IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33115-0.html
   My bibliography  Save this article

Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues

Author

Listed:
  • Guillermo Martínez-Ara

    (European Molecular Biology Laboratory (EMBL) Barcelona)

  • Núria Taberner

    (European Molecular Biology Laboratory (EMBL) Barcelona
    RIKEN Center for Biosystems Dynamics Research (RIKEN BDR))

  • Mami Takayama

    (RIKEN Center for Biosystems Dynamics Research (RIKEN BDR))

  • Elissavet Sandaltzopoulou

    (European Molecular Biology Laboratory (EMBL) Barcelona)

  • Casandra E. Villava

    (European Molecular Biology Laboratory (EMBL) Barcelona)

  • Miquel Bosch-Padrós

    (The Barcelona Institute for Science and Technology (BIST))

  • Nozomu Takata

    (RIKEN Center for Biosystems Dynamics Research (RIKEN BDR))

  • Xavier Trepat

    (The Barcelona Institute for Science and Technology (BIST)
    Biomateriales y Nanomedicina (CIBER-BBN)
    Institució Catalana de Recerca i Estudis Avançats (ICREA))

  • Mototsugu Eiraku

    (RIKEN Center for Biosystems Dynamics Research (RIKEN BDR))

  • Miki Ebisuya

    (European Molecular Biology Laboratory (EMBL) Barcelona
    RIKEN Center for Biosystems Dynamics Research (RIKEN BDR))

Abstract

The emerging field of synthetic developmental biology proposes bottom-up approaches to examine the contribution of each cellular process to complex morphogenesis. However, the shortage of tools to manipulate three-dimensional (3D) shapes of mammalian tissues hinders the progress of the field. Here we report the development of OptoShroom3, an optogenetic tool that achieves fast spatiotemporal control of apical constriction in mammalian epithelia. Activation of OptoShroom3 through illumination in an epithelial Madin-Darby Canine Kidney (MDCK) cell sheet reduces the apical surface of the stimulated cells and causes displacements in the adjacent regions. Light-induced apical constriction provokes the folding of epithelial cell colonies on soft gels. Its application to murine and human neural organoids leads to thickening of neuroepithelia, apical lumen reduction in optic vesicles, and flattening in neuroectodermal tissues. These results show that spatiotemporal control of apical constriction can trigger several types of 3D deformation depending on the initial tissue context.

Suggested Citation

  • Guillermo Martínez-Ara & Núria Taberner & Mami Takayama & Elissavet Sandaltzopoulou & Casandra E. Villava & Miquel Bosch-Padrós & Nozomu Takata & Xavier Trepat & Mototsugu Eiraku & Miki Ebisuya, 2022. "Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33115-0
    DOI: 10.1038/s41467-022-33115-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33115-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-33115-0?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. Léo Valon & Ariadna Marín-Llauradó & Thomas Wyatt & Guillaume Charras & Xavier Trepat, 2017. "Optogenetic control of cellular forces and mechanotransduction," Nature Communications, Nature, vol. 8(1), pages 1-10, April.
    2. Madeline A. Lancaster & Magdalena Renner & Carol-Anne Martin & Daniel Wenzel & Louise S. Bicknell & Matthew E. Hurles & Tessa Homfray & Josef M. Penninger & Andrew P. Jackson & Juergen A. Knoblich, 2013. "Cerebral organoids model human brain development and microcephaly," Nature, Nature, vol. 501(7467), pages 373-379, September.
    3. Emiliano Izquierdo & Theresa Quinkler & Stefano De Renzis, 2018. "Guided morphogenesis through optogenetic activation of Rho signalling during early Drosophila embryogenesis," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    4. Kei Yamamoto & Haruko Miura & Motohiko Ishida & Yusuke Mii & Noriyuki Kinoshita & Shinji Takada & Naoto Ueno & Satoshi Sawai & Yohei Kondo & Kazuhiro Aoki, 2021. "Optogenetic relaxation of actomyosin contractility uncovers mechanistic roles of cortical tension during cytokinesis," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    5. Michael Elowitz & Wendell A. Lim, 2010. "Build life to understand it," Nature, Nature, vol. 468(7326), pages 889-890, December.
    6. Mototsugu Eiraku & Nozomu Takata & Hiroki Ishibashi & Masako Kawada & Eriko Sakakura & Satoru Okuda & Kiyotoshi Sekiguchi & Taiji Adachi & Yoshiki Sasai, 2011. "Self-organizing optic-cup morphogenesis in three-dimensional culture," Nature, Nature, vol. 472(7341), pages 51-56, 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. Ariadna Marín-Llauradó & Sohan Kale & Adam Ouzeri & Tom Golde & Raimon Sunyer & Alejandro Torres-Sánchez & Ernest Latorre & Manuel Gómez-González & Pere Roca-Cusachs & Marino Arroyo & Xavier Trepat, 2023. "Mapping mechanical stress in curved epithelia of designed size and shape," Nature Communications, Nature, vol. 14(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. Kei Yamamoto & Haruko Miura & Motohiko Ishida & Yusuke Mii & Noriyuki Kinoshita & Shinji Takada & Naoto Ueno & Satoshi Sawai & Yohei Kondo & Kazuhiro Aoki, 2021. "Optogenetic relaxation of actomyosin contractility uncovers mechanistic roles of cortical tension during cytokinesis," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    2. Ariadna Marín-Llauradó & Sohan Kale & Adam Ouzeri & Tom Golde & Raimon Sunyer & Alejandro Torres-Sánchez & Ernest Latorre & Manuel Gómez-González & Pere Roca-Cusachs & Marino Arroyo & Xavier Trepat, 2023. "Mapping mechanical stress in curved epithelia of designed size and shape," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Jessica D. Rosarda & Sarah Giles & Sarah Harkins-Perry & Elizabeth A. Mills & Martin Friedlander & R. Luke Wiseman & Kevin T. Eade, 2023. "Imbalanced unfolded protein response signaling contributes to 1-deoxysphingolipid retinal toxicity," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Hannah J. Gustafson & Nikolas Claussen & Stefano Renzis & Sebastian J. Streichan, 2022. "Patterned mechanical feedback establishes a global myosin gradient," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    5. Jessica M. Vanslambrouck & Sean B. Wilson & Ker Sin Tan & Ella Groenewegen & Rajeev Rudraraju & Jessica Neil & Kynan T. Lawlor & Sophia Mah & Michelle Scurr & Sara E. Howden & Kanta Subbarao & Melissa, 2022. "Enhanced metanephric specification to functional proximal tubule enables toxicity screening and infectious disease modelling in kidney organoids," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    6. Elizabeth A. Werren & Geneva R. LaForce & Anshika Srivastava & Delia R. Perillo & Shaokun Li & Katherine Johnson & Safa Baris & Brandon Berger & Samantha L. Regan & Christian D. Pfennig & Sonja Munnik, 2024. "TREX tetramer disruption alters RNA processing necessary for corticogenesis in THOC6 Intellectual Disability Syndrome," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    7. Wendiao Zhang & Ming Zhang & Zhenhong Xu & Hongye Yan & Huimin Wang & Jiamei Jiang & Juan Wan & Beisha Tang & Chunyu Liu & Chao Chen & Qingtuan Meng, 2023. "Human forebrain organoid-based multi-omics analyses of PCCB as a schizophrenia associated gene linked to GABAergic pathways," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    8. Anna Pagliaro & Roxy Finger & Iris Zoutendijk & Saskia Bunschuh & Hans Clevers & Delilah Hendriks & Benedetta Artegiani, 2023. "Temporal morphogen gradient-driven neural induction shapes single expanded neuroepithelium brain organoids with enhanced cortical identity," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    9. Yuqi Zhang & Yizeng Li & Keyata N. Thompson & Konstantin Stoletov & Qinling Yuan & Kaustav Bera & Se Jong Lee & Runchen Zhao & Alexander Kiepas & Yao Wang & Panagiotis Mistriotis & Selma A. Serra & Jo, 2022. "Polarized NHE1 and SWELL1 regulate migration direction, efficiency and metastasis," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    10. Sijia Zhou & Peng Li & Jiaying Liu & Juan Liao & Hao Li & Lin Chen & Zhihua Li & Qiongyu Guo & Karine Belguise & Bin Yi & Xiaobo Wang, 2022. "Two Rac1 pools integrate the direction and coordination of collective cell migration," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    11. Tatsuya Osaki & Tomoya Duenki & Siu Yu A. Chow & Yasuhiro Ikegami & Romain Beaubois & Timothée Levi & Nao Nakagawa-Tamagawa & Yoji Hirano & Yoshiho Ikeuchi, 2024. "Complex activity and short-term plasticity of human cerebral organoids reciprocally connected with axons," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    12. Maura Galimberti & Maria R. Nucera & Vittoria D. Bocchi & Paola Conforti & Elena Vezzoli & Matteo Cereda & Camilla Maffezzini & Raffaele Iennaco & Andrea Scolz & Andrea Falqui & Chiara Cordiglieri & M, 2024. "Huntington’s disease cellular phenotypes are rescued non-cell autonomously by healthy cells in mosaic telencephalic organoids," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    13. Nilay Kumar & Jennifer Rangel Ambriz & Kevin Tsai & Mayesha Sahir Mim & Marycruz Flores-Flores & Weitao Chen & Jeremiah J. Zartman & Mark Alber, 2024. "Balancing competing effects of tissue growth and cytoskeletal regulation during Drosophila wing disc development," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    14. Olga A. Balashova & Alexios A. Panoutsopoulos & Olesya Visina & Jacob Selhub & Paul S. Knoepfler & Laura N. Borodinsky, 2024. "Noncanonical function of folate through folate receptor 1 during neural tube formation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Adrien Méry & Artur Ruppel & Jean Revilloud & Martial Balland & Giovanni Cappello & Thomas Boudou, 2023. "Light-driven biological actuators to probe the rheology of 3D microtissues," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    16. Tom Brandstätter & David B. Brückner & Yu Long Han & Ricard Alert & Ming Guo & Chase P. Broedersz, 2023. "Curvature induces active velocity waves in rotating spherical tissues," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    17. Christina Kyrousi & Adam C. O’Neill & Agnieska Brazovskaja & Zhisong He & Pavel Kielkowski & Laure Coquand & Rossella Giaimo & Pierpaolo D’ Andrea & Alexander Belka & Andrea Forero Echeverry & Davide , 2021. "Extracellular LGALS3BP regulates neural progenitor position and relates to human cortical complexity," Nature Communications, Nature, vol. 12(1), pages 1-22, December.
    18. Teresa L. Rapp & Cole A. DeForest, 2023. "Tricolor visible wavelength-selective photodegradable hydrogel biomaterials," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    19. Elaine T. Lim & Yingleong Chan & Pepper Dawes & Xiaoge Guo & Serkan Erdin & Derek J. C. Tai & Songlei Liu & Julia M. Reichert & Mannix J. Burns & Ying Kai Chan & Jessica J. Chiang & Katharina Meyer & , 2022. "Orgo-Seq integrates single-cell and bulk transcriptomic data to identify cell type specific-driver genes associated with autism spectrum disorder," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    20. Pamela E. Capendale & Inés García-Rodríguez & Anoop T. Ambikan & Lance A. Mulder & Josse A. Depla & Eline Freeze & Gerrit Koen & Carlemi Calitz & Vikas Sood & Renata Vieira de Sá & Ujjwal Neogi & Dasj, 2024. "Parechovirus infection in human brain organoids: host innate inflammatory response and not neuro-infectivity correlates to neurologic disease," Nature Communications, Nature, vol. 15(1), pages 1-14, 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:13:y:2022:i:1:d:10.1038_s41467-022-33115-0. 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.