Stiffness of primordial germ cells is required for their extravasation in avian embryos

Daisuke Saito; Ryosuke Tadokoro; Arata Nagasaka; Daisuke Yoshino; Takayuki Teramoto; Kanta Mizumoto; Kenichi Funamoto; Hinako Kidokoro; Takaki Miyata; Koji Tamura; Yoshiko Takahashi

doi:10.1016/j.isci.2022.105629

Stiffness of primordial germ cells is required for their extravasation in avian embryos

iScience. 2022 Nov 18;25(12):105629. doi: 10.1016/j.isci.2022.105629. eCollection 2022 Dec 22.

Authors

Daisuke Saito^{1

2

3}, Ryosuke Tadokoro^{4

5}, Arata Nagasaka^{6

7}, Daisuke Yoshino^{1

8}, Takayuki Teramoto³, Kanta Mizumoto⁴, Kenichi Funamoto⁹, Hinako Kidokoro^{2

10}, Takaki Miyata⁷, Koji Tamura², Yoshiko Takahashi⁴

Affiliations

¹ Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Sendai, Miyagi 980-8578, Japan.
² Department of Ecological Developmental Adaptability Life Sciences, Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi 980-8578, Japan.
³ Department of Biology, Faculty of Science, Kyushu University, Fukuoka, Fukuoka 819-0395, Japan.
⁴ Department of Zoology, Graduate School of Science, Kyoto University, Kyoto, Kyoto 606-8502, Japan.
⁵ Department of Bioscience, Okayama University of Science, Okayama, Okayama 700-0005, Japan.
⁶ Division of Histology, Meikai University School of Dentistry, Sakado, Saitama 350-0283, Japan.
⁷ Department of Anatomy and Cell Biology, Nagoya University Graduate School of Medicine, Nagoya, Aichi 466-8550, Japan.
⁸ Institute of Engineering, Tokyo University of Agriculture and Technology, Koganei, Tokyo 184-8588, Japan.
⁹ Institute of Fluid Science, Tohoku University, Sendai, Miyagi 980-8577, Japan.
¹⁰ Organization for Research Initiatives and Development, Doshisha University, Kyotanabe, Kyoto 610-0394, Japan.

Abstract

Unlike mammals, primordial germ cells (PGCs) in avian early embryos exploit blood circulation to translocate to the somatic gonadal primordium, but how circulating PGCs undergo extravasation remains elusive. We demonstrate with single-cell level live-imaging analyses that the PGCs are arrested at a specific site in the capillary plexus, which is predominantly governed by occlusion at a narrow path in the vasculature. The occlusion is enabled by a heightened stiffness of the PGCs mediated by actin polymerization. Following the occlusion, PGCs reset their stiffness to soften in order to squeeze through the endothelial lining as they transmigrate. Our discovery also provides a model for the understanding of metastasizing cancer extravasation occurring mainly by occlusion.

Keywords: Biological sciences; Cell biology; Developmental biology.