IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42643-2.html
   My bibliography  Save this article

Optogenetic control of YAP reveals a dynamic communication code for stem cell fate and proliferation

Author

Listed:
  • Kirstin Meyer

    (University of California, San Francisco
    University of California, San Francisco)

  • Nicholas C. Lammers

    (University of California at Berkeley
    University of Washington)

  • Lukasz J. Bugaj

    (University of Pennsylvania)

  • Hernan G. Garcia

    (University of California at Berkeley
    University of California at Berkeley
    University of California Berkeley
    University of California at Berkeley)

  • Orion D. Weiner

    (University of California, San Francisco
    University of California, San Francisco)

Abstract

YAP is a transcriptional regulator that controls pluripotency, cell fate, and proliferation. How cells ensure the selective activation of YAP effector genes is unknown. This knowledge is essential to rationally control cellular decision-making. Here we leverage optogenetics, live-imaging of transcription, and cell fate analysis to understand and control gene activation and cell behavior. We reveal that cells decode the steady-state concentrations and timing of YAP activation to control proliferation, cell fate, and expression of the pluripotency regulators Oct4 and Nanog. While oscillatory YAP inputs induce Oct4 expression and proliferation optimally at frequencies that mimic native dynamics, cellular differentiation requires persistently low YAP levels. We identify the molecular logic of the Oct4 dynamic decoder, which acts through an adaptive change sensor. Our work reveals how YAP levels and dynamics enable multiplexing of information transmission for the regulation of developmental decision-making and establishes a platform for the rational control of these behaviors.

Suggested Citation

  • Kirstin Meyer & Nicholas C. Lammers & Lukasz J. Bugaj & Hernan G. Garcia & Orion D. Weiner, 2023. "Optogenetic control of YAP reveals a dynamic communication code for stem cell fate and proliferation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42643-2
    DOI: 10.1038/s41467-023-42643-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42643-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-42643-2?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. Ohad Gafni & Leehee Weinberger & Abed AlFatah Mansour & Yair S. Manor & Elad Chomsky & Dalit Ben-Yosef & Yael Kalma & Sergey Viukov & Itay Maza & Asaf Zviran & Yoach Rais & Zohar Shipony & Zohar Mukam, 2013. "Derivation of novel human ground state naive pluripotent stem cells," Nature, Nature, vol. 504(7479), pages 282-286, December.
    2. Takashi Kurahashi & Anna Menini, 1997. "Mechanism of odorant adaptation in the olfactory receptor cell," Nature, Nature, vol. 385(6618), pages 725-729, February.
    3. Yi I. Wu & Daniel Frey & Oana I. Lungu & Angelika Jaehrig & Ilme Schlichting & Brian Kuhlman & Klaus M. Hahn, 2009. "A genetically encoded photoactivatable Rac controls the motility of living cells," Nature, Nature, vol. 461(7260), pages 104-108, September.
    4. Sirio Dupont & Leonardo Morsut & Mariaceleste Aragona & Elena Enzo & Stefano Giulitti & Michelangelo Cordenonsi & Francesca Zanconato & Jimmy Le Digabel & Mattia Forcato & Silvio Bicciato & Nicola Elv, 2011. "Role of YAP/TAZ in mechanotransduction," Nature, Nature, vol. 474(7350), pages 179-183, June.
    5. N. Barkai & S. Leibler, 1997. "Robustness in simple biochemical networks," Nature, Nature, vol. 387(6636), pages 913-917, June.
    6. J. Matthew Franklin & Rajarshi P. Ghosh & Quanming Shi & Michael P. Reddick & Jan T. Liphardt, 2020. "Concerted localization-resets precede YAP-dependent transcription," Nature Communications, Nature, vol. 11(1), pages 1-18, December.
    7. U. Alon & M. G. Surette & N. Barkai & S. Leibler, 1999. "Robustness in bacterial chemotaxis," Nature, Nature, vol. 397(6715), pages 168-171, January.
    8. Jeremy B. Chang & James E. Ferrell Jr, 2013. "Mitotic trigger waves and the spatial coordination of the Xenopus cell cycle," Nature, Nature, vol. 500(7464), pages 603-607, August.
    9. Dominik Niopek & Pierre Wehler & Julia Roensch & Roland Eils & Barbara Di Ventura, 2016. "Optogenetic control of nuclear protein export," Nature Communications, Nature, vol. 7(1), pages 1-9, April.
    10. Lei Chang & Luca Azzolin & Daniele Di Biagio & Francesca Zanconato & Giusy Battilana & Romy Lucon Xiccato & Mariaceleste Aragona & Stefano Giulitti & Tito Panciera & Alessandro Gandin & Gianluca Sigis, 2018. "The SWI/SNF complex is a mechanoregulated inhibitor of YAP and TAZ," Nature, Nature, vol. 563(7730), pages 265-269, November.
    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. Jiaxi Zhao & Nicholas C. Lammers & Simon Alamos & Yang Joon Kim & Gabriella Martini & Hernan G. Garcia, 2024. "Optogenetic dissection of transcriptional repression in a multicellular organism," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

    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. Jae Kyoung Kim & Trachette L Jackson, 2013. "Mechanisms That Enhance Sustainability of p53 Pulses," PLOS ONE, Public Library of Science, vol. 8(6), pages 1-11, June.
    2. Junjie Luo & Jun Wang & Ting Martin Ma & Zhirong Sun, 2010. "Reverse Engineering of Bacterial Chemotaxis Pathway via Frequency Domain Analysis," PLOS ONE, Public Library of Science, vol. 5(3), pages 1-8, March.
    3. Jinlong Yuan & Lei Wang & Xu Zhang & Enmin Feng & Hongchao Yin & Zhilong Xiu, 2015. "Parameter identification for a nonlinear enzyme-catalytic dynamic system with time-delays," Journal of Global Optimization, Springer, vol. 62(4), pages 791-810, August.
    4. Miri Adler & Avi Mayo & Uri Alon, 2014. "Logarithmic and Power Law Input-Output Relations in Sensory Systems with Fold-Change Detection," PLOS Computational Biology, Public Library of Science, vol. 10(8), pages 1-14, August.
    5. Liyuan Zhu & Harold M. McNamara & Jared E. Toettcher, 2023. "Light-switchable transcription factors obtained by direct screening in mammalian cells," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Cornelis J. Boogerd & Ilaria Perini & Eirini Kyriakopoulou & Su Ji Han & Phit La & Britt Swaan & Jari B. Berkhout & Danielle Versteeg & Jantine Monshouwer-Kloots & Eva Rooij, 2023. "Cardiomyocyte proliferation is suppressed by ARID1A-mediated YAP inhibition during cardiac maturation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    7. 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.
    8. Zeina Shreif & Vipul Periwal, 2014. "A Network Characteristic That Correlates Environmental and Genetic Robustness," PLOS Computational Biology, Public Library of Science, vol. 10(2), pages 1-23, February.
    9. Diana Clausznitzer & Olga Oleksiuk & Linda Løvdok & Victor Sourjik & Robert G Endres, 2010. "Chemotactic Response and Adaptation Dynamics in Escherichia coli," PLOS Computational Biology, Public Library of Science, vol. 6(5), pages 1-11, May.
    10. Guillermo Rodrigo & Santiago F Elena, 2011. "Structural Discrimination of Robustness in Transcriptional Feedforward Loops for Pattern Formation," PLOS ONE, Public Library of Science, vol. 6(2), pages 1-7, February.
    11. Hongyu Shen & Xun Huang & Yiheng Zhao & Dongmei Wu & Kaili Xue & Jingfei Yao & Yushuang Wang & Nan Tang & Yifu Qiu, 2022. "The Hippo pathway links adipocyte plasticity to adipose tissue fibrosis," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    12. Burton W Andrews & Tau-Mu Yi & Pablo A Iglesias, 2006. "Optimal Noise Filtering in the Chemotactic Response of Escherichia coli," PLOS Computational Biology, Public Library of Science, vol. 2(11), pages 1-12, November.
    13. Diana Clausznitzer & Gabriele Micali & Silke Neumann & Victor Sourjik & Robert G Endres, 2014. "Predicting Chemical Environments of Bacteria from Receptor Signaling," PLOS Computational Biology, Public Library of Science, vol. 10(10), pages 1-14, October.
    14. 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.
    15. Robyn P. Araujo & Lance A. Liotta, 2023. "Universal structures for adaptation in biochemical reaction networks," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    16. Mintao Ji & Dongsheng Chen & Yinyin Shu & Shuai Dong & Zhisen Zhang & Haimeng Zheng & Xiaoni Jin & Lijun Zheng & Yang Liu & Yifei Zheng & Wensheng Zhang & Shiyou Wang & Guangming Zhou & Bingyan Li & B, 2023. "The role of mechano-regulated YAP/TAZ in erectile dysfunction," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    17. Aurore Claude-Taupin & Pierre Isnard & Alessia Bagattin & Nicolas Kuperwasser & Federica Roccio & Biagina Ruscica & Nicolas Goudin & Meriem Garfa-Traoré & Alice Regnier & Lisa Turinsky & Martine Burti, 2023. "The AMPK-Sirtuin 1-YAP axis is regulated by fluid flow intensity and controls autophagy flux in kidney epithelial cells," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    18. Oliver Pohl & Marius Hintsche & Zahra Alirezaeizanjani & Maximilian Seyrich & Carsten Beta & Holger Stark, 2017. "Inferring the Chemotactic Strategy of P. putida and E. coli Using Modified Kramers-Moyal Coefficients," PLOS Computational Biology, Public Library of Science, vol. 13(1), pages 1-24, January.
    19. Adel Dayarian & Madalena Chaves & Eduardo D Sontag & Anirvan M Sengupta, 2009. "Shape, Size, and Robustness: Feasible Regions in the Parameter Space of Biochemical Networks," PLOS Computational Biology, Public Library of Science, vol. 5(1), pages 1-12, January.
    20. Jiaxi Zhao & Nicholas C. Lammers & Simon Alamos & Yang Joon Kim & Gabriella Martini & Hernan G. Garcia, 2024. "Optogenetic dissection of transcriptional repression in a multicellular organism," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

    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:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42643-2. 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: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    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.