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Stephen J. Hersey
10.1002/cphy.cp060314
Source: Supplement 18: Handbook of Physiology, The Gastrointestinal System, Salivary, Gastric, Pancreatic, and Hepatobiliary Secretion
Originally published: 1989
Published online: January 2011
Full Article on Wiley Online Library
The sections in this article are:
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Figure 1. Model for basic features of pepsinogen secretion by gastric chief cells. Major events include synthesis of pepsinogen (Pg) by endoplasmic reticulum, storage in secretory granules, and release of pepsinogen through apical surface on stimulation of cell. Released pepsinogen is converted to active pepsin in presence of acid. |
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Figure 2. Cholinergic stimulation of both acid and pepsinogen secretions are mediated by M‐2‐subtype receptor. Secretions of acid and pepsinogen by gastric glands are inhibited more potently by atropine (Atr) (nonselective) than by M‐1‐selective antagonist pirenzepine (Pz). Acid and pepsinogen secretions were stimulated by carbachol. Acid secretion was measured by accumulation of aminopyrine and pepsinogen secretion as percent of total released. |
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Figure 3. Adrenergic stimulation of pepsinogen secretion occurs through β2‐adrenoceptor. Stimulation of pepsinogen secretion by isoproterenol in gastric glands is antagonized with a potency sequence of propranolol (nonselective) > ICI 118551 (β2‐selective) > > betaxolol (β1‐selective). |
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Figure 4. Selective stimulation of acid and pepsinogen secretions by gastric glands. Isoproterenol (IPR) stimulates pepsinogen release (left) but not acid formation (right). In contrast, histamine (HIST) stimulates acid but not pepsinogen secretion. Pepsinogen secretion was measured as percent of total released, and acid secretion was measured as accumulation ratio of aminopyrine (AP). Selective action indicates independent regulation of the 2 secretory processes. |
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Figure 5. Pepsinogen secretion by gastric glands shows selectivity for cholecystokinin (CCK) over peptide analogues. Potency sequence is CCK‐8‐S (sulfated) > > gastrin 7 (sulfated) (G‐7‐S) = CCK‐8‐des (desulfated) > > G‐7‐des (desulfated). Sequence indicates receptor specificity for both sulfation of tyrosine residue and position of tyrosine residue. |
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Figure 6. Selective inhibition of peptide stimulation by asperlicin. Asperlicin inhibits pepsinogen secretion stimulated by either CCK‐8 or gastrin (left) but does not inhibit peptide‐stimulated acid secretion (right). Both pepsinogen secretion and acid secretion (aminopyrine accumulation) are expressed as percent of control (C). Selective inhibition indicates that acid and pepsinogen secretions are mediated by distinct receptor types. |
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Figure 7. Proposed model for cellular events in pepsinogen secretion by gastric chief cells. Adrenergic agonists and secretin bind to cell membrane receptors that are coupled to adenylate cyclase (AC). Subsequent increase in cAMP activates a protein kinase (PK‐A). Cholinergic agonists and CCK‐type peptides produce receptor‐mediated activation of phospholipase C (PL‐C). Phospholipase generates intracellular inositol phosphates (IP) that lead to release of Ca from intracellular stores. PL‐C also generates diacylglycerol (DAG), which activates second protein kinase (PK‐C). Activities of protein kinases and Ca result in secretion of pepsinogen by compound exocytotic process. Identifying mechanisms by which intracellular mediators activate exocytosis remains major challenge. |
| References | |
| 1. | Andreeva, N. S. Structure of pepsin. Mol. Biol. 19: 185–190, 1985. |
| 2. | Andreeva, N. S., A. E. Gustchina, A. A. Fedorov, N. E. Shutzkever, and T. V. Volnova. X‐ray crystallographic studies of pepsin. Adv. Exp Med. Biol. 95: 3–22, 1976. |
| 3. | Anson, M. L., and A. E. Mirsky. The estimation of pepsin with hemoglobin. J. Gen. Physiol. 16: 59–63, 1932. |
| 4. | Barros, D., S. R. Bloom, and J. H. Baron. Inhibition by somatostatin (growth hormone release‐inhibiting hormone, GH‐RIH) of gastric acid and pepsin and G cell release of gastrin. Gut 19: 315–320, 1978. |
| 5. | Berger, S., and J.‐P. Raufman. Prostaglandin‐induced pepsinogen secretion from dispersed gastric glands from guinea pig stomach. Am. J. Physiol. 249 (Gastrointest. Liver Physiol. 12): G592–G598, 1985. |
| 6. | Berger, W., G. Dohl, and H. P. Meissner. Structural and functional alterations in fused membranes of secretory granules during exocytosis in pancreatic islet cells of the mouse. Cytobiologie 12: 119–139, 1975. |
| 7. | Berglindh, T., and K. J. Obrink. A method for preparing isolated glands from the rabbit gastric mucosa. Acta Physiol. Scand. 96: 150–159, 1976. |
| 8. | Berquist, E., and K. J. Obrink. Gastrin‐histamine as a normal sequence in gastric acid stimulation in the rabbit. Upsala J. Med. Sci. 84: 145–154, 1979. |
| 9. | Berstad, A., and H. Petersen. Dose‐response relationship of the effect of secretin on acid and pepsin secretion in man. Scand. J. Gastroenterol. 5: 647–654, 1970. |
| 10. | Bilinski, M., H. Plattner, and H. Matt. Secretory protein decondensation as a distinct Ca mediated event during the final steps of exocytosis in paramecium cells. J. Cell Biol. 88: 179–188, 1981. |
| 11. | Bilski, A. J., S. E. Halliday, J. D. Fitzgerald, and J. L. Wale. The pharmacology of a β2‐selective adrenoceptor antagonist (ICI 118,551). J. Cardiovasc. Pharmacol. 5: 430–437, 1983. |
| 12. | Bojamic, D., J. D. Jansen, S. R. Nahyorski, and J. Zaagsma. Atypical characteristic of the β‐adrenoceptor mediating cyclic AMP generation and lipolysis in the rat adipocyte. Br. J. Pharmacol. 84: 131–137, 1985. |
| 13. | Bondot, J. P., I. Cavero, S. Fenard, F. Lefevre‐Borg, P. Manoury, and A. G. Roach. Preliminary studies on SL75212, a new potent cardioselective β‐adrenoceptor antagonist. Br. J. Pharmacol. 66: 445P, 1979. |
| 14. | Braganza, J. M., H. T. Howat, and G. H. Kay. A comparison of the pepsin stimulating effects of secretin preparations. J. Physiol. Lond. 258: 63–72, 1976. |
| 15. | Busa, W. B., and R. Nuccitelli. Metabolic regulation via intracellular pH. Am. J. Physiol. 246 (Regulatory Integrative Comp. Physiol. 15): R409–R438, 1984. |
| 16. | Castagna, M., Y. Takai, K. Kaibuchi, K. Sano, J. Kikkawa, and Y. Nishizuka. Direct activation of calcium‐activated, phospholipid‐dependent protein kinase by tumor promoting phorbol esters. J. Biol. Chem. 257: 7847–7851, 1982. |
| 17. | Chang, R. S. L., V. J. Lotti, R. L. Monaghan, J. Birnbaum, E. O. Stapley, M. A. Goetz, G. Albero‐Schonberg, A. A. Patchett, J. M. Liesch, O. D. Hensens, and J. P. Springer. A potent nonpeptide cholecystokinin antagonist selective for peripheral tissues isolated from Aspergillus alliaceus. Science Wash. DC 230: 177–179, 1985. |
| 18. | Cherner, J. A., V. E. Sutliff, D. M. Grybowski, R. T. Jensen, and J. D. Garner. Functionally distinct receptors for cholecystokinin and gastrin on dispersed chief cells from guinea pig stomach. Am. J. Physiol. 254 (Gastrointest. Liver Physiol. 17): G151–G155, 1988. |
| 19. | Chew, C. S., and M. R. Brown. Release of intracellular Ca and elevation of inositol trisphosphate by secretagogues in parietal and chief cells isolated from rabbit gastric mucosa. Biochim. Biophys. Acta 888: 116–125, 1986. |
| 20. | Chew, C. S., and S. J. Hersey. Gastrin stimulation of isolated gastric glands. Am. J. Physiol. 242 (Gastrointest. Liver Physiol. 5): G504–G512, 1982. |
| 21. | Cohen, F. S., J. Zimmerberg, and A. Finkelstein. Fusion of phospholipid vesicles with planar phospholipid bilayers. II. Incorporation of a vesicular membrane marker into the planar membrane. J. Gen. Physiol. 75: 251–270, 1980. |
| 22. | Feldman, E. J., and M. I. Grossman. Liver extract and its free amino acids equally stimulate gastric acid secretion. Am. J. Physiol. 239 (Gastrointest. Liver Physiol. 2): G493–G496, 1980. |
| 23. | Fimmel, C. J., M. M. Berger, and A. L. Blum. Dissociated response of acid and pepsin secretion to omeprazole in an in vitro perfused mouse stomach. Am. J. Physiol. 247 (Gastrointest. Liver Physiol. 10): G240–G247, 1984. |
| 24. | Foltman, B., and V. B. Pedersen. Comparison of primary structures of acid proteases and their zymogens. Adv. Exp. Med. Biol. 95: 3–22, 1976. |
| 25. | Friedman, M. H. Oesophageal and gastric secretion in the frog. J. Cell Comp. Physiol. 10: 37–50, 1937. |
| 26. | Fruton, J. S. The mechanism of the catalytic action of pepsin and related acid proteinases. Adv. Enzymol. 44: 1–36, 1976. |
| 27. | Gespach, C., D. Bataille, C. Dupont, G. Rosselin, E. Wunch, and E. Jaeger. Evidence for a cyclic AMP system highly sensitive to secretin in gastric glands isolated from the rat fundus and antrum. Biochim. Biophys. Acta 630: 433–441, 1980. |
| 28. | Gibert, A. J., and S. J. Hersey. Exocytosis in isolated gastric glands induced by secretagogues and hyperosmolarity. Cell Tissue Res. 227: 535–542, 1982. |
| 29. | Gibert, A. J., and S. J. Hersey. Effect of ouabain and furosemide on pepsinogen secretion by gastric glands in vitro. J. Cell Physiol. 119: 220–226, 1984. |
| 30. | Gibson, R., B. I. Hirschowitz, and G. Hutchison. Actions of metiamide, an H2‐histamine receptor antagonist, on gastric H+ and pepsin secretion in dogs. Gastroenterology 67: 93–99, 1977. |
| 31. | Gregory, R. A., and H. J. Tracey. The constitution and properties of two gastrins extracted from hog antral mucosa. Gut 5: 103–117, 1964. |
| 32. | Hammer, R., and A. Giachetti. Muscarinic receptor subtypes: M1 and M2. Biochemical and functional characterization. Life Sci. 31: 2991–2998, 1982. |
| 33. | Harden, T. K., L. I. Tanner, M. W. Martin, N. Nakahata, A. R. Hughes, J. R. Hepler, T. Evans, S. B. Masters, and J. H. Brown. Characteristics of two biochemical responses to stimulation of muscarinic cholinergic receptors. Trends Pharmacol. Sci. 247, Suppl.: 14–18, 1986. |
| 34. | Helander, H. F. Quantitative ultrastructural studies on rat gastric zymogen cells under different physiological and experimental conditions. Cell Tissue Res. 189: 287–303, 1965. |
| 35. | Helander, H. F. The cells of the gastric mucosa. Int. Rev. Cytol. 70: 217–289, 1981. |
| 36. | Herawi, M., G. Lambrecht, E. Mutschler, U. Moser, and A. Pfieffer. Different binding properties of muscarinic M2‐receptor subtypes for agonists and antagonists in porcine gastric smooth muscle and mucosa. Gastroenterology 94: 630–637, 1988. |
| 37. | Hersey, S. J., D. May, and D. Schyberg. Stimulation of pepsinogen release from isolated gastric glands by cholecys‐tokininlike peptides. Am. J. Physiol. 244 (Gastrointest. Liver Physiol. 7): G192–G197, 1983. |
| 38. | Hersey, S. J., M. Miller, D. May, and S. H. Norris. Lack of interaction between acid and pepsinogen secretion in isolated gastric glands. Am. J. Physiol. 245 (Gastrointest. Liver Physiol. 8): G775–G779, 1983. |
| 39. | Hersey, S. J., A. Owirodu, and M. Miller. Forskolin stimulation of acid and pepsinogen secretion by gastric glands. Biochim. Biophys. Acta 755: 293–299, 1983. |
| 40. | Hirschowitz, B. I. Secretion of pepsinogen. In: Handbook of Physiology. Alimentary Canal. Secretion, edited by C. F. Code. Washington, DC: Am. Physiol. Soc., 1967, vol. II, chapt. 50, p. 889–918. |
| 41. | Hirschowitz, B. I., J. Fong, and E. Molina. Effects of pirenzepine and atropine on vagal and cholinergic gastric secretion and gastrin release and on heart rate in the dog. J. Pharmacol. Exp. Ther. 225: 263–268, 1983. |
| 42. | Hirschowitz, B. I., and R. G. Gibson. Effect of cimetidine on stimulated gastric secretion and serum gastrin in the dog. Am. J. Gastroenterol. 70: 437–447, 1978. |
| 43. | Hirschowitz, B. I., and G. A. Hutchison. Evidence for a histamine H2 receptor that inhibits pepsin secretion in the dog. Am. J. Physiol. 233 (Endocrinol. Metab. Gastrointest. Physiol. 2): E225–E228, 1977. |
| 44. | Hirschowitz, B. I., and G. A. Hutchison. Kinetics of atropine inhibition of pentagastrin‐stimulated H+, electrolyte, and pepsin secretion in the dog. Am. J. Dig. Dis. 22: 99–107, 1977. |
| 45. | Hirschowitz, B. I., and E. Molina. Relation of gastric acid and pepsin secretion to serum gastrin levels in dogs given bombesin and gastrin‐17. Am. J. Physiol. 244 (Gastrointest. Liver Physiol. 7): G546–G551, 1983. |
| 46. | Hirst, B. H., J. M. Conlon, D. H. Coy, J. Holland, and B. Shaw. Comparison of the gastric exocrine inhibitory activities and plasma kinetics of somatostatin‐28 and somatostatin‐14 in cats. Regul. Pept. 4: 227–237, 1982. |
| 47. | Ichihara, Y., K. Sogawa, and K. Takahashi. Rat gastric prepepsinogen: in vitro synthesis and partial amino‐terminal signal sequence. J. Biochem. Tokyo 92: 603–606, 1982. |
| 48. | Johnson, L. R. Regulation of pepsin secretion by topical acid in the stomach. Am. J. Physiol. 223: 847–850, 1972. |
| 49. | Johnson, L. R., G. E. Stenning, and M. I. Grossman. Effect of sulfation on the gastrointestinal actions of caerulein. Gastroenterology 58: 208–216, 1970. |
| 50. | Kageyama, T., and K. Takahashi. Isolation of an activation intermediate and determination of the amino acid sequence of the activation segment of human pepsinogen A. J. Biochem. Tokyo 88: 571–582, 1980. |
| 51. | Kaminski, D. L., M. J. Ruwart, and M. Jellinek. Structure‐function relationships of peptide fragments of gastrin and cholecystokinin. Am. J. Physiol. 233 (Endocrinol. Metab. Gastrointest. Physiol. 2): E286–E292, 1977. |
| 52. | Kasbekar, D. K., R. T. Jensen, and J. D. Gardner. Pepsinogen secretion from dispersed glands from rabbit stomach. Am. J. Physiol. 244 (Gastrointest. Liver Physiol. 7): G392–G396, 1983. |
| 53. | Kay, J., and C. W. Dykes. The first cleavage site in pepsinogen activation. Adv. Exp. Med. Biol. 95: 103–127, 1976. |
| 54. | Koelz, H. R., S. J. Hersey, G. Sachs, and C. S. Chew. Pepsinogen release from isolated gastric glands. Am. J. Physiol. 243 (Gastrointest. Liver Physiol. 6): G218–G225, 1982. |
| 55. | Konturek, S. J., J. Biernat, N. Kwiecien, and J. Oleksy. Effect of glucagon on meal‐induced gastric secretion in man. Gastroenterology 68: 448–454, 1975. |
| 56. | Konturek, S. J., N. Kwiecien, W. Obtulowicz, W. Bielanski, J. Oleksy, and A. V. Schally. Effects of somatostatin‐14 and somatostatin‐28 on plasma hormonal and gastric secretory responses to cephalic and gastrointestinal stimulation in man. Scand. J. Gastroenterol. 20: 31–38, 1985. |
| 57. | Kumar, P. M. H., P. H. Ward, and B. Kassell. Chemical modification of a pepsin inhibitor from the activation peptides of pepsinogen. Adv. Exp. Med. Biol. 95: 211–221, 1976. |
| 58. | Langley, J. N. On the histology and physiology of pepsin‐forming glands. Phil. Trans. R. Soc. Lond. Ser. B 172: 664–711, 1881. |
| 59. | Langley, J. N., and J. S. Edkins. Pepsinogen and pepsin. J. Physiol. Lond. 7: 371–415, 1886. |
| 60. | Lichtenberger, L. M. Importance of food in the regulation of gastrin release and formation. Am. J. Physiol. 243 (Gastrointest. Liver Physiol. 6): G429–G441, 1982. |
| 61. | Magous, R., B. Baudiere, and J.‐P. Balie. Muscarinic receptors in isolated gastric fundic mucosal cells. Biochem. Pharmacol. 34: 2269–2274, 1985. |
| 62. | Marciniszyn, J., J. S. Huang, J. A. Hartsuck, and J. Tang. Mechanisms of intramolecular activation of pepsinogen. J. Biol. Chem. 251: 7095–7102, 1976. |
| 63. | Matsumoto, H., K. Komiyama, T. Shirakawa, A. Heldman, W. Anderson, and B. I. Hirschowitz. Stimuli of pepsinogen secretion from frog isolated peptic cells. Federation Proc. 45: 1043, 1986. |
| 64. | Muller‐Lissner, S. A., I. Szelenyi, H. Engler, and A. L. Blum. Pirenzepine inhibits acid and pepsinogen secretion by the isolated perfused mouse stomach. Scand. J. Gastroenterol. Suppl. 72: 101–103, 1982. |
| 65. | Nakajima, S., and D. F. Magee. Influences of duodenal acidification on acid and pepsin secretion of the stomach in dogs. Am. J. Physiol. 218: 545–549, 1970. |
| 66. | Norris, S. H., and S. J. Hersey. Inhibition of pepsinogen secretion in isolated gastric glands by amphotericin B is secretagogue specific. Can. J. Physiol. Pharmacol. 62: 1518–1524, 1984. |
| 67. | Norris, S. H., and S. J. Hersey. Stimulation of pepsinogen secretion in permeable isolated gastric glands. Am. J. Physiol. 249 (Gastrointest. Liver Physiol. 12): G408–G415, 1985. |
| 68. | Pace, C. S., and G. Sachs. Glucose induced proton uptake in secretory granules of B‐cells in monolayer culture. Am. J. Physiol. 242 (Cell Physiol. 11): C382–C387, 1982. |
| 69. | Pagani, F., A. Schiavone, E. Monferini, R. Hammer, and A. Giachetti. Distinct muscarinic receptor subtypes (M1 and M2) controlling acid secretion in rodents. Trends Pharmacol. Sci. 5, Suppl.: 66–68, 1984. |
| 70. | Peerce, B. E., A. Smolka, and G. Sachs. Isolation of pepsinogen granules from rabbit gastric mucosa. J. Biol. Chem. 259: 9255–9262, 1984. |
| 71. | Peikin, S. R., C. L. Costenbader, and J. D. Gardner. Actions of derivatives of cyclic nucleotides on dispersed acini from guinea pig pancreas: discovery of a competitive antagonist of the action of cholecystokinin. J. Biol. Chem. 254: 5321–5327, 1979. |
| 72. | Pohl, J., M. Baudys, and V. Kostka. Chromophoric peptide substrates for activity determination of animal aspartic proteinases in the presence of their zymogens: a novel assay. Anal. Biochem. 133: 104–109, 1983. |
| 73. | Pollard, H. B., C. J. Pazoles, C. E. Crentz, and O. Sinder. The chromaffin granule and possible mechanisms of exocytosis. Int. Rev. Cytol. 58: 159–197, 1979. |
| 74. | Praissman, M., M. E. Walden, and C. Pellecchia. Identification and characterization of a specific receptor for cholecystokinin on isolated fundic glands from guinea pig gastric mucosa using a biologically active 125I‐CCK‐8 probe. J. Receptor Res. 3: 647–665, 1983. |
| 75. | Raufman, J.‐P., D. K. Kasbekar, R. T. Jensen, and J. D. Gardner. Potentiation of pepsinogen secretion from dispersed glands from rat stomach. Am. J. Physiol. 245 (Gastrointest. Liver Physiol. 8): G525–G530, 1983. |
| 76. | Raufman, J.‐P., V. E. Sutliff, D. K. Kasbekar, R. T. Jensen, and J. D. Gardner. Pepsinogen secretion from dispersed chief cells from guinea pig stomach. Am. J. Physiol. 247 (Gastrointest. Liver Physiol. 10): G95–G104, 1984. |
| 77. | Rehfeld, J. F. Four basic characteristics of gastrin‐cholecys‐tokinin system. Am. J. Physiol. 240 (Gastrointest. Liver Physiol. 3): G255–G266, 1981. |
| 78. | Reimann, E. M., D. A. Walsh, and E. G. Krebs. Purification and properties of rabbit skeletal muscle adenosine 3',5'‐mon‐ophosphate‐dependent protein kinase. J. Biol. Chem. 246: 1986–1995, 1971. |
| 79. | Sakamoto, C., T. Matozaki, M. Nagao, and S. Baba. Combined effect of phorboester and A23187 or dibutyryl cyclic AMP on pepsinogen secretion from isolated gastric glands. Biochem. Biophys. Res. Commun. 131: 319–324, 1985. |
| 80. | Samloff, I. M. Slow moving protease and the seven pepsinogens. Electrophoretic demonstration of the existence of eight proteolytic fractions in human gastric mucosa. Gastroenterology 57: 659–669, 1966. |
| 81. | Samloff, I. M. Pepsinogens, pepsins, and pepsin inhibitors. Gastroenterology 60: 586–604, 1971. |
| 82. | Samloff, I. M. Cellular localization of group I pepsinogens in human gastric mucosa by immunofluorescence. Gastroenterology 61: 185–188, 1971. |
| 83. | Samloff, I. M. Pepsinogens I and II: purification from gastric mucosa and radioimmunoassay in serum. Gastroenterology 82: 26–33, 1982. |
| 84. | Samloff, I. M., and W. M. Liebman. Cellular localization of the group II pepsinogens in human stomach and duodenum. Gastroenterology 65: 36–42, 1973. |
| 85. | Samloff, I. M., and W. M. Liebman. Radioimmunoassay of group I pepsinogens in serum. Gastroenterology 66: 494–502, 1984. |
| 86. | Sanders, M. J., D. A. Amirian, A. Ayalon, and A. H. Soll. Regulation of pepsinogen release from canine chief cells in primary monolayer culture. Am. J. Physiol. 245 (Gastrointest. Liver Physiol. 8): G641–G646, 1983. |
| 87. | Sankaran, H., I. D. Goldfine, C. W. Deveney, K.‐Y. Wong, and J. A. Williams. Binding of cholecystokinin to high affinity receptors on isolated rat pancreatic acini. J. Biol. Chem. 255: 1849–1853, 1980. |
| 88. | Schafer, D. E., and G. N. Garshfield. Cholera enterotoxin stimulates marked pepsinogen secretion by isolated gastric fundic glands. Federation Proc. 41: 1432, 1982. |
| 89. | Schuurmans Stekhoven, F., and S. L. Bonting. Transport adenosine triphosphatases: properties and functions. Physiol. Rev. 61: 1–76, 1981. |
| 90. | Schwann, T. L. Ueber das wesen des verdauungsprozessen. Poggendorf Ann. Phys. Chem. 38: 358–364, 1836. |
| 91. | Seijffers, M. J., M. D. Turner, L. L. Miller, and H. L. Segal. Human pepsinogens and pepsins. Gastroenterology 48: 122–125, 1965. |
| 92. | Sherman, O., and J. P. Henry. Role of the proton electrochemical gradient monoamine transport by bovine chromaffin granules. Biochim. Biophys. Acta 601: 64–677, 1980. |
| 93. | Shirakawa, T., and B. I. Hirschowitz. Bombesin‐induced pepsinogen secretion from frog esophagus peptic glands in vitro. Gastroenterology 86: 1250, 1984. |
| 94. | Shugerman, R. P., B. I. Hirschowitz, A. S. Bhown, R. E. Schrohenloher, and J. G. Spenney. A unique “mini” pepsinogen isolated from bullfrog esophageal glands. J. Biol. Chem. 257: 795–798, 1982. |
| 95. | Simpson, L., D. Goldenberg, and B. I. Hirschowitz. Pepsinogen secretion by the frog esophagus in vitro. Am. J. Physiol. 238 (Gastrointest. Liver Physiol. 1): G79–G84, 1980. |
| 96. | Singer, M. V., W. Niebel, C. Lamers, S. Becker, J. Vesper, W. Hartmann, J. Diemel, and H. Goebell. Effects of truncal vagotomy and antrectomy on bombesin‐stimulated pancreatic secretion, release of gastrin, and pancreatic polypeptide in the anesthetized dog. Dig. Dis. Sci. 26: 871–877, 1981. |
| 97. | Skouho‐Kristensen, E., and J. Fryklund. Adrenergic stimulation of pepsinogen release from rabbit isolated gastric glands. Naunyn‐Schmeideberg's Arch. Pharmacol. 330: 37–41, 1985. |
| 98. | Sogawa, K., Y. Fujii‐Kuriyama, Y. Mizukami, Y. Ischihara, and K. Takahashi. Primary structure of human pepsinogen gene. J. Biol. Chem. 258: 5306–5311, 1983. |
| 99. | Sogawa, K., Y. Ichihara, Y. Takahashi, Y. Fujii‐Kuriyama, and M. Muramatsu. Molecular cloning of complementary DNA to swine pepsinogen mRNA. J. Biol. Chem. 256: 12561–12565, 1981. |
| 100. | Soll, A. H., D. A. Amirian, L. P. Thomas, T. J. Reedy, and J. D. Elashoff. Gastrin receptors on isolated canine parietal cells. J. Clin. Invest. 73: 1434–1447, 1984. |
| 101. | Soumaron, A., A. M. Cheret, and M. J. M. Lewin. Localization of gastrin receptors in intact isolated and separated rat fundic cells. Gastroenterology 73: 900–903, 1977. |
| 102. | Stening, G. F., L. R. Johnson, and M. I. Grossman. Effect of secretin on acid and pepsin secretion in cat and dog. Gastroenterology 56: 468–475, 1969. |
| 103. | Streb, H., E. Bayerdorffer, W. Haase, R. F. Irvine, and I. Schulz. Effect of inositol‐1,4,5‐triphosphate on isolated subcellular fractions of rat pancreas. J. Membr. Biol. 81: 241–253, 1984. |
| 104. | Streb, H., R. F. Irvine, M. J. Berridge, and I. Schulz. Release of Ca from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol‐1,4,5‐trisphosphate. Nature Lond. 306: 67–69, 1983. |
| 105. | Sutton, D. R., and R. M. Donaldson. Synthesis and secretion of protein and pepsinogen by rabbit gastric mucosa in organ culture. Gastroenterology 69: 166–174, 1975. |
| 106. | Taggart, R. T., T. K. Mohandas, T. B. Shows, and I. B. Graeme. Variable numbers of pepsinogen genes are located in the centromeric region of human chromosome 11 and determine the high‐frequency electrophoretic polymorphism. Proc. Natl. Acad. Sci. USA 82: 6240–6244, 1985. |
| 107. | Takeuchi, K., G. R. Speir, and L. R. Johnson. Mucosal gastrin receptor. I. Assay standardization and fulfillment of receptor criteria. Am. J. Physiol. 237 (Endocrinol. Metab. Gastrointest. Physiol. 6): E284–E294, 1979. |
| 108. | Takeuchi, K., G. R. Speir, and L. R. Johnson. Mucosal gastrin receptor. IV. Binding specificity. Am. J. Physiol. 239 (Gastrointest. Liver Physiol. 2): G395–G399, 1980. |
| 109. | Tang, J. (editor). Advances in Experimental Medicine and Biology. Acid Proteases. New York: Plenum, 1976, vol. 95. |
| 110. | Tang, J. Evolution in the structure and function of carboxyl proteases. Mol. Cell. Biochem. 26: 93–109, 1979. |
| 111. | Vagne, M., C. Roche, J. A. Chayvialle, and C. Gespach. Effect of somatostatin on the secretin‐induced gastric secretions of pepsin and mucus in cats. Regul. Pept. 3: 183–191, 1982. |
| 112. | Vatier, M. M., A. M. Cheret, and S. Bonfils. Le dosage automatique de l'activite proteolytique du suc gastrique. Biol. Gastro‐Enterol. 1: 15–29, 1968. |
| 113. | Williamson, J. R., R. H. Cooper, S. K. Joseph, and A. P. Thomas. Inositol triphosphate and diacylglycerol as intracellular second messengers in liver. Am. J. Physiol. 248 (Cell Physiol. 19): C203–C216, 1985. |
| 114. | Wolf, J., D. Londos, and D. M. F. Cooper. Adenosine receptors and the regulation of adenylate cyclase. Adv. Cyclic Nucleotide Res. 14: 199–214, 1981. |
| 115. | Wollin, A., A. H. Soll, and I. M. Samloff. Actions of histamine, secretin and PGE2 on cyclic AMP production by isolated canine fundic mucosal cells. Am. J. Physiol. 237 (Endocrinol. Metab. Gastrointest. Physiol. 6): E437–E443, 1979. |
| 116. | Zimmerberg, J., F. S. Cohen, and A. Finkelstein. Fusion of phospholipid vesicles with planar phospholipid bilayer membranes. I. Discharge of vesicular contents across the planar membrane. J. Gen. Physiol. 75: 241–250, 1980. |
