Comparative neurochemical features of the innervation patterns of the gut of the basal actinopterygian, Lepisosteus oculatus, and the euteleost, Clarias batrachus

Abstract

Zaccone, G., Lauriano, E. R., Silvestri, G., Kenaley, C., Icardo, J. M., Pergolizzi, S., Alesci, A., Sengar, M., Kuciel, M. and Gopesh, A. 2015. Comparative neurochemical features of the innervation patterns of the gut of the basal actinopterygian, Lepisosteus oculatus, and the euteleost, Clarias batrachus. -Acta Zoologica (Stockholm) (Stockholm) 96: 127-139.The structure and physiology of enteric system are very similar in all classes of vertebrates, although they have been investigated only occasionally in non-mammalian vertebrates. Very little is known about the distribution of the neurotransmitters in the gut of actinopterygian fishes. Anatomical and physiological studies of enteric nervous systems in the spotted gar (Lepisosteus oculatus) and airbreathing catfish (Clarias batrachus), a non-teleost and teleost actinopterygian, respectively, have not been undertaken. This study provides the first comprehensive characterization of the range of neurochemical coding in the enteric nervous system of these two species, including the chemical diversity of the mucosal endocrine cells in the pyloric stomach of Clarias. Autonomic innervation of the secretory glands is also described and reported herein for the first time for fishes. We also report splanchnic (spinal) innervation of the stomach, submucosal ganglia (that also colocalize with nNOS) and caudal intestine of Clarias. In both fish species, numerous 5HT, ChAT, nNOS and TH-positive nerve fibres have been observed. These discoveries demonstrate that much more physiological and pharmacological data are needed before a comprehensive model of enteric nervous system control in vertebrates can be developed.

Immunohistochemical colocalization of G protein alpha subunits and 5-HT in the rectal gland of the cartilaginous fishScyliorhinus canicula

“…The generality of the role of VIP in controlling rectal gland secretion has been challenged (Shuttleworth, ), because the glands of S. canicula did not respond to VIP (Anderson et al, ; Thorndyke & Shuttleworth, ). But in the present study has been demonstrated numerous nerve fibers both of the capsule that of the parenchyma of the rectal gland peptide (VIP) and substance P positive; furthermore nNOS immunoreactivity in nerve fibers of the gland capsular wall and nerve varicosities in close proximity to the secretory cells, show that these substances are expressed by nerves close glandular parenchyma and the nerve fibers directly innervate the secretory epithelium (Zaccone et al, , ). Already, Chan and Phillips () described argentaffin cells in lip‐shark Hemiscyllium plagiosum rectal gland, we detected VIP and substance P immunoreactive cells (neuroendocrine like cell) in the glandular parenchyma between secretary cells.…”

“…Already, Chan and Phillips () described argentaffin cells in lip‐shark Hemiscyllium plagiosum rectal gland, we detected VIP and substance P immunoreactive cells (neuroendocrine like cell) in the glandular parenchyma between secretary cells. Endocrine cells, have been observed in the gut of our studied species: the spotted gar ( L. oculatus ) and air breathing catfish ( C. batrachus ) (Zaccone et al, ). Gut endocrine cells secrete hormones that are involved in the paracrine regulation of muscular movement, secretion by intestinal and associated glands and microcirculation in local tissues (Pillans et al ; Rehfeld, ).…”

“…oculatus) and air breathing catfish (C. batrachus) (Zaccone et al, 2015b). Gut endocrine cells secrete hormones that are involved in the paracrine regulation of muscular movement, secretion by intestinal and associated glands and microcirculation in local tissues (Pillans et al 2008;Rehfeld, 2004).…”

“…The authors stated that 5‐HT shows various functions such as muscle contraction and the regulation of ion selection in epithelial cells. Numerous 5HT‐positive nerve fibers and enteroendocrine cells have been observed in the gut of the basal actinopterygian, Lepisosteus oculatus , and the euteleost, Clarias batrachus (Zaccone et al, ). In the polymorphous granular cells (PGCs) that find in the mucociliated epithelium of the lung in the air breathing fish Polypterus senegalus (Lauriano et al, ) has been demonstrated the simultaneous occurrence of piscidin 1 and 5‐HT, suggesting the involvement of serotonin in immune responses.…”

Fine structure of diffused pseudobranchial neurosecretory cells associated with carotid labyrinth in an air‐breathing catfish Clarias batrachus

“…The cells are similar in ultrastructure to NECs of gill and other respiratory organs of non-catfish teleosts (Dunel-Erb et al 1982;Zaccone et al 1989a,b). Such cells formed the diffuse neuroendocrine system (DNES) at various sites in the gills (Dunel-Erb et al 1982;Bailly et al 1992;Zaccone et al 1997), swimbladder and air-breathing organs (ABOs) of fish (Zaccone et al 1989a), gut (Zaccone et al 2014) and the lungs of lung fish (Zaccone et al 1989a). The ultrastructural observations clearly revealed the neurosecretory organization of PNS in C. batrachus.…”