Single cell RNA sequencing identifies early diversity of sensory neurons forming via bi-potential intermediates

Louis Faure; Yiqiao Wang; Maria Eleni Kastriti; Paula Fontanet; Kylie K.Y. Cheung; Charles Petitpré; Haohao Wu; Lynn Linyu Sun; Karen Runge; Laura Croci; Mark A. Landy; Helen C. Lai; Gian Giacomo Consalez; Antoine de Chevigny; François Lallemend; Igor Adameyko; Saida Hadjab

doi:10.1038/s41467-020-17929-4

Single cell RNA sequencing identifies early diversity of sensory neurons forming via bi-potential intermediates

Louis Faure, Yiqiao Wang, Maria Eleni Kastriti, Paula Fontanet, Kylie K.Y. Cheung, Charles Petitpré, Haohao Wu, Lynn Linyu Sun, Karen Runge, Laura Croci, Mark A. Landy, Helen C. Lai, Gian Giacomo Consalez, Antoine de Chevigny, François Lallemend, Igor Adameyko, Saida Hadjab

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30 Scopus citations

Abstract

Somatic sensation is defined by the existence of a diversity of primary sensory neurons with unique biological features and response profiles to external and internal stimuli. However, there is no coherent picture about how this diversity of cell states is transcriptionally generated. Here, we use deep single cell analysis to resolve fate splits and molecular biasing processes during sensory neurogenesis in mice. Our results identify a complex series of successive and specific transcriptional changes in post-mitotic neurons that delineate hierarchical regulatory states leading to the generation of the main sensory neuron classes. In addition, our analysis identifies previously undetected early gene modules expressed long before fate determination although being clearly associated with defined sensory subtypes. Overall, the early diversity of sensory neurons is generated through successive bi-potential intermediates in which synchronization of relevant gene modules and concurrent repression of competing fate programs precede cell fate stabilization and final commitment.

Original language	English (US)
Article number	4175
Journal	Nature communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-17929-4
State	Published - Dec 1 2020

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

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10.1038/s41467-020-17929-4

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Faure, L., Wang, Y., Kastriti, M. E., Fontanet, P., Cheung, K. K. Y., Petitpré, C., Wu, H., Sun, L. L., Runge, K., Croci, L., Landy, M. A., Lai, H. C., Consalez, G. G., de Chevigny, A., Lallemend, F., Adameyko, I., & Hadjab, S. (2020). Single cell RNA sequencing identifies early diversity of sensory neurons forming via bi-potential intermediates. Nature communications, 11(1), [4175]. https://doi.org/10.1038/s41467-020-17929-4

Faure, L, Wang, Y, Kastriti, ME, Fontanet, P, Cheung, KKY, Petitpré, C, Wu, H, Sun, LL, Runge, K, Croci, L, Landy, MA, Lai, HC, Consalez, GG, de Chevigny, A, Lallemend, F, Adameyko, I & Hadjab, S 2020, 'Single cell RNA sequencing identifies early diversity of sensory neurons forming via bi-potential intermediates', Nature communications, vol. 11, no. 1, 4175. https://doi.org/10.1038/s41467-020-17929-4

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title = "Single cell RNA sequencing identifies early diversity of sensory neurons forming via bi-potential intermediates",

abstract = "Somatic sensation is defined by the existence of a diversity of primary sensory neurons with unique biological features and response profiles to external and internal stimuli. However, there is no coherent picture about how this diversity of cell states is transcriptionally generated. Here, we use deep single cell analysis to resolve fate splits and molecular biasing processes during sensory neurogenesis in mice. Our results identify a complex series of successive and specific transcriptional changes in post-mitotic neurons that delineate hierarchical regulatory states leading to the generation of the main sensory neuron classes. In addition, our analysis identifies previously undetected early gene modules expressed long before fate determination although being clearly associated with defined sensory subtypes. Overall, the early diversity of sensory neurons is generated through successive bi-potential intermediates in which synchronization of relevant gene modules and concurrent repression of competing fate programs precede cell fate stabilization and final commitment.",

author = "Louis Faure and Yiqiao Wang and Kastriti, {Maria Eleni} and Paula Fontanet and Cheung, {Kylie K.Y.} and Charles Petitpr{\'e} and Haohao Wu and Sun, {Lynn Linyu} and Karen Runge and Laura Croci and Landy, {Mark A.} and Lai, {Helen C.} and Consalez, {Gian Giacomo} and {de Chevigny}, Antoine and Fran{\c c}ois Lallemend and Igor Adameyko and Saida Hadjab",

note = "Funding Information: We thank Y. Groner and D. Levanon for the Runx3 mice; C. Ibanez for the R26tdTOM mice; A. Moqrich for the Fam19a4YFP; T. Jessell for the RUNX3 antibody; the CLICK imaging Facility supported by the Knut and Alice Wallenberg Foundation; Single Cell Facility at SciLife Laboratory. We are thankful to Jaromir Mikes for sorting the cells. We are grateful to Prof. Patrik Ernfors and Prof. Abdel El Manira for critical reading of the manuscript. We are also grateful to Dr. Ruslan A. Soldatov (Kharchenko Lab) for sharing codes. I.A. was supported by ERC Consolidator grant “STEMMING-FROM-NERVE”, Bertil Hallsten Foundation, Swedish Research Council, Paradifference Foundation. F.L. was supported by the Swedish Research Council (VR), the Ragnar S{\"o}derberg Foundation, Knut and Alice Wallenberg Foundation, Swedish Brain Foundation, Karolinska Institutet, the Karolinska Institutet Strategic Research program in Neuroscience (StratNeuro) and the Ming Wai Lau Foundation. L.F. is supported by the Austrian Science Fund DOC 33-B27. S.H. is supported by the Swedish Research Council (VR), the Swedish Brain Foundation and Kar-olinska Institutet. Open access funding provided by Karolinska Institute. Publisher Copyright: {\textcopyright} 2020, The Author(s).",

year = "2020",

month = dec,

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doi = "10.1038/s41467-020-17929-4",

language = "English (US)",

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T1 - Single cell RNA sequencing identifies early diversity of sensory neurons forming via bi-potential intermediates

AU - Faure, Louis

AU - Wang, Yiqiao

AU - Kastriti, Maria Eleni

AU - Fontanet, Paula

AU - Cheung, Kylie K.Y.

AU - Petitpré, Charles

AU - Wu, Haohao

AU - Sun, Lynn Linyu

AU - Runge, Karen

AU - Croci, Laura

AU - Landy, Mark A.

AU - Lai, Helen C.

AU - Consalez, Gian Giacomo

AU - de Chevigny, Antoine

AU - Lallemend, François

AU - Adameyko, Igor

AU - Hadjab, Saida

N1 - Funding Information: We thank Y. Groner and D. Levanon for the Runx3 mice; C. Ibanez for the R26tdTOM mice; A. Moqrich for the Fam19a4YFP; T. Jessell for the RUNX3 antibody; the CLICK imaging Facility supported by the Knut and Alice Wallenberg Foundation; Single Cell Facility at SciLife Laboratory. We are thankful to Jaromir Mikes for sorting the cells. We are grateful to Prof. Patrik Ernfors and Prof. Abdel El Manira for critical reading of the manuscript. We are also grateful to Dr. Ruslan A. Soldatov (Kharchenko Lab) for sharing codes. I.A. was supported by ERC Consolidator grant “STEMMING-FROM-NERVE”, Bertil Hallsten Foundation, Swedish Research Council, Paradifference Foundation. F.L. was supported by the Swedish Research Council (VR), the Ragnar Söderberg Foundation, Knut and Alice Wallenberg Foundation, Swedish Brain Foundation, Karolinska Institutet, the Karolinska Institutet Strategic Research program in Neuroscience (StratNeuro) and the Ming Wai Lau Foundation. L.F. is supported by the Austrian Science Fund DOC 33-B27. S.H. is supported by the Swedish Research Council (VR), the Swedish Brain Foundation and Kar-olinska Institutet. Open access funding provided by Karolinska Institute. Publisher Copyright: © 2020, The Author(s).

PY - 2020/12/1

Y1 - 2020/12/1

N2 - Somatic sensation is defined by the existence of a diversity of primary sensory neurons with unique biological features and response profiles to external and internal stimuli. However, there is no coherent picture about how this diversity of cell states is transcriptionally generated. Here, we use deep single cell analysis to resolve fate splits and molecular biasing processes during sensory neurogenesis in mice. Our results identify a complex series of successive and specific transcriptional changes in post-mitotic neurons that delineate hierarchical regulatory states leading to the generation of the main sensory neuron classes. In addition, our analysis identifies previously undetected early gene modules expressed long before fate determination although being clearly associated with defined sensory subtypes. Overall, the early diversity of sensory neurons is generated through successive bi-potential intermediates in which synchronization of relevant gene modules and concurrent repression of competing fate programs precede cell fate stabilization and final commitment.

AB - Somatic sensation is defined by the existence of a diversity of primary sensory neurons with unique biological features and response profiles to external and internal stimuli. However, there is no coherent picture about how this diversity of cell states is transcriptionally generated. Here, we use deep single cell analysis to resolve fate splits and molecular biasing processes during sensory neurogenesis in mice. Our results identify a complex series of successive and specific transcriptional changes in post-mitotic neurons that delineate hierarchical regulatory states leading to the generation of the main sensory neuron classes. In addition, our analysis identifies previously undetected early gene modules expressed long before fate determination although being clearly associated with defined sensory subtypes. Overall, the early diversity of sensory neurons is generated through successive bi-potential intermediates in which synchronization of relevant gene modules and concurrent repression of competing fate programs precede cell fate stabilization and final commitment.

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VL - 11

JO - Nature Communications

JF - Nature Communications

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Single cell RNA sequencing identifies early diversity of sensory neurons forming via bi-potential intermediates

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