Silver Nanoparticle-Induced Phosphorylation of Histone H3 at Serine 10 Involves MAPK Pathways
Abstract
:1. Introduction
2. Materials and Methods
2.1. Preparation of AgNPs
2.2. Cells and Cell Culture Conditions
2.3. Treatment of Cells with AgNPs or Ag Ions
2.4. Western Blot Analysis
3. Results
3.1. Induction of p-H3S10 Formation after Treatment with AgNPs Independent of DNA Damage
3.2. Histone H3S10 Was Phosphorylated via MAPK Pathways
3.3. Release of Ag Ions from AgNPs and MAPK Pathways
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Cury Camargo, P.H.; Satyanarayana, K.G.; Wypych, F. Nanocomposites: Synthesis, Structure, Properties and New Application Opportunities. Mater. Res. 2009, 12, 1–39. [Google Scholar] [CrossRef]
- Nowack, B.; Krug, H.F.; Height, M. 120 Years of Nanosilver History: Implications for Policy Makers. Environ. Sci. Technol. 2011, 45, 1177–1183. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guo, H.; Zhang, J.; Boudreau, M.; Meng, J.; Yin, J.-J.; Liu, J.; Xu, H. Intravenous administration of silver nanoparticles causes organ toxicity through intracellular ROS-related loss of inter-endothelial junction. Part. Fibre Toxicol. 2016, 13. [Google Scholar] [CrossRef] [PubMed]
- Jiang, X.; Foldbjerg, R.; Miclaus, T.; Wang, L.; Singh, R.; Hayashi, Y.; Sutherland, D.; Chen, C.; Autrup, H.; Beer, C. Multi-platform genotoxicity analysis of silver nanoparticles in the model cell line CHO-K1. Toxicol. Lett. 2013, 222, 55–63. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.; Choi, J.E.; Choi, J.; Chung, K.-H.; Park, K.; Yi, J.; Ryu, D.-Y. Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol. In Vitro 2009, 23, 1076–1084. [Google Scholar] [CrossRef]
- Singh, R.P.; Ramarao, P. Cellular uptake, intracellular trafficking and cytotoxicity of silver nanoparticles. Toxicol. Lett. 2012, 213, 249–259. [Google Scholar] [CrossRef]
- Chernousova, S.; Epple, M. Silver as Antibacterial Agent: Ion, Nanoparticle, and Metal. Angew. Chem. Int. Ed. 2013, 52, 1636–1653. [Google Scholar] [CrossRef]
- Chen, X.; Schluesener, H.J. Nanosilver: A nanoproduct in medical application. Toxicol. Lett. 2008, 176, 1–12. [Google Scholar] [CrossRef]
- Simon-Deckers, A.; Gouget, B.; Mayne-L’Hermite, M.; Herlin-Boime, N.; Reynaud, C.; Carriere, M. In vitro investigation of oxide nanoparticle and carbon nanotube toxicity and intracellular accumulation in A549 human pneumocytes. Toxicology 2008, 253, 137–146. [Google Scholar] [CrossRef]
- Cho, J.-G.; Kim, K.-T.; Ryu, T.-K.; Lee, J.-W.; Kim, J.-E.; Kim, J.; Lee, B.-C.; Jo, E.-H.; Yoon, J.; Eom, I.-C.; et al. Stepwise Embryonic Toxicity of Silver Nanoparticles on Oryzias latipes. BioMed Res. Int. 2013. [Google Scholar] [CrossRef]
- Zhao, X.X.; Takabayashi, F.; Ibuki, Y. Coexposure to silver nanoparticles and ultraviolet A synergistically enhances the phosphorylation of histone H2AX. J. Photochem. Photobiol. B Biol. 2016, 162, 213–222. [Google Scholar] [CrossRef] [PubMed]
- Mills, K.D.; Ferguson, D.O.; Alt, F.W. The role of DNA breaks in genomic instability and tumorigenesis. Immunol. Rev. 2003, 194, 77–95. [Google Scholar] [CrossRef] [PubMed]
- Bonner, W.M.; Redon, C.E.; Dickey, J.S.; Nakamura, A.J.; Sedelnikova, O.A.; Solier, S.; Pommier, Y. OPINION gamma H2AX and cancer. Nat. Rev. Cancer 2008, 8, 957–967. [Google Scholar] [CrossRef] [PubMed]
- Mytych, J.; Zebrowski, J.; Lewinska, A.; Wnuk, M. Prolonged Effects of Silver Nanoparticles on p53/p21 Pathway-Mediated Proliferation, DNA Damage Response, and Methylation Parameters in HT22 Hippocampal Neuronal Cells. Mol. Neurobiol. 2017, 54, 1285–1300. [Google Scholar] [CrossRef] [PubMed]
- Zhao, X.X.; Ibuki, Y. Evaluating the Toxicity of Silver Nanoparticles by Detecting Phosphorylation of Histone H3 in Combination with Flow Cytometry Side-Scattered Light. Environ. Sci. Technol. 2015, 49, 5003–5012. [Google Scholar] [CrossRef] [PubMed]
- Hendzel, M.J.; Wei, Y.; Mancini, M.A.; VanHooser, A.; Ranalli, T.; Brinkley, B.R.; BazettJones, D.P.; Allis, C.D. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 1997, 106, 348–360. [Google Scholar] [CrossRef] [PubMed]
- Wei, Y.; Yu, L.L.; Bowen, J.; Gorovsky, M.A.; Allis, C.D. Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 1999, 97, 99–109. [Google Scholar] [CrossRef]
- Choi, H.S.; Choi, B.Y.; Cho, Y.Y.; Mizuno, H.; Kang, B.S.; Bode, A.M.; Dong, Z.G. Phosphorylation of histone H3 at serine 10 is indispensable for neoplastic cell transformation. Cancer Res. 2005, 65, 5818–5827. [Google Scholar] [CrossRef]
- Kim, H.-G.; Lee, K.W.; Cho, Y.-Y.; Kang, N.J.; Oh, S.-M.; Bode, A.M.; Dong, Z. Mitogen- and stress-activated kinase 1-mediated histone H3 phosphorylation is crucial for cell transformation. Cancer Res. 2008, 68, 2538–2547. [Google Scholar] [CrossRef]
- Li, J.; Gorospe, M.; Barnes, J.; Liu, Y. Tumor promoter arsenite stimulates histone H3 phosphoacetylation of proto-oncogenes c-fos and c-jun chromatin in human diploid fibroblasts. J. Biol. Chem. 2003, 278, 13183–13191. [Google Scholar] [CrossRef]
- Ke, Q.; Li, Q.; Ellen, T.P.; Sun, H.; Costa, M. Nickel compounds induce phosphorylation of histone H3 at serine 10 by activating JNK-MAPK pathway. Carcinogenesis 2008, 29, 1276–1281. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Keum, Y.S.; Kim, H.G.; Bode, A.M.; Surh, Y.J.; Dong, Z. UVB-induced COX-2 expression requires histone H3 phosphorylation at Ser10 and Ser28. Oncogene 2013, 32, 444–452. [Google Scholar] [CrossRef] [PubMed]
- Ibuki, Y.; Toyooka, T.; Zhao, X.X.; Yoshida, I. Cigarette sidestream smoke induces histone H3 phosphorylation via JNK and PI3K/Akt pathways, leading to the expression of proto-oncogenes. Carcinogenesis 2014, 35, 1228–1237. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, X.X.; Toyooka, T.; Ibuki, Y. Silver nanoparticle-induced phosphorylation of histone H3 at serine 10 is due to dynamic changes in actin filaments and the activation of Aurora kinases. Toxicol. Lett. 2017, 276, 39–47. [Google Scholar] [CrossRef] [PubMed]
- Toduka, Y.; Toyooka, T.; Ibuki, Y. Flow Cytometric Evaluation of Nanoparticles Using Side-Scattered Light and Reactive Oxygen Species-Mediated Fluorescence-Correlation with Genotoxicity. Environ. Sci. Technol. 2012, 46, 7629–7636. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.J.; Shukla, S.D. 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. 2007, 573, 29–38. [Google Scholar] [CrossRef] [PubMed]
- Liu, F.; Killian, J.K.; Yang, M.; Walker, R.L.; Hong, J.A.; Zhang, M.; Davis, S.; Zhang, Y.; Hussain, M.; Xi, S.; et al. Epigenomic alterations and gene expression profiles in respiratory epithelia exposed to cigarette smoke condensate. Oncogene 2010, 29, 3650–3664. [Google Scholar] [CrossRef] [Green Version]
- Husgafvel-Pursiainen, K. Genotoxicity of environmental tobacco smoke: A review. Mutat. Res. Rev. Mutat. Res. 2004, 567, 427–445. [Google Scholar] [CrossRef]
- Kim, S.-Y.; Lee, J.-H.; Huh, J.W.; Ro, J.Y.; Oh, Y.-M.; Lee, S.-D.; An, S.; Lee, Y.-S. Cigarette Smoke Induces Akt Protein Degradation by the Ubiquitin-Proteasome System. J. Biol. Chem. 2011, 286, 31932–31943. [Google Scholar] [CrossRef] [Green Version]
- Eom, H.J.; Choi, J. p38 MAPK Activation, DNA Damage, Cell Cycle Arrest and Apoptosis as Mechanisms of Toxicity of Silver Nanoparticles in Jurkat T Cells. Environ. Sci. Technol. 2010, 44, 8337–8342. [Google Scholar] [CrossRef]
- Ceulemans, H.; Bollen, M. Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiol. Rev. 2004, 84, 1–39. [Google Scholar] [CrossRef] [PubMed]
- Park, E.-J.; Yi, J.; Kim, Y.; Choi, K.; Park, K. Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol. In Vitro 2010, 24, 872–878. [Google Scholar] [CrossRef] [PubMed]
- Zhao, X.X.; Toyooka, T.; Ibuki, Y. Synergistic bactericidal effect by combined exposure to Ag nanoparticles and UVA. Sci. Total Environ. 2013, 458, 54–62. [Google Scholar] [CrossRef] [PubMed]
- Lok, C.N.; Ho, C.M.; Chen, R.; He, Q.Y.; Yu, W.Y.; Sun, H.; Tam, P.K.H.; Chiu, J.F.; Che, C.M. Silver nanoparticles: Partial oxidation and antibacterial activities. J. Biol. Inorg. Chem. 2007, 12, 527–534. [Google Scholar] [CrossRef] [PubMed]
- Murugan, K.; Choonara, Y.E.; Kumar, P.; Bijukumar, D.; du Toit, L.C.; Pillay, V. Parameters and characteristics governing cellular internalization and trans-barrier trafficking of nanostructures. Int. J. Nanomed. 2015, 10, 2191–2206. [Google Scholar] [CrossRef] [Green Version]
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Zhao, X.; Rao, Y.; Liang, J.; Lin, S.; Wang, X.; Li, Z.; Huang, J. Silver Nanoparticle-Induced Phosphorylation of Histone H3 at Serine 10 Involves MAPK Pathways. Biomolecules 2019, 9, 78. https://doi.org/10.3390/biom9020078
Zhao X, Rao Y, Liang J, Lin S, Wang X, Li Z, Huang J. Silver Nanoparticle-Induced Phosphorylation of Histone H3 at Serine 10 Involves MAPK Pathways. Biomolecules. 2019; 9(2):78. https://doi.org/10.3390/biom9020078
Chicago/Turabian StyleZhao, Xiaoxu, Yanying Rao, Jie Liang, Shoukai Lin, Xiumei Wang, Zhangliang Li, and Jianhui Huang. 2019. "Silver Nanoparticle-Induced Phosphorylation of Histone H3 at Serine 10 Involves MAPK Pathways" Biomolecules 9, no. 2: 78. https://doi.org/10.3390/biom9020078