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The emergence of transcriptional identity in somatosensory neurons

Author

Listed:
  • Nikhil Sharma

    (Harvard Medical School
    Harvard Medical School)

  • Kali Flaherty

    (Harvard Medical School
    Harvard Medical School)

  • Karina Lezgiyeva

    (Harvard Medical School
    Harvard Medical School)

  • Daniel E. Wagner

    (Harvard Medical School)

  • Allon M. Klein

    (Harvard Medical School)

  • David D. Ginty

    (Harvard Medical School
    Harvard Medical School)

Abstract

More than twelve morphologically and physiologically distinct subtypes of primary somatosensory neuron report salient features of our internal and external environments1–4. It is unclear how specialized gene expression programs emerge during development to endow these subtypes with their unique properties. To assess the developmental progression of transcriptional maturation of each subtype of principal somatosensory neuron, we generated a transcriptomic atlas of cells traversing the primary somatosensory neuron lineage in mice. Here we show that somatosensory neurogenesis gives rise to neurons in a transcriptionally unspecialized state, characterized by co-expression of transcription factors that become restricted to select subtypes as development proceeds. Single-cell transcriptomic analyses of sensory neurons from mutant mice lacking transcription factors suggest that these broad-to-restricted transcription factors coordinate subtype-specific gene expression programs in subtypes in which their expression is maintained. We also show that neuronal targets are involved in this process; disruption of the prototypic target-derived neurotrophic factor NGF leads to aberrant subtype-restricted patterns of transcription factor expression. Our findings support a model in which cues that emanate from intermediate and final target fields promote neuronal diversification in part by transitioning cells from a transcriptionally unspecialized state to transcriptionally distinct subtypes by modulating the selection of subtype-restricted transcription factors.

Suggested Citation

  • Nikhil Sharma & Kali Flaherty & Karina Lezgiyeva & Daniel E. Wagner & Allon M. Klein & David D. Ginty, 2020. "The emergence of transcriptional identity in somatosensory neurons," Nature, Nature, vol. 577(7790), pages 392-398, January.
  • Handle: RePEc:nat:nature:v:577:y:2020:i:7790:d:10.1038_s41586-019-1900-1
    DOI: 10.1038/s41586-019-1900-1
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    Cited by:

    1. Mayank Gautam & Akihiro Yamada & Ayaka I. Yamada & Qinxue Wu & Kim Kridsada & Jennifer Ling & Huasheng Yu & Peter Dong & Minghong Ma & Jianguo Gu & Wenqin Luo, 2024. "Distinct local and global functions of mouse Aβ low-threshold mechanoreceptors in mechanical nociception," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Prach Techameena & Xiaona Feng & Kaiwen Zhang & Saida Hadjab, 2024. "The single-cell transcriptomic atlas iPain identifies senescence of nociceptors as a therapeutical target for chronic pain treatment," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Shambhu Yadav & Markus Waldeck-Weiermair & Fotios Spyropoulos & Roderick Bronson & Arvind K. Pandey & Apabrita Ayan Das & Alexander C. Sisti & Taylor A. Covington & Venkata Thulabandu & Shari Caplan &, 2023. "Sensory ataxia and cardiac hypertrophy caused by neurovascular oxidative stress in chemogenetic transgenic mouse lines," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Stephan Dietrich & Carlos Company & Kun Song & Elijah David Lowenstein & Levin Riedel & Carmen Birchmeier & Gaetano Gargiulo & Niccolò Zampieri, 2022. "Molecular identity of proprioceptor subtypes innervating different muscle groups in mice," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    5. Min Jung & Michelle Dourado & James Maksymetz & Amanda Jacobson & Benjamin I. Laufer & Miriam Baca & Oded Foreman & David H. Hackos & Lorena Riol-Blanco & Joshua S. Kaminker, 2023. "Cross-species transcriptomic atlas of dorsal root ganglia reveals species-specific programs for sensory function," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Charles Petitpré & Louis Faure & Phoebe Uhl & Paula Fontanet & Iva Filova & Gabriela Pavlinkova & Igor Adameyko & Saida Hadjab & Francois Lallemend, 2022. "Single-cell RNA-sequencing analysis of the developing mouse inner ear identifies molecular logic of auditory neuron diversification," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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