CD1-mediated Gamma/delta T Cell Maturation of Dendritic Cells

Overview

Journal J Exp Med

Specialties Allergy & Immunology
General Medicine

Date 2002 Dec 18

PMID 12486100

Citations 90

Authors

David S Leslie

Michael S Vincent

Franca M Spada

Hiranmoy Das

Masahiko Sugita

Craig T Morita

Michael B Brenner

Affiliations

Soon will be listed here.

Abstract

Immature myeloid dendritic cells (DCs) express only low levels of major histocompatibility complex (MHC) class II but express high levels of CD1 a, b, and c antigen-presenting molecules at the cell surface. As Vdelta1+ gamma/delta T cells are the main tissue subset of gamma/delta T cells and they are known to recognize CD1c in the absence of specific foreign antigen recognition, we examined the possible interaction of these T cells with immature DCs. We show that CD1-restricted gamma/delta T cells can mediate the maturation of DCs. DC maturation required cell-cell contact and could be blocked by antibodies against CD1c. The maturation process was partially mediated by tumor necrosis factor alpha. Importantly, immature DCs matured in the presence of lipopolysaccharide and CD1-restricted gamma/delta T cells produced bioactive interleukin-12p70. In addition, these DCs were able to efficiently present peptide antigens to naive CD4+ T cells. CD1-restricted gamma/delta T cell recognition of immature DCs provides the human immune system with the capacity to rapidly generate a pool of mature DCs early during microbial invasion. This may be an important source of critical host signals for T helper type 1 polarization of antigen-specific naive T cells and the subsequent adaptive immune response.

Citing Articles

γδ T cells in oral diseases.

Wei X, Tan Y, Zhou G Inflamm Res. 2024; 73(5):867-876.

PMID: 38563967 DOI: 10.1007/s00011-024-01870-z.

From Host Defense to Metabolic Signatures: Unveiling the Role of γδ T Cells in Bacterial Infections.

Nanda N, Alphonse M Biomolecules. 2024; 14(2).

PMID: 38397462 PMC: 10886488. DOI: 10.3390/biom14020225.

IL-22 Binding Protein Controls IL-22-Driven Bleomycin-Induced Lung Injury.

Zhang Z, Chakawa M, Galeas-Pena M, Frydman J, Allen M, Jones M Am J Pathol. 2023; 194(3):338-352.

PMID: 38101567 PMC: 10913761. DOI: 10.1016/j.ajpath.2023.11.011.

γδ T Cells in the Tumor Microenvironment-Interactions With Other Immune Cells.

Chan K, Duarte J, Ostrouska S, Behren A Front Immunol. 2022; 13:894315.

PMID: 35880177 PMC: 9307934. DOI: 10.3389/fimmu.2022.894315.

SARS-CoV-2 spike and nucleocapsid proteins fail to activate human dendritic cells or γδ T cells.

Singh K, Cogan S, Elekes S, Murphy D, Cummins S, Curran R PLoS One. 2022; 17(7):e0271463.

PMID: 35834480 PMC: 9282473. DOI: 10.1371/journal.pone.0271463.

References

Mellman I, Steinman R . Dendritic cells: specialized and regulated antigen processing machines. Cell. 2001; 106(3):255-8. DOI: 10.1016/s0092-8674(01)00449-4. View

Rescigno M, Piguet V, Valzasina B, Lens S, Zubler R, French L . Fas engagement induces the maturation of dendritic cells (DCs), the release of interleukin (IL)-1beta, and the production of interferon gamma in the absence of IL-12 during DC-T cell cognate interaction: a new role for Fas ligand in inflammatory.... J Exp Med. 2000; 192(11):1661-8. PMC: 2193091. DOI: 10.1084/jem.192.11.1661. View

Grant E, Degano M, Rosat J, Stenger S, Modlin R, Wilson I . Molecular recognition of lipid antigens by T cell receptors. J Exp Med. 1999; 189(1):195-205. PMC: 1887682. DOI: 10.1084/jem.189.1.195. View

Steinman R, Inaba K, Turley S, Pierre P, Mellman I . Antigen capture, processing, and presentation by dendritic cells: recent cell biological studies. Hum Immunol. 1999; 60(7):562-7. DOI: 10.1016/s0198-8859(99)00030-0. View

Cella M, Scheidegger D, 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(2):747-52. PMC: 2192696. DOI: 10.1084/jem.184.2.747. View

Janeway Jr C, Medzhitov R . Innate immune recognition. Annu Rev Immunol. 2002; 20:197-216. DOI: 10.1146/annurev.immunol.20.083001.084359. View

Hilkens C, Kalinski P, de Boer M, Kapsenberg M . Human dendritic cells require exogenous interleukin-12-inducing factors to direct the development of naive T-helper cells toward the Th1 phenotype. Blood. 1997; 90(5):1920-6. View

Langenkamp A, Messi M, Lanzavecchia A, Sallusto F . Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat Immunol. 2001; 1(4):311-6. DOI: 10.1038/79758. View

De Paoli P, Gennari D, Martelli P, Basaglia G, Crovatto M, Battistin S . A subset of gamma delta lymphocytes is increased during HIV-1 infection. Clin Exp Immunol. 1991; 83(2):187-91. PMC: 1535251. DOI: 10.1111/j.1365-2249.1991.tb05612.x. View

10.

Morita , Lee , Leslie , Tanaka , Bukowski . Recognition of nonpeptide prenyl pyrophosphate antigens by human gammadelta T cells. Microbes Infect. 1999; 1(3):175-86. View

11.

Wu J, Groh V, Spies T . T cell antigen receptor engagement and specificity in the recognition of stress-inducible MHC class I-related chains by human epithelial gamma delta T cells. J Immunol. 2002; 169(3):1236-40. DOI: 10.4049/jimmunol.169.3.1236. View

12.

Porcelli S, Morita C, Brenner M . CD1b restricts the response of human CD4-8- T lymphocytes to a microbial antigen. Nature. 1992; 360(6404):593-7. DOI: 10.1038/360593a0. View

13.

Anderson D, Maraskovsky E, Billingsley W, Dougall W, Tometsko M, Roux E . A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature. 1997; 390(6656):175-9. DOI: 10.1038/36593. View

14.

Shreedhar V, Moodycliffe A, Ullrich S, Bucana C, Kripke M, Flores-Romo L . Dendritic cells require T cells for functional maturation in vivo. Immunity. 1999; 11(5):625-36. DOI: 10.1016/s1074-7613(00)80137-5. View

15.

Das H, Wang L, Kamath A, Bukowski J . Vgamma2Vdelta2 T-cell receptor-mediated recognition of aminobisphosphonates. Blood. 2001; 98(5):1616-8. DOI: 10.1182/blood.v98.5.1616. View

16.

Olive D, Dubreuil P, Mawas C . Two distinct TL-like molecular subsets defined by monoclonal antibodies on the surface of human thymocytes with different expression on leukemia lines. Immunogenetics. 1984; 20(3):253-64. DOI: 10.1007/BF00364207. View

17.

Sugita M, Grant E, van Donselaar E, Hsu V, Rogers R, Peters P . Separate pathways for antigen presentation by CD1 molecules. Immunity. 2000; 11(6):743-52. DOI: 10.1016/s1074-7613(00)80148-x. View

18.

Spada F, Grant E, Peters P, Sugita M, Melian A, Leslie D . Self-recognition of CD1 by gamma/delta T cells: implications for innate immunity. J Exp Med. 2000; 191(6):937-48. PMC: 2193122. DOI: 10.1084/jem.191.6.937. View

19.

Hviid L, Kurtzhals J, Adabayeri V, Loizon S, Kemp K, Goka B . Perturbation and proinflammatory type activation of V delta 1(+) gamma delta T cells in African children with Plasmodium falciparum malaria. Infect Immun. 2001; 69(5):3190-6. PMC: 98276. DOI: 10.1128/IAI.69.5.3190-3196.2001. View

20.

Bukowski J, Morita C, Brenner M . Human gamma delta T cells recognize alkylamines derived from microbes, edible plants, and tea: implications for innate immunity. Immunity. 1999; 11(1):57-65. DOI: 10.1016/s1074-7613(00)80081-3. View