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Gastric cytoprotection 30 years after its discovery by André Robert: a personal perspective

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Abstract

It is generally accepted that the development of gastric mucosal injury and protection is a consequence of an imbalance between the existing aggressive and defensive factors in the gastric mucosa. The excess secretion of gastric acid and increased production of pepsin have been considered as the main etiological factors in the development of peptic ulcer diseases in humans. André Robert and his coworkers (Kalamazoo, Michigan, USA) identified a new pathway for the gastric mucosal protection against the gastric mucosal damage injury (e.g. from HCl, NaOH, NaCl, ethanol, or thermal injury) by small doses of prostaglandins (1–5 μg/kg given ig or sc), without presence of any gastric acid secretory properties in rats. This phenomenon was termed “gastric cytoprotection” (1979). The results of this basic research offered a lot of new possibilities to test this hypothesis in different experimental models under different experimental conditions, in both human healthy subjects as well as in patients with various gastrointestinal disorders (acute and chronic gastrointestinal inflammatory conditions in the stomach and intestines, as well as GI precancerous states, i.e., oesophageal, stomach, pancreatic, liver and colon cancers). An international symposium on “gastric cytoprotection: 30 years after André Robert’s concept” was organized at Split (Croatia) on September 13, 2009, at which invited experts from China, Croatia, Italy, Japan, Poland, and USA gave presentations and discussed the studies performed in the field of cytoprotection between 1979 and 2009. This paper provides a short critical summary of this meeting in the context of an “official historic background” of the events underlying the discovery of “gastric cytoprotection” which originated from the pioneering work of André Robert.

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Acknowledgments

The author wishes to express his sincere thanks to Professor K.D.Rainsford (Shefield University, U.K.) for his valuable help and criticism in the preparation of this paper. The author expresses his thanks to Viktoria Vas (First Department of Medicine, University of Pécs, Hungary) for the preparation of the manuscript and the references.

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  1. Medical and Health Centre, First Department of Medicine, University of Pécs, Ifjúság u. 13., 7624, Pécs, Hungary

    Gyula Mózsik

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  1. Gyula Mózsik
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Correspondence to Gyula Mózsik.

Appendix 1: publications by André Robert on prostaglandins and early work on experimental ulcer formation and therapy

Appendix 1: publications by André Robert on prostaglandins and early work on experimental ulcer formation and therapy

Cytoprotection papers

Robert A, Leung FW, Guth PH (1992) Morphological and functional gastric cytoprotection by prostaglandin in rats receiving absolute ethanol orally. Gut 33(4):444–451. [This paper appeared after André Robert passed away].

Robert A, Saperas E, Zhang WR, Olafsson AS, Lancaster C, Tracey DE, Chosay JG, Taché Y (1991). Gastric cytoprotection by intracisternal interleukin-1 beta in the rat. Biochem Biophys Res Commun 174(3):1117–1124.

Robert A, Olafsson AS, Lancaster C, Zhang WR (1991). Interleukin-1 is cytoprotective, antisecretory, stimulates PGE2 synthesis by the stomach, and retards gastric emptying. Life Sci 48(2):123–134.

Robert A, Guth PH, Schmidt KL, Miller TA (1989). Response to an editorial on gastric cytoprotection. Gastroenterology 96(2 Pt 1):548–551.

Lu SC, Kuhlenkamp J, Robert A, Kaplowitz N (1989). Role of glutathione status in protection against ethanol-induced gastric lesions. Pharmacology 38(1):57–60.

Kolbasa KP, Lancaster C, Olafsson AS, Gilbertson SK, Robert A (1988). Indomethacin-induced gastric antral ulcers in hamsters. Gastroenterology 95(4):932–944.

Elliott G, Whited BA, Purmalis A, Davis JP, Field SO, Lancaster C, Robert A (1986). Effect of 16,16-dimethyl PGE2 on renal papillary necrosis and gastrointestinal ulcerations (gastric, duodenal, intestinal) produced in rats by mefenamic acid. Life Sci 39(5):423–432.

Robert A (1986). Cytoprotection and prostaglandins. Klin Wochenschr 64 Suppl 7:40–43.

Robert A, Lancaster C, Davis JP, Kolbasa KP, Nezamis JE (1986). Ulcer formation and cytoprotection by acetazolamide. Eur J Pharmacol 118(3):193–201.

Robert A, Aristoff PA, Wendling MG, Kimball FA, Miller WL Jr, Gorman RR (1985). Cytoprotective and antisecretory properties of a non-diarrheogenic and non-uterotonic prostacyclin analog: U-68,215. Prostaglandins 30(4):619–649.

Leung FW, Robert A, Guth PH (1985). Gastric mucosal blood flow in rats after administration of 16,16-dimethyl prostaglandin E2 at a cytoprotective dose. Gastroenterology 88(6):1948–1953.

Robert A, Lancaster C, Davis JP, Field SO, Sinha AJ, Thornburgh BA (1985). Cytoprotection by prostaglandin occurs in spite of penetration of absolute ethanol into the gastric mucosa. Gastroenterology 88(1 Pt 2):328–333.

Guth PH, Paulsen G, Nagata H, Leung F, Robert A, Ohya Y (1985). Prostaglandin cytoprotection: role of microcirculatory changes. Adv Prostaglandin Thromboxane Leukot Res 15:637–639.

Robert A (1984). [Gastrointestinal cytoprotection by prostaglandins]. Gastroenterol Clin Biol 8(11):819–827.

Robert A, Eberle D, Kaplowitz N (1984). Role of glutathione in gastric mucosal cytoprotection. Am J Physiol 247(3 Pt 1):G296–G304.

Robert A, Böttcher W, Golanska E, Kauffman GL Jr (1984). Lack of correlation between mucus gel thickness and gastric cytoprotection in rats. Gastroenterology 86(4):670–674.

Robert A, Lancaster C, Davis JP, Field SO, Nezamis JE (1984). Distinction between antiulcer effect and cytoprotection. Scand J Gastroenterol Suppl 101:69–73.

Robert A (1984). Prostaglandins: effects on the gastrointestinal tract. Clin Physiol Biochem 2(2–3):61–69.

Robert A, Nezamis JE, Lancaster C, Davis JP, Field SO, Hanchar AJ (1983). Mild irritants prevent gastric necrosis through “adaptive cytoprotection” mediated by prostaglandins. Am J Physiol 245(1):G113–G121.

Robert A (1983). Cytoprotection of the gastrointestinal mucosa. Adv Intern Med 28:325–337.

Vantrappen G, Janssens J, Popiela T, Kulig J, Tytgat GN, Huibregtse K, Lambert R, Pauchard JP, Robert A (1982). Effect of 15(R)-15-methyl prostaglandin E2 (arbaprostil) on the healing of duodenal ulcer: a double-blind multicenter study. Gastroenterology 83(2):357–363.

Konturek SJ, Robert A (1982). Cytoprotection of canine gastric mucosa by prostacyclin: possible mediation by increased mucosal blood flow. Digestion 25(3):155–163.

Robert A (1981). Gastric cytoprotection by sodium salicylate. Prostaglandins 21 suppl:139–146.

Ruppin H, Person B, Robert A, Domschke W (1981). Gastric cytoprotection in man by prostaglandin E2. Scand J Gastroenterol 16(5):647–652.

Robert A (1981). Current history of cytoprotection. Prostaglandins 21 Suppl:89–96.

Robert A (1981). Cytoprotection by prostaglandins. Scand J Gastroenterol Suppl 67:223–227.

Chaudhury TK, Robert A (1980). Prevention by mild irritants of gastric necrosis produced in rats by sodium taurocholate. Dig Dis Sc 25(11):830–836.

Robert A (1979). Cytoprotection by prostaglandins. Gastroenterology 77(4Pt 1):761–767.

Robert A, Nezamis JE, Lancaster C, Hanchar AJ (1979). Cytoprotection by prostaglandins in rats. Prevention of gastric necrosis produced by alcohol, HCl, NaOH, hypertonic NaCl, and thermal injury. Gastroenterology 77(3):433–443.

Lancaster C, Robert A (1978). Intestinal lesions produced by prednisolone: prevention (cytoprotection) by 16,16-dimethyl prostaglandin E2. Am J Physiol 235(6):E703–E708.

Robert A, Asano T (1977). Resistance of germfree rats to indomethacin-induced intestinal lesions. Prostaglandins 14(2):333–341.

Other publications related to ulcer formation and therapy

Robert A, Selye H (1952). [Effect of somatotropic hormone and cortisone on experimental gastric ulcer.]. Ann Endocrinol (Paris) 13(5):845–848.

Robert A (1954). [Production of progressive renal atrophy.]. Rev Can Biol 13(1):3–10.

Robert A (1956). Complete prevention of cerebral accidents in malignant hypertension. Circ Res 4(5):527–532.

Robert A, Nezamis JE (1957). The granuloma pouch as a routine assay for antiphlogistic compounds. Acta Endocrinol (Copenh) 25(1):105–112.

Robert A, Nezamis JE (1957). Effect of desoxycorticosterone on inflammation after local administration. Acta Endocrinol (Copenh) 25(3):298–302.

Robert A, Nezamis JE (1957). Hypertensive eye lesions in the rat; effect of carotid ligation. Experientia 13(11):457–459.

Robert A, Nezamis JE (1958). Effect of cortisol on gastric ulcers of the Shay rat. Proc Soc Exp Biol Med 98(1):9–12.

Robert A, Nezamis JE (1958). Ulcerogenic property of steroids. Proc Soc Exp Biol Med 99(2):443–447.

Robert A, Nezamis JE (1959). Prevention of steroid induced ulcers with an anticholinergic drug. Proc Soc Exp Biol Med 100(3):596–597.

Stafford RO, Robert A, Lyster SC, Schmidt FL, Dulin WE (1959). Fluorometholone, a preferentially anti-inflammatory corticoid. Proc Soc Exp Biol Med 101:653–655.

Robert A, Nezamis JE (1959). Effect of cortisol on an experimental inflammation already established. Endocrinology 65:725–727.

Robert A, Nezamis JE (1961). Antiphlogistic property of certain 11-desoxysteroids after systemic administration. Endocrinology 68:937–943.

Robert A, Nezamis JE (1961). Antiphlogistic property of desoxycorticosterone after partial hepatectomy, adrenalectomy, force-feeding and KCl ingestion in the rat. Endocrinology 68:932–936.

Robert A, Nezamis JE (1962). Effect of a histamine releaser on steroid induced ulcers. Proc Soc Exp Biol Med 109:698–700.

Robert A, Phillips JP, Nezamis JE (1966). Production, by restraint, of gastric ulcers and of hydrothorax in the rat. Gastroenterology 51(1):75–81.

Robert A, Phillips JP, Nezamis JE (1966). Gastric secretion and ulcer formation after hypophysectomy and administration of somatotrophic hormone. Am J Dig Dis 11(7):546–552.

Robert A, Phillips JP, Nezamis JE (1966). Prevention of ulcer formation by hypophysectomy. Proc Soc Exp Biol Med 121(4):992–995.

Robert A, Nezamis JE (1964). Effect of an anti-acetylcholine drug, methscopolamine bromide, on ulcer formation and gastric mucus. J Pharm Pharmacol 16:690–695.

Robert A, Nezamis JE (1964). Histopathology of steroid-induced ulcers. An experimental study in the rat. Arch Pathol 77:407–423.

Robert A, Bayer RB, Nezamis JE (1963). Gastric mucus content during development of ulcers in fasting rats. Gastroenterology 5:740–751.

Robert A, Nezamis JE (1963) Effcet of prednisolone on gastric mucus content and ulcer formation. Proc Soc Exp Biol Med 14:545–550.

Robert A, Stout TJ, Dale JE(1970). Production by secretagogues of duodenal ulcers in the rat. Gastroenterology 59(1):95–102.

Robert A, Northam JI, Nezamis JE, Phillips JP (1970). Exertion ulcers in the rat. Am J Dig Dis 15(5):497–507.

Robert A (1971). The pro-ulcer effect of nicotine. An experimental study in the rat. J Lab Clin Med 78(5):831.

Robert A, Stowe DF, Nezamis JE (1971). Possible relationship between smoking and peptic ulcer. Nature 233(5320):497–498.

Moffett RB, Robert A, Skaletzky LL (1971). Antiulcer agents. p-aminobenzamido aromatic compounds. J Med Chem 14(10):963–968.

Nezamis JE, Robert A, Stowe DF (1971). Inhibition by prostaglandin E1 of gastric secretion in the dog. J Physiol 218(2):369–383.

Robert A, Dale JE (1971). Prevention of duodenal ulcers in rats by feeding. Proc Soc Exp Biol Med 136(2):439–440.

Robert A (1971). Proposed terminology for the anatomy of the rat stomach. Gastroenterology 60(2):344–345.

Nylander B, Robert A, Andersson S (1974). Gastric secretory inhibition by certain methyl analogs of prostaglandin E2 following intestinal administration in man. Scand J Gastroenterol 9(8):759–762.

Robert A (1974). Experimental production of duodenal ulcers. Biol Gastroenterol (Paris) 7(2):145–161.

Robert A, Mylander B, Andersson S (1974). Marked inhibition of gastric secretion by two prostaglandin analogs given orally to man. Life Sci 14(3):533–538.

Robert A, Nezamis JE, Lancaster C, Badalamenti JN (1974). Cysteamine-induced duodenal ulcers: a new model to test antiulcer agents. Digestion 11(3–4):199–214.

Robert A (1972). Potentiation, by nicotine of duodenal ulcers in the rat. Proc Soc Exp Biol Med 139(1):319–322.

Robert A, Nezamis JE, Dale JE, Stowe DF (1972). Role of gastric acid in the development of duodenal ulcers in the rat. Digestion 6(1):34–45.

Robert A (1976). Antisecretory, antiulcer, cytoprotective and diarrheogenic properties of prostaglandins. Adv Prostaglandin Thromboxane Res 2:507–520.

Robert A (1975). An intestinal disease produced experimentally by a prostaglandin deficiency. Gastroenterology 69(4):1045–1047.

Robert A, Nezamis JE, Lancaster C (1975). Duodenal ulcers produced in rats by propionitrile: factors inhibiting and aggravating such ulcers. Toxicol Appl Pharmacol 31(2):201–207.

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Mózsik, G. Gastric cytoprotection 30 years after its discovery by André Robert: a personal perspective. Inflammopharmacol 18, 209–221 (2010). https://doi.org/10.1007/s10787-010-0045-5

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