Zileuton, 5-lipoxygenase inhibitor, acts as a chemopreventive agent in intestinal polyposis, by modulating polyp and systemic inflammation

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Gounaris, Elias ^a   Heiferman, Michael J ^a   Heiferman, Jeffrey R ^a   Shrivastav, Manisha ^a   Vitello, Dominic ^a   Blatner, Nichole R ^a   Knab, Lawrence M ^a   Phillips, Joseph D ^a   Cheon, Eric C ^a   Grippo, Paul J ^a   Khazaie, Khashayarsha ^a   Munshi, Hidayatullah G ^a   Bentrem, David J ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONATE 5 LIPOXYGENASE; INTERLEUKIN 17; INTERLEUKIN 1BETA; LEUKOTRIENE B4; TUMOR NECROSIS FACTOR ALPHA; ZILEUTON; HYDROXYUREA; LIPOXYGENASE INHIBITOR;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER PREVENTION; COLON CANCER; CONTROLLED STUDY; CYTOKINE RESPONSE; DRUG BLOOD LEVEL; ENZYME INHIBITION; GASTROINTESTINAL POLYPOSIS; HIGH RISK PATIENT; IN VIVO STUDY; INNATE IMMUNITY; MACROPHAGE; MAST CELL; MITOSIS INHIBITION; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; SUPPRESSOR CELL; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; ANALOGS AND DERIVATIVES; ANIMAL; COLONIC NEOPLASMS; DISEASE MODEL; FEMALE; HUMAN; INFLAMMATORY BOWEL DISEASES; INTESTINAL POLYPOSIS; MALE; MUTANT MOUSE STRAIN; PATHOLOGY;

MUS;

ANIMALS; COLONIC NEOPLASMS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; HYDROXYUREA; INFLAMMATORY BOWEL DISEASES; INTESTINAL POLYPOSIS; LIPOXYGENASE INHIBITORS; MALE; MICE; MICE, MUTANT STRAINS;

EID: 84929094242     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121402     Document Type: Article

References (43)

1. Farraye FA, Odze RD, Eaden J, Itzkowitz SH. AGA technical review on the diagnosis and management of colorectal neoplasia in inflammatory bowel disease. Gastroenterology, 2010; 138: 746-774, doi: 10.1053/j.gastro.2009.12.035 PMID: 20141809
2. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature, 2008; 454: 436-444. doi: 10.1038/nature07205 PMID: 18650914
3. Bennett J, Blanchet M, Zhao L, Zbytnuik L, Antignano F, Gold M, et al. Bone marrow-derived mast cells accumulate in the central nervous system during inflammation but are dispensable for experimental autoimmune encephalomyelitis pathogenesis. The Journal of Immunology, 2009: 182: 5507. doi: 10.4049/jimmunol.0801485 PMID: 19380799
4. Marx J. Cancer research. Inflammation and cancer: the link grows stronger. Science, 2004: 306: 966-968. PMID: 15528423
5. Coussens LM, Raymond WW, Bergers G, Laig-Webster M, Behrendtsen O, Werb Z, et al. Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev. 1999; 13: 1382-1397. PMID: 10364156
6. Kulbe H, Chakravarty P, Leinster DA, Charles KA, Kwong J, Thompson RG, et al. A dynamic inflammatory cytokine network in the human ovarian cancer microenvironment. Cancer Res, 2012: 72: 66-75. doi: 10.1158/0008-5472.CAN-11-2178 PMID: 22065722
7. Strouch MJ, Cheon EC, Salabat MR, Krantz SB, Gounaris E, Melstrom LG, et al. Crosstalk between mast cells and pancreatic cancer cells contributes to pancreatic tumor progression. Clin Cancer Res 2010; 16, 2257-2265. doi: 10.1158/1078-0432.CCR-09-1230 PMID: 20371681
8. Quante M, Tu SP, Tomita H, Gonda T, Wang SSW, Takashi S, et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell, 2011; 19: 257-272. doi: 10.1016/j.ccr.2011.01.020 PMID: 21316604
9. Wang H-W, Joyce JA. Alternative activation of tumor-associated macrophages by IL-4: priming for protumoral functions. Cell Cycle, 2010; 9: 4824-4835. PMID: 21150330
10. Pulendran B, Ono SJ. A shot in the arm for mast cells. Nat Med, 2008; 14: 489-490. doi: 10.1038/nm0508-489 PMID: 18463655
11. Tripodo C, Gri G, Piccaluga PP, Frossi B, Guarnotta C, Piconese S, et al. Mast cells and Th17 cells contribute to the lymphoma-associated pro-inflammatory microenvironment of angioimmunoblastic T-cell lymphoma. Am J Pathol, 2010; 177: 792-802. doi: 10.2353/ajpath.2010.091286 PMID: 20595635
12. Maltby S, Khazaie K, McNagny KM. Mast cells in tumor growth: angiogenesis, tissue remodelling and immune-modulation. Biochim Biophys Acta, 2009; 1796: 19-26. doi: 10.1016/j.bbcan.2009.02.001 PMID: 19233249
13. Clarke SL, Betts GJ, Plant A, Wright KL, El-Shanawany TM, Harrop R, et al. CD4+CD25+FOXP3+ Regulatory T Cells Suppress Anti-Tumor Immune Responses in Patients with Colorectal Cancer. PLoS ONE 2006; 1
14. Youn J-I, Gabrilovich DI. The biology of myeloid-derived suppressor cells: the blessing and the curse of morphological and functional heterogeneity. Eur J Immunol, 2010; 40: 2969-2975. doi: 10.1002/eji.201040895 PMID: 21061430
15. Melstrom LG, Bentrem DJ, Salabat MR, Kennedy TJ, Ding X-Z, Strouch M, et al. Overexpression of 5-lipoxygenase in colon polyps and cancer and the effect of 5-LOX inhibitors in vitro and in a murine model. Clin Cancer Res, 2008; 14: 6525-6530. doi: 10.1158/1078-0432.CCR-07-4631 PMID: 18927292
16. Rådmark O, Werz O, Steinhilber D, Samuelsson B. 5-Lipoxygenase: regulation of expression and enzyme activity. Trends Biochem Sci., 2007; 32: 332-341. PMID: 17576065
17. Peters-Golden M, Brock TG. Intracellular compartmentalization of leukotriene synthesis: unexpected nuclear secrets. FEBS Lett., 2001; 487: 323-326. PMID: 11163352
18. Cheon EC, Khazaie K, Khan MW, Strouch MJ, Krantz SB, Phillips J, et al. Mast cell 5-lipoxygenase activity promotes intestinal polyposis in APCDelta468 mice. Cancer Res, 2011; 71: 1627-1636. doi: 10.1158/0008-5472.CAN-10-1923 PMID: 21216893
19. Gunning WT, Kramer PM, Steele VE, Pereira MA. Chemoprevention by lipoxygenase and leukotriene pathway inhibitors of vinyl carbamate-induced lung tumors in mice. Cancer Res, 2002; 62: 4199-4201. PMID: 12154018
20. Gounaris E, Martin J, Ishihara Y, Khan MW, Lee G, Sinh P, et al. Fluorescence Endoscopy of Cathepsin Activity Discriminates Dysplasia from Colitis. Inflamm Bowel Dis, 2013; 19: 1339-1345. doi: 10.1097/MIB.0b013e318281f3f8 PMID: 23591598
21. Gounaris E, Tung CH, Restaino C, Maehr R, Kohler R, Joyce JA, et al. Live imaging of cysteine-cathepsin activity reveals dynamics of focal inflammation, angiogenesis, and polyp growth. PLoS ONE, 2008; 3: e2916. doi: 10.1371/journal.pone.0002916 PMID: 18698347
22. Chen Q, Snapper CM. Inflammatory monocytes are critical for induction of a polysaccharide-specific antibody response to an intact bacterium. J Immunol, 2013; 190: 1048-1055. doi: 10.4049/jimmunol.1202455 PMID: 23269244
23. Bertrán X, Mañé J, Fernández-Bañares F, Castellá E, Bartolí R, Ojanguren I, et al. Intracolonic administration of zileuton, a selective 5-lipoxygenase inhibitor, accelerates healing in a rat model of chronic colitis. Gut, 1996; 38: 899-904. PMID: 8984030
24. Zingarelli B, Squadrito F, Graziani P, Camerini R, Caputi AP. Effects of zileuton, a new 5-lipoxygenase inhibitor, in experimentally induced colitis in rats. Agents and Actions, 1993; 39: 150-156. PMID: 7905704
25. Gounaris E, Erdman SE, Restaino C, Gurish MF, Friend DS, Gounari F, et al. Mast cells are an essential hematopoietic component for polyp development. Proc Natl Acad Sci USA, 2007; 104: 19977-19982. PMID: 18077429
26. Coussens LM, Tinkle CL, Hanahan D, Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell, 2000; 103: 481-490. PMID: 11081634
27. Tlsty TD, Coussens LM. Tumor stroma and regulation of cancer development. Annual review of pathology, 2006; 1: 119-150. PMID: 18039110
28. Khazaie K, Blatner NR, Khan MW, Gounari F, Gounaris E, Dennis K, et al. The significant role of mast cells in cancer. Cancer Metastasis Rev, 2011; 30: 45-60. doi: 10.1007/s10555-011-9286-z PMID: 21287360
29. Hu B, Elinav E, Huber S, Booth CJ, Strowig T, Jin C, et al. Inflammation-induced tumorigenesis in the colon is regulated by caspase-1 and NLRC4. Proc Natl Acad Sci USA., 2010.
30. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol, 2010; 182: 4499-4506.
31. Tsopanoglou NE, Maragoudakis ME. On the mechanism of thrombin-induced angiogenesis. Potentiation of vascular endothelial growth factor activity on endothelial cells by up-regulation of its receptors. J Biol Chem, 1999; 274: 23969-23976. PMID: 10446165
32. Kim G-Y, Lee J-W, Cho S-H, Seo J-M, Kim J-H. Role of the low-affinity leukotriene B4 receptor BLT2 in VEGF-induced angiogenesis. Arterioscler Thromb Vasc Biol., 2009; 29: 915-920. doi: 10.1161/ATVBAHA.109.185793 PMID: 19286633
33. Kim G-Y, Lee J-W, Ryu H-C, Wei J-D, Seong C-M, Kim J-H. Proinflammatory cytokine IL-1beta stimulates IL-8 synthesis in mast cells via a leukotriene B4 receptor 2-linked pathway, contributing to angiogenesis. J Immunol, 2010; 184: 3946-3954. doi: 10.4049/jimmunol.0901735 PMID: 20194723
34. Ye YN, Wu WKK, Shin VY, Cho CH. A mechanistic study of colon cancer growth promoted by cigarette smoke extract. Eur J Pharmacol, 2005; 519: 52-57. PMID: 16125168
35. Giantonio BJ, Catalano PJ, Meropol NJ, O'Dwyer PJ, Mitchell EP, Alberts SR, et al. Bevacizumab in combination with oxaliplatin, fluorouracil, and leucovorin (FOLFOX4) for previously treated metastatic colorectal cancer: results from the Eastern Cooperative Oncology Group Study E3200. J Clin Oncol, 2007; 25: 1539-1544. PMID: 17442997
36. Cohen MH, Gootenberg J, Keegan P, Pazdur R. FDA drug approval summary: bevacizumab plus FOLFOX4 as second-line treatment of colorectal cancer. Oncologist, 2007; 12: 356-361. PMID: 17405901
37. Wang D, Dubois RN. The role of COX-2 in intestinal inflammation and colorectal cancer. Oncogene, 2010; 29: 781-788. doi: 10.1038/onc.2009.421 PMID: 19946329
38. Bertagnolli MM, Eagle CJ, Zauber AG, Redston M, Solomon SD, Kim KM, et al. Celecoxib for the prevention of sporadic colorectal adenomas. N Engl J Med, 2006; 355: 873-884. PMID: 16943400
39. Arber N, Eagle CJ, Spicak J, Rácz I, Dite P, Hajer J, et al. Celecoxib for the prevention of colorectal adenomatous polyps. N Engl J Med, 2006; 355: 885-895. PMID: 16943401
40. Rostom A, Dubé C, Lewin G, Tsertsvadze A, Barrowman N, Code C, et al. Nonsteroidal anti-inflammatory drugs and cyclooxygenase-2 inhibitors for primary prevention of colorectal cancer: a systematic review prepared for the U.S. Preventive Services Task Force. Ann Intern Med, 2007; 146: 376-389. PMID: 17339623
41. Edelman MJ, Watson D, Wang X, Morrison C, Kratzke RA, Jewell S, et al. Eicosanoid modulation in advanced lung cancer: cyclooxygenase-2 expression is a positive predictive factor for celecoxib + chemotherapy - Cancer and Leukemia Group B Trial 30203. J Clin Oncol, 2008; 26: 848-855. doi: 10.1200/JCO.2007.13.8081 PMID: 18281656
42. Rossi A, Pergola C, Koeberle A, Hoffmann M, Dehm F, Bramanti P, et al. The 5-lipoxygenase inhibitor, zileuton, suppresses prostaglandin biosynthesis by inhibition of arachidonic acid release in macrophages. Br J Pharmacol, 2010; 161: 555-570. doi: 10.1111/j.1476-5381.2010.00930.x PMID: 20880396
43. Cathcart M-C, Lysaght J, Pidgeon GP. Eicosanoid signalling pathways in the development and progression of colorectal cancer: novel approaches for prevention/intervention. Cancer Metastasis Rev, 2010; 30: 363-385.