Olive phenolics as c-Met inhibitors: (-)-Oleocanthal attenuates cell proliferation, invasiveness, and tumor growth in breast cancer models

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Akl, Mohamed R ^a   Ayoub, Nehad M ^b   Mohyeldin, Mohamed M ^a   Busnena, Belnaser A ^a   Foudah, Ahmed I ^a   Liu, Yong Yu ^a   Ei Sayed, Khalid A ^a  

^a UNIVERSITY OF LOUISIANA AT MONROE   (United States)

^b JORDAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Jordan)

Author keywords

[No Author keywords available]

Indexed keywords

OLEOCANTHAL; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SECOIRIDOID; UNCLASSIFIED DRUG; ALDEHYDE; ANTINEOPLASTIC AGENT; MITOGEN ACTIVATED PROTEIN KINASE; PHENOL DERIVATIVE; PROTEIN KINASE B; PROTEIN KINASE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL MIGRATION; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; FEMALE; IN VIVO STUDY; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; TUMOR INVASION; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BREAST TUMOR; CELL CYCLE; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; INTRACELLULAR SPACE; METABOLISM; OLIVE TREE; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

ALDEHYDES; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HEPATOCYTE GROWTH FACTOR; HUMANS; INTRACELLULAR SPACE; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM INVASIVENESS; OLEA; PHENOLS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MET; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84901334559     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097622     Document Type: Article

References (48)

1. American Cancer Society, http://www.cancer.org/Cancer/BreastCancer/ OverviewGuide/breast-cancer-overview-key-statistics (Accessed November 2013).
2. Giordano S, Ponzetto C, Di Renzo M, Cooper C, Comoglio P (1989) Tyrosine kinase receptor indistinguishable from the c-met protein. Nature 11: 155-156. (Pubitemid 19122275)
3. Park M, Dean M, Kaul K, Braun MJ, Gonda MA, et al. (1987) Sequence of MET protooncogene cDNA has features characteristic of the tyrosine kinase family of growth-factor receptors. Proc Natl Acad Sci USA 84: 6379-6383. (Pubitemid 18002806)
4. Eder JP, Woude GFV, Boerner SA, LoRusso PM (2009) Novel therapeutic inhibitors of the c-Met signaling pathway in cancer. Clin Cancer Res 15: 2207-2214.
5. Peruzzi B, Bottaro DP (2006) Targeting the c-Met signaling pathway in cancer. Clin Cancer Res 12: 3657-3660. (Pubitemid 44000247)
6. Castro NE, Lange CA (2010) Breast tumor kinase and extracellular signal-regulated kinase 5 mediate Met receptor signaling to cell migration in breast cancer cells. Breast Cancer Res 12: R60.
7. Chen H-Y, Shen C-H, Tsai Y-T, Lin F-C, Huang Y-P, et al. (2004) Brk activates rac1 and promotes cell migration and invasion by phosphorylating paxillin. Mol Cell Biol 24: 10558-10572. (Pubitemid 39603116)
8. Francone TD, Landmann RG, Chen C-T, Sun MY, Kuntz EJ, et al. (2007) Novel xenograft model expressing human hepatocyte growth factor shows ligand-dependent growth of c-Met-expressing tumors. Mol Cancer Ther 6: 1460-1466. (Pubitemid 46712010)
9. Nuwer R (2013) Mediterranean Mystery. Scientific American Magazine 308: 22.
10. Rosignoli P, Fuccelli R, Fabiani R, Servili M, Morozzi G (2013) Effect of olive oil phenols on the production of inflammatory mediators in freshly isolated human monocytes. J Nutr Biochem 24: 1513-1519.
11. Abuznait AH, Qosa H, Busnena BA, El Sayed KA, Kaddoumi A (2013) Olive-oil-derived oleocanthal enhances b-amyloid clearance as a potential nNeuroprotective mechanism against Alzheimer's disease: In vitro and in vivo studies. ACS Chem Neurosci 4: 973-982.
12. Busnena BA, Foudah AI, Melancon T, El Sayed KA (2013) Olive secoiridoids and semisynthetic bioisostere analogues for the control of metastatic breast cancer. Bioorg Med Chem 21: 2117-2127.
13. Scotece M, Gómez R, Conde J, Lopez V, Gómez-Reino J, et al. (2013) Oleocanthal inhibits proliferation and MIP-1 expression in human multiple myeloma cells. Curr Med Chem 20: 2467-2475.
14. Monti MC, Margarucci L, Tosco A, Riccio R, Casapullo A (2011) New insights on the interaction mechanism between tau protein and oleocanthal, an extra-virgin olive-oil bioactive component. Food Funct 2: 423-428.
15. Monti MC, Margarucci L, Riccio R, Casapullo A (2012) Modulation of tau protein fibrillization by oleocanthal. J Nat Prod 75: 1584-1588.
16. Lucas L, Russell A, Keast R (2011) Molecular mechanisms of inflammation. Anti-inflammatory benefits of virgin olive oil and the phenolic compound oleocanthal. Curr Pharm Des 17: 754-768.
17. Elnagar AY, Sylvester PW, El Sayed KA (2011) (-)-Oleocanthal as a c-Met inhibitor for the control of metastatic breast and prostate cancers. Planta Medica 77: 1013-1019.
18. Iacono A, Gómez R, Sperry J, Conde J, Bianco G, et al. (2010) Effect of oleocanthal and its derivatives on inflammatory response induced by lipopolysaccharide in a murine chondrocyte cell line. Arthritis Rheum 62: 1675-1682.
19. Pitt J, Roth W, Lacor P, Smith III AB, Blankenship M, et al. (2009) Alzheimer's-associated Aβ oligomers show altered structure, immunoreactivity and synaptotoxicity with low doses of oleocanthal. Toxicol Appl Pharmacol 240: 189-197.
20. Li W, Sperry JB, Crowe A, Trojanowski JQ, Smith III AB, et al. (2009) Inhibition of tau fibrillization by oleocanthal via reaction with the amino groups of tau. J Neurochem 110: 1339-1351.
21. Cicerale S, Breslin PA, Beauchamp GK, Keast RS (2009) Sensory characterization of the irritant properties of oleocanthal, a natural anti-inflammatory agent in extra virgin olive oils. Chem Senses 34: 333-339.
22. Ma PC, Jagadeeswaran R, Jagadeesh S, Tretiakova MS, Nallasura V, et al. (2005) Functional expression and mutations of c-Met and its therapeutic inhibition with SU11274 and small interfering RNA in non-small cell lung cancer. Cancer Res 65: 1479-1488. (Pubitemid 40270177)
23. Akl MR, Ayoub NM, Abuasal B, Kaddoumi A, Sylvester PW (2012) Sesamin synergistically potentiates the anticancer effects of γ-tocotrienol in mammary cancer cell lines. Fitoterapia 84: 347-359.
24. Ponzo MG, Lesurf R, Petkiewicz S, O'Malley FP, Pinnaduwage D, et al. (2012) Met induces mammary tumors with diverse histologies and is associated with poor outcome and human basal breast cancer. Proc Natl Acad Sci U S A 106: 12903-12908.
25. Graveel CR, DeGroot JD, Su Y, Koeman J, Dykema K, et al. (2009) Met induces diverse mammary carcinomas in mice and is associated with human basal breast cancer. Proc Natl Acad Sci U S A 106: 12909-12914.
26. Rho O1, Kim DJ, Kiguchi K, Digiovanni J (2011) Growth factor signaling pathways as targets for prevention of epithelial carcinogenesis. Mol Carcinog 50: 264-279.
27. Nakamura T, Sakai K, Matsumoto K (2011) Hepatocyte growth factor twenty years on: Much more than a growth factor. J Gastroenterol Hepatol 26 Suppl 1: 188-202.
28. Kim EJ, Eom SJ, Hong JE, Lee JY, Choi MS, et al. (2012) Benzyl isothiocyanate inhibits basal and hepatocyte growth factor-stimulated migration of breast cancer cells. Mol Cell Biochem 359: 431-440.
29. Agarwal S, Zerillo C, Kolmakova J, Christensen JG, Harris LN, et al. (2009) Association of constitutively activated hepatocyte growth factor receptor (Met) with resistance to a dual EGFR/Her2 inhibitor in non-small-cell lung cancer cells. Br J Cancer 100: 941-949.
30. Sattler M, Salgia R (2009) The MET axis as a therapeutic target. Update Cancer Ther 3: 109-118.
31. Lawrence RE, Salgia R (2010) MET molecular mechanisms and therapies in lung cancer. Cell Adh Migr 4: 146-152.
32. Sattler M, Pride YB, Ma P, Gramlich JL, Chu SC, et al. (2003) Novel small molecule met inhibitor induces apoptosis in cells transformed by the oncogenic TPR-MET tyrosine kinase. Cancer Res 63: 5462-5469. (Pubitemid 37139865)
33. Sattler M, Salgia R (2007) c-Met and hepatocyte growth factor: potential as novel targets in cancer therapy. Curr Oncol Rep 9: 102-108. (Pubitemid 46332381)
34. Wang Y, Blelloch R (2009) Cell cycle regulation by MicroRNAs in embryonic stem cells. Cancer Res 69: 4093-4096.
35. Lin Y, Devin A, Rodriguez Y, Liu Z-g (1999) Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev 13: 2514-2526. (Pubitemid 29489643)
36. Tuck AB, Park M, Sterns EE, Boag A, Elliott BE (1996) Coexpression of hepatocyte growth factor and receptor (Met) in human breast carcinoma. Am J Pathol 148: 225-232. (Pubitemid 26022451)
37. Ma PC, Maulik G, Christensen J, Salgia R (2003) c-Met: structure, functions and potential for therapeutic inhibition. Cancer Metastasis Rev 22: 309-325. (Pubitemid 36791889)
38. Cooke VG, LeBleu VS, Keskin D, Khan Z, O'Connell JT, et al. (2012) Pericyte depletion results in hypoxia-associated epithelial-to-mesenchymal transition and metastasis mediated by met signaling pathway. Cancer Cell 21: 66-81.
39. Kalluri R, Weinberg RA (2009) The basics of epithelial-mesenchymal transition. J Clin Invest 119: 1420-1428.
40. Vuoriluoto K, Haugen H, Kiviluoto S, Mpindi J, Nevo J, et al. (2010) Vimentin regulates EMT induction by Slug and oncogenic H-Ras and migration by governing Axl expression in breast cancer. Oncogene 30: 1436-1448.
41. Tomaskovic-Crook E, Thompson EW, Thiery JP (2009) Epithelial to mesenchymal transition and breast cancer. Breast Cancer Res 11: 213.
42. Elliott BE, Hung WL, Boag AH, Tuck AB (2002) The role of hepatocyte growth factor (scatter factor) in epithelial-mesenchymal transition and breast cancer. Can J Physiol Pharmacol 80: 91-102. (Pubitemid 34258657)
43. Reshetnikova G, Troyanovsky S, Rimm DL (2007) Definition of a direct extracellular interaction between Met and E-cadherin. Cell Biol Int 31: 366-373. (Pubitemid 46483110)
44. Bellon SF, Kaplan-Lefko P, Yang Y, Zhang Y, Moriguchi J, et al. (2008) c-Met inhibitors with novel binding mode show activity against several hereditary papillary renal cell carcinoma-related mutations. J Biol Chem 283: 2675-2683.
45. Scotece M, Gómez R, Conde J, Lopez V, Gómez-Reino JJ, et al. (2012) Further evidence for the anti-inflammatory activity of oleocanthal: inhibition of MIP-1α and IL-6 in J774 macrophages and in ATDC5 chondrocytes. Life Sci 10; 91(23-24): 1229-1235.
46. Vougogiannopoulou K, Lemus C, Halabalaki M, Pergola C, Werz O, et al. (2014) One-Step Semisynthesis of Oleacein and the Determination as a 5-Lipoxygenase Inhibitor. J Nat Prod Feb 25.
47. Margarucci L, Monti MC, Cassiano C, Mozzicafreddo M, Angeletti M, et al. (2013) Chemical proteomics-driven discovery of oleocanthal as an Hsp90 inhibitor. Chem Commun (Camb). 4; 49(52): 5844-5846.
48. Fogliano V, Sacchi R (2006) Oleocanthal in olive oil: Between myth and reality. Mol. Nutr. Food Res 50, 5-6. (Pubitemid 43155091)