Extreme deformability of insect cell membranes is governed by phospholipid scrambling

Akifumi Shiomi; Kohjiro Nagao; Nobuhiro Yokota; Masaki Tsuchiya; Utako Kato; Naoto Juni; Yuji Hara; Masayuki X Mori; Yasuo Mori; Kumiko Ui-Tei; Motohide Murate; Toshihide Kobayashi; Yuri Nishino; Atsuo Miyazawa; Akihisa Yamamoto; Ryo Suzuki; Stefan Kaufmann; Motomu Tanaka; Kazuya Tatsumi; Kazuyoshi Nakabe; Hirofumi Shintaku; Semen Yesylevsky; Mikhail Bogdanov; Masato Umeda

doi:10.1016/j.celrep.2021.109219

Extreme deformability of insect cell membranes is governed by phospholipid scrambling

Cell Rep. 2021 Jun 8;35(10):109219. doi: 10.1016/j.celrep.2021.109219.

Authors

Akifumi Shiomi¹, Kohjiro Nagao², Nobuhiro Yokota¹, Masaki Tsuchiya¹, Utako Kato¹, Naoto Juni¹, Yuji Hara¹, Masayuki X Mori¹, Yasuo Mori¹, Kumiko Ui-Tei³, Motohide Murate⁴, Toshihide Kobayashi⁴, Yuri Nishino⁵, Atsuo Miyazawa⁵, Akihisa Yamamoto⁶, Ryo Suzuki⁶, Stefan Kaufmann⁷, Motomu Tanaka⁸, Kazuya Tatsumi⁹, Kazuyoshi Nakabe⁹, Hirofumi Shintaku¹⁰, Semen Yesylevsky¹¹, Mikhail Bogdanov¹², Masato Umeda¹³

Affiliations

¹ Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering, Kyoto University, Katsura, Kyoto 615-8510, Japan.
² Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering, Kyoto University, Katsura, Kyoto 615-8510, Japan. Electronic address: nagao@sbchem.kyoto-u.ac.jp.
³ Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
⁴ UMR 7021 CNRS, Faculté de Pharmacie, Université de Strasbourg, 74 Route du Rhin, 67401 Illkirch, France.
⁵ Graduate School of Life Science, University of Hyogo, Kouto, Kamigori-cho, Ako-gun, Hyogo 678-1297, Japan.
⁶ Center for Integrative Medicine and Physics, Institute for Advanced Study, Kyoto University, Kyoto 606-8501, Japan.
⁷ Physical Chemistry of Biosystems, Institute of Physical Chemistry, University of Heidelberg, 69120 Heidelberg, Germany.
⁸ Center for Integrative Medicine and Physics, Institute for Advanced Study, Kyoto University, Kyoto 606-8501, Japan; Physical Chemistry of Biosystems, Institute of Physical Chemistry, University of Heidelberg, 69120 Heidelberg, Germany.
⁹ Department of Mechanical Engineering and Science, Kyoto University, Katsura, Kyoto 615-8540, Japan.
¹⁰ Microfluidics RIKEN Hakubi Research Team, RIKEN Cluster for Pioneering Research, Wako, Saitama 351-0198, Japan.
¹¹ Laboratoire Chrono Environnement UMR CNRS 6249, Université de Bourgogne Franche-Comté, 16 Route de Gray, 25030 Besançon Cedex, France; Department of Physics of Biological Systems, Institute of Physics of the National Academy of Sciences of Ukraine, Prospect Nauky 46, 03680 Kyiv, Ukraine.
¹² Department of Biochemistry & Molecular Biology, University of Texas Health Science Center at Houston, McGovern Medical School, 6431 Fannin, Houston, TX 77030, USA.
¹³ Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering, Kyoto University, Katsura, Kyoto 615-8510, Japan. Electronic address: umeda@sbchem.kyoto-u.ac.jp.

PMID: 34107250
DOI: 10.1016/j.celrep.2021.109219

Abstract

Organization of dynamic cellular structure is crucial for a variety of cellular functions. In this study, we report that Drosophila and Aedes have highly elastic cell membranes with extremely low membrane tension and high resistance to mechanical stress. In contrast to other eukaryotic cells, phospholipids are symmetrically distributed between the bilayer leaflets of the insect plasma membrane, where phospholipid scramblase (XKR) that disrupts the lipid asymmetry is constitutively active. We also demonstrate that XKR-facilitated phospholipid scrambling promotes the deformability of cell membranes by regulating both actin cortex dynamics and mechanical properties of the phospholipid bilayer. Moreover, XKR-mediated construction of elastic cell membranes is essential for hemocyte circulation in the Drosophila cardiovascular system. Deformation of mammalian cells is also enhanced by the expression of Aedes XKR, and thus phospholipid scrambling may contribute to formation of highly deformable cell membranes in a variety of living eukaryotic cells.

Keywords: Drosophila; XK-related protein; actin cortex; hemocyte; insect; mechanical stress; membrane tension; phospholipid asymmetry; phospholipid scramblase; plasma membrane.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Cell Membrane / metabolism*
Drosophila
Insecta
Phospholipid Transfer Proteins / metabolism*

Substances

Phospholipid Transfer Proteins