Abstract
Nitrergic myenteric neurons are especially susceptible to the development of neuropathy in functional gastrointestinal disorders. Investigations of the similarities and dissimilarities in the organization of nitrergic neurons in the various mammalian species are therefore important in an effort to determine the extent to which the results obtained in different animal models can be generalized. In the present work, the density and the spatial organization of the nitrergic neurons in the myenteric plexus of the duodenum were investigated in 7 mammalian species. After nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d) histochemistry, the Plexus Pattern Analysis software (PPAs) was applied to count the nuclei of nitrergic neurons, calculate the proportions of the areas covered by the plexus and perform randomization analysis. All 7 species exhibited a large population of nitrergic myenteric neurons, with densities in the range 12–56 cells/mm2. The distribution patterns of these neurons differed markedly in the different species, however, the rat was the only species in which the nitrergic neurons appeared to be randomly distributed. The PPAs in conjunction with NADPH-d histochemistry proved to be a simple and fast tool with which to reveal similarities and dissimilarities in the spatial arrangement of the nitrergic neurons in the different species.
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Balaskas, C., Saffrey, M. J., Burnstock, G. (1995) Distribution of NADPH-diaphorase activity in the embryonic chicken gut. Anat. Embryol. (Berl) 192, 239–245.
Belai, A., Cooper, S., Burnstock, G. (1995) Effect of age on NADPH-diaphorase-containing myenteric neurons of rat ileum and proximal colon. Cell Tissue Res. 279, 379–383.
Belai, A., Schmidt, H. H., Hoyle, C. H., Hassall, C. J., Saffrey, M. J., Moss, J., Förstermann, U., Murad, F., Burnstock, G. (1992) Colocalization of nitric oxide synthase and NADPH-diaphorase in the myenteric plexus of the rat gut. Neurosci. Lett. 143, 60–64.
Boeckxstaens, G. E., Pelckmans, P. A., Ruytjens, I. F., Bult, H., DeMan, J. G., Herman, A. G., Van Maercke, Y. M. (1991) Bioassay of nitric oxide released upon stimulation of non-adrenergic noncholinergic nerves in the canine ileocolonic junction. Br. J. Pharmacol. 103, 1085–1091.
Bosman, C., Devito, R., Fusilli, S., Boldrini, R. (2001) A new hypothesis on the pathogenesis of intestinal pseudo-obstruction by intestinal neuronal dysplasia (IND). Pathol. Res. Pract. 197, 789–796.
Bult, H., Boeckxstaens, G. E., Pelckmans, P. A., Jordaens, F. H., Van Maercke, Y. M., Herman, A. G. (1990) Nitric oxide as an inhibitory non-adrenergic non-cholinergic neurotransmitter. Nature 345, 346–347.
Cellek, S., Qu, W., Schmidt, A. M., Moncada, S. (2004) Synergistic action of advanced glycation end products and endogenous nitric oxide leads to neuronal apoptosis in vitro: a new insight into selective nitrergic neuropathy in diabetes. Diabetologia 47, 331–339.
Chaudhury, A., Shariff, A., Srinivas, M., Sabherwal, U. (2004) Changes in nitrergic innervation of defunctionalized rat colon after diversion colostomy. Neurogastroenterol. Motil. 16, 475–487.
Cracco, C., Filogamo, G. (1994) Quantitative study of the NADPH-diaphorase-positive myenteric neurons of the rat ileum. Neuroscience 61, 351–359.
Cserni, T., Paran, S., Puri, P. (2007) The effect of age on colocalization of acetylcholinesterase and nicotinamide adenine dinucleotide phosphate diaphorase staining in enteric neurons in an experimental model. J. Pediatr. Surg. 42, 300–304.
De Giorgio, R., Parodi, J. E., Brecha, N. C., Brunicardi, F. C., Becker, J. M., Go, V. L., Sternini, C. (1994) Nitric oxide producing neurons in the monkey and human digestive system. J. Comp. Neurol. 342, 619–627.
Furness, J. B., Li, Z. S., Young, H. M., Förstermann, U. (1994) Nitric oxide synthase in the enteric nervous system of the guinea-pig: a quantitative description. Cell Tissue Res. 277, 139–149.
Gábriel, R., Pásztor, I., Dénes,V., Wilhelm, M. (1998) Some neurohistochemical properties of nerve elements in myenteric plexus of rabbit ileum: similarities and dissimilarities to the rodent pattern. Cell Tissue Res. 292, 283–291.
Hope, B. T., Michael, G. J., Knigge, K. M., Vincent, S. R. (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. Natl. Acad. Sci. USA. 88, 2811–2814.
Izbéki, F., Wittman, T., Rosztóczy, A., Linke, N., Bódi, N., Fekete, E., Bagyánszki, M. (2008) Immediate insulin treatment prevents gut motility alterations and loss of nitrergic neurons in the ileum and colon of rats with streptozotocin-induced diabetes. Diabetes. Res. Clin. Pract. 80, 192–198.
Jarvinen, M. K., Wollmann, W. J., Powrozek, T. A., Schultz, J. A., Powley, T. L. (1999) Nitric oxide synthase-containing neurons in the myenteric plexus of the rat gastrointestinal tract: distribution and regional density. Anat. Embryol. (Berl). 199, 99–112.
Karaosmanoglu, T., Aygun, B., Wade, P. R., Gershon, M. D. (1996) Regional differences in the number of neurons in the myenteric plexus of the guinea pig small intestine and colon: an evaluation of markers used to count neurons. Anat. Rec. 244, 470–480.
Krecsmarik, M., Izbéki, F., Bagyánszki, M., Linke, N., Bódi, N., Kaszaki, J., Katarova, Z., Szabó, A., Fekete, E., Wittmann, T. (2006) Chronic ethanol exposure impairs neuronal nitric oxide synthase in the rat intestine. Alcohol. Clin. Exp. Res. 30, 967–973.
Lefebvre, R. A., Barthó, L. (1997) Mechanism of nitric oxide-induced contraction in the rat isolated small intestine. Br. J. Pharmacol. 120, 975–981.
Lefebvre, R. A. (1995) Nitric oxide in the peripheral nervous system. Ann. Med. 27, 379–388.
Mizuta, Y., Takahashi, T., Owyang, C. (1999) Nitrergic regulation of colonic transit in rats. Am. J. Physiol. 277, G275–279.
Phillips, R. J., Powley, T. L. (2007) Innervation of the gastrointestinal tract: patterns of aging. Auton. Neurosci. 136, 1–19.
Porter, A. J., Wattchow, D. A., Brookes, S. J., Costa, M. (2002) Cholinergic and nitrergic interneurons in the myenteric plexus of the human colon. Gut 51, 70–75.
Román, V., Bagyánszki, M., Krecsmarik, M., Horváth, A., Resch, B. A., Fekete, E. (2004) Spatial pattern analysis of nitrergic neurons in the developing myenteric plexus of the human fetal intestine. Cytometry A.57, 108–112.
Scherer-Singler, U., Vincent, S. R., Kimura, H., McGeer, E. G. (1983) Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J. Neurosci. Methods 9, 229–234.
Spångéus, A., Suhr, O., El-Salhy, M. (2000) Diabetic state affects the innervation of gut in an animal model of human type 1 diabetes. Histol. Histopathol. 15, 739–744.
Takaki, M., Wood, J. D., Gershon, M. D. (1985) Heterogeneity of ganglia of the guinea pig myenteric plexus: an in vitro study of the origin of terminals within single ganglia using a covalently bound fluorescent retrograde tracer. J. Comp. Neurol. 235, 488–502.
Teramoto, M., Domoto, T., Tanigawa, K., Yasui, Y., Tamura, K. (1996) Distribution of nitric oxide synthase-containing nerves in the aganglionic intestine of mutant rats: a histochemical study. J. Gastroenterol. 31, 214–223.
Timmermans, J. P., Barbiers, M., Scheuermann, D. W., Bogers, J. J., Adriaensen, D., Fekete, E., Mayer, B., Van Marck, E. A., De Groodt-Lasseel, M. H. (1994) Nitric oxide synthase immunoreactivity in the enteric nervous system of the developing human digestive tract. Cell Tissue Res. 275, 235–245.
Van Ginneken, C., Van Meir, F., Sommereyns, G., Sys, S., Weyns, A. (1998) Nitric oxide synthase expression in enteric neurons during development in the pig duodenum. Anat. Embryol. (Berl). 198, 399–408.
Van Ginneken, C., van Meir, F., Sys, S., Weyns, A. (2001) Stereologic description of the changing expression of constitutive nitric oxide synthase and heme oxygenase in the enteric plexuses of the pig small intestine during development. J. Comp. Neurol. 437, 118–128.
Wang, Z. Q., Watanabe, Y., Toki, A., Kohno, S., Hasegawa, S., Hamazaki, M. (2000) Involvement of endogenous nitric oxide and c-kit-expressing cells in chronic intestinal pseudo-obstruction. J. Pediatr. Surg. 35, 539–544.
Wiley, J. W. (2002) Aging and neural control of the GI tract: III. Senescent enteric nervous system: lessons from extraintestinal sites and nonmammalian species. Am. J. Physiol. Gastrointest. Liver Physiol. 283, G1020–1026.
Wilhelm, M., Bátori, Z., Pásztor, I., Gábriel, R. (1998) NADPH-diaphorase positive myenteric neurons in the ileum of guinea-pig, rat, rabbit and cat: a comparative study. Eur. J. Morphol. 36, 143–152.
Young, H. M., Furness, J. B., Sewell, P., Burcher, E. F., Kandiah, C. J. (1993) Total numbers of neurons in myenteric ganglia of the guinea-pig small intestine. Cell Tissue Res. 272, 197–200.
Young, H. M., Furness, J. B., Shuttleworth, C. W., Bredt, D. S., Snyder, S. H. (1992) Co-localization of nitric oxide synthase immunoreactivity and NADPH diaphorase staining in neurons of the guineapig intestine. Histochemistry 97, 375–378.
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Supported by a grant from the National Scientific Research Programs (OTKA) No. F46201 to M.B.
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Bódi, N., Battonyai, I., Talapka, P. et al. Spatial Pattern Analysis of Nitrergic Neurons in the Myenteric Plexus of the Duodenum of Different Mammalian Species. BIOLOGIA FUTURA 60, 347–358 (2009). https://doi.org/10.1556/ABiol.60.2009.4.2
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DOI: https://doi.org/10.1556/ABiol.60.2009.4.2