Summary
The enteric nervous and enteroendocrine systems regulate different processes in the small intestine. Ablation of myenteric plexus with benzalkonium chloride (BAC) stimulates epithelial cell proliferation, whereas endocrine serotonin cells may inhibit the process. To evaluate the connection between the systems and the influence of myenteric plexus on serotoninergic cells in rats during postnatal development, the ileal plexus was partially removed with BAC. Rats were treated at 13 or 21 days and sacrificed after 15 days. The cell bodies of myenteric neurons were stained by β NADH-diaphorase to detect the extension of denervation. The number of enteroendocrine cells in the ileum was estimated in crypts and villi in paraffin sections immunostained for serotonin. The number of neurons was reduced by 27.6 and 45% in rats treated on the 13th and 21st days, respectively. We tried to establish a correlation of denervation and the serotonin population according to the age of treatment. We observed a reduction of immunolabelled cells in the crypts of rats treated at 13 days, whereas this effect was seen in the villi of rats denervated at 21 days. These results suggest that the enteric nervous system might control the enteroendocrine cell population and this complex mechanism could be correlated to changes in cell proliferation.
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References
Bjerknes M, Cheng H (2001) Modulation of specific intestinal epithelial progenitors by enteric neurons. PNAS 98: 12497–12502
Crowell MD (2004) Role of serotonin in the pathophysiology of the irritable bowel syndrome. Brit J Pharmacol 141: 1285–1293
Dahl JL, Bloom DD, Epstein ML, Fox DA, Bass P (1987) Effect of chemical ablation of myenteric neurons on neurotransmitter levels in the rat jejunum. Gastroenterology 92: 338–344
Faussone-Pellegrini MS, Matini P, Starch W (1996) Differentiation of enteric plexuses and interstitial cells of Cajal in the rat gut during pre- and postnatal life. Acta Anat 155: 113–125
Fox DA, Bass P (1986) Pharmacological characterization of rat jejunal contractility after chronic ablation of the myenteric neurons. J Pharmacol Exp Ther 238: 372–377
Fox DA, Epstein ML, Bass P (1983) Surfactants selectively ablate enteric neurons of the rat jejunum. Pharmacol Exp Ther 227: 583–544
Furness JB, Costa M (1987) (Arrangement of the enteric plexuses). In: The Enteric Nervous System, 1st edn., New York: Churchil Livingstone, pp. 7–25
Gabella G (1987) The number of neurons in the small intestine of mice, guinea-pigs and sheep. Neuroscience 22: 737–752
Gomes JR, Alvares EP (1998) Cell proliferation and migration in the jejunum of suckling rats submitted to progressive fasting. Braz J Med Biol Res 31: 281–288
Hadzijahic N, Renehan WE, Ma CK, Zhang X, Fogel R (1993) Myenteric plexus destruction alters morphology of rat intestine. Gastroenterology 105: 1017–1028
Hanani M, Ledder O, Yutkin V, Abu-Dalu R, Huang TY, Hartig W, Vannucchi MG, Faussone-Pellegrini MS (2003) Regeneration of myenteric plexus in the mouse colon after experimental denervation with benzalkonium chloride. J Comp Neurol 462: 315–327
Hansen MB (2003) The enteric nervous system II: gastrointestinal Functions. Pharmacol Toxicol 92: 249–257
Henning SJ (1981) Postnatal development coordination of feeding, digestion, and metabolism. Am J Physiol 241: G199–G214
Hernandes L, Gama P, Alvares EP (2004) Ileal VIP submucous neurons: confocal study of the are enlargement induced by myenteric denervation in weanling rats. Regul Pept 117(1): 69–72
Hernandes L, Pereira LCMS, Alvares EP (2003) Goblet cell number in the ileum of rats denervated during suckling and weaning. Biocell 27(3): 347–351
Hernandes L, Zucoloto S, Alvares EP (2000) Effect of myenteric denervation on intestinal epithelium proliferation and migration of suckling and weanling rats. Cell Prolif 33: 127–138
Hocker M, Wiedenmann B (1998) Molecular mechanisms of enteroendocrine differentiation. Ann New York Acad Sci 859: 160–174
Holle GE (1991) Changes in the structure and regeneration mode of the rat small intestinal mucosa following benzalkonium chloride treatment. Gastroenterology 101: 1264–1273
Inokuchi H, Fujimoto S, Kawai K (1983) Cellular kinetics of gastrointestinal mucosa with special reference to gut endocrine cells. Arch Histol Jap 46(2): 137–157
Klein RM, McKenzie JC (1983) The role of cell renewal in the ontogeny of the intestine. I Cell proliferation patterns in adult, fetal, and neonatal intestine. J Gastroenterol Nutr 2: 10–43
Krause JW, Yamada J, Cutts JH (1989) Enteroendocrine cells in the developing opossum small intestine and colon. J Anat 162: 83–96
Luck MS, Dahl JL, Boyeson MG, Bass P (1993) Neuroplasticity in the smooth muscle of the myenterically and extrinsecally denervated rat jejunum. Cell Tissue Res 271: 363–374
Matini P, Mayer B, Faussone-Pellegrini MS (1997) Neurochemical differentiation of rat enteric neurons during pre- and postnatal life. Cell Tissue Res 288: 11–23
Nichols DB, Cheng H, Leblond CP (1974) Variability of the shape and argentaffinity of the granules in the enteroendocrine cells of the mouse duodenum. J Histochem Cytochem 22(10):929–944
O’Hara JR, HO W, Linden DR, Mawe GM, Sharkey KA (2004) Endocrine cells and 5-HT availability are altered in mucosa of guinea pigs with TNBS ileitis. Am J Physiol Gastrointest Liver Physiol 287: G998-G1007
Ormsbee HS 3rd, Fondacaro JD (1985) Action of serotonin on the gastrointestinal tract. Proc Soc Exp Biol Med 178(3): 333–338
Palanch AC, Alvares EP (1998) Feeding manipulation elicits different proliferative responses in the gastrointestinal tract of suckling and weanling rats. Braz J Med Biol Res 31: 565–572
Pham TD, Gershom MD, Rothman TP (1991) Time of origin of neurons in the murine enteric nervous system: sequence in relation to phenotype. J Comp Neurol 314: 789–798
Rothman TP, Nilaver G, Gershon MD (1984) Colonization of the developing murine enteric nervous system and subsequent phenotype expression by the precursors of peptidergic neurons. J Comp Neurol 225: 13–23
Santos GC, Zucoloto S, Garcia SB (2000) Endocrine cells in denervated intestine. Int J Exp Path 81(4):265–270
Sjólund K, Sandén G, Hakanson R, Sundler F (1983) Endocrine cells in human intestine: an immunocytochemical study. Gastroenterology 85: 1120
See NA, Epstein ML, Dahl JL, Bass P (1990) The myenteric plexus regulates cell growth in rat jejunum. J Auton Nerv Sys 31: 219–229
See NA, Epstein ML, Schultz E, Pienkowski TP, Bass P (1988) Hyperplasia of jejunal smooth muscle in the myenterically denervated rat. Cell Tissue Res 253: 609–617
Toumi F, Neunlist M, Cassagnau E, Parois S, Laboisse CL, Galmiche JP, Jarry A (2003) Human submucosal neurons regulate intestinal epithelial cell proliferation: evidence from a novel co-culture model. Neurograstroenterol Motil 15: 239–242
Zachrisson K, Uribe A (1998) Serotonin and neuroendocrine peptides influence DNA syntheses in rat and human small intestinal cells in vitro. Acta Physiol Scand 163: 195–200
Zucoloto S, Deus DA, Martins AA, Muglia VF, Kajiwara JK, Garcia SB (1997) The relationship between myenteric, neuronal denervation, smooth muscle thickening and epithelial cell proliferation in the rat colon. Res Exp Med 197: 117–124
Zucoloto S, Diaz JA, Oliveira JSM, Muccilo G, Sales Neto VN, Kajiwara JK (1988) Effect of chemical ablation of myenteric neurones on intestinal cell proliferation. Cell Tissue Kinet 21: 213–219
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Hernandes, L., Fernandes, M., Pereira, L. et al. Myenteric denervation differentially reduces enteroendocrine serotonin cell population in rats during postnatal development. J Mol Hist 37, 95–100 (2006). https://doi.org/10.1007/s10735-006-9016-y
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DOI: https://doi.org/10.1007/s10735-006-9016-y