Olive oil's bitter principle reverses acquired autoresistance to trastuzumab (Herceptin™) in HER2-overexpressing breast cancer cells

BMC Cancer

Volumn 7, Issue , 2007, Pages

  Menendez, Javier A ^a,b,c   Vazquez Martin, Alejandro ^a,b,c   Colomer, Ramon ^d   Brunet, Joan ^a,b,c   Carrasco Pancorbo, Alegria ^e   Garcia Villalba, Rocio ^e   Fernandez Gutierrez, Alberto ^e   Segura Carretero, Antonio ^e  

^a CATALAN INSTITUTE OF ONCOLOGY   (Spain)

^b GIRONA BIOMEDICAL RESEARCH INSTITUTE IDIBGI   (Spain)

^c HOSPITAL JOSEP TRUETA   (Spain)

^d MD ANDERSON CANCER CENTER   (Spain)

^e UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; OLEUROPEIN; OLIVE OIL; TRASTUZUMAB; MONOCLONAL ANTIBODY; PLANT EXTRACT; PYRAN DERIVATIVE; VEGETABLE OIL;

APOPTOSIS; ARTICLE; BREAST CANCER; CELL LINE; CELL VIABILITY; COCULTURE; DOWN REGULATION; DRUG DETERMINATION; DRUG EFFICACY; DRUG POTENTIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE ACTIVATION; GENE AMPLIFICATION; GENE OVEREXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; ISOLATION AND PURIFICATION; ONCOGENE NEU; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; RETROVIRUS INFECTION; BREAST TUMOR; COMPARATIVE STUDY; DRUG EFFECT; DRUG RESISTANCE; FEMALE; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY; PROTO ONCOGENE; TUMOR CELL LINE;

ANTIBODIES, MONOCLONAL; BREAST NEOPLASMS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, ERBB-2; HUMANS; PLANT EXTRACTS; PLANT OILS; PYRANS;

EID: 34249863300     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-7-80     Document Type: Article

References (82)

1. Simopoulos AP The Mediterranean diets: What is so special about the diet of Greece? The scientific evidence Nutr 2001 131 11 Suppl 3065S-3073S
2. Visioli F Galli C The role of antioxidants in the Mediterranean diet Lipids 2001 36 Suppl S49-S52 10.1007/s11745-001-0682-z 11837993
3. Stark AH Madar Z Olive oil as a functional food: Epidemiology and nutritional approaches Nutr Rev 2002 60 170-176 10.1301/ 002966402320243250 12078915
4. La Vecchia C Mediterranean diet and cancer Public Health Nutr 2004 7 965-968 10.1079/PHN2004562 15482626
5. Martinez-Gonzalez MA Estruch R Mediterranean diet, antioxidants and cancer: The need for randomized trials Eur J Cancer Prev 2004 13 327-335 10.1097/01.cej.0000137512.71845.bf 15554561
6. Wahle KW Caruso D Ochoa JJ Quiles JL Olive oil and modulation of cell signaling in disease prevention Lipids 2004 39 1223-1231 10.1007/ s11745-004-1351-y 15736919
7. Perez-Jimenez F Alvarez de Cienfuegos G Badimon L Barja G Battino M Blanco A Bonanome A Colomer R Corella-Piquer D Covas I Chamorro-Quiros J Escrich E Gaforio JJ Garcia Luna PP Hidalgo L Kafatos A Kris-Etherton PM Lairon D Lamuela-Raventos R Lopez-Miranda J Lopez-Segura F Martinez-Gonzalez MA Mata P Mataix J Ordovas J Osada J Pacheco-Reyes R Perucho M Pineda-Priego M Quiles JL Ramirez-Tortosa MC Ruiz-Gutierrez V Sanchez-Rovira P Solfrizzi V Soriguer-Escofet F de la Torre-Fornell R Trichopoulos A Villalba-Montoro JM Villar-Ortiz JR Visioli F International conference on the healthy effect of virgin olive oil Eur J Clin Invest 2005 35 421-424 10.1111/j.1365-2362.2005.01516.x 16008542
8. Serra-Majem L Roman B Estruch R Scientific evidence of interventions using the Mediterranean diet: A systematic review Nutr Rev 2006 64 2 Pt 2 S27-S47 10.1301/nr.2006.feb.S27-S47 16532897
9. Colomer R Menendez JA Mediterranean diet, olive oil and cancer Clin Transl Oncol 2006 8 15-21 16632435
10. Bougnoux P Giraudeau B Couet C Diet, cancer, and the lipidome Cancer Epidemiol Biomarkers Prev 2006 15 416-421 10.1158/1055-9965.EPI-05-0546 16537692
11. Menendez JA Lupu R Mediterranean dietary traditions for the molecular treatment of human cancer: Anti-oncogenic actions of the main olive oil's monounsaturated fatty acid oleic acid (18:1N-9) Curr Pharm Biotechnol 2006 7 495-502 10.2174/138920106779116900 17168666
12. Visioli F Galli C Olive oil: More than just oleic acid Am J Clin Nutr 2000 72 853 10966910
13. Tuck KL Hayball PJ Major phenolic compounds in olive oil: Metabolism and health effects J Nutr Biochem 2002 13 636-644 10.1016/ S0955-2863(02)00229-2 12550060
14. Gutierrez-Rosales F Rios JJ Gomez-Rey ML Main polyphenols in the bitter taste of olive oil. Structural confirmation by on-line high-performance liquid chromatography electrospray ionization mass spectrometry J Agric Food Chem 2003 51 6021-6025 10.1021/jf021199x 13129311
15. Bonoli M Bendini A Cerretani L Lercker G Toschi TG Qualitative and semiquantitative analysis of phenolic compounds in extra virgin oils as a function of the ripening degree of olive fruits by different analytical techniques J Agric Food Chem 2004 52 7026-7032 10.1021/ jf048868m 15537313
16. Visioli F Bellomo G Galli C Free radical-scavenging properties of olive oil polyphenols Biochem Biophys Res Commun 1998 247 60-64 10.1006/ bbrc.1998.8735 9636654
17. Visioli F Poli A Galli C Antioxidant and other biological activities of phenols from olives and olive oil Med Res Rev 2002 22 65-75 10.1002/ med.1028 11746176
18. Owen RW Giacosa A Hull WE Haubner R Spiegelhalder B Bartsch H The antioxidant/anticancer potential of phenolic compounds isolated from olive oil Eur J Cancer 2000 36 1235-1247 10.1016/S0959-8049(00)00103-9 10882862
19. Menendez JA Ropero S Lupu R Colomer R Dietary fatty acids regulate the activation status of Her-2/neu (c-erbB-2) oncogene in breast cancer cells Ann Oncol 2004 15 1719-1721 10.1093/annonc/mdh442 15520077
20. Menendez JA Vellon L Colomer R Lupu R Oleic acid, the main monounsaturated fatty acid of olive oil, suppresses Her-2/neu (erbB-2) expression and synergistically enhances the growth inhibitory effects of trastuzumab (Herceptin) in breast cancer cells with Her-2/neu oncogene amplification Ann Oncol 2005 16 359-371 10.1093/annonc/mdi090 15642702
21. Menendez JA Papadimitropoulou A Vellon L Lupu R A genomic explanation connecting "Mediterranean diet", olive oil and cancer: Oleic acid, the main monounsaturated Fatty acid of olive oil, induces formation of inhibitory "PEA3 transcription factor-PEA3 DNA binding site" complexes at the Her-2/neu (erbB-2) oncogene promoter in breast, ovarian and stomach cancer cells Eur J Cancer 2006 42 2425-2432 10.1016/j.ejca.2005.10.016 16406575
22. Neve RM Lane HA Hynes NE The role of overexpressed HER2 in transformation Ann Oncol 2001 12 Suppl 1 S9-S13 10.1023/A:1011199404516 11521729
23. Yarden Y Biology of HER2 and its importance in breast cancer Oncology 2001 61 Suppl 2 1-13 10.1159/000055396 11694782
24. Rubin I Yarden Y The basic biology of HER2 Ann Oncol 2001 12 Suppl 1 S3-S8 10.1023/A:1011195320446 11521719
25. Menard S Pupa SM Campiglio M Tagliabue E Biological and therapeutic role of HER2 in cancer Oncogene 2003 22 6570-6578 10.1038/sj.onc.1206779 14528282
26. Slamon DJ Clark GM Wong SG Levin WJ Ullrich A McGuire WL Human breast cancer: Correlation of relapse and survival with amplification of the HER-2/neu oncogene Science 1987 235 177-182 10.1126/science.3798106 3798106
27. Pegram MD Konecny G Slamon DJ The molecular and cellular biology of HER2/ neu gene amplification/overexpression and the clinical development of Herceptin (trastuzumab) therapy for breast cancer Cancer Treat Res 2000 103 57-75 10948442
28. Nelson R Oleic acid suppresses overexpression of ERBB2 oncogene Lancet Oncol 2005 6 69 10.1016/S1470-2045(05)01722-5 15704291
29. Marchetti P Natural medicine: A 'new frontier' in oncology? Ann Oncol 2005 16 339-340 10.1093/annonc/mdi069 15722460
30. Fogliano V Sacchi R Oleocanthal in olive oil: Between myth and reality Mol Nutr Food Res 2006 50 5-6 10.1002/mnfr.200690002 16397870
31. Gomez Caravaca AM Carrasco Pancorbo A Canabate Diaz B Segura Carretero A Fernandez Gutierrez A Electrophoretic identification and quantitation of compounds in the polyphenolic fraction of extra-virgin olive oil Electrophoresis 2005 26 3538-3551 10.1002/elps.200500202 16167367
32. Carrasco-Pancorbo A Cerretani L Bendini A Segura-Carretero A Del Carlo M Gallina-Toschi T Lercker G Compagnone D Fernandez-Gutierrez A Evaluation of the antioxidant capacity of individual phenolic compounds in virgin olive oil J Agric Food Chem 2005 53 8918-8925 10.1021/jf0515680 16277383
33. Carrasco-Pancorbo A Arraez-Roman D Segura-Carretero A Fernandez-Gutierrez A Capillary electrophoresis-electrospray ionization-mass spectrometry method to determine the phenolic fraction of extra-virgin olive oil Electrophoresis 2006 27 2182-2196 10.1002/ elps.200500650 16736455
34. Carrasco-Pancorbo A Gomez-Caravaca AM Cerretani L Bendini A Segura-Carretero A Fernandez-Gutierrez A Rapid Quantification of the Phenolic Fraction of Spanish Virgin Olive Oils by Capillary Electrophoresis with UV Detection J Agric Food Chem 2006 54 7984-7991 10.1021/jf0617925 17031999
35. Berenbaum MC What is synergy? Pharmacol Rev 1989 41 93-193 2692037
36. Benz CC Scott GK Sarup JC Johnson RM Tripathy D Coronado E Shepard HM Osborne CK Estrogen-dependent, tamoxifen-resistant tumorigenic growth of MCF-7 cells transfected with HER2/neu Breast Cancer Res Treat 1992 24 85-95 10.1007/BF01961241 8095168
37. Yakes FM Chinratanalab W Ritter CA King W Seelig S Arteaga CL Herceptin-induced inhibition of phosphatidylinositol-3 kinase and Akt is required for antibody-mediated effects on p27, cyclin D1, and antitumor action Cancer Res 2002 62 4132-4141 12124352
38. Carter P Presta L Gorman CM Ridgway JB Henner D Wong WL Rowland AM Kotts C Carver ME Shepard HM Humanization of an anti-p185HER2 antibody for human cancer therapy Proc Natl Acad Sci USA 1992 89 4285-4289 49066 1350088 10.1073/pnas.89.10.4285
39. Harries M Smith I The development and clinical use of trastuzumab (Herceptin) Endocr Relat Cancer 2002 9 75-85 10.1677/erc.0.0090075 12121832
40. Nathta R Esteva FJ HER-2-targeted therapy: Lessons learned and future directions Clin Cancer Res 2003 9 5078-5084 14613984
41. Thor AD Liu S Edgerton S Moore D 2nd Kasowitz KM Benz CC Stern DF DiGiovanna MP Activation (tyrosine phosphorylation) of ErbB-2 (HER-2/ neu): A study of incidence and correlation with outcome in breast cancer J Clin Oncol 2000 18 3230-3239 10986055
42. DiGiovanna MP Chu P Davison TL Howe CL Carter D Claus EB Stern DF Active signaling by HER-2/neu in a subpopulation of HER-2/neu-overexpressing ductal carcinoma in situ: Clinicopathological correlates Cancer Res 2002 62 6667-6673 12438265
43. DiGiovanna MP Stern DF Edgerton SM Whalen SG Moore D 2nd Thor AD Relationship of epidermal growth factor receptor expression to ErbB-2 signaling activity and prognosis in breast cancer patients J Clin Oncol 2005 23 1152-1160 10.1200/JCO.2005.09.055 15718311
44. Hudelist G Kostler WJ Attems J Czerwenka K Muller R Manavi M Steger GG Kubista E Zielinski CC Singer CF Her-2/neu-triggered intracellular tyrosine kinase activation: In vivo relevance of ligand-independent activation mechanisms and impact upon the efficacy of trastuzumab-based treatment Br J Cancer 2003 89 983-991 10.1038/sj.bjc.6601160 12966413
45. Hudelist G Kostler WJ Czerwenka K Kubista E Attems J Muller R Gschwantler-Kaulich D Manavi M Huber I Hoschutzky H Zielinski CC Singer CF Her-2/neu and EGFR tyrosine kinase activation predict the efficacy of trastuzumab-based therapy in patients with metastatic breast cancer Int J Cancer 2006 118 1126-1134 10.1002/ijc.21492 16161043
46. Baselga J Albanell J Mechanism of action of anti-HER2 monoclonal antibodies Ann Oncol 2001 12 Suppl 1 S35-S41 10.1023/A:1011163824080 11521720
47. Molina MA Codony-Servat J Albanell J Rojo F Arribas J Baselga J Trastuzumab (Herceptin), a humanizad anti-HER2 receptor monoclonal antibody, inhibits basal and activated HER2 ectodomain cleavage in breast cancer cells Cancer Res 2001 61 4744-4749 11406546
48. DiGiovanna MP Stern DF Activation state-specific monoclonal antibody detects tyrosine phosphorylated p185neu/erbB-2 in a subset of human breast tumors overexpressing this receptor Cancer Res 1995 55 1946-1955 7728765
49. DiGiovanna MP Carter D Flynn SD Stern DF Functional assay for HER-2/neu demonstrates active signalling in a minority of HER-2/neu-overexpressing invasive human breast tumours Br J Cancer 1996 74 802-806 8795585
50. Sliwkowski MX Lofgren JA Lewis GD Hotaling TE Fendly BM Fox JA Nonclinical studies addressing the mechanism of action of trastuzumab (Herceptin) Semin Oncol 1999 26 4 Suppl 12 60-70 10482195
51. Baselga J Albanell J Molina MA Arribas J Mechanism of action of trastuzumab and scientific update Semin Oncol 2001 28 5 Suppl 16 4-11 10.1016/S0093-7754(01)90276-3 11706390
52. Lan KH Lu CH Yu D Mechanisms of trastuzumab resistance and their clinical implications Ann N Y Acad Sci 2005 1059 70-75 10.1196/ annals.1339.026 16382045
53. Nahta R Yu D Hung MC Hortobagyi GN Esteva FJ Mechanisms of disease: understanding resistance to HER2-targeted therapy in human breast cancer Nat Clin Pract Oncol 2006 3 269-280 10.1038/ncponc0509 16683005
54. Nahta R Esteva FJ Herceptin: Mechanisms of actions and resistance Cancer Lett 2006 232 123-138 10.1016/j.canlet.2005.01.041 16458110
55. Hortobagyi GN Trastuzumab in the treatment of breast cancer N Engl J Med 2005 353 1734-1736 10.1056/NEJMe058196 16236745
56. Gonzalez-Angulo AM Hortobagyi GN Esteva FJ Adjuvant therapy with trastuzumab for HER-2/neu-positive breast cancer Oncologist 2006 11 857-867 10.1634/theoncologist.11-8-857 16951389
57. Piccart-Gebhart MJ Adjuvant trastuzumab therapy for HER2-overexpressing breast cancer: What we know and what we still need to learn Eur J Cancer 2006 42 1715-1719 10.1016/j.ejca.2006.04.008 16806901
58. Konecny GE Pegram MD Venkatesan N Finn R Yang G Rahmeh M Untch M Rusnak DW Spehar G Mullin RJ Keith BR Gilmer TM Berger M Podratz KC Slamon DJ Activity of the dual kinase inhibitor lapatinib (GW572016) against HER-2-overexpressing and trastuzumab-treated breast cancer cells Cancer Res 2006 66 1630-1639 10.1158/0008-5472.CAN-05-1182 16452222
59. Nahta R Takahashi T Ueno NT Hung MC Esteva FJ P27(kip1) down-regulation is associated with trastuzumab resistance in breast cancer cells Cancer Res 2004 64 3981-3986 10.1158/0008-5472.CAN-03-3900 15173011
60. Nahta R Yuan LX Zhang B Kobayashi R Esteva FJ Insulin-like growth factor-I receptor/human epidermal growth factor receptor 2 heterodimerization contributes to trastuzumab resistance of breast cancer cells Cancer Res 2005 65 11118-11128 10.1158/ 0008-5472.CAN-04-3841 16322262
61. Olayioye MA Neve RM Lane HA Hynes NE The ErbB signaling network: receptor heterodimerization in development and cancer EMBO J 2000 19 3159-3167 313958 10880430 10.1093/emboj/19.13.3159
62. Yarden Y Sliwkowski MX Untangling the ErbB signaling network Nature Rev Mol Cell Biol 2001 2 127-137 10.1038/35052073
63. Hynes NE Lane HA ERBB receptors and cancer: The complexity of targeted inhibitors Nature Rev Cancer 2005 5 341-354 10.1038/nrc1609
64. Citri A Yarden Y EGF-ERBB signalling: Towards the systems level Nat Rev Mol Cell Biol 2006 7 505-516 10.1038/nrm1962 16829981
65. Diermeier S Horvath G Knuechel-Clarke R Hofstaedter F Szollosi J Brockhoff G Epidermal growth factor receptor coexpression modulates susceptibility to Herceptin in HER2/neu overexpressing breast cancer cells via specific erbB-receptor interaction and activation Exp Cell Res 2005 304 604-619 10.1016/j.yexcr.2004.12.008 15748904
66. Galli C Visioli F Antioxidant and other activities of phenolics in olives/olive oil, typical components of the Mediterranean diet Lipids 1999 34 S23-S26 10.1007/BF02562224 10419084
67. Saija A Trombetta D Tomaino A In vitro evaluation of the antioxidant activity and biomembrane interaction of the plant phenols oleuropein and hydroxytyrosol Int J Pharm 1998 166 123-133 10.1016/S0378-5173(98)00018-0
68. Scalbert A Williamson G Dietary intake and bioavailability of polyphenols J Nutr 2000 130 2073S-2085S 10917926
69. Vissers MN Zock PL Roodenburg AJC Leenen R Katan MB Olive oil phenols are absorbed in humans J Nutr 2002 132 409-417 11880564
70. Paganga G RiceEvans CA The identification of flavonoids as glycosides in human plasma FEBS Lett 1997 401 78-82 10.1016/S0014-5793(96)01442-1 9003810
71. Konno K Hirayama C Yasui H Nakamura M Enzymatic activation of oleuropein: A protein crosslinker used as a chemical defense in the privet tree Proc Natl Acad Sci USA 1999 96 9159-9164 17749 10430912 10.1073/pnas.96.16.9159
72. Carluccio MA Siculella L Ancora MA Massaro M Scoditti E Storelli C Visioli F Distante A De Caterina R Olive oil and red wine antioxidant polyphenols inhibit endothelial activation: Antiatherogenic properties of Mediterranean diet phytochemicals Arterioscler Thromb Vasc Biol 2003 23 622-629 10.1161/01.ATV.0000062884.69432.A0 12615669
73. Hamdi HK Castellon R Oleuropein, a non-toxic olive iridoid, is an anti-tumor agent and cytoskeleton disruptor Biochem Biophys Res Commun 2005 334 769-778 10.1016/j.bbrc.2005.06.161 16024000
74. Way TD Kao MC Lin JK Apigenin induces apoptosis through proteasomal degradation of HER2/neu in HER2/neu-overexpressing breast cancer cells via the phosphatidylinositol 3-kinase/Akt-dependent pathway J Biol Chem 2004 279 4479-4489 10.1074/jbc.M305529200 14602723
75. Petkov V Manolov P Pharmacological analysis of the iridoid Oleuropein Arzneimittelforschung 1972 22 1476-1486 4678608
76. Visioli F Galli C Phenolics from olive oil and its waste products. Biological activities in in vitro and in vivo studies World Rev Nutr Diet 2001 88 233-237 11935962
77. Speroni GM Minghetti A Crespi-Perellino N Pasini P Piazza F Roda A Oleuropein evaluated in vitro and in vivo as an antioxidant Phytother Res 1998 12 S98-S100 10.1002/(SICI)1099-1573(1998)12:1+ 3>3.0.CO;2-M
78. Gonzalez P Florido F Saenz de San Pedro B de la Torre F Rico P Martin S Immunotherapy with an extract of Olea europaea quantified in mass units. Evaluation of the safety and efficacy after one year of treatment J Investig Allergol Clin Immunol 2002 12 263-271 12926186
79. Visioli F Galli C Bornet F Mattei A Patelli R Galli G Caruso D Olive oil phenolics are dose-dependently absorbed in humans FEBS Lett 2000 468 159-160 10.1016/S0014-5793(00)01216-3 10692578
80. Miles EA Zoubouli P Calder PC Differential anti-inflammatory effects of phenolic compounds from extra virgin olive oil identified in human whole blood cultures Nutr 2005 21 389-394 10.1016/j.nut.2004.06.031
81. Menendez JA Lupu R Colomer R Exogenous supplementation with omega-3 polyunsaturated fatty acid docosahexaenoic acid (DHA; 22:6N-3) synergistically enhances taxane cytotoxicity and downregulates Her-2/neu (c-erbB-2) oncogene expression in human breast cancer cells Eur J Cancer Prev 2005 14 263-270 10.1097/00008469-200506000-00011 15901996
82. Menendez JA Vazquez-Martin A Ropero S Colomer R Lupu R HER2 (erbB-2)-targeted effects of the ω-3 polyunsaturated fatty acid α-linolenic acid (ALA; 18:3N-3) in breast cancer cells: The "fat features" of the "Mediterranean diet" as an "anto-HER2 cocktail" Clin Transl Oncol 2006 8 812-820 17134970