Summary
The three-dimensional distribution of vasoactive intestinal polypeptide (VIP)-like immunoreactive (VIPLI) structures in rat stomach and their origins were investigated using the indirect immunofluorescence method in whole mounted tissue.
The present study demonstrates a very dense VIPLI fiber meshwork in the circular muscle layer, longitudinal muscle layer and myenteric plexus. In the muscle layers VIPLI immunoreactive fibers run parallel to the muscle. VIPLI fibers are distributed evenly throughout the entire stomach. We have also shown by experimental manipulations that the fibers in the stomach originate from VIPLI neurons in the myenteric plexus.
Similar content being viewed by others
References
Alumets, J., Fahrenkrug, J., Håkanson, R., Schaffalitzky de Muckadell, O. B., Sundler, F., Uddman, R.: A rich VIP nerve supply is characteristic of sphincters. Nature280, 155–156 (1979).
Barbezat, G. O., Grossman, M. I.: Intestinal secretion: stimulation by peptides. Science174, 422–423 (1971).
Bryant, M. G., Polak, J. M., Modlin, I., Bloom, S. R., Albuquerque, R. H., Pearse, A. G. E.: Possible dual role for vasoactive intestinal peptide as gastrointestinal hormone and neurotransmitter substance. Lancet1, 991–993 (1976).
Coons, A. H.: Fluorescent antibody method. In: General Cytochemical Methods (Danielli, J. F., ed.), pp. 1–90. New York: Academic Press. 1958.
Costa, M., Buffa, R., Furness, J. B., Solcia, E. L.: Immunohistochemical localization of polypeptides in peripheral autonomic nerves using whole mount preparations. Histochemistry65, 157–165 (1980 a).
Costa, M., Furness, J. B.: Origins, pathways and terminations of neurons with VIP-like immunoreactivity in the guinea-pig small intestine. Neuroscience8, 665–676 (1983).
Costa, M., Furness, J. B., Buffa, R., Said, S. I.: Distribution of enteric nerve cell bodies and axons showing immunoreactive for vasoactive intestinal polypeptide (VIP) in the guinea-pig intestine. Neuroscience5, 587–596 (1980 b).
Costa, M., Furness, J. B., Llewellyn-Smith, I. J., Cuello, A. C.: Projection of substance P neurons within the guinea-pig small intestine.Neuroscience 6, 411–428 (1981).
Costa, M., Furness, J. B., Llewellyn-Smith, I. J., Davies, B., Oliver, J.: An immuno-histochemical study of the profections of somatostatin-containing neurons in the guinea-pig intestine. Neuroscience5, 841–852 (1980 c).
Dahlström, A.: Effect of colchicine on transport of amine storage granules in sympathetic nerve of rat. Eur. J. Pharmacol.5, 111–112 (1986).
Dalsgaard, C. J., Hökfelt, T., Schultzberg, M., Lundberg, J. M., Terenius, L., Dockray, G. J., Cuello, C., Goldstein, M.: Origin of peptide-containing fibers in the inferior mesenteric ganglion of the guinea-pig: immunohistochemical studies with antisera to substance P, enkephalin, vasoactive intestinal polypeptide, cholecystokinin and bombesin. Neuroscience9, 191–211 (1983).
Eklund, S., Jodal, M., Lundgre, O., Sjoqvist, A.: Effects of vasoactive intestinal polypeptide on blood flow, motility and fluid transport in the gastrointestinal tract of the cat. Acta Physiol. Scand.105, 461–468 (1979).
Fahrenkrug, J.: Vasoactive intestinal polypeptide: Measurement, distribution and putative neurotransmitter function. Digestion19, 149–169 (1979).
Fahrenkrug, J., Haglund, U., Jodal, M., Lundgren, O., Olbe, L., Schaffalizky de Muckdell, O. B.: Nervous release of vasoactive intestinal polypeptide in the gastrointestinal tract of cats: Possible physiological implications. J. Physiol. (Lond.)284, 291–305 (1978).
Furness, J. B., Costa, M.: Projections of intestinal neurons showing immuno-reactivity for vasoactive intestinal polypeptide are consistent with these neurons being the enteric inhibitory neurons. Neurosci. Lett.15, 199–204 (1979).
Furness, J. B., Costa, M.: Enteric inhibitory nerves and VIP. In: Vasoactive Intestinal Peptide, Advances in Peptide Hormone Research Series (Said, S. I., ed.), pp. 391–406. New York: Raven Press. 1982.
Furness, J. B., Costa, M.: Neurons with 5-hydroxytryptamine-like immuno-reactivity in the enteric nervous system: Their projections in the guineapig small intestine. Neuroscience7, 341–349 (1982).
Furness, J. B., Costa, M., Walsh, J. H.: Evidence for and significance of the projection of VIP neurons from the myenteric plexus to the taenia coli in the guinea-pig. Gastroenterology80, 1557–1561 (1981).
Fuxe, K., Hökfelt, T., Said, S. I., Mutt, V.: Vasoactive intestinal polypeptide and the nervous system: immunohistochemical evidence for localization in central and peripheral neurons, particularly intracortical neurons. Neurosci. Lett.5, 241–246 (1977).
Jessen, K. R., Saffrey, M. J., Van Noorden, S., Bloom, S. R., Polak, J. M., Burnstock, K.: Immunohistochemical studies of the enteric nervous system in tissue culture and in situ. Localization of vasoactive intestinal polypeptide (VIP), substance P and endephalin immunoreactive nerves in the guinea-pig gut. Neuroscience5, 1717–1735 (1980).
Krejs, G. J., Brakley, R. M., Read, N. W., Fordtran, J. S.: Intestinal secretion induced by vasoactive intestinal polypeptide. J. Clin. Invest.61, 1337–1345 (1978).
Kreutzberg, G.: Neuronal dynamics and flow-IV. Blockage of intra-axonal enzyme transport by colchicine. Proc. Nat. Acad. Sci. U.S.A.62, 722–728 (1969).
Larsson, L. I.: Ultrastructural localization of a new neuronal peptide (VIP). Histochemistry54, 173–176 (1977).
Larsson, L. I., Fahrenkrug, J., Schaffalizky de Muckdell, O. B., Sundler, F., Håkanson, R., Rehfeld, J. F.: Localization of vasoactive intestinal polypeptide to central and peripheral neurons. Proc. Nat. Acad. Sci. U.S.A.73, 3197–3200 (1976).
Malmfors, G., Leander, S., Brodin, F., Håkanson, R., Holmin, T., Sundler, F.: Peptide-containing neurons intrinsic to the gut wall, an experimental study in the pig. Cell Tissue Res.214, 225–238 (1981).
Minagawa, H., Shiosaka, S., Inoue, H., Hayashi, N., Kasahara, A., Kamata, T., Tohyama, M., Shiotani, Y.: Three-dimensional distribution of substance P-containing structures in the rat stomach and their origins using whole-mount tissue. Gastroenterology86, 51–59 (1984).
Racusen, L. C., Binder, H. J.: Alteration in large intestinal electrolyte transport by vasoactive intestinal polypeptide in the rat. Gastroenterology73, 790–796 (1977).
Said, S. I., Mutt, V.: Polypeptide with broad biological activity: Isolation from small intestine. Science169, 1217–1218 (1970 a).
Said, M. I., Mutt, V.: Potent peripheral and splanchnic vasodilator peptide from normal gut. Nature225, 863–864 (1970 b).
Schwartz, C. J., Kimberg, D. V., Scheerin, H. F., Field, M., Said, S. I.: Vasoactive intestinal peptide stimulation of adenylate cyclase and active electrolyte secretion intestinal mucosa. J. Clin. Invest.54, 536–544 (1974).
Schiltzberg, M., Dreyfus, C. F., Gershon, M. D., Hökfelt, T., Eldem, R. P., Nilsson, G., Said, S. I., Goldstein, M.: VIP-, enkephalin-, substance P-, and somatostatin-like immunoreactivity in neurons intrinsic to the intestine. Brain Res.155, 239–248 (1978).
Schultzberg, M., Hökfelt, T., Nilsson, G., Terenius, L., Rehfeld, J., Brown, M., Elde, R. P., Goldstein, M., Said, S. I.: Distribution of peptide and catechol-amine neurons in the gastrointestinal tract of rat and guinea-pig. Neuroscience5, 689–744 (1980).
Thulin, L., Olsson, P.: Effects of intestinal peptide mixture G2 and vasoactive intestinal peptide VIP on splanchnic circulation in the dog. Acta Chir. Scand.139, 691–697 (1973).
Uddman, R., Alumets, J., Edvinsson, L., Hakanson, R., Sundler, F.: Peptidergic (VIP) innervation of the esophagus. Gastroenterology75, 5–8 (1978).
Williams, J. T., North, R. A.: Vasoactive intestinal polypeptide excites neurones of the myenteric plexus. Brain Res.175, 174–177.
Zamboni, L., De Martino, C.: Buffered picric-acid formaldehyde: a new rapid fixative for electronmicroscopy. J. Cell. Biol.35, 148 a (1967).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Inoue, H., Shiosaka, S., Sasaki, Y. et al. Three-dimensional distribution of vasoactive intestinal polypeptide-containing structures in the rat stomach and their origins using whole mount tissue. J. Neural Transmission 59, 195–205 (1984). https://doi.org/10.1007/BF01250008
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01250008