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High-throughput mechanical phenotyping and transcriptomics of single cells

Author

Listed:
  • Akifumi Shiomi

    (RIKEN
    Kyoto University)

  • 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
    Kyoto University)

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.

Suggested Citation

  • Akifumi Shiomi & Taikopaul Kaneko & Kaori Nishikawa & Arata Tsuchida & Takashi Isoshima & Mayuko Sato & Kiminori Toyooka & Kentaro Doi & Hidekazu Nishikii & Hirofumi Shintaku, 2024. "High-throughput mechanical phenotyping and transcriptomics of single cells," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48088-5
    DOI: 10.1038/s41467-024-48088-5
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    References listed on IDEAS

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    1. Kazuya Tsujita & Reiko Satow & Shinobu Asada & Yoshikazu Nakamura & Luis Arnes & Keisuke Sako & Yasuyuki Fujita & Kiyoko Fukami & Toshiki Itoh, 2021. "Homeostatic membrane tension constrains cancer cell dissemination by counteracting BAR protein assembly," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    2. Jin Suk Park & Christoph J. Burckhardt & Rossana Lazcano & Luisa M. Solis & Tadamoto Isogai & Linqing Li & Christopher S. Chen & Boning Gao & John D. Minna & Robert Bachoo & Ralph J. DeBerardinis & Ga, 2020. "Mechanical regulation of glycolysis via cytoskeleton architecture," Nature, Nature, vol. 578(7796), pages 621-626, February.
    3. Kiyosumi Ochi & Maiko Morita & Adam C. Wilkinson & Atsushi Iwama & Satoshi Yamazaki, 2021. "Non-conditioned bone marrow chimeric mouse generation using culture-based enrichment of hematopoietic stem and progenitor cells," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
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