Directional selectivity of afferent neurons in zebrafish neuromasts is regulated by Emx2 in presynaptic hair cells

  1. Young Rae Ji
  2. Sunita Warrier
  3. Tao Jiang
  4. Doris K Wu  Is a corresponding author
  5. Katie Kindt  Is a corresponding author
  1. National Institutes of Health, United States

Abstract

The orientation of hair bundles on top of sensory hair cells (HCs) in neuromasts of the lateral line system allows fish to detect direction of water flow. Each neuromast shows hair bundles arranged in two opposing directions and each afferent neuron only innervate HCs of the same orientation. In previous paper, we show that this opposition is established by expression of Emx2 in half of the HCs, where it mediates hair bundle reversal (Jiang et al. 2017). Here, we show that Emx2 also regulates neuronal selection: afferent neurons innervate either Emx2-positive or negative HCs. In emx2 knockout and gain-of-function neuromasts, all HCs are unidirectional and the innervation patterns and physiological responses of the afferent neurons are dependent on the presence or absence of Emx2. Our results indicate that Emx2 mediates the directional selectivity of neuromasts by two distinct processes: regulating hair bundle orientation in HCs and selecting afferent neuronal targets.

Data availability

All data generated or analysed during this study are included in the manuscript. Source data files have been provided for Table1 and figure 2, 4, 5, 6, 7, and 8.

Article and author information

Author details

  1. Young Rae Ji

    Section on Sensory Cell Regeneration and Development, Laboratory of Molecular Biology, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Sunita Warrier

    Section on Sensory Cell Development and Function, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Tao Jiang

    Section on Sensory Cell Regeneration and Development, Laboratory of Molecular Biology, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Doris K Wu

    Section on Sensory Cell Regeneration and Development, Laboratory of Molecular Biology, National Institutes of Health, Bethesda, United States
    For correspondence
    wud@nidcd.nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1400-3558
  5. Katie Kindt

    Section on Sensory Cell Development, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, United States
    For correspondence
    katie.kindt@nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1065-8215

Funding

National Institute on Deafness and Other Communication Disorders (Intramural Research Program Grant 1ZIADC000085-01)

  • Katie Kindt

National Institute on Deafness and Other Communication Disorders (Intramural Research Program Grant 1ZIADC000021)

  • Doris K Wu

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

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Metrics

  • 2,368
    views
  • 373
    downloads
  • 34
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Young Rae Ji
  2. Sunita Warrier
  3. Tao Jiang
  4. Doris K Wu
  5. Katie Kindt
(2018)
Directional selectivity of afferent neurons in zebrafish neuromasts is regulated by Emx2 in presynaptic hair cells
eLife 7:e35796.
https://doi.org/10.7554/eLife.35796

Share this article

https://doi.org/10.7554/eLife.35796

Further reading

    1. Developmental Biology
    Wei Yan
    Editorial

    The articles in this special issue highlight the diversity and complexity of research into reproductive health, including the need for a better understanding of the fundamental biology of reproduction and for new treatments for a range of reproductive disorders.

    1. Developmental Biology
    Anastasiia Lozovska, Ana Casaca ... Moises Mallo
    Research Article

    During the trunk to tail transition the mammalian embryo builds the outlets for the intestinal and urogenital tracts, lays down the primordia for the hindlimb and external genitalia, and switches from the epiblast/primitive streak (PS) to the tail bud as the driver of axial extension. Genetic and molecular data indicate that Tgfbr1 is a key regulator of the trunk to tail transition. Tgfbr1 has been shown to control the switch of the neuromesodermal competent cells from the epiblast to the chordoneural hinge to generate the tail bud. We now show that in mouse embryos Tgfbr1 signaling also controls the remodeling of the lateral plate mesoderm (LPM) and of the embryonic endoderm associated with the trunk to tail transition. In the absence of Tgfbr1, the two LPM layers do not converge at the end of the trunk, extending instead as separate layers until the caudal embryonic extremity, and failing to activate markers of primordia for the hindlimb and external genitalia. The vascular remodeling involving the dorsal aorta and the umbilical artery leading to the connection between embryonic and extraembryonic circulation was also affected in the Tgfbr1 mutant embryos. Similar alterations in the LPM and vascular system were also observed in Isl1 null mutants, indicating that this factor acts in the regulatory cascade downstream of Tgfbr1 in LPM-derived tissues. In addition, in the absence of Tgfbr1 the embryonic endoderm fails to expand to form the endodermal cloaca and to extend posteriorly to generate the tail gut. We present evidence suggesting that the remodeling activity of Tgfbr1 in the LPM and endoderm results from the control of the posterior PS fate after its regression during the trunk to tail transition. Our data, together with previously reported observations, place Tgfbr1 at the top of the regulatory processes controlling the trunk to tail transition.