Tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK) induces cell proliferation in normal human bronchial epithelial cells through NFκB activation and cyclin D1 up-regulation

Toxicology and Applied Pharmacology

Volumn 205, Issue 2, 2005, Pages 133-148

  Ho, Yuan Soon ^a   Chen, Chien Ho ^a   Wang, Ying Jan ^b   Pestell, Richard G ^c   Albanese, Chris ^c   Chen, Rong Jane ^b   Chang, Mei Chi ^d   Jeng, Jiiang Huei ^e   Lin, Shyr Yi ^f   Liang, Yu Chih ^a   Tseng, How ^a   Lee, Wen Sen ^a   Lin, Jen Kun ^e   Chu, Jan Show ^f   Chen, Li Ching ^g   Lee, Chia Hwa ^a   Tso, Wei Ling ^a   Lai, Yann Chwen ^a   Wu, Chih Hsiung ^f  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d CHANG GUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^e NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^f TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^g TZU CHI UNIVERSITY   (Taiwan)

Author keywords

Cyclin D1; Lung cancer; NF B; Nicotine; NNK

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; CARCINOGEN; CHOLINERGIC RECEPTOR; CYCLIN D1; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; SERINE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRONCHUS MUCOSA; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MOUSE; NONHUMAN; NORMAL HUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; UPREGULATION;

BRONCHI; CARCINOGENS; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN D1; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; HUMANS; LUNG NEOPLASMS; MITOGEN-ACTIVATED PROTEIN KINASE 3; NF-KAPPA B; NITROSAMINES; PHOSPHORYLATION; RECEPTORS, NICOTINIC; RETINOBLASTOMA PROTEIN; UP-REGULATION;

NICOTIANA TABACUM;

EID: 21044454180     PISSN: 0041008X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.taap.2004.09.019     Document Type: Article

References (79)

1. N. Agopyan, T. Bhatti, S. Yu, and S.A. Simon Vanilloid receptor activation by 2- and 10-micron particles induces responses leading to apoptosis in human airway epithelial cells Toxicol. Appl. Pharmacol. 192 2003 21 35
2. C. Albanese, M. D'Amico, A.T. Reutens, M. Fu, G. Watanabe, R.J. Lee, R.N. Kitsis, B. Henglein, M. Avantaggiati, K. Somasundaram, B. Thimmapaya, and R.G. Pestell Activation of the cyclin D1 gene by the E1A-associated protein p300 through AP-1 inhibits cellular apoptosis J. Biol. Chem. 274 1999 34186 34195
3. C. Albanese, K. Wu, M. D'Amico, C. Jarrett, D. Joyce, J. Hughes, J. Hulit, T. Sakamaki, M. Fu, A. Ben-Ze'ev, J.F. Bromberg, C. Lamberti, U. Verma, R.B. Gaynor, S.W. Byers, and R.G. Pestell IKKalpha regulates mitogenic signaling through transcriptional induction of cyclin D1 via Tcf Mol. Biol. Cell 14 2003 585 599
4. A.L. Allan, C. Albanese, R.G. Pestell, and J. LaMarre Activating transcription factor 3 induces DNA synthesis and expression of cyclin D1 in hepatocytes J. Biol. Chem. 276 2001 27272 27280
5. R.J. Anto, A. Mukhopadhyay, S. Shishodia, C.G. Gairola, and B.B. Aggarwal Cigarette smoke condensate activates nuclear transcription factor-kappaB through phosphorylation and degradation of IkappaB(alpha): correlation with induction of cyclooxygenase-2 Carcinogenesis 23 2002 1511 1518
6. A.K. Armitage, C.T. Dollery, C.F. George, T.H. Houseman, P.J. Lewis, and D.M. Turner Absorption and metabolism of nicotine from cigarettes Br. Med. J. 4 1975 313 316
7. J. Arredondo, V.T. Nguyen, A.I. Chernyavsky, D.L. Jolkovsky, K.E. Pinkerton, and S.A. Grando A receptor-mediated mechanism of nicotine toxicity in oral keratinocytes Lab. Invest. 81 2001 1653 1668
8. J. Arredondo, V.T. Nguyen, A.I. Chernyavsky, D. Bercovich, A. Orr-Urtreger, W. Kummer, K. Lips, D.E. Vetter, and S.A. Grando Central role of alpha7 nicotinic receptor in differentiation of the stratified squamous epithelium J. Cell Biol. 159 2002 325 336
9. J. Arredondo, L.L. Hall, A. Ndoye, V.T. Nguyen, A.I. Chernyavsky, D. Bercovich, A. Orr-Urtreger, A.L. Beaudet, and S.A. Grando Central role of fibroblast alpha3 nicotinic acetylcholine receptor in mediating cutaneous effects of nicotine Lab. Invest. 83 2003 207 225
10. N.L. Benowitz Clinical pharmacology of nicotine Annu. Rev. Med. 37 1986 21 32
11. N.L. Benowitz, S.M. Hall, R.I. Herning, P. Jacob III, R.T. Jones, and A.L. Osman Smokers of low-yield cigarettes do not consume less nicotine N. Engl. J. Med. 309 1983 139 142
12. N.L. Benowitz, P. Jacob III, L.T. Kozlowski, and L. Yu Influence of smoking fewer cigarettes on exposure to tar, nicotine, and carbon monoxide N. Engl. J. Med. 315 1986 1310 1313
13. N.L. Benowitz, P. Jacob III, L. Yu, R. Talcott, S. Hall, and R.T. Jones Reduced tar, nicotine, and carbon monoxide exposure while smoking ultralow- but not low-yield cigarettes JAMA 256 1986 241 246
14. N.L. Benowitz, S. Zevin, and P. Jacob III Suppression of nicotine intake during ad libitum cigarette smoking by high-dose transdermal nicotine J. Pharmacol. Exp. Ther. 287 1998 958 962
15. S. Benzeno, G. Narla, J. Allina, G.Z. Cheng, H.L. Reeves, M.S. Banck, J.A. Odin, J.A. Diehl, D. Germain, and S.L. Friedman Cyclin-dependent kinase inhibition by the KLF6 tumor suppressor protein through interaction with cyclin D1 Cancer Res. 64 2004 3885 3891
16. J.O. Boyle, J. Langenfeld, F. Lonardo, D. Sekula, P. Reczek, V. Rusch, M.I. Dawson, and E. Dmitrovsky Cyclin D1 proteolysis: a retinoid chemoprevention signal in normal, immortalized, and transformed human bronchial epithelial cells J. Natl. Cancer Inst. 91 1999 373 379
17. K.D. Brunnemann, and D. Hoffmann Analytical studies on tobacco-specific N-nitrosamines in tobacco and tobacco smoke Crit. Rev. Toxicol. 21 1991 235 240
18. A. Castonguay, P. Pepin, and G.D. Stoner Lung tumorigenicity of NNK given orally to A/J mice: its application to chemopreventive efficacy studies Exp. Lung Res. 17 1991 485 499
19. L.G. Cavin, R. Romieu-Mourez, G.R. Panta, J. Sun, V.M. Factor, S.S. Thorgeirsson, G.E. Sonenshein, and M. Arsura Inhibition of CK2 activity by TGF-beta1 promotes IkappaB-alpha protein stabilization and apoptosis of immortalized hepatocytes Hepatology 38 2003 1540 1551
20. L.E. Chavez-Noriega, A. Gillespie, K.A. Stauderman, J.H. Crona, B.O. Claeps, K.J. Elliott, R.T. Reid, T.S. Rao, G. Velicelebi, M.M. Harpold, E.C. Johnson, and J. Corey-Naeve Characterization of the recombinant human neuronal nicotinic acetylcholine receptors alpha3beta2 and alpha4beta2 stably expressed in HEK293 cells Neuropharmacology 39 2000 2543 2560
21. F.A. Dajas-Bailador, L. Soliakov, and S. Wonnacott 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 2002 520 530
22. M. de Andrade, J.O. Ebbert, J.A. Wampfler, D.L. Miller, R.S. Marks, G.A. Croghan, A. Jatoi, E.E. Finke, T.A. Sellers, and P. Yang Environmental tobacco smoke exposure in women with lung cancer Lung Cancer 43 2004 127 134
23. R.V. Ebert, M.E. McNabb, K.T. McCusker, and S.L. Snow Amount of nicotine and carbon monoxide inhaled by smokers of low-tar, low-nicotine cigarettes JAMA 250 1983 2840 2842
24. V. Gajalakshmi, R.J. Hung, A. Mathew, C. Varghese, P. Brennan, and P. Boffetta Tobacco smoking and chewing, alcohol drinking and lung cancer risk among men in southern India Int. J. Cancer 107 2003 441 447
25. M.N. Garnovskaya, Y.V. Mukhin, T.M. Vlasova, J.S. Grewal, M.E. Ullian, B.G. Tholanikunnel, and J.R. Raymond Mitogen-induced rapid phosphorylation of serine 795 of the retinoblastoma gene product in vascular smooth muscle cells involves ERK activation J. Biol. Chem. 279 2004 24899 24905
26. R.H. Grafstrom, W. Pan, and R.H. Hoess Defining the substrate specificity of cdk4 kinase-cyclin D1 complex Carcinogenesis 20 1999 193 198
27. D.C. Guttridge, C. Albanese, J.Y. Reuther, R.G. Pestell, and A.S. Baldwin Jr. NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1 Mol. Cell. Biol. 19 1999 5785 5799
28. S.S. Hecht Biochemistry, biology, and carcinogenicity of tobacco-specific N-nitrosamines Chem. Res. Toxicol. 11 1998 559 603
29. S.S. Hecht Tobacco smoke carcinogens and lung cancer J. Natl. Cancer Inst. 91 1999 1194 1210
30. S.S. Hecht Cigarette smoking and lung cancer: chemical mechanisms and approaches to prevention Lancet Oncol. 3 2002 461 469
31. C. Heeschen, M. Weis, A. Aicher, S. Dimmeler, and J.P. Cooke A novel angiogenic pathway mediated by non-neuronal nicotinic acetylcholine receptors J. Clin. Invest. 110 2002 527 536
32. T. Hideshima, T. Hayashi, D. Chauhan, M. Akiyama, P. Richardson, and K. Anderson Biologic sequelae of c-Jun NH(2)-terminal kinase (JNK) activation in multiple myeloma cell lines Oncogene 22 2003 8797 8801
33. D. Hoffmann, and I. Hoffmann The changing cigarette, 1950-1995 J. Toxicol. Environ. Health 50 1997 307 364
34. Y. Hosokawa, and A. Arnold Mechanism of cyclin D1 (CCND1, PRAD1) overexpression in human cancer cells: analysis of allele-specific expression Genes Chromosomes Cancer 22 1998 66 71
35. Q.J. Hu, N. Dyson, and E. Harlow The regions of the retinoblastoma protein needed for binding to adenovirus E1A or SV40 large T antigen are common sites for mutations EMBO J. 9 1990 1147 1155
36. H. Huang, S.B. Petkova, A.W. Cohen, B. Bouzahzah, J. Chan, J.N. Zhou, S.M. Factor, L.M. Weiss, M. Krishnamachary, S. Mukherjee, M. Wittner, R.N. Kitsis, R.G. Pestell, M.P. Lisanti, C. Albanese, and H.B. Tanowitz Activation of transcription factors AP-1 and NF-kappa B in murine Chagasic myocarditis Infect. Immun. 71 2003 2859 2867
37. M. Katabami, H. Dosaka-Akita, T. Mishina, K. Honma, K. Kimura, Y. Uchida, K. Morikawa, H. Mikami, S. Fukuda, Y. Inuyama, Y. Ohsaki, and Y. Kawakami Frequent cyclin D1 expression in chromate-induced lung cancers Hum. Pathol. 31 2000 973 979
38. W.S. Lee, M.K. Jain, B.M. Arkonac, D. Zhang, S.Y. Shaw, S. Kashiki, K. Maemura, S.L. Lee, N.K. Hollenberg, M.E. Lee, and E. Haber Thy-1, a novel marker for angiogenesis upregulated by inflammatory cytokines Circ. Res. 82 1998 845 851
39. R.J. Lee, C. Albanese, M. Fu, M. D'Amico, B. Lin, G. Watanabe, G.K. Haines III, P.M. Siegel, M.C. Hung, Y. Yarden, J.M. Horowitz, W.J. Muller, and R.G. Pestell Cyclin D1 is required for transformation by activated Neu and is induced through an E2F-dependent signaling pathway Mol. Cell. Biol. 20 2000 672 683
40. W.S. Lee, R.J. Chen, Y.J. Wang, H. Tseng, J.H. Jeng, S.Y. Lin, Y.C. Liang, C.H. Chen, C.H. Lin, J.K. Lin, P.Y. Ho, J.S. Chu, W.L. Ho, L.C. Chen, and Y.S. Ho In vitro and in vivo studies of the anticancer action of terbinafine in human cancer cell lines: G0/G1 p53-associated cell cycle arrest Int. J. Cancer 106 2003 125 137
41. J.A. Lees, K.J. Buchkovich, D.R. Marshak, C.W. Anderson, and E. Harlow The retinoblastoma protein is phosphorylated on multiple sites by human cdc2 EMBO J. 10 1991 4279 4290
42. B. Leistikow Lung cancer rates as an index of tobacco smoke exposures: validation against black male approximate non-lung cancer death rates, 1969-2000 Prev. Med. 38 2004 511 515
43. G. Lindell, L.O. Farnebo, D. Chen, E. Nexo, J. Rask Madsen, K. Bukhave, and H. Graffner 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 1993 487 494
44. F. Lonardo, K.H. Dragnev, S.J. Freemantle, Y. Ma, N. Memoli, D. Sekula, E.A. Knauth, J.S. Beebe, and E. Dmitrovsky Evidence for the epidermal growth factor receptor as a target for lung cancer prevention Clin. Cancer Res. 8 2002 54 60
45. S. Majumdar, and B.B. Aggarwal Methotrexate suppresses NF-kappaB activation through inhibition of IkappaBalpha phosphorylation and degradation J. Immunol. 167 2001 2911 2920
46. A.M. Malkinson Molecular comparison of human and mouse pulmonary adenocarcinomas Exp. Lung Res. 24 1998 541 555
47. D.P. Miller, I. De Vivo, D. Neuberg, J.C. Wain, T.J. Lynch, L. Su, and D.C. Christiani Association between self-reported environmental tobacco smoke exposure and lung cancer: modification by GSTP1 polymorphism Int. J. Cancer 104 2003 758 763
48. E.J. Molinari, O. Delbono, M.L. Messi, M. Renganathan, S.P. Arneric, J.P. Sullivan, and M. Gopalakrishnan Up-regulation of human alpha7 nicotinic receptors by chronic treatment with activator and antagonist ligands Eur. J. Pharmacol. 347 1998 131 139
49. P. Pepin, L. Bouchard, P. Nicole, and A. Castonguay Effects of sulindac and oltipraz on the tumorigenicity of 4-(methylnitrosamino)1-(3-pyridyl)-1- butanone in A/J mouse lung Carcinogenesis 13 1992 341 348
50. W.J. Petty, K.H. Dragnev, and E. Dmitrovsky Cyclin D1 as a target for chemoprevention Lung Cancer 41 Suppl. 1 2003 S155 S161
51. D. Ratschiller, J. Heighway, M. Gugger, A. Kappeler, F. Pirnia, R.A. Schmid, M.M. Borner, and D.C. Betticher Cyclin D1 overexpression in bronchial epithelia of patients with lung cancer is associated with smoking and predicts survival J. Clin. Oncol. 21 2003 2085 2093
52. M.A. Russell, M. Jarvis, R. Iyer, and C. Feyerabend Relation of nicotine yield of cigarettes to blood nicotine concentrations in smokers Br. Med. J. 280 1980 972 976
53. H.M. Schuller Cell type specific, receptor-mediated modulation of growth kinetics in human lung cancer cell lines by nicotine and tobacco-related nitrosamines Biochem. Pharmacol. 38 1989 3439 3442
54. C.J. Sherr G1 phase progression: cycling on cue Cell 79 1994 551 555
55. P.G. Shields Molecular epidemiology of smoking and lung cancer Oncogene 21 2002 6870 6876
56. S. Shishodia, P. Potdar, C.G. Gairola, and B.B. Aggarwal Curcumin (diferuloylmethane) down-regulates cigarette smoke-induced NF-kappaB activation through inhibition of IkappaBalpha kinase in human lung epithelial cells: correlation with suppression of COX-2, MMP-9 and cyclin D1 Carcinogenesis 24 2003 1269 1279
57. D.H. Song, B. Rana, J.R. Wolfe, G. Crimmins, C. Choi, C. Albanese, T.C. Wang, R.G. Pestell, and M.M. Wolfe Gastrin induced gastric adenocarcinoma growth is mediated through cyclin D1 Am. J. Physiol.: Gastrointest. Liver Physiol. 285 2003 G217 G222
58. Y. Sugimoto, Y. Iba, R. Kayasuga, Y. Kirino, M. Nishiga, M. Alejandra Hossen, K. Okihara, H. Sugimoto, H. Yamada, and C. Kamei Inhibitory effects of propolis granular APC on 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-induced lung tumorigenesis in A/J mice Cancer Lett. 193 2003 155 159
59. H. Suyama, T. Igishi, H. Sano, S. Matsumoto, Y. Shigeoka, H. Nakanishi, M. Endo, N. Burioka, Y. Hitsuda, and E. Shimizu ERK activation and subsequent RB phosphorylation are important determinants of the sensitivity to paclitaxel in lung adenocarcinoma cells Int. J. Oncol. 24 2004 1499 1504
60. M. Suzui, M. Masuda, J.T. Lim, C. Albanese, R.G. Pestell, and I.B. Weinstein Growth inhibition of human hepatoma cells by acyclic retinoid is associated with induction of p21(CIP1) and inhibition of expression of cyclin D1 Cancer Res. 62 2002 3997 4006
61. T. Takebayashi, H. Higashi, H. Sudo, H. Ozawa, E. Suzuki, O. Shirado, H. Katoh, and M. Hatakeyama NF-kappa B-dependent induction of cyclin D1 by retinoblastoma protein (pRB) family proteins and tumor-derived pRB mutants J. Biol. Chem. 278 2003 14897 14905
62. D. Tang, D. Warburton, S.R. Tannenbaum, P. Skipper, R.M. Santella, G.S. Cereijido, F.G. Crawford, and F.P. Perera Molecular and genetic damage from environmental tobacco smoke in young children Cancer Epidemiol., Biomarkers Prev. 8 1999 427 431
63. J.E. Tonder, and P.H. Olesen Agonists at the alpha4beta2 nicotinic acetylcholine receptors: structure-activity relationships and molecular modelling Curr. Med. Chem. 8 2001 651 674
64. S. Toyooka, R. Maruyama, K.O. Toyooka, D. McLerran, Z. Feng, Y. Fukuyama, A.K. Virmani, S. Zochbauer-Muller, K. Tsukuda, K. Sugio, N. Shimizu, K. Shimizu, H. Lee, C.Y. Chen, K.M. Fong, M. Gilcrease, J.A. Roth, J.D. Minna, and A.F. Gazdar Smoke exposure, histologic type and geography-related differences in the methylation profiles of non-small cell lung cancer Int. J. Cancer 103 2003 153 160
65. P. Upadhyaya, P.M. Kenney, J.B. Hochalter, M. Wang, and S.S. Hecht Tumorigenicity and metabolism of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol enantiomers and metabolites in the A/J mouse Carcinogenesis 20 1999 1577 1582
66. K. Utsugisawa, Y. Nagane, D. Obara, and H. Tohgi Over-expression of alpha7 nicotinic acetylcholine receptor induces sustained ERK phosphorylation and N-cadherin expression in PC12 cells Brain Res., Mol. Brain Res. 106 2002 88 93
67. G.M. Videtic, L.W. Stitt, A.R. Dar, W.I. Kocha, A.T. Tomiak, P.T. Truong, M.D. Vincent, and E.W. Yu Continued cigarette smoking by patients receiving concurrent chemoradiotherapy for limited-stage small-cell lung cancer is associated with decreased survival J. Clin. Oncol. 21 2003 1544 1549
68. M. Volm, and R. Koomagi Association of cyclin D1 expression in lung cancer and the smoking habits of patients Cancer Lett. 141 1999 147 150
69. J.Y. Wang, E.S. Knudsen, and P.J. Welch The retinoblastoma tumor suppressor protein Adv. Cancer Res. 64 1994 25 85
70. N.H. Waseem, and D.P. Lane Monoclonal antibody analysis of the proliferating cell nuclear antigen (PCNA). Structural conservation and the detection of a nucleolar form J. Cell Sci. 96 Pt. 1 1990 121 129
71. P.J. Welch, and J.Y. Wang Disruption of retinoblastoma protein function by coexpression of its C pocket fragment Genes Dev. 9 1995 31 46
72. K.A. West, J. Brognard, A.S. Clark, I.R. Linnoila, X. Yang, S.M. Swain, C. Harris, S. Belinsky, and P.A. Dennis Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells J. Clin. Invest. 111 2003 81 90
73. M.G. Wilkinson, and J.B. Millar Control of the eukaryotic cell cycle by MAP kinase signaling pathways FASEB J. 14 2000 2147 2157
74. E.T. Wong, S.G. Holstad, S.J. Mennerick, S.E. Hong, C.F. Zorumski, and K.E. Isenberg Pharmacological and physiological properties of a putative ganglionic nicotinic receptor, alpha 3 beta 4, expressed in transfected eucaryotic cells Brain Res., Mol. Brain Res. 28 1995 101 109
75. E.L. Wynder, and J.E. Muscat The changing epidemiology of smoking and lung cancer histology Environ. Health Perspect. 103 Suppl. 8 1995 143 148
76. G. Yang, Z.Y. Wang, S. Kim, J. Liao, D.N. Seril, X. Chen, T.J. Smith, and C.S. Yang Characterization of early pulmonary hyperproliferation and tumor progression and their inhibition by black tea in a 4-(methylnitrosamino)-1-(3- pyridyl)-1-butanone-induced lung tumorigenesis model with A/J mice Cancer Res. 57 1997 1889 1894
77. Y.N. Ye, E.S. Liu, V.Y. Shin, W.K. Wu, and C.H. Cho The modulating role of NF-kappaB in the action of alpha7 nAChR and cross-talk between 5-lipoxygenase and cyclooxygenase-2 in colon cancer growth induced by NNK J. Pharmacol. Exp. Ther. 311 2004 123 130
78. D.G. Zaridze, R.D. Safaev, G.A. Belitsky, K.D. Brunnemann, and D. Hoffmann Carcinogenic substances in Soviet tobacco products IARC Sci. 1991 485 488
79. B.P. Zhou, Y. Liao, W. Xia, B. Spohn, M.H. Lee, and M.C. Hung Cytoplasmic localization of p21Cip1/WAF1 by Akt-induced phosphorylation in HER-2/neu-overexpressing cells Nat. Cell Biol. 3 2001 245 252