In-silico analysis of myeloid cells across the animal kingdom reveals neutrophil evolution by colony-stimulating factors.

Damilola Pinheiro,Kevin J Woollard,Maria Prendecki,Marie-Anne Mawhin

doi:10.7554/elife.60214

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.

Highlights

Phagocytes are key effector immune cells responsible for various biological processes; from orchestrating responses against invading pathogens to maintaining tissue homeostasis and neutrophils are the most abundant population of granulocytic phagocytes present in mammalian blood (Adrover et al, 2019; Hidalgo et al, 2019; Ng et al, 2019; Yvan-Charvet and Ng, 2019; Evrard et al, 2018)
There is a large body of evidence demonstrating the requirement of CSFs for cell development as multiple studies in knockout mice have shown that CSF1R/CSF1 and CSF3R/CSF3 are linked to the development of monocytes and neutrophils in vivo
The presence of analogous myeloid granulocytes and agranulocytes was examined by comparing available complete blood count (CBC) data, where applicable, for various animal orders and demonstrated the possible distribution of myeloid cells in blood across evolution

Summary

Introduction

Phagocytes are key effector immune cells responsible for various biological processes; from orchestrating responses against invading pathogens to maintaining tissue homeostasis and neutrophils are the most abundant population of granulocytic phagocytes present in mammalian blood (Adrover et al, 2019; Hidalgo et al, 2019; Ng et al, 2019; Yvan-Charvet and Ng, 2019; Evrard et al, 2018). Neutrophil and heterophils (a functionally analogous granulocytic phagocyte population present in non-mammals and some mammals; Montali, 1988) arise from a shared pool of haematopoietic stem cells and mitotic myeloid progenitor cells that can differentiate into monocytes, eosinophils and basophils following exposure to the relevant growth factor (Adrover et al, 2019; Yvan-Charvet and Ng, 2019; Mehta et al, 2014).

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