Auraptene is an inhibitor of cholesterol esterification and a modulator of estrogen receptors

Molecular Pharmacology

Volumn 78, Issue 5, 2010, Pages 827-836

  De Medina, Philippe ^a,c   Genovese, Salvatore ^e   Paillasse, Michael R ^a,c   Mazaheri, Mahta ^d   Caze Subra, Stephanie ^d   Bystricky, Kerstin ^b,d   Curini, Massimo ^f   Silvente Poirot, Sandrine ^a,b   Epifano, Francesco ^e   Poirot, Marc ^b  

^a INSERM   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c Affichem   (France)

^d CNRS   (France)

^e UNIVERSITY OF CHIETI   (Italy)

^f UNIVERSITY OF PERUGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

3 DECYLDIMETHYLSILYL N [2 (4 METHYLPHENYL) 1 PHENYLETHYL]PROPIONAMIDE; AURAPTENE; CHOLESTEROL ACYLTRANSFERASE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; N BUTYL 11 (3,17BETA DIHYDROXYESTRA 1,3,5(10) TRIEN 7ALPHA YL) N METHYLUNDECANAMIDE;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; CANCER CELL; CELL INVASION; CELL PROLIFERATION; CHOLESTEROL ESTERIFICATION; COLONY FORMATION; DRUG MECHANISM; DRUG RECEPTOR BINDING; DRUG STRUCTURE; ENZYME INHIBITION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IC 50; LIVER MICROSOME; MOLECULAR MODEL; NONHUMAN; PHARMACOPHORE; PRIORITY JOURNAL; RAT; REPORTER GENE;

ANIMALS; ANTICARCINOGENIC AGENTS; BINDING SITES; BINDING, COMPETITIVE; CELL LINE, TUMOR; CELL PROLIFERATION; COUMARINS; EPOXIDE HYDROLASES; ESTROGEN ANTAGONISTS; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GENE EXPRESSION REGULATION; GENES, REPORTER; HUMANS; LUCIFERASES; MICE; MICROSOMES, LIVER; MODELS, MOLECULAR; NEOPLASM INVASIVENESS; RADIOLIGAND ASSAY; RATS; STEROL O-ACYLTRANSFERASE; TRANSCRIPTION, GENETIC;

EID: 77958140983     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.110.065250     Document Type: Article

References (40)

1. Batetta B, Mulas MF, Sanna F, Putzolu M, Bonatesta RR, Gasperi-Campani A, Roncuzzi L, Baiocchi D, and Dessì S (2003) Role of cholesterol ester pathway in the control of cell cycle in human aortic smooth muscle cells. FASEB J 17:746-748.
2. Booth C, Hargreaves DF, Hadfield JA, McGown AT, and Potten CS (1999) Isoflavones inhibit intestinal epithelial cell proliferation and induce apoptosis in vitro. Br J Cancer 80:1550-1557. (Pubitemid 29308633)
3. Brzozowski AM, Pike AC, Dauter Z, Hubbard RE, Bonn T, Engström O, Ohman L, Greene GL, Gustafsson JA, and Carlquist M (1997) Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 389:753-758. (Pubitemid 27458965)
4. Curini M, Cravotto G, Epifano F, and Giannone G (2006) Chemistry and biological activity of natural and synthetic prenyloxycoumarins. Curr Med Chem 13:199-222.
5. Curini M, Epifano F, Maltese F, Marcotullio MC, Tubaro A, Altinier G, Gonzales SP, and Rodriguez JC (2004) Synthesis and anti-inflammatory activity of natural and semisynthetic geranyloxycoumarins. Bioorg Med Chem Lett 14:2241-2243. (Pubitemid 38481397)
6. de Medina P, Boubekeur N, Balaguer P, Favre G, Silvente-Poirot S, and Poirot M (2006) The prototypical inhibitor of cholesterol esterification, Sah 58-035 [3-[decyldimethylsilyl]- n-[2-(4-methylphenyl)-1-phenylethyl]propanamide] , is an agonist of estrogen receptors. J Pharmacol Exp Ther 319:139-149. (Pubitemid 44455118)
7. de Médina P, Favre G, and Poirot M (2004) Multiple targeting by the antitumor drug tamoxifen: a structure-activity study. Curr Med Chem Anticancer Agents 4:491-508. (Pubitemid 39406262)
8. de Medina P, Paillasse MR, Segala G, Poirot M, and Silvente-Poirot S (2010) Identification and pharmacological characterization of cholesterol-5,6-epoxide hydrolase as a target for tamoxifen and AEBS ligands. Proc Natl Acad Sci USA 107:13520-13525.
9. de Medina P, Payré B, Boubekeur N, Bertrand-Michel J, Tercé F, Silvente-Poirot S, and Poirot M (2009a) Ligands of the antiestrogen-binding site induce active cell death and autophagy in human breast cancer cells through the modulation of cholesterol metabolism. Cell Death Differ 16:1372-1384.
10. de Medina P, Payré BL, Bernad J, Bosser I, Pipy B, Silvente-Poirot S, Favre G, Faye JC, and PoirotM(2004) Tamoxifen is a potent inhibitor of cholesterol esterification and prevents the formation of foam cells. J Pharmacol Exp Ther 308:1165-1173.
11. de Medina P, Silvente-Poirot S, and Poirot M (2009b) Tamoxifen and AEBS ligands induced apoptosis and autophagy in breast cancer cells through the stimulation of sterol accumulation. Autophagy 5:1066-1067.
12. Epifano F, Genovese S and Curini M (2008) Auraptene: phytochemical and pharmacological properties, in Phytochemistry Research Progress (Matsumoto T ed) pp 145-162, Nova Science Publishers, Inc., New York.
13. Galés C, Sanchez D, Poirot M, Pyronnet S, Buscail L, Cussac D, Pradayrol L, Fourmy D, and Silvente-Poirot S (2003) High tumorigenic potential of a constitutively active mutant of the cholecystokinin 2 receptor. Oncogene 22:6081-6089. (Pubitemid 37175886)
14. Holbeck S, Chang J, Best AM, Bookout AL, Mangelsdorf DJ, and Martinez ED (2010) Expression profiling of nuclear receptors in the NCI60 cancer cell panel reveals receptor-drug and receptor-gene interactions. Mol Endocrinol 24:1287-1296.
15. Janakiram NB, Steele VE, and Rao CV (2009) Estrogen receptor-beta as a potential target for colon cancer prevention: chemoprevention of azoxymethane-induced colon carcinogenesis by raloxifene in F344 rats. Cancer Prev Res (Phila Pa) 2:52-59.
16. Jensen EV and Jordan VC (2003) The estrogen receptor: a model for molecular medicine. Clin Cancer Res 9:1980-1989. (Pubitemid 36687616)
17. Jordan VC (2003) Tamoxifen: a most unlikely pioneering medicine. Nat Rev Drug Discov 2:205-213.
18. Jordan VC (2004) Selective estrogen receptor modulation: concept and consequences in cancer. Cancer Cell 5:207-213. (Pubitemid 38402112)
19. Jordan VC (2007) SERMs: meeting the promise of multifunctional medicines. J Natl Cancer Inst 99:350-356.
20. Kedjouar B, de Médina P, Oulad-Abdelghani M, Payré B, Silvente-Poirot S, Favre G, Faye JC, and Poirot M (2004) Molecular characterization of the microsomal tamoxifen binding site. J Biol Chem 279:34048-34061. (Pubitemid 39063057)
21. Kohno H, Suzuki R, Curini M, Epifano F, Maltese F, Gonzales SP, and Tanaka T (2006) Dietary administration with prenyloxycoumarins, auraptene and collinin, inhibits colitis-related colon carcinogenesis in mice. Int J Cancer 118:2936-2942.
22. Krishnan P, Yan KJ, Windler D, Tubbs J, Grand R, Li BD, Aldaz CM, McLarty J, and Kleiner-Hancock HE (2009) Citrus auraptene suppresses cyclin D1 and significantly delays N-methyl nitrosourea induced mammary carcinogenesis in female Sprague-Dawley rats. BMC Cancer 9:259.
23. Levenson AS and Jordan VC (1998) The key to the antiestrogenic mechanism of raloxifene is amino acid 351 (aspartate) in the estrogen receptor. Cancer Res 58:1872-1875.
24. McDonnell DP, Clemm DL, Hermann T, Goldman ME, and Pike JW (1995) Analysis of estrogen receptor function in vitro reveals three distinct classes of antiestrogens. Mol Endocrinol 9:659-669.
25. Ogawa K, Kawasaki A, Yoshida T, Nesumi H, Nakano M, Ikoma Y, and Yano M (2000) Evaluation of auraptene content in citrus fruits and their products. J Agric Food Chem 48:1763-1769. (Pubitemid 30331522)
26. Ohnishi H, Asamoto M, Tujimura K, Hokaiwado N, Takahashi S, Ogawa K, Kuribayashi M, Ogiso T, Okuyama H, and Shirai T (2004) Inhibition of cell proliferation by nobiletin, a dietary phytochemical, associated with apoptosis and characteristic gene expression, but lack of effect on early rat hepatocarcinogenesis in vivo. Cancer Sci 95:936-942. (Pubitemid 40089584)
27. Paillasse MR, de Medina P, Amouroux G, Mhamdi L, Poirot M, and Silvente-Poirot S (2009) Signaling through cholesterol esterification: a new pathway for the cholecystokinin 2 receptor involved in cell growth and invasion. J Lipid Res 50:2203-2211.
28. Payré B, de Medina P, Boubekeur N, Mhamdi L, Bertrand-Michel J, Tercé F, Fourquaux I, Goudounèche D, Record M, Poirot M, et al. (2008) Microsomal antiestrogen-binding site ligands induce growth control and differentiation of human breast cancer cells through the modulation of cholesterol metabolism. Mol Cancer Ther 7:3707-3718.
29. Poirot M, De Medina P, Delarue F, Perie JJ, Klaebe A, and Faye JC (2000) Synthesis, binding and structure-affinity studies of new ligands for the microsomal antiestrogen binding site (AEBS). Bioorg Med Chem 8:2007-2016.
30. Renoir JM, Bouclier C, Seguin A, Marsaud V, and Sola B (2008) Antioestrogenmediated cell cycle arrest and apoptosis induction in breast cancer and multiple myeloma cells. J Mol Endocrinol 40:101-112. (Pubitemid 351586820)
31. Shiau AK, Barstad D, Loria PM, Cheng L, Kushner PJ, Agard DA, and Greene GL (1998) The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 95:927-937. (Pubitemid 29019045)
32. Tanaka T, de Azevedo MB, Durán N, Alderete JB, Epifano F, Genovese S, Tanaka M, Tanaka T, and Curini M (2010) Colorectal cancer chemoprevention by 2 beta-cyclodextrin inclusion compounds of auraptene and 4′- geranyloxyferulic acid. Int J Cancer 126:830-840.
33. Tanaka T, Kawabata K, Kakumoto M, Matsunaga K, Mori H, Murakami A, Kuki W, Takahashi Y, Yonei H, Satoh K, et al. (1998) Chemoprevention of 4-nitroquinoline 1-oxide-induced oral carcinogenesis by citrus auraptene in rats. Carcinogenesis 19:425-431. (Pubitemid 28375444)
34. Tanaka T, Kohno H, Murakami M, Kagami S, and El-Bayoumy K (2000) Suppressing effects of dietary supplementation of the organoselenium 1,4-phenylenebis(methylene) selenocyanate and the Citrus antioxidant auraptene on lung metastasis of melanoma cells in mice. Cancer Res 60:3713-3716. (Pubitemid 32204556)
35. Tosi MR and Tugnoli V (2005) Cholesteryl esters in malignancy. Clin Chim Acta 359:27-45.
36. Vedin LL, Lewandowski SA, Parini P, Gustafsson JA, and Steffensen KR (2009) The oxysterol receptor LXR inhibits proliferation of human breast cancer cells. Carcinogenesis 30:575-579.
37. Weige CC, Allred KF, and Allred CD (2009) Estradiol alters cell growth in nonmalignant colonocytes and reduces the formation of preneoplastic lesions in the colon. Cancer Res 69:9118-9124.
38. Wittmann BM, Sherk A, and McDonnell DP (2007) Definition of functionally important mechanistic differences among selective estrogen receptor down-regulators. Cancer Res 67:9549-9560. (Pubitemid 47535946)
39. Xu X and Thomas ML (1994) Estrogen receptor-mediated direct stimulation of colon cancer cell growth in vitro. Mol Cell Endocrinol 105:197-201. (Pubitemid 24313988)
40. Zheng Q, Hirose Y, Yoshimi N, Murakami A, Koshimizu K, Ohigashi H, Sakata K, Matsumoto Y, Sayama Y, and Mori H (2002) Further investigation of the modifying effect of various chemopreventive agents on apoptosis and cell proliferation in human colon cancer cells. J Cancer Res Clin Oncol 128:539-546. (Pubitemid 35244929)