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Self-organizing optic-cup morphogenesis in three-dimensional culture

Author

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  • Mototsugu Eiraku

    (Organogenesis and Neurogenesis Group, RIKEN Center for Developmental Biology
    Four-Dimensional Tissue Analysis Unit, RIKEN Center for Developmental Biology)

  • Nozomu Takata

    (Organogenesis and Neurogenesis Group, RIKEN Center for Developmental Biology)

  • Hiroki Ishibashi

    (Institute for Frontier Medical Sciences, Kyoto University)

  • Masako Kawada

    (Organogenesis and Neurogenesis Group, RIKEN Center for Developmental Biology)

  • Eriko Sakakura

    (Organogenesis and Neurogenesis Group, RIKEN Center for Developmental Biology
    Four-Dimensional Tissue Analysis Unit, RIKEN Center for Developmental Biology)

  • Satoru Okuda

    (Institute for Frontier Medical Sciences, Kyoto University)

  • Kiyotoshi Sekiguchi

    (Laboratory of Extracellular Matrix Biochemistry, Institute for Protein Research, Osaka University)

  • Taiji Adachi

    (Institute for Frontier Medical Sciences, Kyoto University
    Computational Cell Biomechanics Team, VCAD System Research Program)

  • Yoshiki Sasai

    (Organogenesis and Neurogenesis Group, RIKEN Center for Developmental Biology
    Four-Dimensional Tissue Analysis Unit, RIKEN Center for Developmental Biology)

Abstract

Balanced organogenesis requires the orchestration of multiple cellular interactions to create the collective cell behaviours that progressively shape developing tissues. It is currently unclear how individual, localized parts are able to coordinate with each other to develop a whole organ shape. Here we report the dynamic, autonomous formation of the optic cup (retinal primordium) structure from a three-dimensional culture of mouse embryonic stem cell aggregates. Embryonic-stem-cell-derived retinal epithelium spontaneously formed hemispherical epithelial vesicles that became patterned along their proximal–distal axis. Whereas the proximal portion differentiated into mechanically rigid pigment epithelium, the flexible distal portion progressively folded inward to form a shape reminiscent of the embryonic optic cup, exhibited interkinetic nuclear migration and generated stratified neural retinal tissue, as seen in vivo. We demonstrate that optic-cup morphogenesis in this simple cell culture depends on an intrinsic self-organizing program involving stepwise and domain-specific regulation of local epithelial properties.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:nature:v:472:y:2011:i:7341:d:10.1038_nature09941
    DOI: 10.1038/nature09941
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    Cited by:

    1. 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.
    2. 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.
    3. 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.

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