Characterisation of putative oxygen chemoreceptors in bowfin (Amia calva)

Abstract

Serotonin containing neuroepithelial cells (NECs) are putative oxygen sensing cells found in different locations within the gills of fish. In this study we wished to determine the effect of sustained internal (blood) hypoxaemia versus external (aquatic) hypoxia on the size and density of NECs in the first gill arch of bowfin (Amia calva), a facultative air breather. We identified five different populations of serotonergic NECs in this species (Types I-V) based on location, presence of synaptic vesicles (SV) that stain for the antibody SV2, innervation and labelling with the neural crest marker HNK-1. Cell Types I-III were innervated, and these cells, which participate in central O 2 chemoreflexes, were studied further. Although there was no change in the density of any cell type in bowfin after exposure to sustained hypoxia (6.0 kPa for 7 days) without access to air, all three of these cell types increased in size. In contrast, only Type II and III cells increased in size in bowfin exposed to sustained hypoxia with access to air. These data support the suggestion that NECs are putative oxygen-sensing cells, that they occur in several locations, and that Type I cells monitor only hypoxaemia, whereas both other cell types monitor hypoxia and hypoxaemia.

Evolution of the hypoxia-sensitive cells involved in amniote respiratory reflexes

“…Glomus cells are neural crest-derived, as demonstrated in birds by quail-chick neural fold grafts (Le Douarin et al, 1972; Pearse et al, 1973), and in mouse by Wnt1-Cre genetic lineage-tracing (Pardal et al, 2007), but the embryonic origin of NECs is unknown. Lack of immunoreactivity for the HNK1 antibody, which labels migrating neural crest cells in many but not all vertebrates, has been reported for NECs (Porteus et al, 2013, 2014). However, the carbohydrate epitope recognized by the HNK1 antibody (Voshol et al, 1996) is borne by multiple glycoproteins and glycolipids, and gene or antigen expression in itself cannot indicate lineage.…”

Neuroendocrine and Eosinophilic Granule Cells in the Gills of Tilapia, Oreochromis niloticus: Effects of Waterborne Copper Exposure

“…In different fish species, it was shown that the number or size of NECs (5-HT ? and 5-HT -) was increased by chronic hypoxia (Jonz et al 2004;Porteus et al 2014;Regan et al 2011). Therefore, a possible condition of hypoxia may have also contributed to the increase of NECs' relative volume.…”

First demonstration of the neuroepithelial cells and their chemical code in the accessory respiratory organ and the gill of the sharptooth catfish, Clarias gariepinus: A preliminary study

“…Fish gill NECs may be involved in local and central control of branchial functions through the paracrine production of 5-HT and their synaptic relationships with the sympathetic and intrinsic branchial nervous system (Bailly, 2009;Zaccone et al, 2017). They may be considered as possible candidates of receptor cell populations involving in chemosensing O 2 levels in water, blood or both thus suggesting that some NECs are potentially indicated in cardiorespiratory control (Porteus et al, 2014). Jonz and Zaccone (2009) have also argued for a similar role of the nitrergic nerves in the nervous control of the fish gill.…”

“…nNOS has gained in recent years considerable experimental support as a neurotransmitter substance in mammalian carotid body and neuroepithelial bodies, and it seems to be largely confined to intrinsic efferent nerves (Campanucci & Nurse, 2007). Also, the gills are innervated by extrinsic and intrinsic nerves, and they may be serotonergic, cholinergic and adrenergic (Porteus et al, 2014;Zaccone et al, 2017). They may be considered as possible candidates of receptor cell populations involving in chemosensing O 2 levels in water, blood or both thus suggesting that some NECs are potentially indicated in cardiorespiratory control (Porteus et al, 2014).…”

“…Oxygensensing cells have been comprehensively studied in fish where these cells are called neuroepithelial cells (NECs) that are found dispersed throughout the gill arches of fishes and the lung of air-breathing fishes (Jonz, Buck, Perry, Schwerte, & Zaccone, 2016;Porteus, Wright, & Milsom, 2014;Porteus et al, 2015;Zaccone, Fasulo, & Ainis,1995;Zaccone, Mauceri, & Fasulo,2006;Zaccone, Mauceri, Giannetto, Parrino, & Fasulo,2007;Zaccone et al,2003Zaccone et al, ,2017. Oxygensensing cells have been comprehensively studied in fish where these cells are called neuroepithelial cells (NECs) that are found dispersed throughout the gill arches of fishes and the lung of air-breathing fishes (Jonz, Buck, Perry, Schwerte, & Zaccone, 2016;Porteus, Wright, & Milsom, 2014;Porteus et al, 2015;Zaccone, Fasulo, & Ainis,1995;Zaccone, Mauceri, & Fasulo,2006;Zaccone, Mauceri, Giannetto, Parrino, & Fasulo,2007;Zaccone et al,2003Zaccone et al, ,2017.…”