Insights into the Mechanisms of Gastric Adaptation to Aspirin-Induced Injury: A Role for Regenerating Protein but Not Trefoil Peptides

Laboratory Investigation

Volumn 83, Issue 10, 2003, Pages 1415-1425

  Alderman, Barbara M ^a   Ulaganathan, Meera ^a   Judd, Louise M ^a   Howlett, Meegan ^a   Parker, Lorraine M ^a   Yeomans, Neville D ^a   Giraud, Andrew S ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; NONSTEROID ANTIINFLAMMATORY AGENT; PROTEIN; PROTEIN TFF1; PROTEIN TFF2; TREFOIL PEPTIDE; UNCLASSIFIED DRUG;

ADAPTATION; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; STOMACH INJURY; STOMACH PROTECTION; TISSUE REPAIR;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ASPIRIN; BLOTTING, NORTHERN; CALCIUM-BINDING PROTEINS; GASTRIC MUCOSA; GENE EXPRESSION; GROWTH SUBSTANCES; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LITHOSTATHINE; MUCINS; MUSCLE PROTEINS; NERVE TISSUE PROTEINS; NEUROPEPTIDES; PEPTIDES; PROTEINS; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STOMACH; TUMOR SUPPRESSOR PROTEINS;

EID: 0142043009     PISSN: 00236837     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.LAB.0000092231.54761.CD     Document Type: Article

References (59)

1. Alderman BM, Cook GA, Familari M, Yeomans ND, and Giraud AS (2000). Resistance to apoptosis is a mechanism of adaptation of rat stomach to aspirin. Am J Physiol Gastrointest Liver Physiol 278:G839-G846.
2. Alison MR, Chinery R, Poulsom R, Ashwood P, Longcroft JM, and Wright NA (1995). Experimental ulceration leads to sequential expression of spasmolytic polypeptide, intestinal trefoil factor, epidermal growth factor and transforming growth factor alpha mRNAs in rat stomach. J Pathol 175:405-414.
3. Asahara M, Mushiake S, Shimada S, Fukui H, Kinoshita Y, Kawanami C, Watanabe T, Tanaka S, Ichikawa A, Uchiyama Y, Narushima Y, Takasawa S, Okamoto H, Tohyama M, and Chiba T (1996). Reg gene expression is increased in rat gastric enterochromaffin-like cells following water immersion stress. Gastroenterology 111:45-55.
4. Baumgartner A, Koelz HR, and Halter F (1986). Indomethacin and turnover of gastric mucosal cells in the rat. Am J Physiol 250:G830-G835.
5. Chinery R and Playford RJ (1995). Combined intestinal trefoil factor and epidermal growth factor is prophylactic against indomethacin-induced gastric damage in the rat. Clin Sci (Colch) 88:401-403.
6. Chomczynski P and Sacchi N (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenolchloroform extraction. Anal Biochem 162:156-159.
7. Cook GA, Yeomans ND, and Giraud AS (1997). Temporal expression of trefoil peptides in the TGF-alpha knockout mouse after gastric ulceration. Am J Physiol 272:G1540-G1549.
8. Dignass A, Lynch-Devaney K, Kindon H, Thim L, and Podolsky DK (1994). Trefoil peptides promote epithelial migration through a transforming growth factor beta-independent pathway. J Clin Invest 94:376-383.
9. Doljanin K, Skeljo MV, Yeomans ND, and Giraud AS (1996). Adaptation of the gastric epithelium to injury is maintained in vitro and is associated with increased TGF-alpha expression. J Gastroenterol Hepatol 11:259-263.
10. Dusetti NJ, Mallo GV, Ortiz EM, Keim V, Dagorn JC, and Iovanna JL (1996). Induction of lithostathine/reg mRNA expression by serum from rats with acute pancreatitis and cytokines in pancreatic acinar AR-42J cells. Arch Biochem Biophys 330:129-132.
11. Dusetti NJ, Ortiz EM, Mallo GV, Dagorn JC, and Iovanna JL (1995). Pancreatitis-associated protein I (PAP I), an acute phase protein induced by cytokines: Identification of two functional interleukin-6 response elements in the rat PAP I promoter region. J Biol Chem 270:22417-22421.
12. Eastwood GL and Quimby GF (1982). Effect of chronic aspirin ingestion on epithelial proliferation in rat fundus, antrum, and duodenum. Gastroenterology 82:852-856.
13. Familari M, Cook GA, Taupin DR, Marryatt G, Yeomans ND, and Giraud AS (1998). Trefoil peptides are early markers of gastrointestinal maturation in the rat. Int J Dev Biol 42:783-789.
14. Francis PJ, Southgate JL, Wilkin TJ, and Bone AJ (1992). Expression of an islet regenerating (reg) gene in isolated rat islets: Effects of nutrient and non-nutrient growth factors. Diabetologia 35:238-242.
15. Fukui H, Kinoshita Y, Maekawa T, Okada A, Waki S, Hassan S, Okamoto H, and Chiba T (1998). Regenerating gene protein may mediate gastric mucosal proliferation induced by hypergastrinemia in rats. Gastroenterology 115:1483-1493.
16. Graham DY, Smith JL, and Dobbs SM (1983). Gastric adaptation occurs with aspirin administration in man. Dig Dis Sci 28:1-6.
17. Graham DY, Smith JL, Spjut HJ, and Torres E (1988). Gastric adaptation: Studies in humans during continuous aspirin administration. Gastroenterology 95:327-333.
18. Gurr W, Yavari R, Wen L, Shaw M, Mora C, Christa L, and Sherwin RS (2002). A Reg family protein is overexpressed in islets from a patient with new-onset type 1 diabetes and acts as T-cell autoantigen in NOD mice. Diabetes 51:339-346.
19. Hanby AM, Poulsom R, Singh S, Elia G, Jeffery RE, and Wright NA (1993). Spasmolytic polypeptide is a major antral peptide: Distribution of the trefoil peptides human spasmolytic polypeptide and pS2 in the stomach. Gastroenterology 105:1110-1116.
20. Higham AD, Bishop LA, Dimaline R, Blackmore CG, Dobbins AC, Varro A, Thompson DG, and Dockray GJ (1999). Mutations of Reglalpha are associated with enterochromaffin-like cell tumor development in patients with hypergastrinemia. Gastroenterology 116:1310-1318.
21. Hurley JW and Crandall LA (1964). The effect of salicylates upon the stomachs of dogs. Gastroenterology 46:36-43.
22. Jeffrey GP, Oates PS, Wang TC, Babyatsky MW, and Brand SJ (1994). Spasmolytic polypeptide: A trefoil peptide secreted by rat gastric mucous cells. Gastroenterology 106:336-345.
23. Jones MK, Tomikawa M, Mohajer B, and Tarnawski AS (1999). Gastrointestinal mucosal regeneration: Role of growth factors. Front Biosci 4:D303-D309.
24. Kawanami C, Fukui H, Kinoshita Y, Nakata H, Asahara M, Matsushima Y, Kishi K, and Chiba T (1997). Regenerating gene expression in normal gastric mucosa and indomethacin-induced mucosal lesions of the rat. J Gastroenterol 32:12-18.
25. Kazumori H, Ishihara S, Hoshino E, Kawashima K, Moriyama N, Suetsugu H, Sato H, Adachi K, Fukuda R, Watanabe M, Takasawa S, Okamoto H, Fukui H, Chiba T, and Kinoshita Y (2000). Neutrophil chemoattractant 2 beta regulates expression of the Reg gene in injured gastric mucosa in rats. Gastroenterology 119:1610-1622.
26. Kindon H, Pothoulakis C, Thim L, Lynch-Devaney K, and Podolsky DK (1995). Trefoil peptide protection of intestinal epithelial barrier function: Cooperative interaction with mucin glycoprotein. Gastroenterology 109:516-523.
27. Kobayashi S, Akiyama T, Nata K, Abe M, Tajima M, Shervani NJ, Unno M, Matsuno S, Sasaki H, Takasawa S, and Okamoto H (2000). Identification of a receptor for reg (regenerating gene) protein, a pancreatic beta-cell regeneration factor. J Biol Chem 275:10723-10726.
28. Konturek JW, Dembinski A, Stoll R, Domschke W, and Konturek SJ (1994a). Mucosal adaptation to aspirin induced gastric damage in humans: Studies on blood flow, gastric mucosal growth, and neutrophil activation. Gut 35:1197-1204.
29. Konturek JW, Konturek SJ, Stachura J, and Domschke W (1998a). Helicobacter pylori-positive peptic ulcer patients do not adapt to aspirin. Aliment Pharmacol Ther 12:857-864.
30. Konturek PC, Brzozowski T, Konturek SJ, Elia G, Wright N, Sliwowski Z, Thim L, and Hahn EG (1997). Role of spasmolytic polypeptide in healing of stress-induced gastric lesions in rats. Regul Pept 68:71-79.
31. Konturek PC, Brzozowski T, Konturek SJ, Taut A, Sliwowski Z, Stachura J, and Hahn EG (1998b). Activation of genes for growth factors and cyclooxygenases in rat gastric mucosa during recovery from stress damage. Eur J Pharmacol 342:55-65.
32. Konturek SJ, Brzozowski T, Stachura J, Dembinski A, and Majka J (1994b). Role of gastric blood flow, neutrophil infiltration, and mucosal cell proliferation in gastric adaptation to aspirin in the rat. Gut 35:1189-1196.
33. Lev R, Siegel HI, and Glass GB (1972). Effects of salicylates on the canine stomach: A morphological and histochemical study. Gastroenterology 62:970-980.
34. Levi S, Goodlad RA, Lee CY, Walport MJ, Wright NA, and Hodgson HJ (1992). Effects of nonsteroidal anti-inflammatory drugs and misoprostol on gastroduodenal epithelial proliferation in arthritis. Gastroenterology 102:1605-1611.
35. Lipscomb GR, Wallis N, Armstrong G, Goodman MJ, and Rees WD (1995). Gastric mucosal adaptation to etodolac and naproxen. Aliment Pharmacol Ther 9:379-385.
36. Mahr S, Neumayer N, Kolb HJ, Schepp W, Classen M, and Prinz C (1998). Growth factor effects on apoptosis of rat gastric enterochromaffin-like cells. Endocrinology 139:4380-4390.
37. Miyaura C, Chen L, Appel M, Alam T, Inman L, Hughes SD, Milburn JL, Unger RH, and Newgard CB (1991). Expression of reg/PSP, a pancreatic exocrine gene: Relationship to changes in islet beta-cell mass. Mol Endocrinol 5:226-234.
38. Playford RJ, Marchbank T, Chinery R, Evison R, Pignatelli M, Boulton RA, Thim L, and Hanby AM (1995). Human spasmolytic polypeptide is a cytoprotective agent that stimulates cell migration. Gastroenterology 108:108-116.
39. Podolsky DK, Lynch-Devaney K, Stow JL, Oates P, Murgue B, DeBeaumont M, Sands BE, and Mahida YR (1993). Identification of human intestinal trefoil factor: Goblet cell-specific expression of a peptide targeted for apical secretion. J Biol Chem 268:6694-6702.
40. Rio MC, Bellocq JP, Daniel JY, Tomasetto C, Lathe R, Chenard MP, Batzenschlager A, and Chambon P (1988). Breast cancer-associated pS2 protein: Synthesis and secretion by normal stomach mucosa. Science 241:705-708.
41. Romano M, Lesch CA, Meise KS, Veljaca M, Sanchez B, Kraus ER, Boland CR, Guglietta A, and Coffey RJ (1996). Increased gastroduodenal concentrations of transforming growth factor alpha in adaptation to aspirin in monkeys and rats. Gastroenterology 110:1448-1455.
42. Shorrock CJ, Prescott RJ, and Rees WD (1990). The effects of indomethacin on gastroduodenal morphology and mucosal pH gradient in the healthy human stomach. Gastroenterology 99:334-339.
43. Shorrock CJ and Rees WD (1992). Mucosal adaptation to indomethacin induced gastric damage in man: Studies on morphology, blood flow, and prostaglandin E2 metabolism. Gut 33:164-169.
44. Skeljo MV, Cook GA, Elliott SL, Giraud AS, and Yeomans ND (1996). Gastric mucosal adaptation to diclofenac injury. Dig Dis Sci 41:32-39.
45. Skeljo MV, Giraud AS, and Yeomans ND (1992). Adaptation of rat gastric mucosa to repeated doses of non-salicylate non-steroidal anti-inflammatory drugs. J Gastroenterol Hepatol 7:586-590.
46. St John DJ, Yeomans ND, McDermott FT, and De Boer WG (1973). Adaptation of the gastric mucosa to repeated administration of aspirin in the rat. Am J Dig Dis 18:881-885.
47. Stachura J, Konturek JW, Dembinski A, and Domschke W (1994). Do infiltrating leukocytes contribute to the adaptation of human gastric mucosa to continued aspirin administration? Scand J Gastroenterol 29:966-972.
48. Stachura J, Konturek JW, Dembinski A, and Domschke W (1996). Growth markers in the human gastric mucosa during adaptation to continued aspirin administration. J Clin Gastroenterol 22:282-287.
49. Suemori S, Lynch-Devaney K, and Podolsky DK (1991). Identification and characterization of rat intestinal trefoil factor: Tissue- and cell-specific member of the trefoil protein family. Proc Natl Acad Sci USA 88:11017-11021.
50. Taupin D, Pedersen J, Familari M, Cook G, Yeomans N, and Giraud AS (2001). Augmented intestinal trefoil factor (TFF3) and loss of pS2 (TFF1) expression precedes metaplastic differentiation of gastric epithelium. Lab Invest 81:397-408.
51. Taupin DR, Pang KC, Green SP, and Giraud AS (1995). The trefoil peptides spasmolytic polypeptide and intestinal trefoil factor are major secretory products of the rat gut. Peptides 16:1001-1005.
52. Terazono K, Yamamoto H, Takasawa S, Shiga K, Yonemura Y, Tochino Y, and Okamoto H (1988). A novel gene activated in regenerating islets. J Biol Chem 263:2111-2114.
53. Tomasetto C, Masson R, Linares JL, Wendling C, Lefebvre O, Chenard MP, and Rio MC (2000). pS2/TFF1 interacts directly with the VWFC cysteine-rich domains of mucins. Gastroenterology 118:70-80.
54. Tomasetto C, Rio MC, Gautier C, Wolf C, Hareuveni M, Chambon P, and Lathe R (1990). hSP, the domain-duplicated homolog of pS2 protein, is co-expressed with pS2 in stomach but not in breast carcinoma. EMBO J 9:407-414.
55. Ulaganathan M, Familari M, Yeomans ND, Giraud AS, and Cook GA (2001). Spatio-temporal expression of trefoil peptide following severe gastric ulceration in the rat implicates it in late-stage repair processes. J Gastroenterol Hepatol 16:506-512.
56. Wallace JL, McKnight GW, and Bell CJ (1995). Adaptation of rat gastric mucosa to aspirin requires mucosal contact. Am J Physiol 268:G134-G138.
57. Watanabe T, Yonekura H, Terazono K, Yamamoto H, and Okamoto H (1990). Complete nucleotide sequence of human reg gene and its expression in normal and tumoral tissues: The reg protein, pancreatic stone protein, and pancreatic thread protein are one and the same product of the gene. J Biol Chem 265:7432-7439.
58. Watanabe T, Yonemura Y, Yonekura H, Suzuki Y, Miyashita H, Sugiyama K, Moriizumi S, Unno M, Tanaka O, Kondo H, and et al (1994). Pancreatic beta-cell replication and amelioration of surgical diabetes by Reg protein. Proc Natl Acad Sci USA 91:3589-3592.
59. Yeomans ND, Saint John DJ, and de Boer WG (1973). Regeneration of gastric mucosa after aspirin-induced injury in the rat. Am J Dig Dis 18:773-780.