Seminars in Immunopathology

, Volume 35, Issue 2, pp 151–161 | Cite as

Resolution of inflammation as a novel chemopreventive strategy

Review

Abstract

Acute inflammation, a physiologic response to protect cells from microbial infection and other noxious stimuli, is automatically terminated by endogenous anti-inflammatory and pro-resolving mediators to restore homeostatic conditions. However, if timely resolution of inflammation is failed, inflammation persists and can progress to a chronic inflammation which has long been thought as a predisposing factor to carcinogenesis. Excessive and pathologic inflammation causes DNA damage, genomic instability, epigenetic dysregulation, and alteration of intracellular signaling, all of which are involved in neoplastic transformation. To prevent chronic inflammation and resulting inflammation-promoted cancer development, understanding the process that resolves inflammation is essential. Resolution of inflammation is an active coordinated process regulated by distinct anti-inflammatory and pro-resolving endogenous lipid mediators, such as resolvins and lipoxins. The role of pro-inflammatory signaling in carcinogenesis has become more and more evident and well characterized, but the potential role of pro-resolving mediators in cancer prevention remains still elusive. In searching for an efficacious way to prevent chronic inflammation-associated cancer, the pro-resolving signal transduction pathways and their regulators should be unraveled.

Keywords

Cancer Chemoprevention Inflammation-associated carcinogenesis Lipid mediators Lipid mediator class switching Prostaglandins Resolution of inflammation Resolvins 

References

  1. 1.
    Medzhitov R (2008) Origin and physiological roles of inflammation. Nature 454:428–435PubMedCrossRefGoogle Scholar
  2. 2.
    Philip M, Rowley DA, Schreiber H (2004) Inflammation as a tumor promoter in cancer induction. Semin Cancer Biol 14:433–439PubMedCrossRefGoogle Scholar
  3. 3.
    Vendramini-Costa DB, Carvalho JE (2012) Molecular link mechanisms between inflammation and cancer. Curr Pharm Des 18:3831–3852PubMedCrossRefGoogle Scholar
  4. 4.
    Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454:436–444PubMedCrossRefGoogle Scholar
  5. 5.
    Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420:860–867PubMedCrossRefGoogle Scholar
  6. 6.
    Radisky DC, Kenny PA, Bissell MJ (2007) Fibrosis and cancer: do myofibroblasts come also from epithelial cells via EMT? J Cell Biochem 101:830–839PubMedCrossRefGoogle Scholar
  7. 7.
    Colville-Nash PR, Gilroy DW (2001) Potential adverse effects of cyclooxygenase-2 inhibition: evidence from animal models of inflammation. BioDrugs 15:1–9PubMedCrossRefGoogle Scholar
  8. 8.
    Stevens DL (1995) Could nonsteroidal antiinflammatory drugs (NSAIDs) enhance the progression of bacterial-infections to toxic shock syndrome. Clin Infect Dis 21:977–980PubMedCrossRefGoogle Scholar
  9. 9.
    Rodriguez-Vita J, Lawrence T (2010) The resolution of inflammation and cancer. Cytokine Growth Factor Rev 21:61–65PubMedCrossRefGoogle Scholar
  10. 10.
    Wilting J, Becker J, Buttler K, Weich HA (2009) Lymphatics and inflammation. Curr Med Chem 16:4581–4592PubMedCrossRefGoogle Scholar
  11. 11.
    Huynh MLN, Fadok VA, Henson PM (2002) Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta 1 secretion and the resolution of inflammation. J Clin Invest 109:41–50PubMedGoogle Scholar
  12. 12.
    Opal SM, DePalo VA (2000) Anti-inflammatory cytokines. Chest 117:1162–1172PubMedCrossRefGoogle Scholar
  13. 13.
    Samuelsson B (1983) From studies of biochemical-mechanism to novel biological mediators—prostaglandin endoperoxides, thromboxanes, and leukotrienes. Angew Chem Int Edit 22:805–815CrossRefGoogle Scholar
  14. 14.
    Ricciotti E, FitzGerald GA (2011) Prostaglandins and inflammation. Arterioscler Thromb Vasc 31:986–1000CrossRefGoogle Scholar
  15. 15.
    Oshima H, Hioki K, Popivanova BK, Oguma K, Van Rooijen N, Ishikawa TO, Oshima M (2011) Prostaglandin E2 signaling and bacterial infection recruit tumor-promoting macrophages to mouse gastric tumors. Gastroenterology 140:596–607.e7PubMedCrossRefGoogle Scholar
  16. 16.
    Trebino CE, Stock JL, Gibbons CP, Naiman BM, Wachtmann TS, Umland JP, Pandher K, Lapointe JM, Saha S, Roach ML, Carter D, Thomas NA, Durtschi BA, McNeish JD, Hambor JE, Jakobsson PJ, Carty TJ, Perez JR, Audoly LP (2003) Impaired inflammatory and pain responses in mice lacking an inducible prostaglandin E synthase. Proc Natl Acad Sci U S A 100:9044–9049PubMedCrossRefGoogle Scholar
  17. 17.
    McCoy JM, Wicks JR, Audoly LP (2002) The role of prostaglandin E2 receptors in the pathogenesis of rheumatoid arthritis. J Clin Invest 110:651–658PubMedGoogle Scholar
  18. 18.
    Byrum RS, Goulet JL, Snouwaert JN, Griffiths RJ, Koller BH (1999) Determination of the contribution of cysteinyl leukotrienes and leukotriene B4 in acute inflammatory responses using 5-lipoxygenase- and leukotriene A4 hydrolase-deficient mice. J Immunol 163:6810–6819PubMedGoogle Scholar
  19. 19.
    Serhan CN, Savill J (2005) Resolution of inflammation: the beginning programs the end. Nat Immunol 6:1191–1197PubMedCrossRefGoogle Scholar
  20. 20.
    Lawrence T, Willoughby DA, Gilroy DW (2002) Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nat Rev Immunol 2:787–795PubMedCrossRefGoogle Scholar
  21. 21.
    Il Lee S, Zuo XS, Shureiqi I (2011) 15-Lipoxygenase-1 as a tumor suppressor gene in colon cancer: is the verdict in? Cancer Metastasis Rev 30:481–491PubMedCrossRefGoogle Scholar
  22. 22.
    Serhan CN, Petasis NA (2011) Resolvins and protectins in inflammation resolution. Chem Rev 111:5922–5943PubMedCrossRefGoogle Scholar
  23. 23.
    Schwab JM, Chiang N, Arita M, Serhan CN (2007) Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 447:869–874PubMedCrossRefGoogle Scholar
  24. 24.
    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 U S A 102:7671–7676PubMedCrossRefGoogle Scholar
  25. 25.
    Hasturk H, Kantarci A, Ohira T, Arita M, Ebrahimi N, Chiang N, Petasis NA, Levy BD, Serhan CN, Van Dyke TE (2006) RvE1 protects from local inflammation and osteoclast-mediated bone destruction in periodontitis. FASEB J 20:401–403PubMedGoogle Scholar
  26. 26.
    Levy BD, Clish CB, Schmidt B, Gronert K, Serhan CN (2001) Lipid mediator class switching during acute inflammation: signals in resolution. Nat Immunol 2:612–619PubMedCrossRefGoogle Scholar
  27. 27.
    Spite M, Serhan CN (2010) Novel lipid mediators promote resolution of acute inflammation impact of aspirin and statins. Circ Res 107:1170–1184PubMedCrossRefGoogle Scholar
  28. 28.
    Hammad H, de Heer HJ, Soullie T, Hoogsteden HC, Trottein F, Lambrecht BN (2003) Prostaglandin D2 inhibits airway dendritic cell migration and function in steady state conditions by selective activation of the D prostanoid receptor 1. J Immunol 171:3936–3940PubMedGoogle Scholar
  29. 29.
    Shibata T, Kondo M, Osawa T, Shibata N, Kobayashi M, Uchida K (2002) 15-Deoxy-Δ12,14-prostaglandin J2—a prostaglandin D2 metabolite generated during inflammatory processes. J Biol Chem 277:10459–10466PubMedCrossRefGoogle Scholar
  30. 30.
    Surh YJ, Na HK, Park JM, Lee HN, Kim W, Yoon IS, Kim DD (2011) 15-Deoxy-Δ12,14-prostaglandin J2, an electrophilic lipid mediator of anti-inflammatory and pro-resolving signaling. Biochem Pharmacol 82:1335–1351PubMedCrossRefGoogle Scholar
  31. 31.
    Lee YC (2004) The role of PTEN in allergic inflammation. Arch Immunol Ther Exp 52:250–254Google Scholar
  32. 32.
    Croker BA, Kiu H, Pellegrini M, Toe J, Preston S, Metcalf D, O’Donnell JA, Cengia LH, McArthur K, Nicola NA, Alexander WS, Roberts AW (2012) IL-6 promotes acute and chronic inflammatory disease in the absence of SOCS3. Immunol Cell Biol 90:124–129PubMedCrossRefGoogle Scholar
  33. 33.
    Lawrence T, Bebien M, Liu GY, Nizet V, Karin M (2005) IKK alpha limits macrophage NF-kappa B activation and contributes to the resolution of inflammation. Nature 434:1138–1143PubMedCrossRefGoogle Scholar
  34. 34.
    Balode L, Strazda G, Jurka N, Kopeika U, Kislina A, Bukovskis M, Beinare M, Gardjusina V, Taivans I (2012) Lipoxygenase-derived arachidonic acid metabolites in chronic obstructive pulmonary disease. Medicina (Kaunas) 48:292–298Google Scholar
  35. 35.
    Wu WKK, Sung JJY, Lee CW, Yu J, Cho CH (2010) Cyclooxygenase-2 in tumorigenesis of gastrointestinal cancers: an update on the molecular mechanisms. Cancer Lett 295:7–16PubMedCrossRefGoogle Scholar
  36. 36.
    Greenhough A, Smartt HJM, Moore AE, Roberts HR, Williams AC, Paraskeva C, Kaidi A (2009) The COX-2/PGE2 pathway: key roles in the hallmarks of cancer and adaptation to the tumour microenvironment. Carcinogenesis 30:377–386PubMedCrossRefGoogle Scholar
  37. 37.
    Castellone MD, Teramoto H, Williams BO, Druey KM, Gutkind JS (2005) Prostaglandin E2 promotes colon cancer cell growth through a Gs-axin-beta-catenin signaling axis. Science 310:1504–1510PubMedCrossRefGoogle Scholar
  38. 38.
    Sheng HM, Shao JY, Washington MK, DuBois RN (2001) Prostaglandin E2 increases growth and motility of colorectal carcinoma cells. J Biol Chem 276:18075–18081PubMedCrossRefGoogle Scholar
  39. 39.
    Fukuda R, Kelly B, Semenza GL (2003) Vascular endothelial growth factor gene expression in colon cancer cells exposed to prostaglandin E2 is mediated by hypoxia-inducible factor 1. Cancer Res 63:2330–2334PubMedGoogle Scholar
  40. 40.
    Sakai H, Suzuki T, Takahashi Y, Ukai M, Tauchi K, Fujii T, Horikawa N, Minamimura T, Tabuchi Y, Morii M, Tsukada K, Takeguchi N (2006) Upregulation of thromboxane synthase in human colorectal carcinoma and the cancer cell proliferation by thromboxane A2. FEBS Lett 580:3368–3374PubMedCrossRefGoogle Scholar
  41. 41.
    Daniel TO, Liu H, Morrow JD, Crews BC, Marnett LJ (1999) Thromboxane A2 is a mediator of cyclooxygenase-2-dependent endothelial migration and angiogenesis. Cancer Res 59:4574–4577PubMedGoogle Scholar
  42. 42.
    Pradono P, Tazawa R, Maemondo M, Tanaka M, Usui K, Saijo Y, Hagiwara K, Nukiwa T (2002) Gene transfer of thromboxane A2 synthase and prostaglandin I2 synthase antithetically altered tumor angiogenesis and tumor growth. Cancer Res 62:63–66PubMedGoogle Scholar
  43. 43.
    Gustafsson A, Hansson E, Kressner U, Nordgren S, Andersson M, Lonnroth C, Lundholm K (2007) Prostanoid receptor expression in colorectal cancer related to tumor stage, differentiation and progression. Acta Oncol 46:1107–1112PubMedCrossRefGoogle Scholar
  44. 44.
    Cutler NS, Graves-Deal R, LaFleur BJ, Gao ZQ, Boman BM, Whitehead RH, Terry E, Morrow JD, Coffey RJ (2003) Stromal production of prostacyclin confers an antiapoptotic effect to colonic epithelial cells. Cancer Res 63:1748–1751PubMedGoogle Scholar
  45. 45.
    Mutoh M, Watanabe K, Kitamura T, Shoji Y, Takahashi M, Kawamori T, Tani K, Kobayashi M, Maruyama T, Kobayashi K, Ohuchida S, Sugimoto Y, Narumiya S, Sugimura T, Wakabayashi K (2002) Involvement of prostaglandin E receptor subtype EP4 in colon carcinogenesis. Cancer Res 62:28–32PubMedGoogle Scholar
  46. 46.
    Qualtrough D, Kaidi A, Chell S, Jabbour HN, Williams AC, Paraskeva C (2007) Prostaglandin F stimulates motility and invasion in colorectal tumor cells. Int J Cancer 121:734–740PubMedCrossRefGoogle Scholar
  47. 47.
    Goldblatt D, Thrasher AJ (2000) Chronic granulomatous disease. Clin Exp Immunol 122:1–9PubMedCrossRefGoogle Scholar
  48. 48.
    Morimoto K, Janssen WJ, Terada M (2012) Defective efferocytosis by alveolar macrophages in IPF patients. Respir Med 106:1800–1803PubMedCrossRefGoogle Scholar
  49. 49.
    Imanishi T, Akasaka T (2013) Novel strategies to target inflammatory processes in atherosclerosis. Curr Pharm Des (in press)Google Scholar
  50. 50.
    Herlong JL, Scott TR (2006) Positioning prostanoids of the D and J series in the immunopathogenic scheme. Immunol Lett 102:121–131PubMedCrossRefGoogle Scholar
  51. 51.
    Ragolia L, Palaia T, Hall CE, Klein J, Buyud A (2010) Diminished lipocalin-type prostaglandin D2 synthase expression in human lung tumors. Lung Cancer 70:103–109PubMedCrossRefGoogle Scholar
  52. 52.
    Payne CA, Maleki S, Messina M, O’Sullivan MG, Stone G, Hall NR, Parkinson JF, Wheeler HR, Cook RJ, Biggs MT, Little NS, Teo C, Robinson BG, McDonald KL (2008) Loss of prostaglandin D2 synthase: a key molecular event in the transition of a low-grade astrocytoma to an anaplastic astrocytoma. Mol Cancer Ther 7:3420–3428PubMedCrossRefGoogle Scholar
  53. 53.
    Eichele K, Ramer R, Hinz B (2008) Decisive role of cyclooxygenase-2 and lipocalin-type prostaglandin D synthase in chemotherapeutics-induced apoptosis of human cervical carcinoma cells. Oncogene 27:3032–3044PubMedCrossRefGoogle Scholar
  54. 54.
    Murata T, Aritake K, Matsumoto S, Kamauchi S, Nakagawa T, Hori M, Momotani E, Urade Y, Ozaki H (2011) Prostagladin D2 is a mast cell-derived antiangiogenic factor in lung carcinoma. Proc Natl Acad Sci U S A 108:19802–19807PubMedCrossRefGoogle Scholar
  55. 55.
    Park JM, Kanaoka Y, Eguchi N, Aritake K, Grujic S, Materi AM, Buslon VS, Tippin BL, Kwong AM, Salido E, French SW, Urade Y, Lin HJ (2007) Hematopoietic prostaglandin D synthase suppresses intestinal adenomas in ApcMin/+ mice. Cancer Res 67:881–889PubMedCrossRefGoogle Scholar
  56. 56.
    Janakiram NB, Rao CV (2009) Role of lipoxins and resolvins as anti-inflammatory and proresolving mediators in colon cancer. Curr Mol Med 9:565–579PubMedCrossRefGoogle Scholar
  57. 57.
    Shureiqi I, Wojno KJ, Poore JA, Reddy RG, Moussali MJ, Spindler SA, Greenson JK, Normolle D, Hasan AA, Lawrence TS, Brenner DE (1999) Decreased 13-S-hydroxyoctadecadienoic acid levels and 15-lipoxygenase-1 expression in human colon cancers. Carcinogenesis 20:1985–1995Google Scholar
  58. 58.
    Kamitani H, Geller M, Eling T (1998) Expression of 15-lipoxygenase by human colorectal carcinoma Caco-2 cells during apoptosis and cell differentiation. J Biol Chem 273:21569–21577PubMedCrossRefGoogle Scholar
  59. 59.
    Kim JS, Baek SJ, Bottone FG, Sali T, Eling TE (2005) Overexpression of 15-lipoxygenase-1 induces growth arrest through phosphorylation of p53 in human colorectal cancer cells. Mol Cancer Res 3:511–517PubMedCrossRefGoogle Scholar
  60. 60.
    Yuri M, Sasahira T, Nakai K, Ishimaru S, Ohmori H, Kuniyasu H (2007) Reversal of expression of 15-lipoxygenase-1 to cyclooxygenase-2 is associated with development of colonic cancer. Histopathology 51:520–527PubMedCrossRefGoogle Scholar
  61. 61.
    Jiang WG, Douglas-Jones A, Mansel RE (2003) Levels of expression of lipoxygenases and cyclooxygenase-2 in human breast cancer. Prostaglandins Leukot Essent 69:275–281CrossRefGoogle Scholar
  62. 62.
    Kure I, Nishiumi S, Nishitani Y, Tanoue T, Ishida T, Mizuno M, Fujita T, Kutsumi H, Arita M, Azuma T, Yoshida M (2010) Lipoxin A4 reduces lipopolysaccharide-induced inflammation in macrophages and intestinal epithelial cells through inhibition of nuclear factor-kappaB activation. J Pharmacol Exp Ther 332:541–548PubMedCrossRefGoogle Scholar
  63. 63.
    Jozsef L, Zouki C, Petasis NA, Serhan CN, Filep JG (2002) Lipoxin A4 and aspirin-triggered 15-epi-lipoxin A4 inhibit peroxynitrite formation, NF-kappa B and AP-1 activation, and IL-8 gene expression in human leukocytes. Proc Natl Acad Sci U S A 99:13266–13271PubMedCrossRefGoogle Scholar
  64. 64.
    Hachicha M, Pouliot M, Petasis NA, Serhan CN (1999) Lipoxin (LX)A4 and aspirin-triggered 15-epi-LXA4 inhibit tumor necrosis factor 1 alpha-initiated neutrophil responses and trafficking: regulators of a cytokine-chemokine axis. J Exp Med 189:1923–1929PubMedCrossRefGoogle Scholar
  65. 65.
    Hao H, Liu M, Wu P, Cai L, Tang K, Yi P, Li YS, Chen Y, Ye DY (2011) Lipoxin A4 and its analog suppress hepatocellular carcinoma via remodeling tumor microenvironment. Cancer Lett 309:85–94PubMedCrossRefGoogle Scholar
  66. 66.
    Ishida T, Yoshida M, Arita M, Nishitani Y, Nishiumi S, Masuda A, Mizuno S, Takagawa T, Morita Y, Kutsumi H, Inokuchi H, Serhan CN, Blumberg RS, Azuma T (2010) Resolvin E1, an endogenous lipid mediator derived from eicosapentaenoic acid, prevents dextran sulfate sodium-induced colitis. Inflamm Bowel Dis 16:87–95PubMedCrossRefGoogle Scholar
  67. 67.
    Nowak J, Weylandt KH, Habbel P, Wang J, Dignass A, Glickman JN, Kang JX (2007) Colitis-associated colon tumorigenesis is suppressed in transgenic mice rich in endogenous n-3 fatty acids. Carcinogenesis 28:1991–1995PubMedCrossRefGoogle Scholar
  68. 68.
    Harris SG, Smith RS, Phipps RP (2002) 15-Deoxy-Δ12,14-PGJ2 induces IL-8 production in human T cells by a mitogen-activated protein kinase pathway. J Immunol 168:1372–1379PubMedGoogle Scholar
  69. 69.
    Okano H, Shiraki K, Inoue H, Yamanaka Y, Kawakita T, Saitou Y, Yamaguchi Y, Enokimura N, Yamamoto N, Sugimoto K, Murata K, Nakano T (2003) 15-Deoxy-Δ12,14-PGJ2 regulates apoptosis induction and nuclear factor-kappa B activation via a peroxisome proliferator-activated receptor-gamma-independent mechanism in hepatocellular carcinoma. Lab Invest 83:1529–1539PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Tumor Microenvironment Global Core Research Center, College of PharmacySeoul National UniversitySeoulSouth Korea
  2. 2.Department of Food and NutritionSungshin Women’s UniversitySeoulSouth Korea
  3. 3.WCU Department of Molecular Medicine and Biopharmaceutical Sciences, Graduate School of Convergence Science and TechnologySeoul National UniversitySeoulSouth Korea
  4. 4.Cancer Research InstituteSeoul National UniversitySeoulSouth Korea

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