Lipoxins, the novel mediators of gastroprotection and gastric adaptation to ulcerogenic action of aspirin

Current Pharmaceutical Design

Volumn 17, Issue 16, 2011, Pages 1541-1551

  Pajdo, Robert ^a   Brzozowski, Tomasz ^a   Szlachcic, Aleksandra ^a   Konturek, Peter C ^b   Ptak Belowska, Agata ^a   Drozdowicz, Danuta ^a   Targosz, Aneta ^a   Konturek, Stanislaw J ^a   Pawlik, Wieslaw W ^a  

^a JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

^b Thuringia Clinic Saalfeld   (Germany)

Author keywords

Aspirin; Aspirin triggered lipoxin; Cyclooxygenase; Gastric adaptation; Gastroprotection; Lipoxin; Nitric oxide releasing aspirin; Nonsteroidal anti inflammatory drugs

Indexed keywords

5 (4 CHLOROPHENYL) 1 (4 METHOXYPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOLE; ACETYLSALICYLIC ACID; ACETYLSALICYLIC ACID 3 (NITROXYMETHYL)PHENYL ESTER; CELECOXIB; CYCLOOXYGENASE 1 INHIBITOR; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; LIPOXIN; LIPOXIN A; LIPOXIN B; NAPROXCINOD; NAPROXEN; NITRIC OXIDE; NONSTEROID ANTIINFLAMMATORY AGENT; PROSTAGLANDIN; PROSTANOID; PROTON PUMP INHIBITOR; ROFECOXIB;

ANGINA PECTORIS; DIGESTIVE SYSTEM ULCER; GASTROINTESTINAL TOXICITY; GASTROPROTECTION; HEART INFARCTION; HUMAN; LOW DRUG DOSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; REVIEW; STOMACH PH; STOMACH ULCER; ULCER HEALING;

ADAPTATION, PHYSIOLOGICAL; ASPIRIN; HUMANS; LIPOXINS; STOMACH; STOMACH ULCER;

EID: 79959999333     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/138161211796197043     Document Type: Review

References (85)

1. Gerhardt C. Untersuchungen über die wasserfreien organischen Säuren. Annalen der Chemie und Pharmacie 1853; 87: 149-79.
2. Douthwaite AH., Lintott SAM. Gastroscopic observation of the effect of aspirin and certain other substances on the stomach. Lancet 1938; 2: 1222-25.
3. Vane JR. Inhibition of prostaglandin synthesis as a mechanism of action for the aspirin-like drugs. Nature 1971; 231: 232-5.
4. Jones R. Non steroid anti-inflammatory drug prescribing: past, present, and future. Am J Med 2001; 110: 4S-7S.
5. McCarthy DM. Nonsteroidal anti-inflammatory drugs - the clinical dilemmas. Scand J Gastroenterol 1992; 27 (suppl.): 9-16.
6. Talley NJ. Chronic peptic ulceration and nonsteroidal antiinflammatory drugs: More to be said about NSAIDs? Gastroenterology 1992; 102: 1074-8.
7. Hawkey CJ. Gastroduodenal problems associated with nonsteroidal anti-inflammatory drugs. Scand J Gastroenterol 1993; 28, suppl. 200: 94-5.
8. Wallace JL. Nonsteroidal anti-inflammatory drugs and gastroenteropathy: the second hundred years. Gastroenterology 1997; 112: 1000-16.
9. Wallace JL. Recent advances in gastric ulcer therapeutics. Curr Opin Pharmacol 2005; 5: 573-7.
10. Konturek SJ, Piastucki I, Brzozowski T, et al. Role of prostaglandins in the formation of aspirin-induced gastric ulcers. Gastroenterology 1981; 80: 4-9.
11. Pihan G, Rogers C, Szabo S. Vascular injury in acute gastric mucosal damage; mediatory role of leukotrienes. Dig Dis Sci 1998; 33: 625-32.
12. Wallace JL. Prostaglandins NSAIDs, and gastric mucosal protection: why doesn't the stomach digest itself? Physiol Rev 2008; 88:1547-65.
13. Konturek SJ, Brzozowski T, Drozdowicz D, Beck G. Role of leukotrienes in acute gastric lesions induced by ethanol, taurocholate, aspirin, platelet activating factor and stress in rats. Dig Dis Sci 1988; 33: 806-13.
14. Baumgartner HK, Starodub OT, Joehl JS, Tackett L, Monterose MH. Cyclooxygenase 1 is required for pH control at the mouse gastric surface. Gut 2004; 53: 1751-7.
15. Asako H, Kubes P, Wallace JL., Woy RE., Granger DN. Modulation of leukocyte adhesion in rat mesenteric venules by aspirin and salicylate. Gastroenterology 1992; 103: 146-52.
16. Andrews FJ, Malcontenti-Wilson C, O'Brien PE. Expression of adhesion molecules and leukocyte recruitment into gastric mucosa following ischemia-reperfusion. Dig Dis Sci 1997; 42: 326-9.
17. Santucci L, Fiorucci S, Giansaqnti M, et al. Pentoxyfilline prevents indomethacin-induced acute gastric mucosal damage in rats: role of tumor necrosis factor alpha. Gut 1994; 35: 909-15.
18. Appleyard CB, McCafferty DM, Tigley AW, Swain MG, Wallace JL. Tumor necrosis factor mediation of NSAID-induced gastric damage: role of leukocyte adherence. Am J Physiol 1996; 270: G-42-G48.
19. Fujiwara Y, Schmassmann A, Arakawa T, Halter F, Tarnawski A. Indomethacin interferes with epidermal growth factor binding and proliferative response of gastric KATO III cells. Digestion 1995; 56: 364-9.
20. Pai R, Szabo IL, Giap AQ, Kawanaka H, Tarnawski AS. Nonsteroidal anti-inflammatory drugs inhibit re-epithelialization of wounded gastric monolayer by interfering with actin, Sre, FAK, tensin signaling. Life Sci 2001; 69: 3055-71.
21. Coruzzi G, Venturi N, Spaggiari S. Gastrointestinal safety of novel nonsteroidal anti-inflammatory drugs: selective COX-2 inhibitors and beyond. Acta Biomed 2007; 78: 96-110.
22. Hawkey CJ, Karrasch JA, Szczepañski L, et al. Omeprazole compared with misoprostol for ulcers associated with nonsteroidal antiinflammatory drugs. Omeprazole versus misoprostol for NSAIDinduced ulcer management (IMNIUM) study group. N Engl J Med 1998; 338: 727-34.
23. Gana TJ, Huhlewych R, Koo J. Focal gastric mucosal blond flow In aspiryn-induced ulceration. Ann Surg 1987; 205: 399-403.
24. Funatsu T, Chono K, Hirata T, Keto Y, Kimota A, Sasamata M. Mucosal acid causes gastric mucosal microcirculatory disturbance In nonsteroidal anti-inflammatory drug-treated rats. Eur J Pharamcol 2007; 554; 53-9.
25. Feldman M, Colturi TJ. Effect of indomethacin on gastric acid and bicarbonate secretion in humans. Gastroenterology 1984; 87: 1339-43.
26. Levine RA, Schwartzel EH. Effect of indomethacin on basal and histamine-stimulated human gastric acid secretion. Gut 1984; 25: 718-22.
27. Barnett K, Bell CJ, McKnight W, Dicay M, Sharkey KA, Wallace JL. Role of cyclooxygenase-2 in modulating gastric acid secretion in the normal and inflamed rat stomach. Am J Physiol Gastrointest Liver Physiol 2000; 279: G1292-7.
28. Vane JR, Bakhle S, Botting RM. Cyclooxygenase 1 and 2. Ann Rev Pharmacol Toxicology 1998; 38: 97-120.
29. Jackson LM., Wu KC, Mahida YR, Jenkins D, Hawkey CJ. Cyclooxygenase (COX) 1 and 2 in normal, inflamed and ulcerated human gastric mucosa. Gut 2000; 47: 762-70.
30. Schmassman A, Peskar B, Stettler C, et al. Effect of inhibition of prostaglandin endoperoxide synthase 2 in chronic gastrointestinal ulcer models in rats. Br J Pharmacol 1998; 123: 795-804.
31. Langenbach R, Morhan SG, Tiano HF, et al. Prostaglandin synthase 1 gene disruption in mice reduces arachidonic acid-induced inflammation and indomethacin-induced gastric ulceration. Cell 1995; 83: 483-92.
32. Brzozowski T, Konturek PC, Konturek SJ, et al. Role of prostaglandins generated by cyclooxygenase-1 and cyclooxygenase-2 in healing of ischemia-reperfusion-induced gastric lesions. Eur J Pharmacol 1999; 385: 47-61.
33. Wallace JL, McKnight W, Reuter BK, Vergnolle N. NSAIDinduced gastric damage in rats: requirement for the inhibition of both cyclooxygenase 1 and 2. Gastroenterology 2000; 119: 706-14.
34. Davis NM, Sharkey KA, Asfaha S, et al. Aspirin causes rapid upregulation of cyclooxygenase-2 expression in the stomach of rats. Aliment Pharmacol Ther 1997; 11: 1101-8.
35. Brzozowski T, Konturek PC, Konturek SJ. Classic NSAID and selective cyclooxygenase (COX)-1 and COX-2 inhibitors in healing of chronic gastric ulcers. Microsc Res Technique 2001; 53: 343-53.
36. Wallace JL. COX-2: a pivotal enzyme in mucosal protection and resolution of inflammation. Sci World Journal 2006; 6: 577-88.
37. Bombardier C, Laine L, Reicin A, et al. Comparison of upper gastrointestinal toxicity of rofecoxib and naproxen in patients with rheumatoid arthritis. VIGOR Study Group. N England J Med 2000; 343: 1520-9.
38. Fiorucci S, Santucci L, Distrutti E. NSAID, coxibs, CINOD and H2S-releasing NSAIDs: what lies beyond the horizon. Dig Liver Dis 2007; 39: 1043-51.
39. Eastwood GL, Quimby F. Effect of chronic aspirin ingestion on epithelial proliferation in rat gastric body, antrum and duodenum. Gastroenterology 1982; 82: 852-6.
40. Olivero JJ, Graham DY. Gastric adaptation to nonsteroidal antiinflammatory drugs in man. Scand J Gastroenterol 1992; 27, suppl 193: 53-8.
41. Konturek SJ, Brzozowski T, Stachura J, Dembinski, Majka J. Role of gastric blond flow, neutrophil infiltration and mcosal cell proliferation in gastric adaptation to aspirin in rat. Gut 1994; 35: 1189-96.
42. Konturek SJ, Dembinski A., Stoll R, Domschke W, Konturek SJ. Mucosal adaptation to aspirin induced gastric damage in humans. Studies on blood flow, gastric mucosal growth and neutrophil activation. Gut 1994; 35: 1197-204.
43. Alderman BM, Cook GA, Familiary M, Yeomans ND, Giraud AS. Resistance to apoptosis is a mechanism of adaptation of rat stomach to aspirin. Am J Physiol 2000; 278: G839-46.
44. Ashley SW, Sonnenschein LA, Cheung LY. Focal gastric mucosal blood flow at the site of aspirin-induced ulceration. Am J Surg 1985; 149: 53-9.
45. Asako H, Kubes P, Wallace J, Gaginella T, Wolf RE, Granger DN. Indomethacin-induced leukocyte adhesion in mesenteric venules: role of lipoxygenase products. Am J Physiol Gastrointest Liver Physiol 1992; 262: G903-8.
46. Asako H, Kubes P, Wallace J, Wolf RE, Granger DN. Modulation of leukocyte adhesion in rat mesenteric venules by aspirin and salicylate. Gastroenterology 1992; 103: 146-52.
47. Brzozowski T, Konturek PC, Konturek SJ, et al. Gastric adaptation to injury by repeated doses of aspirin strengthens mucosal defense against subsequent exposure to various strong irritants in rats. Gut 1995; 37: 749-57.
48. Wallace JL, McKnight GW, Bell CJ. Adaptation of rat gastric mucosa to aspirin requires mucosal contact. Am J Physiol 1995; 268: G134-8.
49. Brzozowski T, Konturek PC, Konturek SJ, Brzozowska I, Pawlik T. Role of prostaglandins in gastroprotection and adaptation. J Physiol Pharmacol 2005; 56, Suppl. 5: 75-88.
50. Whittle BJR, Lopez-Belmonte J, Moncada S. Regulation of gastric mucosal integrity by endogenous nitric oxide: interactions with prostanoids and sensory neuropeptides in the rat. Br J Pharmacol 1990; 99: 607-11.
51. Brzozowski T. Experimental production of peptic ulcer, gastric damage and cancer models and their use in pathophysiological studies and pharmacological treatment - Polish achievements. J Physiol Pharmacol 2003; 54 suppl. 3: 99-126.
52. Serhan CN. Lipoxins and novel aspirin-triggered 15-epi-lipoxins (ATL): a jungle of cell-cell interactions or a therapeutic opportunity? Prostaglandins 1997; 53: 107-37.
53. Chiang N, Fierro IM, Gronert K, Serhan CN. Activation of lipoxin A(4) receptors by aspirin-triggered lipoxins and select peptides evokes ligand-specific responses in inflammation. J Exp Med 2000; 191: 1197-208.
54. Serhan CN. Lipoxins and aspirin-triggered 15-epilipoxin biosynthesis: an update and role in anti-inflammation and pro-resolution. Prostaglandins Other Lipid Mediat 2002; 68-69: 433-55.
55. Chiang N, Gronert K, Clish CB, O'Brien JA, Freeman MW, Serhan CN. Leukotriene B4 receptor transgenic mice reveal novel protective roles for lipoxins and aspirin-triggered lipoxins in reperfusion. J Clin Invest 1999; 104: 309-16.
56. Serhan CN, Takano T, Chiang N, Gronert K, Clish CB. Formation of endogenous "anti-inflammatory" lipid mediators by transcellular biosynthesis. Lipoxins and aspirin-triggered lipoxins inhibit neutrophil recruitment and vascular permeability. Am J Respir Crit Care Med 2000; 161: S95-101.
57. von der Weid PY, Hollenberg MD, Fiorucci S, Wallace JL. Aspirin- triggered, cyclooxygenase-2-dependent lipoxin synthesis modulates vascular tone. Circulation 2004; 110: 1320-5.
58. Wallace JL, Bak A, McKnight W, Asfaha S, Sharkey KA, Mac- Naughton WK. Cyclooxygenase-1 contributes to inflammatory responses in rats and mice: implications for GI toxicity. Gastroenterology 1998; 115: 101-9.
59. Warner TD, Giuliano F, Vojnovic I., Bukasa A., Mitchell JA., Vane JR. Nonsteroid drug selectivity for cyclo-oxygenase-1 rather than cyclo-oxygenase-2 are associated with human gastrointestinal toxicity: a full in vitro analysis. Proc Natl Acad Sci 1999; 96: 7563- 8.
60. Wallace JL, de Lima OM., Fiorucci S. Lipoxins in gastric mucosal health and disease. Prostaglandins Leukot Essent Fatty Acids 2005; 73: 251-5.
61. Serhan CN, Maddox JF, Petasis NA, et al. Design of lipoxin A4 stable analogs that block transmigration and adhesion of human neutrophils. Biochemistry 1995; 34: 14609-15.
62. Ohira T, Bannenberg G, Arita M, et al. A stable aspirin-triggered lipoxin A4 analog blocks phosphorylation of leukocyte-specific protein 1 in human neutrophils. J Immunol 2004; 173: 2091-8.
63. Brzozowski T, Konturek PC, Pajdo R, et al. Physiological mediators in non-steroidal anti-inflammatory drugs (NSAIDs) - induced impairment of gastric mucosal defense and adaptation Focus on nitric oxide and lipoxins. J Physiol Pharmacol 2008; 59 Suppl 2: 89- 102.
64. Perretti M, Chiang N, La M, et al. Endogenous lipid - and peptidederived anti-inflammatory pathways generated with glucocorticoid and aspirin treatment activate the lipoxin A4 receptor. Nature Med 2002: 1296-302.
65. Martin GR, Perretti M, Flower RJ, Wallace JL. Annexin-1 modulates gastric mucosal healing. Am J Physiol Gastrointest Liver Physiol 2008; 294: G764-9.
66. Hawkey CJ, Tullassay Z, Szczepanski L, et al. Randomized controlled trial of Helicobacter pylori eradication in patients on nonsteroidal anti-inflammatory drugs: HELP NSAIDs study. Helicobacter eradication for lesion prevention. Lancet 1998; 352: 1016-21.
67. Brzozowski T, Konturek PC, Sliwowski Z, et al. Interaction of nonsteroidal anti-inflammatory drugs (NSAID) with Helicobacter pylori in the stomach of humans and experimental animals. J Physiol Pharmacol 2006, 57 suppl. 3: 67-79.
68. Konturek JW, Dembinski A, Konturek SJ, Stachura J, Domschke W. Infection of Helicobacter pylori in gastric adaptation to continued administration of aspirin in humans. Gastroenterology 1998; 114: 245-55.
69. Souza MH, de Lima OM., Zamuner SR, Fiorucci S, Wallace JL. Gastritis increases resistance to aspirin-induced mucosal injury via COX-2-mediated lipoxin synthesis. Am J Physiol Gastrointestinal Liver Physiol. 2003; 285: 54-61.
70. Brzozowski T, Konturek PC, Konturek SJ, et al. Gastroprotective and ulcer healing effects of nitric oxide-releasing nonsteroidal antiinflammatory drugs. Dig Liver Dis 2000; 3: 583-94.
71. Brzozowska I, Targosz A, Sliwowski Z, et al. Healing of chronic gastric ulcers in diabetic rats treated with native aspirin, nitric oxide (NO)-derivative of aspirin and cyclooxygenase COX)-2 inhibitor. J Physiol Pharmacol 2004; 55: 773-90.
72. Fiorucci S, Del Soldato P. NO-aspirin: mechanism of action and gastrointestinal safety. Dig Liv Dis 2003; 35 (suppl 2): S9-19.
73. Fiorucci S, Distrutti E, Menezes de Lima O, et al. Relative contribution of acetylated cyclooxygenase (COX)-2 and 5-lipooxygenase (LOX) in regulating gastric mucosal integrity and adaptation to aspirin. FASEB J 2003; 17: 1171-3.
74. Wallace JL. Nitric oxide, aspirin-triggered lipoxins and NO-aspirin in gastric protection. Inflamm Allergy Drug Targets 2006; 5: 133-7.
75. Fiorucci S, Di Lorenzo A, Renga B, Farneti S, Morelli A, Cirino G. Nitric oxide (NO)-releasing naproxen (HCT-3012 [(S)-6-methoxyalpha-methyl-2-naphthaleneacetic Acid 4-(nitrooxy)butyl ester]) interactions with aspirin in gastric mucosa of arthritic rats reveal a role for aspirin-triggered lipoxin, prostaglandins, and NO in gastric protection. J Pharmacol Exp Ther 2004; 311: 1264-71.
76. Fiorucci S, Santucci L, Wallace JL, et al. Interaction of a selective cyclooxygenase-2 inhibitor with aspirin and NO-releasing aspirin in the human gastric mucosa. Proc Natl Acad Sci USA 2003; 100: 10937-41.
77. Grosser N, Abate A, Oberle S, et al. Heme oxygenase-1 induction may explain the antioxidant profile of aspirin. Biochem Biophys Res Commun 2003; 308: 956-60.
78. Nascimento-Silva V, Arruda MA, Barja-Fidalgo C, Villela CG, Fierro IM. Novel lipid mediator aspirin-triggered lipoxin A4 induces heme oxygenase-1 in endothelial cells. Am J Physiol Cell Physiol 2005; 289: C557-63.
79. Grosser N, Hemmerle A, Berndt G, et al. The antioxidant defense protein heme oxygenase-1 is a novel target for statins in endothelial cells. Free Radic Biol Med 2004; 37: 2064-71.
80. Cezar-de-Mello PF, Vieira AM, Nascimento-Silva V, Villela CG, Barja-Fidalgo C, Fierro IM. ATL-1, an analogue of aspirintriggered lipoxin A4 is a potent inhibitor of several steps in angiogenesis induced by vascular endothelial growth factor. Br J Pharmacol 2008; 153: 956-65.
81. Cezar-de-Mello PF, Nascimento-Silva V, Villela CG, Fierro IM. Aspirin-triggered Lipoxin A4 inhibition of VEGF-induced endothelial cell migration involves actin polymerization and focal adhesion assembly. Oncogene 2006; 25: 122-9.
82. Spite M, Serhan CN. Novel lipid mediators promote resolution of acute inflammation: impact of aspirin and statins. Circ Res 2010; 107: 1170-84.
83. Serhan CN, Krishnamoorthy S, Recchiuti A, Chiang N. Novel antiinflammatory-pro-resolving mediators and their receptors. Curr Top Med Chem 2011; Jan 25 (ahead of print).
84. Hirohata M, Ono K, Yamada M. Non-steroidal anti-inflammatory drugs as anti-amyloidogenic compounds. Curr Pharm Des 2008; 14: 3280-94.
85. Menna C, Olivieri F, Catalano A, Procopio A. Lipoxygenase inhibitors for cancer prevention: promises and risks. Curr Pharm Des 2010; 16: 725-33.