Simultaneous detection of membrane contact dynamics and associated Ca2+ signals by reversible chemogenetic reporters

Paloma García Casas, Michela Rossini, Linnea Påvénius, Mezida Saeed, Nikita Arnst, Sonia Sonda, Tânia Fernandes, Irene D’Arsiè, Matteo Bruzzone, Valeria Berno, Andrea Raimondi, Maria Livia Sassano, Luana Naia, Elisa Barbieri, Sara Sigismund, Patrizia Agostinis, Mattia Sturlese, Barbara A. Niemeyer, Hjalmar Brismar, Maria Ankarcrona, Arnaud Gautier, Paola Pizzo () and Riccardo Filadi ()
Additional contact information
Paloma García Casas: University of Padua
Michela Rossini: University of Padua
Linnea Påvénius: Karolinska Institutet
Mezida Saeed: Royal Institute of Technology
Nikita Arnst: University of Padua
Sonia Sonda: University of Padua
Tânia Fernandes: University of Padua
Irene D’Arsiè: University of Padua
Matteo Bruzzone: University of Padua
Valeria Berno: IRCCS San Raffaele Scientific Institute
Andrea Raimondi: IRCCS San Raffaele Scientific Institute
Maria Livia Sassano: KU Leuven
Luana Naia: Karolinska Institutet
Elisa Barbieri: European Institute of Oncology IRCCS
Sara Sigismund: European Institute of Oncology IRCCS
Patrizia Agostinis: KU Leuven
Mattia Sturlese: University of Padua
Barbara A. Niemeyer: Saarland University
Hjalmar Brismar: Karolinska Institutet
Maria Ankarcrona: Karolinska Institutet
Arnaud Gautier: LBM
Paola Pizzo: University of Padua
Riccardo Filadi: University of Padua

Nature Communications, 2024, vol. 15, issue 1, 1-21

Abstract: Abstract Membrane contact sites (MCSs) are hubs allowing various cell organelles to coordinate their activities. The dynamic nature of these sites and their small size hinder analysis by current imaging techniques. To overcome these limitations, we here design a series of reversible chemogenetic reporters incorporating improved, low-affinity variants of splitFAST, and study the dynamics of different MCSs at high spatiotemporal resolution, both in vitro and in vivo. We demonstrate that these versatile reporters suit different experimental setups well, allowing one to address challenging biological questions. Using these probes, we identify a pathway in which calcium (Ca2+) signalling dynamically regulates endoplasmic reticulum-mitochondria juxtaposition, characterizing the underlying mechanism. Finally, by integrating Ca2+-sensing capabilities into the splitFAST technology, we introduce PRINCESS (PRobe for INterorganelle Ca2+-Exchange Sites based on SplitFAST), a class of reporters to simultaneously detect MCSs and measure the associated Ca2+ dynamics using a single biosensor.

Date: 2024
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DOI: 10.1038/s41467-024-52985-0

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