The organisation of the enteric nervous system in the submucous and mucous layers of the small intestine of the pig studied by VIP and neurofilament protein immunohistochemistry
Abstract:The arrangement of the enteric ganglia and nerve fibre plexuses was examined in the submucous and mucous layers and around Peyer's patches of the porcine small intestine to clarify their organisation. Immunohistochemistry of vasoactive intestinal peptide (VIP) and neurofilament proteins in wholemounts, chopped or paraffin sections was used to locate the neural elements. The ganglia of the internal and external submucous plexuses were situated at 2 different topographic locations, being clearly demarcat… Show more
“…Besides studies in rat (Bridges et al 1986;Mestres et al 1992), cattle and pig (Balemba et al 1998(Balemba et al , 1999, the interest on human mucosal neurons derived mainly from clinical and pathohistological background (Lassmann 1975;Hirschowitz and Rode 1991;Fang et al 1993;Tunru-Dinh and Wu 2007). These investigators evaluated sections stained with classical histological or histochemical methods and found that the presence of mucosal neurons in human intestines is variable.…”
The consequence of presence versus absence of mucosal neurons is not consistently assessed. Here, we addressed two questions. First, based on resected gut specimens of 65 patients/body donors suffering from different diseases, counts of mucosal neurons per mm(2) were analysed with respect to age, gender and region. Second, we evaluated resected megacolonic specimens of four patients suffering from chronic Chagas' disease. Mucosal wholemounts were triple-stained for calretinin (CALR), peripherin (PER) and human neuronal protein Hu C/D (HU). Counts revealed no clear correlation between the presence of mucosal neurons and age, gender or region. Mucosal neurons were present in 30 of 36 specimens derived from males (83%) and in 20 of 29 from females (69%). The numbers per mm(2) increased from duodenum to ileum (1.7-10.8) and from ascending to sigmoid colon (3.2-9.9). Out of 149 small intestinal mucosal neurons, 47% were co-reactive for CALR, PER and HU (large intestine: 76% of 300 neurons) and 48% for PER and HU only (large intestine: 23%). In 12 megacolonic specimens (each 3 from 4 patients), all 23 mucosal neurons found (1.9 per mm(2)) displayed co-reactivity for CALR, PER and HU. We suggest that the presence or the absence of mucosal neurons is variable, ongoing studies will address our assumption that they correspond in their morphochemical characteristics to submucosal neurons. Furthermore, both the architecture and neuron number of the megacolonic mucosal plexus displayed no dramatic changes indicating that mucosal nerves might be less involved in chagasic/megacolonic neurodegeneration as known from the myenteric plexus.
“…Besides studies in rat (Bridges et al 1986;Mestres et al 1992), cattle and pig (Balemba et al 1998(Balemba et al , 1999, the interest on human mucosal neurons derived mainly from clinical and pathohistological background (Lassmann 1975;Hirschowitz and Rode 1991;Fang et al 1993;Tunru-Dinh and Wu 2007). These investigators evaluated sections stained with classical histological or histochemical methods and found that the presence of mucosal neurons in human intestines is variable.…”
The consequence of presence versus absence of mucosal neurons is not consistently assessed. Here, we addressed two questions. First, based on resected gut specimens of 65 patients/body donors suffering from different diseases, counts of mucosal neurons per mm(2) were analysed with respect to age, gender and region. Second, we evaluated resected megacolonic specimens of four patients suffering from chronic Chagas' disease. Mucosal wholemounts were triple-stained for calretinin (CALR), peripherin (PER) and human neuronal protein Hu C/D (HU). Counts revealed no clear correlation between the presence of mucosal neurons and age, gender or region. Mucosal neurons were present in 30 of 36 specimens derived from males (83%) and in 20 of 29 from females (69%). The numbers per mm(2) increased from duodenum to ileum (1.7-10.8) and from ascending to sigmoid colon (3.2-9.9). Out of 149 small intestinal mucosal neurons, 47% were co-reactive for CALR, PER and HU (large intestine: 76% of 300 neurons) and 48% for PER and HU only (large intestine: 23%). In 12 megacolonic specimens (each 3 from 4 patients), all 23 mucosal neurons found (1.9 per mm(2)) displayed co-reactivity for CALR, PER and HU. We suggest that the presence or the absence of mucosal neurons is variable, ongoing studies will address our assumption that they correspond in their morphochemical characteristics to submucosal neurons. Furthermore, both the architecture and neuron number of the megacolonic mucosal plexus displayed no dramatic changes indicating that mucosal nerves might be less involved in chagasic/megacolonic neurodegeneration as known from the myenteric plexus.
“…The porcine small intestine contains three major ganglionated plexuses: a myenteric plexus and two submucosal plexuses; the submucosal plexus is further subdivided into the internal submucosal plexus (ISP) and external submucosal plexus (ESP; Timmermans et al 1990;Balemba et al 1998). The porcine ISP is structurally less complex than the myenteric plexus or ESP (Timmermans et al 1997).…”
With its abundance of neurons and immunocytes, the gut is a potentially important site for the study of the interaction between the nervous and immune systems. Using immunohistochemical techniques, we tested the hypothesis that gut-associated lymphoid tissue in the porcine small intestine might receive catecholaminergic, cholinergic and peptidergic innervation. Antibodies against protein gene product (PGP) 9.5 were employed to detect neuronal membranes; antibodies against tyrosine hydroxylase (TH), type 2 vesicular monoamine transporter (VMAT-2) and choline acetyltransferase (ChAT) were used to detect catecholaminergic and cholinergic neurons; and antibodies to neuromedin U-8 (NMU-8), substance P (SP) and vasoactive intestinal peptide (VIP) were also used. PGP9.5-immunoreactive nerve fibers were observed between jejunal Peyer's patch (PP) follicles and in submucosal ganglia localized at the base of continuous ileal PP. Many ChAT-positive and a few TH-/VMAT-2-immunoreactive neurons or axons adjacent to jejunal and ileal PP were observed. Neurons and fibers from ganglia situated between or at the base of PP follicles manifested robust immunoreactivities to VIP and NMU-8; relatively less SP immunoreactivity was observed at these locations. All neuromedin-U 8-positive neurons observed exhibited immunoreactivity to ChAT as did some VIP-positive neurons. The specific chemical coding of enteric neurons in close apposition to jejunal and ileal PP and the differential localization of neuropeptides within the jejunal and ileal PP are indicative of neuroimmunomodulation at these sites.
“…These neurons have been also found to contain neuropeptides (Schultzeberg et al 1980;Korman et al 1989;Vittoria et al 1992;Bredkjaer et al 1994;Balemba et al 1998) and the NADPH-d enzyme (Fang et al 1993). Neverthless, mucosal ganglia and single neurons are considered to be ectopic from the submucous plexus (Stöhr 1934;Lassmann 1975) and the mucous plexus to be aganglionic (Schultzeberg et al 1980;Costa et al 1987;Timmermans et al 1990;Burns Fig.…”
The topographical distribution of the enteric ganglia has been investigated in the proventriculus of the duck using protein gene product 9.5 (PGP 9.5) immunohistochemistry. Myenteric ganglia were usually located between the outer longitudinal and the inner circular muscle layer. Submucous ganglia were sparsely distributed and seemed to be substituted by ganglia located in the tunica mucosa. The neurochemical profile of proventricular ganglion cells was also investigated using nicotinamide adenine dinucleotide phosphate reduced-diaphorase (NADPH-d)-histochemistry and pituitary adenylate cyclase activating peptide (PACAP)/galanin (Gal) double-labelling immunohistochemistry. The majority of mucosal ganglion cells were shown to contain the NADPH-d enzyme and both the investigated peptides. These findings provide evidence for the presence of a mucosal ganglionated plexus in the glandular stomach of birds. Moreover, the neurochemical characteristics of this plexus suggest that it plays an important role in regulating several mucosal functions and, in particular, the production and the composition of the gastric juice.
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