NeuroD1 mediates nicotine-induced migration and invasion via regulation of the nicotinic acetylcholine receptor subunits in a subset of neural and neuroendocrine carcinomas

Molecular Biology of the Cell

Volumn 25, Issue 11, 2014, Pages 1782-1792

  Osborne, Jihan K ^a   Guerra, Marcy L ^a   Gonzales, Joshua X ^a   McMillan, Elizabeth A ^a   Minna, John D ^a,b   Cobb, Melanie H ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROGENIC DIFFERENTIATION FACTOR; NICOTINE; NICOTINIC RECEPTOR; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALCIUM; MITOGEN ACTIVATED PROTEIN KINASE; NERVE PROTEIN; PROTEIN P53; PROTEIN SUBUNIT;

ARTICLE; BRONCHUS MUCOSA; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; LUNG CANCER CELL LINE; LUNG SMALL CELL CANCER; NEUROENDOCRINE TUMOR; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOKING; UNDIFFERENTIATED CARCINOMA; BIOLOGICAL MODEL; BRONCHUS; CARCINOMA; CELL CLONE; CELL DIFFERENTIATION; CELL MOTION; DRUG EFFECTS; EPITHELIUM CELL; LUNG TUMOR; METABOLISM; MUTATION; PATHOLOGY; PROTEIN SUBUNIT; TUMOR CELL LINE; TUMOR INVASION; UPREGULATION;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRONCHI; CALCIUM; CARCINOMA, NEUROENDOCRINE; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL MOVEMENT; CLONE CELLS; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; LUNG NEOPLASMS; MODELS, BIOLOGICAL; MUTATION; NEOPLASM INVASIVENESS; NERVE TISSUE PROTEINS; NICOTINE; PROTEIN SUBUNITS; RECEPTOR, TRKB; RECEPTORS, NICOTINIC; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84901675766     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-06-0316     Document Type: Article

References (77)

1. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW (2009). Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89, 73-120.
2. Alessi DR, Smythe C, Keyse SM (1993). The human CL100 gene encodes a Tyr/Thr-protein phosphatase which potently and specifically inactivates MAP kinase and suppresses its activation by oncogenic ras in Xenopus oocyte extracts. Oncogene 8, 2015-2020. (Pubitemid 23212436)
3. Amos CI et al. (2008). Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1. Nat Genet 40, 616-622. (Pubitemid 351601203)
4. Andrews PW (1984). Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev Biol 103, 285-293.
5. Ball DW, Azzoli CG, Baylin SB, Chi D, Dou S, Donis-Keller H, Cumaraswamy A, Borges M, Nelkin BD (1993). Identification of a human achaete-scute homolog highly expressed in neuroendocrine tumors. Proc Natl Acad Sci USA 90, 5648-5652. (Pubitemid 23176218)
6. Ben-David U, Benvenisty N (2011). The tumorigenicity of human embryonic and induced pluripotent stem cells. Nat Rev Cancer 11, 268-277.
7. Ben-David U, Mayshar Y, Benvenisty N (2011). Large-scale analysis reveals acquisition of lineage-specific chromosomal aberrations in human adult stem cells. Cell Stem Cell 9, 97-102.
8. Carney DN, Bepler G, Gazdar AF (1985a). The serum-free establishment and in vitro growth properties of classic and variant small cell lung cancer cell lines. Recent Results Cancer Research 99, 157-166.
9. Carney DN, Gazdar AF, Bepler G, Guccion JG, Marangos PJ, Moody TW, Zweig MH, Minna JD (1985b). Establishment and identification of small cell lung cancer cell lines having classic and variant features. Cancer Res 45, 2913-2923. (Pubitemid 15232769)
10. Cau E, Gradwohl G, Fode C, Guillemot F (1997). Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors. Development 124, 1611-1621. (Pubitemid 27223176)
11. Chen RJ, Ho YS, Guo HR, Wang YJ (2008). Rapid activation of Stat3 and ERK1/2 by nicotine modulates cell proliferation in human bladder cancer cells. Toxicol Sci 104, 283-293.
12. + stores. J Neurochem 81, 606-614. (Pubitemid 34809339)
13. Dajas-Bailador FA, Soliakov L, Wonnacott S (2002b). Nicotine activates the extracellular signal-regulated kinase 1/2 via the alpha7 nicotinic acetylcholine receptor and protein kinase A, in SH-SY5Y cells and hippocampal neurones. J Neurochem 80, 520-530. (Pubitemid 36383035)
14. Dasgupta P et al. (2009). Nicotine induces cell proliferation, invasion and epithelial-mesenchymal transition in a variety of human cancer cell lines. Int. J Cancer 124, 36-45.
15. Dasgupta P, Chellappan SP (2006). Nicotine-mediated cell proliferation and angiogenesis: new twists to an old story. Cell Cycle 5, 2324-2328. (Pubitemid 44801377)
16. 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, 2208-2217. (Pubitemid 44162330)
17. Dufton C, Marcora E, Chae JH, McCullough J, Eby J, Hausburg M, Stein GH, Khoo S, Cobb MH, Lee JE (2005). Context-dependent regulation of NeuroD activity and protein accumulation. Mol Cell Neurosci 28, 727-736. (Pubitemid 40387887)
18. Fratticci A et al. (2007). Differential expression of neurogenins and NeuroD1 in human pituitary tumours. J Endocrinol 194, 475-484. (Pubitemid 47471216)
19. Gazdar AF, Carney DN, Nau MM, Minna JD (1985). Characterization of variant subclasses of cell lines derived from small cell lung cancer having distinctive biochemical, morphological, and growth properties. Cancer Res 45, 2924-2930. (Pubitemid 15232770)
20. Gerzanich V, Wang F, Kuryatov A, Lindstrom J (1998). alpha 5 Subunit alters desensitization, pharmacology, Ca++ permeability and Ca++ modulation of human neuronal alpha 3 nicotinic receptors. J Pharmacol Exp Ther 286, 311-320. (Pubitemid 28318005)
21. Govindan R et al. (2012). Genomic landscape of non-small cell lung cancer in smokers and never-smokers. Cell 150, 1121-1134.
22. Gu G, Dubauskaite J, Melton DA (2002). Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 129, 2447-2457. (Pubitemid 34863851)
23. Guo J, Ibaragi S, Zhu T, Luo LY, Hu GF, Huppi PS, Chen CY (2008). Nicotine promotes mammary tumor migration via a signaling cascade involving protein kinase C and CDC42. Cancer Res 68, 8473-8481.
24. Hecht SS (1999). Tobacco smoke carcinogens and lung cancer. J Natl Cancer Inst 91, 1194-1210. (Pubitemid 29357186)
25. Huang HP, Liu M, El-Hodiri HM, Chu K, Jamrich M, Tsai MJ (2000). Regulation of the pancreatic islet-specific gene BETA2 (neuroD) by neurogenin 3. Mol Cell Biol 20, 3292-3307. (Pubitemid 30215041)
26. Huang P, Kishida S, Cao D, Murakami-Tonami Y, Mu P, Nakaguro M, Koide N, Takeuchi I, Onishi A, Kadomatsu K (2011). The neuronal differentiation factor NeuroD1 downregulates the neuronal repellent factor Slit2 expression and promotes cell motility and tumor formation of neuroblastoma. Cancer Res 71, 2938-2948.
27. Hukkanen J, Jacob P 3rd, Benowitz NL (2005). Metabolism and disposition kinetics of nicotine. Pharmacol Rev 57, 79-115. (Pubitemid 40283970)
28. Hu Y, Wang T, Stormo GD, Gordon JI (2004). RNA interference of achaete-scute homolog 1 in mouse prostate neuroendocrine cells reveals its gene targets and DNA binding sites. Proc Natl Acad Sci USA 101, 5559-5564. (Pubitemid 38488831)
29. Hung RJ et al. (2008). A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature 452, 633-637. (Pubitemid 351483367)
30. Improgo MR, Schlichting NA, Cortes RY, Zhao-Shea R, Tapper AR, Gardner PD (2010a). ASCL1 regulates the expression of the CHRNA5/A3/B4 lung cancer susceptibility locus. Mol Cancer Res 8, 194-203.
31. Improgo MR, Scofield MD, Tapper AR, Gardner PD (2010b). The nicotinic acetylcholine receptor CHRNA5/A3/B4 gene cluster: dual role in nicotine addiction and lung cancer. Prog Neurobiol 92, 212-226.
32. Ito T, Udaka N, Yazawa T, Okudela K, Hayashi H, Sudo T, Guillemot F, Kageyama R, Kitamura H (2000). Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 127, 3913-3921.
33. Jackman DM, Johnson BE (2005). Small-cell lung cancer. Lancet 366, 1385-1396. (Pubitemid 41443406)
34. Jackson KJ, Marks MJ, Vann RE, Chen X, Gamage TF, Warner JA, Damaj MI (2010). Role of alpha5 nicotinic acetylcholine receptors in pharmacological and behavioral effects of nicotine in mice. J Pharmacol Exp Ther 334, 137-146.
35. Jiang T, Collins BJ, Jin N, Watkins DN, Brock MV, Matsui W, Nelkin BD, Ball DW (2009). Achaete-scute complex homologue 1 regulates tumor-initiating capacity in human small cell lung cancer. Cancer Res 69, 845-854.
36. Jin Z, Gao F, Flagg T, Deng X (2004). Tobacco-specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone promotes functional cooperation of Bcl2 and c-Myc through phosphorylation in regulating cell survival and proliferation. J Biol Chem 279, 40209-40219. (Pubitemid 39258297)
37. Kalamida D, Poulas K, Avramopoulou V, Fostieri E, Lagoumintzis G, Lazaridis K, Sideri A, Zouridakis M, Tzartos SJ (2007). Muscle and neuronal nicotinic acetylcholine receptors. Structure, function and pathogenicity. FEBS J 274, 3799-3845.
38. Khoo S, Griffen SC, Xia Y, Baer RJ, German MS, Cobb MH (2003). Regulation of insulin gene transcription by ERK1 and ERK2 in pancreatic beta cells. J Biol Chem 278, 32969-32977. (Pubitemid 37055741)
39. Lam DC et al. (2007). Expression of nicotinic acetylcholine receptor subunit genes in non-small-cell lung cancer reveals differences between smokers and nonsmokers. Cancer Res 67, 4638-4647. (Pubitemid 46910168)
40. Lawrence MC, McGlynn K, Park BH, Cobb MH (2005). ERK1/2-dependent activation of transcription factors required for acute and chronic effects of glucose on the insulin gene promoter. J Biol Chem 280, 26751-26759. (Pubitemid 41040708)
41. Lee JE, Hollenberg SM, Snider L, Turner DL, Lipnick N, Weintraub H (1995). Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268, 836-844.
42. Li M, He Y, Dubois W, Wu X, Shi J, Huang J (2012). Distinct regulatory mechanisms and functions for p53-activated and p53-repressed DNA damage response genes in embryonic stem cells. Mol Cell 46, 30-42.
43. Linnoila RI (2006). Functional facets of the pulmonary neuroendocrine system. Lab Invest 86, 425-444.
44. Lopez-Carballo G, Moreno L, Masia S, Perez P, Barettino D (2002). Activation of the phosphatidylinositol 3-kinase/Akt signaling pathway by retinoic acid is required for neural differentiation of SH-SY5Y human neuroblastoma cells. J Biol Chem 277, 25297-25304. (Pubitemid 34951839)
45. Magenheim J, Klein AM, Stanger BZ, Ashery-Padan R, Sosa-Pineda B, Gu G, Dor Y (2011). Ngn3(+) endocrine progenitor cells control the fate and morphogenesis of pancreatic ductal epithelium. Dev Biol 359, 26-36.
46. Maier CR, Hollander MC, Hobbs EA, Dogan I, Linnoila RI, Dennis PA (2011). Nicotine does not enhance tumorigenesis in mutant K-ras-driven mouse models of lung cancer. Cancer Prev Res (Phila) 4, 1743-1751.
47. Mavilio F (1993). Regulation of vertebrate homeobox-containing genes by morphogens. Eur J Biochem 212, 273-288. (Pubitemid 23076092)
48. McNay DE, Pelling M, Claxton S, Guillemot F, Ang SL (2006). Mash1 is required for generic and subtype differentiation of hypothalamic neuroendocrine cells. Mol Endocrinol 20, 1623-1632. (Pubitemid 43967569)
49. Menendez S et al. (2012). Increased dosage of tumor suppressors limits the tumorigenicity of iPS cells without affecting their pluripotency. Aging Cell 11, 41-50.
50. Mitsudomi T, Viallet J, Mulshine JL, Linnoila RI, Minna JD, Gazdar AF (1991). Mutations of ras genes distinguish a subset of non-small-cell lung cancer cell lines from small-cell lung cancer cell lines. Oncogene 6, 1353-1362. (Pubitemid 21924231)
51. Neptune ER, Podowski M, Calvi C, Cho JH, Garcia JG, Tuder R, Linnoila RI, Tsai MJ, Dietz HC (2008). Targeted disruption of NeuroD, a proneural basic helix-loop-helix factor, impairs distal lung formation and neuroendocrine morphology in the neonatal lung. J Biol Chem 283, 21160-21169.
52. Osborne JK et al. (2013b). NeuroD1 regulates survival and migration of neuroendocrine lung carcinomas via signaling molecules TrkB and NCAM. Proc Natl Acad Sci USA 110, 6524-6529.
53. Osborne JK, Larsen JE, Gonzales JX, Shames DS, Sato M, Wistuba II, Girard L, Minna JD, Cobb MH (2013a). NeuroD1 regulation of migration accompanies the differential sensitivity of neuroendocrine carcinomas to TrkB inhibition. Oncogenesis 2, e63.
54. Pfeifer GP, Denissenko MF, Olivier M, Tretyakova N, Hecht SS, Hainaut P (2002). Tobacco smoke carcinogens, DNA damage and p53 mutations in smoking-associated cancers. Oncogene 21, 7435-7451. (Pubitemid 35305599)
55. Pillai S, Rizwani W, Li X, Rawal B, Nair S, Schell MJ, Bepler G, Haura E, Coppola D, Chellappan S (2011). ID1 facilitates the growth and metastasis of non-small cell lung cancer in response to nicotinic acetylcholine receptor and epidermal growth factor receptor signaling. Mol Cell Biol 31, 3052-3067.
56. Pleasance ED et al. (2010). A small-cell lung cancer genome with complex signatures of tobacco exposure. Nature 463, 184-190.
57. Przyborski SA, Morton IE, Wood A, Andrews PW (2000). Developmental regulation of neurogenesis in the pluripotent human embryonal carcinoma cell line NTERA-2. Eur J Neurosci 12, 3521-3528.
58. Puliyappadamba VT, Cheriyan VT, Thulasidasan AK, Bava SV, Vinod BS, Prabhu PR, Varghese R, Bevin A, Venugopal S, Anto RJ (2010). Nicotine-induced survival signaling in lung cancer cells is dependent on their p53 status while its down-regulation by curcumin is independent. Mol Cancer 9, 220.
59. Quan AL, Videtic GM, Suh JH (2004). Brain metastases in small cell lung cancer. Oncology 18, 961-972; discussion, 974, 979-980, 987.
60. Ramirez-Latorre J, Yu CR, Qu X, Perin F, Karlin A, Role L (1996). Functional contributions of alpha5 subunit to neuronal acetylcholine receptor channels. Nature 380, 347-351.
61. Ravi RK et al. (1998). Activated Raf-1 causes growth arrest in human small cell lung cancer cells. J Clin Invest 101, 153-159. (Pubitemid 28058914)
62. Rostomily RC, Bermingham-McDonogh O, Berger MS, Tapscott SJ, Reh TA, Olson JM (1997). Expression of neurogenic basic helix-loop-helix genes in primitive neuroectodermal tumors. Cancer Res 57, 3526-3531. (Pubitemid 27355503)
63. Russell MA, Jarvis M, Iyer R, Feyerabend C (1980). Relation of nicotine yield of cigarettes to blood nicotine concentrations in smokers. Br Med J 280, 972-976. (Pubitemid 10071875)
64. Sato M et al. (2006). Multiple oncogenic changes (K-RAS(V12), p53 knockdown, mutant EGFRs, p16 bypass, telomerase) are not sufficient to confer a full malignant phenotype on human bronchial epithelial cells. Cancer Res 66, 2116-2128.
65. Sato M et al. (2013). Human lung epithelial cells progressed to malignancy through specific oncogenic manipulations. Mol Cancer Res 11, 638-650.
66. Sato T, Abe T, Nakamoto N, Tomaru Y, Koshikiya N, Nojima J, Kokabu S, Sakata Y, Kobayashi A, Yoda T (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.
67. Schneider JW, Gao Z, Li S, Farooqi M, Tang TS, Bezprozvanny I, Frantz DE, Hsieh J (2008). Small-molecule activation of neuronal cell fate. Nat Chem Biol 4, 408-410. (Pubitemid 351860552)
68. Serres F, Carney SL (2006). Nicotine regulates SH-SY5Y neuroblastoma cell proliferation through the release of brain-derived neurotrophic factor. Brain Res 1101, 36-42. (Pubitemid 44055925)
69. Sun S, Schiller JH, Spinola M, Minna JD (2007). New molecularly targeted therapies for lung cancer. J Clin Invest 117, 2740-2750. (Pubitemid 47529602)
70. Syder AJ, Karam SM, Mills JC, Ippolito JE, Ansari HR, Farook V, Gordon JI (2004). A transgenic mouse model of metastatic carcinoma involving transdifferentiation of a gastric epithelial lineage progenitor to a neuroendocrine phenotype. Proc Natl Acad Sci USA 101, 4471-4476. (Pubitemid 38437435)
71. Tournier JM et al. (2006). alpha3alpha5beta2-Nicotinic acetylcholine receptor contributes to the wound repair of the respiratory epithelium by modulating intracellular calcium in migrating cells. Am J Pathol 168, 55-68.
72. Tsurutani J, Castillo SS, Brognard J, Granville CA, Zhang C, Gills JJ, Sayyah J, Dennis PA (2005). Tobacco components stimulate Akt-dependent proliferation and NFkappaB-dependent survival in lung cancer cells. Carcinogenesis 26, 1182-1195. (Pubitemid 41417895)
73. van Meerbeeck JP, Fennell DA, De Ruysscher DK (2011). Small-cell lung cancer. Lancet 378, 1741-1755.
74. 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, 81-90. (Pubitemid 36134851)
75. Wong DJ, Liu H, Ridky TW, Cassarino D, Segal E, Chang HY (2008). Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2, 333-344. (Pubitemid 351455242)
76. Xu L, Deng X (2004). Tobacco-specific nitrosamine 4-(methylnitrosamino)- 1-(3-pyridyl)-1-butanone induces phosphorylation of mu- and m-calpain in association with increased secretion, cell migration, and invasion. J Biol Chem 279, 53683-53690. (Pubitemid 40051876)
77. Xu X et al. (2008). Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell 132, 197-207. (Pubitemid 351181232)