The Olfactory Organ Is Populated by Neutrophils and Macrophages During Early Development

The immune system of vertebrates is characterized by innate and adaptive immunity that function together to form the natural defense system of the organism. During development innate immunity is the first to become functional and is mediated primarily by phagocytic cells, including macrophages, neut...

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Main Authors: M. Fernanda Palominos, Kathleen E. Whitlock
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-01-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2020.604030/full
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author M. Fernanda Palominos
Kathleen E. Whitlock
author_facet M. Fernanda Palominos
Kathleen E. Whitlock
author_sort M. Fernanda Palominos
collection DOAJ
description The immune system of vertebrates is characterized by innate and adaptive immunity that function together to form the natural defense system of the organism. During development innate immunity is the first to become functional and is mediated primarily by phagocytic cells, including macrophages, neutrophils, and dendritic cells. In the olfactory sensory system, the same sensory neurons in contact with the external environment have their first synapse within the central nervous system. This unique architecture presents a potential gateway for the entry of damaging or infectious agents to the nervous system. Here we used zebrafish as a model system to examine the development of the olfactory organ and to determine whether it shares immune characteristics of a host defense niche described in other tissues. During early development, both neutrophils and macrophages appear coincident with the generation of the primitive immune cells. The appearance of neutrophils and macrophages in the olfactory organs occurs as the blood and lymphatic vascular system is forming in the same region. Making use of the neurogenic properties of the olfactory organ we show that damage to the olfactory sensory neurons in larval zebrafish triggers a rapid immune response by local and non-local neutrophils. In contrast, macrophages, although present in greater numbers, mount a slower response to damage. We anticipate our findings will open new avenues of research into the role of the olfactory-immune response during normal neurogenesis and damage-induced regeneration and contribute to our understanding of the formation of a potential host defense immune niche in the peripheral nervous system.
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spelling doaj.art-b20c2f36cde84957a801dc5c924226202022-12-21T22:56:05ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2021-01-01810.3389/fcell.2020.604030604030The Olfactory Organ Is Populated by Neutrophils and Macrophages During Early DevelopmentM. Fernanda PalominosKathleen E. WhitlockThe immune system of vertebrates is characterized by innate and adaptive immunity that function together to form the natural defense system of the organism. During development innate immunity is the first to become functional and is mediated primarily by phagocytic cells, including macrophages, neutrophils, and dendritic cells. In the olfactory sensory system, the same sensory neurons in contact with the external environment have their first synapse within the central nervous system. This unique architecture presents a potential gateway for the entry of damaging or infectious agents to the nervous system. Here we used zebrafish as a model system to examine the development of the olfactory organ and to determine whether it shares immune characteristics of a host defense niche described in other tissues. During early development, both neutrophils and macrophages appear coincident with the generation of the primitive immune cells. The appearance of neutrophils and macrophages in the olfactory organs occurs as the blood and lymphatic vascular system is forming in the same region. Making use of the neurogenic properties of the olfactory organ we show that damage to the olfactory sensory neurons in larval zebrafish triggers a rapid immune response by local and non-local neutrophils. In contrast, macrophages, although present in greater numbers, mount a slower response to damage. We anticipate our findings will open new avenues of research into the role of the olfactory-immune response during normal neurogenesis and damage-induced regeneration and contribute to our understanding of the formation of a potential host defense immune niche in the peripheral nervous system.https://www.frontiersin.org/articles/10.3389/fcell.2020.604030/fullnervous systemmicrogliazebrafishvasculatureneuronmacrophage
spellingShingle M. Fernanda Palominos
Kathleen E. Whitlock
The Olfactory Organ Is Populated by Neutrophils and Macrophages During Early Development
Frontiers in Cell and Developmental Biology
nervous system
microglia
zebrafish
vasculature
neuron
macrophage
title The Olfactory Organ Is Populated by Neutrophils and Macrophages During Early Development
title_full The Olfactory Organ Is Populated by Neutrophils and Macrophages During Early Development
title_fullStr The Olfactory Organ Is Populated by Neutrophils and Macrophages During Early Development
title_full_unstemmed The Olfactory Organ Is Populated by Neutrophils and Macrophages During Early Development
title_short The Olfactory Organ Is Populated by Neutrophils and Macrophages During Early Development
title_sort olfactory organ is populated by neutrophils and macrophages during early development
topic nervous system
microglia
zebrafish
vasculature
neuron
macrophage
url https://www.frontiersin.org/articles/10.3389/fcell.2020.604030/full
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