Universal recording of immune cell interactions in vivo

Sandra Nakandakari-Higa, Sarah Walker, Maria C. C. Canesso, Verena Heide, Aleksey Chudnovskiy, Dong-Yoon Kim, Johanne T. Jacobsen, Roham Parsa, Jana Bilanovic, S. Martina Parigi, Karol Fiedorczuk, Elaine Fuchs, Angelina M. Bilate, Giulia Pasqual, Daniel Mucida, Alice O. Kamphorst, Yuri Pritykin () and Gabriel D. Victora ()
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Sandra Nakandakari-Higa: The Rockefeller University
Sarah Walker: Princeton University
Maria C. C. Canesso: The Rockefeller University
Verena Heide: Icahn School of Medicine at Mount Sinai
Aleksey Chudnovskiy: The Rockefeller University
Dong-Yoon Kim: The Rockefeller University
Johanne T. Jacobsen: The Rockefeller University
Roham Parsa: The Rockefeller University
Jana Bilanovic: The Rockefeller University
S. Martina Parigi: The Rockefeller University
Karol Fiedorczuk: The Rockefeller University
Elaine Fuchs: The Rockefeller University
Angelina M. Bilate: The Rockefeller University
Giulia Pasqual: University of Padova
Daniel Mucida: The Rockefeller University
Alice O. Kamphorst: Icahn School of Medicine at Mount Sinai
Yuri Pritykin: Princeton University
Gabriel D. Victora: The Rockefeller University

Nature, 2024, vol. 627, issue 8003, 399-406

Abstract: Abstract Immune cells rely on transient physical interactions with other immune and non-immune populations to regulate their function1. To study these ‘kiss-and-run’ interactions directly in vivo, we previously developed LIPSTIC (labelling immune partnerships by SorTagging intercellular contacts)2, an approach that uses enzymatic transfer of a labelled substrate between the molecular partners CD40L and CD40 to label interacting cells. Reliance on this pathway limited the use of LIPSTIC to measuring interactions between CD4+ T helper cells and antigen-presenting cells, however. Here we report the development of a universal version of LIPSTIC (uLIPSTIC), which can record physical interactions both among immune cells and between immune and non-immune populations irrespective of the receptors and ligands involved. We show that uLIPSTIC can be used, among other things, to monitor the priming of CD8+ T cells by dendritic cells, reveal the steady-state cellular partners of regulatory T cells and identify germinal centre-resident T follicular helper cells on the basis of their ability to interact cognately with germinal centre B cells. By coupling uLIPSTIC with single-cell transcriptomics, we build a catalogue of the immune populations that physically interact with intestinal epithelial cells at the steady state and profile the evolution of the interactome of lymphocytic choriomeningitis virus-specific CD8+ T cells in multiple organs following systemic infection. Thus, uLIPSTIC provides a broadly useful technology for measuring and understanding cell–cell interactions across multiple biological systems.

Date: 2024
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DOI: 10.1038/s41586-024-07134-4

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