Cigarette sidestream smoke induces histone H3 phosphorylation via JNK and PI3K/Akt pathways, leading to the expression of proto-oncogenes

Carcinogenesis

Volumn 35, Issue 6, 2014, Pages 1228-1237

  Ibuki, Yuko ^a   Toyooka, Tatsushi ^a   Zhao, Xiaoxu ^a   Yoshida, Ikuma ^a  

^a UNIVERSITY OF SHIZUOKA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE; ATM PROTEIN; ATR PROTEIN; CIGARETTE SMOKE; DNA; FORMALDEHYDE; HISTONE H2AX; HISTONE H3; HYDROQUINONE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; HISTONE; PROTEIN C FOS; PROTEIN C JUN;

ARTICLE; CARCINOGENESIS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA DAMAGE; DNA DAMAGE RESPONSE; GENE EXPRESSION; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; LUNG FIBROBLAST; ONCOGENE C FOS; ONCOGENE C JUN; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION INITIATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASM; PASSIVE SMOKING; PHOSPHORYLATION; PROTO ONCOGENE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CELL LINE, TUMOR; DNA DAMAGE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; PROTO-ONCOGENES; SIGNAL TRANSDUCTION; TOBACCO SMOKE POLLUTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84905405993     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgt492     Document Type: Article

References (49)

1. IARC. (2004) Tobacco smoke and involuntary smoking. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Vol. 83 IARC, Lyon.
2. Subramanian, J. et al. (2007) Lung cancer in never smokers: a review. J. Clin. Oncol., 25, 561-570.
3. Besaratinia, A. et al. (2008) Second-hand smoke and human lung cancer. Lancet Oncol., 9, 657-666.
4. Haussmann, H.J. (2012) Use of hazard indices for a theoretical evaluation of cigarette smoke composition. Chem. Res. Toxicol., 25, 794-810.
5. DeMarini, D.M. (2004) Genotoxicity of tobacco smoke and tobacco smoke condensate: a review. Mutat. Res., 567, 447-474.
6. Husgafvel-Pursiainen, K. (2004) Genotoxicity of environmental tobacco smoke: a review. Mutat. Res., 567, 427-445.
7. Toyooka, T. et al. (2009) Cigarette sidestream smoke induces phosphorylated histone H2AX. Mutat. Res., 676, 34-40.
8. Mills, K.D. et al. (2003) The role of DNA breaks in genomic instability and tumorigenesis. Immunol. Rev., 194, 77-95.
9. Chen, Q.W. et al. (2010) Cigarette smoke extract promotes human vascular smooth muscle cell proliferation and survival through ERK1/2-and NF-κB-dependent pathways. ScientificWorldJournal, 10, 2139-2156.
10. Zhong, C.Y. et al. (2005) MAPK/AP-1 signal pathway in tobacco smokeinduced cell proliferation and squamous metaplasia in the lungs of rats. Carcinogenesis, 26, 2187-2195.
11. Narayan, S. et al. (2004) Cigarette smoke condensate-induced transformation of normal human breast epithelial cells in vitro. Oncogene, 23, 5880-5889.
12. Veljkovic, E. et al. (2011) Chronic exposure to cigarette smoke condensate in vitro induces epithelial to mesenchymal transition-like changes in human bronchial epithelial cells, BEAS-2B. Toxicol. In Vitro, 25, 446-453.
13. Zhao, J. et al. (2007) Identification of multiple MAPK-mediated transcription factors regulated by tobacco smoke in airway epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol., 293, L480-L490.
14. Gensch, E. et al. (2004) Tobacco smoke control of mucin production in lung cells requires oxygen radicals AP-1 and JNK. J. Biol. Chem., 279, 39085-39093.
15. Gonzalez, R. et al. (2009) Cigarette smoke condensate stimulates urokinase production through the generation of reactive oxygen species and activation of the mitogen activated protein kinase pathways in human gingival fibroblasts. J. Periodontal Res., 44, 386-394.
16. Choi, H.S. et al. (2005) Phosphorylation of histone H3 at serine 10 is indispensable for neoplastic cell transformation. Cancer Res., 65, 5818-5827.
17. Kim, H.G. et al. (2008) Mitogen-and stress-activated kinase 1-mediated histone H3 phosphorylation is crucial for cell transformation. Cancer Res., 68, 2538-2547.
18. Strahl, B.D. et al. (2000) The language of covalent histone modifications. Nature, 403, 41-45.
19. Kouzarides, T. (2007) Chromatin modifications and their function. Cell, 128, 693-705.
20. Cerutti, H. et al. (2009) Histone H3 phosphorylation: universal code or lineage specific dialects? Epigenetics, 4, 71-75.
21. Prigent, C. et al. (2003) Phosphorylation of serine 10 in histone H3, what for? J. Cell Sci., 116, 3677-3685.
22. Thomson, S. et al. (2001) Independent dynamic regulation of histone phosphorylation and acetylation during immediate-early gene induction. Mol. Cell, 8, 1231-1241.
23. Drobic, B. et al. (2010) Promoter chromatin remodeling of immediateearly genes is mediated through H3 phosphorylation at either serine 28 or 10 by the MSK1 multi-protein complex. Nucleic Acids Res., 38, 3196-3208.
24. Li, J. et al. (2003) Tumor promoter arsenite stimulates histone H3 phosphoacetylation of proto-oncogenes c-fos and c-jun chromatin in human diploid fibroblasts. J. Biol. Chem., 278, 13183-13191.
25. Ke, Q. et al. (2008) Nickel compounds induce phosphorylation of histone H3 at serine 10 by activating JNK-MAPK pathway. Carcinogenesis, 29, 1276-1281.
26. Keum, Y.S. et al. (2013) UVB-induced COX-2 expression requires histone H3 phosphorylation at Ser10 and Ser28. Oncogene, 32, 444-452.
27. He, Z. et al. (2005) Regulation of ultraviolet B-induced phosphorylation of histone H3 at serine 10 by Fyn kinase. J. Biol. Chem., 280, 2446-2454.
28. Sundar, I.K. et al. (2012) Mitogen-and stress-activated kinase 1 (MSK1) regulates cigarette smoke-induced histone modifications on NF-κBdependent genes. PLoS One, 7, e31378.
29. Yang, S.R. et al. (2008) IKK alpha causes chromatin modification on proinflammatory genes by cigarette smoke in mouse lung. Am. J. Respir. Cell Mol. Biol., 38, 689-698.
30. Cooperation Centre for Scientific Research Relative to Tobacco. (2002) Coresta recommended method No. 54, Determination of nicotine and nicotine-free dry particulate matter in sidestream smoke using a fishtail chimney and a routine analytical/linear smoking machine. 1-24.
31. Cheung, P. et al. (2000) Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol. Cell, 5, 905-915.
32. Winter, S. et al. (2008) 14-3-3 proteins recognize a histone code at histone H3 and are required for transcriptional activation. EMBO J., 27, 88-99.
33. Bonner, W.M. et al. (2008) GammaH2AX and cancer. Nat. Rev. Cancer, 8, 957-967.
34. Mögel, I. et al. (2011) The aromatic volatile organic compounds toluene, benzene and styrene induce COX-2 and prostaglandins in human lung epithelial cells via oxidative stress and p38 MAPK activation. Toxicology, 289, 28-37.
35. Volpi, G. et al. (2011) Cigarette smoke and α, β-unsaturated aldehydes elicit VEGF release through the p38 MAPK pathway in human airway smooth muscle cells and lung fibroblasts. Br. J. Pharmacol., 163, 649-661.
36. Funakoshi-Tago, M. et al. (2003) TRAF6 and C-SRC induce synergistic AP-1 activation via PI3-kinase-AKT-JNK pathway. Eur. J. Biochem., 270, 1257-1268.
37. Cheng, C.Y. et al. (2012) PI3-K/Akt/JNK/NF-κB is essential for MMP-9 expression and outgrowth in human limbal epithelial cells on intact amniotic membrane. Stem Cell Res., 9, 9-23.
38. Shrotriya, S. et al. (2010) Diallyl trisulfide inhibits phorbol ester-induced tumor promotion, activation of AP-1, and expression of COX-2 in mouse skin by blocking JNK and Akt signaling. Cancer Res., 70, 1932-1940.
39. He, Z. et al. (2003) Arsenite-induced phosphorylation of histone H3 at serine 10 is mediated by Akt1, extracellular signal-regulated kinase 2, and p90 ribosomal S6 kinase 2 but not mitogen-and stress-activated protein kinase 1. J. Biol. Chem., 278, 10588-10593.
40. Weber, S.M. et al. (2011) Tobacco-specific carcinogen nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone induces AKT activation in head and neck epithelia. Int. J. Oncol., 39, 1193-1198.
41. Tsurutani, J. et al. (2005) Tobacco components stimulate Akt-dependent proliferation and NFkappaB-dependent survival in lung cancer cells. Carcinogenesis, 26, 1182-1195.
42. Romashkova, J.A. et al. (1999) NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature, 401, 86-90.
43. Yamamoto, Y. et al. (2003) Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature, 423, 655-659.
44. Kim, S.Y. et al. (2011) Cigarette smoke induces Akt protein degradation by the ubiquitin-proteasome system. J. Biol. Chem., 286, 31932-31943.
45. Tannheimer, S.L. et al. (1998) Benzo[a]pyrene-and TCDD-induced alterations in tyrosine phosphorylation and insulin-like growth factor signaling pathways in the MCF-10A human mammary epithelial cell line. Carcinogenesis, 19, 1291-1297.
46. Wichmann, A.E. et al. (2003) Genotoxic methylating agents modulate extracellular signal regulated kinase activity through MEK-dependent, glutathione-, and DNA methylation-independent mechanisms in lung epithelial cells. Chem. Res. Toxicol., 16, 87-94.
47. Ruiz-Ramos, R. et al. (2005) Benzoquinone activates the ERK/MAPK signaling pathway via ROS production in HL-60 cells. Toxicology, 209, 279-287.
48. Lee, Y.J. et al. (2007) Histone H3 phosphorylation at serine 10 and serine 28 is mediated by p38 MAPK in rat hepatocytes exposed to ethanol and acetaldehyde. Eur. J. Pharmacol., 573, 29-38.
49. Liu, F. et al. (2010) Epigenomic alterations and gene expression profiles in respiratory epithelia exposed to cigarette smoke condensate. Oncogene, 29, 3650-3664.