Role of iron in the pathogenesis of cysteamine-induced duodenal ulceration in rats

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 296, Issue 6, 2009, Pages

  Khomenko, Tetyana ^a,b   Szabo, Sandor ^a,b   Deng, Xiaoming ^a,b   Ishikawa, Hideki ^a,b   Anderson, Gregory J ^c   McLaren, Gordon D ^a,b  

^a VA LONG BEACH HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD71 ANTIGEN; CIMETIDINE; DEFEROXAMINE; FERRIC GLUCONATE; FERRIC ION; FERRITIN; FERROPORTIN; FERROUS ION; IRON; IRON REGULATORY PROTEIN 1; MERCAPTAMINE; MESSENGER RNA; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DUODENUM MUCOSA; DUODENUM ULCER; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ULCEROGENESIS;

ANIMAL STRUCTURES; ANIMALS; CATION TRANSPORT PROTEINS; CIMETIDINE; COLON; CYSTEAMINE; DEFEROXAMINE; DUODENAL ULCER; DUODENUM; FEMALE; FERRIC COMPOUNDS; FERRITINS; FERROUS COMPOUNDS; GASTRIC MUCOSA; GENE EXPRESSION; ILEUM; INTESTINAL MUCOSA; IRON; IRON REGULATORY PROTEIN 1; JEJUNUM; MODELS, BIOLOGICAL; RATS; RATS, MUTANT STRAINS; RATS, SPRAGUE-DAWLEY; RECEPTORS, TRANSFERRIN;

EID: 67049146669     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.90257.2008     Document Type: Article

References (70)

1. Adamama-Moraitou K, Rallis T, Papasteriadis A, Roubies N, Kaldrimidou H. Iron, zinc, and copper concentration in serum, various organs, and hair of dogs with experimentally induced exocrine pancreatic insufficiency. Dig Dis Sci 46: 1444-1457, 2001. (Pubitemid 32655042)
2. Adler RS, Gallagher GT, Szabo S. Duodenal ulcerogens cysteamine and propionitrile decrease duodenal neutralization of acid in the rat. Dig Dis Sci 288: 716-723, 1983.
3. Anderson GJ, Vulpe CD. Regulation of intestinal iron transport. In: Molecular and Cellular Iron Transport, edited by D. Templeton New York: Marcel Dekker, 2001, pp. 559-596.
4. Aziz N, Munro HN. Iron regulates ferritin mRNA translation through a segment of its 5′ untranslated region. Proc Natl Acad Sci USA 84: 8478-8482, 1987.
5. Berruyer C, Martin FM, Castellano R, Macone A, Malergue F, Garrido-Urbani S, Millet V, Imbert J, Dupre S, Pitari G, Naquet P, Galland F. Vanin-1-/- mice exhibit a glutathione-mediated tissue resistance to oxidative stress. Mol Cell Biol 24: 7214-7224, 2004. (Pubitemid 39014447)
6. Biaglow JE, Issels RW, Gerweck LE, Varnes ME, Jacobson B, Mitchell JB, Russo A. Factors influencing the oxidation of cysteamine and other thiols: implications for hyperthermic sensitization and radiation protection. Radiat Res 100: 298-312, 1984. (Pubitemid 15223904)
7. Bougle D, Vaghefi-Vaezzadeh N, Roland N, Bouvard G, Arhan P, Bureau F, Neuville D, Maubois JL. Influence of short-chain fatty acids on iron absorption by proximal colon. Scand J Gastroenterol 37: 1008-1011, 2002.
8. Bouton C, Hirling H, Drapier JC. Redox modulation of iron regulatory proteins by peroxynitrite. J Biol Chem 272: 19969-19975, 1997. (Pubitemid 27340098)
9. 2 on the expression and function of iron-responsive element-containing mRNAs in B6 fibroblasts. J Biol Chem 276: 19738-19745, 2001.
10. Canonne-Hergaux F, Gruenheid S, Ponka P, Gros P. Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron. Blood 93: 4406-4417, 1999. (Pubitemid 29279284)
11. Capozzi G, Modena G. Oxidation of thiols. In: The Chemistry of the Thiol Group, edited by S. Patai. London, UK: John Wiley & Sons, 1974, pp. 785-840.
12. Champagne ET. Low gastric hydrochloric acid secretion and mineral bioavailability. Adv Exp Med Biol 249: 173-184, 1989.
13. Chan FK, Leung WK. Peptic-ulcer disease. Lancet 360: 933-941, 2002. (Pubitemid 35283840)
14. De Silva DM, Askwith CC, Kaplan J. Molecular mechanisms of iron uptake in eukaryotes. Physiol Rev 76: 31-47, 1996. (Pubitemid 26048277)
15. Donovan A, Brownlie A, Zhou Y, Shepard J, Pratt SJ, Moynihan J, Paw BH, Drejer A, Barut B, Zapata A, Law TC, Brugnara C, Lux SE, Pinkus GS, Pinkus JL, Kingsley PD, Palis J, Fleming MD, Andrews NC, Zon LI. Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature 403: 776-781, 2000. (Pubitemid 30111839)
16. Dupre S, Graziani MT, Rosei MA, Fabi A, Del Grosso E. The enzymatic breakdown of pantethine to pantothenic acid and cysteamine. Eur J Biochem 16: 571-578, 1970.
17. Eichholz A, Howell KE. Binding studies as an approach to the study of intestinal transport. Gastroenterology 62: 647-667, 1972.
18. Fillebeen C, Pantopoulos K. Redox control of iron regulatory proteins. Redox Rep 7: 15-22, 2002. (Pubitemid 34285103)
19. Fleming MD, Romano MA, Su MA, Garrick LM, Garrick MD, Andrews NC. Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc Natl Acad Sci USA 95: 1148-1153, 1998. (Pubitemid 28124927)
20. Frankel D, Schipper HM. Cysteamine pretreatment of the astroglial substratum (mitochondrial iron sequestration) enhances PC12 cell vulnerability to oxidative injury. Exp Neurol 160: 376-385, 1999.
21. Gallagher GT, Szabo S. Direct measurement of duodenal acid-pepsin exposure at site of ulceration in rats. Am J Physiol Gastrointest Liver Physiol 246: G660-G665, 1984. (Pubitemid 14079065)
22. Galy B, Ferring D, Minana B, Bell O, Janser HG, Muckenthaler M, Schumann K, Hentze MW. Altered body iron distribution and microcytosis in mice deficient in iron regulatory protein 2 (IRP2). Blood 106: 2580-2589, 2005. (Pubitemid 41510837)
23. Ganz T, Nemeth E. Iron imports. IV. Hepcidin and regulation of body iron metabolism. Am J Physiol Gastrointest Liver Physiol 290: G199-G203, 2006.
24. Gruenheid S, Canonne-Hergaux F, Gauthier S, Hackam DJ, Gristein S, Gros P. The iron transport protein NRAMP2 is an integral membrane glycoprotein that colocalizes with transferring in recycling endosomes. J Exp Med 189: 831-841, 1999. (Pubitemid 29189688)
25. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388: 482-488, 1997. (Pubitemid 27328927)
26. Haig A, Driman DK. Iron-induced mucosal injury to the upper gastrointestinal tract. Histopathology 48: 808-812, 2006. (Pubitemid 43800940)
27. Halliwell B, Gutteridge JMC. Free radicals, aging and diseases. In: Free Radicals in Biology and Medicine, edited by Halliwell B and Gutteridge JMC. Oxford, UK: Clarendon Press, 1989, pp. 416-508.
28. Halliwell B, Gutteridge JMC. The role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol 186: 1-85, 1990. (Pubitemid 20279941)
29. Held KD, Biaglow JE. Mechanisms for the oxygen radical-mediated toxicity of various thiol-containing compounds in cultured mammalian cells. Radiat Res 139: 15-23, 1994. (Pubitemid 24230918)
30. Hentze MW, Caughman SW, Rouault TA, Barriocanal JG, Dancis A, Harford JB, Klausner RD. Identification of the iron-responsive element for the translational regulation of human ferritin mRNA. Science 238: 1570-1573, 1987. (Pubitemid 18032473)
31. Hentze MW, Rouault TA, Harford JB, Klausner RD. Oxidationreduction and the molecular mechanism of a regulatory RNA-protein interaction. Science 244: 357-359, 1989. (Pubitemid 19117876)
32. Jaffrey SR, Cohen NA, Rouault TA, Klausner RD, Snyder SH. The iron-responsive element binding protein: a target for synaptic actions of nitric oxide. Proc Natl Acad Sci USA 91: 12994-12998, 1994.
33. Jeitner TM, Lawrence DA. Mechanisms for the cytotoxicity of cysteamine. Toxicol Sci 63: 57-64, 2001. (Pubitemid 32799024)
34. Khomenko T, Deng XM, Jadus MR, Szabo S. Effect of cysteamine on redox-sensitive thiol- containing proteins in the duodenal mucosa. Biochem Biophys Res Commun 309: 910-916, 2003. (Pubitemid 37122616)
35. Khomenko T, Deng X, Sandor Z, Tarnawski AS, Szabo S. Cysteamine alters redox state, HIF-1alpha transcriptional interactions and reduces duodenal mucosal oxygenation: novel insight into the mechanisms of duodenal ulceration. Biochem Biophys Res Commun 317: 121-127, 2004. (Pubitemid 38401972)
36. Khomenko T, Szabo S, Deng XM, Jadus MR, Ishikawa H, Osapay K, Sandor ZS, Chen L. Suppression of early growth response factor-1 with egr-1 antisense oligodeoxynucleotide aggravates experimental duodenal ulcers. Am J Physiol Gastrointest Liver Physiol 290: G1211-G1218, 2006. (Pubitemid 43788304)
37. Kim DW, Kim KY, Choi BS, Youn P, Ryu DY, Klaassen CD, Park JD. Regulation of metal transporters by dietary iron, and the relationship between body iron levels and cadmium uptake. Arch Toxicol 81: 327-334, 2007. (Pubitemid 46701591)
38. Koeller DM, Casey JL, Hentze MW, Gerhardt EM, Chan LN, Klausner RD, Harford JB. A cytosolic protein binds to structural elements within the iron regulatory region of the transferrin receptor mRNA. Proc Natl Acad Sci USA 86: 3574-3578, 1989.
39. Leibold EA, Munro HN. Cytoplasmic protein binds in vitro to a highly conserved sequence in the 5′ untranslated region of ferritin heavy- and light-subunit mRNAs. Proc Natl Acad Sci USA 85: 2171-2175, 1988. (Pubitemid 24315851)
40. Lichtenberger LM, Szabo S, Reynolds ES. Gastric emptying in the rat is inhibited by the duodenal ulcerogens, cysteamine and propionitrile. Gastroenterology 73: 1072-1076, 1977. (Pubitemid 8213111)
41. Lichtenberger LM, Szabo S, Trier JS. Duodenal ulcerogens, cysteamine and propionitrile, stimulate serum gastrin levels in the rat. Gastroenterology 73: 1305-1308, 1977. (Pubitemid 8229281)
42. Martin F, Penet MF, Malergue F, Lepidi H, Dessein A, Galland F, de Reggi M, Naquet P, Gharib B. Vanin-1(-/-) mice show decreased NSAID- and Schistosoma-induced intestinal inflammation associated with higher glutathione stores. J Clin Invest 113: 591-597, 2004. (Pubitemid 38542508)
43. Miller SL, Schlesinger G. Prebiotic syntheses of vitamin coenzymes. I. Cysteamine and 2-mercaptoethanesulfonic acid (coenzyme M). J Mol Evol 36: 302-307, 1993. (Pubitemid 23121897)
44. Mueller S, Pantopoulos K, Hubner CA, Stremmel W, Hentze MW. IRP1 activation by extracellular oxidative stress in the perfused rat liver. J Biol Chem 276: 23192-23196, 2001. (Pubitemid 37411017)
45. Novelli GD, Kaplan NO, Lipmann F. The liberation of pantothenic acid from coenzyme A. J Biol Chem 177: 97-107, 1949.
46. Pantopoulos K, Hentze MW. Activation of iron regulatory protein-1 by oxidative stress in vitro. Proc Natl Acad Sci USA 95: 10559-10563, 1998. (Pubitemid 28413106)
47. Pantopoulos K. Iron metabolism and the IRE/IRP regulatory system: an update. Ann NY Acad Sci 1012: 1-13, 2004. (Pubitemid 38453511)
48. Pitari G, Malergue F, Martin F, Philippe JM, Massucci MT, Chabret C, Maras B, Dupre S, Naquet P, Galland F. Pantetheinase activity of membrane-bound Vanin-1: lack of free cysteamine in tissues of Vanin-1 deficient mice. FEBS Lett 483: 149-154, 2000.
49. Raja KB, Bjarnason I, Simpson RJ, Peters TJ. In vitro measurement and adaptive response of Fe3+ uptake by mouse intestine. Cell Biochem Funct 5: 69-76, 1987. (Pubitemid 17215958)
50. Russell ES, Nash DJ, Bernstein SE, Kent EL, McFarland EC, Matthews SM, Norwood MS. Characterization and genetic studies of microcytic anemia in house mouse. Blood 35: 838-850, 1970.
51. Samaniego F, Chin J, Iwai K, Rouault TA, Klausner RD. Molecular characterization of a second iron-responsive element binding protein, iron regulatory protein 2. Structure, function, and post-translational regulation. J Biol Chem 269: 30904-30910, 1994. (Pubitemid 24377576)
52. Schade SG, Cohen RJ, Conrad MD. Effect of hydrochloric acid secretion on iron absorption. N Engl J Med 279: 672-674, 1968.
53. Schipper HM. Glial HO-1 expression, iron deposition and oxidative stress in neurodegenerative diseases. Neurotox Res 1: 57-70, 1999.
54. Selye H, Szabo S. Experimental model for production of perforating duodenal ulcers by cysteamine in rats. Nature 224: 458-459, 1973.
55. Simovich M, Hainsworth LN, Fields PA, Umbreit JN, Conrad ME. Localization of the iron transport proteins Mobilferrin and DMT-1 in the duodenum: the surprising role of mucin. Am J Hematol 74: 32-45, 2003. (Pubitemid 37040192)
56. Sonnenberg A, Everhart JE. Health impact of peptic ulcer in the United States. Am J Gastroenterol 92: 614-620, 1997. (Pubitemid 27184374)
57. Szabo S. Animal model of human disease. Duodenal ulcer disease animal model: cysteamine-induced acute and chronic ulcer in the rat. Am J Pathol 93: 273-276, 1978. (Pubitemid 9003864)
58. Szabo S, Haith LR Jr, Reynolds ES. Pathogenesis of duodenal ulceration produced by cysteamine or propionitrile: influence of vagotomy, sympathectomy, histamine depletion, H-2 receptor antagonists and hormones. Dig Dis Sci 24: 471-477, 1979. (Pubitemid 9211602)
59. Szabo S, Horner HC, Maull H, Schnoor J, Chiueh CC, Palkovits M. Biochemical changes in tissue catecholamines and serotonin in duodenal ulceration caused by cysteamine or propionitrile in the rat. J Pharmacol Exp Ther 2403: 871-878, 1987. (Pubitemid 17043587)
60. Szabo S, Pihan G. Development and significance of cysteamine and propionitrile models of duodenal ulcer. Chronobiol Int 4: 31-42, 1987. (Pubitemid 17096302)
61. Szabo S, Reichlin S. Somatostatin in rat tissues is depleted by cysteamine administration. Endocrinology 109: 2255-2257, 1981. (Pubitemid 12252359)
62. Szabo S, Reynolds ES, Lictenberger LM, Haith LR Jr, Dzau VJ. Pathogenesis of duodenal ulcer. Gastric hyperacidity caused by propionitrile and cysteamine in rats. Res Commun Chem Pathol Pharmacol 16: 311-323, 1977. (Pubitemid 8047048)
63. Tahsildar HI, Biaglow JE, Kligerman MM, Varnes ME. Factors influencing the oxidation of the radio protector WR-1065. Radiat Res 113: 243-251, 1998.
64. Tanaka H, Takeuchi K, Okabe S, Murakami M. Pathogenesis of the earliest cell damage induced by mepirizole and epithelial cysteamine in the rat duodenum. Jpn J Pharmacol 51: 509-519, 1989. (Pubitemid 20002043)
65. Thomas SR, Schulz E, Keaney JF Jr. Hydrogen peroxide restrains endothelium-derived nitric oxide bioactivity - role for iron-dependent oxidative stress. Free Radic Biol Med 41: 681-688, 2006. (Pubitemid 44080516)
66. Toth I, Yuan L, Rogers JT, Boyce H, Bridges KR. Hypoxia alters iron-regulatory protein-1 binding capacity and modulates cellular iron homeostasis in human hepatoma and erythroleukemia cells. J Biol Chem 274: 4467-4473, 1999. (Pubitemid 129503095)
67. Troost FJ, Brummer RJ, Haenen GR, Bast A, van Haaften RI, Evelo CT, Saris WH. Gene expression in human small intestinal mucosa in vivo is mediated by iron-induced oxidative stress. Physiol Genomics 25: 242-249, 2006.
68. Wang X, Manganaro F, Schipper HM. A cellular stress model for the sequestration of redox-active glial iron in the aging and degenerating nervous system. J Neurochem 64: 1868-1877, 1995.
69. Wheby MS, Crosby WH. The gastrointestinal tract and iron absorption. Blood 22: 416-422, 1963.
70. Wheby MS, Jones LG, Crosby WH. Studies on iron absorption. Intestinal regulatory mechanisms. J Clin Invest 43: 1433-1442, 1964.