Nicotine-induced human breast cancer cell proliferation attenuated by garcinol through down-regulation of the nicotinic receptor and cyclin D3 proteins

Breast Cancer Research and Treatment

Volumn 125, Issue 1, 2011, Pages 73-87

  Chen, Ching Shyang ^a   Lee, Chia Hwa ^a   Hsieh, Chang Da ^a   Ho, Chi Tang ^b   Pan, Min Hsiung ^c   Huang, Ching Shui ^a,d   Tu, Shih Hsin ^a,d   Wang, Ying Jan ^e   Chen, Li Ching ^a   Chang, Yu Jia ^a   Wei, Po Li ^a   Yang, Yi Yuan ^a   Wu, Chih Hsiung ^a,f   Ho, Yuan Soon ^a  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b RUTGERS UNIVERSITY   (United States)

^c NATIONAL KAOHSIUNG UNIVERSITY OF APPLIED SCIENCES   (Taiwan)

^d CATHAY GENERAL HOSPITAL   (Taiwan)

^e NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^f TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Breast cancer; Cyclin D3; Garcinol; Nicotinic acetylcholine receptors; Smoking

Indexed keywords

ADENOVIRUS VECTOR; ADRENALIN; BENZOPHENONE DERIVATIVE; CYCLIN D3; ESTROGEN RECEPTOR; GARCINOL; MESSENGER RNA; NICOTINE; NICOTINIC RECEPTOR; NORADRENALIN; SMALL INTERFERING RNA; TETRACYCLINE; UNCLASSIFIED DRUG;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CANCER CELL; CANCER CELL CULTURE; CARCINOGENICITY; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CELL TRANSFORMATION; CIGARETTE SMOKING; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; EPITHELIUM CELL; GARCINIA; GARCINIA INDICA; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INHIBITION KINETICS; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR BINDING; RECEPTOR DOWN REGULATION; TUMOR XENOGRAFT;

ADULT; AGED; ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN D3; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; MICE, NUDE; MICE, SCID; MIDDLE AGED; NEOPLASM STAGING; NICOTINE; NICOTINIC AGONISTS; POLYMERASE CHAIN REACTION; RECEPTORS, NICOTINIC; RNA INTERFERENCE; RNA, MESSENGER; SMOKING; TERPENES; TIME FACTORS; TRANSCRIPTION FACTOR AP-1; TRANSFECTION; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 78651107917     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-010-0821-3     Document Type: Article

References (56)

1. Y Lin S Kikuchi K Tamakoshi K Wakai T Kondo Y Niwa H Yatsuya K Nishio S Suzuki S Tokudome A Yamamoto H Toyoshima M Mori A Tamakoshi 2008 Active smoking, passive smoking, and breast cancer risk: findings from the Japan Collaborative Cohort Study for Evaluation of Cancer Risk J Epidemiol 18 77 83 10.2188/jea.18.77 18403857
2. ML Slattery K Curtin AR Giuliano C Sweeney R Baumgartner S Edwards RK Wolff KB Baumgartner T Byers 2008 Active and passive smoking, IL6, ESR1, and breast cancer risk Breast Cancer Res Treat 109 101 111 1:CAS:528: DC%2BD1cXkslKhsrs%3D 10.1007/s10549-007-9629-1 17594514 (Pubitemid 351538759)
3. AK Armitage CT Dollery CF George TH Houseman PJ Lewis DM Turner 1975 Absorption and metabolism of nicotine from cigarettes Br Med J 4 313 316 1:CAS:528:DyaE28Xis1Cquw%3D%3D 10.1136/bmj.4.5992.313 1192046
4. NL Benowitz P Jacob III 1984 Nicotine and carbon monoxide intake from high- and low-yield cigarettes Clin Pharmacol Ther 36 265 270 1:STN:280:DyaL2c3mtValug%3D%3D 10.1038/clpt.1984.173 6744784
5. G Lindell LO Farnebo D Chen E Nexo J Rask Madsen K Bukhave H Graffner 1993 Acute effects of smoking during modified sham feeding in duodenal ulcer patients. An analysis of nicotine, acid secretion, gastrin, catecholamines, epidermal growth factor, prostaglandin E2, and bile acids Scand J Gastroenterol 28 487 494 1:CAS:528:DyaK3sXlslGktrk%3D 10.3109/00365529309098254 8322024
6. J Mei H Hu M McEntee H Plummer III P Song HC Wang 2003 Transformation of non-cancerous human breast epithelial cell line MCF10A by the tobacco-specific carcinogen NNK Breast Cancer Res Treat 79 95 105 1:CAS:528:DC%2BD3sXivFOitLs%3D 10.1023/A:1023326121951 12779086 (Pubitemid 36561047)
7. N Siriwardhana S Choudhary HC Wang 2008 Precancerous model of human breast epithelial cells induced by NNK for prevention Breast Cancer Res Treat 109 427 441 10.1007/s10549-007-9666-9 17653854 (Pubitemid 351692053)
8. C Heeschen JJ Jang M Weis A Pathak S Kaji RS Hu PS Tsao FL Johnson JP Cooke 2001 Nicotine stimulates angiogenesis and promotes tumor growth and atherosclerosis Nat Med 7 833 839 1:CAS:528:DC%2BD3MXltVagt70%3D 10.1038/89961 11433349 (Pubitemid 32691639)
9. KJ Kellar MI Davila-Garcia Y Xiao 1999 Pharmacology of neuronal nicotinic acetylcholine receptors: effects of acute and chronic nicotine Nicotine Tob Res 1 Suppl 2 S117 S120 10.1080/14622299050011921 11768167 discussion S139-S140
10. K Brejc WJ van Dijk RV Klaassen M Schuurmans J van Der Oost AB Smit TK Sixma 2001 Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors Nature 411 269 276 1:CAS:528:DC%2BD3MXjvF2qsbc%3D 10.1038/35077011 11357122 (Pubitemid 32467026)
11. HM Schuller M Orloff 1998 Tobacco-specific carcinogenic nitrosamines. Ligands for nicotinic acetylcholine receptors in human lung cancer cells Biochem Pharmacol 55 1377 1384 1:CAS:528:DyaK1cXislemsb4%3D 10.1016/S0006-2952(97) 00651-5 10076528 (Pubitemid 28298517)
12. YS Ho CH Chen YJ Wang RG Pestell C Albanese RJ Chen MC Chang JH Jeng SY Lin YC Liang H Tseng WS Lee JK Lin JS Chu LC Chen CH Lee WL Tso YC Lai CH Wu 2005 Tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK) induces cell proliferation in normal human bronchial epithelial cells through NFkappaB activation and cyclin D1 up-regulation Toxicol Appl Pharmacol 205 133 148 1:CAS:528:DC%2BD2MXktVGks7c%3D 10.1016/j.taap.2004.09.019 15893541 (Pubitemid 40704648)
13. PL Wei YJ Chang YS Ho CH Lee YY Yang J An SY Lin 2009 Tobacco-specific carcinogen enhances colon cancer cell migration through alpha7-nicotinic acetylcholine receptor Ann Surg 249 978 985 10.1097/SLA.0b013e3181a6ce7e 19474681
14. RJ Chen YS Ho HR Guo YJ Wang 2008 Rapid activation of Stat3 and ERK1/2 by nicotine modulates cell proliferation in human bladder cancer cells Toxicol Sci 104 283 293 1:CAS:528:DC%2BD1cXoslGhsbk%3D 10.1093/toxsci/kfn086 18448488 (Pubitemid 352038251)
15. G Troncone M Volante A Iaccarino P Zeppa I Cozzolino U Malapelle EA Palmieri G Conzo M Papotti L Palombini 2009 Cyclin D1 and D3 overexpression predicts malignant behavior in thyroid fine-needle aspirates suspicious for Hurthle cell neoplasms Cancer Cytopathol 117 522 529 1:CAS:528: DC%2BC3cXpvFOitA%3D%3D 19787802
16. S Maier MC Daroqui S Scherer S Roepcke A Velcich SM Shenoy RH Singer LH Augenlicht 2009 Butyrate and vitamin D3 induce transcriptional attenuation at the cyclin D1 locus in colonic carcinoma cells J Cell Physiol 218 638 642 1:CAS:528:DC%2BD1MXit1KhtL0%3D 10.1002/jcp.21642 19034928
17. I Joshi LM Minter J Telfer RM Demarest AJ Capobianco JC Aster P Sicinski A Fauq TE Golde BA Osborne 2009 Notch signaling mediates G1/S cell-cycle progression in T cells via cyclin D3 and its dependent kinases Blood 113 1689 1698 1:CAS:528:DC%2BD1MXisV2iu78%3D 10.1182/blood-2008-03-147967 19001083
18. Q Zhou M Stetler-Stevenson PS Steeg 1997 Inhibition of cyclin D expression in human breast carcinoma cells by retinoids in vitro Oncogene 15 107 115 1:CAS:528:DyaK2sXkslygtr8%3D 10.1038/sj.onc.1201142 9233783
19. M Chu J Guo CY Chen 2005 Long-term exposure to nicotine, via ras pathway, induces cyclin D1 to stimulate G1 cell cycle transition J Biol Chem 280 6369 6379 1:CAS:528:DC%2BD2MXhsV2qsrw%3D 10.1074/jbc.M408947200 15574422 (Pubitemid 40341183)
20. X Yu Y Luo Y Zhou Q Zhang J Wang N Wei M Mi J Zhu B Wang H Chang Y Tang 2008 BRCA1 overexpression sensitizes cancer cells to lovastatin via regulation of cyclin D1-CDK4-p21WAF1/CIP1 pathway: analyses using a breast cancer cell line and tumoral xenograft model Int J Oncol 33 555 563 1:CAS:528:DC%2BD1cXht1Wmu7vN 18695886
21. M Rudas M Lehnert A Huynh R Jakesz C Singer S Lax W Schippinger O Dietze R Greil W Stiglbauer W Kwasny R Grill M Stierer MF Gnant M Filipits 2008 Cyclin D1 expression in breast cancer patients receiving adjuvant tamoxifen-based therapy Clin Cancer Res 14 1767 1774 1:CAS:528:DC%2BD1cXjtlejur0%3D 10.1158/1078-0432.CCR-07-4122 18347178 (Pubitemid 351469462)
22. K Aaltonen RM Amini G Landberg H Eerola K Aittomaki P Heikkila H Nevanlinna C Blomqvist 2009 Cyclin D1 expression is associated with poor prognostic features in estrogen receptor positive breast cancer Breast Cancer Res Treat 113 75 82 1:CAS:528:DC%2BD1cXhsFWrs7bL 10.1007/s10549-008-9908-5 18240019
23. F Yamaguchi T Ariga Y Yoshimura H Nakazawa 2000 Antioxidative and anti-glycation activity of garcinol from Garcinia indica fruit rind J Agric Food Chem 48 180 185 1:CAS:528:DC%2BD3cXjsFWnsQ%3D%3D 10.1021/jf990845y 10691613 (Pubitemid 30120339)
24. F Yamaguchi M Saito T Ariga Y Yoshimura H Nakazawa 2000 Free radical scavenging activity and antiulcer activity of garcinol from Garcinia indica fruit rind J Agric Food Chem 48 2320 2325 1:CAS:528:DC%2BD3cXjt1emtrk%3D 10.1021/jf990908c 10888544 (Pubitemid 30431234)
25. MH Pan WL Chang SY Lin-Shiau CT Ho JK Lin 2001 Induction of apoptosis by garcinol and curcumin through cytochrome c release and activation of caspases in human leukemia HL-60 cells J Agric Food Chem 49 1464 1474 1:CAS:528: DC%2BD3MXhtVymsrs%3D 10.1021/jf001129v 11312881 (Pubitemid 32884979)
26. T Tanaka H Kohno R Shimada S Kagami F Yamaguchi S Kataoka T Ariga A Murakami K Koshimizu H Ohigashi 2000 Prevention of colonic aberrant crypt foci by dietary feeding of garcinol in male F344 rats Carcinogenesis 21 1183 1189 1:CAS:528:DC%2BD3cXksF2gs7g%3D 10.1093/carcin/21.6.1183 10837008
27. CM Yang IT Lee CC Lin YL Yang SF Luo YR Kou LD Hsiao 2009 Cigarette smoke extract induces COX-2 expression via a PKCalpha/c-Src/EGFR, PDGFR/PI3K/Akt/NF-kappaB pathway and p300 in tracheal smooth muscle cells Am J Physiol Lung Cell Mol Physiol 297 L892 L902 1:CAS:528:DC%2BD1MXhsVahtrrK 10.1152/ajplung.00151.2009 19717552
28. MH Pan MC Huang YJ Wang JK Lin CH Lin 2003 Induction of apoptosis by hydroxydibenzoylmethane through coordinative modulation of cyclin D3, Bcl-X(L), and Bax, release of cytochrome c, and sequential activation of caspases in human colorectal carcinoma cells J Agric Food Chem 51 3977 3984 1:CAS:528: DC%2BD3sXktlyqu7c%3D 10.1021/jf034094i 12822933
29. Chen LC, Liu YC, Liang YC, Ho YS and Lee WS (2009) Magnolol inhibits human glioblastoma cell proliferation through upregulation of p21/Cip1. J Agric Food Chem (in press)
30. Tu SH, Chang CC, Chen CS, Tam KW, Wang YJ, Lee CH, Lin HW, Cheng TC, Huang CS, Chu JS, Shih NY, Chen LC, Leu SJ, Ho YS, Wu CH (2009). Increased expression of enolase alpha in human breast cancer confers tamoxifen resistance in human breast cancer cells. Breast Cancer Res Treat (in press)
31. KA West J Brognard AS Clark IR Linnoila X Yang SM Swain C Harris S Belinsky PA Dennis 2003 Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells J Clin Invest 111 81 90 1:CAS:528:DC%2BD3sXhvVamsg%3D%3D 12511591
32. S Narayan AS Jaiswal D Kang P Srivastava GM Das CG Gairola 2004 Cigarette smoke condensate-induced transformation of normal human breast epithelial cells in vitro Oncogene 23 5880 5889 1:CAS:528:DC%2BD2cXmt1Krt7o%3D 10.1038/sj.onc.1207792 15208684 (Pubitemid 39093532)
33. F Chen E Kim CC Wang LE Harrison 2005 Ciglitazone-induced p27 gene transcriptional activity is mediated through Sp1 and is negatively regulated by the MAPK signaling pathway Cell Signal 17 1572 1577 1:CAS:528: DC%2BD2MXpvV2ltr4%3D 10.1016/j.cellsig.2005.03.012 15951157 (Pubitemid 41253996)
34. DS Wilkinson SK Ogden SA Stratton JL Piechan TT Nguyen GA Smulian MC Barton 2005 A direct intersection between p53 and transforming growth factor beta pathways targets chromatin modification and transcription repression of the alpha-fetoprotein gene Mol Cell Biol 25 1200 1212 1:CAS:528: DC%2BD2MXptF2jsA%3D%3D 10.1128/MCB.25.3.1200-1212.2005 15657445 (Pubitemid 40165825)
35. AP Govind P Vezina WN Green 2009 Nicotine-induced upregulation of nicotinic receptors: underlying mechanisms and relevance to nicotine addiction Biochem Pharmacol 78 756 765 1:CAS:528:DC%2BD1MXhtVSmsLnJ 10.1016/j.bcp.2009.06. 011 19540212
36. S Nuutinen E Ekokoski E Lahdensuo RK Tuominen 2006 Nicotine-induced upregulation of human neuronal nicotinic alpha7-receptors is potentiated by modulation of cAMP and PKC in SH-EP1-halpha7 cells Eur J Pharmacol 544 21 30 1:CAS:528:DC%2BD28XotV2gt7o%3D 10.1016/j.ejphar.2006.06.038 16846598 (Pubitemid 44148574)
37. HA Al-Wadei HK Plummer 3rd HM Schuller 2009 Nicotine stimulates pancreatic cancer xenografts by systemic increase in stress neurotransmitters and suppression of the inhibitory neurotransmitter gamma-aminobutyric acid Carcinogenesis 30 506 511 1:CAS:528:DC%2BD1MXivFSitbw%3D 10.1093/carcin/bgp010 19131543
38. G Ramazzotti I Faenza GC Gaboardi M Piazzi A Bavelloni R Fiume L Manzoli AM Martelli L Cocco 2008 Catalytic activity of nuclear PLC-beta(1) is required for its signalling function during C2C12 differentiation Cell Signal 20 2013 2021 1:CAS:528:DC%2BD1cXhtFOmtL7N 10.1016/j.cellsig.2008.07.009 18694821
39. AB Elgoyhen DS Johnson J Boulter DE Vetter S Heinemann 1994 Alpha 9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells Cell 79 705 715 1:CAS:528:DyaK2MXit1Gksrc%3D 10.1016/0092-8674(94)90555-X 7954834 (Pubitemid 24363813)
40. J Arredondo AI Chernyavsky DL Jolkovsky KE Pinkerton SA Grando 2008 Receptor-mediated tobacco toxicity: acceleration of sequential expression of alpha5 and alpha7 nicotinic receptor subunits in oral keratinocytes exposed to cigarette smoke FASEB J 22 1356 1368 1:CAS:528:DC%2BD1cXltlWksr8%3D 10.1096/fj.07-9965.com 18450646 (Pubitemid 351656777)
41. M Noda Y Furutani H Takahashi M Toyosato T Tanabe S Shimizu S Kikyotani T Kayano T Hirose S Inayama, et al. 1983 Cloning and sequence analysis of calf cDNA and human genomic DNA encoding alpha-subunit precursor of muscle acetylcholine receptor Nature 305 818 823 1:CAS:528:DyaL2cXks1ahsg%3D%3D 10.1038/305818a0 6688857
42. P Nef C Oneyser C Alliod S Couturier M Ballivet 1988 Genes expressed in the brain define three distinct neuronal nicotinic acetylcholine receptors EMBO J 7 595 601 1:CAS:528:DyaL1cXltVGltbk%3D 3267226
43. K Wada M Ballivet J Boulter J Connolly E Wada ES Deneris LW Swanson S Heinemann J Patrick 1988 Functional expression of a new pharmacological subtype of brain nicotinic acetylcholine receptor Science 240 330 334 1:CAS:528:DyaL1cXls1Cmtbc%3D 10.1126/science.2832952 2832952
44. LR Lustig 2006 Nicotinic acetylcholine receptor structure and function in the efferent auditory system Anat Rec A Discov Mol Cell Evol Biol 288 424 434 16550589
45. VT Nguyen A Ndoye SA Grando 2000 Novel human alpha9 acetylcholine receptor regulating keratinocyte adhesion is targeted by Pemphigus vulgaris autoimmunity Am J Pathol 157 1377 1391 1:CAS:528:DC%2BD3cXnsVKisr8%3D 11021840
46. M Vincler S Wittenauer R Parker M Ellison BM Olivera JM McIntosh 2006 Molecular mechanism for analgesia involving specific antagonism of alpha9alpha10 nicotinic acetylcholine receptors Proc Natl Acad Sci USA 103 17880 17884 1:CAS:528:DC%2BD28Xht1Klur%2FP 10.1073/pnas.0608715103 17101979 (Pubitemid 44852254)
47. F Sgard E Charpantier S Bertrand N Walker D Caput D Graham D Bertrand F Besnard 2002 A novel human nicotinic receptor subunit, alpha10, that confers functionality to the alpha9-subunit Mol Pharmacol 61 150 159 1:CAS:528:DC%2BD38XltlWl 10.1124/mol.61.1.150 11752216 (Pubitemid 34049522)
48. AB Elgoyhen DE Vetter E Katz CV Rothlin SF Heinemann J Boulter 2001 alpha10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells Proc Natl Acad Sci USA 98 3501 3506 1:CAS:528:DC%2BD3MXit1alu7Y%3D 10.1073/pnas.051622798 11248107 (Pubitemid 32220874)
49. AI Chernyavsky J Arredondo DE Vetter SA Grando 2007 Central role of alpha9 acetylcholine receptor in coordinating keratinocyte adhesion and motility at the initiation of epithelialization Exp Cell Res 313 3542 3555 1:CAS:528:DC%2BD2sXhtVOlsbbM 10.1016/j.yexcr.2007.07.011 17706194 (Pubitemid 47404552)
50. J Arredondo AI Chernyavsky DL Jolkovsky KE Pinkerton SA Grando 2007 Receptor-mediated tobacco toxicity: alterations of the NF-kappaB expression and activity downstream of alpha7 nicotinic receptor in oral keratinocytes Life Sci 80 2191 2194 1:CAS:528:DC%2BD2sXmtVehsbg%3D 10.1016/j.lfs.2007.01.013 17291542 (Pubitemid 46824132)
51. P Song HS Sekhon XW Fu M Maier Y Jia J Duan BJ Proskosil C Gravett J Lindstrom GP Mark S Saha ER Spindel 2008 Activated cholinergic signaling provides a target in squamous cell lung carcinoma Cancer Res 68 4693 4700 1:CAS:528:DC%2BD1cXnt1aqurg%3D 10.1158/0008-5472.CAN-08-0183 18559515
52. T Sato T Abe N Nakamoto Y Tomaru N Koshikiya J Nojima S Kokabu Y Sakata A Kobayashi T Yoda 2008 Nicotine induces cell proliferation in association with cyclin D1 up-regulation and inhibits cell differentiation in association with p53 regulation in a murine pre-osteoblastic cell line Biochem Biophys Res Commun 377 126 130 1:CAS:528:DC%2BD1cXhtlaqsLfE 10.1016/j.bbrc.2008.09.114 18835254
53. R Duan E Ginsburg BK Vonderhaar 2008 Estrogen stimulates transcription from the human prolactin distal promoter through AP1 and estrogen responsive elements in T47D human breast cancer cells Mol Cell Endocrinol 281 9 18 1:CAS:528:DC%2BD2sXhsVOltrfJ 10.1016/j.mce.2007.10.004 18022314 (Pubitemid 350296603)
54. MG Cattaneo A Codignola LM Vicentini F Clementi E Sher 1993 Nicotine stimulates a serotonergic autocrine loop in human small-cell lung carcinoma Cancer Res 53 5566 5568 1:CAS:528:DyaK2cXisFeruw%3D%3D 8221698
55. R Seger EG Krebs 1995 The MAPK signaling cascade FASEB J 9 726 735 1:CAS:528:DyaK2MXmvFCltb0%3D 7601337
56. J Guo M Chu T Abbeyquaye CY Chen 2005 Persistent nicotine treatment potentiates amplification of the dihydrofolate reductase gene in rat lung epithelial cells as a consequence of Ras activation J Biol Chem 280 30422 30431 1:CAS:528:DC%2BD2MXos1Cqsro%3D 10.1074/jbc.M504688200 15983034 (Pubitemid 41216226)