Intrinsically disordered protein biosensor tracks the physical-chemical effects of osmotic stress on cells

Cesar L. Cuevas-Velazquez (), Tamara Vellosillo, Karina Guadalupe, Hermann Broder Schmidt, Feng Yu, David Moses, Jennifer A. N. Brophy, Dante Cosio-Acosta, Alakananda Das, Lingxin Wang, Alexander M. Jones, Alejandra A. Covarrubias (), Shahar Sukenik () and José R. Dinneny ()
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Cesar L. Cuevas-Velazquez: Stanford University
Tamara Vellosillo: Stanford University
Karina Guadalupe: Center for Cellular and Biomolecular Machines (CCBM), University of California
Hermann Broder Schmidt: Stanford University School of Medicine
Feng Yu: Center for Cellular and Biomolecular Machines (CCBM), University of California
David Moses: Center for Cellular and Biomolecular Machines (CCBM), University of California
Jennifer A. N. Brophy: Stanford University
Dante Cosio-Acosta: Instituto de Biotecnología, Universidad Nacional Autónoma de México
Alakananda Das: Stanford University
Lingxin Wang: Stanford University
Alexander M. Jones: Sainsbury Laboratory, Cambridge University
Alejandra A. Covarrubias: Instituto de Biotecnología, Universidad Nacional Autónoma de México
Shahar Sukenik: Center for Cellular and Biomolecular Machines (CCBM), University of California
José R. Dinneny: Stanford University

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

Abstract: Abstract Cell homeostasis is perturbed when dramatic shifts in the external environment cause the physical-chemical properties inside the cell to change. Experimental approaches for dynamically monitoring these intracellular effects are currently lacking. Here, we leverage the environmental sensitivity and structural plasticity of intrinsically disordered protein regions (IDRs) to develop a FRET biosensor capable of monitoring rapid intracellular changes caused by osmotic stress. The biosensor, named SED1, utilizes the Arabidopsis intrinsically disordered AtLEA4-5 protein expressed in plants under water deficit. Computational modeling and in vitro studies reveal that SED1 is highly sensitive to macromolecular crowding. SED1 exhibits large and near-linear osmolarity-dependent changes in FRET inside living bacteria, yeast, plant, and human cells, demonstrating the broad utility of this tool for studying water-associated stress. This study demonstrates the remarkable ability of IDRs to sense the cellular environment across the tree of life and provides a blueprint for their use as environmentally-responsive molecular tools.

Date: 2021
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DOI: 10.1038/s41467-021-25736-8

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