Abstract
The maintenance of peripheral naive T lymphocytes in humans is dependent on their homeostatic division, not continuing emigration from the thymus, which undergoes involution with age. However, postthymic maintenance of naive T cells is still poorly understood. Previously we reported that recent thymic emigrants (RTEs) are contained in CD31+CD25− naive T cells as defined by their levels of signal joint T cell receptor rearrangement excision circles (sjTRECs). Here, by differential gene expression analysis followed by protein expression and functional studies, we define that the naive T cells having divided the least since thymic emigration express complement receptors (CR1 and CR2) known to bind complement C3b- and C3d-decorated microbial products and, following activation, produce IL-8 (CXCL8), a major chemoattractant for neutrophils in bacterial defense. We also observed an IL-8–producing memory T cell subpopulation coexpressing CR1 and CR2 and with a gene expression signature resembling that of RTEs. The functions of CR1 and CR2 on T cells remain to be determined, but we note that CR2 is the receptor for Epstein-Barr virus, which is a cause of T cell lymphomas and a candidate environmental factor in autoimmune disease.
Highlights
The maintenance of a diverse, naive T cell repertoire arising from the thymus is critical for health [1]
CD31+CD25− naive CD4+ T cells decreased with age and this decrease was compensated for by the homeostatic maintenance of 3 subsets of naive T cells: CD31+CD25+, CD31−CD25−, and CD31−CD25+
complement receptor 2 (CR2), AOAH, TOX and CACHD1, an uncharacterized gene that may encode a protein that regulates voltage-dependent calcium channels, were higher in CD31+CD25− cells when they were compared with both CD31−CD25− (Figure 1C) and CD31+CD25+ cells (Supplemental Figure 1D)
Summary
The maintenance of a diverse, naive T cell repertoire arising from the thymus (recent thymic emigrants, RTEs) is critical for health [1]. Thymic involution decreases naive CD4+ T cell production with age in humans and is compensated for by the homeostatic maintenance of naive cells that have emigrated from the thymus earlier in life [2, 3]. CD31 (PECAM-1) expression identifies cells that have divided more often in the periphery (CD31−) from those that have not (CD31+), CD31+ T cells still divide as a function of age as evidenced by the approximately 5-fold dilution of signal joint T cell receptor rearrangement excision circles (sjTRECs) between the ages of 20 and 60 [2, 6].
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