Decoupling from yolk sac is required for extraembryonic tissue spreading in the scuttle fly Megaselia abdita

  1. Francesca Caroti
  2. Everardo González Avalos
  3. Viola Noeske
  4. Paula González Avalos
  5. Dimitri Kromm
  6. Maike Wosch
  7. Lucas Schütz
  8. Lars Hufnagel
  9. Steffen Lemke  Is a corresponding author
  1. Ruprecht Karls University, Germany
  2. Ruprecht Karls Universität, Germany
  3. European Molecular Biology Laboratory, Germany

Abstract

Extraembryonic tissues contribute to animal development, which often entails spreading over embryo or yolk. Apart from changes in cell shape, the requirements for this tissue spreading are not well understood. Here we analyze spreading of the extraembryonic serosa in the scuttle fly Megaselia abdita. The serosa forms from a columnar blastoderm anlage, becomes a squamous epithelium, and eventually spreads over the embryo proper. We describe the dynamics of this process in long-term, whole-embryo time-lapse recordings, demonstrating that free serosa spreading is preceded by a prolonged pause in tissue expansion. Closer examination of this pause reveals mechanical coupling to the underlying yolk sac, which is later released. We find mechanical coupling prolonged and serosa spreading impaired after knockdown of M. abdita Matrix metalloprotease 1. We conclude that tissue-tissue interactions provide a critical functional element to constrain spreading epithelia.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Custom Matlab functions are available via GitHub (https://github.com/lemkelab/SPIMaging).

Article and author information

Author details

  1. Francesca Caroti

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Everardo González Avalos

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Viola Noeske

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Paula González Avalos

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Dimitri Kromm

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Maike Wosch

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Lucas Schütz

    Centre for Organismal Studies Heidelberg, Ruprecht Karls Universität, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Lars Hufnagel

    European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Steffen Lemke

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    For correspondence
    steffen.lemke@cos.uni-heidelberg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5807-2865

Funding

Deutsche Forschungsgemeinschaft (LE 2787/1-1)

  • Francesca Caroti
  • Paula González Avalos
  • Maike Wosch
  • Steffen Lemke

HSFP (RGY0082/2015)

  • Everardo González Avalos
  • Viola Noeske
  • Paula González Avalos

EMBL International PhD Programme

  • Dimitri Kromm

Center of Modeling and Simulation in the Biosciences , University of Heidelberg

  • Lars Hufnagel

HBIGS predoctoral fellowship

  • Lucas Schütz

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

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Publication history

  1. Received: December 22, 2017
  2. Accepted: October 24, 2018
  3. Accepted Manuscript published: October 30, 2018 (version 1)
  4. Version of Record published: November 12, 2018 (version 2)

Copyright

© 2018, Caroti 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

  • 1,091
    Page views
  • 140
    Downloads
  • 8
    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. Francesca Caroti
  2. Everardo González Avalos
  3. Viola Noeske
  4. Paula González Avalos
  5. Dimitri Kromm
  6. Maike Wosch
  7. Lucas Schütz
  8. Lars Hufnagel
  9. Steffen Lemke
(2018)
Decoupling from yolk sac is required for extraembryonic tissue spreading in the scuttle fly Megaselia abdita
eLife 7:e34616.
https://doi.org/10.7554/eLife.34616

Further reading

    1. Developmental Biology
    2. Genetics and Genomics
    Elizabeth A Bearce, Zoe H Irons ... Daniel T Grimes
    Research Article

    The spine provides structure and support to the body, yet how it develops its characteristic morphology as the organism grows is little understood. This is underscored by the commonality of conditions in which the spine curves abnormally such as scoliosis, kyphosis and lordosis. Understanding the origin of such spinal curves has been challenging in part due to the lack of appropriate animal models. Recently, zebrafish have emerged as promising tools with which to understand the origin of spinal curves. Using zebrafish, we demonstrate that the Urotensin II-related peptides (URPs), Urp1 and Urp2, are essential for maintaining spine morphology. Urp1 and Urp2 are 10-amino acid cyclic peptides expressed by neurons lining the central canal of the spinal cord. Upon combined genetic loss of Urp1 and Urp2, adolescent-onset planar curves manifested in the caudal region of the spine. Highly similar curves were caused by mutation of Uts2r3, an URP receptor. Quantitative comparisons revealed that Urotensin-associated curves were distinct from other zebrafish spinal curve mutants in curve position and direction. Last, we found that the Reissner fiber, a proteinaceous thread that sits in the central canal and has been implicated in the control of spine morphology, breaks down prior to curve formation mutants with perturbed cilia motility but was unaffected by loss of Uts2r3. This suggests a Reissner fiber-independent mechanism of curvature in Urotensin-deficient mutants. Overall, our results show that Urp1 and Urp2 control zebrafish spine morphology and establish new animal models of spine deformity.

    1. Developmental Biology
    Zhongxiao Wang, Felix Yemanyi ... Jing Chen
    Research Article

    Amino acid (AA) metabolism in vascular endothelium is important for sprouting angiogenesis. SLC38A5 (solute carrier family 38 member 5), an AA transporter, shuttles neutral AAs across cell membrane, including glutamine, which may serve as metabolic fuel for proliferating endothelial cells (ECs) to promote angiogenesis. Here, we found that Slc38a5 is highly enriched in normal retinal vascular endothelium, and more specifically, in pathological sprouting neovessels. Slc38a5 is suppressed in retinal blood vessels from Lrp5−/− and Ndpy/− mice, both genetic models of defective retinal vascular development with Wnt signaling mutations. Additionally, Slc38a5 transcription is regulated by Wnt/β-catenin signaling. Genetic deficiency of Slc38a5 in mice substantially delays retinal vascular development and suppresses pathological neovascularization in oxygen-induced retinopathy modeling ischemic proliferative retinopathies. Inhibition of SLC38A5 in human retinal vascular ECs impairs EC proliferation and angiogenic function, suppresses glutamine uptake, and dampens vascular endothelial growth factor receptor 2. Together these findings suggest that SLC38A5 is a new metabolic regulator of retinal angiogenesis by controlling AA nutrient uptake and homeostasis in ECs.