nach oben

Erschienen in:

01.09.2011 | Preclinical study

Crosstalk between nicotine and estrogen-induced estrogen receptor activation induces α9-nicotinic acetylcholine receptor expression in human breast cancer cells

verfasst von: Chia-Hwa Lee, Ya-Chieh Chang, Ching-Shyang Chen, Shih-Hsin Tu, Ying-Jan Wang, Li-Ching Chen, Yu-Jia Chang, Po-Li Wei, Hui-Wen Chang, Chien-Hsi Chang, Ching-Shui Huang, Chih-Hsiung Wu, Yuan-Soon Ho

Erschienen in: Breast Cancer Research and Treatment | Ausgabe 2/2011

Einloggen, um Zugang zu erhalten

Abstract

The primary aim of this study was to elucidate the role of the estrogen receptor (ER), a transcription factor involved in the nicotine- and 17β-estradiol (E2)-mediated up-regulation of α9-nAChR gene expression. A real-time polymerase chain reaction (PCR) assay was used to quantify the α9-nAChR mRNA expression levels of surgically isolated (n = 339) and laser-capture microdissected tissues (ER+ versus ER−, n = 6 per group). Chromatin immunoprecipitation (ChIP) and luciferase-promoter activity assays were used to investigate the ER-mediated transcriptional regulation of α9-nAChR gene expression. We observed that breast tumors with higher α9-nAChR mRNA expression levels (i.e., a mean fold ratio in the tumor/normal-paired samples of greater than tenfold) were associated with the lowest 5-year disease-specific survival rate (50%, dead/alive = 4/4, total = 8 patients, P = 0.006), in contrast to breast tumors with low levels (i.e., a mean fold ratio of less than onefold) of α9-nAChR expression (88%, dead/alive = 3/22, total = 25 patients). Furthermore, higher α9-nAChR mRNA expression levels were preferentially detected in ER+ tumor tissues in comparison to ER− tumor tissues (ER+ versus ER− patients: n = 160 vs. 72; mean fold ratios of α9-nAChR expression = 11 ± 3 vs. 6.7 ± 2.3 fold, respectively). In vitro promoter-binding assays demonstrated that the ER is a major transcription factor that mediates nicotine- and E2-induced up-regulation of α9-nAChR gene expression in MCF-7 cells. In conclusion, our data indicate that the ER plays a central role in mediating α9-nAChR gene up-regulation in response to either nicotine or E2 stimulation.

Nur mit Berechtigung zugänglich

Poola I, De Witty RL, Marshalleck JJ, Bhatnagar R, Abraham J, Leffall LD (2005) Identification of MMP-1 as a putative breast cancer predictive marker by global gene expression analysis. Nat Med 11:481–483PubMedCrossRef

Sagiv SK, Gaudet MM, Eng SM, Abrahamson PE, Shantakumar S, Teitelbaum SL, Britton JA, Bell P, Thomas JA, Neugut AI, Santella RM, Gammon MD (2007) Active and passive cigarette smoke and breast cancer survival. Ann Epidemiol 17:385–393PubMedCrossRef

Lin Y, Kikuchi S, Tamakoshi K, Wakai K, Kondo T, Niwa Y, Yatsuya H, Nishio K, Suzuki S, Tokudome S, Yamamoto A, Toyoshima H, Mori M, Tamakoshi A (2008) Active smoking, passive smoking, and breast cancer risk: findings from the Japan collaborative cohort study for evaluation of cancer risk. J Epidemiol 18:77–83PubMedCrossRef

Slattery ML, Curtin K, Giuliano AR, Sweeney C, Baumgartner R, Edwards S, Wolff RK, Baumgartner KB, Byers T (2008) Active and passive smoking, IL6, ESR1, and breast cancer risk. Breast Cancer Res Treat 109:101–111PubMedCrossRef

Benowitz NL, Jacob P III (1984) Nicotine and carbon monoxide intake from high- and low-yield cigarettes. Clin Pharmacol Ther 36:265–270PubMedCrossRef

Armitage AK, Dollery CT, George CF, Houseman TH, Lewis PJ, Turner DM (1975) Absorption and metabolism of nicotine from cigarettes. Br Med J 4:313–316PubMedCrossRef

Lindell G, Farnebo LO, Chen D, Nexo E, Rask Madsen J, Bukhave K, Graffner H (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 28:487–494PubMedCrossRef

Mei J, Hu H, McEntee M, Plummer H III, Song P, Wang HC (2003) Transformation of non-cancerous human breast epithelial cell line MCF10A by the tobacco-specific carcinogen NNK. Breast Cancer Res Treat 79:95–105PubMedCrossRef

Siriwardhana N, Choudhary S, Wang HC (2008) Precancerous model of human breast epithelial cells induced by NNK for prevention. Breast Cancer Res Treat 109:427–441PubMedCrossRef

10.

Wong HP, Yu L, Lam EK, Tai EK, Wu WK, Cho CH (2007) Nicotine promotes colon tumor growth and angiogenesis through beta-adrenergic activation. Toxicol Sci 97:279–287PubMedCrossRef

11.

Dasgupta P, Rizwani W, Pillai S, Kinkade R, Kovacs M, Rastogi S, Banerjee S, Carless M, Kim E, Coppola D, Haura E, Chellappan S (2008) Nicotine induces cell proliferation, invasion and epithelial-mesenchymal transition in a variety of human cancer cell lines. Int J Cancer 124:36–45CrossRef

12.

Heeschen C, Jang JJ, Weis M, Pathak A, Kaji S, Hu RS, Tsao PS, Johnson FL, Cooke JP (2001) Nicotine stimulates angiogenesis and promotes tumor growth and atherosclerosis. Nat Med 7:833–839PubMedCrossRef

13.

Brejc K, van Dijk WJ, Klaassen RV, Schuurmans M, van Der Oost J, Smit AB, Sixma TK (2001) Crystal structure of an ach-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 411:269–276PubMedCrossRef

14.

Avramopoulou V, Mamalaki A, Tzartos SJ (2004) Soluble, oligomeric, and ligand-binding extracellular domain of the human alpha7 acetylcholine receptor expressed in yeast: replacement of the hydrophobic cysteine loop by the hydrophilic loop of the ACh-binding protein enhances protein solubility. J Biol Chem 279:38287–38293PubMedCrossRef

15.

Schuller HM (2007) Nitrosamines as nicotinic receptor ligands. Life Sci 80:2274–2280PubMedCrossRef

16.

Schuller HM, Orloff M (1998) Tobacco-specific carcinogenic nitrosamines. Ligands for nicotinic acetylcholine receptors in human lung cancer cells. Biochem Pharmacol 55:1377–1384PubMedCrossRef

17.

Dasgupta P, Chellappan SP (2006) Nicotine-mediated cell proliferation and angiogenesis: new twists to an old story. Cell Cycle 5:2324–2328PubMedCrossRef

18.

Dasgupta P, Kinkade R, Joshi B, Decook C, Haura E, Chellappan S (2006) Nicotine inhibits apoptosis induced by chemotherapeutic drugs by up-regulating XIAP and survivin. Proc Natl Acad Sci USA 103:6332–6337PubMedCrossRef

19.

Dasgupta P, Rastogi S, Pillai S, Ordonez-Ercan D, Morris M, Haura E, Chellappan S (2006) Nicotine induces cell proliferation by beta-arrestin-mediated activation of Src and Rb-Raf-1 pathways. J Clin Invest 116:2208–2217PubMedCrossRef

20.

Jin Z, Gao F, Flagg T, Deng X (2004) Nicotine induces multi-site phosphorylation of bad in association with suppression of apoptosis. J Biol Chem 279:23837–23844PubMedCrossRef

21.

Xu J, Huang H, Pan C, Zhang B, Liu X, Zhang L (2007) Nicotine inhibits apoptosis induced by cisplatin in human oral cancer cells. Int J Oral Maxillofac Surg 36:739–744PubMedCrossRef

22.

Chlebowski RT, Kuller LH, Prentice RL, Stefanick ML, Manson JE, Gass M, Aragaki AK, Ockene JK, Lane DS, Sarto GE, Rajkovic A, Schenken R, Hendrix SL, Ravdin PM, Rohan TE, Yasmeen S, Anderson G (2009) Breast cancer after use of estrogen plus progestin in postmenopausal women. N Engl J Med 360:573–587PubMedCrossRef

23.

Brzozowski AM, Pike AC, Dauter Z, Hubbard RE, Bonn T, Engstrom O, Ohman L, Greene GL, Gustafsson JA, Carlquist M (1997) Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 389:753–758PubMedCrossRef

24.

Rosenfeld MG, Glass CK (2001) Coregulator codes of transcriptional regulation by nuclear receptors. J Biol Chem 276:36865–36868PubMedCrossRef

25.

Daniell HW (1980) Estrogen receptors, breast cancer, and smoking. N Engl J Med 302:1478PubMed

26.

Lee CH, Huang CS, Chen CS, Tu SH, Wang YJ, Chang YJ, Tam KW, Wei PL, Cheng TC, Chu JS, Chen LC, Wu CH, Ho YS (2010) Overexpression and activation of the {alpha}9-nicotinic receptor during tumorigenesis in human breast epithelial cells. J Natl Cancer Inst 102(17):1322–1335PubMedCrossRef

27.

Umayahara Y, Kawamori R, Watada H, Imano E, Iwama N, Morishima T, Yamasaki Y, Kajimoto Y, Kamada T (1994) Estrogen regulation of the insulin-like growth factor I gene transcription involves an AP-1 enhancer. J Biol Chem 269:16433–16442PubMed

28.

Lewis JS, Thomas TJ, Pestell RG, Albanese C, Gallo MA, Thomas T (2005) Differential effects of 16alpha-hydroxyestrone and 2-methoxyestradiol on cyclin D1 involving the transcription factor ATF-2 in MCF-7 breast cancer cells. J Mol Endocrinol 34:91–105PubMedCrossRef

29.

Ho YS, Lai CS, Liu HI, Ho SY, Tai C, Pan MH, Wang YJ (2007) Dihydrolipoic acid inhibits skin tumor promotion through anti-inflammation and anti-oxidation. Biochem Pharmacol 73:1786–1795PubMed

30.

Aerts JL, Gonzales MI, Topalian SL (2004) Selection of appropriate control genes to assess expression of tumor antigens using real-time RT-PCR. Biotechniques 36:84–86, 88, 90–81PubMed

31.

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 (2010) Increased expression of enolase alpha in human breast cancer confers tamoxifen resistance in human breast cancer cells. Breast Cancer Res Treat 121(3):539–553PubMedCrossRef

32.

Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, Yankner BA (2004) Gene regulation and DNA damage in the ageing human brain. Nature 429:883–891PubMedCrossRef

33.

Huang C, Yang L, Li Z, Yang J, Zhao J, Dehui X, Liu L, Wang Q, Song T (2007) Detection of CCND1 amplification using laser capture microdissection coupled with real-time polymerase chain reaction in human esophageal squamous cell carcinoma. Cancer Genet Cytogenet 175:19–25PubMedCrossRef

34.

McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM (2005) Reporting recommendations for tumor marker prognostic studies (remark). J Natl Cancer Inst 97:1180–1184PubMedCrossRef

35.

McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM (2006) Reporting recommendations for tumor marker prognostic studies (remark). Breast Cancer Res Treat 100:229–235PubMedCrossRef

36.

Liu Z, Yu X, Shaikh ZA (2008) Rapid activation of ERK1/2 and AKT in human breast cancer cells by cadmium. Toxicol Appl Pharmacol 228:286–294PubMedCrossRef

37.

Lee YR, Park J, Yu HN, Kim JS, Youn HJ, Jung SH (2005) Up-regulation of PI3K/Akt signaling by 17beta-estradiol through activation of estrogen receptor-alpha, but not estrogen receptor-beta, and stimulates cell growth in breast cancer cells. Biochem Biophys Res Commun 336:1221–1226PubMedCrossRef

38.

Likhite VS, Stossi F, Kim K, Katzenellenbogen BS, Katzenellenbogen JA (2006) Kinase-specific phosphorylation of the estrogen receptor changes receptor interactions with ligand, deoxyribonucleic acid, and coregulators associated with alterations in estrogen and tamoxifen activity. Mol Endocrinol 20:3120–3132PubMedCrossRef

39.

Thomas RS, Sarwar N, Phoenix F, Coombes RC, Ali S (2008) Phosphorylation at serines 104 and 106 by Erk1/2 MAPK is important for estrogen receptor-alpha activity. J Mol Endocrinol 40:173–184PubMedCrossRef

40.

Chen D, Washbrook E, Sarwar N, Bates GJ, Pace PE, Thirunuvakkarasu V, Taylor J, Epstein RJ, Fuller-Pace FV, Egly JM, Coombes RC, Ali S (2002) Phosphorylation of human estrogen receptor alpha at serine 118 by two distinct signal transduction pathways revealed by phosphorylation-specific antisera. Oncogene 21:4921–4931PubMedCrossRef

41.

Pasapera Limon AM, Herrera-Munoz J, Gutierrez-Sagal R, Ulloa-Aguirre A (2003) The phosphatidylinositol 3-kinase inhibitor LY294002 binds the estrogen receptor and inhibits 17beta-estradiol-induced transcriptional activity of an estrogen sensitive reporter gene. Mol Cell Endocrinol 200:199–202PubMedCrossRef

42.

Yamashita H, Nishio M, Toyama T, Sugiura H, Kondo N, Kobayashi S, Fujii Y, Iwase H (2008) Low phosphorylation of estrogen receptor alpha (ERalpha) serine 118 and high phosphorylation of ERalpha serine 167 improve survival in ER-positive breast cancer. Endocr Relat Cancer 15:755–763PubMedCrossRef

43.

Huang J, Li X, Maguire CA, Hilf R, Bambara RA, Muyan M (2005) Binding of estrogen receptor beta to estrogen response element in situ is independent of estradiol and impaired by its amino terminus. Mol Endocrinol 19:2696–2712PubMedCrossRef

44.

Glidewell-Kenney C, Weiss J, Lee EJ, Pillai S, Ishikawa T, Ariazi EA, Jameson JL (2005) Ere-independent ERalpha target genes differentially expressed in human breast tumors. Mol Cell Endocrinol 245:53–59PubMedCrossRef

45.

Lustig LR, Peng H (2002) Chromosome location and characterization of the human nicotinic acetylcholine receptor subunit alpha (alpha) 9 (CHRNA9) gene. Cytogenet Genome Res 98:154–159PubMedCrossRef

46.

Nezbedova P, Brtko J (2004) 1alpha,25-dihydroxyvitamin D3 inducible transcription factor and its role in the vitamin D action. Endocr Regul 38:29–38PubMed

47.

Duan R, Ginsburg E, Vonderhaar BK (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 281:9–18PubMedCrossRef

48.

Coughlin SS, Ekwueme DU (2009) Breast cancer as a global health concern. Cancer Epidemiol 33:315–318PubMedCrossRef

49.

Maskarinec G, Zhang Y, Takata Y, Pagano I, Shumay DM, Goodman MT, Le Marchand L, Nomura AM, Wilkens LR, Kolonel LN (2006) Trends of breast cancer incidence and risk factor prevalence over 25 years. Breast Cancer Res Treat 98:45–55PubMedCrossRef

50.

Terry PD, Goodman M (2006) Is the association between cigarette smoking and breast cancer modified by genotype? A review of epidemiologic studies and meta-analysis. Cancer Epidemiol Biomarkers Prev 15:602–611PubMedCrossRef

51.

Crabb C (2003) Is breast cancer linked to smoking? Bull World Health Organ 81:74PubMed

52.

Egan KM, Stampfer MJ, Hunter D, Hankinson S, Rosner BA, Holmes M, Willett WC, Colditz GA (2002) Active and passive smoking in breast cancer: prospective results from the nurses’ health study. Epidemiology 13:138–145PubMedCrossRef

53.

Nagata C, Mizoue T, Tanaka K, Tsuji I, Wakai K, Inoue M, Tsugane S (2006) Tobacco smoking and breast cancer risk: an evaluation based on a systematic review of epidemiological evidence among the Japanese population. Jpn J Clin Oncol 36:387–394PubMedCrossRef

54.

Reynolds P, Hurley S, Goldberg DE, Anton-Culver H, Bernstein L, Deapen D, Horn-Ross PL, Peel D, Pinder R, Ross RK, West D, Wright WE, Ziogas A (2004) Active smoking, household passive smoking, and breast cancer: evidence from the California teachers study. J Natl Cancer Inst 96:29–37PubMedCrossRef

55.

Hanaoka T, Yamamoto S, Sobue T, Sasaki S, Tsugane S (2005) Active and passive smoking and breast cancer risk in middle-aged Japanese women. Int J Cancer 114:317–322PubMedCrossRef

56.

Gram IT, Braaten T, Terry PD, Sasco AJ, Adami HO, Lund E, Weiderpass E (2005) Breast cancer risk among women who start smoking as teenagers. Cancer Epidemiol Biomarkers Prev 14:61–66PubMed

57.

Morabia A, Costanza MC, Bernstein MS, Rielle JC (2002) Ages at initiation of cigarette smoking and quit attempts among women: a generation effect. Am J Public Health 92:71–74PubMedCrossRef

58.

Steinetz BG, Gordon T, Lasano S, Horton L, Ng SP, Zelikoff JT, Nadas A, Bosland MC (2006) The parity-related protection against breast cancer is compromised by cigarette smoke during rat pregnancy: observations on tumorigenesis and immunological defenses of the neonate. Carcinogenesis 27:1146–1152PubMedCrossRef

59.

Al-Delaimy WK, Cho E, Chen WY, Colditz G, Willet WC (2004) A prospective study of smoking and risk of breast cancer in young adult women. Cancer Epidemiol Biomarkers Prev 13:398–404PubMed

60.

Coyle YM (2004) The effect of environment on breast cancer risk. Breast Cancer Res Treat 84:273–288PubMedCrossRef

61.

Hecht SS (1999) DNA adduct formation from tobacco-specific N-nitrosamines. Mutat Res 424:127–142PubMed

62.

Heeschen C, Weis M, Aicher A, Dimmeler S, Cooke JP (2002) A novel angiogenic pathway mediated by non-neuronal nicotinic acetylcholine receptors. J Clin Invest 110:527–536PubMed

63.

West KA, Brognard J, Clark AS, Linnoila IR, Yang X, Swain SM, Harris C, Belinsky S, Dennis PA (2003) Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells. J Clin Invest 111:81–90PubMed

64.

Maneckjee R, Minna JD (1990) Opioid and nicotine receptors affect growth regulation of human lung cancer cell lines. Proc Natl Acad Sci USA 87:3294–3298PubMedCrossRef

65.

Trombino S, Cesario A, Margaritora S, Granone P, Motta G, Falugi C, Russo P (2004) Alpha7-nicotinic acetylcholine receptors affect growth regulation of human mesothelioma cells: role of mitogen-activated protein kinase pathway. Cancer Res 64:135–145PubMedCrossRef

66.

Teixeira C, Reed JC, Pratt MA (1995) Estrogen promotes chemotherapeutic drug resistance by a mechanism involving Bcl-2 proto-oncogene expression in human breast cancer cells. Cancer Res 55:3902–3907PubMed

67.

Ahmad S, Singh N, Glazer RI (1999) Role of AKT1 in 17beta-estradiol- and insulin-like growth factor I (IGF-I)-dependent proliferation and prevention of apoptosis in MCF-7 breast carcinoma cells. Biochem Pharmacol 58:425–430PubMedCrossRef

Titel: Crosstalk between nicotine and estrogen-induced estrogen receptor activation induces α9-nicotinic acetylcholine receptor expression in human breast cancer cells
verfasst von: Chia-Hwa Lee
Ya-Chieh Chang
Ching-Shyang Chen
Shih-Hsin Tu
Ying-Jan Wang
Li-Ching Chen
Yu-Jia Chang
Po-Li Wei
Hui-Wen Chang
Chien-Hsi Chang
Ching-Shui Huang
Chih-Hsiung Wu
Yuan-Soon Ho
Publikationsdatum: 01.09.2011
Verlag: Springer US
Erschienen in: Breast Cancer Research and Treatment / Ausgabe 2/2011
Print ISSN: 0167-6806
Elektronische ISSN: 1573-7217
DOI: https://doi.org/10.1007/s10549-010-1209-0

Springer Medizin

Crosstalk between nicotine and estrogen-induced estrogen receptor activation induces α9-nicotinic acetylcholine receptor expression in human breast cancer cells

Abstract

Neu im Fachgebiet Onkologie

Adjuvante Immuntherapie verlängert Leben bei RCC

Alectinib verbessert krankheitsfreies Überleben bei ALK-positivem NSCLC

Bei Senioren mit Prostatakarzinom auf Anämie achten!

ICI-Therapie in der Schwangerschaft wird gut toleriert

Update Onkologie

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 2/2011

Surgery of the primary tumor does not improve survival in stage IV breast cancer

Androgen receptor polyglutamine tract length in Egyptian male breast cancer patients

The PI3 kinase/mTOR blocker NVP-BEZ235 overrides resistance against irreversible ErbB inhibitors in breast cancer cells

Two patients with germline mutations in both BRCA1 and BRCA2 discovered unintentionally: a case series and discussion of BRCA testing modalities

Cancer risk in Jewish BRCA1 and BRCA2 mutation carriers: Effects of oral contraceptive use and parental origin of mutation

Ras-related protein 1 and the insulin-like growth factor type I receptor are associated with risk of progression in patients diagnosed with carcinoma in situ

Neu im Fachgebiet Onkologie

Adjuvante Immuntherapie verlängert Leben bei RCC

Alectinib verbessert krankheitsfreies Überleben bei ALK-positivem NSCLC

Bei Senioren mit Prostatakarzinom auf Anämie achten!

ICI-Therapie in der Schwangerschaft wird gut toleriert

Update Onkologie