1. Cell Biology
  2. Developmental Biology

The fat body cortical actin network regulates Drosophila inter-organ nutrient trafficking, signaling, and adipose cell size

  1. Rupali Ugrankar-Banerjee
  2. Son Tran
  3. Jade Bowerman
  4. Anastasiia Kovalenko
  5. Blessy Paul
  6. W Mike Henne  Is a corresponding author
  1. The University of Texas Southwestern Medical Center, United States
  2. University of Texas Southwestern Medical Center, United States
https://doi.org/10.7554/eLife.81170
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  1. Rupali Ugrankar-Banerjee
  2. Son Tran
  3. Jade Bowerman
  4. Anastasiia Kovalenko
  5. Blessy Paul
  6. W Mike Henne
(2023)
The fat body cortical actin network regulates Drosophila inter-organ nutrient trafficking, signaling, and adipose cell size
eLife 12:e81170.
https://doi.org/10.7554/eLife.81170
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Abstract

Defective nutrient storage and adipocyte enlargement (hypertrophy) are emerging features of metabolic syndrome and type 2 diabetes. Within adipose tissues, how the cytoskeletal network contributes to adipose cell size, nutrient uptake, fat storage, and signaling remain poorly understood. Utilizing the Drosophila larval fat body (FB) as a model adipose tissue, we show that a specific actin isoform-Act5C-forms the cortical actin network necessary to expand adipocyte cell size for biomass storage in development. Additionally, we uncover a non-canonical role for the cortical actin cytoskeleton in inter-organ lipid trafficking. We find Act5C localizes to the FB cell surface and cell-cell boundaries, where it intimately contacts peripheral LDs (pLDs), forming a cortical actin network for cell architectural support. FB-specific loss of Act5C perturbs FB triglyceride (TG) storage and LD morphology, resulting in developmentally delayed larvae that fail to develop into flies. Utilizing temporal RNAi-depletion approaches, we reveal that Act5C is indispensable post-embryogenesis during larval feeding as FB cells expand and store fat. Act5C-deficient FBs fail to grow, leading to lipodystrophic larvae unable to accrue sufficient biomass for complete metamorphosis. In line with this, Act5C-deficient larvae display blunted insulin signaling and reduced feeding. Mechanistically, we also show this diminished signaling correlates with decreased lipophorin (Lpp) lipoprotein-mediated lipid trafficking, and find Act5C is required for Lpp secretion from the FB for lipid transport. Collectively, we propose that the Act5C-dependent cortical actin network of Drosophila adipose tissue is required for adipose tissue size-expansion and organismal energy homeostasis in development, and plays an essential role in inter-organ nutrient transport and signaling.

Data availability

We have now provided raw datasets for the manuscript on a Dryad file site (doi:10.5061/dryad.4mw6m90d4).

The following data sets were generated

Article and author information

Author details

  1. Rupali Ugrankar-Banerjee

    Ugrankar-Banerjee, The University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Son Tran

    Department of Cell Biology, The University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Jade Bowerman

    Department of Cell Biology, The University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Anastasiia Kovalenko

    Department of Cell Biology, The University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Blessy Paul

    Department of Cell Biology, The University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. W Mike Henne

    Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, United States
    For correspondence
    mike.henne@utsouthwestern.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2135-2799

Funding

NIDDK (DK126887)

  • Rupali Ugrankar-Banerjee
  • Son Tran
  • Jade Bowerman
  • Anastasiia Kovalenko
  • Blessy Paul
  • W Mike Henne

NIGMS (GM119768)

  • W Mike Henne

Welch Foundation (I-1873)

  • W Mike Henne

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

Reviewing Editor

  1. Hugo J Bellen, Baylor College of Medicine, United States

Version history

  1. Preprint posted: June 16, 2022 (view preprint)
  2. Received: June 17, 2022
  3. Accepted: April 25, 2023
  4. Accepted Manuscript published: May 5, 2023 (version 1)
  5. Version of Record published: May 22, 2023 (version 2)

Copyright

© 2023, Ugrankar-Banerjee 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.

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  1. Rupali Ugrankar-Banerjee
  2. Son Tran
  3. Jade Bowerman
  4. Anastasiia Kovalenko
  5. Blessy Paul
  6. W Mike Henne
(2023)
The fat body cortical actin network regulates Drosophila inter-organ nutrient trafficking, signaling, and adipose cell size
eLife 12:e81170.
https://doi.org/10.7554/eLife.81170

Share this article

https://doi.org/10.7554/eLife.81170

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