Comprehensive transcriptome analysis of cochlear spiral ganglion neurons at multiple ages

  1. Chao Li
  2. Xiang Li
  3. Zhenghong Bi
  4. Ken Sugino
  5. Guangqin Wang
  6. Tong Zhu
  7. Zhiyong Liu  Is a corresponding author
  1. Chinese Academy of Sciences, China
  2. Janelia Research Campus, Howard Hughes Medical Institute, United States

Abstract

Inner ear cochlear spiral ganglion neurons (SGNs) transmit auditory information to the brainstem. Recent single cell RNA-Seq studies have revealed heterogeneities within SGNs. Nonetheless, much remains unknown about the transcriptome of SGNs, especially which genes are specifically expressed in SGNs. To address these questions we needed a deeper and broader gene coverage than that in previous studies. We performed bulk RNA-Seq on mouse SGNs at five ages, and on two reference cell types (hair cells and glia). Their transcriptome comparison identified genes previously unknown to be specifically expressed in SGNs. To validate our dataset and provide useful genetic tools for this research field, we generated two knockin mouse strains: Scrt2-P2A-tdTomato and Celf4-3xHA-P2A-iCreER-T2A-EGFP. Our comprehensive analysis confirmed the SGN-selective expression of the candidate genes, testifying to the quality of our transcriptome data. These two mouse strains can be used to temporally label SGNs or to sort them.

Data availability

Sequencing data have been deposited in GEO under accession codes GSE132925.

The following data sets were generated

Article and author information

Author details

  1. Chao Li

    Institute of Neuroscience, State Key Laboratory of Neuroscience,CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Xiang Li

    Institute of Neuroscience, State Key Laboratory of Neuroscience,CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Zhenghong Bi

    Institute of Neuroscience, State Key Laboratory of Neuroscience,CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Ken Sugino

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5795-0635
  5. Guangqin Wang

    Institute of Neuroscience, State Key Laboratory of Neuroscience,CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Tong Zhu

    Institute of Neuroscience, State Key Laboratory of Neuroscience,CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Zhiyong Liu

    Institute of Neuroscience, State Key Laboratory of Neuroscience,CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China
    For correspondence
    zhiyongliu@ion.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9675-1233

Funding

Ministry of Science and Technology of the People's Republic of China (2017YFA0103901)

  • Zhiyong Liu

Chinese Academy of Sciences (XDB32060100)

  • Zhiyong Liu

National Natural Science Foundation of China (81771012)

  • Zhiyong Liu

Shanghai Municipal Education Commission (2018SHZDZX05)

  • Zhiyong Liu

Boehringer Ingelheim (DE811138149)

  • Zhiyong Liu

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All mice were bred and raised in SPF level animal rooms and animal procedures were performed according to guidelines (NA-032-2019) of the IACUC of Institute of Neuroscience (ION), Chinese Academy of Sciences.

Reviewing Editor

  1. Tanya T Whitfield, University of Sheffield, United Kingdom

Publication history

  1. Received: July 24, 2019
  2. Accepted: January 7, 2020
  3. Accepted Manuscript published: January 8, 2020 (version 1)
  4. Version of Record published: January 24, 2020 (version 2)

Copyright

© 2020, Li et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 4,622
    Page views
  • 667
    Downloads
  • 12
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Chao Li
  2. Xiang Li
  3. Zhenghong Bi
  4. Ken Sugino
  5. Guangqin Wang
  6. Tong Zhu
  7. Zhiyong Liu
(2020)
Comprehensive transcriptome analysis of cochlear spiral ganglion neurons at multiple ages
eLife 9:e50491.
https://doi.org/10.7554/eLife.50491

Further reading

    1. Developmental Biology
    Danelle Devenport
    Insight

    Advanced imaging techniques reveal details of the interactions between the two layers of the embryonic midgut that influence its ultimate shape.

    1. Developmental Biology
    2. Evolutionary Biology
    Katelyn Mika et al.
    Research Advance

    Structural and physiological changes in the female reproductive system underlie the origins of pregnancy in multiple vertebrate lineages. In mammals, the glandular portion of the lower reproductive tract has transformed into a structure specialized for supporting fetal development. These specializations range from relatively simple maternal nutrient provisioning in egg-laying monotremes to an elaborate suite of traits that support intimate maternal-fetal interactions in Eutherians. Among these traits are the maternal decidua and fetal component of the placenta, but there is considerable uncertainty about how these structures evolved. Previously we showed that changes in uterine gene expression contributes to several evolutionary innovations during the origins of pregnancy (Marinic, Mika, and Lynch 2021). Here we reconstruct the evolution of entire transcriptomes ('ancestral transcriptome reconstruction') and show that maternal gene expression profiles are correlated with degree of placental invasion. These results indicate that an epitheliochorial-like placenta evolved early in the mammalian stem-lineage and that the ancestor of Eutherians had a hemochorial placenta, and suggest maternal control of placental invasiveness. These data resolve major transitions in the evolution of pregnancy and indicate that ancestral transcriptome reconstruction can be used to study the function of ancestral cell, tissue, and organ systems.