Lung Cancer
Volume 69, Issue 1 , Pages 33-39 , July 2010

Chronic exposure to estrogen and the tobacco carcinogen NNK cooperatively modulates nicotinic receptors in small airway epithelial cells

  • Hussein A.N. Al-Wadei

      Affiliations

    • Experimental Oncology Laboratory, University of Tennessee, Knoxville, TN, USA
    • Department of Preventive Medicine, Sana’a University, Sana’a, Yemen
    • Department of Pathobiology, College of Veterinary Medicine, University of Tennessee, Knoxville, TN, USA
  • ,
  • Mohammed H. Al-Wadei

      Affiliations

    • Experimental Oncology Laboratory, University of Tennessee, Knoxville, TN, USA
    • Department of Pathobiology, College of Veterinary Medicine, University of Tennessee, Knoxville, TN, USA
  • ,
  • Thomas Masi

      Affiliations

    • Department of Microbiology, College of Arts and Sciences, University of Tennessee, Knoxville, TN, USA
  • ,
  • Hildegard M. Schuller

      Affiliations

    • Experimental Oncology Laboratory, University of Tennessee, Knoxville, TN, USA
    • Department of Pathobiology, College of Veterinary Medicine, University of Tennessee, Knoxville, TN, USA
    • Corresponding Author InformationCorresponding author at: Department of Pathobiology, College of Veterinary Medicine, University of Tennessee, 2407 River Drive, Knoxville, TN 37996, USA. Tel.: +1 865 974 8217; fax: +1 865 974 5616.

Received 18 May 2009 ,Revised 23 September 2009 ,Accepted 26 September 2009.

References 

  1. Devesa SS, Bray F, Vizcaino AP, Parkin DM. International lung cancer trends by histologic type: male:female differences diminishing and adenocarcinoma rates rising. Int J Cancer. 2005;117:294–299
  2. Harris RE, Zang EA, Anderson JI, Wynder EL. Race and sex differences in lung cancer risk associated with cigarette smoking. Int J Epidemiol. 1993;22:592–595
  3. Garber ME, Troyanskaya OG, Schluens K, Petersen S, Thaesler Z, Pacyna-Gengelbach M, et al. Diversity of gene expression in adenocarcinoma of the lung. Proc Natl Acad Sci USA. 2001;98:13784–13789
  4. Schuller HM, Witschi HP, Nylen E, Joshi PA, Correa E, Becker KL. Pathobiology of lung tumors induced in hamsters by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone and the modulating effect of hyperoxia. Cancer Res. 1990;50:1960–1965
  5. Schuller HM. Is cancer triggered by altered signalling of nicotinic acetylcholine receptors?. Nat Rev Cancer. 2009;9:195–205
  6. Schuller HM, Orloff M. Tobacco-specific carcinogenic nitrosamines. Ligands for nicotinic acetylcholine receptors in human lung cancer cells. Biochem Pharmacol. 1998;55:1377–1384
  7. Arredondo J, Chernyavsky AI, Grando SA. Nicotinic receptors mediate tumorigenic action of tobacco-derived nitrosamines on immortalized oral epithelial cells. Cancer Biol Ther. 2006;5:511–517
  8. Schuller HM, Tithof PK, Williams M, Plummer H. The tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone is a beta-adrenergic agonist and stimulates DNA synthesis in lung adenocarcinoma via beta-adrenergic receptor-mediated release of arachidonic acid. Cancer Res. 1999;59:4510–4515
  9. Laag E, Majidi M, Cekanova C, Masi T, Takahashi T, Schuller HM. NNK activates ERK1/2 and CREB/ATF-1 via beta-1-AR and EGFR signaling in human lung adenocarcinoma and small airway epithelial cells. Int J Cancer. 2006;119:1547–1552
  10. Majidi M, Al-Wadei HA, Takahashi T, Schuller HM. Nongenomic beta estrogen receptors enhance beta1 adrenergic signaling induced by the nicotine-derived carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in human small airway epithelial cells. Cancer Res. 2007;67:6863–6871
  11. West KA, Brognard J, Clark AS, Linnoila IR, Yang X, Swain SM, et al. Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells. J Clin Invest. 2003;111:81–90
  12. Lam DC, Girard L, Ramirez R, Chau WS, Suen WS, Sheridan S, et al. Expression of nicotinic acetylcholine receptor subunit genes in non-small-cell lung cancer reveals differences between smokers and nonsmokers. Cancer Res. 2007;67:4638–4647
  13. Markou A. Review. Neurobiology of nicotine dependence. Philos Trans R Soc Lond B: Biol Sci. 2008;
  14. Harkness PC, Millar NS. Changes in conformational and subcellular distribution of alpha4beta2 nicotinic actylcholine receptors revealed by chronic nicotine treatment and expression of subunit chimeras. J Neurosci. 2002;22:10172–10181
  15. Lindstrom J, Anand R, Gerzanich V, Peng X, Wang F, Wells G. Structure and function of neuronal nicotinic acetylcholine receptors. Prog Brain Res. 1996;109:125–137
  16. Schuller HM, Al-Wadei HA, Majidi M. Gamma-aminobutyric acid, a potential tumor suppressor for small airway-derived lung adenocarcinoma. Carcinogenesis. 2008;
  17. Schuller HM, Al-Wadei HA, Majidi M. GABA(B) receptor is a novel drug target for pancreatic cancer. Cancer. 2008;112:767–778
  18. Joseph J, Niggemann B, Zaenker KS, Entschladen F. The neurotransmitter gamma-aminobutyric acid is an inhibitory regulator for the migration of SW 480 colon carcinoma cells. Cancer Res. 2002;62:6467–6469
  19. Palm D, Lang K, Niggemann B, Drell TLt, Masur K, Zaenker KS, et al. The norepinephrine-driven metastasis development of PC-3 human prostate cancer cells in BALB/c nude mice is inhibited by beta-blockers. Int J Cancer. 2006;118:2744–2749
  20. Drell TLt, Joseph J, Lang K, Niggemann B, Zaenker KS, Entschladen F. Effects of neurotransmitters on the chemokinesis and chemotaxis of MDA-MB-468 human breast carcinoma cells. Breast Cancer Res Treat. 2003;80:63–70
  21. Shin VY, Wu WK, Chu KM, Koo MW, Wong HP, Lam EK, et al. Functional role of beta-adrenergic receptors in the mitogenic action of nicotine on gastric cancer cells. Toxicol Sci. 2007;96:21–29
  22. Yang EV, Sood AK, Chen M, Li Y, Eubank TD, Marsh CB, et al. Norepinephrine up-regulates the expression of vascular endothelial growth factor, matrix metalloproteinase (MMP)-2, and MMP-9 in nasopharyngeal carcinoma tumor cells. Cancer Res. 2006;66:10357–10364
  23. Wong HP, Yu L, Lam EK, Tai EK, Wu WK, Cho CH. Nicotine promotes cell proliferation via alpha7-nicotinic acetylcholine receptor and catecholamine-synthesizing enzymes-mediated pathway in human colon adenocarcinoma HT-29 cells. Toxicol Appl Pharmacol. 2007;221:261–267
  24. Barik J, Wonnacott S. Indirect modulation by alpha7 nicotinic acetylcholine receptors of noradrenaline release in rat hippocampal slices: interaction with glutamate and GABA systems and effect of nicotine withdrawal. Mol Pharmacol. 2006;69:618–628
  25. Haass M, Kubler W. Nicotine and sympathetic neurotransmission. Cardiovasc Drugs Ther. 1997;19:657–665
  26. Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ. Two genes encode distinct glutamate decarboxylases. Neuron. 1991;7:91–100
  27. Al-Wadei HAN, Majidi M, Schuller HM. COPD-associated modulation of the alpha7 nicotinic acetylcholine receptor in SCLC. In: American Association for Cancer Research annual meeting. San Diego: AACR; 2008;
  28. Al-Wadei HA, Schuller HM. beta-Carotene promotes the development of NNK-induced small airway-derived lung adenocarcinoma. Eur J Cancer. 2009;45:1257–1264
  29. Wallukat G. The beta-adrenergic receptors. Herz. 2002;27:683–690
  30. Hirano T, Watanabe D, Kawaguchi SY, Pastan I, Nakanishi S. Roles of inhibitory interneurons in the cerebellar cortex. Ann NY Acad Sci. 2002;978:405–412
  31. Wonnacott S, Barik J, Dickinson J, Jones IW. Nicotinic receptors modulate transmitter cross talk in the CNS: nicotinic modulation of transmitters. J Mol Neurosci. 2006;30:137–140
  32. Schuller HM, Porter B, Riechert A, Walker K, Schmoyer R. Neuroendocrine lung carcinogenesis in hamsters is inhibited by green tea or theophylline while the development of adenocarcinomas is promoted: implications for chemoprevention in smokers. Lung Cancer. 2004;45:11–18
  33. Schuller HM, Porter B, Riechert A. Beta-adrenergic modulation of NNK-induced lung carcinogenesis in hamsters. J Cancer Res Clin Oncol. 2000;126:624–630
  34. Centeno ML, Henderson JA, Pau KY, Bethea CL. Estradiol increases alpha7 nicotinic receptor in serotonergic dorsal raphe and noradrenergic locus coeruleus neurons of macaques. J Comp Neurol. 2006;497:489–501
  35. Marks MJ, Pauly JR, Gross SD, Deneris ES, Hermans-Borgmeyer I, Heinemann SF, et al. Nicotine binding and nicotine receptor subunit RNA after chronic nicotine treatment. J Neurosci. 1992;12:2765–2784
  36. Xu Q, Hamada T, Kiyama R, Sakuma Y, Wada-Kiyama Y. Site-specific regulation of gene expression by estrogen in the hypothalamus of adult female rats. Neurosci Lett. 2008;436:35–39
  37. Curtis L, Buisson B, Bertrand S, Bertrand D. Potentiation of human alpha4beta2 neuronal nicotinic acetylcholine receptor by estradiol. Mol Pharmacol. 2002;61:127–135
  38. Nakazawa K, Ohno Y. Block by phytoestrogens of recombinant human neuronal nicotinic receptors. J Pharmacol Sci. 2003;93:118–121

PII: S0169-5002(09)00495-4

doi: 10.1016/j.lungcan.2009.09.011

Lung Cancer
Volume 69, Issue 1 , Pages 33-39 , July 2010