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A combined transcriptional and dynamic roadmap of single human pancreatic endocrine progenitors reveals proliferative capacity and differentiation continuum

View ORCID ProfileBelin Selcen Beydag-Tasöz, View ORCID ProfileJoyson Verner D’Costa, View ORCID ProfileLena Hersemann, View ORCID ProfileFederica Luppino, View ORCID ProfileYung Hae Kim, View ORCID ProfileChristoph Zechner, View ORCID ProfileAnne Grapin-Botton
doi: https://doi.org/10.1101/2021.12.15.472220
Belin Selcen Beydag-Tasöz
1The Novo Nordisk Foundation Center for Stem Cell Biology, Copenhagen, København N, 2200, Denmark
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Saxony 01307, Germany
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  • ORCID record for Belin Selcen Beydag-Tasöz
Joyson Verner D’Costa
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Saxony 01307, Germany
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  • ORCID record for Joyson Verner D’Costa
Lena Hersemann
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Saxony 01307, Germany
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  • ORCID record for Lena Hersemann
Federica Luppino
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Saxony 01307, Germany
3Center for Systems Biology Dresden, Dresden, 01307, Germany
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Yung Hae Kim
1The Novo Nordisk Foundation Center for Stem Cell Biology, Copenhagen, København N, 2200, Denmark
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Saxony 01307, Germany
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Christoph Zechner
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Saxony 01307, Germany
3Center for Systems Biology Dresden, Dresden, 01307, Germany
4Cluster of Excellence Physics of Life, TU Dresden, Dresden, 01062, Germany
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Anne Grapin-Botton
1The Novo Nordisk Foundation Center for Stem Cell Biology, Copenhagen, København N, 2200, Denmark
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Saxony 01307, Germany
3Center for Systems Biology Dresden, Dresden, 01307, Germany
4Cluster of Excellence Physics of Life, TU Dresden, Dresden, 01062, Germany
5Paul Langerhans Institute Dresden, TU Dresden, Dresden, 01062, Germany
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  • For correspondence: botton@mpi-cbg.de
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Summary

Basic helix-loop-helix genes, particularly proneural genes, are well-described triggers of cell differentiation, yet limited information exists on their dynamics, notably in human development. Here, we focus on Neurogenin 3 (NEUROG3), which is crucial for pancreatic endocrine lineage initiation. Using a double reporter to monitor endogenous NEUROG3 transcription and protein expression in single cells in 2D and 3D models of human pancreas development, we show peaks of expression for the RNA and protein at 22 and 11 hours respectively, approximately two-fold slower than in mice, and remarkable heterogeneity in peak expression levels all triggering differentiation. We also reveal that some human endocrine progenitors proliferate once, mainly at the onset of differentiation, rather than forming a subpopulation with sustained proliferation. Using reporter index-sorted single-cell RNA-seq data, we statistically map transcriptome to dynamic behaviors of cells in live imaging and uncover transcriptional states associated with variations in motility as NEUROG3 levels change, a method applicable to other contexts.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted December 16, 2021.
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A combined transcriptional and dynamic roadmap of single human pancreatic endocrine progenitors reveals proliferative capacity and differentiation continuum
Belin Selcen Beydag-Tasöz, Joyson Verner D’Costa, Lena Hersemann, Federica Luppino, Yung Hae Kim, Christoph Zechner, Anne Grapin-Botton
bioRxiv 2021.12.15.472220; doi: https://doi.org/10.1101/2021.12.15.472220
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A combined transcriptional and dynamic roadmap of single human pancreatic endocrine progenitors reveals proliferative capacity and differentiation continuum
Belin Selcen Beydag-Tasöz, Joyson Verner D’Costa, Lena Hersemann, Federica Luppino, Yung Hae Kim, Christoph Zechner, Anne Grapin-Botton
bioRxiv 2021.12.15.472220; doi: https://doi.org/10.1101/2021.12.15.472220

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