IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0026901.html
   My bibliography  Save this article

A Quorum-Sensing Factor in Vegetative Dictyostelium Discoideum Cells Revealed by Quantitative Migration Analysis

Author

Listed:
  • Laurent Golé
  • Charlotte Rivière
  • Yoshinori Hayakawa
  • Jean-Paul Rieu

Abstract

Background: Many cells communicate through the production of diffusible signaling molecules that accumulate and once a critical concentration has been reached, can activate or repress a number of target genes in a process termed quorum sensing (QS). In the social amoeba Dictyostelium discoideum, QS plays an important role during development. However little is known about its effect on cell migration especially in the growth phase. Methods and Findings: To investigate the role of cell density on cell migration in the growth phase, we use multisite timelapse microscopy and automated cell tracking. This analysis reveals a high heterogeneity within a given cell population, and the necessity to use large data sets to draw reliable conclusions on cell motion. In average, motion is persistent for short periods of time (), but normal diffusive behavior is recovered over longer time periods. The persistence times are positively correlated with the migrated distances. Interestingly, the migrated distance decreases as well with cell density. The adaptation of cell migration to cell density highlights the role of a secreted quorum sensing factor (QSF) on cell migration. Using a simple model describing the balance between the rate of QSF generation and the rate of QSF dilution, we were able to gather all experimental results into a single master curve, showing a sharp cell transition between high and low motile behaviors with increasing QSF. Conclusion: This study unambiguously demonstrates the central role played by QSF on amoeboid motion in the growth phase.

Suggested Citation

  • 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.
    • Handle: RePEc:plo:pone00:0026901
    DOI: 10.1371/journal.pone.0026901
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0026901
    Download Restriction: no
    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0026901&type=printable
    Download Restriction: no
    File URL: https://libkey.io/10.1371/journal.pone.0026901?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Alka A Potdar & Junhwan Jeon & Alissa M Weaver & Vito Quaranta & Peter T Cummings, 2010. "Human Mammary Epithelial Cells Exhibit a Bimodal Correlated Random Walk Pattern," PLOS ONE, Public Library of Science, vol. 5(3), pages 1-10, March.
    2. 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.
    3. Hiroaki Takagi & Masayuki J Sato & Toshio Yanagida & Masahiro Ueda, 2008. "Functional Analysis of Spontaneous Cell Movement under Different Physiological Conditions," PLOS ONE, Public Library of Science, vol. 3(7), pages 1-7, July.
    4. Leonard Bosgraaf & Peter J M Van Haastert, 2009. "The Ordered Extension of Pseudopodia by Amoeboid Cells in the Absence of External Cues," PLOS ONE, Public Library of Science, vol. 4(4), pages 1-13, April.
    5. Peter J M Van Haastert & Leonard Bosgraaf, 2009. "Food Searching Strategy of Amoeboid Cells by Starvation Induced Run Length Extension," PLOS ONE, Public Library of Science, vol. 4(8), pages 1-7, August.
    6. 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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Cao, Shan & Wang, Jiadao & Li, Dangguo & Chen, Darong, 2013. "Ecological and social modeling for migration and adhesion pattern of a benthic diatom," Ecological Modelling, Elsevier, vol. 250(C), pages 269-278.
    2. Can Guven & Erin Rericha & Edward Ott & Wolfgang Losert, 2013. "Modeling and Measuring Signal Relay in Noisy Directed Migration of Cell Groups," PLOS Computational Biology, Public Library of Science, vol. 9(5), pages 1-13, May.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Can Guven & Erin Rericha & Edward Ott & Wolfgang Losert, 2013. "Modeling and Measuring Signal Relay in Noisy Directed Migration of Cell Groups," PLOS Computational Biology, Public Library of Science, vol. 9(5), pages 1-13, May.
    2. Peter J M Van Haastert, 2010. "A Model for a Correlated Random Walk Based on the Ordered Extension of Pseudopodia," PLOS Computational Biology, Public Library of Science, vol. 6(8), pages 1-11, August.
    3. Priscila C A da Silva & Tiago V Rosembach & Anésia A Santos & Márcio S Rocha & Marcelo L Martins, 2014. "Normal and Tumoral Melanocytes Exhibit q-Gaussian Random Search Patterns," PLOS ONE, Public Library of Science, vol. 9(9), pages 1-13, September.
    4. Chopra, Abha & Nanjundiah, Vidyanand, 2013. "The precision with which single cells of Dictyostelium discoideum can locate a source of cyclic AMP," Chaos, Solitons & Fractals, Elsevier, vol. 50(C), pages 3-12.
    5. 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.
    6. de Almeida, Rita M.C. & Giardini, Guilherme S.Y. & Vainstein, Mendeli & Glazier, James A. & Thomas, Gilberto L., 2022. "Exact solution for the Anisotropic Ornstein–Uhlenbeck process," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 587(C).
    7. Azevedo, T.N. & Rizzi, L.G., 2022. "Time-correlated forces and biological variability in cell motility," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 604(C).
    8. Robert M Cooper & Ned S Wingreen & Edward C Cox, 2012. "An Excitable Cortex and Memory Model Successfully Predicts New Pseudopod Dynamics," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-12, March.
    9. Murguía, J.S. & Rosu, H.C. & Jimenez, A. & Gutiérrez-Medina, B. & García-Meza, J.V., 2015. "The Hurst exponents of Nitzschia sp. diatom trajectories observed by light microscopy," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 417(C), pages 176-184.
    10. Jonathan R. Potts, 2019. "Directionally Correlated Movement Can Drive Qualitative Changes in Emergent Population Distribution Patterns," Mathematics, MDPI, vol. 7(7), pages 1-11, July.
    11. Toman, Kellan & Voulgarakis, Nikolaos K., 2022. "Stochastic pursuit-evasion curves for foraging dynamics," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 597(C).
    12. 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.
    13. Yuta Yamamoto & Shota Miyazaki & Kenshiro Maruyama & Ryo Kobayashi & Minh Nguyen Tuyet Le & Ayumu Kano & Akiko Kondow & Shuji Fujii & Kiyoshi Ohnuma, 2018. "Random migration of induced pluripotent stem cell-derived human gastrulation-stage mesendoderm," PLOS ONE, Public Library of Science, vol. 13(9), pages 1-13, September.
    14. Sui Huang, 2016. "Where to Go: Breaking the Symmetry in Cell Motility," PLOS Biology, Public Library of Science, vol. 14(5), pages 1-10, May.
    15. 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.
    16. Tatiane Souza Vilela Podestá & Tiago Venzel Rosembach & Anésia Aparecida dos Santos & Marcelo Lobato Martins, 2017. "Anomalous diffusion and q-Weibull velocity distributions in epithelial cell migration," PLOS ONE, Public Library of Science, vol. 12(7), pages 1-19, July.
    17. Hélia Serrano & Ramón F. Álvarez-Estrada, 2023. "Characterization of the Mean First-Passage Time Function Subject to Advection in Annular-like Domains," Mathematics, MDPI, vol. 11(24), pages 1-17, December.
    18. Oliver Nagel & Can Guven & Matthias Theves & Meghan Driscoll & Wolfgang Losert & Carsten Beta, 2014. "Geometry-Driven Polarity in Motile Amoeboid Cells," PLOS ONE, Public Library of Science, vol. 9(12), pages 1-20, December.
    19. 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.
    20. Visakan Kadirkamanathan & Sean R Anderson & Stephen A Billings & Xiliang Zhang & Geoffrey R Holmes & Constantino C Reyes-Aldasoro & Philip M Elks & Stephen A Renshaw, 2012. "The Neutrophil's Eye-View: Inference and Visualisation of the Chemoattractant Field Driving Cell Chemotaxis In Vivo," PLOS ONE, Public Library of Science, vol. 7(4), pages 1-11, April.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pone00:0026901. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.