Abstract
Somatostatin messenger RNA in the antrum and corpus of rat stomach was quantified by Northern and slot blotting using a probe generated by the polymerase chain reaction. Fasting for 48 h enhanced the abundance of somatostatin mRNA in the pyloric antral region, but not in the acid-secreting region of the stomach. In fasted rats, somatostatin mRNA in antrum, but not corpus, was decreased by inhibition of acid secretion with omeprazole. In contrast, in rats treated with capsaicin to lesion small diameter afferents there was a significant decrease in somatostatin mRNA abundance in the corpus but not antrum. The effects of capsaicin cannot be attributed to nonspecific changes in gastric endocrine cell gene expression, since the abundance of histidine decarboxylase mRNA (which is a functionally regulated marker for a different gastric endocrine cell type) did not change with capsaicin. Gastric capsaicin-sensitive afferents are rich in calcitonin gene-related peptide, and in rats with antibodies to this peptide there was reduced corpus somatostatin mRNA. Moreover, infusion of calcitonin gene-related peptide in control rats produced a significant increase in somatostatin mRNA in the gastric corpus. The results indicate that somatostatin mRNA abundance is controlled by the gastric luminal contents and the extrinsic afferent innervation, but the relative importance of these factors differs in antrum and corpus: luminal contents are relatively more important in antrum and primary afferents using calcitonin gene-related peptide in the corpus.
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- Beglinger C., Born W., Hildebrand P., Ensinck J. W., Burkhardt F., Fischer J. A., Gyr K. Calcitonin gene-related peptides I and II and calcitonin: distinct effects on gastric acid secretion in humans. Gastroenterology. 1988 Oct;95(4):958–965. doi: 10.1016/0016-5085(88)90169-2. [DOI] [PubMed] [Google Scholar]
- Brand S. J., Stone D. Reciprocal regulation of antral gastrin and somatostatin gene expression by omeprazole-induced achlorhydria. J Clin Invest. 1988 Sep;82(3):1059–1066. doi: 10.1172/JCI113662. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bunnett N. W., Helton W. S., Debas H. T., Ensinck J. W. CGRP stimulates the release of pro-somatostatin-derived peptides from the gastric fundus. Am J Physiol. 1990 Feb;258(2 Pt 1):G316–G319. doi: 10.1152/ajpgi.1990.258.2.G316. [DOI] [PubMed] [Google Scholar]
- Chiba T., Taminato T., Kadowaki S., Abe H., Chihara K., Seino Y., Matsukura S., Fujita T. Effects of glucagon, secretin, and vasoactive intestinal polypeptide on gastric somatostatin and gastrin release from isolated perfused rat stomach. Gastroenterology. 1980 Jul;79(1):67–71. [PubMed] [Google Scholar]
- Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
- Dimaline R., Evans D., Varro A., Dockray G. J. Reversal by omeprazole of the depression of gastrin cell function by fasting in the rat. J Physiol. 1991 Feb;433:483–493. doi: 10.1113/jphysiol.1991.sp018439. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dimaline R., Sandvik A. K. Histidine decarboxylase gene expression in rat fundus is regulated by gastrin. FEBS Lett. 1991 Apr 9;281(1-2):20–22. doi: 10.1016/0014-5793(91)80348-7. [DOI] [PubMed] [Google Scholar]
- Dockray G. J., Best L., Taylor I. L. Immunochemical characterization of gastrin in pancreatic islets of normal and genetically obese mice. J Endocrinol. 1977 Feb;72(2):143–151. doi: 10.1677/joe.0.0720143. [DOI] [PubMed] [Google Scholar]
- Dunning B. E., Taborsky G. J., Jr Calcitonin gene-related peptide: a potent and selective stimulator of gastrointestinal somatostatin secretion. Endocrinology. 1987 May;120(5):1774–1781. doi: 10.1210/endo-120-5-1774. [DOI] [PubMed] [Google Scholar]
- Forster E. R., Dockray G. J. Immunoneutralization suggests that calcitonin gene related peptide regulates gastric emptying in the rat. Neurosci Lett. 1991 Sep 30;131(1):5–7. doi: 10.1016/0304-3940(91)90324-m. [DOI] [PubMed] [Google Scholar]
- Forster E. R., Dockray G. J. The role of calcitonin gene-related peptide in gastric mucosal protection in the rat. Exp Physiol. 1991 Jul;76(4):623–626. doi: 10.1113/expphysiol.1991.sp003532. [DOI] [PubMed] [Google Scholar]
- Gibbins I. L., Furness J. B., Costa M., MacIntyre I., Hillyard C. J., Girgis S. Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs. Neurosci Lett. 1985 Jun 12;57(2):125–130. doi: 10.1016/0304-3940(85)90050-3. [DOI] [PubMed] [Google Scholar]
- Goodman R. H., Aron D. C., Roos B. A. Rat pre-prosomatostatin. Structure and processing by microsomal membranes. J Biol Chem. 1983 May 10;258(9):5570–5573. [PubMed] [Google Scholar]
- Green T., Dockray G. J. Characterization of the peptidergic afferent innervation of the stomach in the rat, mouse and guinea-pig. Neuroscience. 1988 Apr;25(1):181–193. doi: 10.1016/0306-4522(88)90017-6. [DOI] [PubMed] [Google Scholar]
- Gulbenkian S., Merighi A., Wharton J., Varndell I. M., Polak J. M. Ultrastructural evidence for the coexistence of calcitonin gene-related peptide and substance P in secretory vesicles of peripheral nerves in the guinea pig. J Neurocytol. 1986 Aug;15(4):535–542. doi: 10.1007/BF01611735. [DOI] [PubMed] [Google Scholar]
- Helton W. S., Mulholland M. M., Bunnett N. W., Debas H. T. Inhibition of gastric and pancreatic secretion in dogs by CGRP: role of somatostatin. Am J Physiol. 1989 Apr;256(4 Pt 1):G715–G720. doi: 10.1152/ajpgi.1989.256.4.G715. [DOI] [PubMed] [Google Scholar]
- Holst J. J., Jensen S. L., Knuhtsen S., Nielsen O. V., Rehfeld J. F. Effect of vagus, gastric inhibitory polypeptide, and HCl on gastrin and somatostatin release from perfused pig antrum. Am J Physiol. 1983 May;244(5):G515–G522. doi: 10.1152/ajpgi.1983.244.5.G515. [DOI] [PubMed] [Google Scholar]
- Holzer P., Peskar B. M., Peskar B. A., Amann R. Release of calcitonin gene-related peptide induced by capsaicin in the vascularly perfused rat stomach. Neurosci Lett. 1990 Jan 1;108(1-2):195–200. doi: 10.1016/0304-3940(90)90730-w. [DOI] [PubMed] [Google Scholar]
- Inui T., Kinoshita Y., Yamaguchi A., Yamatani T., Chiba T. Linkage between capsaicin-stimulated calcitonin gene-related peptide and somatostatin release in rat stomach. Am J Physiol. 1991 Nov;261(5 Pt 1):G770–G774. doi: 10.1152/ajpgi.1991.261.5.G770. [DOI] [PubMed] [Google Scholar]
- Karnik P. S., Wolfe M. M. Somatostatin stimulates gastrin mRNA turnover in dog antral mucosa. J Biol Chem. 1990 Feb 15;265(5):2550–2555. [PubMed] [Google Scholar]
- Lee Y., Kawai Y., Shiosaka S., Takami K., Kiyama H., Hillyard C. J., Girgis S., MacIntyre I., Emson P. C., Tohyama M. Coexistence of calcitonin gene-related peptide and substance P-like peptide in single cells of the trigeminal ganglion of the rat: immunohistochemical analysis. Brain Res. 1985 Mar 18;330(1):194–196. doi: 10.1016/0006-8993(85)90027-7. [DOI] [PubMed] [Google Scholar]
- Montminy M. R., Goodman R. H., Horovitch S. J., Habener J. F. Primary structure of the gene encoding rat preprosomatostatin. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3337–3340. doi: 10.1073/pnas.81.11.3337. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mulderry P. K., Ghatei M. A., Spokes R. A., Jones P. M., Pierson A. M., Hamid Q. A., Kanse S., Amara S. G., Burrin J. M., Legon S. Differential expression of alpha-CGRP and beta-CGRP by primary sensory neurons and enteric autonomic neurons of the rat. Neuroscience. 1988 Apr;25(1):195–205. doi: 10.1016/0306-4522(88)90018-8. [DOI] [PubMed] [Google Scholar]
- Pappas T., Debas H. T., Walsh J. H., Rivier J., Taché Y. Calcitonin gene-related peptide-induced selective inhibition of gastric acid secretion in dogs. Am J Physiol. 1986 Jan;250(1 Pt 1):G127–G133. doi: 10.1152/ajpgi.1986.250.1.G127. [DOI] [PubMed] [Google Scholar]
- Pfeiffer C. J., Evangelista S. Gastric and jejunal ultrastructure in capsaicin-treated rats with and without experimental ulcer. Adv Exp Med Biol. 1991;298:85–96. doi: 10.1007/978-1-4899-0744-8_8. [DOI] [PubMed] [Google Scholar]
- Saffouri B., Weir G. C., Bitar K. N., Makhlouf G. M. Gastrin and somatostatin secretion by perfused rat stomach: functional linkage of antral peptides. Am J Physiol. 1980 Jun;238(6):G495–G501. doi: 10.1152/ajpgi.1980.238.6.G495. [DOI] [PubMed] [Google Scholar]
- Schubert M. L., Edwards N. F., Arimura A., Makhlouf G. M. Paracrine regulation of gastric acid secretion by fundic somatostatin. Am J Physiol. 1987 Apr;252(4 Pt 1):G485–G490. doi: 10.1152/ajpgi.1987.252.4.G485. [DOI] [PubMed] [Google Scholar]
- Short G. M., Doyle J. W., Wolfe M. M. Effect of antibodies to somatostatin on acid secretion and gastrin release by the isolated perfused rat stomach. Gastroenterology. 1985 Apr;88(4):984–988. doi: 10.1016/s0016-5085(85)80018-4. [DOI] [PubMed] [Google Scholar]
- Soll A. H., Yamada T., Park J., Thomas L. P. Release of somatostatinlike immunoreactivity from canine fundic mucosal cells in primary culture. Am J Physiol. 1984 Nov;247(5 Pt 1):G558–G566. doi: 10.1152/ajpgi.1984.247.5.G558. [DOI] [PubMed] [Google Scholar]
- Sternini C., Reeve J. R., Jr, Brecha N. Distribution and characterization of calcitonin gene-related peptide immunoreactivity in the digestive system of normal and capsaicin-treated rats. Gastroenterology. 1987 Oct;93(4):852–862. doi: 10.1016/0016-5085(87)90450-1. [DOI] [PubMed] [Google Scholar]
- Su H. C., Bishop A. E., Power R. F., Hamada Y., Polak J. M. Dual intrinsic and extrinsic origins of CGRP- and NPY-immunoreactive nerves of rat gut and pancreas. J Neurosci. 1987 Sep;7(9):2674–2687. doi: 10.1523/JNEUROSCI.07-09-02674.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Taché Y., Pappas T., Lauffenburger M., Goto Y., Walsh J. H., Debas H. Calcitonin gene-related peptide: potent peripheral inhibitor of gastric acid secretion in rats and dogs. Gastroenterology. 1984 Aug;87(2):344–349. [PubMed] [Google Scholar]
- Varro A., Green T., Holmes S., Dockray G. J. Calcitonin gene-related peptide in visceral afferent nerve fibres: quantification by radioimmunoassay and determination of axonal transport rates. Neuroscience. 1988 Sep;26(3):927–932. doi: 10.1016/0306-4522(88)90109-1. [DOI] [PubMed] [Google Scholar]
- Walsh J. H. Peptides as regulators of gastric acid secretion. Annu Rev Physiol. 1988;50:41–63. doi: 10.1146/annurev.ph.50.030188.000353. [DOI] [PubMed] [Google Scholar]
- Walsh J. H., Richardson C. T., Fordtran J. S. pH dependence of acid secretion and gastrin release in normal and ulcer subjects. J Clin Invest. 1975 Mar;55(3):462–468. doi: 10.1172/JCI107952. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wiesenfeld-Hallin Z., Hökfelt T., Lundberg J. M., Forssmann W. G., Reinecke M., Tschopp F. A., Fischer J. A. Immunoreactive calcitonin gene-related peptide and substance P coexist in sensory neurons to the spinal cord and interact in spinal behavioral responses of the rat. Neurosci Lett. 1984 Nov 23;52(1-2):199–204. doi: 10.1016/0304-3940(84)90374-4. [DOI] [PubMed] [Google Scholar]
- Wu S. V., Giraud A., Mogard M., Sumii K., Walsh J. H. Effects of inhibition of gastric secretion on antral gastrin and somatostatin gene expression in rats. Am J Physiol. 1990 May;258(5 Pt 1):G788–G793. doi: 10.1152/ajpgi.1990.258.5.G788. [DOI] [PubMed] [Google Scholar]
- Wu S. V., Sumii K., Tari A., Mogard M., Walsh J. H. Regulation of gastric somatostatin gene expression. Metabolism. 1990 Sep;39(9 Suppl 2):125–130. doi: 10.1016/0026-0495(90)90229-6. [DOI] [PubMed] [Google Scholar]
- Yamada T., Soll A. H., Park J., Elashoff J. Autonomic regulation of somatostatin release: studies with primary cultures of canine fundic mucosal cells. Am J Physiol. 1984 Nov;247(5 Pt 1):G567–G573. doi: 10.1152/ajpgi.1984.247.5.G567. [DOI] [PubMed] [Google Scholar]