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Molecular topography of an entire nervous system

View ORCID ProfileSeth R Taylor, Gabriel Santpere, Alexis Weinreb, Alec Barrett, Molly B. Reilly, Chuan Xu, Erdem Varol, Panos Oikonomou, Lori Glenwinkel, Rebecca McWhirter, Abigail Poff, Manasa Basavaraju, Ibnul Rafi, Eviatar Yemini, Steven J Cook, Alexander Abrams, Berta Vidal, Cyril Cros, Saeed Tavazoie, Nenad Sestan, Marc Hammarlund, View ORCID ProfileOliver Hobert, David M. Miller III
doi: https://doi.org/10.1101/2020.12.15.422897
Seth R Taylor
1Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN, USA
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  • ORCID record for Seth R Taylor
Gabriel Santpere
3Department of Neurobiology, Yale University School of Medicine, New Haven, CT, USA
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Alexis Weinreb
3Department of Neurobiology, Yale University School of Medicine, New Haven, CT, USA
4Department of Genetics, Yale University School of Medicine, New Haven, CT, USA
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Alec Barrett
3Department of Neurobiology, Yale University School of Medicine, New Haven, CT, USA
4Department of Genetics, Yale University School of Medicine, New Haven, CT, USA
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Molly B. Reilly
5Department of Biological Sciences, Columbia University, New York, NY, USA
6Howard Hughes Medical Institute
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Chuan Xu
3Department of Neurobiology, Yale University School of Medicine, New Haven, CT, USA
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Erdem Varol
7Department of Statistics, Columbia University, New York, NY, USA
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Panos Oikonomou
5Department of Biological Sciences, Columbia University, New York, NY, USA
8Department of Systems Biology, Columbia University Medical Center, New York, NY, USA
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Lori Glenwinkel
5Department of Biological Sciences, Columbia University, New York, NY, USA
6Howard Hughes Medical Institute
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Rebecca McWhirter
1Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN, USA
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Abigail Poff
1Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN, USA
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Manasa Basavaraju
3Department of Neurobiology, Yale University School of Medicine, New Haven, CT, USA
4Department of Genetics, Yale University School of Medicine, New Haven, CT, USA
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Ibnul Rafi
5Department of Biological Sciences, Columbia University, New York, NY, USA
6Howard Hughes Medical Institute
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Eviatar Yemini
5Department of Biological Sciences, Columbia University, New York, NY, USA
6Howard Hughes Medical Institute
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Steven J Cook
5Department of Biological Sciences, Columbia University, New York, NY, USA
6Howard Hughes Medical Institute
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Alexander Abrams
3Department of Neurobiology, Yale University School of Medicine, New Haven, CT, USA
4Department of Genetics, Yale University School of Medicine, New Haven, CT, USA
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Berta Vidal
5Department of Biological Sciences, Columbia University, New York, NY, USA
6Howard Hughes Medical Institute
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Cyril Cros
5Department of Biological Sciences, Columbia University, New York, NY, USA
6Howard Hughes Medical Institute
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Saeed Tavazoie
5Department of Biological Sciences, Columbia University, New York, NY, USA
8Department of Systems Biology, Columbia University Medical Center, New York, NY, USA
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Nenad Sestan
3Department of Neurobiology, Yale University School of Medicine, New Haven, CT, USA
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Marc Hammarlund
3Department of Neurobiology, Yale University School of Medicine, New Haven, CT, USA
4Department of Genetics, Yale University School of Medicine, New Haven, CT, USA
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  • For correspondence: marc.hammarlund@yale.edu or38@columbia.edu david.miller@vanderbilt.edu
Oliver Hobert
5Department of Biological Sciences, Columbia University, New York, NY, USA
6Howard Hughes Medical Institute
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  • ORCID record for Oliver Hobert
  • For correspondence: marc.hammarlund@yale.edu or38@columbia.edu david.miller@vanderbilt.edu
David M. Miller III
1Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN, USA
2Program in Neuroscience, Vanderbilt University School of Medicine, Nashville, TN, USA
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  • For correspondence: marc.hammarlund@yale.edu or38@columbia.edu david.miller@vanderbilt.edu
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Summary

Nervous systems are constructed from a deep repertoire of neuron types but the underlying gene expression programs that specify individual neuron identities are poorly understood. To address this deficit, we have produced an expression profile of all 302 neurons of the C. elegans nervous system that matches the single cell resolution of its anatomy and wiring diagram. Our results suggest that individual neuron classes can be solely identified by combinatorial expression of specific gene families. For example, each neuron class expresses unique codes of ∼23 neuropeptide-encoding genes and ∼36 neuropeptide receptors thus pointing to an expansive “wireless” signaling network. To demonstrate the utility of this uniquely comprehensive gene expression catalog, we used computational approaches to (1) identify cis-regulatory elements for neuron-specific gene expression across the nervous system and (2) reveal adhesion proteins with potential roles in synaptic specificity and process placement. These data are available at cengen.org and can be interrogated at the web application CengenApp. We expect that this neuron-specific directory of gene expression will spur investigations of underlying mechanisms that define anatomy, connectivity and function throughout the C. elegans nervous system.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵9 Lead Contact

  • We have updated some citations and the acknowledgements.

  • http://www.cengen.org

Copyright 
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 4.0 International license.
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Posted December 24, 2020.
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Molecular topography of an entire nervous system
Seth R Taylor, Gabriel Santpere, Alexis Weinreb, Alec Barrett, Molly B. Reilly, Chuan Xu, Erdem Varol, Panos Oikonomou, Lori Glenwinkel, Rebecca McWhirter, Abigail Poff, Manasa Basavaraju, Ibnul Rafi, Eviatar Yemini, Steven J Cook, Alexander Abrams, Berta Vidal, Cyril Cros, Saeed Tavazoie, Nenad Sestan, Marc Hammarlund, Oliver Hobert, David M. Miller III
bioRxiv 2020.12.15.422897; doi: https://doi.org/10.1101/2020.12.15.422897
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Molecular topography of an entire nervous system
Seth R Taylor, Gabriel Santpere, Alexis Weinreb, Alec Barrett, Molly B. Reilly, Chuan Xu, Erdem Varol, Panos Oikonomou, Lori Glenwinkel, Rebecca McWhirter, Abigail Poff, Manasa Basavaraju, Ibnul Rafi, Eviatar Yemini, Steven J Cook, Alexander Abrams, Berta Vidal, Cyril Cros, Saeed Tavazoie, Nenad Sestan, Marc Hammarlund, Oliver Hobert, David M. Miller III
bioRxiv 2020.12.15.422897; doi: https://doi.org/10.1101/2020.12.15.422897

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