Identification and distribution of neuronal nitric oxide synthase and neurochemical markers in the neuroepithelial cells of the gill and the skin in the giant mudskipper, Periophthalmodon schlosseri

• Published in: Zoology (Jena) 2017-12, Vol.125, p.41-52
• Main Authors: Zaccone, Giacomo, Lauriano, Eugenia Rita, Kuciel, Michał, Capillo, Gioele, Pergolizzi, Simona, Alesci, Alessio, Ishimatsu, Atsushi, Ip, Yuen Kwong, Icardo, Jose M.
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological; Animals; Biomarkers; Carbon Dioxide; Ecosystem; Fishes - metabolism; Gene Expression Regulation, Enzymologic - physiology; Gill; Gills - cytology; Neuroepithelial cells; Neuroepithelial Cells - enzymology; Neuroepithelial Cells - metabolism; Neurotransmitters; Nitric Oxide Synthase Type I - genetics; Nitric Oxide Synthase Type I - metabolism; Oxygen - metabolism; Periophthalmodon schlosseri; Serotonin; Skin; Skin - cytology; Sodium-Potassium-Exchanging ATPase - genetics; Sodium-Potassium-Exchanging ATPase - metabolism; Transaminases; Vesicular Acetylcholine Transport Proteins - genetics; Vesicular Acetylcholine Transport Proteins - metabolism
• ISSN: 0944-2006; 1873-2720
• DOI: 10.1016/j.zool.2017.08.002

•We document the presence of neuroepithelial cells (NECs) in the gill and skin tissues of Periophthalmodon schlosseri.•NECs and their associated innervation may represent a functional system of O2 chemoreceptors.•NECs in the gill and skin are innervated by catecholaminergic nerves, suggesting their involvement in the control of respiration. Mudskippers are amphibious fishes living in mudflats and mangroves. These fishes hold air in their large buccopharyngeal-opercular cavities where respiratory gas exchange takes place via the gills and higher vascularized epithelium lining the cavities and also the skin epidermis. Although aerial ventilation response to changes in ambient gas concentration has been studied in mudskippers, the localization and distribution of respiratory chemoreceptors, their neurochemical coding and function as well as physiological evidence for the gill or skin as site for O2 and CO2 sensing are currently not known. In the present study we assessed the distribution of serotonin, acetylcholine, catecholamines and nitric oxide in the neuroepithelial cells (NECs) of the mudskipper gill and skin epithelium using immunohistochemistry and confocal microscopy. Colocalization studies showed that 5-HT is coexpressed with nNOS, Na+/K+-ATPase, TH and VAChT; nNOS is coexpressed with Na+/K+-ATPase and TH in the skin. In the gill 5-HT is coexpressed with nNOS and VAhHT and nNOS is coexpressed with Na+/K+-ATPase and TH. Acetylcholine is also expressed in chain and proximal neurons projecting to the efferent filament artery and branchial smooth muscle. The serotonergic cells c labeled with VAChT, nNOS and TH, thus indicating the presence of NEC populations and the possibility that these neurotransmitters (other than serotonin) may act as primary transmitters in the hypoxic reflex in fish gills. Immunolabeling with TH antibodies revealed that NECs in the gill and the skin are innervated by catecholaminergic nerves, thus suggesting that these cells are involved in a central control of branchial functions through their relationships with the sympathetic branchial nervous system. The Na+/K+-ATPase in mitochondria-rich cells (MRCs), which are most concentrated in the gill lamellar epithelium, is colabeled with nNOS and associated with TH nerve terminals. TH-immunopositive fine varicosities were also associated with the numerous capillaries in the skin surface and the layers of the swollen cells. Based on the often hypercapnic and hypoxic habitat of the muds