Chemopreventive effects of pterostilbene on urethane-induced lung carcinogenesis in mice via the inhibition of EGFR-mediated pathways and the induction of apoptosis and autophagy

Journal of Agricultural and Food Chemistry

Volumn 60, Issue 46, 2012, Pages 11533-11541

  Chen, Rong Jane ^a,b   Tsai, Shang Jie ^a   Ho, Chi Tang ^c   Pan, Min Hsiung ^d   Ho, Yuan Soon ^b   Wu, Chih Hsiung ^b,e   Wang, Ying Jan ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c RUTGERS UNIVERSITY   (United States)

^d NATIONAL KAOHSIUNG UNIVERSITY OF APPLIED SCIENCES   (Taiwan)

^e TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

autophagy; chemopreventive; EGFR; pterostilbene; urethane

Indexed keywords

AUTOPHAGY; CHEMOPREVENTIVE; EGFR; PTEROSTILBENE; URETHANE;

CELL DEATH; DISEASES; ESTERS; MAMMALS; TUMORS;

BIOLOGICAL ORGANS;

EPIDERMAL GROWTH FACTOR RECEPTOR; PROTECTIVE AGENT; PTEROSTILBENE; STILBENE DERIVATIVE; URETHAN;

ANIMAL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DIVISION; CHEMICALLY INDUCED DISORDER; CHEMOPROPHYLAXIS; DOWN REGULATION; DRUG EFFECT; GENETICS; HUMAN; LUNG; LUNG TUMOR; MALE; METABOLISM; MOUSE; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; AUTOPHAGY; CELL DIVISION; CELL LINE, TUMOR; CHEMOPREVENTION; DOWN-REGULATION; HUMANS; LUNG; LUNG NEOPLASMS; MALE; MICE; PROTECTIVE AGENTS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; STILBENES; URETHANE;

MURINAE; MUS;

EID: 84869390181     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf302778a     Document Type: Article

References (41)

1. Jemal, A.; Bray, F.; Center, M. M.; Ferlay, J.; Ward, E.; Forman, D. Global cancer statistics CA Cancer J. Clin. 2011, 61, 69-90
2. Vahakangas, K. TP53 mutations in workers exposed to occupational carcinogens Hum. Mutat. 2003, 21, 240-251
3. Keith, R. L. Chemoprevention of lung cancer Proc. Am. Thorac. Soc. 2009, 6, 187-193
4. Rimando, A. M.; Cuendet, M.; Desmarchelier, C.; Mehta, R. G.; Pezzuto, J. M.; Duke, S. O. Cancer chemopreventive and antioxidant activities of pterostilbene, a naturally occurring analogue of resveratrol J. Agric. Food Chem. 2002, 50, 3453-3457
5. McCormack, D.; McFadden, D. Pterostilbene and cancer: current review J. Surg. Res. 2011, 173, e53-e61
6. Chiou, Y. S.; Tsai, M. L.; Nagabhushanam, K.; Wang, Y. J.; Wu, C. H.; Ho, C. T.; Pan, M. H. Pterostilbene is more potent than resveratrol in preventing azoxymethane (AOM)-induced colon tumorigenesis via activation of the NF-E2-related factor 2 (Nrf2)-mediated antioxidant signaling pathway J. Agric. Food Chem. 2011, 59, 2725-2733
7. Ferrer, P.; Asensi, M.; Segarra, R.; Ortega, A.; Benlloch, M.; Obrador, E.; Varea, M. T.; Asensio, G.; Jorda, L.; Estrela, J. M. Association between pterostilbene and quercetin inhibits metastatic activity of B16 melanoma Neoplasia 2005, 7, 37-47
8. Remsberg, C. M.; Yanez, J. A.; Ohgami, Y.; Vega-Villa, K. R.; Rimando, A. M.; Davies, N. M. Pharmacometrics of pterostilbene: preclinical pharmacokinetics and metabolism, anticancer, antiinflammatory, antioxidant and analgesic activity Phytother. Res. 2008, 22, 169-179
9. Chen, R. J.; Ho, C. T.; Wang, Y. J. Pterostilbene induces autophagy and apoptosis in sensitive and chemoresistant human bladder cancer cells Mol. Nutr. Food Res. 2010, 54, 1819-1832
10. Suh, N.; Paul, S.; Hao, X.; Simi, B.; Xiao, H.; Rimando, A. M.; Reddy, B. S. Pterostilbene, an active constituent of blueberries, suppresses aberrant crypt foci formation in the azoxymethane-induced colon carcinogenesis model in rats Clin. Cancer Res. 2007, 13, 350-355
11. Paul, S.; DeCastro, A. J.; Lee, H. J.; Smolarek, A. K.; So, J. Y.; Simi, B.; Wang, C. X.; Zhou, R.; Rimando, A. M.; Suh, N. Dietary intake of pterostilbene, a constituent of blueberries, inhibits the β-catenin/p65 downstream signaling pathway and colon carcinogenesis in rats Carcinogenesis 2010, 31, 1272-1278
12. Chiou, Y. S.; Tsai, M. L.; Wang, Y. J.; Cheng, A. C.; Lai, W. M.; Badmaev, V.; Ho, C. T.; Pan, M. H. Pterostilbene inhibits colorectal aberrant crypt foci (ACF) and colon carcinogenesis via suppression of multiple signal transduction pathways in azoxymethane-treated mice J. Agric. Food Chem. 2010, 58, 8833-8841
13. Ikeda, K.; Nomori, H.; Ohba, Y.; Shibata, H.; Mori, T.; Honda, Y.; Iyama, K.; Kobayashi, T. Epidermal growth factor receptor mutations in multicentric lung adenocarcinomas and atypical adenomatous hyperplasias J. Thorac. Oncol. 2008, 3, 467-471
14. Janku, F.; Garrido-Laguna, I.; Petruzelka, L. B.; Stewart, D. J.; Kurzrock, R. Novel therapeutic targets in non-small cell lung cancer J. Thorac. Oncol. 2011, 6, 1601-1612
15. Zhang, Z.; Stiegler, A. L.; Boggon, T. J.; Kobayashi, S.; Halmos, B. EGFR-mutated lung cancer: a paradigm of molecular oncology Oncotarget 2010, 1, 497-514
16. Uribe, P.; Gonzalez, S. Epidermal growth factor receptor (EGFR) and squamous cell carcinoma of the skin: molecular bases for EGFR-targeted therapy Pathol. Res. Pract. 2011, 207, 337-342
17. Tang, X.; Shigematsu, H.; Bekele, B. N.; Roth, J. A.; Minna, J. D.; Hong, W. K.; Gazdar, A. F.; Wistuba, I. I. EGFR tyrosine kinase domain mutations are detected in histologically normal respiratory epithelium in lung cancer patients Cancer Res. 2005, 65, 7568-7572
18. Malkinson, A. M. Primary lung tumors in mice as an aid for understanding, preventing, and treating human adenocarcinoma of the lung Lung Cancer 2001, 32, 265-279
19. Steeves, M. A.; Dorsey, F. C.; Cleveland, J. L. Targeting the autophagy pathway for cancer chemoprevention Curr. Opin. Cell Biol. 2010, 22, 218-225
20. Zhang, Y.; Wang, L.; Zhang, M.; Jin, M.; Bai, C.; Wang, X. Potential mechanism of interleukin-8 production from lung cancer cells: an involvement of EGF-EGFR-PI3K-Akt-Erk pathway J. Cell Physiol. 2012, 227, 35-43
21. Harhaj, E. W.; Dixit, V. M. Regulation of NF-B by deubiquitinases Immunol. Rev. 2012, 246, 107-124
22. Gullett, N. P.; Ruhul Amin, A. R.; Bayraktar, S.; Pezzuto, J. M.; Shin, D. M.; Khuri, F. R.; Aggarwal, B. B.; Surh, Y. J.; Kucuk, O. Cancer prevention with natural compounds Semin. Oncol. 2010, 37, 258-281
23. Lin, H. S.; Yue, B. D.; Ho, P. C. Determination of pterostilbene in rat plasma by a simple HPLC-UV method and its application in pre-clinical pharmacokinetic study Biomed. Chromatogr. 2009, 23, 1308-1315
24. Pan, M. H.; Chiou, Y. S.; Chen, W. J.; Wang, J. M.; Badmaev, V.; Ho, C. T. Pterostilbene inhibited tumor invasion via suppressing multiple signal transduction pathways in human hepatocellular carcinoma cells Carcinogenesis 2009, 30, 1234-1242
25. Birim, O.; Kappetein, A. P.; Takkenberg, J. J.; van Klaveren, R. J.; Bogers, A. J. Survival after pathological stage IA nonsmall cell lung cancer: tumor size matters Ann. Thorac. Surg. 2005, 79, 1137-1141
26. Hoffler, U.; El-Masri, H. A.; Ghanayem, B. I. Cytochrome P450 2E1 (CYP2E1) is the principal enzyme responsible for urethane metabolism: comparative studies using CYP2E1-null and wild-type mice J. Pharmacol. Exp. Ther. 2003, 305, 557-564
27. Ghanayem, B. I. Inhibition of urethane-induced carcinogenicity in cyp2e1-/- in comparison to cyp2e1+/+ mice Toxicol. Sci. 2007, 95, 331-339
28. Mikstacka, R.; Przybylska, D.; Rimando, A. M.; Baer-Dubowska, W. Inhibition of human recombinant cytochromes P450 CYP1A1 and CYP1B1 by trans-resveratrol methyl ethers Mol. Nutr. Food Res. 2007, 51, 517-524
29. Stearman, R. S.; Dwyer-Nield, L.; Zerbe, L.; Blaine, S. A.; Chan, Z.; Bunn, P. A., Jr.; Johnson, G. L.; Hirsch, F. R.; Merrick, D. T.; Franklin, W. A.; Baron, A. E.; Keith, R. L.; Nemenoff, R. A.; Malkinson, A. M.; Geraci, M. W. Analysis of orthologous gene expression between human pulmonary adenocarcinoma and a carcinogen-induced murine model Am. J. Pathol. 2005, 167, 1763-1775
30. Xu, C. X.; Jere, D.; Jin, H.; Chang, S. H.; Chung, Y. S.; Shin, J. Y.; Kim, J. E.; Park, S. J.; Lee, Y. H.; Chae, C. H.; Lee, K. H.; Beck, G. R., Jr.; Cho, C. S.; Cho, M. H. Poly(ester amine)-mediated, aerosol-delivered Akt1 small interfering RNA suppresses lung tumorigenesis Am. J. Res. Crit. Care Med. 2008, 178, 60-73
31. Aggarwal, B. B.; Kunnumakkara, A. B.; Harikumar, K. B.; Gupta, S. R.; Tharakan, S. T.; Koca, C.; Dey, S.; Sung, B. Signal transducer and activator of transcription-3, inflammation, and cancer: how intimate is the relationship? Ann. N.Y. Acad. Sci. 2009, 1171, 59-76
32. Luqman, S.; Pezzuto, J. M. NFB: a promising target for natural products in cancer chemoprevention Phytother. Res. 2010, 24, 949-963
33. Bhardwaj, A.; Sethi, G.; Vadhan-Raj, S.; Bueso-Ramos, C.; Takada, Y.; Gaur, U.; Nair, A. S.; Shishodia, S.; Aggarwal, B. B. Resveratrol inhibits proliferation, induces apoptosis, and overcomes chemoresistance through down-regulation of STAT3 and nuclear factor-B-regulated antiapoptotic and cell survival gene products in human multiple myeloma cells Blood 2007, 109, 2293-2302
34. Ramasamy, K.; Dwyer-Nield, L. D.; Serkova, N. J.; Hasebroock, K. M.; Tyagi, A.; Raina, K.; Singh, R. P.; Malkinson, A. M.; Agarwal, R. Silibinin prevents lung tumorigenesis in wild-type but not in iNOS-/- mice: potential of real-time micro-CT in lung cancer chemoprevention studies Clin. Cancer Res. 2011, 17, 753-761
35. Singhal, S.; Vachani, A.; Antin-Ozerkis, D.; Kaiser, L. R.; Albelda, S. M. Prognostic implications of cell cycle, apoptosis, and angiogenesis biomarkers in non-small cell lung cancer: a review Clin. Cancer Res. 2005, 11, 3974-3986
36. Kelly-Spratt, K. S.; Philipp-Staheli, J.; Gurley, K. E.; Hoon-Kim, K.; Knoblaugh, S.; Kemp, C. J. Inhibition of PI-3K restores nuclear p27Kip1 expression in a mouse model of Kras-driven lung cancer Oncogene 2009, 28, 3652-3662
37. Wang, Y.; James, M.; Wen, W.; Lu, Y.; Szabo, E.; Lubet, R. A.; You, M. Chemopreventive effects of pioglitazone on chemically induced lung carcinogenesis in mice Mol. Cancer Ther. 2010, 9, 3074-3082
38. Chu, I. M.; Hengst, L.; Slingerland, J. M. The Cdk inhibitor p27 in human cancer: prognostic potential and relevance to anticancer therapy Nat. Rev. Cancer 2008, 8, 253-267
39. Dworakowska, D.; Jassem, E.; Jassem, J.; Karmolinski, A.; Lapinski, M.; Tomaszewski, D.; Rzyman, W.; Jaskiewicz, K.; Sworczak, K.; Grossman, A. B. Prognostic value of the apoptotic index analysed jointly with selected cell cycle regulators and proliferation markers in non-small cell lung cancer Lung Cancer 2009, 66, 127-133
40. Abbas, T.; Dutta, A. p21 in cancer: intricate networks and multiple activities Nat. Rev. Cancer 2009, 9, 400-414
41. Mencher, S. K.; Wang, L. G. Promiscuous drugs compared to selective drugs (promiscuity can be a virtue) BMC Clin. Pharmacol. 2005, 5, 3