Heterogeneous yet stable Vδ2(+) T-cell profiles define distinct cytotoxic effector potentials in healthy human individuals

Proc Natl Acad Sci U S A. 2016 Dec 13;113(50):14378-14383. doi: 10.1073/pnas.1611098113. Epub 2016 Nov 28.

Abstract

Human γδ T cells display potent responses to pathogens and malignancies. Of particular interest are those expressing a γδ T-cell receptor (TCR) incorporating TCRδ-chain variable-region-2 [Vδ2(+)], which are activated by pathogen-derived phosphoantigens (pAgs), or host-derived pAgs that accumulate in transformed cells or in cells exposed to aminobisphosphonates. Once activated, Vδ2(+) T cells exhibit multiple effector functions that have made them attractive candidates for immunotherapy. Despite this, clinical trials have reported mixed patient responses, highlighting a need for better understanding of Vδ2(+) T-cell biology. Here, we reveal previously unappreciated functional heterogeneity between the Vδ2(+) T-cell compartments of 63 healthy individuals. In this cohort, we identify distinct "Vδ2 profiles" that are stable over time; that do not correlate with age, gender, or history of phosphoantigen activation; and that develop after leaving the thymus. Multiple analyses suggest these Vδ2 profiles consist of variable proportions of two dominant but contrasting Vδ2(+) T-cell subsets that have divergent transcriptional programs and that display mechanistically distinct cytotoxic potentials. Importantly, an individual's Vδ2 profile predicts defined effector capacities, demonstrated by contrasting mechanisms and efficiencies of killing of a range of tumor cell lines. In short, these data support patient stratification to identify individuals with Vδ2 profiles that have effector mechanisms compatible with tumor killing and suggest that tailored Vδ2-profile-specific activation protocols may maximize the chances of future treatment success.

Keywords: Vδ2(+) T cells; antitumor cytotoxicity; functional heterogeneity; human immunology; human γδ T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • CX3C Chemokine Receptor 1 / metabolism
  • Child
  • Child, Preschool
  • Cytotoxicity, Immunologic
  • Female
  • Gene Expression Profiling
  • Genes, T-Cell Receptor delta
  • Healthy Volunteers
  • Humans
  • Immunophenotyping
  • Lymphocyte Activation / immunology
  • Male
  • Middle Aged
  • Receptors, Antigen, T-Cell, gamma-delta / genetics
  • Receptors, Antigen, T-Cell, gamma-delta / metabolism*
  • Receptors, CCR6 / metabolism
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocytes, Cytotoxic / immunology*
  • Young Adult

Substances

  • CCR6 protein, human
  • CX3C Chemokine Receptor 1
  • CX3CR1 protein, human
  • Receptors, Antigen, T-Cell, gamma-delta
  • Receptors, CCR6