High-throughput mechanical phenotyping and transcriptomics of single cells

Akifumi Shiomi, Taikopaul Kaneko, Kaori Nishikawa, Arata Tsuchida, Takashi Isoshima, Mayuko Sato, Kiminori Toyooka, Kentaro Doi, Hidekazu Nishikii and Hirofumi Shintaku ()
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Akifumi Shiomi: RIKEN
Taikopaul Kaneko: RIKEN
Kaori Nishikawa: RIKEN
Arata Tsuchida: RIKEN
Takashi Isoshima: RIKEN
Mayuko Sato: RIKEN
Kiminori Toyooka: RIKEN
Kentaro Doi: Toyohashi University of Technology
Hidekazu Nishikii: University of Tsukuba
Hirofumi Shintaku: RIKEN

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: Abstract The molecular system regulating cellular mechanical properties remains unexplored at single-cell resolution mainly due to a limited ability to combine mechanophenotyping with unbiased transcriptional screening. Here, we describe an electroporation-based lipid-bilayer assay for cell surface tension and transcriptomics (ELASTomics), a method in which oligonucleotide-labelled macromolecules are imported into cells via nanopore electroporation to assess the mechanical state of the cell surface and are enumerated by sequencing. ELASTomics can be readily integrated with existing single-cell sequencing approaches and enables the joint study of cell surface mechanics and underlying transcriptional regulation at an unprecedented resolution. We validate ELASTomics via analysis of cancer cell lines from various malignancies and show that the method can accurately identify cell types and assess cell surface tension. ELASTomics enables exploration of the relationships between cell surface tension, surface proteins, and transcripts along cell lineages differentiating from the haematopoietic progenitor cells of mice. We study the surface mechanics of cellular senescence and demonstrate that RRAD regulates cell surface tension in senescent TIG-1 cells. ELASTomics provides a unique opportunity to profile the mechanical and molecular phenotypes of single cells and can dissect the interplay among these in a range of biological contexts.

Date: 2024
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DOI: 10.1038/s41467-024-48088-5

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