The alpha9 nicotinic acetylcholine receptor is the key mediator in nicotine-enhanced cancer metastasis in breast cancer cells

Journal of Experimental and Clinical Medicine

Volumn 3, Issue 6, 2011, Pages 283-292

  Hung, Chin Sheng ^a,b,c   Peng, Yu Jin ^b   Wei, Po Li ^a,b,c   Lee, Chia Hwa ^a   Su, Hou Yu ^f   Ho, Yuan Soon ^a,d   Lin, Shyr Yi ^b,d   Wu, Chih Hsiung ^a,b,c,e   Chang, Yu Jia ^a,b,c  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^e TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^f Saint Mary's Hospital Luodong   (Taiwan)

Author keywords

Breast cancer; Epithelial to mesenchymal transition (EMT); Migration; Nicotine; Nicotinic acetylcholine receptor (nAChR); Smoking

Indexed keywords

FIBRONECTIN; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA9; NICOTINIC RECEPTOR BLOCKING AGENT; SMALL INTERFERING RNA; SMALL MOLECULE INHIBITOR; UNCLASSIFIED DRUG; VIMENTIN;

ARTICLE; BREAST CANCER; CANCER CELL; CELL MIGRATION; CONTROLLED STUDY; DISEASE CONTROL; HUMAN; HUMAN CELL; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; WOUND HEALING;

EID: 83555178424     PISSN: 18783317     EISSN: 18783325     Source Type: Journal    
DOI: 10.1016/j.jecm.2011.10.008     Document Type: Article

References (46)

1. Coughlin S.S., Ekwueme D.U. Breast cancer as a global health concern. Cancer Epidemiol 2009, 33(5):315-318.
2. Jemal A., Siegel R., Xu J., Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010, 60(5):277-300.
3. Shen Y.C., Chang C.J., Hsu C., Cheng C.C., Chiu C.F., Cheng A.L. Significant difference in the trends of female breast cancer incidence between Taiwanese and Caucasian Americans: implications from age-period-cohort analysis. Cancer Epidemiol Biomarkers Prev 2005, 14(8):1986-1990.
4. O'Shaughnessy J. Extending survival with chemotherapy in metastatic breast cancer. Oncologist 2005, 10(Suppl. 3):20-29.
5. Rivera E. Implications of anthracycline-resistant and taxane-resistant metastatic breast cancer and new therapeutic options. Breast J 2010, 16(3):252-263.
6. Porkka K., Blomqvist C., Rissanen P., Elomaa I., Pyrhonen S. Salvage therapies in women who fail to respond to first-line treatment with fluorouracil, epirubicin, and cyclophosphamide for advanced breast cancer. J Clin Oncol 1994, 12(8):1639-1647.
7. Hecht S.S. Tobacco smoke carcinogens and breast cancer. Environ Mol Mutagen 2002, 39(2-3):119-126.
8. Conti-Fine B.M., Navaneetham D., Lei S., Maus A.D. Neuronal nicotinic receptors in non-neuronal cells: new mediators of tobacco toxicity?. Eur J Pharmacol 2000, 393(1-3):279-294.
9. Schuller H.M., Orloff M. Tobacco-specific carcinogenic nitrosamines. Ligands for nicotinic acetylcholine receptors in human lung cancer cells. Biochem Pharmacol 1998, 55(9):1377-1384.
10. Lindstrom J. Nicotinic acetylcholine receptors in health and disease. Mol Neurobiol 1997, 15(2):193-222.
11. Grando S.A., Kawashima K., Wessler I. Introduction: the non-neuronal cholinergic system in humans. Life Sci 2003, 72(18-19):2009-2012.
12. Ho Y.S., Chen C.H., Wang Y.J., Pestell R.G., Albanese C., Chen R.J., Chang M.C., et al. 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 2005, 205(2):133-148.
13. Improgo M.R., Scofield M.D., Tapper A.R., Gardner P.D. From smoking to lung cancer: the CHRNA5/A3/B4 connection. Oncogene 2010, 29(35):4874-4884.
14. Dasgupta P., Kinkade R., Joshi B., Decook C., Haura E., Chellappan S. Nicotine inhibits apoptosis induced by chemotherapeutic drugs by up-regulating XIAP and survivin. Proc Natl Acad Sci U S A 2006, 103(16):6332-6337.
15. Dasgupta P., Rizwani W., Pillai S., Kinkade R., Kovacs M., Rastogi S., Banerjee S., et al. Nicotine induces cell proliferation, invasion and epithelial-mesenchymal transition in a variety of human cancer cell lines. Int J Cancer 2009, 124(1):36-45.
16. Egleton R.D., Brown K.C., Dasgupta P. Nicotinic acetylcholine receptors in cancer: multiple roles in proliferation and inhibition of apoptosis. Trends Pharmacol Sci 2008, 29(3):151-158.
17. Lee C.H., Huang C.S., Chen C.S., Tu S.H., Wang Y.J., Chang Y.J., Tam K.W., et al. Overexpression and activation of the alpha9-nicotinic receptor during tumorigenesis in human breast epithelial cells. J Natl Cancer Inst 2010, 102(17):1322-1335.
18. Ho Y.S., Lee C.H., Wu C.H. a9-nicotinic acetylcholine receptor serves as a molecular target for breast cancer therapy. J Exp Clin Med 2011, 3:246-251.
19. Chen R.J., Ho Y.S., Wu C.H., Wang Y.J. Molecular mechanisms of nicotine-induced bladder cancer. J Exp Clin Med 2011, 3:252-256.
20. Wei P.L., Lin S.Y., Chang Y.J. Cigarette smoking and colorectal cancer: from epidemiology to bench. J Exp Clin Med 2011, 3:257-261.
21. Lai C.S., Pan M.H. Chemopreventive effects of natural dietary compounds on smoking-induced tumorigenesis. J Exp Clin Med 2011, 3:262-271.
22. Guo J., Ibaragi S., Zhu T., Luo L.Y., Hu G.F., Huppi P.S., Chen C.Y. Nicotine promotes mammary tumor migration via a signaling cascade involving protein kinase C and CDC42. Cancer Res 2008, 68(20):8473-8481.
23. Shin V.Y., Wu W.K., Chu K.M., Wong H.P., Lam E.K., Tai E.K., Koo M.W., et al. Nicotine induces cyclooxygenase-2 and vascular endothelial growth factor receptor-2 in association with tumor-associated invasion and angiogenesis in gastric cancer. Mol Cancer Res 2005, 3(11):607-615.
24. Zeidler R., Albermann K., Lang S. Nicotine and apoptosis. Apoptosis 2007, 12(11):1927-1943.
25. Grozio A., Catassi A., Cavalieri Z., Paleari L., Cesario A., Russo P. Nicotine, lung and cancer. Anticancer Agents Med Chem 2007, 7(4):461-466.
26. Brejc K., van Dijk W.J., Klaassen R.V., Schuurmans M., van Der Oost J., Smit A.B., Sixma T.K. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 2001, 411(6835):269-276.
27. Avramopoulou V., Mamalaki A., Tzartos S.J. 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 2004, 279(37):38287-38293.
28. Grando S.A. Basic and clinical aspects of non-neuronal acetylcholine: biological and clinical significance of non-canonical ligands of epithelial nicotinic acetylcholine receptors. J Pharmacol Sci 2008, 106(2):174-179.
29. Wei P.L., Chang Y.J., Ho Y.S., Lee C.H., Yang Y.Y., An J., Lin S.Y. Tobacco-specific carcinogen enhances colon cancer cell migration through alpha7-nicotinic acetylcholine receptor. Ann Surg 2009, 249(6):978-985.
30. Lien Y.C., Wang W., Kuo L.J., Liu J.J., Wei P.L., Ho Y.S., Ting W.C., et al. Nicotine promotes cell mgration through alpha7 nicotinic acetylcholine receptor in gastric cancer cells. Ann Surg Oncol 2011, 18(9):2671-2679.
31. Shih Y.L., Liu H.C., Chen C.S., Hsu C.H., Pan M.H., Chang H.W., Chang C.H., et al. Combination treatment with luteolin and quercetin enhances antiproliferative effects in nicotine-treated MDA-MB-231 cells by down-regulating nicotinic acetylcholine receptors. J Agric Food Chem 2010, 58(1):235-241.
32. Lee C.H., Chang Y.C., Chen C.S., Tu S.H., Wang Y.J., Chen L.C., Chang Y.J., et al. Crosstalk between nicotine and estrogen-induced estrogen receptor activation induces alpha9-nicotinic acetylcholine receptor expression in human breast cancer cells. Breast Cancer Res Treat 2010, 129(2):331-345.
33. Chiou J.F., Tai C.J., Huang M.T., Wei P.L., Wang Y.H., An J., Wu C.H., et al. Glucose-regulated protein 78 is a novel contributor to acquisition of resistance to sorafenib in hepatocellular carcinoma. Ann Surg Oncol 2010, 17(2):603-612.
34. Chang Y.J., Chiu C.C., Wu C.H., An J., Wu C.C., Liu T.Z., Wei P.L., et al. Glucose-regulated protein 78 (GRP78) silencing enhances cell migration but does not influence cell proliferation in hepatocellular carcinoma. Ann Surg Oncol 2010, 17(6):1703-1709.
35. Tai C.J., Chin-Sheng H., Kuo L.J., Wei P.L., Lu H.H., Chen H.A., Liu T.Z., et al. Survivin-mediated cancer cell migration through GRP78 and epithelial-mesenchymal transition (EMT) marker expression in Mahlavu cells. Ann Surg Oncol 2011 Apr 23, [Epub ahead of print].
36. Chang Y.J., Tai C.J., Kuo L.J., Wei P.L., Liang H.H., Liu T.Z., Wang W., et al. Glucose-regulated protein 78 (GRP78) mediated the efficacy to curcumin treatment on hepatocellular carcinoma. Ann Surg Oncol 2011, 18(8):2395-2403.
37. Dong D., Ni M., Li J., Xiong S., Ye W., Virrey J.J., Mao C., et al. Critical role of the stress chaperone GRP78/BiP in tumor proliferation, survival, and tumor angiogenesis in transgene-induced mammary tumor development. Cancer Res 2008, 68(2):498-505.
38. Sowinski S., Jolly C., Berninghausen O., Purbhoo M.A., Chauveau A., Kohler K., Oddos S., et al. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat Cell Biol 2008, 10(2):211-219.
39. Wang S.K., Liang P.H., Astronomo R.D., Hsu T.L., Hsieh S.L., Burton D.R., Wong C.H. Targeting the carbohydrates on HIV-1: Interaction of oligomannose dendrons with human monoclonal antibody 2G12 and DC-SIGN. Proc Natl Acad Sci U S A 2008, 105(10):3690-3695.
40. Wei P.L., Kuo L.J., Huang M.T., Ting W.C., Ho Y.S., Wang W., An J., et al. Nicotine enhances colon cancer cell migration by induction of fibronectin. Ann Surg Oncol 2011, 18(6):1782-1790.
41. Huang M.T., Wei P.L., Liu J.J., Liu D.Z., Huey-Chun H., An J., Wu C.C., et al. Knockdown of thrombomodulin enhances HCC cell migration through increase of ZEB1 and decrease of E-cadherin gene expression. Ann Surg Oncol 2010, 17(12):3379-3385.
42. Chen R.J., Ho Y.S., Guo H.R., Wang Y.J. Long-term nicotine exposure-induced chemoresistance is mediated by activation of Stat3 and downregulation of ERK1/2 via nAChR and beta-adrenoceptors in human bladder cancer cells. Toxicol Sci 2010, 115(1):118-130.
43. Davis R., Rizwani W., Banerjee S., Kovacs M., Haura E., Coppola D., Chellappan S. Nicotine promotes tumor growth and metastasis in mouse models of lung cancer. PLoS One 2009, 4(10):e7524.
44. Lin C.H., Chen Y.C., Chiang C.J., Lu Y.S., Kuo K.T., Huang C.S., Cheng W.F., et al. The emerging epidemic of estrogen-related cancers in young women in a developing Asian country. Int J Cancer 2011 Jun 23, [Epub ahead of print].
45. Tu S.H., Ku C.Y., Ho C.T., Chen C.S., Huang C.S., Lee C.H., Chen L.C., et al. Tea polyphenol (-)-epigallocatechin-3-gallate inhibits nicotine- and estrogen-induced alpha9-nicotinic acetylcholine receptor upregulation in human breast cancer cells. Mol Nutr Food Res 2011, 55(3):455-466.
46. Chen C.S., Lee C.H., Hsieh C.D., Ho C.T., Pan M.H., Huang C.S., Tu S.H., et al. Nicotine-induced human breast cancer cell proliferation attenuated by garcinol through down-regulation of the nicotinic receptor and cyclin D3 proteins. Breast Cancer Res Treat 2011, 125(1):73-87.