Markers shared between dorsal root and enteric ganglia

Abstract

Although the bowel is known to contain intrinsic primary afferent neurons with mucosal projections these cells have not been identified. The current study was undertaken to determine whether carbohydrate differentiation antigens or enzymatic markers common to primary sensory neurons could be found in enteric neurons. Subpopulations of sensory neurons of rat dorsal root ganglia (DRG) can be identified by the immunocytochemical detection of lactoseries and globoseries carbohydrate differentiation antigens with monoclonal antibodies (MAbs) and by the histochemical demonstration of carbonic anhydrase (CA)- or fluoride-resistant acid phosphatase (FRAP) activities; therefore, these markers, and their coincident expression with neuropeptides, were studied in neurons of the rat small intestine. Subsets of enteric neurons were demonstrated by a MAb (1B2/1B7) recognizing ≥ 45%, and by a MAb (α-SSEA-1) recognizing ≤ 0.1 %, of DRG neurons, as well as by CA, but not FRAP activity. 1B2/1B7 + neurons were found in both the submucosal (∑46% of neurons) and myenteric plexuses (∼2% of neurons). Submucosal 1B2/1B7⁺ neurons with mucosal projections also displayed vasoactive intestinal polypeptide (VIP) and neuropeptide Y (NPY) but not substance P (SP) or calcitonin-gene-related peptide (CGRP) immunoreactivities. SSEA-1⁺ neurons were only found in the myenteric plexus, did not project to the mucosa (and thus are unlikely to be primary afferents), and were SOM⁺ or ENK⁺ but VIP⁻ and NPY⁻. CA activity was intense in ∼39% of the neurons of the submucosal plexus and in mucosal nerve fibers. Some (∼20%) of the submucosal CA neurons were also CGRP⁺, but VIP⁻ and NPY⁻; therefore, MAb 1B2/1B7 and CA activity mark different nonoverlapping sets of submucosal neurons. Following the neonatal administration of capsaicin (50 mg/kg), 1B2/1B7 immunoreactivity was lost from all submucosal neurons; however, VIP immunoreactivity was not depleted from the cell bodies. Although it cannot yet be concluded that the MAb 1B2/1B7 or CA markers demonstrate the intrinsic sensory neurons of the gut, the presence in the bowel of both is consistent with the supposition that sensory neurons related to those of DRG are also found in the intestine. The functional and possible developmental significance of this relationship remains to be defined.