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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
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    References listed on IDEAS

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    1. N. Barkai & S. Leibler, 1997. "Robustness in simple biochemical networks," Nature, Nature, vol. 387(6636), pages 913-917, June.
    2. U. Alon & M. G. Surette & N. Barkai & S. Leibler, 1999. "Robustness in bacterial chemotaxis," Nature, Nature, vol. 397(6715), pages 168-171, January.
    3. 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.
    4. 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.
    5. 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.
    6. Takashi Kurahashi & Anna Menini, 1997. "Mechanism of odorant adaptation in the olfactory receptor cell," Nature, Nature, vol. 385(6618), pages 725-729, February.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
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