Quantitative changes of nitrergic neurons during postnatal development of chicken myenteric plexus

ObjectiveInformation regarding the development of the enteric nervous system (ENS) is important for understanding the functional abnormalities of the gut. Because fertilized chicken eggs provide easy access to embryos, chicken models have been widely used to study embryonic development of myenteric plexus; however, no study has been focused on the postnatal period. The aim of this study was to perform a qualitative and quantitative analysis of the nitrergic neurons in the myenteric plexus of developing chickens in the postnatal period.MethodsWhole-mount preparations of the myenteric plexus were made in 7-d, 15-d, and 40-d old (adult) chickens of either sex (n=15). The myenteric plexus was studied after nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d) histochemistry using light microscopy, digital photography, and Image-Pro Plus 6.0 software. The numbers of positively stained neurons and ganglia were counted in the duodenum, jejunum, ileum, caecum, and colon in the different age groups. Data were expressed as mean±standard deviation (SD), and statistical analysis was performed using a one-way analysis of variance (ANOVA) test.ResultsThe positively stained neurons showed various morphologies and staining intensities, and formed bead-shaped and U-shaped arrangements in the myenteric plexus. The densities of neurons and ganglia increased with age. However, the number of positive neurons per ganglion increased. The number of NADPH-d-positive neurons was highest in the colon, followed by the ileum, the jejunum, the duodenum, and the caeca in all age groups.ConclusionsDevelopmental changes in the myenteric plexus of chickens continue in the postnatal period, indicating that the maturation process of the gastrointestinal function is gradual. In addition, no significant difference is happening among different intestinal segments during postnatal development, suggesting that the function of different intestinal segments had been determined after birth.

[1]  Anita C. Thomas,et al.  Nitric Oxide Synthase: Non-Canonical Expression Patterns , 2014, Front. Immunol..

[2]  T. Merrot,et al.  Tonic inhibition of human small intestinal motility by nitric oxide in children but not in adults , 2010, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[3]  N. Bódi,et al.  Spatial Pattern Analysis of Nitrergic Neurons in the Myenteric Plexus of the Duodenum of Different Mammalian Species , 2009, Acta biologica Hungarica.

[4]  U. Rolle,et al.  Age-related changes in the myenteric plexus of the porcine bowel. , 2009, Journal of pediatric surgery.

[5]  P. Puri,et al.  Correlation of Enteric NADPH-d Positive Cell Counts with the Duration of Incubation Period in NADPH-d Histochemistry , 2009, Pathology & Oncology Research.

[6]  N. Németh,et al.  New Insights into the Neuromuscular Anatomy of the Ileocecal Valve , 2009, Anatomical record.

[7]  P. Puri,et al.  New hypothesis on the pathogenesis of ileocecal intussusception. , 2007, Journal of pediatric surgery.

[8]  U. Agrimi,et al.  Nitric Oxide Synthase Immunoreactivity and NADPH-d Histochemistry in the Enteric Nervous System of Sarda Breed Sheep With Different PrP Genotypes in Whole-mount and Cryostat Preparations , 2007, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[9]  M. Krecsmarik,et al.  Spatial pattern analysis of nitrergic neurons in the developing myenteric plexus of the human fetal intestine , 2004, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[10]  E. Ekblad,et al.  Vasoactive intestinal peptide and nitric oxide promote survival of adult rat myenteric neurons in culture , 2003, Journal of neuroscience research.

[11]  P. Wade,et al.  Age-related changes in motility and in nitregic myenteric neurons in guinea pig distal colon , 2003 .

[12]  V. Román,et al.  Quantitative Distribution of NADPH-diaphorase-positive Myenteric Neurons in Different Segments of the Developing Chicken Small Intestine and Colon , 2000, The Histochemical Journal.

[13]  J. Tack,et al.  Neurochemical coding of myenteric neurons in the guinea-pig antrum , 1999, Cell and Tissue Research.

[14]  D. O’Briain,et al.  Notable postnatal alterations in the myenteric plexus of normal human bowel , 1999, Gut.

[15]  G. B. Azzena,et al.  Nitric oxide regenerates the normal colonic peristaltic activity in mdx dystrophic mouse , 1999, Neuroscience Letters.

[16]  M. Azanza,et al.  Distribution of NADPH Diaphorase-Positive Neurons in the Enteric Nervous System of the Rabbit Intestine , 1998, Neurochemical Research.

[17]  G. Burnstock,et al.  Distribution of NADPH-diaphorase activity in the embryonic chicken gut , 1995, Anatomy and Embryology.

[18]  M. Hanani,et al.  Nitric oxide-containing nerves in bowel segments of patients with Hirschsprung's disease. , 1995, Journal of pediatric surgery.

[19]  C. Cracco,et al.  Quantitative study of the NADPH-diaphorase-positive myenteric neurons of the rat ileum , 1994, Neuroscience.

[20]  G. Pearson.  Structural organization and neuropeptide distributions in the equine enteric nervous system: an immunohistochemical study using whole-mount preparations from the small intestine , 1994, Cell and Tissue Research.

[21]  J. Becker,et al.  Nitric oxide producing neurons in the monkey and human digestive system , 1994, The Journal of comparative neurology.

[22]  C. Montagnese,et al.  Distribution and morphological features of nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d) activity in intrinsic neurons of the Oddi sphincter of the cat , 1994, Neuroscience Letters.

[23]  H. Young,et al.  Total numbers of neurons in myenteric ganglia of the guinea-pig small intestine , 1993, Cell and Tissue Research.

[24]  J. Szurszewski,et al.  Nitric oxide mediates inhibitory nerve input in human and canine jejunum. , 1993, Gastroenterology.

[25]  W. Staines,et al.  Histochemical localization of nitric oxide-synthesizing neurons and vascular sites in the guinea-pig intestine , 1992, Neuroscience.

[26]  G. Burnstock,et al.  Colocalization of nitric oxide synthase and NADPH-diaphorase in the myenteric plexus of the rat gut , 1992, Neuroscience Letters.

[27]  S. Schiffmann,et al.  Nitric oxide synthase activity in infantile hypertrophic pyloric stenosis. , 1992, The New England journal of medicine.

[28]  S. Snyder,et al.  NADPH diaphorase and nitric oxide synthase colocalization in enteric neurons of canine proximal colon. , 1992, The American journal of physiology.

[29]  S. Snyder,et al.  Ultrastructural localization of nitric oxide synthese immunoreactivity in guinea-pig enteric neurons , 1992, Brain Research.

[30]  M. Rand,et al.  NITRERGIC TRANSMISSION: NITRIC OXIDE AS A MEDIATOR OF NON‐ADRENERGIC, NON‐CHOLINERGIC NEURO‐EFFECTOR TRANSMISSION , 1992, Clinical and experimental pharmacology & physiology.

[31]  D. Burleigh.  Ng-nitro-L-arginine reduces nonadrenergic, noncholinergic relaxations of human gut. , 1992, Gastroenterology.

[32]  S. Snyder,et al.  Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[33]  G. Boeckxstaens,et al.  Non-adrenergic non-cholinergic relaxation mediated by nitric oxide in the canine ileocolonic junction. , 1990, European journal of pharmacology.

[34]  G. Gabella.  The number of neurons in the small intestine of mice, guinea-pigs and sheep , 1987, Neuroscience.

[35]  J. Okoye.  Cases of intestinal intussusception in young fowls. , 1985, Avian pathology : journal of the W.V.P.A.

[36]  G. Gabella.  Neuron size and number in the myenteric plexus of the newborn and adult rat. , 1971, Journal of anatomy.

[37]  D. Doxey,et al.  The equine enteric nervous system — Neuron characterization and distribution in adults and juveniles , 2005, Veterinary Research Communications.

[38]  P. Puri,et al.  Differences in nitrergic innervation of the developing chick cloaca and colorectum , 2005, Pediatric Surgery International.

[39]  Arthur Getis,et al.  Spatial Pattern Analysis , 2005 .

[40]  Li Lian-jun.  The Morphological Features of NADPH-diaphorase Positive Myenteric Neurons of the Postnatal Piglets Small Intestine , 2004 .

[41]  L. Mei.  Comparison of NOS distribution in myenteric plexus of various segments of gastrointestinal tract of the mandarin vole,Microtus mandarinus , 2003 .

[42]  B. Boots,et al.  Spatial Pattern Analysis , 2016 .

[43]  R. Dubey,et al.  Role of nitric oxide in the biology, physiology and pathophysiology of reproduction. , 1998, Human reproduction update.

[44]  A. Aljada,et al.  Nitric oxide synthase. , 1998, Methods in molecular biology.

[45]  P. Puri,et al.  Absence of NADPH-diaphorase activity in internal anal sphincter (IAS) achalasia. , 1995, Journal of pediatric gastroenterology and nutrition.