Nitrergic and Substance P Immunoreactive Neurons in the Enteric Nervous System of the Bottlenose Dolphin (Tursiops truncatus) Intestine

Compared with other mammals, the digestive system of cetaceans presents some remarkable anatomical and physiological differences. However, the neurochemical features of the enteric nervous system (ENS) in these animals have only been described in part. The present study gives a description of the nitrergic and selected peptidergic systems in the myenteric plexus (MP) and submucosal plexus (SMP) of the intestine of the bottlenose dolphin (Tursiops truncatus). The distribution and morphology of neurons immunoreactive (IR) for the neuronal nitric oxide synthase (nNOS) and Substance P (SP) were immunohistochemically studied in formalin-fixed specimens from the healthy intestine of three animals, and the data were compared with those described in the literature on other mammals (human and non-human). In bottlenose dolphins, the percentages of nitrergic neurons (expressed as median and interquartile range—IQR) were 28% (IQR = 19–29) in the MP and 1% (IQR = 0–2) in the SMP, while the percentages of SP-IR neurons were 31% (IQR = 22–37) in the MP and 41% (IQR = 24–63) in the SMP. Although morphological features of nNOS- and SP-IR neurons were similar to those reported in other mammals, we found some noticeable differences in the percentages of enteric neurons. In fact, we detected a lower proportion of nNOS-IR neurons in the SMP and a higher proportion of SP-IR neurons in the MP compared to other mammals. To the best of the authors’ knowledge, this study represents the first description and quantification of nNOS-IR neurons and the first quantification of SP-IR neurons in the intestine of a cetacean species. As nNOS and SP are important mediators of intestinal functions and the nitrergic population is an important target for many neuroenteropathies, data obtained from a healthy intestine provide a necessary basis to further investigate and understand possible functional differences and motor intestinal dysfunctions/alterations in these special mammals.

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The Orexin System in the Enteric Nervous System of the Bottlenose Dolphin (Tursiops truncatus)

PLoS ONE ◽

10.1371/journal.pone.0105009 ◽

2014 ◽

Vol 9 (8) ◽

pp. e105009 ◽

Cited By ~ 7

Author(s):

Claudia Gatta ◽

Finizia Russo ◽

Maria Grazia Russolillo ◽

Ettore Varricchio ◽

Marina Paolucci ◽

...

Keyword(s):

Nervous System ◽

Enteric Nervous System ◽

Bottlenose Dolphin ◽

Tursiops Truncatus

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Indication of lethal interactions between a solitary bottlenose dolphin (Tursiops truncatus) and harbor porpoises (Phocoena phocoena) in the German Baltic Sea

BMC Zoology ◽

10.1186/s40850-020-00061-7 ◽

2020 ◽

Vol 5 (1) ◽

Author(s):

Stephanie Gross ◽

Philip Claus ◽

Peter Wohlsein ◽

Tina Kesselring ◽

Jan Lakemeyer ◽

...

Keyword(s):

Baltic Sea ◽

Bottlenose Dolphin ◽

Tursiops Truncatus ◽

Bottlenose Dolphins ◽

Temporal Correlation ◽

First Record ◽

Phocoena Phocoena ◽

Cetacean Species ◽

The Baltic ◽

Harbor Porpoises

Abstract Background Aggressive interactions between bottlenose dolphins (Tursiops truncatus) and harbor porpoises (Phocoena phocoena) have been reported in different parts of the world since the late 1990s. In the Baltic Sea, harbor porpoises are the only native cetacean species, while bottlenose dolphins may appear there temporarily. In the fall of 2016, a solitary male photo-identified bottlenose dolphin stayed in the German Baltic Sea of Schleswig-Holstein for 3 months. During that time, the necropsies of the stranded harbor porpoises revealed types of trauma of varying degrees in six animals, which is unusual in this area. The purpose of this study was to determine if the appearance of the bottlenose dolphin could be linked to the trauma of the harbor porpoise carcasses. Results Pathological findings in these animals included subcutaneous, thoracic and abdominal hemorrhages, multiple, mainly bilateral, rib fractures, and one instance of lung laceration. These findings correspond with the previously reported dolphin-caused injuries in other regions. Moreover, public sighting reports showed a spatial and temporal correlation between the appearance of the dolphin and the stranding of fatally injured harbor porpoises. Conclusion Despite the fact that no attack has been witnessed in German waters to date, our findings indicate the first record of lethal interactions between a bottlenose dolphin and harbor porpoises in the German Baltic Sea. Furthermore, to our knowledge, this is the first report of porpoise aggression by a socially isolated bottlenose dolphin.

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Alterations in Galanin-Like Immunoreactivity in the Enteric Nervous System of the Porcine Stomach Following Acrylamide Supplementation

International Journal of Molecular Sciences ◽

10.3390/ijms20133345 ◽

2019 ◽

Vol 20 (13) ◽

pp. 3345 ◽

Cited By ~ 3

Author(s):

Katarzyna Palus ◽

Krystyna Makowska ◽

Jarosław Całka

Keyword(s):

Nervous System ◽

Enteric Nervous System ◽

Daily Intake ◽

Enteric Neurons ◽

Double Labelling ◽

Recovery Processes ◽

High Doses ◽

Oxide Synthase ◽

The Impact ◽

Double Labelling Immunohistochemistry

In recent years, a significant increase in the consumption of products containing large amounts of acrylamide (e.g., chips, fries, coffee), especially among young people has been noted. The present study was created to establish the impact of acrylamide supplementation, in tolerable daily intake (TDI) dose and a dose ten times higher than TDI, on the population of galanin-like immunoreactive (GAL-LI) stomach neurons in pigs. Additionally, in the present study, the possible functional co-operation of GAL with other neuroactive substances and their role in acrylamide intoxication was investigated. Using double-labelling immunohistochemistry, alterations in the expression of GAL were examined in the porcine stomach enteric neurons after low and high doses of acrylamide supplementation. Generally, upregulation in GAL-LI immunoreactivity in both myenteric and submucous plexuses was noted in all stomach fragments studied. Additionally, the proportion of GAL-expressing cell bodies simultaneously immunoreactive to vasoactive intestinal peptide (VIP), neuronal nitric oxide synthase (nNOS) and cocaine- and amphetamine- regulated transcript peptide (CART) also increased. The results suggest neurotrophic or/and neuroprotective properties of GAL and possible co-operation of GAL with VIP, nNOS, CART in the recovery processes in the stomach enteric nervous system (ENS) neurons following acrylamide intoxication.

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Influence of Acrylamide Administration on the Neurochemical Characteristics of Enteric Nervous System (ENS) Neurons in the Porcine Duodenum

International Journal of Molecular Sciences ◽

10.3390/ijms21010015 ◽

2019 ◽

Vol 21 (1) ◽

pp. 15 ◽

Cited By ~ 1

Author(s):

Katarzyna Palus ◽

Jarosław Całka

Keyword(s):

Nervous System ◽

Enteric Nervous System ◽

Low Dose ◽

Daily Intake ◽

Enteric Neurons ◽

Vesicular Acetylcholine Transporter ◽

High Dose ◽

Harmful Action ◽

Calcitonin Gene ◽

Oxide Synthase

The digestive tract, especially the small intestine, is one of the main routes of acrylamide absorption and is therefore highly exposed to the toxic effect of acrylamide contained in food. The aim of this experiment was to elucidate the effect of low (tolerable daily intake—TDI) and high (ten times higher than TDI) doses of acrylamide on the neurochemical phenotype of duodenal enteric nervous system (ENS) neurons using the pig as an animal model. The experiment was performed on 15 immature gilts of the Danish Landrace assigned to three experimental groups: control (C) group—pigs administered empty gelatine capsules, low dose (LD) group—pigs administered capsules with acrylamide at the TDI dose (0.5 μg/kg body weight (b.w.)/day), and the high dose (HD) group—pigs administered capsules with acrylamide at a ten times higher dose than the TDI (5 μg/kg b.w./day) with a morning feeding for 4 weeks. Administration of acrylamide, even in a low (TDI) dose, led to an increase in the percentage of enteric neurons immunoreactive to substance P (SP), calcitonin gene-related peptide (CGRP), galanin (GAL), neuronal nitric oxide synthase (nNOS), and vesicular acetylcholine transporter (VACHT) in the porcine duodenum. The severity of the changes clearly depended on the dose of acrylamide and the examined plexus. The obtained results suggest the participation of these neuroactive substances in acrylamide-inducted plasticity and the protection of ENS neurons, which may be an important line of defence from the harmful action of acrylamide.

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Inhibitory effect of melatonin on nitric oxide synthase in rat enteric nervous system

Gastroenterology ◽

10.1016/s0016-5085(01)80869-6 ◽

2001 ◽

Vol 120 (5) ◽

pp. A176-A176

Author(s):

P KOPPITZ ◽

M STORR ◽

D SAUR ◽

M KURJAK ◽

H ALLESCHER

Keyword(s):

Nitric Oxide ◽

Nervous System ◽

Nitric Oxide Synthase ◽

Enteric Nervous System ◽

Inhibitory Effect ◽

Oxide Synthase

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Automated computational analysis reveals structural changes in the enteric nervous system of nNOS deficient mice

Scientific Reports ◽

10.1038/s41598-021-96677-x ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Ben R. Cairns ◽

Benjamin Jevans ◽

Atchariya Chanpong ◽

Dale Moulding ◽

Conor J. McCann

Keyword(s):

Machine Learning ◽

Nervous System ◽

Enteric Nervous System ◽

Structural Changes ◽

Computational Analysis ◽

Confocal Imaging ◽

Learning Approaches ◽

Composition And Structure ◽

Oxide Synthase ◽

Computational Image Analysis

AbstractNeuronal nitric oxide synthase (nNOS) neurons play a fundamental role in inhibitory neurotransmission, within the enteric nervous system (ENS), and in the establishment of gut motility patterns. Clinically, loss or disruption of nNOS neurons has been shown in a range of enteric neuropathies. However, the effects of nNOS loss on the composition and structure of the ENS remain poorly understood. The aim of this study was to assess the structural and transcriptional consequences of loss of nNOS neurons within the murine ENS. Expression analysis demonstrated compensatory transcriptional upregulation of pan neuronal and inhibitory neuronal subtype targets within the Nos1−/− colon, compared to control C57BL/6J mice. Conventional confocal imaging; combined with novel machine learning approaches, and automated computational analysis, revealed increased interconnectivity within the Nos1−/− ENS, compared to age-matched control mice, with increases in network density, neural projections and neuronal branching. These findings provide the first direct evidence of structural and molecular remodelling of the ENS, upon loss of nNOS signalling. Further, we demonstrate the utility of machine learning approaches, and automated computational image analysis, in revealing previously undetected; yet potentially clinically relevant, changes in ENS structure which could provide improved understanding of pathological mechanisms across a host of enteric neuropathies.

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Involution and Cystic Transformation of the Thymus in the Bottlenose Dolphin, Tursiops truncatus

Veterinary Pathology ◽

10.1177/030098589403100603 ◽

1994 ◽

Vol 31 (6) ◽

pp. 648-653 ◽

Cited By ~ 23

Author(s):

D. F. Cowan

Keyword(s):

Body Size ◽

Bottlenose Dolphin ◽

Tursiops Truncatus ◽

Squamous Epithelium ◽

Gulf Coast ◽

Bottlenose Dolphins ◽

Adult Life ◽

Lymphoid Cells ◽

Texas Gulf Coast ◽

Thymic Cysts

The thymus glands of 10 bottlenose dolphins, Tursiops truncatus, collected along the Texas Gulf coast were examined using standard histologic and immunocytochemical methods. The thymus gland of Tursiops persists into adult life, represented by medulla and progressively thinning cortex. A network of epithelial cells, including Hassal bodies, is demonstrable using polyclonal anti-cytokeratin antibody. The network condenses, with loss of lymphoid cells as involution progresses. Cysts arise within the condensed network. These cysts, found in eight of 10 animals, increase in number and size with increasing body size. Body size tends to reflect age. Thymic cysts typically have an irregular shape when small but tend to become spherical as they enlarge. Theey may be lined by squamous epithelium of variable thickness. Eventually, the cysts become macroscopic and filled with a colloidlike material and may largely replace the thymus, which may be identified by noncystic remnants adjacent to the cysts.

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Substance P and NK1 receptor expression in the enteric nervous system is related to the development of chagasic megacolon

Transactions of the Royal Society of Tropical Medicine and Hygiene ◽

10.1016/j.trstmh.2008.04.043 ◽

2008 ◽

Vol 102 (11) ◽

pp. 1154-1156 ◽

Cited By ~ 7

Author(s):

Alexandre B.M. da Silveira ◽

Michelle A.R. Freitas ◽

Enio C. de Oliveira ◽

Salustiano G. Neto ◽

Alejandro O. Luquetti ◽

...

Keyword(s):

Nervous System ◽

Substance P ◽

Enteric Nervous System ◽

Receptor Expression ◽

Nk1 Receptor ◽

Chagasic Megacolon

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Transplantation of enteric nervous system stem cells rescues nitric oxide synthase deficient mouse colon

Nature Communications ◽

10.1038/ncomms15937 ◽

2017 ◽

Vol 8 (1) ◽

Cited By ~ 24

Author(s):

Conor J. McCann ◽

Julie E. Cooper ◽

Dipa Natarajan ◽

Benjamin Jevans ◽

Laura E. Burnett ◽

...

Keyword(s):

Nitric Oxide ◽

Stem Cells ◽

Nervous System ◽

Nitric Oxide Synthase ◽

Enteric Nervous System ◽

Deficient Mouse ◽

Mouse Colon ◽

Oxide Synthase

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In ovo transplantation of enteric nervous system precursors from vagal to sacral neural crest results in extensive hindgut colonisation

Development ◽

10.1242/dev.129.12.2785 ◽

2002 ◽

Vol 129 (12) ◽

pp. 2785-2796 ◽

Cited By ~ 1

Author(s):

Alan J. Burns ◽

Jean-Marie M. Delalande ◽

Nicole M. Le Douarin

Keyword(s):

Nervous System ◽

Neural Crest ◽

Enteric Nervous System ◽

Enteric Neurons ◽

In Ovo ◽

Neuronal Marker ◽

Sacral Region ◽

Enteric Ganglia ◽

Migration Front ◽

Sacral Neural Crest

The enteric nervous system (ENS) is derived from vagal and sacral neural crest cells (NCC). Within the embryonic avian gut, vagal NCC migrate in a rostrocaudal direction to form the majority of neurons and glia along the entire length of the gastrointestinal tract, whereas sacral NCC migrate in an opposing caudorostral direction, initially forming the nerve of Remak, and contribute a smaller number of ENS cells primarily to the distal hindgut. In this study, we have investigated the ability of vagal NCC, transplanted to the sacral region of the neuraxis, to colonise the chick hindgut and form the ENS in an experimentally generated hypoganglionic hindgut in ovo model. Results showed that when the vagal NC was transplanted into the sacral region of the neuraxis, vagal-derived ENS precursors immediately migrated away from the neural tube along characteristic pathways, with numerous cells colonising the gut mesenchyme by embryonic day (E) 4. By E7, the colorectum was extensively colonised by transplanted vagal NCC and the migration front had advanced caudorostrally to the level of the umbilicus. By E10, the stage at which sacral NCC begin to colonise the hindgut in large numbers, myenteric and submucosal plexuses in the hindgut almost entirely composed of transplanted vagal NCC, while the migration front had progressed into the pre-umbilical intestine, midway between the stomach and umbilicus. Immunohistochemical staining with the pan-neuronal marker, ANNA-1, revealed that the transplanted vagal NCC differentiated into enteric neurons, and whole-mount staining with NADPH-diaphorase showed that myenteric and submucosal ganglia formed interconnecting plexuses, similar to control animals. Furthermore, using an anti-RET antibody, widespread immunostaining was observed throughout the ENS, within a subpopulation of sacral NC-derived ENS precursors, and in the majority of transplanted vagal-to-sacral NCC. Our results demonstrate that: (1) a cell autonomous difference exists between the migration/signalling mechanisms used by sacral and vagal NCC, as transplanted vagal cells migrated along pathways normally followed by sacral cells, but did so in much larger numbers, earlier in development; (2) vagal NCC transplanted into the sacral neuraxis extensively colonised the hindgut, migrated in a caudorostral direction, differentiated into neuronal phenotypes, and formed enteric plexuses; (3) RET immunostaining occurred in vagal crest-derived ENS cells, the nerve of Remak and a subpopulation of sacral NCC within hindgut enteric ganglia.

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