Mechanosensitive Channel-Based Optical Membrane Tension Reporter

Overview

Journal ACS Sens

Publisher American Chemical Society

Specialty Biotechnology

Date 2023 Jan 6

PMID 36608338

Authors

Yen-Yu Hsu

Agnes M Resto Irizarry

Jianping Fu

Allen P Liu

Affiliations

Soon will be listed here.

Abstract

Plasma membrane tension functions as a global physical organizer of cellular activities. Technical limitations of current membrane tension measurement techniques have hampered in-depth investigation of cellular membrane biophysics and the role of plasma membrane tension in regulating cellular processes. Here, we develop an optical membrane tension reporter by repurposing an mechanosensitive channel via insertion of circularly permuted GFP (cpGFP), which undergoes a large conformational rearrangement associated with channel activation and thus fluorescence intensity changes under increased membrane tension.

Citing Articles

Intracellular pressure controls the propagation of tension in crumpled cell membranes.

Dharan R, Barnoy A, Tsaturyan A, Grossman A, Goren S, Yosibash I Nat Commun. 2025; 16(1):91.

PMID: 39747015 PMC: 11696741. DOI: 10.1038/s41467-024-55398-1.

Force versus Response: Methods for Activating and Characterizing Mechanosensitive Ion Channels and GPCRs.

Roeterink R, Casadevall I Solvas X, Collins D, Scott D Adv Healthc Mater. 2024; 13(31):e2402167.

PMID: 39402780 PMC: 11650423. DOI: 10.1002/adhm.202402167.

Research progress on the regulatory role of cell membrane surface tension in cell behavior.

Li M, Xing X, Yuan J, Zeng Z Heliyon. 2024; 10(9):e29923.

PMID: 38720730 PMC: 11076917. DOI: 10.1016/j.heliyon.2024.e29923.

Cell Membrane Tension Gradients, Membrane Flows, and Cellular Processes.

Yan Q, Gomis Perez C, Karatekin E Physiology (Bethesda). 2024; 39(4).

PMID: 38501962 PMC: 11368524. DOI: 10.1152/physiol.00007.2024.

State-of-the-art in engineering small molecule biosensors and their applications in metabolic engineering.

Chaisupa P, Wright R SLAS Technol. 2023; 29(2):100113.

PMID: 37918525 PMC: 11314541. DOI: 10.1016/j.slast.2023.10.005.

References

Ridone P, Vassalli M, Martinac B . Piezo1 mechanosensitive channels: what are they and why are they important. Biophys Rev. 2019; 11(5):795-805. PMC: 6815293. DOI: 10.1007/s12551-019-00584-5. View

Rosholm K, Baker M, Ridone P, Nakayama Y, Rohde P, Cuello L . Activation of the mechanosensitive ion channel MscL by mechanical stimulation of supported Droplet-Hydrogel bilayers. Sci Rep. 2017; 7:45180. PMC: 5366917. DOI: 10.1038/srep45180. View

Heureaux J, Chen D, Murray V, Deng C, Liu A . Activation of a bacterial mechanosensitive channel in mammalian cells by cytoskeletal stress. Cell Mol Bioeng. 2015; 7(3):307-319. PMC: 4297646. DOI: 10.1007/s12195-014-0337-8. View

Martinac B . Mechanosensitive ion channels: molecules of mechanotransduction. J Cell Sci. 2004; 117(Pt 12):2449-60. DOI: 10.1242/jcs.01232. View

Colom A, Derivery E, Soleimanpour S, Tomba C, Molin M, Sakai N . A fluorescent membrane tension probe. Nat Chem. 2018; 10(11):1118-1125. PMC: 6197433. DOI: 10.1038/s41557-018-0127-3. View

Hofherr A, Fakler B, Klocker N . Selective Golgi export of Kir2.1 controls the stoichiometry of functional Kir2.x channel heteromers. J Cell Sci. 2005; 118(Pt 9):1935-43. DOI: 10.1242/jcs.02322. View

Houk A, Jilkine A, Mejean C, Boltyanskiy R, Dufresne E, Angenent S . Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration. Cell. 2012; 148(1-2):175-88. PMC: 3308728. DOI: 10.1016/j.cell.2011.10.050. View

Kirmizis D, Logothetidis S . Atomic force microscopy probing in the measurement of cell mechanics. Int J Nanomedicine. 2010; 5:137-45. PMC: 2865008. DOI: 10.2147/ijn.s5787. View

St-Pierre F, Marshall J, Yang Y, Gong Y, Schnitzer M, Lin M . High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor. Nat Neurosci. 2014; 17(6):884-9. PMC: 4494739. DOI: 10.1038/nn.3709. View

10.

Liu A, Chaudhuri O, Parekh S . New advances in probing cell-extracellular matrix interactions. Integr Biol (Camb). 2017; 9(5):383-405. PMC: 5708530. DOI: 10.1039/c6ib00251j. View

11.

Hochmuth R . Micropipette aspiration of living cells. J Biomech. 1999; 33(1):15-22. DOI: 10.1016/s0021-9290(99)00175-x. View

12.

Masters T, Pontes B, Viasnoff V, Li Y, Gauthier N . Plasma membrane tension orchestrates membrane trafficking, cytoskeletal remodeling, and biochemical signaling during phagocytosis. Proc Natl Acad Sci U S A. 2013; 110(29):11875-80. PMC: 3718161. DOI: 10.1073/pnas.1301766110. View

13.

Gonzalez N, Tao J, Rochman N, Vig D, Chiu E, Wirtz D . Cell tension and mechanical regulation of cell volume. Mol Biol Cell. 2018; 29(21). PMC: 6254581. DOI: 10.1091/mbc.E18-04-0213. View

14.

Heureaux-Torres J, Luker K, Haley H, Pirone M, Lee L, Herrera Y . The effect of mechanosensitive channel MscL expression in cancer cells on 3D confined migration. APL Bioeng. 2019; 2(3):032001. PMC: 6324216. DOI: 10.1063/1.5019770. View

15.

Perozo E, Cortes D, Sompornpisut P, Kloda A, Martinac B . Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature. 2002; 418(6901):942-8. DOI: 10.1038/nature00992. View

16.

Nussenzveig H . Cell membrane biophysics with optical tweezers. Eur Biophys J. 2017; 47(5):499-514. DOI: 10.1007/s00249-017-1268-9. View

17.

Shi Z, Graber Z, Baumgart T, Stone H, Cohen A . Cell Membranes Resist Flow. Cell. 2018; 175(7):1769-1779.e13. PMC: 6541487. DOI: 10.1016/j.cell.2018.09.054. View

18.

Raucher D, Sheetz M . Cell spreading and lamellipodial extension rate is regulated by membrane tension. J Cell Biol. 2000; 148(1):127-36. PMC: 2156205. DOI: 10.1083/jcb.148.1.127. View

19.

Wang Y, Wang N . FRET and mechanobiology. Integr Biol (Camb). 2009; 1(10):565-73. PMC: 2794131. DOI: 10.1039/b913093b. View

20.

Joseph J, Liu A . Mechanical Regulation of Endocytosis: New Insights and Recent Advances. Adv Biosyst. 2020; 4(5):e1900278. DOI: 10.1002/adbi.201900278. View