Involvement of the 5-lipoxygenase/leukotriene A4 hydrolase pathway in 7,12-dimethylbenz[a]anthracene (DMBA)-induced oral carcinogenesis in hamster cheek pouch, and inhibition of carcinogenesis by its inhibitors

Carcinogenesis

Volumn 27, Issue 9, 2006, Pages 1902-1908

  Sun, Zheng ^a,b   Sood, Sandeep ^c   Li, Ning ^d   Ramji, Divya ^c   Yang, Peiying ^e   Newman, Robert A ^e   Yang, Chung S ^c   Chen, Xiaoxin ^a,b,c  

^a NORTH CAROLINA CENTRAL UNIVERSITY   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c RUTGERS UNIVERSITY   (United States)

^d CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

12 HYDROXYICOSATETRAENOIC ACID; 15 HYDROXYICOSATETRAENOIC ACID; 4 DIMETHYLAMINOBENZYL N 3 MERCAPTO 2 METHYLPROPIONYL CYSTEINE; 5 HYDROXYICOSATETRAENOIC ACID; 7,12 DIMETHYLBENZ[A]ANTHRACENE; ARACHIDONATE 5 LIPOXYGENASE; ARACHIDONIC ACID; BESTATIN; CELECOXIB; ENZYME INHIBITOR; LEUKOTRIENE A4 HYDROLASE; LEUKOTRIENE B4; PROSTAGLANDIN E2; SA 6541; UNCLASSIFIED DRUG; ZILEUTON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARACHIDONIC ACID METABOLISM; ARTICLE; CANCER INHIBITION; CARCINOGENESIS; CELL PROLIFERATION; CHEEK POUCH; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFICACY; ENZYME IMMUNOASSAY; HAMSTER; HISTOPATHOLOGY; INFLAMMATION; MALE; MOUTH CANCER; MOUTH MUCOSA; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; SQUAMOUS CELL CARCINOMA;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANILINE COMPOUNDS; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ANTICARCINOGENIC AGENTS; ARACHIDONATE 5-LIPOXYGENASE; CARCINOGENS; CHEEK; CRICETINAE; CYSTEINE; DINOPROSTONE; EPOXIDE HYDROLASES; LEUCINE; MOUTH NEOPLASMS;

EID: 33747875667     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgl039     Document Type: Article

References (55)

1. Magrath,I. and Litvak,J. (1993) Cancer in developing countries: opportunity and challenge. J. Natl Cancer Inst., 85, 862-874.
2. Jemal,A., Murray,T., Ward,E., Samuels,A., Tiwari,R.C., Ghafoor,A., Feuer,E.J. and Thun,M.J. (2005) Cancer statistics, 2005. CA Cancer J. Clin., 55, 10-30.
3. Jemal,A., Tiwari,R.C., Murray,T., Ghafoor,A., Samuels,A., Ward,E., Feuer,E.J. and Thun,M.J. (2004) Cancer statistics, 2004. CA Cancer J. Clin., 54, 8-29.
4. Funk,G.F., Karnell,L.H., Robinson,R.A., Zhen,W.K., Trask,D.K. and Hoffman,H.T. (2002) Presentation, treatment, and outcome of oral cavity cancer: A National Cancer Data Base report. Head Neck, 24, 165-180.
5. el-Hakim,I.E. and Langdon,J.D. (1991) Arachidonic acid cascade and oral squamous cell carcinoma. Clin. Otolaryngol. Allied Sci., 16, 563-573.
6. Shureiqi,I. and Lippman,S.M. (2001) Lipoxygenase modulation to reverse carcinogenesis. Cancer Res., 61, 6307-6312.
7. Haeggstrom,J.Z. and Wetterholm,A. (2002) Enzymes and receptors in the leukotriene cascade. Cell Mol. Life Sci., 59, 742-753.
8. Peters-Golden,M. and Brock,T.G. (2003) 5-lipoxygenase and FLAP. Prostaglandins Leukot Essent Fatty Acids, 69, 99-109.
9. Funk,C.D., Chen,X.S., Johnson,E.N. and Zhao,L. (2002) Lipoxygenase genes and their targeted disruption. Prostaglandins Other Lipid Mediat. 68-69, 303-312.
10. Gupta,S., Srivastava,M., Ahmad,N., Sakamoto,K., Bostwick,D.G. and Mukhtar,H. (2001) Lipoxygenase-5 is overexpressed in prostate adenocarcinoma. Cancer, 91, 737-743.
11. Hennig,R., Ding,X.Z., Tong,W.G., Schneider,M.B., Standop,J., Friess,H., Buchler,M.W., Pour,P.M. and Adrian,T.E. (2002) 5-Lipoxygenase and leukotriene B (4) receptor are expressed in human pancreatic cancers but not in pancreatic ducts in normal tissue. Am. J. Pathol., 161, 421-428.
12. Ohd,J.F., Nielsen,C.K., Campbell,J., Landberg,G., Lofberg,H. and Sjolander,A. (2003) Expression of the leukotriene D4 receptor CysLT1, COX-2, and other cell survival factors in colorectal adenocarcinomas. Gastroenterology, 124, 57-70.
13. Yoshimura,R., Matsuyama,M., Tsuchida,K., Kawahito,Y., Sano,H. and Nakatani,T. (2003) Expression of lipoxygenase in human bladder carcinoma and growth inhibition by its inhibitors. J. Urol., 170, 1994-1999.
14. Yoshimura,R., Matsuyama,M., Mitsuhashi,M., Takemoto,Y., Tsuchida,K., Kawahito,Y., Sano,H. and Nakatani,T. (2004) Relationship between lipoxygenase and human testicular cancer. Int. J. Mol. Med., 13, 389-393.
15. Chen,X., Wang,S., Wu,N. et al. (2004) Overexpression of 5-lipoxygenase in rat and human esophageal adenocarcinoma and inhibitory effects of zileuton and celecoxib on carcinogenesis. Clin. Cancer Res., 10, 6703-9.
16. Edderkaoui,M., Hong,P., Vaquero,E.C., Lee,J.K., Fischer,L., Friess,H., Buchler,M.W., Lerch,M.M., Pandol,S.J. and Gukovskaya,A.S. (2005) Extracellular matrix stimulates reactive oxygen species production and increases pancreatic cancer cell survival through 5-lipoxygenase and NADPH oxidase. Am. J. Physiol. Gastrointest. Liver Physiol., 289, G1137-G1147.
17. Anderson,K.M., Alrefai,W.A., Bonomi,P.A., Anderson,C.A., Dudeja,P. and Harris,J.E. (2000) A genomic response of H-358 bronchiolar carcinoma cells to MK 886, an inhibitor of 5-lipoxygenase, assessed with a cDNA array. Anticancer Res., 20, 2433-2439.
18. Avis,I.M., Jett,M., Boyle,T., Vos,M.D., Moody,T., Treston,A.M., Martinez,A. and Mulshine,J.L. (1996) Growth control of lung cancer by interruption of 5-lipoxygenase-mediated growth factor signaling. J. Clin. Invest., 97, 806-813.
19. Fan,X.M., Tu,S.P., Lam,S.K., Wang,W.P., Wu,J., Wong,W.M., Yuen,M.F., Lin,M.C., Kung,H.F. and Wong,B.C. (2004) Five-lipoxygenase-activating protein inhibitor MK-886 induces apoptosis in gastric cancer through upregulation of p27kip1 and bax. J. Gastroenterol. Hepatol., 19, 31-37.
20. Moody,T.W., Leyton,J., Martinez,A., Hong,S., Malkinson,A. and Mulshine,J.L. (1998) Lipoxygenase inhibitors prevent lung carcinogenesis and inhibit non-small cell lung cancer growth. Exp. Lung Res., 24, 617-628.
21. Tsukada,T., Nakashima,K. and Shirakawa,S. (1986) Arachidonate 5-lipoxygenase inhibitors show potent antiproliferative effects on human leukemia cell lines. Biochem. Biophys Res. Commun., 140, 832-836.
22. Gunning,W.T., Kramer,P.M., Steele,V.E. and Pereira,M.A. (2002) Chemoprevention by lipoxygenase and leukotriene pathway inhibitors of vinyl carbamate-induced lung tumors in mice. Cancer Res., 62, 4199-4201.
23. Jiang,H., Yamamoto,S. and Kato,R. (1994) Inhibition of two-stage skin carcinogenesis as well as complete skin carcinogenesis by oral administration of TMK688, a potent lipoxygenase inhibitor. Carcinogenesis, 15, 807-812.
24. Wenger,F.A., Kilian,M., Achucarro,P., Heinicken,D., Schimke,I., Guski,H., Jacobi,C.A. and Muller,J.M. (2002) Effects of Celebrex and Zyflo on BOP-induced pancreatic cancer in Syrian hamsters. Pancreatology, 2, 54-60.
25. Wenger,F.A., Kilian,M., Bisevac,M., Khodadayan,C., von Seebach,M., Schimke,I., Guski,H. and Muller,J.M. (2002) Effects of Celebrex and Zyflo on liver metastasis and lipidperoxidation in pancreatic cancer in Syrian hamsters. Clin. Exp. Metastasis, 19, 681-687.
26. el-Hakim,I.E., Langdon,J.D., Zakrzewski,J.T. and Costello,J.F. (1990) Leukotriene B4 and oral cancer. Br. J. Oral. Maxillofac. Surg., 28, 155-159.
27. Li,N., Sood,S., Wang,S., Fang,M., Wang,P., Sun,Z., Yang,C.S. and Chen,X. (2005) Overexpression of 5-lipoxygenase and cyclooxygenase 2 in hamster and human oral cancer and chemopreventive effects of zileuton and celecoxib. Clin. Cancer Res., 11, 2089-2096.
28. Tsuji,F., Miyake,Y., Enomoto,H., Horiuchi,M. and Mita,S. (1998) Effects of SA6541, a leukotriene A4 hydrolase inhibitor, and indomethacin on carrageenan-induced murine dermatitis. Eur. J. Pharmacol., 346, 81-85.
29. Tsuji,F., Miyake,Y., Horiuchi,M. and Mita,S. (1998) Involvement of leukotriene B4 in murine dermatitis models. Biochem. Pharmacol., 55, 297-304.
30. Leininger,I. and KJokinen,M. (1982) Tumors of the oral cavity, pharynx, oesophagus and stomach. In Turosov,V. (ed.), Pathology of Tumors in Laboratory Animals. IARC, Albany, NY, Vol. 3, pp. 167-169.
31. Kramer,I., Lucas,R., Pindborg,J. and Sobin,L. (1978) WHO, Collaborating center for oral precancerous lesions: Definitions of leukoplakia and related lesions: An aid to studies on oral precancer. Oral Surg. Oral Med. Oral Pathol., 46, 518-589.
32. Kempen,E.C., Yang,P., Felix,E., Madden,T. and Newman,R.A. (2001) Simultaneous quantification of arachidonic acid metabolites in cultured tumor cells using high-performance liquid chromatography/electrospray ionization tandem mass spectrometry. Anal. Biochem., 297, 183-190.
33. Gimenez-Conti,I.B. and Slaga,T.J. (1993) The hamster cheek pouch carcinogenesis model. J. Cell Biochem., Suppl. 17F, 83-90.
34. Schwartz,J. and Gu,X. (2001) Hamster oral cancer model. In Teicher,B. (ed.), Tumor Models in Cancer Research. Humana Press Inc., Totowa, NJ, pp. 141-171.
35. Li,N., Chen,X., Liao,J., Yang,G., Wang,S., Josephson,Y., Han,C., Chen,J., Huang,M.T. and Yang,C.S. (2002) Inhibition of 7,12-dimethylbenz[a]anthracene (DMBA)-induced oral carcinogenesis in hamsters by tea and curcumin. Carcinogenesis, 23, 1307-1313.
36. Minter,H.A., Eveson,J.W., Huntley,S., Elder,D.J. and Hague,A. (2003) The cyclooxygenase 2-selective inhibitor NS398 inhibits proliferation of oral carcinoma cell lines by mechanisms dependent and independent of reduced prostaglandin E2 synthesis. Clin. Cancer Res., 9, 1885-1897.
37. Jeng,J.H., Wang,Y.J., Chiang,B.L., Lee,P.H., Chan,C.P., Ho,Y.S., Wang,T.M., Lee,J.J., Hahn,L.J. and Chang,M.C. (2003) Roles of keratinocyte inflammation in oral cancer: Regulating the prostaglandin E2, interleukin-6 and TNF-alpha production of oral epithelial cells by areca nut extract and arecoline. Carcinogenesis, 24, 1301-1315.
38. Karmali,R.A., Wustrow,T., Thaler,H.T. and Strong,E.W. (1984) Prostaglandins in carcinomas of the head and neck. Cancer Lett., 22, 333-336.
39. Yang,C.Y., Meng,C.L., Liao,C.L. and Wong,P.Y. (2003) Regulation of cell growth by selective COX-2 inhibitors in oral carcinoma cell lines. Prostaglandins Other Lipid Mediat., 72, 115-130.
40. Shiotani,H., Denda,A., Yamamoto,K., Kitayama,W., Endoh,T., Sasaki,Y., Tsutsumi,N., Sugimura,M. and Konishi,Y. (2001) Increased expression of cyclooxygenase-2 protein in 4-nitroquinoline-1-oxide-induced rat tongue carcinomas and chemopreventive efficacy of a specific inhibitor, nimesulide. Cancer Res., 61, 1451-1456.
41. Hoque,A., Lippman,S.M., Wu,T.T., Xu,Y., Liang,Z.D., Swisher,S., Zhang,H., Cao,L., Ajani,J.A. and Xu,X.C. (2005) Increased 5-lipoxygenase expression and induction of apoptosis by its inhibitors in esophageal cancer: A potential target for prevention. Carcinogenesis, 26, 785-791.
42. Tong,W.G., Ding,X.Z., Hennig,R., Witt,R.C., Standop,J., Pour,P.M. and Adrian,T.E. (2002) Leukotriene B4 receptor antagonist LY293111 inhibits proliferation and induces apoptosis in human pancreatic cancer cells. Clin. Cancer Res., 8, 3232-3242.
43. Qiao,L., Kozoni,V., Tsioulias,G.J., Koutsos,M.I., Hanif,R., Shiff,S.J. and Rigas,B. (1995) Selected eicosanoids increase the proliferation rate of human colon carcinoma cell lines and mouse colonocytes in vivo. Biochim Biophys Acta, 1258, 215-223.
44. Kragballe,K., Desjarlais,L. and Voorhees,J.J. (1985) Leukotrienes B4, C4 and D4 stimulate DNA synthesis in cultured human epidermal keratinocytes. Br. J. Dermatol., 113, 43-52.
45. Bauer,F.W., van de Kerkhof,P.C. and Maassen-de Grood,R.M. (1986) Epidermal hyperproliferation following the induction of microabscesses by leukotriene B4. Br. J. Dermatol., 114, 409-412.
46. Woo,C.H., You,H.J., Cho,S.H., Eom,Y.W., Chun,J.S., Yoo,Y.J. and Kim,J.H. (2002) Leukotriene B(4) stimulates Rac-ERK cascade to generate reactive oxygen species that mediates chemotaxis. J. Biol. Chem., 277, 8572-8578.
47. Steiner,D.R., Gonzalez,N.C. and Wood,J.G. (2001) Leukotriene B(4) promotes reactive oxidant generation and leukocyte adherence during acute hypoxia. J. Appl. Physiol., 91, 1160-1167.
48. Ohd,J.F., Wikstrom,K. and Sjolander,A. (2000) Leukotrienes induce cell-survival signaling in intestinal epithelial cells. Gastroenterology, 119, 1007-1018.
49. de Jong,E.M., van Erp,P.E., van Vlijmen,I.M. and van de Kerkhof,P.C. (1992) The inter-relation between inflammation and epidermal proliferation in normal skin following epicutaneous application of leukotriene-B4 - an immunohistochemical study. Clin. Exp. Dermatol., 17, 413-420.
50. Wang,D., Buchanan,F.G., Wang,H., Dey,S.K. and DuBois,R.N. (2005) Prostaglandin E2 enhances intestinal adenoma growth via activation of the Ras-mitogen-activated protein kinase cascade. Cancer Res., 65, 1822-1829.
51. Kawamori,T., Uchiya,N., Sugimura,T. and Wakabayashi,K. (2003) Enhancement of colon carcinogenesis by prostaglandin E2 administration. Carcinogenesis, 24, 985-990.
52. Ebihara,K., Abe,F., Yamashita,T., Shibuya,K., Hayashi,E., Takahashi,K., Horinishi,H., Enomoto,M., Ishizuka,M. and Umezawa,H. (1986) The effect of ubenimex on N-methyl-N′-nitro-N-nitrosoguanidine-induced stomach tumor in rats. J. Antibiot. (Tokyo), 39, 966-970.
53. Scornik,O.A. and Botbol,V. (2001) Bestatin as an experimental tool in mammals. Curr. Drug Metab., 2, 67-85.
54. Chen,X., Li,N., Wang,S., Wu,N., Hong,J., Jiao,X., Krasna,M.J., Beer,D.G. and Yang,C.S. (2003) Leukotriene A4 hydrolase in rat and human esophageal adenocarcinomas and inhibitory effects of bestatin. J. Natl Cancer Inst., 95, 1053-1061.
55. Ichinose,Y., Genka,K., Koike,T., Kato,H., Watanabe,Y., Mori,T., Iioka,S., Sakuma,A. and Ohta,M. (2003) Randomized double-blind placebo-controlled trial of bestatin in patients with resected stage I squamous-cell lung carcinoma. J. Natl Cancer Inst., 95, 605-610.