Nicotine induces hypoxia-inducible factor-1α expression in human lung cancer cells via nicotinic acetylcholine receptor-mediated signaling pathways

Clinical Cancer Research

Volumn 13, Issue 16, 2007, Pages 4686-4694

  Zhang, Qunzhou ^a   Tang, Xudong ^a   Zhang, Zuo Feng ^b   Velikina, Rita ^b   Shi, Shihong ^a   Le, Anh D ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NICOTINE; NICOTINIC RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE C; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; CANCER CELL; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE TARGETING; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG NON SMALL CELL CANCER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION; UPREGULATION; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL MOVEMENT; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LUNG NEOPLASMS; NEOPLASM INVASIVENESS; NICOTINE; RECEPTORS, NICOTINIC; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 34548102391     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-06-2898     Document Type: Article

References (50)

1. Brognard J, Clark AS, Dennis PA. Akt/protein kinase B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to chemotherapy and radiation. Cancer Res 2001;61:3986-97.
2. Jemal A, Murray T, Samuals A, Ghfoor A, Ward E, Thunn MJ. Cancer statistics 2003. CA Cancer J Clin 2003;53:5-26.
3. Wu XH, Wang HF, Liu YF, Lu XY, Wang JJ, Li K. Histone adduction with nicotine: a bio-AMS study. Radiocarbon 1997;39:293-7.
4. Maneckjee R, Minna JD. Opioid and nicotine receptors affect growth regulation of human lung cancer cell lines. Proc Natl Acad Sci U S A 1990;87:3294-8.
5. Tsurutani J, Castillo SS, Brognard J, et al. Tobacco components stimulate Akt-dependent proliferation and NF-κB-dependent survival in lung cancer cells. Carcinogenesis 2005;26:1182-95.
6. Shin VY, Wu WKK, Ye YN, et al. Nicotine promotes gastric tumor growth and neovascularization by activating extracellular signal-regulated kinase and cyclooxygenase-2. Carcinogenesis 2004;25:2487-95.
7. Bose C, Zhang HL, Udupa KB, Chowdhury P. Activation of p-ERK1/2 by nicotine in pancreatic tumor cell line AR42J: effects on proliferation and secretion. Am J Physiol Gastrointest Liver Physiol 2005;289:926-34.
8. Onoda N, Nehmi A, Weiner D, Mujumdar S, Christen R, Los G. Nicotine affects the signaling of the death pathway, reducing the response of head and neck cancer cell lines to DNA damage agents. Head Neck 2001;23:860-70.
9. Maneckjee R, Minna JD. Opioids induce while nicotine suppresses apoptosis in human lung cancer cells. Cell Growth Differ 1994;5:1033-40.
10. Zhang T, Lu H, Shang X, et al. Nicotine prevents the apoptosis induced by menadione in human lung cancer cells. Biochem Biophys Res Commun 2006;242:928-34.
11. Dasgupta P, Kinkade R, Joshi B, DeCook C, Haura E, Chellapan S. Nicotine inhibits apoptosis induced by chemotherapeutic drugs by up-regulating XIAP and survivin. Proc Natl Acad Sci USA 2006;103:6332-7.
12. Heusch WL, Maneckjee R. Signaling pathways involved in nicotine regulation of apoptosis of human lung cancer cells. Carcinogenesis 1998;19:551-6.
13. Heeschen C, Jang JJ, Weis M, et al. Nicotine stimulates angiogenesis and tumor growth and atherosclerosis. Nat Med 2001;7:833-9.
14. Shin VY, Wu WKK, Chu KM, et al. Nicotine induces cyclooxygenase-2 and vascular endothelial growth factor receptor-2 in associationwith tumor-associated invasion and angiogenesis in gastric cancer. Mol Cancer Res 2005;3:607-15.
15. Mousa S, Mousa SA. Cellular and molecular mechanisms of nicotine's pro-angiogenesis activity and its potential impact on cancer. J Cell Biochem 2006;97:1370-8.
16. López-Lázaro M. HIF-1: hypoxia-inducible factor or dysoxia-inducible factor? FASEB J 2006;20:828-32.
17. Forsythe JA, Jiang BH, Iyer NV, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor-1. Mol Cell Biol 1996;16:4604-13.
18. Kamura T, Sato S, Iwai K, et al. Activation of HIF-1α ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc Natl Acad Sci U S A 2000;97:10430-5.
19. Zundel W, Schindler C, Haas-Kogan D, et al. Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev 2000;14:391-6.
20. Mazure NM, Chen EY, Laderoute KR, Giaccia AJ. Induction of a vascular endothelial growth factor by hypoxia is modulated by a phosphatidylinositol 3-kinase/Akt signaling pathway in Ha-ras-transformed cells through a hypoxia inducible factor-1 transcriptional element. Blood 1997;90:3322-31.
21. Jiang BH, Agani F, Passaniti A, Semenza GL. V-SRC induces expression of hypoxia-inducible factor 1(HIF) and transcription of genes encoding vascular endothelial growth factor and enolase 1: involvement of HIF in tumor progression. Cancer Res 1997;57:5328-35.
22. Li YM, Zhou BP, Deng J, Pan Y, Hay N, Hung MC. A hypoxia-independent hypoxia-inducible factor-1 activation pathway induced by phosphatidylinositol-3 kinase/Akt in HER2 overexpression cells. Cancer Res 2005;65:3257-63.
23. Stiehl DP, Jelkmann W, Wenger RH, Hellwig-Bürgel T. Normoxic induction of the hypoxia-inducible factor 1α by insulin and interleukin-1β involves the phosphatidylinositol-3-kinase pathway. FEBS Lett 2002;512:157-62.
24. Pagé EL, Robitaille GA, Pouysségur J, Richard DE. Induction of hypoxia-inducible factor-1aby transcriptional and translational mechanisms. J Biol Chem 2002;277:48403-9.
25. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003;3:721-32.
26. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 2003;9:677-84.
27. Zagzag D, Zhong H, Scaizitti JM, et al. Expression of hypoxia-inducible factor 1α in brain tumors: association with angiogenesis, invasion, and progression. Cancer 2000;88:2606-18.
28. Zhong H, Chiles K, Feldser D, et al. Modulation of hypoxia-inducible factor 1α expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res 2000;60:1541-5.
29. Giatromanolak A, Koukourakis MI, Sivridis E, et al. Relation of hypoxia inducible factor1α and 2α in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival. Br J Cancer 2001;85:881-90.
30. Swinson DEB, Jones JL, Cox G, Richardson D, Harris AL, O'Byrne KJ. Hypoxia inducible factor 1ain non small cell lung cancer: relation to growth factor, protease and apoptosis pathways. Int J Cancer 2004;111:43-50.
31. Hirami Y, Aoe M, Tsukuda K, et al. Relation of epidermal growth factor receptor, phosphorylated-Akt, and hypoxia inducible factor 1ain non-small cell lung cancers. Cancer Lett 2004;214:157-64.
32. Phillips RJ, Mestas J, Gharaee-Kermani M, et al. Epidermal growth factor and hypoxia-induced expression of CXC chemokine receptor 4 on non-small cell lung cancer cells is regulated by the phosphatidylinositol 3-kinase/PTEN/AKT/ mammalian target of rapamycin signaling pathway and activation of hypoxia inducible factor 1α. J Biol Chem 2005;280:22473-81.
33. Zhang QZ, Zhang ZF, Rao JY, et al. Treatment with siRNA and oligonucleotides targeted to HIF-1α induced apoptosis in human tongue squamous cell carcinomas. Int J Cancer 2004;111:849-57.
34. Cattaneo MG, D'Atri F, Vicentini LM. Mechanisms of mitogen-activated protein kinase activation by nicotine in small-cell lung carcinoma cells. Biochem J 1997;328:499-503.
35. West KA, Brognard J, Clark AS, et al. Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells. J Clin Invest 2003;111:81-90.
36. Lee HY, Oh SH, Woo JK, et al. Chemopreventive effects of deguelin, a novel Akt inhibitor, on tobaccoinduced lung tumorigenesis. J Natl Caner Inst 2005;97:1695-9.
37. Wang Y, Pereira EF, Maus AD, et al. Human bronchial epithelial and endothelial cells express a7 nicotinic acetylcholine receptors. Mol Pharmacol 2001;60:1201-9.
38. Dasgupta P, Rastogi S, Pillai S, et al. Nicotine induces cell proliferation by β-arrestin-mediated activation of Src and Rb-Raf-1pathways. JClin Invest 2006;116:2208-17.
39. Arredondo J, Chernyavsky AI, Jolkovsky DL, Pinkerton KE, Grando SA. Receptor-mediated tobacco toxicity: cooperation of the Ras/Raf-1/MEK1/ERK and JAK-2/STAT-3 pathways downstream of α7 nicotinic receptor in oral keratinocytes. FASEB J 2006;20:2093-101.
40. Xu LJ, Deng XM. Protein kinase CL promotes nicotine-induced migration and invasion of cancer cells via phosphorylation of μ- and m-calpains. J Biol Chem 2006;281:4457-66.
41. Tanaka H, Yamamoto M, Hashimoto N, et al. Hypoxia-independent overexpression of hypoxia-inducible factor-1α as an early change in mouse hepatocarcinogenesis. Cancer Res 2006;66:11263-70.
42. Liao D, Corle C, Seagroves TN, Johnson RS. Hypoxia-inducible factor-1α is a key regulator of metastasis in a transgenic model of cancer initiation and progression. Cancer Res 2007;67:563-72.
43. Vogelstein B, Kinzler KW. Cancer genes and the pathway they control. Nat Med 2004;10:789-99.
44. Dajas-Bailador F, Wonnacott S. Nicotinic acetylcholine receptors and the regulation of neuronal signaling. Trends Pharmacol Sci 2004;25:317-2446.
45. Carlisle DL, Liu XW, Hopkins TM, et al. Nicotine activates cell-signaling pathways through muscletype and neuronal nicotinic acetylcholine receptors in non-small cell lung cancer cells. Pulm Pharmacol Ther 2006. Epub a head of print.
46. Carlisle DL, Hopkins TM, Gaither-Davis A, et al. Nicotine signals through muscle-type and neuronal nicotinic acetylcholine receptors in both human bronchial epithelial cells and airway fibroblasts. Respir Res 2004;5:27.
47. Lopez MG, Montiel C, Herrero CJ, et al. Unmasking the functions of the chromaffin cell α7 nicotinic receptor by using short pulses of acetylcholine and selective blockers. Proc Natl Acad Sci U S A 1998;95:14184-9.
48. Page's G, Pouysse'gur J. Transcriptional regulation of the vascular endothelial growth factor gene - a concert of activating factors. Cardiovasc Res 2005;65:564-73.
49. Lane D, Gray EA, Mathur RS, Mathur SP. Upregulation of vascular endothelial growth factor-C by nicotine in cervical cancer cell lines. Am J Reprod Immunol 2005;53:15853-60.
50. Krishnamachary B, Berg-Dixon S, Kelly B, et al. Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1. Cancer Res 2003;63:1138-43.