Axotomy-Induced Changes in the Chemical Coding Pattern of Colon Projecting Calbindin-Positive Neurons in the Inferior Mesenteric Ganglia of the Pig

Abstract

The present study examines the response of colon-projecting neurons localized in the inferior mesenteric ganglia (IMG) to axotomy in the pig animal model. In all animals (n = 8), a median laparotomy was performed under anesthesia and the retrograde tracer Fast Blue was injected into the descending colon wall. In experimental animals (n = 4), the descending colon was exposed and the bilateral caudal colonic nerves were identified and severed. All animals were euthanized and the inferior mesenteric ganglia were harvested and processed for double-labeling immunofluorescence for calbindin-D28k (CB) in combination with either tyrosine hydroxylase (TH), neuropeptide Y (NPY), somatostatin (SOM), vasoactive intestinal polypeptide (VIP), nitric oxide synthase (NOS), Leu-enkephalin (LENK), substance P, vesicular acetylcholine transporter, or galanin. Immunohistochemistry revealed significant changes in the chemical coding pattern of injured inferior mesenteric ganglion neurons. In control animals, Fast Blue-positive neurons were immunoreactive to TH, NPY, SOM, VIP, NOS, LENK, and CB. In the experimental group, the numbers of TH-, NPY-, and SOM-expressing neurons were reduced, whereas the number of neurons immunoreactive to LENK was increased. Our data indicate that the colon-projecting neurons of the porcine IMG react to the axotomy in a similar, but not an identical manner in a comparison to other species, especially rodents. Further studies are needed to elucidate the detailed factors/mechanisms involved in the response to nerve injury.

Myocardial Infarction Causes Transient Cholinergic Transdifferentiation of Cardiac Sympathetic Nerves via gp130

“…Third, selective deletion of the ChAT gene in adult sympathetic neurons prevented the increase in cardiac ACh content after MI. These data are consistent with ACh production in cardiac sympathetic nerves after MI, which is interesting because cholinergic properties have also been observed in adult sympathetic neurons during heart failure (Kanazawa et al, 2010), but have not been seen in other injury paradigms, including axotomy (Boeshore et al, 2004;Wojtkiewicz et al, 2013) and inflammatory colitis (Skobowiat et al, 2010).…”

“…Many studies implicate target-derived factors in stimulating cholinergic sympathetic differentiation (Schotzinger and Landis, 1988Landis, , 1990Asmus et al, 2000;Hiltunen and Airaksinen, 2004;Stanke et al, 2006), but other data suggest that sympathetic neurons can acquire a cholinergic phenotype during development in the absence of target interactions (Schäfer et al, 1997;Furlan et al, 2013). In contrast to developmental studies, however, the genes and proteins involved in cholinergic transmission have not been detected in sympathetic neuron cell bodies after axotomyinduced nerve injury (Boeshore et al, 2004;Brumovsky et al, 2011;Wojtkiewicz et al, 2013). Instead, inflammatory cytokines such as LIF (Rao et al, 1993;Sun and Zigmond, 1996) suppress noradrenergic properties and induce production of neuropeptides thought to be important for regeneration (Hyatt-Sachs et al, 1996;Klimaschewski et al, 1996;Zigmond and Sun, 1997;Brumovsky et al, 2011;Hesp et al, 2012;Wojtkiewicz et al, 2013).…”

“…In contrast to developmental studies, however, the genes and proteins involved in cholinergic transmission have not been detected in sympathetic neuron cell bodies after axotomyinduced nerve injury (Boeshore et al, 2004;Brumovsky et al, 2011;Wojtkiewicz et al, 2013). Instead, inflammatory cytokines such as LIF (Rao et al, 1993;Sun and Zigmond, 1996) suppress noradrenergic properties and induce production of neuropeptides thought to be important for regeneration (Hyatt-Sachs et al, 1996;Klimaschewski et al, 1996;Zigmond and Sun, 1997;Brumovsky et al, 2011;Hesp et al, 2012;Wojtkiewicz et al, 2013).…”

Development of non‐catecholaminergic sympathetic neurons in para‐ and prevertebral ganglia of cats

“…This suggestion is supported by the observation that VIP was found to rescue a small population (10%) of post‐mitotic sympathetic neurons derived from the neonatal SCG after withdrawal of nerve growth factor (Klimaschewski, 1997). Axotomy induces or increases the number of neurons expressing VIP and/or NOS in sympathetic ganglia in rodents but not in pigs (Shadiack et al, 2001; Wojtkiewicz et al, 2013).…”

T2 Toxin-Induced Changes in Cocaine- and Amphetamine-Regulated Transcript (CART)-Like Immunoreactivity in the Enteric Nervous System Within Selected Fragments of the Porcine Digestive Tract

“…The slices of stomach and intestine were examined using standard double-labeling immunofluorescence technique that has been described previously by Wojtkiewicz et al (2013). In short, it was as follows: after drying (45 min.…”