Tea polyphenols EGCG and TF restrict tongue and liver carcinogenesis simultaneously induced by N-nitrosodiethylamine in mice

Toxicology and Applied Pharmacology

Volumn 300, Issue , 2016, Pages 34-46

  Sur, Subhayan ^a   Pal, Debolina ^a   Roy, Rituparna ^a   Barua, Atish ^a   Roy, Anup ^b   Saha, Prosenjit ^a   Panda, Chinmay Kumar ^a  

^a CHITTARANJAN NATIONAL CANCER INSTITUTE   (India)

^b NORTH BENGAL MEDICAL COLLEGE   (India)

Author keywords

EGCG; Gli1; Liver carcinogenesis; TF; Tongue carcinogenesis; catenin

Indexed keywords

BETA CATENIN; CD44V ANTIGEN; DIETHYLNITROSAMINE; EPIGALLOCATECHIN GALLATE; THEAFLAVIN; UVOMORULIN; BIFLAVONOID; CATECHIN; POLYPHENOL; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY WEIGHT; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LIVER CARCINOGENESIS; MOUSE; MOUTH CAVITY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PREVALENCE; REGULATOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TONGUE CANCER; TONGUE CARCINOGENESIS; UPREGULATION; WNT SIGNALING PATHWAY; ANALOGS AND DERIVATIVES; ANIMAL; CARCINOGENESIS; CHEMICALLY INDUCED; DRUG EFFECTS; LIVER NEOPLASMS; METABOLISM; PATHOLOGY; TONGUE NEOPLASMS;

ANIMALS; APOPTOSIS; BETA CATENIN; BIFLAVONOIDS; BODY WEIGHT; CARCINOGENESIS; CATECHIN; CELL PROLIFERATION; DIETHYLNITROSAMINE; FEMALE; HEDGEHOG PROTEINS; LIVER NEOPLASMS; MICE; POLYPHENOLS; TONGUE NEOPLASMS; UP-REGULATION; WNT PROTEINS;

EID: 84962739111     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2016.03.016     Document Type: Article

References (49)

1. Aguiló R., Macià F., Porta M., Casamitjana M., Minguella J., Novoa A.M. Multiple independent primary cancers do not adversely affect survival of the lung cancer patient. Eur. J. Cardiothorac. Surg. 2008, 34:1075-1080.
2. Annabi B., Currie J.C., Moghrabi A., Béliveau R. Inhibition of HuR and MMP-9 expression in macrophage-differentiated HL-60 myeloid leukemia cells by green tea polyphenol EGCG. Leuk. Res. 2007, 31:1277-1284.
3. Carpenter R.L., Lo H.W. Hedgehog pathway and GLI1 isoforms in human cancer. Discov. Med. 2012, 13:105-113.
4. Chen J.S., Li H.S., Huang J.Q., Zhang L.J., Chen X.L., Wang Q., Lei J., Feng J.T., Liu Q., Huang X.H. Down-regulation of Gli-1 inhibits hepatocellular carcinoma cell migration and invasion. Mol. Cell. Biochem. 2014, 393:283-291.
5. Chin D., Boyle G.M., Theile D.R., Parsons P.G., Coman W.B. Molecular introduction to head and neck cancer HNSCC. carcinogenesis. Br. J. Plast. Surg. 2004, 57:595-602.
6. de Oliveira Santos D., Loyola A.M., Cardoso S.V., Chammas R., Liu F.T., de Faria P.R. Hedgehog signaling pathway mediates tongue tumorigenesis in wild-type mice but not in Gal3-deficient mice. Exp. Mol. Pathol. 2014, 97:332-337.
7. Dimitrova K., Stoehr M., Dehghani F., Dietz A., Wichmann G., Bertolini J., Mozet C. Overexpression of the Hedgehog signalling pathway in head and neck squamous cell carcinoma. Onkologie 2013, 36:279-286.
8. Eberl M., Klingler S., Mangelberger D., Loipetzberger A., Damhofer H., Zoidl K., Schnidar H., Hache H., Bauer H.C., Solca F., Hauser-Kronberger C., Ermilov A.N., Verhaegen M.E., Bichakjian C.K., Dlugosz A.A., Nietfeld W., Sibilia M., Lehrach H., Wierling C., Aberger F. Hedgehog-EGFR cooperation response genes determine the oncogenic phenotype of basal cell carcinoma and tumour-initiating pancreatic cancer cells. EMBO. Mol. Med. 2012, 4:218-233.
9. El Khatib M., Kalnytska A., Palagani V., Kossatz U., Manns M.P., Malek N.P., Wilkens L., Plentz R.R. Inhibition of hedgehog signaling attenuates carcinogenesis in vitro and increases necrosis of cholangiocellular carcinoma. Hepatology 2013, 57:1035-1045.
10. Godeke J., Maier S., Eichenmüller M., Müller-Höcker J., von Schweinitz D., Kappler R. Epigallocatechin-3-gallate inhibits hepatoblastoma growth by reactivating the Wnt inhibitor SFRP1. Nutr. Cancer 2013, 65:1200-1207.
11. Guturi K.K., Mandal T., Chatterjee A., Sarkar M., Bhattacharya S., Chatterjee U., Ghosh M.K. Mechanism of β-catenin-mediated transcriptional regulation of epidermal growth factor receptor expression in glycogen synthase kinase 3 β-inactivated prostate cancer cells. J. Biol. Chem. 2012, 287:18287-18296.
12. Halder B., Das Gupta S., Gomes A. Black tea polyphenols induce human leukemic cell cycle arrest by inhibiting Akt signaling, possible involvement of Hsp90, Wnt/β-catenin signaling and FOXO1. FEBS. J. 2012, 279:2876-2891.
13. Herrold K.M. Effect of route of administration on the carcinogenic action of diethylnitrosamine (N-ditrosodiethylamine). Br. J. Cancer 1964, 18:763-767.
14. Herrold K.M., Dunham L.J. Induction of tumors in the Syrian hamster with diethylnitrosamine (N-nitrosodiethylamine). Cancer Res. 1963, 23:773-777.
15. Hirose M., Hoshiya T., Akagi K., Takahashi S., Hara Y., Ito N. Effects of green tea catechins in a rat multi-organ carcinogenesis model. Carcinogenesis 1993, 14:1549-1553.
16. Jain S., Chang T.T., Hamilton J.P., Lin S.Y., Lin Y.J., Evans A.A., Selaru F.M., Lin P.W., Chen S.H., Block T.M., Hu C.T., Song W., Meltzer S.J., Su Y.H. Methylation of the CpG sites only on the sense strand of the APC gene is specific for hepatocellular carcinoma. PLoS ONE 2011, 6.
17. Ji J., Wang X.W. Clinical implications of cancer stem cell biology in hepatocellular carcinoma. Semin. Oncol. 2012, 39:461-472.
18. Khan M.S., Halagowder D., Devaraj S.N. Methylated chrysin induces co-ordinated attenuation of the canonical Wnt and NF-kB signaling pathway and upregulates apoptotic gene expression in the early hepatocarcinogenesis rat model. Chem. Biol. Interact. 2011, 193:12-21.
19. Kim D.J., Han B.S., Ahn B., Hasegawa R., Shirai T., Ito N., Tsuda H. Enhancement by indole-3-carbinol of liver and thyroid gland neoplastic development in a rat medium-term multiorgan carcinogenesis model. Carcinogenesis 1997, 18:377-381.
20. Lee S.H., Nam H.J., Kang H.J., Kwon H.W., Lim Y.C. Epigallocatechin-3-gallate attenuates head and neck cancer stem cell traits through suppression of Notch pathway. Eur. J. Cancer 2013, 49:3210-3218.
21. Li X., Deng W., Lobo-Ruppert S.M., Ruppert J.M. Gli1 acts through Snail and E-cadherin to promote nuclear signaling by beta-catenin. Oncogene 2007, 371:23-34.
22. Llovet J.M., Bruix J. Molecular targeted therapies in hepatocellular carcinoma. Hepatology 2008, 48:1312-1327.
23. Maeda O., Kondo M., Fujita T., Usami N., Fukui T., Shimokata K., Ando T., Goto H., Sekido Y. Enhancement of GLI1-transcriptional activity by beta-catenin in human cancer cells. Oncol. Rep. 2006, 16:91-96.
24. Manna S., Mukherjee S., Roy A., Das S., Panda C.K. Tea polyphenols can restrict benzo[a]pyrene-induced lung carcinogenesis by altered expression of p53-associated genes and H-ras, c-myc and cyclin D1. J. Nutr. Biochem. 2009, 20:337-349.
25. McCabe J.M., Leahy D.J. Smoothened goes molecular: new pieces in the hedgehog signaling puzzle. J. Biol. Chem. 2015, 290:3500-3507.
26. Mercer K.E., Hennings L., Sharma N., Lai K., Cleves M.A., Wynne R.A., Badqer T.M., Ronis M.J. Alcohol consumption promotes diethylnitrosamine-induced hepatocarcinogenesis in male mice through activation of the Wnt/β-catenin signaling pathway. Cancer Prev. Res. (Phila) 2014, 7:675-685.
27. Noubissi F.K., Goswami S., Sanek N.A., Kawakami K., Minamoto T., Moser A., Grinblat Y., Spiegelman V.S. Wnt signaling stimulates transcriptional outcome of the Hedgehog pathway by stabilizing GLI1 mRNA. Cancer Res. 2009, 69:8572-8578.
28. Osei-Sarfo K., Tang X.H., Urvalek A.M., Scognamiglio T., Gudas L.J. The molecular features of tongue epithelium treated with the carcinogen 4-nitroquinoline-1-oxide and alcohol as a model for HNSCC. Carcinogenesis 2013, 34:2673-2681.
29. Pal D., Sur S., Mandal S., Das A., Roy A., Das S., Panda C.K. Prevention of liver carcinogenesis by amarogentin through modulation of G1/S cell cycle check point and induction of apoptosis. Carcinogenesis 2012, 33:2424-2431.
30. Perez A., Neskey D.M., Wen J., Pereira L., Reategui E.P., Goodwin W.J., Carraway K.L., Franzmann E.J. CD44 interacts with EGFR and promotes head and neck squamous cell carcinoma initiation and progression. Oral Oncol. 2013, 49:306-313.
31. Pérez-Sayáns M., Suárez-Peñaranda J.M., Herranz-Carnero M., Gayoso-Diz P., Barros-Angueira F., Gándara-Rey J.M., García-García A. The role of the adenomatous polyposis coli (APC) in oral squamous cell carcinoma. Oral Oncol. 2012, 48:56-60.
32. Perrone F., Suardi S., Pastore E., Casieri P., Orsenigo M., Caramuta S., Dagrada G., Losa M., Licitra L., Bossi P., Staurengo S., Oggionni M., Locati L., Cantu G., Squadrelli M., Carbone A., Pierotti M.A., Pilotti S. Molecular and cytogenetic subgroups of oropharyngeal squamous cell carcinoma. Clin. Cancer Res. 2006, 12:6643-6651.
33. Pez F., Lopez A., Kim M., Wands J.R., Caron de Fromentel C., Merle P. Wnt signaling and hepatocarcinogenesis: molecular targets for the development of innovative anticancer drugs. J. Hepatol. 2013, 59:1107-1117.
34. Pfeifer G.P., Denissenko M.F., Olivier M., Tretyakova N., Hecht S.S., Hainaut P. Tobacco smoke carcinogens, DNA damage and p53 mutations in smoking-associated cancers. Oncogene 2002, 21:7435-7451.
35. Philips G.M., Chan I.S., Swiderska M., Schroder V.T., Guy C., Karaca G.F., Moylan C., Venkatraman T., Feuerlein S., Syn W.K., Jung Y., Witek R.P., Choi S., Michelotti G.A., Rangwala F., Merkle E., Lascola C., Diehl A.M. Hedgehog signaling antagonist promotes regression of both liver fibrosis and hepatocellular carcinoma in a murine model of primary liver cancer. PLoS ONE 2011, 6.
36. Sarkar F.H., Li Y., Wang Z., Kong D. The role of nutraceuticals in the regulation of Wnt and Hedgehog signaling in cancer. Cancer Metastasis Rev. 2010, 29:383-394.
37. Singh B.N., Doyle M.J., Weaver C.V., Koyano-Nakagawa N., Garry D.J. Hedgehog and Wnt coordinate signaling in myogenic progenitors and regulate limb regeneration. Dev. Biol. 2012, 371:23-34.
38. Sogabe Y., Suzuki H., Toyota M., Ogi K., Imai T., Nojima M., Sasaki Y., Hiratsuka H., Tokino T. Epigenetic inactivation of SFRP genes in oral squamous cell carcinoma. Int. J. Oncol. 2008, 32:1253-1261.
39. Srinivasan P., Suchalatha S., Babu P.V., Devi R.S., Narayan S., Sabitha K.E., Shyamala Devi C.S. Chemopreventive and therapeutic modulation of green tea polyphenols on drug metabolizing enzymes in 4-Nitroquinoline 1-oxide induced oral cancer. Chem. Biol. Interact. 2008, 172:224-234.
40. Sumi T., Shirakami Y., Shimizu M., Kochi T., Ohno T., Kubota M., Shiraki M., Tsurumi H., Tanaka T., Moriwaki H. (-)-Epigallocatechin-3-gallate suppresses hepatic preneoplastic lesions developed in a novel rat model of non-alcoholic steatohepatitis. Springerplus 2013, 2:690.
41. Sur S., Pal D., Mandal S., Roy A., Panda C.K. Tea polyphenols epigallocatechin gallete (EGCG) and theaflavin (TF) restrict mouse liver carcinogenesis through modulation of self renewal Wnt and hedgehog pathways. J. Nutr. Biochem. 2015, (pii, S0955-286315.00210-7. (ahead of print)).
42. Takagi H., Sasaki S., Suzuki H., Toyota M., Maruyama R., Nojima M., Yamamoto H., Omata M., Tokino T., Imai K., Shinomura Y. Frequent epigenetic inactivation of SFRP genes in hepatocellular carcinoma. J. Gastroenterol. 2008, 43:378-389.
43. Tan X., Apte U., Micsenyi A., Kotsagrelos E., Luo J.H., Ranganathan S., Monga D.K., Bell A., Michalopoulos G.K., Monga S.P. Epidermal growth factor receptor: a novel target of the Wnt/beta-catenin pathway in liver. Gastroenterology 2005, 129:285-302.
44. Tang S.N., Fu J., Nall D., Rodova M., Shankar S., Srivastava R.K. Inhibition of sonic hedgehog pathway and pluripotency maintaining factors regulate human pancreatic cancer stem cell characteristics. Int. J. Cancer 2012, 131:30-40.
45. Thakur V.S., Gupta K., Gupta S. The chemopreventive and chemotherapeutic potentials of tea polyphenols. Curr. Pharm. Biotechnol. 2012, 13:191-199.
46. van Veelen W., Le N.H., Helvensteijn W., Blonden L., Theeuwes M., Bakker E.R., Franken P.F., van Gurp L., Meijlink F., van der Valk M.A., Kuipers E.J., Fodde R., Smits R. β-catenin tyrosine 654 phosphorylation increases Wnt signalling and intestinal tumorigenesis. Gut 2011, 60:1204-1212.
47. Wang Z.Y., Hong J.Y., Huang M.T., Reuhl K.R., Conney A.H., Yang C.S. Inhibition of N-nitrosodiethylamine- and 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-induced tumorigenesis in A/J mice by green tea and black tea. Cancer Res. 1992, 52:1943-1947.
48. Williams H.K. Molecular pathogenesis of oral squamous carcinoma. Mol. Pathol. 2000, 53:165-172.
49. Zeilstra J., Joosten S.P., Dokter M., Verwiel E., Spaargaren M., Pals S.T. Deletion of the WNT target and cancer stem cell marker CD44 in Apc (Min/+) mice attenuates intestinal tumorigenesis. Cancer Res. 2008, 68:3655-3661.