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Resolution of mucosal inflammation

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The Resolution of Inflammation

Part of the book series: Progress in Inflammation Research ((PIR))

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Abstract

Inflammation of the mucosal lining of the gastrointestinal tract is not only common, it is often described as ‘normal’. This is particularly the case in the intestine, where a single layer of epithelial cells separates the vascular and immune systems from billions of microbes. Of course, uncontrolled inflammation is also associated with a number of gastrointestinal disorders, some of which are quite common. Many of the current therapies for disease such as inflammatory bowel disease (IBD) are aimed at bringing the inflammatory response under control, by inhibiting production or action of pro-inflammatory mediators, so that repair of tissue injury can proceed. In recent years, there has been increasing interest in the notion that better understanding the endogenous mechanisms for resolution of inflammation will provide important clues for the design of more effective therapies for inflammatory diseases.

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References

  1. Vane JR (1971) Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat New Biol 231: 232–235

    PubMed  CAS  Google Scholar 

  2. Wallace JL, Granger DN (1996) The cellular and molecular basis of gastric mucosal defense. FASEB J 10: 731–740

    PubMed  CAS  Google Scholar 

  3. Xie W, Chipman JG, Robertson DL, Erikson RL, Simmons DL (1991) Expression of a mitogen-responsive gene encoding prostaglandin synthase is regulated by mRNA splicing. Proc Natl Acad Sci USA 88: 2692–2696

    Article  PubMed  CAS  Google Scholar 

  4. Vane JR, Mitchell JA, Appleton I, Tomlinson A, Bishop-Bailey D, Croxtall J, Willoughby DA (1994) Inducible isoforms of cyclooxygenase and nitric-oxide synthase in inflammation. Proc Natl Acad Sci USA 91: 2046–2050

    Article  PubMed  CAS  Google Scholar 

  5. Silverstein FE, Faich G, Goldstein JL, Simon LS, Pincus T, Whelton A, Makuch R, Eisen G, Agrawal NM, Stenson WF et al (2000) Gastrointestinal toxicity with celecoxib vs nonsteroidal anti-inflammatory drugs for osteoarthritis and rheumatoid arthritis: The CLASS study: A randomized controlled trial. Celecoxib Long-term Arthritis Safety Study. JAMA 284: 1247–1255

    Article  PubMed  CAS  Google Scholar 

  6. Hippisley-Cox J, Coupland C, Logan R (2005) Risk of adverse gastrointestinal outcomes in patients taking cyclo-oxygenase-2 inhibitors or conventional non-steroidal anti-inflammatory drugs: Population based nested case-control analysis. BMJ 331: 1310–1316

    Article  PubMed  CAS  Google Scholar 

  7. Fitzgerald GA (2004) Coxibs and cardiovascular disease. N Engl J Med 351: 1709–1711

    Article  PubMed  CAS  Google Scholar 

  8. Reuter BK, Asfaha S, Buret A, Sharkey KA, Wallace JL (1996) Exacerbation of inflammation-associated colonic injury in rat through inhibition of cyclooxygenase-2. J Clin Invest 98: 2076–2085

    Article  PubMed  CAS  Google Scholar 

  9. Wallace JL, Keenan CM, Gale D, Shoupe TS (1992) Exacerbation of experimental colitis by NSAIDs is not related to elevated leukotriene B4 synthesis. Gastroenterology 102: 18–27

    PubMed  CAS  Google Scholar 

  10. Ajuebor MN, Singh A, Wallace JL (2000) Cyclooxygenase-2-derived prostaglandin D2 is an early, anti-inflammatory signal in experimental colitis. Am J Physiol 279: G238–G244

    CAS  Google Scholar 

  11. Wallace JL, Bak A, McKnight W, Asfaha S, Sharkey KA, MacNaughton WK (1998) Cyclooxygenase-1 contributes to inflammatory responses in rats and mice: Implications for GI toxicity. Gastroenterology 115: 101–109

    Article  PubMed  CAS  Google Scholar 

  12. Gilroy DW, Colville-Nash PR, Willis D, Chivers J, Paul-Clark MJ, Willoughby DA (1999) Inducible cyclooxygenase may have anti-inflammatory properties. Nat Med 5: 698–701

    Article  PubMed  CAS  Google Scholar 

  13. Serhan CN (1994) Lipoxin biosynthesis and its impact in inflammatory and vascular events. Biochim Biophys Acta 1212: 1–25

    PubMed  CAS  Google Scholar 

  14. Claria J, Serhan CN (1995) Aspirin triggers previously unrecognized bioactive eicosanoids in human endothelial cell-leukocyte interactions. Proc Natl Acad Sci USA 92: 9475–9479

    Article  PubMed  CAS  Google Scholar 

  15. Takano T, Fiore S, Maddox JF, Brady HR, Petasis NA, Serhan CN (1997) Aspirin-triggered 15-epi-lipoxin A4 (LXA4) and LXA4 stable analogues are potent inhibitors of acute inflammation: Evidence for anti-inflammatory receptors. J Exp Med 185: 1693–1704

    Article  PubMed  CAS  Google Scholar 

  16. Perretti M, Chiang N, La M, Fierro IM, Marullo S, Getting SJ, Solito E, Serhan CN (2002) Endogenous lipid-and peptide-derived anti-inflammatory pathways generated with glucocorticoid and aspirin treatment activate the lipoxin A4 receptor. Nat Med 8: 1296–1302

    Article  PubMed  CAS  Google Scholar 

  17. Serhan CN, Oliw E (2001) Unorthodox routes to prostanoid formation: New twists in cyclooxygenase-initiated pathways. J Clin Invest 107: 1481–1489

    Article  PubMed  CAS  Google Scholar 

  18. Fiorucci S, Menezes de Lima O, Mencarelli A, Palazzetti B, Distrutti E, McKnight W, Dicay M, Ma L, Romano M, Morelli A et al (2002) Cyclooxygenase-2-derived lipoxin A4 increases gastric resistance to aspirin-induced damage. Gastroenterology 123: 1598–1606

    Article  PubMed  CAS  Google Scholar 

  19. Gronert K, Gewirtz A, Madara JL, Serhan CN (1998) Identification of a human enterocyte lipoxin A4 receptor that is regulated by interleukin (IL)-13 and interferon γ and inhibits tumor necrosis factor-induced IL-8 release. J Exp Med 187: 1285–1294

    Article  PubMed  CAS  Google Scholar 

  20. Bonnans C, Fukunaga K, Levy MA, Levy BD (2006) Lipoxin A4 regulates bronchial epithelial cell responses to acid injury. Am J Pathol 168: 1064–1072

    Article  PubMed  CAS  Google Scholar 

  21. Peskar BM (1977) On the synthesis of prostaglandins by human gastric mucosa and its modification by drugs. Biochim Biophys Acta 487: 307–314

    PubMed  CAS  Google Scholar 

  22. Wallace JL (1997) Nonsteroidal anti-inflammatory drugs and gastroenteropathy: The second hundred years. Gastroenterology 112: 1000–1016

    Article  PubMed  CAS  Google Scholar 

  23. Wallace JL, Miller MJS (2000) Nitric oxide and mucosal defence: A little goes a long way. Gastroenterology 119: 512–520

    Article  PubMed  CAS  Google Scholar 

  24. Fiorucci S, Antonelli E, Distrutti E, Mencarelli A, Orlandi S, Zanardo R, Renga B, Rizzo G, Morelli A, Cirino G et al (2005) Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory nonsteroidal drugs. Gastroenterology 129: 1210–1224

    Article  PubMed  CAS  Google Scholar 

  25. Davies NM, Sharkey KA, Asfaha S, MacNaughton WK, Wallace JL (1997) Aspirin induces a rapid up-regulation of cyclooxygenase-2 expression in the rat stomach. Aliment Pharmacol Ther 11: 1101–1108

    Article  PubMed  CAS  Google Scholar 

  26. Gretzer B, Maricic N, Respondek M, Schuligoi R, Peskar BM (2001) Effects of specific inhibition of cyclo-oxygenase-1 and cyclo-oxygenase-2 in the rat stomach with normal mucosa and after acid challenge. Br J Pharmacol 132: 1565–1573

    Article  PubMed  CAS  Google Scholar 

  27. Maricic N, Ehrlich K, Gretzer B, Schuligoi R, Respondek M, Peskar BM (1999) Selective cyclooxygenase-2 inhibitors aggravate ischaemia-reperfusion injury in the rat stomach. Br J Pharmacol 128: 1659–1666

    Article  PubMed  CAS  Google Scholar 

  28. Wallace JL, McKnight W, Reuter BK, Vergnolle N (2000) NSAID-induced gastric damage in rats: Requirement for inhibition of both cyclooxygenase 1 and 2. Gastroenterology 119: 706–714

    Article  PubMed  CAS  Google Scholar 

  29. Fiorucci S, Santucci L, Wallace JL, Sardina M, Fransioli R, Romano M, del Soldato P, Morelli A (2003) Interaction of COX-2 inhibitor with aspirin and NO-aspirin in the human gastric mucosa: Evidence for a protective role of nitric oxide. Proc Natl Acad Sci USA 100: 10937–10941

    Article  PubMed  CAS  Google Scholar 

  30. Robert A, Schultz RJ, Nezamis JE, Lancaster C (1976) Gastric antisecretory and antiulcer properties of PGE2, 15-methyl PGE2, and 16,16-dimethyl PGE2. Intravenous, oral and intrajejunal administration. Gastroenterology 70: 359–370

    PubMed  CAS  Google Scholar 

  31. Souza MHLP, Menezes de Lima O, Zamuner SR, Fiorucci S, Wallace JL (2003) Gastritis increases resistance to aspirin-induced mucosal injury via COX-2-mediated lipoxin synthesis. Am J Physiol 285: G54–G61

    CAS  Google Scholar 

  32. Perretti M, Flower RJ (2004) Annexin-1 and the biology of the neutrophil. J Leukoc Biol 76: 25–29

    Article  PubMed  CAS  Google Scholar 

  33. Parente L, Solito E (2004) Annexin 1: More than an anti-phospholipase protein. Inflamm Res 53: 125–132

    Article  PubMed  CAS  Google Scholar 

  34. Ferlazzo V, D’Agostino P, Milano S, Caruso R, Feo S, Cillari E, Parente L (2003) Antiinflammatory effects of annexin-1: Stimulation of IL-10 release and inhibition of nitric oxide synthesis. Int Immunopharmacol 3: 1363–1369

    Article  PubMed  CAS  Google Scholar 

  35. Gavins FN, Yona S, Kamal AM, Flower RJ, Perretti M (2003) Leukocyte antiadhesive actions of annexin 1: ALXR-and FPR-related anti-inflammatory mechanisms. Blood 101: 4140–4147

    Article  PubMed  CAS  Google Scholar 

  36. Filaretova LP, Filaretov AA, Makara GB (1998) Corticosterone increase inhibits stress-induced gastric erosions in rats. Am J Physiol 274: G1024–G1030

    PubMed  CAS  Google Scholar 

  37. Zanardo RCO, Perretti M, Wallace JL (2005) Annexin-1 mediates the gastroprotective effects of dexamethasone against indomethacin. Am J Physiol 288: G481–G486

    CAS  Google Scholar 

  38. Podolsky DK (1997) Lessons from genetic models of inflammatory bowel disease. Acta Gastroenterol Belg 60: 163–165

    PubMed  CAS  Google Scholar 

  39. Casini-Raggi V, Kam L, Chong YJ, Fiocchi C, Pizarro TT, Cominelli F (1995) Mucosal imbalance of IL-1 and IL-1 receptor antagonist in inflammatory bowel disease. A novel mechanism of chronic intestinal inflammation. J Immunol 154: 2434–2440

    PubMed  CAS  Google Scholar 

  40. Elliott DE, Setiawan T, Metwali A, Blum A, Urban JF, Weinstock JV (2004) Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice. Eur J Immunol 34: 2690–2698

    Article  PubMed  CAS  Google Scholar 

  41. Bonner GF (2001) Exacerbation of inflammatory bowel disease associated with use of celecoxib. Am J Gastroenterol 96: 1306–1308

    Article  PubMed  CAS  Google Scholar 

  42. Matuk R, Crawford J, Abreu MT, Targan SR, Vasiliauskas EA, Papadakis KA (2004) The spectrum of gastrointestinal toxicity and effect on disease activity of selective cyclooxygenase-2 inhibitors in patients with inflammatory bowel disease. Inflamm Bowel Dis 10: 352–356

    Article  PubMed  Google Scholar 

  43. 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

    Article  PubMed  CAS  Google Scholar 

  44. Zamuner SR, Bak AW, Devchand PR, Wallace JL (2005) Predisposition to colorectal cancer in rats with resolved colitis: Role of cyclooxygenase-2-derived prostaglandin D2. Am J Pathol 167: 1293–1300

    PubMed  CAS  Google Scholar 

  45. Vergnolle N, Comera C, Bueno L (1995) Annexin 1 is overexpressed and specifically secreted during experimentally induced colitis in rats. Eur J Biochem 232:603–610

    Article  PubMed  CAS  Google Scholar 

  46. Comera C, Brousset P, More J, Vergnolle N, Bueno L (1999) Inflammatory neutrophils secrete annexin 1 during experimentally induced colitis in rats. Dig Dis Sci 44:1448–1457

    Article  PubMed  CAS  Google Scholar 

  47. Vergnolle N, Pages P, Guimbaud R, Chaussade S, Bueno L, Escourrou J, Comera C (2004) Annexin 1 is secreted in situ during ulcerative colitis in humans. Inflamm Bowel Dis 10: 584–592

    Article  PubMed  Google Scholar 

  48. Gewirtz AT, Collier-Hyams LS, Young AN, Kucharzik T, Guilford WJ, Parkinson JF, Williams IR, Neish AS, Madara JL (2002) Lipoxin A4 analogs attenuate induction of intestinal epithelial proinflammatory gene expression and reduce the severity of dextran sodium sulfate-induced colitis. J Immunol 168: 5260–5267

    PubMed  CAS  Google Scholar 

  49. Fiorucci S, Wallace JL, Mencarelli A, Distrutti E, Rizzo G, Farneti S, Morelli A, Tseng JL, Suramanyam B, Guilford WJ et al (2004) A beta-oxidation-resistant lipoxin A4 analog treats hapten-induced colitis by attenuating inflammation and immune dysfunction. Proc Natl Acad Sci USA 101: 15736–15741

    Article  PubMed  CAS  Google Scholar 

  50. Arita M, Yoshida M, Hong S, Tjonahen E, Glickman JN, Petasis NA, Blumberg RS, Serhan CN (2005) Resolvin E1, an endogenous lipid mediator derived from omega-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis. Proc Natl Acad Sci USA 102: 7671–7676

    Article  PubMed  CAS  Google Scholar 

  51. Mueller C, Macpherson A (2006) Layers of mutualism with commensal bacteria protect us from intestinal inflammation Gut 55: 276–284

    Article  PubMed  CAS  Google Scholar 

  52. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P et al (2006) Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55: 205–211

    Article  PubMed  CAS  Google Scholar 

  53. Johnson-Henry K, Nadjafi M, Avitzur Y, Mitchell D, Ngan B-Y, Galindo-Mata E, Jones NL, Sherman PM (2005) Amelioration of the effects of Citrobacter rodentium infection in mice by pretreatment with probiotics. J Infect Dis 191: 2106–2117

    Article  PubMed  Google Scholar 

  54. Kelly D, Campbell JI, King TP, Grant G, Jansson EA, Coutts AGP, Tettersson S, Conway S (2004) Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol 5: 104–112

    Article  PubMed  CAS  Google Scholar 

  55. Castaneda FE, Walia B, Vijay-Kumar M, Patel NR, Roser S, Kolachala VL, Rojas M, Wang L, Oprea G, Garg P et al (2005) Targeted deletion of metalloproteinase 9 attenuates experimental colitis in mice: Central role of epithelial-derived MMP. Gastroenterology 129: 1991–2008

    Article  PubMed  CAS  Google Scholar 

  56. Howe K, Reardon C, Wang A, Nazli A, McKay DM (2005) Transforming growth factor-beta regulation of epithelial tight junction proteins enhances barrier function and blocks enterohemorrhagic Escherichia coli O157:H7-induced increased permeability. Am J Pathol 167: 1587–1597

    PubMed  CAS  Google Scholar 

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Author information

Authors and Affiliations

  1. Inflammation Research Network, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, T2N 4N1, Canada

    John L. Wallace

  2. Hospital for Sick Children and University of Toronto, 555 University Avenue, Toronto, Ontario, M5G 1X8, Canada

    Philip M. Sherman

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  1. John L. Wallace
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  2. Philip M. Sherman
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Editors and Affiliations

  1. MRC Centre for Inflammation Research, Queen’s Medical Research Institute, University of Edinburgh, 47 Little France Crescent Edinburgh, EH16 4TJ, Scotland, UK

    Adriano G. Rossi  & Deborah A. Sawatzky  & 

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Wallace, J.L., Sherman, P.M. (2008). Resolution of mucosal inflammation. In: Rossi, A.G., Sawatzky, D.A. (eds) The Resolution of Inflammation. Progress in Inflammation Research. Birkhäuser Basel. https://doi.org/10.1007/978-3-7643-7506-5_11

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