BLT2 promotes the invasion and metastasis of aggressive bladder cancer cells through a reactive oxygen species-linked pathway

Free Radical Biology and Medicine

Volumn 49, Issue 6, 2010, Pages 1072-1081

  Kim, Eun Young ^a   Seo, Ji Min ^a   Kim, Cheolmin ^a   Lee, Jung Eun ^a   Lee, Kyung Mi ^a   Kim, Jae Hong ^a  

^a Korea University College of Medicine   (South Korea)

Author keywords

Bladder cancer; BLT2; Free radicals; Invasion; Metastasis; Reactive oxygen species

Indexed keywords

2 (2,6 DIHYDROXYHEXYL) 6 (3 HYDROXY 1,5 UNDECADIENYL)PYRIDINE; 5 ETHYL 2 HYDROXY 4 [6 METHYL 6 (1H TETRAZOL 5 YL)HEPTYLOXY]ACETOPHENONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LEUKOTRIENE B4; LEUKOTRIENE B4 RECEPTOR; LEUKOTRIENE B4 RECEPTOR BLT2; LEUKOTRIENE RECEPTOR; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ADVANCED CANCER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLADDER CANCER; CANCER CELL; CANCER INVASION; CELL INVASION; COMPETITIVE INHIBITION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG METASTASIS; MALE; METASTASIS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSITIONAL CELL CARCINOMA;

MUS;

EID: 77955509484     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.06.023     Document Type: Article

References (46)

1. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Murray T., Thun M.J. Cancer statistics, 2008. CA Cancer J. Clin. 2008, 58:71-96.
2. Youssef R.F., Mitra A.P., Bartsch G., Jones P.A., Skinner D.G., Cote R.J. Molecular targets and targeted therapies in bladder cancer management. World J. Urol. 2009, 27:9-20.
3. Hayashi T., Nishiyama K., Shirahama T. Inhibition of 5-lipoxygenase pathway suppresses the growth of bladder cancer cells. Int. J. Urol. 2006, 13:1086-1091.
4. Cuendet M., Pezzuto J.M. The role of cyclooxygenase and lipoxygenase in cancer chemoprevention. Drug Metab. Drug Interact. 2000, 17:109-157.
5. Ihara A., Wada K., Yoneda M., Fujisawa N., Takahashi H., Nakajima A. Blockade of leukotriene B4 signaling pathway induces apoptosis and suppresses cell proliferation in colon cancer. J. Pharmacol. Sci. 2007, 103:24-32.
6. Tong W.G., Ding X.Z., Talamonti M.S., Bell R.H., Adrian T.E. LTB4 stimulates growth of human pancreatic cancer cells via MAPK and PI-3 kinase pathways. Biochem. Biophys. Res. Commun. 2005, 335:949-956.
7. Tong W.G., Ding X.Z., Hennig R., Witt R.C., Standop J., Pour P.M., Adrian T.E. Leukotriene B4 receptor antagonist LY293111 inhibits proliferation and induces apoptosis in human pancreatic cancer cells. Clin. Cancer Res. 2002, 8:3232-3242.
8. Rocconi R.P., Kirby T.O., Seitz R.S., Beck R., Straughn J.M., Alvarez R.D., Huh W.K. Lipoxygenase pathway receptor expression in ovarian cancer. Reprod. Sci. 2008, 15:321-326.
9. Sveinbjornsson B., Rasmuson A., Baryawno N., Wan M., Pettersen I., Ponthan F., Orrego A., Haeggstrom J.Z., Johnsen J.I., Kogner P. Expression of enzymes and receptors of the leukotriene pathway in human neuroblastoma promotes tumor survival and provides a target for therapy. FASEB J. 2008, 22:3525-3536.
10. el-Hakim I.E., Langdon J.D., Zakrzewski J.T., Costello J.F. Leukotriene B4 and oral cancer. Br. J. Oral Maxillofac. Surg. 1990, 28:155-159.
11. Heukamp I., Kilian M., Gregor J.I., Kiewert C., Schimke I., Kristiansen G., Walz M.K., Jacobi C.A., Wenger F.A. Impact of polyunsaturated fatty acids on hepato-pancreatic prostaglandin and leukotriene concentration in ductal pancreatic cancer-is there a correlation to tumour growth and liver metastasis?. Prostaglandins Leukotrienes Essent. Fatty Acids 2006, 74:223-233.
12. E.Y. Kim, J.M. Seo, K.J. Cho, J.H. Kim, Ras-induced invasion and metastasis are regulated by a leukotriene B4 receptor BLT2-linked pathway. Oncogene 29 1167-1178.
13. Choi J.A., Kim E.Y., Song H., Kim C., Kim J.H. Reactive oxygen species are generated through a BLT2-linked cascade in Ras-transformed cells. Free Radic. Biol. Med. 2008, 44:624-634.
14. 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.
15. Hennig R., Osman T., Esposito I., Giese N., Rao S.M., Ding X.Z., Tong W.G., Buchler M.W., Yokomizo T., Friess H., Adrian T.E. BLT2 is expressed in PanINs, IPMNs, pancreatic cancer and stimulates tumour cell proliferation. Br. J. Cancer 2008, 99:1064-1073.
16. Woo C.H., Kim T.H., Choi J.A., Ryu H.C., Lee J.E., You H.J., Bae Y.S., Kim J.H. Inhibition of receptor internalization attenuates the TNFα-induced ROS generation in non-phagocytic cells. Biochem. Biophys. Res. Commun. 2006, 351:972-978.
17. Dinney C.P. Therapy of invasive bladder cancer. Urology 2006, 67:56-59. discussion 60-51.
18. Stein J.P., Grossfeld G.D., Ginsberg D.A., Esrig D., Freeman J.A., Figueroa A.J., Skinner D.G., Cote R.J. Prognostic markers in bladder cancer: a contemporary review of the literature. J. Urol. 1998, 160:645-659.
19. Montie J.E., Abrahams N.A., Bahnson R.R., Eisenberger M.A., El-Galley R., Herr H.W., Hudes G.R., Kuzel T.M., Lange P.H., Patterson A., Pollack A., Richie J.P., Sexton W.J., Shipley W.U., Small E.J., Trump D.L., Walther P.J., Wilson T.G. Bladder cancer: clinical guidelines in oncology. J. Natl. Compr. Canc. Netw. 2006, 4:984-1014.
20. Yokomizo T., Kato K., Hagiya H., Izumi T., Shimizu T. Hydroxyeicosanoids bind to and activate the low affinity leukotriene B4 receptor, BLT2. J. Biol. Chem. 2001, 276:12454-12459.
21. Behrend L., Henderson G., Zwacka R.M. Reactive oxygen species in oncogenic transformation. Biochem. Soc. Trans. 2003, 31:1441-1444.
22. Hsu T.C., Young M.R., Cmarik J., Colburn N.H. Activator protein 1 (AP-1)- and nuclear factor κB (NF-κB)-dependent transcriptional events in carcinogenesis. Free Radic. Biol. Med. 2000, 28:1338-1348.
23. Kim H.J., Hawke N., Baldwin A.S. NF-kappaB and IKK as therapeutic targets in cancer. Cell Death Differ. 2006, 13:738-747.
24. Yoo M.H., Song H., Woo C.H., Kim H., Kim J.H. Role of the BLT2, a leukotriene B4 receptor, in Ras transformation. Oncogene 2004, 23:9259-9268.
25. Millikan R., Dinney C.P. The role of chemotherapy in the management of the patient with T3b bladder cancer. Semin. Urol. Oncol. 1996, 14:81-85.
26. Hennig R., Ventura J., Segersvard R., Ward E., Ding X.Z., Rao S.M., Jovanovic B.D., Iwamura T., Talamonti M.S., Bell R.H., Adrian T.E. LY293111 improves efficacy of gemcitabine therapy on pancreatic cancer in a fluorescent orthotopic model in athymic mice. Neoplasia 2005, 7:417-425.
27. Irani K., Xia Y., Zweier J.L., Sollott S.J., Der C.J., Fearon E.R., Sundaresan M., Finkel T., Goldschmidt-Clermont P.J. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 1997, 275:1649-1652.
28. Sattler M., Verma S., Shrikhande G., Byrne C.H., Pride Y.B., Winkler T., Greenfield E.A., Salgia R., Griffin J.D. The BCR/ABL tyrosine kinase induces production of reactive oxygen species in hematopoietic cells. J. Biol. Chem. 2000, 275:24273-24278.
29. Vafa O., Wade M., Kern S., Beeche M., Pandita T.K., Hampton G.M., Wahl G.M. c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol. Cell 2002, 9:1031-1044.
30. Wu W.S. The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev. 2006, 25:695-705.
31. Shinohara M., Shang W.H., Kubodera M., Harada S., Mitsushita J., Kato M., Miyazaki H., Sumimoto H., Kamata T. Nox1 redox signaling mediates oncogenic Ras-induced disruption of stress fibers and focal adhesions by down-regulating Rho. J. Biol. Chem. 2007, 282:17640-17648.
32. Mitsushita J., Lambeth J.D., Kamata T. The superoxide-generating oxidase Nox1 is functionally required for Ras oncogene transformation. Cancer Res. 2004, 64:3580-3585.
33. Shimada K., Nakamura M., Anai S., De Velasco M., Tanaka M., Tsujikawa K., Ouji Y., Konishi N. A novel human AlkB homologue, ALKBH8, contributes to human bladder cancer progression. Cancer Res. 2009, 69:3157-3164.
34. Vaquero E.C., Edderkaoui M., Pandol S.J., Gukovsky I., Gukovskaya A.S. Reactive oxygen species produced by NAD(P)H oxidase inhibit apoptosis in pancreatic cancer cells. J. Biol. Chem. 2004, 279:34643-34654.
35. Mochizuki T., Furuta S., Mitsushita J., Shang W.H., Ito M., Yokoo Y., Yamaura M., Ishizone S., Nakayama J., Konagai A., Hirose K., Kiyosawa K., Kamata T. Inhibition of NADPH oxidase 4 activates apoptosis via the AKT/apoptosis signal-regulating kinase 1 pathway in pancreatic cancer PANC-1 cells. Oncogene 2006, 25:3699-3707.
36. Yamaura M., Mitsushita J., Furuta S., Kiniwa Y., Ashida A., Goto Y., Shang W.H., Kubodera M., Kato M., Takata M., Saida T., Kamata T. NADPH oxidase 4 contributes to transformation phenotype of melanoma cells by regulating G2-M cell cycle progression. Cancer Res. 2009, 69:2647-2654.
37. Brar S.S., Corbin Z., Kennedy T.P., Hemendinger R., Thornton L., Bommarius B., Arnold R.S., Whorton A.R., Sturrock A.B., Huecksteadt T.P., Quinn M.T., Krenitsky K., Ardie K.G., Lambeth J.D., Hoidal J.R. NOX5 NAD(P)H oxidase regulates growth and apoptosis in DU 145 prostate cancer cells. Am. J. Physiol. Cell Physiol. 2003, 285:C353-369.
38. Si J., Fu X., Behar J., Wands J., Beer D.G., Souza R.F., Spechler S.J., Lambeth D., Cao W. NADPH oxidase NOX5-S mediates acid-induced cyclooxygenase-2 expression via activation of NF-kappaB in Barrett's esophageal adenocarcinoma cells. J. Biol. Chem. 2007, 282:16244-16255.
39. Levidou G., Saetta A.A., Korkolopoulou P., Papanastasiou P., Gioti K., Pavlopoulos P., Diamantopoulou K., Thomas-Tsagli E., Xiromeritis K., Patsouris E. Clinical significance of nuclear factor (NF)-kappaB levels in urothelial carcinoma of the urinary bladder. Virchows Arch. 2008, 452:295-304.
40. Xie D.H., Tang X.D., Xia S.J., Tan J.M., Wang X.H., Cai Y. Expression of NF-kappa B in human bladder cancer and its clinical significance. Ai Zheng 2002, 21:663-667.
41. Mian B.M., Dinney C.P., Bermejo C.E., Sweeney P., Tellez C., Yang X.D., Gudas J.M., McConkey D.J., Bar-Eli M. Fully human anti-interleukin 8 antibody inhibits tumor growth in orthotopic bladder cancer xenografts via down-regulation of matrix metalloproteases and nuclear factor-kappaB. Clin. Cancer Res. 2003, 9:3167-3175.
42. Karashima T., Sweeney P., Kamat A., Huang S., Kim S.J., Bar-Eli M., McConkey D.J., Dinney C.P. Nuclear factor-kappaB mediates angiogenesis and metastasis of human bladder cancer through the regulation of interleukin-8. Clin. Cancer Res. 2003, 9:2786-2797.
43. Di Carlo A., Terracciano D., Mariano A., Macchia V. Urinary gelatinase activities (matrix metalloproteinases 2 and 9) in human bladder tumors. Oncol. Rep. 2006, 15:1321-1326.
44. Kawamura K., Kamiya N., Suyama T., Shimbo M., Oosumi N., Suzuki H., Ueda T., Tobe T., Igarashi T., Ito H., Ishikura H. In situ gelatinolytic activity correlates with tumor progression and prognosis in patients with bladder cancer. J. Urol. 2004, 172:1480-1484.
45. Kupferman M.E., Fini M.E., Muller W.J., Weber R., Cheng Y., Muschel R.J. Matrix metalloproteinase 9 promoter activity is induced coincident with invasion during tumor progression. Am. J. Pathol. 2000, 157:1777-1783.
46. Bernhard E.J., Muschel R.J., Hughes E.N. Mr 92, 000 gelatinase release correlates with the metastatic phenotype in transformed rat embryo cells. Cancer Res. 1990, 50:3872-3877.