Light-mediated discovery of surfaceome nanoscale organization and intercellular receptor interaction networks

Maik Müller, Fabienne Gräbnitz, Niculò Barandun, Yang Shen, Fabian Wendt, Sebastian N. Steiner, Yannik Severin, Stefan U. Vetterli, Milon Mondal, James R. Prudent, Raphael Hofmann, Marc Oostrum, Roman C. Sarott, Alexey I. Nesvizhskii, Erick M. Carreira, Jeffrey W. Bode, Berend Snijder, John A. Robinson, Martin J. Loessner, Annette Oxenius and Bernd Wollscheid ()
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Maik Müller: ETH Zurich, Institute of Translational Medicine (ITM)
Fabienne Gräbnitz: ETH Zurich, Institute of Microbiology
Niculò Barandun: ETH Zurich, Institute of Microbiology
Yang Shen: Institute of Food Nutrition and Health, Department of Health Sciences and Technology, ETH Zurich
Fabian Wendt: ETH Zurich, Institute of Translational Medicine (ITM)
Sebastian N. Steiner: ETH Zurich, Institute of Translational Medicine (ITM)
Yannik Severin: Institute of Molecular Systems Biology, Department of Biology, ETH Zurich
Stefan U. Vetterli: University of Zurich
Milon Mondal: University of Zurich
James R. Prudent: Centrose LLC
Raphael Hofmann: ETH Zurich
Marc Oostrum: ETH Zurich, Institute of Translational Medicine (ITM)
Roman C. Sarott: ETH Zurich
Alexey I. Nesvizhskii: University of Michigan
Erick M. Carreira: ETH Zurich
Jeffrey W. Bode: ETH Zurich
Berend Snijder: Swiss Institute of Bioinformatics (SIB)
John A. Robinson: University of Zurich
Martin J. Loessner: Institute of Food Nutrition and Health, Department of Health Sciences and Technology, ETH Zurich
Annette Oxenius: ETH Zurich, Institute of Microbiology
Bernd Wollscheid: ETH Zurich, Institute of Translational Medicine (ITM)

Nature Communications, 2021, vol. 12, issue 1, 1-17

Abstract: Abstract The molecular nanoscale organization of the surfaceome is a fundamental regulator of cellular signaling in health and disease. Technologies for mapping the spatial relationships of cell surface receptors and their extracellular signaling synapses would unlock theranostic opportunities to target protein communities and the possibility to engineer extracellular signaling. Here, we develop an optoproteomic technology termed LUX-MS that enables the targeted elucidation of acute protein interactions on and in between living cells using light-controlled singlet oxygen generators (SOG). By using SOG-coupled antibodies, small molecule drugs, biologics and intact viral particles, we demonstrate the ability of LUX-MS to decode ligand receptor interactions across organisms and to discover surfaceome receptor nanoscale organization with direct implications for drug action. Furthermore, by coupling SOG to antigens we achieved light-controlled molecular mapping of intercellular signaling within functional immune synapses between antigen-presenting cells and CD8+ T cells providing insights into T cell activation with spatiotemporal specificity. LUX-MS based decoding of surfaceome signaling architectures thereby provides a molecular framework for the rational development of theranostic strategies.

Date: 2021
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DOI: 10.1038/s41467-021-27280-x

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