Fine Structure of Morphologically Well-Defined Type II Neurons in the Enteric Nervous System of the Porcine Small Intestine Revealed by Immunoreactivity for Calcitonin Gene-Related Peptide

Dw, Scheuermann; Hj, Krammer; Timmermans, J.‐P.; Stach, W; Adriaensen, Dirk; Mh, De Groodt-Lasseel

doi:10.1159/000147195

Cited by 18 publications

(12 citation statements)

References 8 publications

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“…Work on human small intestine (Timmermans et al 1992) has indicated that CGRP immunoreactivity is mainly found in a neuronal population morphologically similar to the CGRP-immunoreactive (IR) somata observed in the porcine small intestine (Scheuermann et al 1987(Scheuermann et al , 1991 and mouse colon (Furness et al 2004b), i.e. in Dogiel type II neurons.…”

Section: Introductionmentioning

confidence: 92%

“…IPANs, identified by their morphology and projections in the mouse colon, are also CGRP-IR (Furness et al 2004b). Furthermore, Dogiel type II neurons, presumed to be IPANs, are CGRP-IR in the pig small intestine (Scheuermann et al 1991) and a proportion are CGRP-IR in human (Timmermans et al 1992;Brehmer et al 2004). Thus, by analogy with other species, we deduce that the CGRP-IR Dogiel type II neurons in sheep are IPANs.…”

Section: Intrinsic Cgrp-ir Neuronsmentioning

confidence: 99%

“…The distribution of CGRP immunoreactivity has been previously investigated in the pig (Scheuermann et al 1987(Scheuermann et al , 1991 and man (Timmermans et al 1992). Work on human small intestine (Timmermans et al 1992) has indicated that CGRP immunoreactivity is mainly found in a neuronal population morphologically similar to the CGRP-immunoreactive (IR) somata observed in the porcine small intestine (Scheuermann et al 1987(Scheuermann et al , 1991 and mouse colon (Furness et al 2004b), i.e.…”

Section: Introductionmentioning

confidence: 99%

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Extrinsic and intrinsic sources of calcitonin gene-related peptide immunoreactivity in the lamb ileum: a morphometric and neurochemical investigation

et al. 2005

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To investigate extrinsic origins of calcitonin gene-related peptide immunoreactive (CGRP-IR) nerve fibres in the sheep ileum, the retrograde fluorescent tracer Fast Blue (FB) was injected into the ileum wall. Sections of thoraco-lumbar dorsal root ganglia (DRG) and distal (nodose) vagal ganglia showing FB-labelled neurons were processed for CGRP immunohistochemistry. The distribution of CGRP-IR in fibres and nerve cell bodies in the ileum was also studied. CGRP-IR enteric neurons were morphometrically analysed in myenteric (MP) and submucosal plexuses (SMP) of lambs (2-4 months). Sensory neurons retrogradely labelled with FB were scattered in T5-L4 DRG but most were located at the upper lumbar levels (L1-L3); only a minor component of the extrinsic afferent innervation of the ileum was derived from nodose ganglia. In the DRG, 57% of retrogradely labelled neurons were also CGRP-IR. In cryostat sections, a dense network of CGRP-IR fibres was observed in the lamina propria beneath the epithelium, around the lacteals and lymphatic follicles (Peyer's platches), and along and around enteric blood vessels. Rare CGRP-IR fibres were also present in both muscle layers. Dense pericellular baskets of CGRP-IR fibres were observed around CGRP-negative somata. The only CGRP-IR nerve cells were well-defined Dogiel type II neurons localised in the MP and in the external and internal components of the SMP. CGRP-IR neurons in the myenteric ganglia were significantly larger than those in the submucosal ganglia (mean profile areas: about 1,400 mum(2) for myenteric neurons, 750 mum(2) for submucosal neurons). About 6% of myenteric neurons and 25% of submucosal neurons were CGRP-IR Dogiel type II neurons. The percentages of CGRP-IR neurons that were also tachykinin-IR were about 9% (MP) and 42% (SMP), whereas no CGRP-IR neurons exhibited immunoreactivity for vasoactive intestinal peptide, nitric oxide synthase or tyrosine hydroxylase in either plexus. Thus, CGRP immunoreactivity occurs in the enteric nervous system of the sheep ileum (as in human small intestine and MP of pig ileum) in only one morphologically defined type of neuron, Dogiel type II cells. These are probably intrinsic primary afferent neurons.

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Section: Introductionmentioning

confidence: 92%

Section: Intrinsic Cgrp-ir Neuronsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Extrinsic and intrinsic sources of calcitonin gene-related peptide immunoreactivity in the lamb ileum: a morphometric and neurochemical investigation

et al. 2005

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“…ness 1988; Scheuermann et al 1991). These neurons are cholinergic in the guinea-pig (Li and Furness 1998) and, throughout all species investigated, non-nitrergic (Costa et al 1992bWard et al 1992;Aimi et al 1993;Furness et al 1994;Timmermans et al 1994 a, b;Brehmer and Stach 1997).…”

Section: Neuron Typesmentioning

confidence: 98%

Morphological classifications of enteric neurons -- 100 years after Dogiel

Brehmer¹,

Schrödl²,

Neuhuber³

1999

Anatomy and Embryology

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The first differentiation of enteric neurons into three morphological types was done by the russian histologist A. S. Dogiel on the basis of the different shapes and lengths of their dendrites. Although a number of authors considered his results during the following decades, only a division into two types withstood time: type I neurons had one long and several short processes, whereas type II neurons were characterized by several long processes. Some further structural features were discussed but substantial progress was not made until the late 1970s. This stagnation was due to some inaccuracies in Dogiel's descriptions, to the fact that most histologists in this field followed the reticular concept of the nervous system, to the idea that enteric neurons represent no more than a vegetative, postganglionic relay station between the central nervous system and the periphery, and to methodological difficulties. With the application of modern neuroanatomical techniques it was realized that the enteric nervous system contains a considerable number of neuronal subpopulations. The search for morphological correlates of the chemical diversity of enteric neurons was done mainly in the pig and the guinea-pig. In the pig, additional structural features such as axonal projection, distribution of neurons within ganglia, within different plexuses and along the length of the gut, blood supply etc. were included as criteria for further refining neuronal classification. Most of our knowledge about functional features of enteric neurons, e.g. chemical coding, neuronal connectivity, electrophysiological behaviour, was derived from studies in the guinea-pig small intestine. In light of interspecies differences, comparison of findings from different species is mandatory. The search for morphological and functional peculiarities of human enteric neuronal circuitry has to consider all methodological and conceptual advances made within the past 100 years since the pioneering work of Dogiel.

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“…Although direct functional evidence is still lacking, type II neurons have been suggested to represent the IPANs in the pig (Cornelissen et al, 1999(Cornelissen et al, , 2000(Cornelissen et al, , 2001Hens et al, 2000). For 20 years, calcitonin gene-related peptide (CGRP) has been used as a marker for type II neurons in the pig ENS (Scheuermann et al, 1987(Scheuermann et al, , 1991Hens et al, 2000). However, several studies revealed that this peptide, in colocalization with a marker for cholinergic neurons (choline acetyl transferase, ChAT), is present also in neurofilament (NF) reactive, non-type II neurons, indicating that the chemical code NF/CGRP/ChAT, with NF as structural marker, is not specific for type II neurons (Brehmer et al, 2002a,b;Jungbauer et al, 2006).…”

mentioning

confidence: 99%

Calcitonin Gene‐Related Peptide: A Marker for Putative Primary Afferent Neurons in the Pig Small Intestinal Myenteric Plexus?

Wolf

Schrödl

Neuhuber

et al. 2007

The Anatomical Record

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For years, calcitonin gene-related peptide (CGRP) has been used as a marker peptide for Dogiel type II neurons, putative intrinsic primary afferent neurons, in the pig enteric nervous system. Recently, some studies showed CGRP-positive neurons displaying distinctly different shapes. The aims of this study were to evaluate (1) the proportion of myenteric type II neurons that contain CGRP and (2) the proportion of myenteric CGRP-positive neurons that display type II vs. non-type II morphologies and to conclude if this peptide could be suited as a marker for type II neurons. For this purpose, nine myenteric whole-mounts (each one from duodenum, jejunum, and ileum, respectively, derived from three pigs) were triple-immunostained for CGRP, neurofilaments (NF), and choline acetyl transferase (ChAT). Each whole-mount was evaluated twice. First, 50 NF-stained type II neurons were selected randomly and their coreactivities for CGRP and ChAT were observed. Second, 50 CGRP-positive neurons were located randomly and their NF morphology and ChAT coreactivity were observed. Altogether, 92% of all type II neurons investigated displayed CGRP immunoreactivity, whereas 94.9% of all CGRP-reactive neurons recorded displayed type II morphology. We observed three further shapes of CGRP-positive neurons: 7 type V neurons (all were ChAT-positive; mainly in the ileal whole-mounts), 6 type I-like neurons (all were ChAT-positive), and 14 type III-like neurons (mostly ChAT-negative; mainly in duodenal and jejunal specimens). We conclude that CGRP-antibodies can be used as markers for type II neurons in the pig small intestinal myenteric plexus in quantitative studies but it should be kept in mind that up to one-tenth of CGRP-reactive neurons may be nontype II neurons. In case of single cell evaluation, CGRP-immunoreactivity alone is not suited as a marker. In such cases additional, morphological analysis is necessary.

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Fine Structure of Morphologically Well-Defined Type II Neurons in the Enteric Nervous System of the Porcine Small Intestine Revealed by Immunoreactivity for Calcitonin Gene-Related Peptide

Cited by 18 publications

References 8 publications

Extrinsic and intrinsic sources of calcitonin gene-related peptide immunoreactivity in the lamb ileum: a morphometric and neurochemical investigation

Extrinsic and intrinsic sources of calcitonin gene-related peptide immunoreactivity in the lamb ileum: a morphometric and neurochemical investigation

Morphological classifications of enteric neurons -- 100 years after Dogiel

Calcitonin Gene‐Related Peptide: A Marker for Putative Primary Afferent Neurons in the Pig Small Intestinal Myenteric Plexus?

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