1. Evolutionary Biology
  2. Immunology and Inflammation

In silico analysis of myeloid cells across animal kingdom reveal neutrophil evolution by colony stimulating factors

  1. Damilola Pinheiro  Is a corresponding author
  2. Marie-Anne Mawhin
  3. Maria Prendecki
  4. Kevin J Woollard  Is a corresponding author
  1. Imperial College London, United Kingdom
https://doi.org/10.7554/eLife.60214
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  1. Damilola Pinheiro
  2. Marie-Anne Mawhin
  3. Maria Prendecki
  4. Kevin J Woollard
(2020)
In silico analysis of myeloid cells across animal kingdom reveal neutrophil evolution by colony stimulating factors
eLife 9:e60214.
https://doi.org/10.7554/eLife.60214
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Abstract

Neutrophils constitute the largest population of phagocytic granulocytes in the blood of mammals. The development and function of neutrophils and monocytes is primarily governed by the granulocyte colony-stimulating factor receptor family (CSF3R/CSF3) and macrophage colony-stimulating factor receptor family (CSF1R/IL34/CSF1) respectively. Using various techniques this study considered how the emergence of receptor:ligand pairings shaped the distribution of blood myeloid cell populations. Comparative gene analysis supported the ancestral pairings of CSF1R/IL34 and CSF3R/CSF3, and the emergence of CSF1 later in lineages after the advent of Jawed/Jawless fish. Further analysis suggested that the emergence of CSF3 lead to reorganisation of granulocyte distribution between amphibian and early reptiles. However, the advent of endothermy likely contributed to the dominance of the neutrophil/heterophil in modern-day mammals and birds. In summary, we show that the emergence of CSF3R/CSF3 was a key factor in the subsequent evolution of the modern-day mammalian neutrophil.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files

Article and author information

Author details

  1. Damilola Pinheiro

    Centre for Inflammatory Disease, Department of Immunology and Inflammation, Imperial College London, London, United Kingdom
    For correspondence
    d.pinheiro@imperial.ac.uk
    Competing interests
    The authors declare that no competing interests exist.

  2. Marie-Anne Mawhin

    Centre for Inflammatory Disease, Department of Immunology and Inflammation, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

  3. Maria Prendecki

    Centre for Inflammatory Disease, Department of Immunology and Inflammation, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7048-7457

  4. Kevin J Woollard

    Centre for Inflammatory Disease, Department of Immunology and Inflammation, Imperial College London, London, United Kingdom
    For correspondence
    k.woollard@imperial.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9839-5463

Funding

Medical Research Council (MR/M003159/1)

  • Kevin J Woollard

Kidney Research UK (RP_019_20160303)

  • Kevin J Woollard

Kidney Research UK (RP_002_20170914)

  • Kevin J Woollard

British Heart Foundation (PG/18/41/33813)

  • Kevin J Woollard

The authors declare that there was no direct funding for this work. Grants from MRC (MR/M003159/1), Kidney Research UK (RP_019_20160303, RP_002_20170914) and BHF (PG/18/41/33813) support the Woollard labKJW is now an employee for AstraZeneca (BioPharmaceuticals R&D, Cambridge, UK). All of this work was performed at Imperial College London. No funding or support was received from AstraZeneca.

Reviewing Editor

  1. Antonis Rokas, Vanderbilt University, United States

Version history

  1. Received: June 21, 2020
  2. Accepted: November 24, 2020
  3. Accepted Manuscript published: November 25, 2020 (version 1)
  4. Version of Record published: December 4, 2020 (version 2)

Copyright

© 2020, Pinheiro 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. Damilola Pinheiro
  2. Marie-Anne Mawhin
  3. Maria Prendecki
  4. Kevin J Woollard
(2020)
In silico analysis of myeloid cells across animal kingdom reveal neutrophil evolution by colony stimulating factors
eLife 9:e60214.
https://doi.org/10.7554/eLife.60214

Share this article

https://doi.org/10.7554/eLife.60214

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