper clones. Immunology 1986; 58: 167–72.
- Michaelsson E, Holmdahl M, Engstom A, Burkhardt H, Scheynius A, Holmdahl R. Macrophages, but not dendritic cells, present collagen to T cells. Eur. J. Immunol. 1995; 25: 2234–41. | PubMed |
- Bosseloir A, Bouzahzah F, Defrance TH, Heinen E, Simar LJ. The influence of follicular dendritic cells on B-cell proliferation depends on the activation of B cells and the mitogen used. Scand. J. Immunol. 1996; 43: 23–30.
- Aiba S, Katz SI. The ability of cultured Langerhans cells to process and present protein antigens is MHC-dependent. J. Immunol. 1991; 146: 2479–87. | PubMed | ChemPort |
- Heufler C, Koch F, Stanzl U et al. 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. 1996; 26: 659–68. | PubMed | ISI | ChemPort |
- Kanangat S, Nair S, Babu JS, Rouse BT. Expression of cytokine mRNA in murine splenic dendritic cells and better induction of T cell-derived cytokines by dendritic cells than by macrophages during in vitro costimulation assay using specific antigens. J. Leukoc. Biot. 1995; 57: 310–16.
- Macatonia SE, Hosken NA, Litton M et al. Dendritic cells produce IL-12 and direct the development of The cells from naive CD4+ T cells. J. Immunol. 1995; 154: 5071–9. | PubMed | ISI | ChemPort |
- Macatonia SE, Hsieh CS, Murphy KM, Ogarra A. Dendritic cells and macrophages are required for Th1 development of CD4+ T cells from alpha beta TCR transgenic mice: IL-12 substitution for macrophages to stimulate IFN-gamma production is IFN-gamma-dependent. Int. Immunol. 1993; 5: 1119–28. | Article | PubMed | ISI | ChemPort |
- Maruo S, Toyo oka K, Oh hora M et al. IL-12 produced by antigen-presenting cells induces IL-2-independent proliferation of T helper cell clones. J. Immunol. 1996; 156: 1748–55. | PubMed | ISI | ChemPort |
- Murphy EE, Terres G, Macatonia SE et al. B7 and interleukin 12 cooperate for proliferation and interferon gamma production by mouse T helper clones that are unresponsive to B7 costimulation. J. Exp. Med. 1994; 180: 223–31. | Article | PubMed | ISI | ChemPort |
- Kubin M, Kamoun M, Trinchieri G. Interleukin 12 synergizes with B7/CD28 interaction in inducing efficient proliferation and cytokine production of human T cells. J. Exp. Med. 1994; 180: 211–22. | Article | PubMed | ISI | ChemPort |
- Kang K, Kubin M, Cooper KD, Lessin SR, Trinchieri G, Rook AH. IL-12 synthesis by human Langerhans cells. J. Immunol. 1996; 156: 1402–7. | PubMed | ISI | ChemPort |
- Koch F, Stanzl U, Jennewein P et al. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J. Exp. Med. 1996; 184: 741–6. | Article | PubMed | ISI | ChemPort |
- Cella M, Scheidegger D, Palmer lehmann K, Lane P, Lanzavecchia A, Alber G. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 1996; 184; 747–52. | Article | PubMed | ISI | ChemPort |
- Everson MP, McDuffie DS, Lemak DG, Koopman WJ, McGhee JR, Beagley KW. Dendritic cells from different tissues induce production of different T cell cytokine profiles. J. Leukoc. Biol. 1996; 59: 494–8.
- Gerosa F, Paganin C, Peritt D et al. Interleukin-12 primes human CD4 and CD8 T cell clones for high production of both interferon-gamma and interleukin-10. J. Exp. Med. 1996; 183; 2559–69. | Article | PubMed | ISI | ChemPort |
- Trinchieri G, Wysocka M, Dandrea A et al. Natural killer cell stimulatory factor (NKSF) or interleukin-12 is a key regulator of immune response and inflammation. Prog. Growth Factor Res. 1992; 4: 355–68. | PubMed | ChemPort |
- Trinchieri G. The two faces of interleukin 12: a pro-inflammatory cytokine and a key immunoregulatory molecule produced by antigen-presenting cells. Ciba Found. Symp., 1995; 195: 203–14.
- Wenner CA, Guler ML, Macatonia SE, Ogarra A, Murphy KM. Roles of IFN-gamma and IFN-alpha in IL-12-induced T helper cell-1 development. J. Immunol. 1996; 156; 1442–7. | PubMed | ISI | ChemPort |
- Dubey C, Croft M, Swain SL. Costimulatory requirements of naive CD4+ T cells. J. Immunol. 1995; 155: 45–57. | PubMed | ISI | ChemPort |
- Kawakami K, Yamamoto Y, Kakimoto K, Onoue K. Requirement for delivery of signals by physical interaction and soluble factors from accessory cells in the induction of receptor-mediated T cell proliferation: Effectiveness of IFN-gamma modulation of accessory cells for physical interaction with T cells. J. Immunol. 1989; 142: 1818–25.
- Garman RD, Jacobs KA, Clark SC, Raulet DH. B cell stimulatory factor 2 (beta 2 interferon) functions as a second signal for interleukin 2 production by mature murine T cells. Proc. Natl Acad. Sci. USA 1987; 84: 7629–33. | Article | PubMed | ChemPort |
- Freeman GJ, Lombard DB, Gimmi CD et al. Expression of CTLA-4 and CD28 mRNA does not correlate with the pattern of lymphokine production. J. Immunol. 1992; 149; 3795–801. | PubMed | ISI | ChemPort |
- Hansen JA, Martin PJ, Nowinski RC. Monoclonal antibodies identifying a novel T cell antigen and Ia antigens of human lymphocytes. Immunogenetics 1980; 10; 247–60. | Article | ISI |
- Turka LA, Ledbetter JA, Lee K, June CH, Thompson CB. CD28 is an inducible T cell surface antigen hat transduces a proliferative signal in CD3+ mature thymocytes. J. Immunol. 1990; 144: 1646–53. | PubMed | ChemPort |
- Yokochi T, Holly RD, Clark EA. B lymphoblast antigen (BB-1) expressed on Epstein Barr virus-activated B cell blasts, B lymphoblastoid ceil lines, and Burkitt's lymphomas. J. Immunol. 1982; 128: 823–7. | PubMed | ISI | ChemPort |
- Freedman AS, Freeman GJ, Horowitz JC, Daley J, Nadler LM. B7, a B-cell-restricted antigen that identifies preactivated B cells. J. Immunol. 1987; 139: 3260–7. | PubMed | ISI | ChemPort |
- Freeman GJ, Freedman AS, Segil JM, Lee G, Whitman JF, Nadler LM. B7, a new member of the Ig superfamily with unique expression on activated and neoplastic B cells. J. Immunol. 1989; 143: 2714–22. | PubMed | ISI | ChemPort |
- Linsley PS, Clark EA, Ledbetter JA. T cell antigen CD28 mediates adhesion with B cells by interacting with activation antigen B7/BB1. Proc. Natl Acad. Sci. USA 1990; 87; 5031–5. | Article | PubMed | ChemPort |
- Razi-Wolf Z, Falo LDJ, Reiser H. Expression and function of the costimulatory molecule B7 and murine Langerhans cells: evidence for an alternative CTLA-4 ligand. Eur. J. Immunol. 1994; 24: 805–11.
- Azuma M, Ito D, Yagita H et al. B70 antigen is a second ligand for CTLA-4 and CD28. Nature 1993; 366: 76–9. | Article | PubMed | ISI | ChemPort |
- Lenschow DJ, Su GH, Zuckerman LA et al. Expression and functional significance of an additional ligand for CTLA-4. Proc. Natl Acad. Sci. USA 1993; 90: 11 054–8.
- Larsen CP, Ritchie SC, Pearson TC, Linsley PS, Lowry RP. Functional expression of the costimulatory molecule, B7/BB1, on murine dendritic cell populations. J. Exp. Med. 1992; 176; 1215–20. | Article | PubMed | ISI | ChemPort |
- Razi-Wolf Z, Freeman GJ, Galvin F, Benacerraf B, Nadler L, Reiser H. Expression and function of the murine B7 gen, the major costimulatory molecule expressed by peritoneal exudate cells. Proc. Natl Acad. Sci. USA 1992; 89: 4210–14. | Article | PubMed | ChemPort |
- Ding L, Linsley PS, Huang LY, Germain RN, Shevach FM. IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J. Immunol. 1993; 151: 1224–34. | PubMed | ISI | ChemPort |
- Hathcock KS, Laszlo G, Pucillo C, Linsley P, Hodes RJ. Comparative analysis of B7-1 and B7-2 costimulatory ligands: expression and function. J. Exp. Med. 1994; 180: 631–40. | Article | PubMed | ISI | ChemPort |
- Sansom DM, Hall ND. B7/BBI, the ligand for CD28, is expressed on repeatedly activated human T cells in vitro. Eur. J. Immunol. 1993; 23: 295–8.
- Girolomoni G, Zambruno G, Manfredini R et al. Expression of B7 costimulatory molecule in cultures of human epidermal Langerhans cells is regulated at the mRNA level. J. Invest. Derm. 1994; 103: 54–9.
- McLellan AD, Starling GC, Williams LA, Hock BD, Hart DNJ. Activation of human peripheral blood dendritic cells induces the CD86 co-stimulatory molecule. Eur J. Immunol. 1995; 25: 2064–8. | PubMed | ISI | ChemPort |
- Larsen CP, Ritchie SC, Hendrix R et al. Regulation of immunostimulatory function and costimulatory molecule (B7-i and B7-2) expression on murine dendritic cells. J. Immunol. 1994; 152: 5208–19. | PubMed | ISI | ChemPort |
- Fagnoni FF, Takamizawa M, Godfrey WR et al. Role of B7O/B7-2 in CD4+ T cell immune responses induced by dendritic cells. Immunology 1995; 85: 467–74. | PubMed | ISI | ChemPort |
- De Fougerolles AR, Springer TA. Intercellular adhesion molecule-3, a third adhesion counter-receptor for lymphocyte function-associated molecule 1 on resting lymphocytes. J. Exp. Med. 1992; 175: 185–90. | Article | PubMed | ChemPort |
- Marlin SD, Springer TA. Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1). Cell 1987; 51: 813–19. | Article | PubMed | ISI | ChemPort |
- Staunton DE, Dustin ML, Springer TA. Functional coining of lCAM-2, a cell adhesion ligand for LFA-1 homologous to ICAM-1 Nature 1989; 339: 61–4. | Article | PubMed | ISI | ChemPort |
- Van Seventer GA, Shimizu Y, Horgan KJ, Shaw S. The LFA-1 ligand ICAM-1 provides an important costimulatory signal for T cell receptor-mediated activation of resting T cells. J. Immunol. 1990; 144: 4579–86. | PubMed | ChemPort |
- Damle NK, Klussman K, Linsley PS, Aruff A, Ledbetter JA. Differential regulatory effects of intercellular adhesion molecule-1 on costimulation by the CD28 counter-receptor B7. J. Immnunol. 1992; 149: 2541–8.
- Ibrahim MAA, Chain BM, Katz DR. The role of non-adhesive T cell-accessory cell interactions in the induction of T cell proliferative hyporesponsiveness. Immunology 1994; 81: 521–31.
- Cavallo F, Martin-Fontecha A, Bellone M et al. Co-expression of B7-1 and ICAM-1 on tumors is required for rejection and the establishment of a memory response. Eur. J. Immunol. 1995; 25: 1154–62. | PubMed | ChemPort |
- Crispe IN, Moore MW, Husmann LA, Smith L, Bevan MJ, Shimonkevitz RP. Differentiation potential of subsets of CD4 8- thymocytes. Nature 1987; 329: 336–9. | Article | PubMed | ChemPort |
- Inaba K, Steinman RM, Witmer-Pack M et al. Identification of proliferating deruiritic cell precursors in mouse blood. J. Exp. Med. 1992; 175: 1157–67. | Article | PubMed | ISI | ChemPort |
- Liu Y, Jones B, Aruffo A, Sullivan KM, Linsley PS, Janeway CAJ. Heat-stable antigen is a costimulatory molecule for CD4 T cell growth. J. Exp. Med. 1992; 175: 437–46. | Article | PubMed | ISI | ChemPort |
- Liu Y, Jones B, Brady W, Janeway CAJ, Linsley PS. Costimulation of murine CD4 T cell growth: cooperation between B7 and heat-stable antigen. Eur. J. Immunol. 1992; 22: 2855–62.
- Enk AH, Katz SI. Heat-stable antigen is an important costimulatory molecule on epidermal Langerhans cells. J. Immunol. 1994; 152: 3264–70.
- Erdmann G, Saloga J, Mohamadzadeh M, Becker D, Knop J, Enk AH. Heat-stable antigen is expressed by murine keratinocytes and delivers costimulatory signals in T-cell activation. Exp. Dermatol. 1995; 4: 291–6.
- Caux C, Massacrier C, Vanbervliet B et al. Activation of human dendritic cells through CD40 cross-linking. J. Exp. Med. 1994; 180: 1263–72. | Article | PubMed | ISI | ChemPort |
- Kwekkeboom J, de Rijk D, Kasran A, Barcy S, de Groot C, de Boer M. Helper effector function of human T cells stimulated by anti-CD3 mAb can be enhanced by co-stimulatory signals s and is partially dependent on CD40-CD40 ligand interaction. Eur. J. Immunol. 1994; 24: 508–17.
- McLellan AD, Sorg RV, Williams LA, Hart DN. Human dendritic cells activate T lymphocytes via a CD40: CD40 ligand-dependent pathway. Eur. J. Immunol. 1996; 26: 1204–10. | PubMed | ISI | ChemPort |
- Springer TA. Adhesion receptors of the immune system. Nature 1990; 346: 425–36. | Article | PubMed | ISI | ChemPort |
- Kyewski BA, Fathman CG, Rouse RV. Intrathymic presentation of circulating non-MHC antigens by medullary dendritic cells: An antigen-dependent microenvironment for T cell differentiation. J. Exp. Med. 1986; 163: 231–46. | Article | PubMed | ISI | ChemPort |
- Khoury SJ, Gallon L, Chen W et al. Mechanisms of acquired thymic tolerance in experimental autoimmune encephalomyelitis: thymic dendritic-enriched cells induce specific peripheral T cell unresponsiveness in vivo. J. Exp. Med. 1995; 182: 357–66. | Article | PubMed | ChemPort |
- Inaha M, Inaba K, Hosono M et al. Distinct mechanisms of neonatal tolerance induced by dendritic cells and thymic B cells. J Exp. Med. 1991; 173: 549–59.
- Matzinger P, Guerder S. Does T-cell tolerance require a dedicated antigen presenting cell? Nature 1989; 338: 74–6. | Article | PubMed | ISI | ChemPort |
- Morikawa Y, Furotian M, Kuribayashi K et al. The role of antigen presenting cells in the regulation of delayed type-hypersensitivity. I: Spleen dendritic cells. Immunology 1992; 77: 81–7. | PubMed | ISI | ChemPort |
- Morikawa Y, Furotain M, Matsuur N, Kakudo K. The role of antigen presenting cells in the regulation of delayed-type hypersensitivity. II: Langerhans cells and peritoneal exudate macrophages. Cell. Immunol 1993; 152: 200–10. | Article | PubMed | ISI | ChemPort |
- Thomson AW, Lu L, Murase N, Demetris AJ, Rao AS, Starzl TE. Microchimerism, dendritic cell progenitors and transplantation tolerance. Stem Cells (Dayt.) 1995; 13: 622–39.
- Rastellini C, Lu L, Ricordi C, Starzl TE, Rao AS, Thomson AW. Granulocyte/macrophage colony-stimulating factors stimulated hepatic dendritic cell progenitors prolong pancreatic islet allograft survival. Transplantation 1995; 60: 1366–70. | PubMed | ChemPort |
- Vremec D, Zorbas M, Scollay R et al. 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. 1992; 176; 47–58. | Article | PubMed | ISI | ChemPort |
- Suss G, Shortman K. A subclass of dendritic cells kills CD4 T cells via Fas/Fas-ligand induced apoptosis. J. Exp. Med. 1996; 183: 1789–96. | Article | PubMed | ISI | ChemPort |
- Finkelman FD, Lees A, Birnbaum R, Gause WC, Morris SC. Dendritic cells can present antigen in vivo in a tolerogenic or immunogenic fashion. J. Immunol. 1996; 157: 1406–14. | PubMed | ISI | ChemPort |
- Romani N, Schuler G. The immunologic properties of epidermal Langerhans cells as a part of the dendritic cell system. Springer Semin. Immunopathol. 1992; 13: 265–79. | PubMed | ISI | ChemPort |
- Heufler C, Koch F, Schuler G. Granulocyte/macrophage colony-stimulating factor and interleukin 1 mediate the maturation of murine epidermal Langerhans cells into potent immunostimulatory dendritic cells. J. Exp. Med. 1988; 167: 700–5. | Article | PubMed | ISI | ChemPort |
- Lu L, McCaslin D, Starzl TE, Thomson AW. Bone marrowderived dendritic cell progenitors (NLDC 145+, MHC class II+, B7-ldim, B7-2-) induce alloantigen-specific hyporesponsiveness in murine T lymphocytes. Transplantation 1995; 60: 1539–45. | PubMed | ChemPort |
- Sallusto F, Lanzavecchia A. 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. 1994; 179: 1109–18. | Article | PubMed | ISI | ChemPort |
- Kimber I, Cumberbatch M. Stimulation of Langerhans cell migration by tumor necrosis factor alpha (TNF-alpha). J. Invest. Dermatol. 1992; 99 (Suppl. 5): S48–50.
- Cumberbatch M, Kimber I. Dermal tumour necrosis factor alpha induces dendritic cell migration to draining lymph nodes, and possibly provides one stimulus for Langerhans' cell migration. Immunology 1992; 75: 257–63. | PubMed | ISI | ChemPort |
- Steinman R, Hoffman L, Pope M. Maturation and migration of cutaneous dendritic cells. J. Invest. Dermatol. 1995; 105 (Suppl. 1): S2–7.
- Peguet Navarro J, Dalbiez Gauthier C, Dezutter Dambuyant C, Schmitt D. Dissection of human Langerhans cells' allostimulatory function: the need for an activation step for full development of accessory function. Eur. J. Immunol. 1993; 23: 376–82.
- Lutz MB, Assmann CU, Girolomoni G, Ricciardi Castagnoli P. Different cytokines regulate antigen uptake and presentation of a precursor dendritic cell line. Eur. J. Immunol. 1996; 26: 586–94. | Article | PubMed | ISI | ChemPort |