Abstract
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.
Highlights
The olfactory sensory system is composed of the peripheral olfactory epithelium (OE), where the continually renewing olfactory sensory neurons (OSNs) are located
Key findings include the following: (1) both local and non-local neutrophils and macrophages are present in the developing olfactory organ (OO), where the local immune cells may play a role in the lifelong neurogenesis of the olfactory epithelia; (2) the appearance of the immune cells is correlated with the developing blood and lymphatic vasculature (LV) of the OOs; (3) copper-induced damage triggers rapid but distinct responses from neutrophils and macrophages
In contrast to the neutrophils, macrophage populations in the developing olfactory OO and the eye were much larger than the other sensory systems, and there was no significant difference in numbers of macrophages found in the OOs and eyes
Summary
The olfactory sensory system is composed of the peripheral olfactory epithelium (OE), where the continually renewing olfactory sensory neurons (OSNs) are located. The axons of the OSNs reach the central nervous system (CNS) via the olfactory nerve (ON), where they make their first synapses in the olfactory bulb (OB) (Sakano, 2010; Whitlock, 2015). Unlike other sensory systems, the first synapses of the OSNs lie within the CNS. This unique organization creates a potential pathway for chemical or biological agents to enter the CNS. Pathogens can enter the CNS via the OE (Pägelow et al, 2018), it is striking that our brains are not besieged by infections that enter through this direct olfactory portal
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