Reconstruction and deconstruction of human somitogenesis in vitro

Yuchuan Miao, Yannis Djeffal, Alessandro Simone, Kongju Zhu, Jong Gwan Lee, Ziqi Lu, Andrew Silberfeld, Jyoti Rao, Oscar A. Tarazona, Alessandro Mongera, Pietro Rigoni, Margarete Diaz-Cuadros, Laura Min Sook Song, Stefano Talia and Olivier Pourquié ()
Additional contact information
Yuchuan Miao: Harvard Medical School
Yannis Djeffal: Harvard Medical School
Alessandro Simone: Duke University Medical Center
Kongju Zhu: Harvard Medical School
Jong Gwan Lee: Harvard Medical School
Ziqi Lu: Duke University Medical Center
Andrew Silberfeld: Harvard Medical School
Jyoti Rao: Harvard Medical School
Oscar A. Tarazona: Harvard Medical School
Alessandro Mongera: Harvard Medical School
Pietro Rigoni: Harvard Medical School
Margarete Diaz-Cuadros: Harvard Medical School
Laura Min Sook Song: Harvard Medical School
Stefano Talia: Duke University Medical Center
Olivier Pourquié: Harvard Medical School

Nature, 2023, vol. 614, issue 7948, 500-508

Abstract: Abstract The vertebrate body displays a segmental organization that is most conspicuous in the periodic organization of the vertebral column and peripheral nerves. This metameric organization is first implemented when somites, which contain the precursors of skeletal muscles and vertebrae, are rhythmically generated from the presomitic mesoderm. Somites then become subdivided into anterior and posterior compartments that are essential for vertebral formation and segmental patterning of the peripheral nervous system1–4. How this key somitic subdivision is established remains poorly understood. Here we introduce three-dimensional culture systems of human pluripotent stem cells called somitoids and segmentoids, which recapitulate the formation of somite-like structures with anteroposterior identity. We identify a key function of the segmentation clock in converting temporal rhythmicity into the spatial regularity of anterior and posterior somitic compartments. We show that an initial ‘salt and pepper’ expression of the segmentation gene MESP2 in the newly formed segment is transformed into compartments of anterior and posterior identity through an active cell-sorting mechanism. Our research demonstrates that the major patterning modules that are involved in somitogenesis, including the clock and wavefront, anteroposterior polarity patterning and somite epithelialization, can be dissociated and operate independently in our in vitro systems. Together, we define a framework for the symmetry-breaking process that initiates somite polarity patterning. Our work provides a platform for decoding general principles of somitogenesis and advancing knowledge of human development.

Date: 2023
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DOI: 10.1038/s41586-022-05655-4

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