Altered Colonic Mucosal Polyunsaturated Fatty Acid (PUFA) Derived Lipid Mediators in Ulcerative Colitis: New Insight into Relationship with Disease Activity and Pathophysiology

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Masoodi, Mojgan ^a,b,c   Pearl, Daniel S ^d,e,f   Eiden, Michael ^b   Shute, Janis K ^e   Brown, James F ^e   Calder, Philip C ^g,h   Trebble, Timothy M ^d  

^a NESTLÉ RESEARCH CENTER   (Switzerland)

^b MEDICAL RESEARCH COUNCIL   (United Kingdom)

^c UNIVERSITY OF TORONTO   (Canada)

^d PORTSMOUTH HOSPITALS NHS TRUST   (United Kingdom)

^e UNIVERSITY OF PORTSMOUTH   (United Kingdom)

^f TAUNTON AND SOMERSET HOSPITAL   (United Kingdom)

^g UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^h UNIVERSITY HOSPITAL SOUTHAMPTON NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

11 HYDROXY 5, 8, 12, 14 EICOSATETRAENOIC ACID; 12 HYDROXYICOSATETRAENOIC ACID; 15 HYDROXYICOSATETRAENOIC ACID; 5 HYDROXYICOSATETRAENOIC ACID; AGENTS AFFECTING LIPID METABOLISM; LIPID MEDIATORS; POLYUNSATURATED FATTY ACID; PROSTAGLANDIN D2; PROSTAGLANDIN E2; THROMBOXANE B2; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CASE CONTROL STUDY; COLON BIOPSY; COLON MUCOSA; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE SEVERITY; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; LIPIDOMICS; LIQUID CHROMATOGRAPHY; MAJOR CLINICAL STUDY; MALE; PATHOPHYSIOLOGY; RELAPSE; TANDEM MASS SPECTROMETRY; TISSUE LEVEL; ULCERATIVE COLITIS;

ADRENAL CORTEX HORMONES; ADULT; AMINOSALICYLIC ACIDS; ARACHIDONATE 5-LIPOXYGENASE; BIOPSY; CASE-CONTROL STUDIES; COLITIS, ULCERATIVE; FATTY ACIDS, UNSATURATED; FEMALE; HUMANS; INFLAMMATION MEDIATORS; INTESTINAL MUCOSA; LIPID METABOLISM; MALE; MIDDLE AGED; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES;

EID: 84885746110     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076532     Document Type: Article

References (59)

1. Stonnington CM, Phillips SF, Melton LJ III, Zinsmeister AR (1987) Chronic ulcerative colitis: incidence and prevalence in a community. Gut 28: 402-409.
2. Pearl DS, Shah K, Whittaker MA, Nitch-Smith H, Brown JF, et al. (2012) Cytokine mucosal expression in ulcerative colitis, the relationship between cytokine release and disease activity. J Crohns Colitis. S1873-9946(12)00333-9 [pii];10.1016/j.crohns.2012.07.022 [doi].
3. Lawson MM, Thomas AG, Akobeng AK (2006) Tumour necrosis factor alpha blocking agents for induction of remission in ulcerative colitis. Cochrane Database Syst Rev CD005112. 10.1002/14651858.CD005112.pub2 [doi].
4. Peyrin-Biroulet L, Lemann M, (2011) Review article: remission rates achievable by current therapies for inflammatory bowel disease. Aliment Pharmacol Ther 33: 870-879 10.1111/j.1365-2036.2011.04599.x [doi].
5. Jakobovits SL, Travis SP, (2005) Management of acute severe colitis. Br Med Bull 75-76: 131-144 75-76/1/131 [pii];10.1093/bmb/ldl001 [doi].
6. Langholz E, Munkholm P, Davidsen M, Binder V (1994) Course of ulcerative colitis: analysis of changes in disease activity over years. Gastroenterology 107: 3-11. S0016508594002155 [pii].
7. Langholz E, (2010) Current trends in inflammatory bowel disease: the natural history. Therap Adv Gastroenterol 3: 77-86 10.1177/1756283X10361304 [doi].
8. Geboes JK (2003) Histopathology of Crohn's disease and ulcerative colitis. In: Satsangi J, Sutherland LR, Colombel JF, Fiocci C, Lofberg R et al., editors. Inflammatory Bowel Disease. Edinburgh, London, Melbourne: Churchill Livingstone. 255-276.
9. Geboes K, Riddell R, Ost A, Jensfelt B, Persson T, et al. (2000) A reproducible grading scale for histological assessment of inflammation in ulcerative colitis. Gut 47: 404-409.
10. Azad S, Sood N, Sood A, (2011) Biological and histological parameters as predictors of relapse in ulcerative colitis: a prospective study. Saudi J Gastroenterol 17: 194-198 SaudiJGastroenterol_2011_17_3_194_80383 [pii];10.4103/1319-3767.80383 [doi].
11. Nielsen OH, Elmgreen J, (1987) Activation of neutrophil chemotaxis by leukotriene B4 and 5-hydroxyeicosatetraenoic acid in chronic inflammatory bowel disease. Scand J Clin Lab Invest 47: 605-611.
12. Palmblad J, (1984) The role of granulocytes in inflammation. Scand J Rheumatol 13: 163-172.
13. Marteau P, Probert CS, Lindgren S, Gassul M, Tan TG, et al. (2005) Combined oral and enema treatment with Pentasa (mesalazine) is superior to oral therapy alone in patients with extensive mild/moderate active ulcerative colitis: a randomised, double blind, placebo controlled study. Gut 54: 960-965 54/7/960 [pii];10.1136/gut.2004.060103 [doi].
14. Sutherland L, Roth D, Beck P, May G, Makiyama K (2000) Oral 5-aminosalicylic acid for inducing remission in ulcerative colitis. Cochrane Database Syst Rev CD000543. CD000543 [pii];10.1002/14651858.CD000543 [doi].
15. Funk CD, (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294: 1871-1875 10.1126/science.294.5548.1871 [doi];294/5548/1871 [pii].
16. Jupp J, Hillier K, Elliott DH, Fine DR, Bateman AC, et al. (2007) Colonic expression of leukotriene-pathway enzymes in inflammatory bowel diseases. Inflamm Bowel Dis 13: 537-546 10.1002/ibd.20094 [doi].
17. Rampton DS, Sladen GE, Youlten LJ, (1980) Rectal mucosal prostaglandin E2 release and its relation to disease activity, electrical potential difference, and treatment in ulcerative colitis. Gut 21: 591-596.
18. Sharon P, Stenson WF (1984) Enhanced synthesis of leukotriene B4 by colonic mucosa in inflammatory bowel disease. Gastroenterology 86: 453-460. S0016508584000500 [pii].
19. Lee TH, Sethi T, Crea AE, Peters W, Arm JP, et al. (1988) Characterization of leukotriene B3: comparison of its biological activities with leukotriene B4 and leukotriene B5 in complement receptor enhancement, lysozyme release and chemotaxis of human neutrophils. Clin Sci (Lond) 74: 467-475.
20. Needleman P, Raz A, Minkes MS, Ferrendelli JA, Sprecher H, (1979) Triene prostaglandins: prostacyclin and thromboxane biosynthesis and unique biological properties. Proc Natl Acad Sci U S A 76: 944-948.
21. Turner D, Steinhart AH, Griffiths AM (2007) Omega 3 fatty acids (fish oil) for maintenance of remission in ulcerative colitis. Cochrane Database Syst Rev CD006443. 10.1002/14651858.CD006443.pub2 [doi].
22. Calder PC, (2008) Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases. Mol Nutr Food Res 52: 885-897 10.1002/mnfr.200700289 [doi].
23. D'Haens GR, Panaccione R, Higgins PD, Vermeire S, Gassull M, et al. (2011) The London Position Statement of the World Congress of Gastroenterology on Biological Therapy for IBD with the European Crohn's and Colitis Organization: when to start, when to stop, which drug to choose, and how to predict response? Am J Gastroenterol 106: 199-212 ajg2010392 [pii];10.1038/ajg.2010.392 [doi].
24. Gomes P, du BC, Smith CL, Holdstock G, (1986) Relationship between disease activity indices and colonoscopic findings in patients with colonic inflammatory bowel disease. Gut 27: 92-95.
25. Sutherland LR, Martin F, Greer S, Robinson M, Greenberger N, et al. (1987) 5-Aminosalicylic acid enema in the treatment of distal ulcerative colitis, proctosigmoiditis, and proctitis. Gastroenterology 92: 1894-1898. S0016508587001811 [pii].
26. Masoodi M, Eiden M, Koulman A, Spaner D, Volmer DA, (2010) Comprehensive lipidomics analysis of bioactive lipids in complex regulatory networks. Anal Chem 82: 8176-8185 10.1021/ac1015563 [doi].
27. Jansen JJ, Hoefsloot HC, van der Greef J, Timmerman ME, Westerhuis JA, et al. (2006) ASCA: analysis of multivariate data obtained from an experimental design. J Chemometrics 19: 469-481.
28. van Velzen EJ, Westerhuis JA, van Duynhoven JP, van Dorsten FA, Hoefsloot HC, et al. (2008) Multilevel data analysis of a crossover designed human nutritional intervention study. J Proteome Res 7: 4483-4491 10.1021/pr800145j [doi].
29. Boughton-Smith NK, Hawkey CJ, Whittle BJ, (1983) Biosynthesis of lipoxygenase and cyclo-oxygenase products from [14C]-arachidonic acid by human colonic mucosa. Gut 24: 1176-1182.
30. Gould SR, (1976) Assay of prostaglandin-like substances in faeces and their measurement in ulcerative colitis. Prostaglandins 11: 489-497.
31. Rampton DS, Sladen GE, Youlten LJ, (1980) Prostaglandins and ulcerative colitis. Gastroenterology 78: 192-193.
32. Vong L, Ferraz JG, Panaccione R, Beck PL, Wallace JL, (2010) A pro-resolution mediator, prostaglandin D(2), is specifically up-regulated in individuals in long-term remission from ulcerative colitis. Proc Natl Acad Sci U S A 107: 12023-12027 1004982107 [pii];10.1073/pnas.1004982107 [doi].
33. Levy BD, Clish CB, Schmidt B, Gronert K, Serhan CN, (2001) Lipid mediator class switching during acute inflammation: signals in resolution. Nat Immunol 2: 612-619 10.1038/89759 [doi];89759 [pii].
34. Vachier I, Chanez P, Bonnans C, Godard P, Bousquet J, et al. (2002) Endogenous anti-inflammatory mediators from arachidonate in human neutrophils. Biochem Biophys Res Commun 290: 219-224 10.1006/bbrc.2001.6155 [doi];S0006291X01961558 [pii].
35. Palmer RM, Stepney RJ, Higgs GA, Eakins KE, (1980) Chemokinetic activity of arachidonic and lipoxygenase products on leuocyctes of different species. Prostaglandins 20: 411-418.
36. Turner SR, Tainer JA, Lynn WS, (1975) Biogenesis of chemotactic molecules by the arachidonate lipoxygenase system of platelets. Nature 257: 680-681.
37. Borgeat P, Samuelsson B, (1979) Arachidonic acid metabolism in polymorphonuclear leukocytes: unstable intermediate in formation of dihydroxy acids. Proc Natl Acad Sci U S A 76: 3213-3217.
38. Borgeat P, Samuelsson B, (1979) Metabolism of arachidonic acid in polymorphonuclear leukocytes. Structural analysis of novel hydroxylated compounds. J Biol Chem 254: 7865-7869.
39. Ford-Hutchinson AW, Bray MA, Doig MV, Shipley ME, Smith MJ, (1980) Leukotriene B, a potent chemokinetic and aggregating substance released from polymorphonuclear leukocytes. Nature 286: 264-265.
40. Shimizu T, Fujii T, Suzuki R, Igarashi J, Ohtsuka Y, et al. (2003) Effects of highly purified eicosapentaenoic acid on erythrocyte fatty acid composition and leukocyte and colonic mucosa leukotriene B4 production in children with ulcerative colitis. J Pediatr Gastroenterol Nutr 37: 581-585.
41. Rask-Madsen J, Bukhave K, Laursen LS, Lauritsen K (1992) 5-Lipoxygenase inhibitors for the treatment of inflammatory bowel disease. Agents Actions Spec No: C37-C46.
42. Pearl DS, Masoodi M, Eiden M, Brummer J, Gullick D, et al. (2013) Altered colonic mucosal availability of n-3 and n-6 polyunsaturated fatty acids in ulcerative colitis and the relationship to disease activity. J Crohns Colitis. S1873-9946(13)00137-2 [pii];10.1016/j.crohns.2013.03.013 [doi].
43. Lobos EA, Sharon P, Stenson WF, (1987) Chemotactic activity in inflammatory bowel disease. Role of leukotriene B4. Dig Dis Sci 32: 1380-1388.
44. Ikehata A, Hiwatashi N, Kinouchi Y, Yamazaki H, Ito K, et al. (1995) Altered leukotriene B4 metabolism in colonic mucosa with inflammatory bowel disease. Scand J Gastroenterol 30: 44-49.
45. Gertner DJ, Rampton DS, Madden MV, Talbot IC, Nicholls RJ, et al. (1994) Increased leukotriene B4 release from ileal pouch mucosa in ulcerative colitis compared with familial adenomatous polyposis. Gut 35: 1429-1432.
46. Eliakim R, Karmeli F, Chorev M, Okon E, Rachmilewitz D, (1992) Effect of drugs on colonic eicosanoid accumulation in active ulcerative colitis. Scand J Gastroenterol 27: 968-972.
47. Cole AT, Pilkington BJ, McLaughlan J, Smith C, Balsitis M, et al. (1996) Mucosal factors inducing neutrophil movement in ulcerative colitis: the role of interleukin 8 and leukotriene B4. Gut 39: 248-254.
48. Casellas F, Papo M, Guarner F, Antolin M, Segura RM, et al. (1995) Effects of thromboxane synthase inhibition on in vivo release of inflammatory mediators in chronic ulcerative colitis. Eur J Gastroenterol Hepatol 7: 221-226.
49. Harizi H, Juzan M, Moreau JF, Gualde N, (2003) Prostaglandins inhibit 5-lipoxygenase-activating protein expression and leukotriene B4 production from dendritic cells via an IL-10-dependent mechanism. J Immunol 170: 139-146.
50. Carty E, De BM, Feakins RM, Rampton DS, (2000) Measurement of in vivo rectal mucosal cytokine and eicosanoid production in ulcerative colitis using filter paper. Gut 46: 487-492.
51. Gilroy DW, Colville-Nash PR, Willis D, Chivers J, Paul-Clark MJ, et al. (1999) Inducible cyclooxygenase may have anti-inflammatory properties. Nat Med 5: 698-701 10.1038/9550 [doi].
52. Ajuebor MN, Singh A, Wallace JL, (2000) Cyclooxygenase-2-derived prostaglandin D(2) is an early anti-inflammatory signal in experimental colitis. Am J Physiol Gastrointest Liver Physiol 279: G238-G244.
53. Rajakariar R, Hilliard M, Lawrence T, Trivedi S, Colville-Nash P, et al. (2007) Hematopoietic prostaglandin D2 synthase controls the onset and resolution of acute inflammation through PGD2 and 15-deoxyDelta12 14 PGJ2. Proc Natl Acad Sci U S A 104: 20979-20984 0707394104 [pii];10.1073/pnas.0707394104 [doi].
54. Zamuner SR, Warrier N, Buret AG, MacNaughton WK, Wallace JL, (2003) Cyclooxygenase 2 mediates post-inflammatory colonic secretory and barrier dysfunction. Gut 52: 1714-1720.
55. Trebble TM, Arden NK, Wootton SA, Calder PC, Mullee MA, et al. (2004) Fish oil and antioxidants alter the composition and function of circulating mononuclear cells in Crohn disease. Am J Clin Nutr 80: 1137-1144. 80/5/1137 [pii].
56. Trebble TM, Wootton SA, Miles EA, Mullee M, Arden NK, et al. (2003) Prostaglandin E2 production and T cell function after fish-oil supplementation: response to antioxidant cosupplementation. Am J Clin Nutr 78: 376-382.
57. Hawthorne AB, Daneshmend TK, Hawkey CJ, Belluzzi A, Everitt SJ, et al. (1992) Treatment of ulcerative colitis with fish oil supplementation: a prospective 12 month randomised controlled trial. Gut 33: 922-928.
58. Ananthakrishnan AN, Higuchi LM, Huang ES, Khalili H, Richter JM, et al. (2012) Aspirin, nonsteroidal anti-inflammatory drug use, and risk for Crohn disease and ulcerative colitis: a cohort study. Ann Intern Med 156: 350-359 156/5/350 [pii];10.1059/0003-4819-156-5-201203060-00007 [doi].
59. D'Haens G, Sandborn WJ, Feagan BG, Geboes K, Hanauer SB, et al. (2007) A review of activity indices and efficacy end points for clinical trials of medical therapy in adults with ulcerative colitis. Gastroenterology 132: 763-786 S0016-5085(06)02688-6 [pii];10.1053/j.gastro.2006.12.038 [doi].