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Membrane tension evolution and mechanical regulation of melittin-induced membrane poration |
| Wanting Zhang(张婉婷)1,2,†, Rong Xu(徐榕)1,2,†, Wendong Ma(马文东)1,3,†, Zhao Lin(林召)1,4, Kai Yang(杨恺)1,‡, and Bing Yuan(元冰)2,§ |
1 Center for Soft Condensed Matter Physics and Interdisciplinary Research & School of Physical Science and Technology, Soochow University, Suzhou 215006, China;
2 Songshan Lake Materials Laboratory, Dongguan 523808, China;
3 Biomedicine Discovery Institute, Infection & Immunity Program, Monash University, Melbourne, Australia;
4 Beijing National Laboratory for Condensed Matter Physics, Institute of Physics, Chinese Academy of Sciences, Beijing 100190, China |
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Abstract Membrane tension plays a crucial role in various fundamental cellular processes, with one notable example being the T cell-mediated elimination of tumor cells through perforin-induced membrane perforation by amplifying cellular force. However, the mechanisms governing the regulation of biomolecular activities at the cell interface by membrane tension remain elusive. In this study, we investigated the correlation between membrane tension and poration activity of melittin, a prototypical pore-forming peptide, using dynamic giant unilamellar vesicle leakage assays combined with flickering tension analysis, molecular dynamics simulations, and live cell assays. The results demonstrate that an increase in membrane tension enhances the activity of melittin, particularly near its critical pore-forming concentration. Moreover, peptide actions such as binding, insertion, and aggregation in the membrane further influence the evolution of membrane tension. Live cell experiments reveal that artificially enhancing membrane tension effectively enhances melittin's ability to induce pore formation and disrupt membranes, resulting in up to a ten-fold increase in A549 cell mortality when exposed to a concentration of 2.0-μg$\cdot$mL$^{-1}$ melittin. Our findings elucidate the relationship between membrane tension and the mechanism of action as well as pore-forming efficiency of melittin, while providing a practical mechanical approach for regulating functional activity of molecules at the cell-membrane interface.
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Received: 11 June 2024
Revised: 03 July 2024
Accepted manuscript online: 12 July 2024
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PACS:
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87.16.D-
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(Membranes, bilayers, and vesicles)
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87.15.K-
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(Molecular interactions; membrane-protein interactions)
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87.15.ap
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(Molecular dynamics simulation)
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87.15.La
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(Mechanical properties)
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| Fund: Project supported by the National Natural Science Foundation of China (Grant Nos. 12274307, 32230063, 21774092, and 12347102) and the Basic and Applied Basic Research Foundation of Guangdong Province, China (Grant No. 2023A1515011610). |
Corresponding Authors:
Kai Yang, Bing Yuan
E-mail: yangkai@suda.edu.cn;yuanbing@sslab.org.cn
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Cite this article:
Wanting Zhang(张婉婷), Rong Xu(徐榕), Wendong Ma(马文东), Zhao Lin(林召), Kai Yang(杨恺), and Bing Yuan(元冰) Membrane tension evolution and mechanical regulation of melittin-induced membrane poration 2024 Chin. Phys. B 33 108701
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