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Ordered Patterns of Cell Shape and Orientational Correlation during Spontaneous Cell Migration

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  • Yusuke T Maeda
  • Junya Inose
  • Miki Y Matsuo
  • Suguru Iwaya
  • Masaki Sano

Abstract

Background: In the absence of stimuli, most motile eukaryotic cells move by spontaneously coordinating cell deformation with cell movement in the absence of stimuli. Yet little is known about how cells change their own shape and how cells coordinate the deformation and movement. Here, we investigated the mechanism of spontaneous cell migration by using computational analyses. Methodology: We observed spontaneously migrating Dictyostelium cells in both a vegetative state (round cell shape and slow motion) and starved one (elongated cell shape and fast motion). We then extracted regular patterns of morphological dynamics and the pattern-dependent systematic coordination with filamentous actin (F-actin) and cell movement by statistical dynamic analyses. Conclusions/Significance: We found that Dictyostelium cells in both vegetative and starved states commonly organize their own shape into three ordered patterns, elongation, rotation, and oscillation, in the absence of external stimuli. Further, cells inactivated for PI3-kinase (PI3K) and/or PTEN did not show ordered patterns due to the lack of spatial control in pseudopodial formation in both the vegetative and starved states. We also found that spontaneous polarization was achieved in starved cells by asymmetric localization of PTEN and F-actin. This breaking of the symmetry of protein localization maintained the leading edge and considerably enhanced the persistence of directed migration, and overall random exploration was ensured by switching among the different ordered patterns. Our findings suggest that Dictyostelium cells spontaneously create the ordered patterns of cell shape mediated by PI3K/PTEN/F-actin and control the direction of cell movement by coordination with these patterns even in the absence of external stimuli.

Suggested Citation

  • Yusuke T Maeda & Junya Inose & Miki Y Matsuo & Suguru Iwaya & Masaki Sano, 2008. "Ordered Patterns of Cell Shape and Orientational Correlation during Spontaneous Cell Migration," PLOS ONE, Public Library of Science, vol. 3(11), pages 1-14, November.
  • Handle: RePEc:plo:pone00:0003734
    DOI: 10.1371/journal.pone.0003734
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    References listed on IDEAS

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    1. Liang Li & Simon F Nørrelykke & Edward C Cox, 2008. "Persistent Cell Motion in the Absence of External Signals: A Search Strategy for Eukaryotic Cells," PLOS ONE, Public Library of Science, vol. 3(5), pages 1-11, May.
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    1. Laurent Golé & Charlotte Rivière & Yoshinori Hayakawa & Jean-Paul Rieu, 2011. "A Quorum-Sensing Factor in Vegetative Dictyostelium Discoideum Cells Revealed by Quantitative Migration Analysis," PLOS ONE, Public Library of Science, vol. 6(11), pages 1-9, November.
    2. Taeseok Daniel Yang & Jin-Sung Park & Youngwoon Choi & Wonshik Choi & Tae-Wook Ko & Kyoung J Lee, 2011. "Zigzag Turning Preference of Freely Crawling Cells," PLOS ONE, Public Library of Science, vol. 6(6), pages 1-9, June.
    3. Thomas Kaindl & Harden Rieger & Lisa-Mareike Kaschel & Ulrike Engel & Anja Schmaus & Jonathan Sleeman & Motomu Tanaka, 2012. "Spatio-Temporal Patterns of Pancreatic Cancer Cells Expressing CD44 Isoforms on Supported Membranes Displaying Hyaluronic Acid Oligomers Arrays," PLOS ONE, Public Library of Science, vol. 7(8), pages 1-10, August.
    4. Hyun Gyu Lee & Kyoung J Lee, 2021. "Neighbor-enhanced diffusivity in dense, cohesive cell populations," PLOS Computational Biology, Public Library of Science, vol. 17(9), pages 1-26, September.

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