Lymphocyte innateness defined by transcriptional states reflects a balance between proliferation and effector functions

Maria Gutierrez-Arcelus, Nikola Teslovich, Alex R. Mola, Rafael B. Polidoro, Aparna Nathan, Hyun Kim, Susan Hannes, Kamil Slowikowski, Gerald F. M. Watts, Ilya Korsunsky, Michael B. Brenner, Soumya Raychaudhuri () and Patrick J. Brennan ()
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Maria Gutierrez-Arcelus: Harvard Medical School
Nikola Teslovich: Harvard Medical School
Alex R. Mola: Harvard Medical School
Rafael B. Polidoro: Harvard Medical School
Aparna Nathan: Harvard Medical School
Hyun Kim: Harvard Medical School
Susan Hannes: Harvard Medical School
Kamil Slowikowski: Harvard Medical School
Gerald F. M. Watts: Harvard Medical School
Ilya Korsunsky: Harvard Medical School
Michael B. Brenner: Harvard Medical School
Soumya Raychaudhuri: Harvard Medical School
Patrick J. Brennan: Harvard Medical School

Nature Communications, 2019, vol. 10, issue 1, 1-15

Abstract: Abstract How innate T cells (ITC), including invariant natural killer T (iNKT) cells, mucosal-associated invariant T (MAIT) cells, and γδ T cells, maintain a poised effector state has been unclear. Here we address this question using low-input and single-cell RNA-seq of human lymphocyte populations. Unbiased transcriptomic analyses uncover a continuous ‘innateness gradient’, with adaptive T cells at one end, followed by MAIT, iNKT, γδ T and natural killer cells at the other end. Single-cell RNA-seq reveals four broad states of innateness, and heterogeneity within canonical innate and adaptive populations. Transcriptional and functional data show that innateness is characterized by pre-formed mRNA encoding effector functions, but impaired proliferation marked by decreased baseline expression of ribosomal genes. Together, our data shed new light on the poised state of ITC, in which innateness is defined by a transcriptionally-orchestrated trade-off between rapid cell growth and rapid effector function.

Date: 2019
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DOI: 10.1038/s41467-019-08604-4

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