Presentation of Exogenous Protein Antigens by Dendritic Cells to T Cell Clones. Intact Protein is Presented Best by Immature, Epidermal Langerhans Cells

Overview

Journal J Exp Med

Specialties Allergy & Immunology
General Medicine

Date 1989 Mar 1

PMID 2522497

Citations 129

Authors

N Romani

S Koide

M Crowley

A M Livingstone

C G Fathman

K Inaba

R M Steinman

Affiliations

Soon will be listed here.

Abstract

The capacity of dendritic cells to present protein antigens has been studied with two MHC class II-restricted, myoglobin-specific, T cell clones. Spleen dendritic cells and cultured epidermal Langerhans cells (LC) presented native myoglobin weakly and often not at all. These same populations were powerful stimulators of allogeneic T cells in the primary MLR. Freshly isolated LC were in contrast very active in presenting proteins to T cell clones but were weak stimulators of the MLR. Both fresh and cultured LC could present specific peptide fragments of myoglobin to the clones. These results suggest that dendritic cells in nonlymphoid tissues like skin can act as sentinels for presenting antigens in situ, their accessory function developing in two phases. First antigens are captured and appropriately presented. Further handling of antigen then is downregulated while the cells acquire strong sensitizing activity for the growth and function of resting T lymphocytes. The potent MLR stimulating activity of cultured epidermal LC and lymphoid dendritic cells probably reflects prior handling of antigens leading to the formation of allogeneic MHC-peptide complexes.

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References

Nussenzweig M, Steinman R . Contribution of dendritic cells to stimulation of the murine syngeneic mixed leukocyte reaction. J Exp Med. 1980; 151(5):1196-212. PMC: 2185855. DOI: 10.1084/jem.151.5.1196. View

Steinman R, Witmer M . Lymphoid dendritic cells are potent stimulators of the primary mixed leukocyte reaction in mice. Proc Natl Acad Sci U S A. 1978; 75(10):5132-6. PMC: 336278. DOI: 10.1073/pnas.75.10.5132. View

Knight S, BALFOUR B, OBrien J, Buttifant L, Sumerska T, Clarke J . Role of veiled cells in lymphocyte activation. Eur J Immunol. 1982; 12(12):1057-60. DOI: 10.1002/eji.1830121214. View

Schuler G, Aubock J, Linert J . Enrichment of epidermal Langerhans cells by immunoadsorption to Staphylococcus aureus cells. J Immunol. 1983; 130(5):2008-10. View

Austyn J, Steinman R, Weinstein D, Granelli-Piperno A, Palladino M . Dendritic cells initiate a two-stage mechanism for T lymphocyte proliferation. J Exp Med. 1983; 157(4):1101-15. PMC: 2186982. DOI: 10.1084/jem.157.4.1101. View

Pugh C, MacPherson G, Steer H . Characterization of nonlymphoid cells derived from rat peripheral lymph. J Exp Med. 1983; 157(6):1758-79. PMC: 2187049. DOI: 10.1084/jem.157.6.1758. View

Shimonkevitz R, Kappler J, Marrack P, Grey H . Antigen recognition by H-2-restricted T cells. I. Cell-free antigen processing. J Exp Med. 1983; 158(2):303-16. PMC: 2187345. DOI: 10.1084/jem.158.2.303. View

Inaba K, Steinman R, Van Voorhis W, Muramatsu S . Dendritic cells are critical accessory cells for thymus-dependent antibody responses in mouse and in man. Proc Natl Acad Sci U S A. 1983; 80(19):6041-5. PMC: 534356. DOI: 10.1073/pnas.80.19.6041. View

Inaba K, Steinman R . Resting and sensitized T lymphocytes exhibit distinct stimulatory (antigen-presenting cell) requirements for growth and lymphokine release. J Exp Med. 1984; 160(6):1717-35. PMC: 2187515. DOI: 10.1084/jem.160.6.1717. View

10.

Schuler G, Steinman R . Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J Exp Med. 1985; 161(3):526-46. PMC: 2187584. DOI: 10.1084/jem.161.3.526. View

11.

Takigawa M, Iwatsuki K, Yamada M, Okamoto H, Imamura S . The Langerhans cell granule is an adsorptive endocytic organelle. J Invest Dermatol. 1985; 85(1):12-5. DOI: 10.1111/1523-1747.ep12274494. View

12.

Steinman R, Inaba K . Stimulation of the primary mixed leukocyte reaction. Crit Rev Immunol. 1985; 5(4):331-48. View

13.

Delisi C, Berzofsky J . T-cell antigenic sites tend to be amphipathic structures. Proc Natl Acad Sci U S A. 1985; 82(20):7048-52. PMC: 391307. DOI: 10.1073/pnas.82.20.7048. View

14.

UNANUE E . Antigen-presenting function of the macrophage. Annu Rev Immunol. 1984; 2:395-428. DOI: 10.1146/annurev.iy.02.040184.002143. View

15.

Inaba K, Koide S, Steinman R . Properties of memory T lymphocytes isolated from the mixed leukocyte reaction. Proc Natl Acad Sci U S A. 1985; 82(22):7686-90. PMC: 391398. DOI: 10.1073/pnas.82.22.7686. View

16.

Inaba K, Schuler G, Witmer M, Valinksy J, Atassi B, Steinman R . Immunologic properties of purified epidermal Langerhans cells. Distinct requirements for stimulation of unprimed and sensitized T lymphocytes. J Exp Med. 1986; 164(2):605-13. PMC: 2188243. DOI: 10.1084/jem.164.2.605. View

17.

Hanau D, Fabre M, Schmitt D, Garaud J, Pauly G, Tongio M . Human epidermal Langerhans cells cointernalize by receptor-mediated endocytosis "nonclassical" major histocompatibility complex class I molecules (T6 antigens) and class II molecules (HLA-DR antigens). Proc Natl Acad Sci U S A. 1987; 84(9):2901-5. PMC: 304768. DOI: 10.1073/pnas.84.9.2901. View

18.

Livingstone A, Fathman C . The structure of T-cell epitopes. Annu Rev Immunol. 1987; 5:477-501. DOI: 10.1146/annurev.iy.05.040187.002401. View

19.

Morel P, Livingstone A, Fathman C . Correlation of T cell receptor V beta gene family with MHC restriction. J Exp Med. 1987; 166(2):583-8. PMC: 2189600. DOI: 10.1084/jem.166.2.583. View

20.

Bjorkman P, Saper M, Samraoui B, Bennett W, Strominger J, Wiley D . The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature. 1987; 329(6139):512-8. DOI: 10.1038/329512a0. View