Lipoxins: Pro-resolution lipid mediators in intestinal inflammation

Gastroenterology

Volumn 124, Issue 4, 2003, Pages 1043-1054

  Goh, Jason ^a   Godson, Catherine ^b   Brady, Hugh R ^b   MacMathuna, Padraic ^b  

^a SELLY OAK HOSPITAL   (United Kingdom)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; ASPIRIN TRIGGERED LIPOXIN; ASPIRIN TRIGGERED LIPOXIN DERIVATIVE; CELL RECEPTOR; CHEMOKINE; CYCLOOXYGENASE 2; ICOSANOID; LIPOXIN; LIPOXIN A; LIPOXIN A DERIVATIVE; LIPOXIN B; LIPOXIN DERIVATIVE; LIPOXIN RECEPTOR; NONSTEROID ANTIINFLAMMATORY AGENT; PROSTAGLANDIN SYNTHASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; BIOAVAILABILITY; BIOSYNTHESIS; CELL ADHESION; CELL INTERACTION; CELL PROTECTION; CELL TRANSPORT; DIGESTIVE SYSTEM CANCER; DIGESTIVE SYSTEM INFLAMMATION; DRUG EFFICACY; DRUG POTENCY; ENTERITIS; EPITHELIUM CELL; EXPERIMENTAL MODEL; HUMAN; ICOSANOID METABOLISM; INFLAMMATION; INTESTINE CELL; INTESTINE EPITHELIUM; LEUKOCYTE; MEDIATOR; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 0037379738     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/gast.2003.50154     Document Type: Review

References (113)

1. Wilks and Moxon. Lectures on pathological anatomy. 2nd ed. Philadelphia: Lindsay and Blakiston, 1932.
2. Crohn BB, Ginzburg L, Oppenheimer GD. Regional ileitis: a pathological and clinical entity. JAMA 1932;99:1323-1329.
3. Sands BE. Therapy of inflammatory bowel disease. Gastroenterology 2000;118:S68-S82.
4. Shanahan F. Inflammatory bowel disease: immunogenetics, immunotherapeutics, and ecotherapeutics. Gastroenterology 2001;120:622-635.
5. Fiocchi C. Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology 1998;115:182-205.
6. O'Farrelly C. Just how inflamed is the normal gut? Gut 1998;42: 603-604.
7. Sartor RB. Role of the enteric microflora in the pathogenesis of intestinal inflammation and arthritis. Aliment Pharmacol Ther 1997;11(suppl 3):17-22.
8. Madara JL. Pathobiology of neutrophil interaction with intestinal epithelia (review). Aliment Pharmacol Ther 1997;11(suppl 3): 57-62.
9. Grisham MB, Kvietys P. Role of neutrophils in the pathogenesis of inflammatory bowel disease. In: Allan RN, Rhodes JM, Hanauer SB, Keighley MRB, Alexander-Williams J, Fazio VW, eds. Inflammatory bowel disease. 3rd ed. New York: Churchill Livingston, 1997:73-80.
10. Serhan CN. Lipoxin biosynthesis and its impact in inflammatory and vascular events. Biochim Biophys Acta 1994;1212:1-25.
11. Schreiber S, Heinig T, Thiele HG, Raedler A. Immunoregulatory role of interleukin 10 in patients with inflammatory bowel disease. Gastroenterology 1995;108:1434-1444.
12. Casini-Raggi V, Kam L, Chong YJ, Fiocchi C, Pizarro TT, Cominelli F. Mucosal imbalance of IL-1 and IL-1 receptor antagonist in inflammatory mechanism of chronic intestinal inflammation. J Immunol 1995;154:2343-2340.
13. Savill J, Fadok V. Corpse clearance defines the meaning of cell death. Nature 2000;407:784-788.
14. Serhan CN, Lipoxins and novel aspirin-triggered 15-epi-lipoxins (ATL): a jungle of cell-cell interactions or a therapeutic opportunity? Prostaglandins 1997;53:107-137.
15. McMahon B, Mitchell S, Brady HR, Godson C. Lipoxins: revelations on resolution. Trends Pharmacol Sci 2001;22:391-395.
16. Godson C, Brady HR. Lipoxins: novel antiinflammatory therapeutics? Curr Opin Invest Drugs 2000;1:380-385.
17. Gewirtz AT, Madara JL. Lipoxin stable analogs: potential therapeutic downregulators of intestinal inflammation. Ernst Schering Res Found Workshop 2000;31:187-199.
18. 4 receptor that is regulated by interleukin (IL)-13 and interferon gamma and inhibits tumor necrosis factor α-induced IL-8 release. J Exp Med 1998;187:1285-1294.
19. 4 antagonize TNF-α-stimulated neutrophil-enterocyte interactions in vitro and attenuate TNF-α-induced chemokine release and colonocyte apoptosis in human intestinal mucosa ex vivo. J Immunol 2001;167:2772-2780.
20. 4 by platelet 12-lipoxygenase in vitro. J Clin Invest 1990;85:772-780.
21. Romano M, Chen S-X, Takahashi Y, Yamamoto S, Funk CD, Serhan CN. Lipoxin synthase activity of human platelet 12-lipoxygenase. Biochem J 1993;296:127-133.
22. Fiore S, Serhan CN. Formation of lipoxins and leukotrienes during receptor-mediated interactions of human platelets and recombinant human granulocyte/macrophage colony-stimulating factor-primed neutrophils. J Exp Med 1990;172;1451-1457.
23. Claria J, Serhan CN. Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions. Proc Natl Acad Sci U S A 1995;92:9475-9479.
24. Kim SJ, Tominaga T. Formation of lipoxins by the brain. Ann N Y Acad Sci 1989;559:461-464.
25. Papayianni A, Serhan CN, Philips ML, Rennke HG, Brady HR. Transcellular biosynthesis of lipoxin A during adhesion of platelets and neutrophils in experimental immune complex glomerulonephritis. Kidney Int 1995;47:1295-1302.
26. Sanak M, Levy BD, Clish CB, Chiang N, Gronert K, Mastalerz L, Serhan CN, Szczeklik A. Aspirin-tolerant asthmatics generate more Lipoxins than aspirin-intolerant asthmatics. Eur Respir J 2000;16:44-49.
27. Lee TH, Crea AEG, Spur BW, Marron BE, Nicolaou KC, Reardon E, Brezinski M, Serhan CN. Identification of lipoxin A and its relationship to the sulphidopeptide leukotrienes C4, D4, and E4 in the brochoalveolar lavage fluids obtained from patients with selected pulmonary diseases. Am Rev Respir Dis 1990;141: 1453-1460.
28. Edenius C, Kumlin M, Bjork T, Anggard A, Lindgren JA. Lipoxin formation in human nasal polyps and bronchial tissue. FEBS Lett 1990;272:25-31.
29. Levy BD, Clish CB, Schmidt B, Gronert K, Serhan CN. Lipid mediator class switching during acute inflammation: signals in resolution. Nat Immunol 2001;2:612-619.
30. 4: impact of aspirin therapy. Circulation 1992;86:56-63.
31. 4 analogues inhibit leukocyte recruitment to Polyphyromonas gingivalis: a role for cyclooxygenase-2 and lipoxins in periodontal disease. Biochemistry 2000;39:4761-4768.
32. 4 ELISA. J Pharmacol Exp Ther 1998;287:779-790.
33. 4 ELISA. Adv Exp Med Biol 1997;400B:611-615.
34. 4 metabolism by differentiated HL-60 cells and human monocytes: conversion to novel 15-oxo and dihydro products. Biochemistry 1993;32:6313-6319.
35. 4 are potent stimuli for human monocyte migration and adhesion: selective inactivation by dehydrogenation and reduction. J Exp Med 1996;183:137-146.
36. 4 metabolic inactivation: a novel role for 15-oxoprostaglandin 13-reductase/leukotriene B 120hydroxydehydrogenase in inflammation. J Biol Chem 2000;275:25372-25380.
37. 4. Eur J Biochem 1994;224: 959-965.
38. 4 stable analogs that block transmigration and adhesion of human neutrophils. Biochemistry 1995;34:14609-146145.
39. Clish CB, Gronert K, Serhan CN. Local and systemic delivery of an aspirin-triggered lipoxin stable analog inhibit neutrophil trafficking. Ann N Y Acad Sci 2000;905:274-278.
40. 4 stable analogs inhibit neutrophil-mediated changes in vascular permeability. Adv Exp Med Biol 1999;469:287-293.
41. Weiss SJ. Tissue destruction by neutrophils. N Engl J Med 1989;320:365-376.
42. Godson C, Mitchell S, Harvey K, Petasis NA, Hogg N, Brady HR. Cutting edge: Lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J Immunol 2000;164:1663-1667.
43. 4 block allergen-induced eosinophil trafficking. J Immunol 2000;164:2261-2271.
44. O'Meara YM, Brady HR. Lipoxins, leukocyte recruitment and the resolution phase of acute glomerulonephritis. Kidney Int 1997; 51(suppl 58):S56-S61.
45. 4 receptor. J Biol Chem 1997;272:6972-6978.
46. Papayianni A, Serhan CN, Brady HR. Lipoxins inhibit leukotrienestimulated interactions of human neutrophils and endothelial cells. J Immunol 1996;156:2264-2272.
47. 4 and N-formyl-L-methionyl-L-leucyl-L-phenylalanine. Clin Sci 1989;77:195-203.
48. 4 stable analogs are demonstrable in human whole blood: modulation of leukocyte adhesion molecules and inhibition of neutrophil-endothelial interactions. Blood 1999;94:4132-4142.
49. 4 inhibit tumor necrosis factor 1-αinitiated neutrophil responses and trafficking: regulators of a cytokine-chemokine axis. J Exp Med 1999;189:1923-1929.
50. Hedqvist P, Raud J, Palmertz J, Haeggstrom J, Nicolaou KC, Dahlen S-E. Lipoxin A inhibits leukotriene B-induced inflammation in the hamster cheek pouch. Acta Physiol Scand 1989;137: 571-581.
51. 4 is protective in experimental ischemic acute renal failure. J Am Soc Nephol 2002;13:1657-1662.
52. 4 is protective in experimental renal ischemia reperfusion injury. J Am Soc Nephrol 2000;11:A3167.
53. Pouliot M, Clish CB, Petasis NA, Van Dyke TE, Serhan CN. Lipoxin A analogues inhibit leukocyte recruitment to Polyphyromonas gingivalis: a role for cyclooxygenase-2 and lipoxins in periodontal disease. Biochemistry 2000;39:4761-4768.
54. 4 receptor transgenic mice reveal novel protective roles for lipoxins and aspirin-triggered lipoxins in reperfusion. J Clin Invest 1999;104:309-316.
55. 4 and cytokine-stimulated phagocytosis of apoptotic neutrophils by bone marrow-derived macrophages: evidence for distinct regulatory pathways that may contribute to the resolution phase of inflammation. J Am Soc Nephrol 2000;11:A2282.
56. Nusrat A, Parkos CA, Liang TW, Carnes DK, Madara JL. Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair. Gastroenterology 1997;113:1489-1500.
57. Grisham MB. Oxidants and free radicals in inflammatory bowel disease. Lancet 1994;344:859-861.
58. Madara JL, Parkos C, Colgan S, MacLeod RJ, Nash S, Matthews J, Delp C, Lencer W. Chloride secretion in a model intestinal epithelium induced by a neutrophil derived secretagogue. J Clin Invest 1992;89:1938-1944.
59. 4 receptor. J Exp Med 1994;180:253-260.
60. 4 stable analogs are potent inhibitors of acute inflammation: evidence for anti-inflammatory receptors. J Exp Med 1997;185:1693-1704.
61. 4 modulates transmigration of human neutrophils across intestinal epithelial monolayers. J Clin Invest 1993;92: 75-82.
62. Colgan SP, Parkos C, Delp C, Arnaout MA, Madara JL. Neutrophil migration across cultured intestinal epithelial monolayers is modulated by epithelial exposure to IFN-γ in a highly polarized fashion. J Cell Biol 1993;120:785-798.
63. Nash S, Parkos CA, Nusrat A, Delp C, Madara JL. In vitro model of intestinal crypt abscess: a novel neutrophil-derived secretagogue activity. J Clin Invest 1991;87:1474-1477.
64. Reinecker H-C, Loh EY, Ringler DJ, Mehta A, Rombeau JL, MacDermott RP. Monocyte-chemoattractant protein 1 gene expression in intestinal epithelial cells and inflammatory bowel disease mucosa. Gastroenterology 1995;108:40-50.
65. Yang SK, Eckmann L, Panja A, Kagnoff MF. Differential and regulated expression of C-X-C, C-C and C-chemokines by human colon epithelial cells. Gastroenterology 1997;113:1214-1223.
66. Daig R, Andus T, Aschenbrenner E, Falk W, Scholmerich J, Gross V. Increased interleukin 8 expression in the colon mucosa of patients with inflammatory bowel disease. Gut 1996;38:216-222.
67. 4 analogs. J Clin Invest 1998;101:1860-1869.
68. Targan SR, Hanauer SB, van Deventer JH, Mayer L, Present DH, Braakman T, DeWoody KL, Schaible TF, Rutgeerts PJ. A short-term study of chimeric monoclonal antibody cA2 to tumor necrosis factor for Crohn's disease. N Engl J Med 1997;337: 1029-1035.
69. Blam ME, Stein RB, Lichtenstein GR. Integrating anti-tumour necrosis factor therapy in inflammatory bowel disease: current and future perspectives. Am J Gastroenterol 2001;96:1977-1997.
70. 4 inhibits IL-1β-induced IL-6, IL-8, and matrix metalloproteinase-3 production in human synovial fibroblasts and enhances synthesis of tissue inhibitors of metalloproteinases. J Immunol 2000; 164:2660-2666.
71. Canny G, Levy O, Furuta GT, Narravula-Alipati S, Sisson RB, Serhan CN, Colgan SP. Lipid mediator-induced expression of bactericidal/permeability-increasing protein BPI) in human mucosal epithelia. Proc Natl Acad Sci U S A 2002;99:3902-3907.
72. 4 analogs attenuate induction of intestinal epithelial proinflammatory gene expression and reduce the severity of dextran sodium sulfate-induced colitis. J Immunol 2002;168:5260-5267.
73. Watson RW, Rotstein OD, Nathens AB, Parodo J, Marshall JC. Neutrophil apoptosis is modulated by endothelial transmigration and adhesion molecule engagement. J Immunol 1997;158: 945-953.
74. Branigan EA, O'Connell PR, Hurley H, O'Neill A, Brady HR, Fitzpatrick JM, Watson RW. Neutrophil apoptosis is delayed in patients with inflammatory bowel disease. Shock 2000;13:361-366.
75. Hebert MJ, Takano T, Holthofer H, Brady HR. Sequential morphologic events during apoptosis of human neutrophils: modulation by lipoxygenase-derived eicosanoids. J Immunol 1996; 157:3105-3115.
76. Allison MC, Cornwall S, Poulter LW, Dhillon AP, Pounder RE. Macrophage heterogeneity in normal colonic mucosa and in inflammatory bowel disease. Gut 1988;28:1531-1538.
77. Mahida YR. The key role of macrophages in the immunopathogenesis of inflammatory bowel disease. Inflamm Bowel Dis 2000;6:21-33.
78. Mahida YR, Wu K, Patel S, Jewell DP. Respiratory burst activity of intestinal macrophages in normal and inflammatory bowel disease. Gut 1989;30:1362-1370.
79. Awtry EH, Loscalzo J. Aspirin. Circulation 2000;101:1206-1218.
80. Hawkey CJ. Nonsteroidal anti-inflammatory drugs and the gastrointestinal tract: consensus and controversy. Am J Med 2000; 110:S1-S3.
81. Dubois RN. Cyclooxygenase: a target for colon cancer prevention. Aliment Pharmacol Ther 2000;(suppl 14):64-67.
82. Felder JB, Korelitz BI, Rajapakse R, Schwarz S, Horatagis AP, Gleim G. Effects of nonsteroical anti-inflammatory drugs on inflammatory bowel disease: a case-control study. Am J Gastroenterol 2000;95:1949-1954.
83. Goh J, Wight D, Parkes M, Middleton SJ, Hunter JO. Rofecoxib and cytomegalovirus in acute flare-up of ulcerative colitis: coprecipitants or coincidence? Am J Gastroenterol 2002;97:1061.
84. Bonner GF. Exacerbation of inflammatory bowel disease associated with use of celecoxib. Am J Gastroenterol 2001;96: 1306-1308.
85. Bonner GF, Walczak M, Kitchen L, Bayona M. Tolerance of nonsteroidal anti-inflammatory drugs in patients with inflammatory bowel disease. Am J Gastroenterol 2000;95:1946-1948.
86. Mahadevan U, Loftus EV, Tremaine WJ, Sanborn WJ. Safety of selective cyclooxygenase-2 inhibitors in inflammatory bowel disease. Am J Gastroenterol 2002;97:910-914.
87. Roberts PJ, Morgan K, Miller R, Hunter JO, Middleton SJ. Neuronal COX-2 expression in human myenteric plexus in active inflammatory bowel disease. Gut 2001;48:468-472.
88. Halter F, Tarnawski AS, Schmassmann A, Peskar BM. Cyclooxygenase 2- implications on maintenance of gastric integrity and ulcer healing: controversial issues and perspectives. Gut 2001; 49:443-453.
89. Guo X, Liu ES, Ko JK, Wong BC, Ye Y, Lam S, Cho C. Protective role of cyclooxygenase inhibitors in the adverse action of passive cigarette smoking on the initiation of experimental colitis in rats. Eur J Pharmacol 2001;411:193-203.
90. Sheehan KM, Sheahan K, O'Donoghue DP, MacSweeney F, Conroy RM, Fitzgerald DJ, Murray FE. The relationship between cyclooxygenase-2 expression and colorectal cancer. JAMA 1999;282:1254-1257.
91. Morgan G, Vainio H. Barrett's oesophagus, oesophageal cancer and colon cancer: an explanation of the association and cancer chemopreventive potential of non-steroidal anti-inflammatory drugs. Eur J Cancer Prev 1998;7:195-199.
92. Souza RF, Morales CP, Spechler SJ. A conceptual approach to understanding the molecular mechanisms of cancer development in Barrett's oesophagus (review). Aliment Pharmacol Ther 2001;15:1087-1100.
93. Souza RF, Shewmake K, Beer DG, Cryer B, Spechler SJ. Selective inhibition of cyclooxygenase-2 suppresses growth and induces apoptosis in human oesophageal adenocarcinoma cells. Cancer Res 2000;60:5767-5772.
94. 4. J Pharmacol Exp Ther 2002;300: 385-392.
95. 4 in renal mesangial cells: differential activation of MAP kinases through distinct receptors. J Biol Chem 2000;275: 27566-27575.
96. Serhan CN, Clish CB, Brannon J, Colgan SP, Gronert K, Chiang N. Anti-microinflammatory lipid signals generated from dietary omega-3 fatty acids via cyclooxygenase-2 and transcellular processing: a novel mechanism for NSAID and n-3 PUFA therapeutic actions. J Physiol Pharmacol 2000;51:643-654.
97. Serhan CN, Oliw E. Unorthodox routes to prostanoid formation: new twists in cyclooxygenase-initiated pathways. J Clin Invest 2001;107:1481-1489.
98. Teitelbaum JE, Allan Walker W. The role of omega 3 fatty acids in intestinal inflammation (review). J Nutr Biochem 2001;12: 21-32.
99. Rao CV, Hirose Y, Indranie C, Reddy BS. Modulation of experimental colon tumorigenesis by types and amounts of dietary fatty acids. Cancer Res 2001;61:1927-1933.
100. Collett ED, Davidson LA, Fan YY, Lupton JR, Chapkin RS. N-6 and n-3 polyunsaturated fatty acids differentially modulate oncogenic Ras activation in colonocytes. Am J Physiol Cell Physiol 2001;280:C1066-C1075.
101. Terry P, Lichtenstein P, Feychting M, Ahlbom A, Wolk A. Fatty fish consumption and risk of prostate cancer. Lancet 2001; 357:1764-1766.
102. Harris WS, Isley WL. Clinical trial evidence of the cardioprotective effects of omega-3 fatty acids. Curr Artheroscler Rep 2001; 3:174-179.
103. Mischoulon D, Fava M. Dososahexanoic acid and omega-3 fatty acids in depression. Psychiatr Clin North Am 2000;23:785-794.
104. 4 with human neutrophils. J Biol Chem 1992;267:16168-16174.
105. 4's anti-inflammatory actions on intestinal epithelium. Am J Physiol Cell Physiol 2002;
106. 4 and regulation of vascular and inflammatory responses. Am J Pathol 2001;158:3-9.
107. 4 receptors by aspirin-triggered lipoxins and select peptides evokes ligand-specific responses in inflammation. J Exp Med 2000;191:1197-1207.
108. 4 stimulate the release but not oxygenation of arachidonic acid in human neutrophils: dissociation between lipid remodelling and adhesion. J Cell Physiol 1990;143: 512-523.
109. Van Deventer SJ. Small therapeutic molecules for the treatment of inflammatory bowel disease. Gut 2002;50(suppl 3):iii47-iii53.
110. Brady HR, Persson U, Ballermann BJ, Brenner BM, Serhan CN. Leukotrienes stimulate neutrophil adhesion to mesangial cells: modulation with lipoxins. Am J Physiol 1990;259: F809-F815.
111. Brady HR, Denton MD, Brenner BM, Sehan CN. Neutrophil adhesion to glomeruli mesangial cells: regulation by lipoxygenase-derived eicosanoids. Adv Exp Med Biol 1991;314:347-359.
112. Clarkson MR, McGinty A, Godson C, Brady HR. Leukotrienes and lipoxins: lipoxygenase-derived modulators of leukocyte recruitment and vascular tone in glomerulonephritis. Nephrol Dial Transplant 1998;13:3043-3051.
113. 4 on airway responses in asthmatic subjects. Am Rev Respir Dis 1992;145: 1281-1284.