Occurrence of neurotrophin receptors and transmitters in the developing Xenopus gut

Abstract

The ontogeny of gut innervation in the anuran amphibian Xenopus laevis was studied using immunohistochemistry on sections of whole larvae from NF stages 38-52. Immunoreactivity to acetylated tubulin confirmed the presence of nerve fibres as early as stages 38-39. Actin immunoreactivity was found at stage 41, indicating the presence of smooth muscle cells. Trk-like neurotrophin receptors were occasionally found in nerve fibres as soon as stages 38-39. Vasoactive intestinal polypeptide (VIP) and pituitary adenylate cyclase-activating peptide (PACAP) immunoreactivities coexisted in nerves innervating the gut wall from stages 40-41, and nitric oxide synthase (NOS) from stage 42. Substance P/neurokinin A (SP/NKA) occurred at stage 42. In all these cases, the first fibres were observed in the oesophagus. Calcitonin gene-related peptide (CGRP) was first observed in nerves at stage 48. In general, VIP/PACAP and NOS innervation was denser than the tachykinin innervation. In conclusion, the development of nerve fibres in the Xenopus gut is probably dependent on neurotrophins that may act via Trk-like receptors and occur before the gut wall is fully organised morphologically. Feeding in Xenopus larvae starts at NF stage 45. The study demonstrates that several of the transmitters investigated are expressed in the gut innervation (and in endocrine cells) prior to this stage.

Ontogeny of the gut motility control system in zebrafishDanio rerioembryos and larvae

“…In birds and mammals, occasional nerves (and endocrine cells) showing tachykinin-like immunoreactivity occur early during fetal development, and mature into a more extensive nerve net before birth (human, Paulin et al, 1986;Larsson et al, 1987;sheep, Wathuta and Harrison, 1987;guinea-pig, Saffrey and Burnstock, 1988;chicken, Saffrey et al, 1982;Epstein et al, 1983;duck, Lucini et al, 1993). Similarly, in the amphibian Xenopus laevis, both nerves and endocrine cells are present in the gut before the onset of feeding (Holmberg et al, 2001). However, to our knowledge, this is the first demonstration of functional tachykinin receptors during this period.…”

“…In the axolotl, PACAP coexisted with VIP and was found in gut neurons at an early stage (Badawy and Reinecke, 2003). In Xenopus laevis larvae, several transmitters, including PACAP and NKA, have been detected by immunohistochemistry in neurons before the onset of feeding (Holmberg et al, 2001). These findings suggest that the neuronal control system, if not already fully functioning, is ready to play a role in the processing of food from the first feed.…”

“…Enteric neurons as such have been detected in the zebrafish embryo before the onset of feeding (Bisgrove et al, 1997;Holmberg et al, 2003), but so far there are no reports on the expression of different transmitters in these nerves. Earlier studies have shown the presence of regulatory neuropeptides in neurons in the developing gut of another teleost (Reinecke et al, 1997), as well as in amphibians (Holmberg et al, 2001;Maake et al, 2001), birds (Epstein et al, 1981(Epstein et al, , 1983Epstein and Poulsen, 1991) and mammals (Larsson et al, 1987;Pham et al, 1991;Van Ginneken et al, 1998).…”

“…Acetylcholine and substance P/neurokinin A (NKA) are major excitatory transmitters in the ENS in adult animals, and the vasoactive intestinal polypeptide (VIP)-related peptide PACAP often participates in inhibitory control (Costa et al, 2000;Matsuda et al, 2000;Olsson and Holmgren, 2001). Furthermore, SP/NKA and VIP/PACAP are neuropeptides that have been detected in larval gut neurons before the onset of feeding in some other fish and amphibian species (turbot Scophthalmus maximus, Reinecke et al, 1997; axolotl Ambystoma mexicanum, Maake et al, 2001; Xenopus laevis, Holmberg et al, 2001). In the present study, gut motility in vivo in zebrafish embryos and larvae is investigated following microinjections of acetylcholine, atropine, NKA and PACAP, in combination with video recordings of the frequency of anterior anterograde motility waves in the developing gut with subsequent motion analysis.…”

The effects of endogenous and exogenous nitric oxide on gut motility in zebrafish Danio rerio embryos and larvae

“…A variety of neurotransmitters have been identified in the developing gut in mammals (Gintzler et al, 1980;Rothman and Gershon, 1982;Larsson et al, 1987;Timmermans et al, 1994;Brandt et al, 1996;van Ginneken et al, 1998), birds (Epstein et al, 1985;Rothman et al, 1986;Balaskas et al, 1995), amphibians (Holmberg et al, 2001;Maake et al, 2001;Badawy and Reinecke, 2003) and teleosts (Reinecke et al, 1997;Villani, 1999;Poon et al, 2003;Holmberg et al, 2004;Holmqvist et al, 2004;Pederzoli et al, 2004). In the zebrafish, enteric neurons are present in the gut before the onset of exogenous feeding (Raible et al, 1992;Bisgrove et al, 1997;Holmberg et al, 2003).…”