Interleukin-10 induces a long-term antigen-specific anergic state in human CD4+ T cells - PubMed (original) (raw)
Interleukin-10 induces a long-term antigen-specific anergic state in human CD4+ T cells
H Groux et al. J Exp Med. 1996.
Abstract
Human CD4+ T cells, activated by allogeneic monocytes in a primary mixed lymphocyte reaction in the presence of exogenous interleukin (IL) 10, specifically failed to proliferate after restimulation with the same alloantigens. A comparable state of T cell unresponsiveness could be induced by activation of CD4+ T cells by cross-linked anti-CD3 monoclonal antibodies (mAbs) in the presence of exogenous IL-10. The anergic T cells failed to produce IL-2, IL-5, IL-10, interferon gamma, tumor necrosis factor alpha, and granulocyte/macrophage colony-stimulating factor. The IL-10-induced anergic state was long-lasting. T cell anergy could not be reversed after restimulation of the cells with anti-CD3 and anti-CD28 mAbs, although CD3 and CD28 expression was normal. In addition, restimulation of anergized T cells with anti-CD3 mAbs induced normal Ca2+ fluxes and resulted in increased CD3, CD28, and class II major histocompatibility complex expression, indicating that calcineurin-mediated signaling occurs in these anergic cells. However, the expression of the IL-2 receptor alpha chain was not upregulated, which may account for the failure of exogenous IL-2 to reverse the anergic state. Interestingly, anergic T cells and their nonanergic counterparts showed comparable levels of proliferation and cytokine production after activation with phorbol myristate acetate and Ca2+ ionophore, indicating that a direct activation of a protein kinase C-dependent pathway can overcome the tolerizing effect of IL-10. Taken together, these data demonstrate that IL-10 induces T cell anergy and therefore may play an important role in the induction and maintenance of antigen-specific T cell tolerance.
Comment in
- Models of T cell anergy: is there a common molecular mechanism?
Schwartz RH. Schwartz RH. J Exp Med. 1996 Jul 1;184(1):1-8. doi: 10.1084/jem.184.1.1. J Exp Med. 1996. PMID: 8691122 Free PMC article. Review. No abstract available.
Similar articles
- Immunologic self-tolerance maintained by CD25+CD4+ naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state.
Takahashi T, Kuniyasu Y, Toda M, Sakaguchi N, Itoh M, Iwata M, Shimizu J, Sakaguchi S. Takahashi T, et al. Int Immunol. 1998 Dec;10(12):1969-80. doi: 10.1093/intimm/10.12.1969. Int Immunol. 1998. PMID: 9885918 - IL-2 unresponsiveness in anergic CD4+ T cells is due to defective signaling through the common gamma-chain of the IL-2 receptor.
Grundström S, Dohlsten M, Sundstedt A. Grundström S, et al. J Immunol. 2000 Feb 1;164(3):1175-84. doi: 10.4049/jimmunol.164.3.1175. J Immunol. 2000. PMID: 10640728 - Mechanisms of interleukin-10-mediated immune suppression.
Akdis CA, Blaser K. Akdis CA, et al. Immunology. 2001 Jun;103(2):131-6. doi: 10.1046/j.1365-2567.2001.01235.x. Immunology. 2001. PMID: 11412299 Free PMC article. Review.
Cited by
- Syngeneic Mouse Models for Pre-Clinical Evaluation of CAR T Cells.
Ahmed EN, Cutmore LC, Marshall JF. Ahmed EN, et al. Cancers (Basel). 2024 Sep 18;16(18):3186. doi: 10.3390/cancers16183186. Cancers (Basel). 2024. PMID: 39335157 Free PMC article. Review. - Therapeutic induction of antigen-specific immune tolerance.
Kenison JE, Stevens NA, Quintana FJ. Kenison JE, et al. Nat Rev Immunol. 2024 May;24(5):338-357. doi: 10.1038/s41577-023-00970-x. Epub 2023 Dec 12. Nat Rev Immunol. 2024. PMID: 38086932 Free PMC article. Review. - CD4+CD25+FOXP3+ regulatory T cells: a potential "armor" to shield "transplanted allografts" in the war against ischemia reperfusion injury.
Jeyamogan S, Leventhal JR, Mathew JM, Zhang ZJ. Jeyamogan S, et al. Front Immunol. 2023 Oct 6;14:1270300. doi: 10.3389/fimmu.2023.1270300. eCollection 2023. Front Immunol. 2023. PMID: 37868962 Free PMC article. Review. - Role of Regulatory T Cells and Their Potential Therapeutic Applications in Celiac Disease.
Camarca A, Rotondi Aufiero V, Mazzarella G. Camarca A, et al. Int J Mol Sci. 2023 Sep 22;24(19):14434. doi: 10.3390/ijms241914434. Int J Mol Sci. 2023. PMID: 37833882 Free PMC article. Review. - Impact of immune tolerance mechanisms on the efficacy of immunotherapy in primary and secondary liver cancers.
Sankar K, Pearson AN, Worlikar T, Perricone MD, Holcomb EA, Mendiratta-Lala M, Xu Z, Bhowmick N, Green MD. Sankar K, et al. Transl Gastroenterol Hepatol. 2023 Jun 27;8:29. doi: 10.21037/tgh-23-11. eCollection 2023. Transl Gastroenterol Hepatol. 2023. PMID: 37601739 Free PMC article. Review.
References
- J Exp Med. 1991 Oct 1;174(4):915-24 - PubMed
- J Immunol. 1991 Nov 15;147(10):3261-7 - PubMed
- Immunol Today. 1992 Feb;13(2):69-73 - PubMed
- J Immunol. 1992 May 15;148(10):3133-9 - PubMed
- Science. 1992 Aug 7;257(5071):792-5 - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Research Materials
Miscellaneous