Age-related changes in substance P-immunoreactive nerve structures of the rat recto-anal region

• Authors: Nikolai Lazarov , Dimitar Itzev , Kamen Usunoff , Negrin Negrev , Radomir Radomirov
• Languages of publication: EN

Abstracts

EN

The recto-anal region is innervated by extrinsic and intrinsic nerves and a number of neuropeptides including substance P (SP) have been suggested to participate in the regulation of intestinal movements. We examined the age-related changes in the distribution of SP-immunoreactive nerve structures in the distal part of the rat large intestine. Using immunohistochemistry, the presence of SP was studied in fresh tissues from Wistar rats at different ages taken at three sampling sites, the distal rectum, anal canal and internal anal sphincter. In the 15-day old rats the myenteric plexus of the distal rectum and anal canal was well outlined by numerous SP-immunoreactive varicose nerve fibres encircling immunonegative perikarya. In the circular muscle layer, nerve fibres and small nerve bundles ran parallel to the muscle cells, while in the longitudinal muscle layer, only occasional nerve fibres were seen. At the level of the internal anal sphincter, no myenteric ganglia were present. Here, thin varicose fibers ran parallel to the smooth muscle cells. In the 3-month old rats, a larger number of intensely staining SP-immunoreactive nerve fibres were found and in the circular muscle layer, thicker nerve strands were observed. In the 26-month old rats, the density and staining intensity of SP-immunopositive nerve fibres in the myenteric plexus was lower than in the 3-month-old rats. Similar changes in the SP-immunostained fibres in the internal anal sphincter were observed. Degenerative alterations in SP-containing fibres during aging appear to play a role in ano-rectal motility and sphincter control.

Keywords

EN

Aging, Anal canal; Distal rectum; Internal anal sphincter; Myentric ganglia; Substance P; Recto-anal region; Rat

• Publisher: De Gruyter Open
• Journal: Open Medicine
• Year: 2010
• Volume: 5
• Issue: 3
• Pages: 358-364

Dates

published

1 - 6 - 2010

online

9 - 4 - 2010

Contributors

author

Nikolai Lazarov

• Department of Anatomy and Histology, Medical University-Sofia, 1431, Sofia, Bulgaria

author

Dimitar Itzev

• Institute of Neurobiology, Bulgarian Academy of Sciences, 1113, Sofia, Bulgaria

author

Kamen Usunoff

• Department of Anatomy and Histology, Medical University-Sofia, 1431, Sofia, Bulgaria

author

Negrin Negrev

• Department of Physiology, Medical University, 9000, Varna, Bulgaria

author

Radomir Radomirov

• Institute of Neurobiology, Bulgarian Academy of Sciences, 1113, Sofia, Bulgaria

References

• [1] Reeve D.R.E., Anatomy of the sphincters of the alimentary canal. In: P.A. Thomas, C.V. Mann (Eds.), Surgical Sphincters and Their Disorders, Macmillan, London, 1981, 1–26
• [2] Howard E.R., Garrett J.R., The intrinsic myenteric innervation of the hind-gut and accessory muscles of defaecation in the cat, Z. Zellforsch. Mikrosk. Anat., 1973, 136, 31–44 http://dx.doi.org/10.1007/BF00307678[Crossref]
• [3] Bouvier M., Gonella J., Nervous control of the internal anal sphincter of the cat, J. Physiol., 1981, 310, 457–69
• [4] Cook T.A., Brading A.F., Mortensen N.J., The pharmacology of the internal anal sphincter and new treatments of ano-rectal disorders, Aliment. Pharmacol. Ther., 2001, 15, 887–898 http://dx.doi.org/10.1046/j.1365-2036.2001.00995.x[Crossref]
• [5] Burleigh D.E., D’Mello A., Neural and pharmacologic factors affecting motility of the internal anal sphincter, Gastroenterology, 1983, 84, 409–417
• [6] Venkova K., Greenwood-Van Meerveld B., Krier J., Neural control of the large intestine, In: S.J.H. Brookes, M. Costa (Eds.), Innervation of the Gastrointestinal Tract, Taylor and Francis, New York, 2002, 171–187
• [7] Goyal R.K., Hirano I., The enteric nervous system, N. Eng. J. Med., 1996, 334, 1106–1115 http://dx.doi.org/10.1056/NEJM199604253341707[Crossref]
• [8] Said S.I., Peptides of the brain, gastrointestinal tract and other organs, In: McCann, Weiner (Eds.), Integrative Neuroendocrinology: Molecular, Cellular and Clinical Aspects, Karger, Basel, 1987, 127–136
• [9] Ferri G.-L., Adrian T.E., Allen J.M., Soimero L., Cancellieri A., Yeats J.C., Blank M., Polak J.M., Bloom S.R., Intramural distribution of regulatory peptides in the sigmoid-recto-anal region of the human gut, Gut, 1988, 29, 762–768 http://dx.doi.org/10.1136/gut.29.6.762[Crossref]
• [10] Itzev D.E., Usunoff K.G., Negrev N.N., Radomirov R.G., Histo- and immunohistochemical investigation of the innervation of rat recto-anal region, Compt. Rend. Acad. Bulg. Sci., 2009, 62, 123–130
• [11] von Euler U.S., Gaddum J.H., An unidentified depressor substance in certain tissue extracts, J. Physiol., 1931, 72, 74–87
• [12] Nilsson G., Larsson L.I., Håkanson R., Brodin E., Pernow B., Sundler F., Localization of substance P-like immunoreactivity in mouse gut, Histochemistry, 1975, 43, 97–99 http://dx.doi.org/10.1007/BF00490158[Crossref]
• [13] Llewellyn-Smith I.J., Furness J.B., Murphy R., O’Brien P.E., Costa M., Substance P-containing nerves in the human small intestine. Distribution, ultrastructure, and characterization of the immunoreactive peptide, Gastroenterology, 1984, 86, 421–435
• [14] Tomita R., Morita K., Tanjoh K., Munakata K., A role of peptidergic nerves in the internal anal sphincter of Hirschsprung’s disease, Surgery, 1999, 125, 60–66 [Crossref]
• [15] Otsuka, M., Yoshioka K., Neurotransmitter functions of mammalian tachykinins, Physiol. Rev., 1993, 73, 229–308
• [16] Holzer P., Holzer-Petsche, U., Tachykinin receptors in the gut: physiological and pathological implication, Curr. Opin. Pharmacol., 2001, 1, 583–590 http://dx.doi.org/10.1016/S1471-4892(01)00100-X[Crossref]
• [17] Hsu S.M., Raine L., Fanger H., Use of avidin-biotinperoxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedure, J. Histochem. Cytochem., 1981, 29, 577–580 [Crossref]
• [18] Bitar K.N., Hillemeier C., Biancani P., Differential regulation of smooth muscle contraction in rabbit internal anal sphincter by substance P and bombesin, Life Sci., 1990, 47, 2429–2434 http://dx.doi.org/10.1016/0024-3205(90)90487-C[Crossref]
• [19] Lolova I., Itzev D., Davidoff M., Innervation of the smooth muscle in human large intestine during ontogenesis, Z. Mikrosk.-Anat. Forsch., 1987, 101, 871–880
• [20] Fehér E., Léránth C., Williams T.H., Ultrastructural identification of substance P cells and processes in the rat myenteric plexus, Acta Morphol. Hung., 1984, 32, 23–29
• [21] Schultzberg M., Hökfelt T., Nilsson G., Terenius L., Rehfeld G.F., Brown M., Elde R., Goldstein M., Said S., Distribution of peptide- and catecholaminecontaining neurons in the gastro-intestinal tract of rat and guinea-pig: immunohistochemical studies with antisera to substance P, vasoactive intestinal polypeptide, enkephalins, somatostatin, gastrin/cholecystokinin, neurotensin and dopamine-bhydroxylase, Neuroscience, 1980, 5, 689–744 http://dx.doi.org/10.1016/0306-4522(80)90166-9[Crossref]
• [22] De Laet M.-H., Dassonville M., Steyaert H., Vanderveken E., Lotstra F., Vierendeels G., Przedborski S., Vaudry H., Vanderhaeghen J.-J., Decrease of vasoactive intestinal peptide, methionine-enkephalin, substance P and increase of neuropeptide Y immunoreactive nerve fibres in aganglionic colon of Hirschsprung’s disease, Neurochem. Int., 1989, 14, 135–141 http://dx.doi.org/10.1016/0197-0186(89)90113-7[Crossref]
• [23] Fehér E., Pénzes L., Density of substance P, vasoactive intestinal polypeptide and somatostatin-containing nerve fibers in the ageing small intestine of the rats, Gerontology, 1987, 33, 341–348 http://dx.doi.org/10.1159/000212901[Crossref]
• [24] Santer R.M., Conboy V.B., Prenatal undernutrition permanently decreases enteric neuron number and sympathetic innervation of Auerbach’s plexus in the rat, J. Anat., 1990, 168, 57–62
• [25] Gomez O.A., Castelucci P., Fontes R.B.V., Liberti E.A., Effects of pre- and postnatal protein deprivation and postnatal refeeding on myenteric neurons on the rat small intestine: A quantitative morphological study, Auton. Neurosci., 2006, 126–127, 277–285 http://dx.doi.org/10.1016/j.autneu.2006.03.003[Crossref]
• [26] Wade P.R., Cowen, T., Neurodegeneration: a key factor in the ageing gut, Neurogastroenterol. Motilit., 2004, 16Suppl. 1, 19–23 http://dx.doi.org/10.1111/j.1743-3150.2004.00469.x[Crossref]
• [27] Camilleri M., Cowen, T., Koch, T.R., Enteric neurodegeneration in ageing, Neurogastroenterol. Motilit., 2008, 20, 418–427 http://dx.doi.org/10.1111/j.1365-2982.2008.01134.x[Crossref]
• [28] Husberg B., Schultzberg M., Peptidergic innervation of the internal anal sphincter in Hirschsprung’s disease, Pediatr. Surg. Int., 1995, 11, 33–40

Identifiers

DOI

10.2478/s11536-009-0098-2