The dietary terpene lupeol targets colorectal cancer cells with constitutively active Wnt/β-catenin signaling

Molecular Nutrition and Food Research

Volumn 57, Issue 11, 2013, Pages 1950-1958

  Tarapore, Rohinton S ^a,b   Siddiqui, Imtiaz A ^a,b   Adhami, Vaqar M ^a   Spiegelman, Vladimir S ^a   Mukhtar, Hasan ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

catenin pathway; Chemoprevention; Colorectal cancer; Dietary triterpene; Lupeol; Wnt

Indexed keywords

BETA CATENIN; CTNNB1 PROTEIN, HUMAN; LUPEOL; PENTACYCLIC TRITERPENE;

APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; CHEMOPROPHYLAXIS; COLORECTAL CANCER; COLORECTAL TUMOR; DIETARY TRITERPENE; DOSE RESPONSE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE; WNT; WNT SIGNALING PATHWAY; Β CATENIN PATHWAY;

CHEMOPREVENTION; COLORECTAL CANCER; DIETARY TRITERPENE; LUPEOL; WNT; Β CATENIN PATHWAY;

APOPTOSIS; BETA CATENIN; CELL LINE, TUMOR; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; COLORECTAL NEOPLASMS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; PENTACYCLIC TRITERPENES; PHOSPHORYLATION; WNT SIGNALING PATHWAY;

EID: 84886769058     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201300155     Document Type: Article

References (44)

1. Phelps, R. A., Broadbent, T. J., Stafforini, D. M., Jones, D. A., New perspectives on APC control of cell fate and proliferation in colorectal cancer. Cell Cycle 2009, 8, 2549-2556.
2. Chandra, S. H., Wacker, I., Appelt, U. K., Behrens, J. et al., A common role for various human truncated adenomatous polyposis coli isoforms in the control of beta-catenin activity and cell proliferation. PloS One 2012, 7, e34479.
3. Siegel, R., Naishadham, D., Jemal, A., Cancer statistics, 2013. CA Cancer J. Clin. 2013, 63, 11-30.
4. Giles, R. H., van Es, J. H., Clevers, H., Caught up in a Wnt storm: Wnt signaling in cancer. Biochim. Biophys. Acta 2003, 1653, 1-24.
5. Lustig, B., Behrens, J., The Wnt signaling pathway and its role in tumor development. J. Cancer Res. Clin. Oncol. 2003, 129, 199-221.
6. Weeraratna, A. T., A Wnt-er wonderland: the complexity of Wnt signaling in melanoma. Cancer Metastasis Rev. 2005, 24, 237-250.
7. Korinek, V., Barker, N., Morin, P. J., van Wichen, D. et al., Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 1997, 275, 1784-1787.
8. Elcheva, I., Tarapore, R. S., Bhatia, N., Spiegelman, V. S., Overexpression of mRNA-binding protein CRD-BP in malignant melanomas. Oncogene 2008, 27, 5069-5074.
9. Fuchs, S. Y., Ougolkov, A. V., Spiegelman, V. S., Minamoto, T., Oncogenic beta-catenin signaling networks in colorectal cancer. Cell Cycle 2005, 4, 1522-1539.
10. Kim, T. H., Xiong, H., Zhang, Z., Ren, B., beta-Catenin activates the growth factor endothelin-1 in colon cancer cells. Oncogene 2005, 24, 597-604.
11. Taketo, M. M., Shutting down Wnt signal-activated cancer. Nat. Genet. 2004, 36, 320-322.
12. Morin, P. J., Sparks, A. B., Korinek, V., Barker, N. et al., Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997, 275, 1787-1790.
13. Beveridge, T. H., Li, T. S., Drover, J. C., Phytosterol content in American ginseng seed oil. J. Agric. Food Chem. 2002, 50, 744-750.
14. Fernandez, M. A., de las Heras, B., Garcia, M. D., Saenz, M. T. et al., New insights into the mechanism of action of the anti-inflammatory triterpene lupeol. J. Pharm. Pharmacol. 2001, 53, 1533-1539.
15. Imam, S., Azhar, I., Hasan, M. M., Ali, M. S. et al., Two triterpenes lupanone and lupeol isolated and identified from Tamarindus indica linn. Pak. J. Pharm. Sci. 2007, 20, 125-127.
16. Saleem, M., Lupeol, a novel anti-inflammatory and anti-cancer dietary triterpene. Cancer Lett. 2009, 285, 109-115.
17. You, Y. J., Nam, N. H., Kim, Y., Bae, K. H. et al., Antiangiogenic activity of lupeol from Bombax ceiba. Phytother. Res. 2003, 17, 341-344.
18. Lima, L. M., Perazzo, F. F., Tavares Carvalho, J. C., Bastos, J. K., Anti-inflammatory and analgesic activities of the ethanolic extracts from Zanthoxylum riedelianum (Rutaceae) leaves and stem bark. J. Pharm. Pharmacol. 2007, 59, 1151-1158.
19. Saleem, M., Kaur, S., Kweon, M. H., Adhami, V. M. et al., Lupeol, a fruit and vegetable based triterpene, induces apoptotic death of human pancreatic adenocarcinoma cells via inhibition of Ras signaling pathway. Carcinogenesis 2005, 26, 1956-1964.
20. Vasconcelos, J. F., Teixeira, M. M., Barbosa-Filho, J. M., Lucio, A. S. et al., The triterpenoid lupeol attenuates allergic airway inflammation in a murine model. Int. Immunopharmacol. 2008, 8, 1216-1221.
21. Tarapore, R. S., Siddiqui, I. A., Saleem, M., Adhami, V. M. et al., Specific targeting of Wnt/beta-catenin signaling in human melanoma cells by a dietary triterpene lupeol. Carcinogenesis 2010, 31, 1844-1853.
22. Saleem, M., Maddodi, N., Abu Zaid, M., Khan, N. et al., Lupeol inhibits growth of highly aggressive human metastatic melanoma cells in vitro and in vivo by inducing apoptosis. Clin. Cancer Res. 2008, 14, 2119-2127.
23. Fang, D., Hawke, D., Zheng, Y., Xia, Y. et al., Phosphorylation of beta-catenin by AKT promotes beta-catenin transcriptional activity. J. Biol. Chem. 2007, 282, 11221-11229.
24. Taurin, S., Sandbo, N., Qin, Y., Browning, D. et al., Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase. J. Biol. Chem. 2006, 281, 9971-9976.
25. Hino, S., Tanji, C., Nakayama, K. I., Kikuchi, A., Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase stabilizes beta-catenin through inhibition of its ubiquitination. Mol. Cell Biol. 2005, 25, 9063-9072.
26. Afaq, F., Adhami, V. M., Ahmad, N., Mukhtar, H., Botanical antioxidants for chemoprevention of photocarcinogenesis. Front Biosci. 2002, 7, d784-d792.
27. Becker, J. C., Kirkwood, J. M., Agarwala, S. S., Dummer, R. et al., Molecularly targeted therapy for melanoma: current reality and future options. Cancer 2006, 107, 2317-2327.
28. Khan, N., Afaq, F., Mukhtar, H., Cancer chemoprevention through dietary antioxidants: progress and promise. Antioxid. Redox. Signal 2008, 10, 475-510.
29. Nichenametla, S. N., Taruscio, T. G., Barney, D. L., Exon, J. H., A review of the effects and mechanisms of polyphenolics in cancer. Crit. Rev. Food Sci. Nutr. 2006, 46, 161-183.
30. Hata, K., Mukaiyama, T., Tsujimura, N., Sato, Y. et al., Differentiation-inducing activity of lupane triterpenes on a mouse melanoma cell line. Cytotechnology 2006, 52, 151-158.
31. Ogiwara, K., Hata, K., Melanoma cell differentiation induced by lupeol separates into two stages: morphological and functional changes. J. Nat. Med. 2009, 63, 323-326.
32. Tarapore, R. S., Siddiqui, I. A., Mukhtar, H., Modulation of Wnt/beta-catenin signaling pathway by bioactive food components. Carcinogenesis 2012, 33, 483-491.
33. Prasad, S., Kalra, N., Shukla, Y., Induction of apoptosis by lupeol and mango extract in mouse prostate and LNCaP cells. Nutr. Cancer 2008, 60, 120-130.
34. Saleem, M., Murtaza, I., Witkowsky, O., Kohl, A. M. et al., Lupeol triterpene, a novel diet-based microtubule targeting agent: disrupts survivin/cFLIP activation in prostate cancer cells. Biochem. Biophys. Res. Commun. 2009, 388, 576-582.
35. Zhang, L., Zhang, Y., Yang, X., Lv, Z., Lupeol, a dietary triterpene, inhibited growth, and induced apoptosis through down-regulation of DR3 in SMMC7721 cells. Cancer Invest. 2009, 27, 163-170.
36. Deng, J., Miller, S. A., Wang, H. Y., Xia, W. et al., Beta-catenin interacts with and inhibits NF-kappa B in human colon and breast cancer. Cancer Cell 2002, 2, 323-334.
37. Zhang, Z., Deb, A., Pachori, A., He, W. et al., Secreted frizzled related protein 2 protects cells from apoptosis by blocking the effect of canonical Wnt3a. J. Mol. Cell Cardiol. 2009, 46, 370-377.
38. Noubissi, F. K., Elcheva, I., Bhatia, N., Shakoori, A. et al., CRD-BP mediates stabilization of betaTrCP1 and c-myc mRNA in response to beta-catenin signalling. Nature 2006, 441, 898-901.
39. Jho, E. H., Zhang, T., Domon, C., Joo, C. K. et al., Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell Biol. 2002, 22, 1172-1183.
40. Yan, D., Wiesmann, M., Rohan, M., Chan, V. et al., Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/beta-catenin signaling is activated in human colon tumors. Proc. Natl. Acad. Sci. USA 2001, 98, 14973-14978.
41. Roose, J., Huls, G., van Beest, M., Moerer, P. et al., Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science 1999, 285, 1923-1926.
42. Elcheva, I., Tarapore, R. S., Bhatia, N., Spiegelman, V. S., Overexpression of mRNA-binding protein CRD-BP in malignant melanomas. Oncogene 2008, 27, 5069-5074.
43. Chen, B., Dodge, M. E., Tang, W., Lu, J. et al., Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat. Chem. Biol. 2009, 5, 100-107.
44. MacDonald, B. T., Tamai, K., He, X., Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 2009, 17, 9-26.