Metabolic control of cellular immune-competency by odors in Drosophila

  1. Sukanya Madhwal
  2. Mingyu Shin
  3. Ankita Kapoor
  4. Manisha Goyal
  5. Manish K Joshi
  6. Pirzada Mujeeb Ur Rehman
  7. Kavan Gor
  8. Jiwon Shim  Is a corresponding author
  9. Tina Mukherjee  Is a corresponding author
  1. inStem, India
  2. Hanyang University, Republic of Korea
  3. Institut de Biologie, Aix Marseille Université, CNRS, France
  4. European Molecular Biology Laboratory, Germany

Abstract

Studies in different animal model systems have revealed the impact of odors on immune cells, however, any understanding on why and how odors control cellular immunity remained unclear. We find that Drosophila employ an olfactory-immune cross-talk to tune a specific cell type, the lamellocytes, from hematopoietic-progenitor cells. We show that neuronally released GABA derived upon olfactory stimulation, is utilized by blood-progenitor cells as a metabolite and through its catabolism, these cells stabilize Sima/HIFα protein. Sima capacitates blood-progenitor cells with the ability to initiate lamellocyte differentiation. This systemic axis becomes relevant for larvae dwelling in wasp-infested environments where chances of infection are high. By co-opting the olfactory route, the pre-conditioned animals elevate their systemic GABA levels leading to the up-regulation of blood-progenitor cell Sima expression. This elevates their immune-potential and primes them to respond rapidly when infected with parasitic wasps. The present work highlights the importance of the olfaction in immunity and shows how odor detection during animal development is utilized to establish a long-range axis in the control of blood-progenitor competency and immune-priming.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1-5 and Extended Data Figure 1-10.

Article and author information

Author details

  1. Sukanya Madhwal

    Regulation of Cell Fate, inStem, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  2. Mingyu Shin

    Hanyang University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  3. Ankita Kapoor

    Regulation of Cell Fate, inStem, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  4. Manisha Goyal

    Regulation of Cell Fate, inStem, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  5. Manish K Joshi

    Développement de Marseille (IBDM), Institut de Biologie, Aix Marseille Université, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Pirzada Mujeeb Ur Rehman

    Regulation of Cell Fate, inStem, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  7. Kavan Gor

    SCB unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Jiwon Shim

    Hanyang University, Seoul, Republic of Korea
    For correspondence
    jshim@hanyang.ac.kr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2409-1130
  9. Tina Mukherjee

    Regulation of Cell Fate, inStem, Bangalore, India
    For correspondence
    tinam@instem.res.in
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3776-5536

Funding

Department of Biotechnology, Ministry of Science and Technology, India (DBT/PR13446/COE/34/30/2015)

  • Tina Mukherjee

Department of Science and Technology, Ministry of Science and Technology, India (DST/ECR/2015/000390)

  • Tina Mukherjee

Department of Biotechnology, Ministry of Science and Technology, India (Ramalingaswami Fellowship)

  • Tina Mukherjee

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

Reviewing Editor

  1. Bruno Lemaitre, École Polytechnique Fédérale de Lausanne, Switzerland

Version history

  1. Received: June 26, 2020
  2. Accepted: December 28, 2020
  3. Accepted Manuscript published: December 29, 2020 (version 1)
  4. Version of Record published: January 14, 2021 (version 2)

Copyright

© 2020, Madhwal 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. Sukanya Madhwal
  2. Mingyu Shin
  3. Ankita Kapoor
  4. Manisha Goyal
  5. Manish K Joshi
  6. Pirzada Mujeeb Ur Rehman
  7. Kavan Gor
  8. Jiwon Shim
  9. Tina Mukherjee
(2020)
Metabolic control of cellular immune-competency by odors in Drosophila
eLife 9:e60376.
https://doi.org/10.7554/eLife.60376

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