IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0014624.html
   My bibliography  Save this article

Detection of Dynamic Spatiotemporal Response to Periodic Chemical Stimulation in a Xenopus Embryonic Tissue

Author

Listed:
  • YongTae Kim
  • Sagar D Joshi
  • William C Messner
  • Philip R LeDuc
  • Lance A Davidson

Abstract

Embryonic development is guided by a complex and integrated set of stimuli that results in collective system-wide organization that is both time and space regulated. These regulatory interactions result in the emergence of highly functional units, which are correlated to frequency-modulated stimulation profiles. We have determined the dynamic response of vertebrate embryonic tissues to highly controlled, time-varying localized chemical stimulation using a microfluidic system with feedback control. Our approach has enabled localized spatiotemporal manipulation of the steroid hormone dexamethasone (DEX) in Animal Cap (AC) tissues isolated from gastrulating Xenopus embryos. Using this approach we investigated cell-scale responses to precisely controlled stimulation by tracking the redistribution of a GFP-tagged DEX-reporter constructed from the human glucocorticoid receptor (GR). We exposed defined regions of a single AC explant to different stimulation conditions—continuous stimulation, periodic stimulation, and no stimulation. We observed collective behavior of the GR transport into the nucleus was first-order. Furthermore, the dynamic response was well-modeled by a first-order differential equation with a single time derivative. The model predicted that responses to periodic stimulations closely matched the results of the frequency-based experiments. We find that stimulation with localized bursts versus continuous stimulation can result in highly distinct responses. This finding is critical as controlled space and time exposure to growth factors is a hallmark of complex processes in embryonic development. These complex responses to cellular signaling and transport machinery were similar to emergent behaviors in other complex systems, suggesting that even within a complex embryonic tissue, the overall system can converge toward a predictive first-order response.

Suggested Citation

  • YongTae Kim & Sagar D Joshi & William C Messner & Philip R LeDuc & Lance A Davidson, 2011. "Detection of Dynamic Spatiotemporal Response to Periodic Chemical Stimulation in a Xenopus Embryonic Tissue," PLOS ONE, Public Library of Science, vol. 6(1), pages 1-11, January.
  • Handle: RePEc:plo:pone00:0014624
    DOI: 10.1371/journal.pone.0014624
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0014624
    Download Restriction: no

    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0014624&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pone.0014624?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. Javier Atencia & David J. Beebe, 2005. "Controlled microfluidic interfaces," Nature, Nature, vol. 437(7059), pages 648-655, September.
    2. Long Cai & Chiraj K. Dalal & Michael B. Elowitz, 2008. "Frequency-modulated nuclear localization bursts coordinate gene regulation," Nature, Nature, vol. 455(7212), pages 485-490, September.
    3. Johannes Jaeger & Svetlana Surkova & Maxim Blagov & Hilde Janssens & David Kosman & Konstantin N. Kozlov & Manu & Ekaterina Myasnikova & Carlos E. Vanario-Alonso & Maria Samsonova & David H. Sharp & J, 2004. "Dynamic control of positional information in the early Drosophila embryo," Nature, Nature, vol. 430(6997), pages 368-371, July.
    4. Matthew Freeman, 2000. "Feedback control of intercellular signalling in development," Nature, Nature, vol. 408(6810), pages 313-319, November.
    5. Elena M. Lucchetta & Ji Hwan Lee & Lydia A. Fu & Nipam H. Patel & Rustem F. Ismagilov, 2005. "Dynamics of Drosophila embryonic patterning network perturbed in space and time using microfluidics," Nature, Nature, vol. 434(7037), pages 1134-1138, April.
    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. John R Lake & Keith C Heyde & Warren C Ruder, 2017. "Low-cost feedback-controlled syringe pressure pumps for microfluidics applications," PLOS ONE, Public Library of Science, vol. 12(4), pages 1-12, April.

    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. Stefano Ciliberti & Olivier C Martin & Andreas Wagner, 2007. "Robustness Can Evolve Gradually in Complex Regulatory Gene Networks with Varying Topology," PLOS Computational Biology, Public Library of Science, vol. 3(2), pages 1-10, February.
    2. Kolja Becker & Eva Balsa-Canto & Damjan Cicin-Sain & Astrid Hoermann & Hilde Janssens & Julio R Banga & Johannes Jaeger, 2013. "Reverse-Engineering Post-Transcriptional Regulation of Gap Genes in Drosophila melanogaster," PLOS Computational Biology, Public Library of Science, vol. 9(10), pages 1-16, October.
    3. Francisco J P Lopes & Fernando M C Vieira & David M Holloway & Paulo M Bisch & Alexander V Spirov, 2008. "Spatial Bistability Generates hunchback Expression Sharpness in the Drosophila Embryo," PLOS Computational Biology, Public Library of Science, vol. 4(9), pages 1-14, September.
    4. Ronald Thenius & Michael Bodi & Thomas Schmickl & Karl Crailsheim, 2013. "Novel method of virtual embryogenesis for structuring Artificial Neural Network controllers," Mathematical and Computer Modelling of Dynamical Systems, Taylor & Francis Journals, vol. 19(4), pages 375-387.
    5. Shawn C Little & Gašper Tkačik & Thomas B Kneeland & Eric F Wieschaus & Thomas Gregor, 2011. "The Formation of the Bicoid Morphogen Gradient Requires Protein Movement from Anteriorly Localized mRNA," PLOS Biology, Public Library of Science, vol. 9(3), pages 1-17, March.
    6. Andreas Doncic & Umut Eser & Oguzhan Atay & Jan M Skotheim, 2013. "An Algorithm to Automate Yeast Segmentation and Tracking," PLOS ONE, Public Library of Science, vol. 8(3), pages 1-11, March.
    7. Maksat Ashyraliyev & Ken Siggens & Hilde Janssens & Joke Blom & Michael Akam & Johannes Jaeger, 2009. "Gene Circuit Analysis of the Terminal Gap Gene huckebein," PLOS Computational Biology, Public Library of Science, vol. 5(10), pages 1-16, October.
    8. Brian S. Flowers & Ryan L. Hartman, 2012. "Particle Handling Techniques in Microchemical Processes," Challenges, MDPI, vol. 3(2), pages 1-18, August.
    9. Joachim Almquist & Loubna Bendrioua & Caroline Beck Adiels & Mattias Goksör & Stefan Hohmann & Mats Jirstrand, 2015. "A Nonlinear Mixed Effects Approach for Modeling the Cell-To-Cell Variability of Mig1 Dynamics in Yeast," PLOS ONE, Public Library of Science, vol. 10(4), pages 1-32, April.
    10. Ziya Kalay & Takahiro K Fujiwara & Akihiro Kusumi, 2012. "Confining Domains Lead to Reaction Bursts: Reaction Kinetics in the Plasma Membrane," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-8, March.
    11. Vera Bettenworth & Simon Vliet & Bartosz Turkowyd & Annika Bamberger & Heiko Wendt & Matthew McIntosh & Wieland Steinchen & Ulrike Endesfelder & Anke Becker, 2022. "Frequency modulation of a bacterial quorum sensing response," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    12. Gabriele Micali & Gerardo Aquino & David M Richards & Robert G Endres, 2015. "Accurate Encoding and Decoding by Single Cells: Amplitude Versus Frequency Modulation," PLOS Computational Biology, Public Library of Science, vol. 11(6), pages 1-21, June.
    13. Zhou, Peipei & Cai, Shuiming & Liu, Zengrong & Chen, Luonan & Wang, Ruiqi, 2013. "Coupling switches and oscillators as a means to shape cellular signals in biomolecular systems," Chaos, Solitons & Fractals, Elsevier, vol. 50(C), pages 115-126.
    14. Bernd Boehm & Henrik Westerberg & Gaja Lesnicar-Pucko & Sahdia Raja & Michael Rautschka & James Cotterell & Jim Swoger & James Sharpe, 2010. "The Role of Spatially Controlled Cell Proliferation in Limb Bud Morphogenesis," PLOS Biology, Public Library of Science, vol. 8(7), pages 1-21, July.
    15. Stradner, Jürgen & Thenius, Ronald & Zahadat, Payam & Hamann, Heiko & Crailsheim, Karl & Schmickl, Thomas, 2013. "Algorithmic requirements for swarm intelligence in differently coupled collective systems," Chaos, Solitons & Fractals, Elsevier, vol. 50(C), pages 100-114.
    16. David M Holloway & Francisco J P Lopes & Luciano da Fontoura Costa & Bruno A N Travençolo & Nina Golyandina & Konstantin Usevich & Alexander V Spirov, 2011. "Gene Expression Noise in Spatial Patterning: hunchback Promoter Structure Affects Noise Amplitude and Distribution in Drosophila Segmentation," PLOS Computational Biology, Public Library of Science, vol. 7(2), pages 1-18, February.
    17. David M Holloway & Alexander V Spirov, 2017. "Transcriptional bursting in Drosophila development: Stochastic dynamics of eve stripe 2 expression," PLOS ONE, Public Library of Science, vol. 12(4), pages 1-24, April.
    18. Debasish Mondal & Edward Dougherty & Abhishek Mukhopadhyay & Adria Carbo & Guang Yao & Jianhua Xing, 2014. "Systematic Reverse Engineering of Network Topologies: A Case Study of Resettable Bistable Cellular Responses," PLOS ONE, Public Library of Science, vol. 9(8), pages 1-12, August.
    19. Jens Grauer & Falko Schmidt & Jesús Pineda & Benjamin Midtvedt & Hartmut Löwen & Giovanni Volpe & Benno Liebchen, 2021. "Active droploids," Nature Communications, Nature, vol. 12(1), pages 1-8, December.
    20. Theodore J Perkins & Johannes Jaeger & John Reinitz & Leon Glass, 2006. "Reverse Engineering the Gap Gene Network of Drosophila melanogaster," PLOS Computational Biology, Public Library of Science, vol. 2(5), pages 1-12, May.

    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:pone00:0014624. 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.