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Self-organization and symmetry breaking in intestinal organoid development

Serra, Denise ; Mayr, Urs ; Boni, Andrea ; Lukonin, Ilya ; Rempfler, Markus ; Challet Meylan, Ludivine ; Stadler, Michael B ; Strnad, Petr ; Papasaikas, Panagiotis ; Vischi, Dario ; Waldt, Annick ; Roma, Guglielmo ; Liberali, Prisca

Nature (London), 2019-05, Vol.569 (7754), p.66-72 [Peer Reviewed Journal]

England: Nature Publishing Group

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Title:
Self-organization and symmetry breaking in intestinal organoid development
Author: Serra, Denise ; Mayr, Urs ; Boni, Andrea ; Lukonin, Ilya ; Rempfler, Markus ; Challet Meylan, Ludivine ; Stadler, Michael B ; Strnad, Petr ; Papasaikas, Panagiotis ; Vischi, Dario ; Waldt, Annick ; Roma, Guglielmo ; Liberali, Prisca
Subjects: Adaptor Proteins, Signal Transducing - genetics ; Adaptor Proteins, Signal Transducing - metabolism ; Animals ; Asymmetric structures ; Broken symmetry ; Calcium-Binding Proteins ; Cell Cycle Proteins ; Crypts ; DELTA protein ; Gene expression ; Intercellular Signaling Peptides and Proteins - metabolism ; Intestine ; Intestines ; Intestines - cytology ; Mice ; Observations ; Organoids ; Organoids - cytology ; Organoids - growth & development ; Organoids - metabolism ; Paneth cells ; Paneth Cells - cytology ; Phosphoproteins - genetics ; Phosphoproteins - metabolism ; Physiological aspects ; Receptors, G-Protein-Coupled - metabolism ; Regeneration ; Single-Cell Analysis ; Spheres ; Stem cells ; Symmetry ; Symmetry (Biology) ; Transcription activation ; YAP-Signaling Proteins ; Yes-associated protein
Is Part Of: Nature (London), 2019-05, Vol.569 (7754), p.66-72
Notes: ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
Current address: Viventis Microscopy Sàrl, EPFL Innovation Park, Building C, 1015 Lausanne, Switzerland
Description: Intestinal organoids are complex three-dimensional structures that mimic the cell-type composition and tissue organization of the intestine by recapitulating the self-organizing ability of cell populations derived from a single intestinal stem cell. Crucial in this process is a first symmetry-breaking event, in which only a fraction of identical cells in a symmetrical sphere differentiate into Paneth cells, which generate the stem-cell niche and lead to asymmetric structures such as the crypts and villi. Here we combine single-cell quantitative genomic and imaging approaches to characterize the development of intestinal organoids from single cells. We show that their development follows a regeneration process that is driven by transient activation of the transcriptional regulator YAP1. Cell-to-cell variability in YAP1, emerging in symmetrical spheres, initiates Notch and DLL1 activation, and drives the symmetry-breaking event and formation of the first Paneth cell. Our findings reveal how single cells exposed to a uniform growth-promoting environment have the intrinsic ability to generate emergent, self-organized behaviour that results in the formation of complex multicellular asymmetric structures.
Publisher: England: Nature Publishing Group
Language: English

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Self-organization and symmetry breaking in intestinal organoid development

Serra, Denise ; Mayr, Urs ; Boni, Andrea ; Lukonin, Ilya ; Rempfler, Markus ; Challet Meylan, Ludivine ; Stadler, Michael B ; Strnad, Petr ; Papasaikas, Panagiotis ; Vischi, Dario ; Waldt, Annick ; Roma, Guglielmo ; Liberali, Prisca

England: Nature Publishing Group

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