Two subsets of stem-like CD8 + memory T cell progenitors with distinct fate commitments in humans

Giovanni Galletti1, Gabriele De Simone1, Emilia M C Mazza1, Simone Puccio1, Claudia Mezzanotte2, Timothy M Bi3, Alexey N Davydov4, Maria Metsger4, Eloise Scamardella1, Giorgia Alvisi1, Federica De Paoli1, Veronica Zanon1, Alice Scarpa1, Barbara Camisa2, Federico S Colombo5, Achille Anselmo5, Clelia Peano6,7, Sara Polletti8, Domenico Mavilio9,10, Luca Gattinoni11,12,13, Shannon K Boi14, Benjamin A Youngblood14, Rhiannon E Jones15, Duncan M Baird15, Emma Gostick16, Sian Llewellyn-Lacey16, Kristin Ladell16, David A Price16,17, Dmitriy M Chudakov18,19,20, Evan W Newell3, Monica Casucci2, Enrico Lugli21,22

  1. Laboratory of Translational Immunology, Humanitas Clinical and Research Center - IRCCS, Rozzano, Milan, Italy.
  2. Innovative Immunotherapies Unit, Division of Immunology, Transplantation, and Infectious Diseases, IRCCS San Raffaele Scientific Institute, Milan, Italy.
  3. Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
  4. Central European Institute of Technology, Brno, Czech Republic.
  5. Humanitas Flow Cytometry Core, Humanitas Clinical and Research Center - IRCCS, Rozzano, Milan, Italy.
  6. Institute of Genetic and Biomedical Research, UoS Milan, National Research Council, Rozzano, Milan, Italy.
  7. Genomic Unit, Humanitas Clinical and Research Center - IRCCS, Rozzano, Milan, Italy.
  8. Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy.
  9. Unit of Clinical and Experimental Immunology, Humanitas Clinical and Research Center - IRCCS, Rozzano, Milan, Italy.
  10. Department of Medical Biotechnologies and Translational Medicine, University of Milan, Milan, Italy.
  11. Center for Cancer Research, National Cancer Institute, Bethesda, MD, USA.
  12. Regensburg Center for Interventional Immunology, Regensburg, Germany.
  13. University of Regensburg, Regensburg, Germany.
  14. St. Jude Children's Research Hospital, Memphis, TN, USA.
  15. Division of Cancer and Genetics, Cardiff University School of Medicine, Cardiff, UK.
  16. Division of Infection and Immunity, Cardiff University School of Medicine, Cardiff, UK.
  17. Systems Immunity Research Institute, Cardiff University School of Medicine, Cardiff, UK.
  18. Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russia.
  19. Pirogov Russian National Research Medical University, Moscow, Russia.
  20. Center of Life Sciences, Skolkovo Institute of Science and Technology, Moscow, Russia.
  21. Laboratory of Translational Immunology, Humanitas Clinical and Research Center - IRCCS, Rozzano, Milan, Italy. enrico.lugli@humanitasresearch.it.
  22. Humanitas Flow Cytometry Core, Humanitas Clinical and Research Center - IRCCS, Rozzano, Milan, Italy. enrico.lugli@humanitasresearch.it.

Abstract

T cell memory relies on the generation of antigen-specific progenitors with stem-like properties. However, the identity of these progenitors has remained unclear, precluding a full understanding of the differentiation trajectories that underpin the heterogeneity of antigen-experienced T cells. We used a systematic approach guided by single-cell RNA-sequencing data to map the organizational structure of the human CD8+ memory T cell pool under physiological conditions. We identified two previously unrecognized subsets of clonally, epigenetically, functionally, phenotypically and transcriptionally distinct stem-like CD8+ memory T cells. Progenitors lacking the inhibitory receptors programmed death-1 (PD-1) and T cell immunoreceptor with Ig and ITIM domains (TIGIT) were committed to a functional lineage, whereas progenitors expressing PD-1 and TIGIT were committed to a dysfunctional, exhausted-like lineage. Collectively, these data reveal the existence of parallel differentiation programs in the human CD8+ memory T cell pool, with potentially broad implications for the development of immunotherapies and vaccines.

Presented By Giovanni Galletti | ORCID iD