Differential Immunomodulatory Effect of Graphene Oxide and Vanillin-Functionalized Graphene Oxide Nanoparticles in Human Acute Monocytic Leukemia Cell Line (THP-1)
Abstract
:1. Introduction
2. Results
2.1. Synthesis and Characterization of Graphene Oxide (GO) and Vanillin-Functionalized GO (V-rGO)
2.2. Effect of GO and V-rGO on Cell Viability and Proliferation of THP-1 Cells
2.3. GO and V-rGO Enhance Lactate Dehydrogenase (LDH) Leakage
2.4. GO and V-rGO Induce Mitochondrial Dysfunctions
2.5. Impact of GO and V-rGO on Reactive Oxygen Species (ROS) Generation and Lipid Peroxidation
2.6. Effect of GO and V-rGO on Antioxidants
2.7. GO and V-rGO Induce Expression of Apoptotic Genes and Suppress Anti-Apoptotic Genes
2.8. Effect of GO and V-rGO on DNA Damage
2.9. Effect of GO and V-rGO on Cytokine and Chemokine Production
3. Materials and Methods
3.1. Materials
3.2. GO Synthesis, Reduction, and Characterization
3.3. Cell Viability Assay
3.4. BrdU Cell Proliferation Assay
3.5. Measurement of Cytotoxicity
3.6. Cell Mortality Assay
3.7. Determination of ROS
3.8. Determination of Malondialdehyde (MDA)
3.9. Mitochondrial Membrane Potential (MMP)
3.10. Measurement of ATP
3.11. Measurement of Anti-Oxidative Markers
3.12. Reverse Transcription-Quantitative Polymerase Chain Reaction (RT-qPCR)
3.13. Measurement of Cytokines and Chemokines
3.14. Statistical Analysis
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Bitounis, D.; Ali-Boucetta, H.; Hong, B.H.; Min, D.H.; Kostarelos, K. Prospects and challenges of graphene in biomedical applications. Adv. Mater. 2013, 25, 2258–2268. [Google Scholar] [CrossRef] [PubMed]
- Bhattacharya, M. Polymer nanocomposites—A comparison between carbon nanotubes, graphene, and clay as nanofillers. Materials 2016, 9, 262. [Google Scholar] [CrossRef] [PubMed]
- Gurunathan, S.; Kim, J.-H. Synthesis, toxicity, biocompatibility, and biomedical applications of graphene and graphene-related materials. Int. J. Nanomed. 2016, 11, 1927. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mukherjee, S.P.; Bottini, M.; Fadeel, B. Graphene and the immune system: A romance of many dimensions. Front. Immunol. 2017, 8, 673. [Google Scholar] [CrossRef] [PubMed]
- Yue, H.; Wei, W.; Yue, Z.; Wang, B.; Luo, N.; Gao, Y.; Ma, D.; Ma, G.; Su, Z. The role of the lateral dimension of graphene oxide in the regulation of cellular responses. Biomaterials 2012, 33, 4013–4021. [Google Scholar] [CrossRef] [PubMed]
- Mendes, R.G.; Koch, B.; Bachmatiuk, A.; Ma, X.; Sanchez, S.; Damm, C.; Schmidt, O.G.; Gemming, T.; Eckert, J.; Rümmeli, M.H. A size dependent evaluation of the cytotoxicity and uptake of nanographene oxide. J. Mater. Chem. B 2015, 3, 2522–2529. [Google Scholar] [CrossRef] [Green Version]
- Zhang, W.; Yan, L.; Li, M.; Zhao, R.; Yang, X.; Ji, T.; Gu, Z.; Yin, J.-J.; Gao, X.; Nie, G. Deciphering the underlying mechanisms of oxidation-state dependent cytotoxicity of graphene oxide on mammalian cells. Toxicol. Lett. 2015, 237, 61–71. [Google Scholar] [CrossRef]
- Avouris, P.; Dimitrakopoulos, C.; Farmer, D.B.; Steiner, M.B.; Engel, M.; Krupke, R.; Lin, Y.-M. Solution-Assisted Carbon Nanotube Placement with Graphene Electrodes. U.S. Patent 8,859,439, 14 October 2014. [Google Scholar]
- Subrahmanyam, K.; Vivekchand, S.; Govindaraj, A.; Rao, C. A study of graphenes prepared by different methods: Characterization, properties and solubilization. J. Mater. Chem. 2008, 18, 1517–1523. [Google Scholar] [CrossRef]
- Kim, K.S.; Zhao, Y.; Jang, H.; Lee, S.Y.; Kim, J.M.; Kim, K.S.; Ahn, J.-H.; Kim, P.; Choi, J.-Y.; Hong, B.H. Large-scale pattern growth of graphene films for stretchable transparent electrodes. Nature 2009, 457, 706. [Google Scholar] [CrossRef]
- Stankovich, S.; Dikin, D.A.; Piner, R.D.; Kohlhaas, K.A.; Kleinhammes, A.; Jia, Y.; Wu, Y.; Nguyen, S.T.; Ruoff, R.S. Synthesis of graphene-based nanosheets via chemical reduction of exfoliated graphite oxide. Carbon 2007, 45, 1558–1565. [Google Scholar] [CrossRef]
- Kosynkin, D.V.; Higginbotham, A.L.; Sinitskii, A.; Lomeda, J.R.; Dimiev, A.; Price, B.K.; Tour, J.M. Longitudinal unzipping of carbon nanotubes to form graphene nanoribbons. Nature 2009, 458, 872–876. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gurunathan, S.; Han, J.W.; Dayem, A.A.; Eppakayala, V.; Kim, J.H. Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa. Int. J. Nanomed. 2012, 7, 5901–5914. [Google Scholar] [CrossRef] [PubMed]
- Gurunathan, S.; Han, J.W.; Eppakayala, V.; Dayem, A.A.; Kwon, D.N.; Kim, J.H. Biocompatibility effects of biologically synthesized graphene in primary mouse embryonic fibroblast cells. Nanoscale Res. Lett. 2013, 8, 393. [Google Scholar] [CrossRef] [PubMed]
- Gurunathan, S.; Han, J.; Park, J.H.; Kim, J.H. An in vitro evaluation of graphene oxide reduced by Ganoderma spin human breast cancer cells (MDA-MB-231). Int. J. Nanomed. 2014, 9, 1783. [Google Scholar] [CrossRef] [PubMed]
- Gurunathan, S.; Han, J.W.; Park, J.H.; Kim, E.; Choi, Y.-J.; Kwon, D.-N.; Kim, J.-H. Reduced graphene oxide–silver nanoparticle nanocomposite: A potential anticancer nanotherapy. Int. J. Nanomed. 2015, 10, 6257. [Google Scholar] [CrossRef] [PubMed]
- Gurunathan, S.; Kim, J.H. Graphene Oxide-Silver Nanoparticles Nanocomposite Stimulates Differentiation in Human Neuroblastoma Cancer Cells (SH-SY5Y). Int. J. Mol. Sci. 2017, 18, 2549. [Google Scholar] [CrossRef] [PubMed]
- Chatterjee, N.; Eom, H.-J.; Choi, J. A systems toxicology approach to the surface functionality control of graphene–cell interactions. Biomaterials 2014, 35, 1109–1127. [Google Scholar] [CrossRef]
- Jaworski, S.; Sawosz, E.; Kutwin, M.; Wierzbicki, M.; Hinzmann, M.; Grodzik, M.; Winnicka, A.; Lipińska, L.; Włodyga, K.; Chwalibog, A. In vitro and in vivo effects of graphene oxide and reduced graphene oxide on glioblastoma. Int. J. Nanomed. 2015, 10, 1585. [Google Scholar] [Green Version]
- Feito, M.; Vila, M.; Matesanz, M.; Linares, J.; Gonçalves, G.; Marques, P.; Vallet-Regí, M.; Rojo, J.; Portolés, M. In vitro evaluation of graphene oxide nanosheets on immune function. J. Colloid Interface Sci. 2014, 432, 221–228. [Google Scholar] [CrossRef] [Green Version]
- Zhang, B.; Wang, Y.; Zhai, G. Biomedical applications of the graphene-based materials. Mater. Sci. Eng. C 2016, 61, 953–964. [Google Scholar] [CrossRef]
- Liao, K.-H.; Lin, Y.-S.; Macosko, C.W.; Haynes, C.L. Cytotoxicity of graphene oxide and graphene in human erythrocytes and skin fibroblasts. ACS Appl. Mater. Interfaces 2011, 3, 2607–2615. [Google Scholar] [CrossRef]
- Ding, D.Q.; Matsuda, A.; Okamasa, K.; Nagahama, Y.; Haraguchi, T.; Hiraoka, Y. Meiotic cohesin-based chromosome structure is essential for homologous chromosome pairing in Schizosaccharomyces pombe. Chromosoma 2016, 125, 205–214. [Google Scholar] [CrossRef]
- Ma, J.; Liu, R.; Wang, X.; Liu, Q.; Chen, Y.; Valle, R.P.; Zuo, Y.Y.; Xia, T.; Liu, S. Crucial role of lateral size for graphene oxide in activating macrophages and stimulating pro-inflammatory responses in cells and animals. ACS Nano 2015, 9, 10498–10515. [Google Scholar] [CrossRef]
- Orecchioni, M.; Ménard-Moyon, C.; Delogu, L.G.; Bianco, A. Graphene and the immune system: Challenges and potentiality. Adv. Drug Deliv. Rev. 2016, 105, 163–175. [Google Scholar] [CrossRef]
- Sun, P.; Wang, K.; Zhu, H. Recent developments in graphene-based membranes: Structure, mass-transport mechanism and potential applications. Adv. Mater. 2016, 28, 2287–2310. [Google Scholar] [CrossRef]
- Russier, J.; Treossi, E.; Scarsi, A.; Perrozzi, F.; Dumortier, H.; Ottaviano, L.; Meneghetti, M.; Palermo, V.; Bianco, A. Evidencing the mask effect of graphene oxide: A comparative study on primary human and murine phagocytic cells. Nanoscale 2013, 5, 11234–11247. [Google Scholar] [CrossRef]
- Sasidharan, A.; Panchakarla, L.S.; Sadanandan, A.R.; Ashokan, A.; Chandran, P.; Girish, C.M.; Menon, D.; Nair, S.V.; Rao, C.; Koyakutty, M. Hemocompatibility and macrophage response of pristine and functionalized graphene. Small 2012, 8, 1251–1263. [Google Scholar] [CrossRef]
- Li, Y.; Liu, Y.; Fu, Y.; Wei, T.; Le Guyader, L.; Gao, G.; Liu, R.-S.; Chang, Y.-Z.; Chen, C. The triggering of apoptosis in macrophages by pristine graphene through the MAPK and TGF-beta signaling pathways. Biomaterials 2012, 33, 402–411. [Google Scholar] [CrossRef]
- Zhou, H.; Zhao, K.; Li, W.; Yang, N.; Liu, Y.; Chen, C.; Wei, T. The interactions between pristine graphene and macrophages and the production of cytokines/chemokines via TLR-and NF-κB-related signaling pathways. Biomaterials 2012, 33, 6933–6942. [Google Scholar] [CrossRef]
- Xu, M.; Zhu, J.; Wang, F.; Xiong, Y.; Wu, Y.; Wang, Q.; Weng, J.; Zhang, Z.; Chen, W.; Liu, S. Improved in vitro and in vivo biocompatibility of graphene oxide through surface modification: Poly (acrylic acid)-functionalization is superior to PEGylation. ACS Nano 2016, 10, 3267–3281. [Google Scholar] [CrossRef]
- Zhou, K.; Thouas, G.A.; Bernard, C.C.; Nisbet, D.R.; Finkelstein, D.I.; Li, D.; Forsythe, J.S. Method to impart electro-and biofunctionality to neural scaffolds using graphene–polyelectrolyte multilayers. ACS Appl. Mater. Interfaces 2012, 4, 4524–4531. [Google Scholar] [CrossRef]
- Zhou, K.; Motamed, S.; Thouas, G.A.; Bernard, C.C.; Li, D.; Parkington, H.C.; Coleman, H.A.; Finkelstein, D.I.; Forsythe, J.S. Graphene functionalized scaffolds reduce the inflammatory response and supports endogenous neuroblast migration when implanted in the adult brain. PLoS ONE 2016, 11, e0151589. [Google Scholar] [CrossRef]
- Singh, S.K.; Singh, M.K.; Kulkarni, P.P.; Sonkar, V.K.; Grácio, J.J.; Dash, D. Amine-modified graphene: Thrombo-protective safer alternative to graphene oxide for biomedical applications. ACS Nano 2012, 6, 2731–2740. [Google Scholar] [CrossRef]
- Yan, J.; Chen, L.; Huang, C.-C.; Lung, S.-C.C.; Yang, L.; Wang, W.-C.; Lin, P.-H.; Suo, G.; Lin, C.-H. Consecutive evaluation of graphene oxide and reduced graphene oxide nanoplatelets immunotoxicity on monocytes. Colloids Surf. B 2017, 153, 300–309. [Google Scholar] [CrossRef]
- Hummers, W.S., Jr.; Offeman, R.E. Preparation of graphitic oxide. J. Am. Chem. Soc. 1958, 80, 1339. [Google Scholar] [CrossRef]
- Dikin, D.A.; Stankovich, S.; Zimney, E.J.; Piner, R.D.; Dommett, G.H.; Evmenenko, G.; Nguyen, S.T.; Ruoff, R.S. Preparation and characterization of graphene oxide paper. Nature 2007, 448, 457. [Google Scholar] [CrossRef]
- Zhang, X.-F.; Gurunathan, S. Biofabrication of a novel biomolecule-assisted reduced graphene oxide: An excellent biocompatible nanomaterial. Int. J. Nanomed. 2016, 11, 6635. [Google Scholar] [CrossRef]
- Lammel, T.; Boisseaux, P.; Fernández-Cruz, M.-L.; Navas, J.M. Internalization and cytotoxicity of graphene oxide and carboxyl graphene nanoplatelets in the human hepatocellular carcinoma cell line Hep G2. Part. Fibre Toxicol. 2013, 10, 27. [Google Scholar] [CrossRef] [Green Version]
- Muthoosamy, K.; Bai, R.G.; Abubakar, I.B.; Sudheer, S.M.; Lim, H.N.; Loh, H.S.; Huang, N.M.; Chia, C.H.; Manickam, S. Exceedingly biocompatible and thin-layered reduced graphene oxide nanosheets using an eco-friendly mushroom extract strategy. Int. J. Nanomed. 2015, 10, 1505–1519. [Google Scholar]
- Gurunathan, S.; Han, J.W.; Kim, J.-H. Green chemistry approach for the synthesis of biocompatible graphene. Int. J. Nanomed. 2013, 8, 2719. [Google Scholar] [CrossRef]
- Gurunathan, S.; Han, J.W.; Park, J.H.; Eppakayala, V.; Kim, J.-H. Ginkgo biloba: A natural reducing agent for the synthesis of cytocompatible graphene. Int. J. Nanomed. 2014, 9, 363. [Google Scholar] [CrossRef]
- Ferrari, A.C. Raman spectroscopy of graphene and graphite: Disorder, electron–phonon coupling, doping and nonadiabatic effects. Solid State Commun. 2007, 143, 47–57. [Google Scholar] [CrossRef]
- Zhang, X.F.; Liu, Z.G.; Shen, W.; Gurunathan, S. Silver Nanoparticles: Synthesis, Characterization, Properties, Applications, and Therapeutic Approaches. Int. J. Mol. Sci. 2016, 17, 1534. [Google Scholar] [CrossRef]
- Krishnamoorthy, K.; Veerapandian, M.; Zhang, L.-H.; Yun, K.; Kim, S.J. Antibacterial efficiency of graphene nanosheets against pathogenic bacteria via lipid peroxidation. J. Phys. Chem. C 2012, 116, 17280–17287. [Google Scholar] [CrossRef]
- Perumbilavil, S.; Sankar, P.; Priya Rose, T.; Philip, R. White light Z-scan measurements of ultrafast optical nonlinearity in reduced graphene oxide nanosheets in the 400–700 nm region. Appl. Phys. Lett. 2015, 107, 051104. [Google Scholar] [CrossRef]
- Gurunathan, S.; Han, J.W.; Dayem, A.A.; Eppakayala, V.; Park, M.-R.; Kwon, D.-N.; Kim, J.-H. Antibacterial activity of dithiothreitol reduced graphene oxide. J. Ind. Eng. Chem. 2013, 19, 1280–1288. [Google Scholar] [CrossRef]
- Duan, G.; Zhang, Y.; Luan, B.; Weber, J.K.; Zhou, R.W.; Yang, Z.; Zhao, L.; Xu, J.; Luo, J.; Zhou, R. Graphene-induced pore formation on cell membranes. Sci. Rep. 2017, 7, 42767. [Google Scholar] [CrossRef]
- Gurunathan, S.; Han, J.W.; Kim, E.S.; Park, J.H.; Kim, J.-H. Reduction of graphene oxide by resveratrol: A novel and simple biological method for the synthesis of an effective anticancer nanotherapeutic molecule. Int. J. Nanomed. 2015, 10, 2951. [Google Scholar] [CrossRef]
- Akhavan, O.; Ghaderi, E. Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano 2010, 4, 5731–5736. [Google Scholar] [CrossRef]
- Liu, S.; Zeng, T.H.; Hofmann, M.; Burcombe, E.; Wei, J.; Jiang, R.; Kong, J.; Chen, Y. Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: Membrane and oxidative stress. ACS Nano 2011, 5, 6971–6980. [Google Scholar] [CrossRef]
- Sasidharan, A.; Panchakarla, L.; Chandran, P.; Menon, D.; Nair, S.; Rao, C.; Koyakutty, M. Differential nano-bio interactions and toxicity effects of pristine versus functionalized graphene. Nanoscale 2011, 3, 2461–2464. [Google Scholar] [CrossRef]
- Das, S.; Singh, S.; Singh, V.; Joung, D.; Dowding, J.M.; Reid, D.; Anderson, J.; Zhai, L.; Khondaker, S.I.; Self, W.T. Oxygenated functional group density on graphene oxide: Its effect on cell toxicity. Part. Part. Syst. Charact. 2013, 30, 148–157. [Google Scholar] [CrossRef]
- Wu, Y.; Wang, F.; Wang, S.; Ma, J.; Xu, M.; Gao, M.; Liu, R.; Chen, W.; Liu, S. Reduction of graphene oxide alters its cyto-compatibility towards primary and immortalized macrophages. Nanoscale 2018, 10, 14637–14650. [Google Scholar] [CrossRef]
- Jaworski, S.; Sawosz, E.; Grodzik, M.; Winnicka, A.; Prasek, M.; Wierzbicki, M.; Chwalibog, A. In vitro evaluation of the effects of graphene platelets on glioblastoma multiforme cells. Int. J. Nanomed. 2013, 8, 413. [Google Scholar] [Green Version]
- Tabish, T.A.; Pranjol, M.Z.I.; Hayat, H.; Rahat, A.A.; Abdullah, T.M.; Whatmore, J.L.; Zhang, S. In vitro toxic effects of reduced graphene oxide nanosheets on lung cancer cells. Nanotechnology 2017, 28, 504001. [Google Scholar] [CrossRef] [Green Version]
- Akhavan, O.; Ghaderi, E.; Akhavan, A. Size-dependent genotoxicity of graphene nanoplatelets in human stem cells. Biomaterials 2012, 33, 8017–8025. [Google Scholar] [CrossRef]
- Habiba, K.; Bracho-Rincon, D.P.; Gonzalez-Feliciano, J.A.; Villalobos-Santos, J.C.; Makarov, V.I.; Ortiz, D.; Avalos, J.A.; Gonzalez, C.I.; Weiner, B.R.; Morell, G. Synergistic antibacterial activity of PEGylated silver–graphene quantum dots nanocomposites. Appl. Mater. Today 2015, 1, 80–87. [Google Scholar] [CrossRef] [Green Version]
- Sasidharan, A.; Swaroop, S.; Chandran, P.; Nair, S.; Koyakutty, M. Cellular and molecular mechanistic insight into the DNA-damaging potential of few-layer graphene in human primary endothelial cells. Nanomed. Nanotechnol. Biol. Med. 2016, 12, 1347–1355. [Google Scholar] [CrossRef]
- Jarosz, A.; Skoda, M.; Dudek, I.; Szukiewicz, D. Oxidative stress and mitochondrial activation as the main mechanisms underlying graphene toxicity against human cancer cells. Oxidative Med. Cell. Longev. 2016, 2016. [Google Scholar] [CrossRef]
- Yuan, Y.-G.; Wang, Y.-H.; Xing, H.-H.; Gurunathan, S. Quercetin-mediated synthesis of graphene oxide-silver nanoparticle nanocomposites: A suitable alternative nanotherapy for neuroblastoma. Int. J. Nanomed. 2017, 12, 5819–5839. [Google Scholar] [CrossRef]
- Pinto, A.M.; Goncalves, I.C.; Magalhaes, F.D. Graphene-based materials biocompatibility: A review. Colloids Surf. B 2013, 111, 188–202. [Google Scholar] [CrossRef]
- Zhou, H.; Zhang, B.; Zheng, J.; Yu, M.; Zhou, T.; Zhao, K.; Jia, Y.; Gao, X.; Chen, C.; Wei, T. The inhibition of migration and invasion of cancer cells by graphene via the impairment of mitochondrial respiration. Biomaterials 2014, 35, 1597–1607. [Google Scholar] [CrossRef]
- Tabish, T.A.; Zhang, S.; Winyard, P.G. Developing the next generation of graphene-based platforms for cancer therapeutics: The potential role of reactive oxygen species. Redox Boil. 2018, 15, 34–40. [Google Scholar] [CrossRef]
- BarathManiKanth, S.; Kalishwaralal, K.; Sriram, M.; Pandian, S.R.K.; Youn, H.-s.; Eom, S.; Gurunathan, S. Anti-oxidant effect of gold nanoparticles restrains hyperglycemic conditions in diabetic mice. J. Nanobiotechnol. 2010, 8, 16. [Google Scholar] [CrossRef] [Green Version]
- Yuan, Y.G.; Gurunathan, S. Combination of graphene oxide-silver nanoparticle nanocomposites and cisplatin enhances apoptosis and autophagy in human cervical cancer cells. Int. J. Nanomed. 2017, 12, 6537–6558. [Google Scholar] [CrossRef]
- Van Oijen, M.G.; Slootweg, P.J. Gain-of-function mutations in the tumor suppressor gene p53. Clin. Cancer Res. 2000, 6, 2138–2145. [Google Scholar]
- Vaseva, A.V.; Marchenko, N.D.; Ji, K.; Tsirka, S.E.; Holzmann, S.; Moll, U.M. p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 2012, 149, 1536–1548. [Google Scholar] [CrossRef]
- Cho, Y.C.; Pak, P.J.; Joo, Y.H.; Lee, H.-S.; Chung, N. In vitro and in vivo comparison of the immunotoxicity of single-and multi-layered graphene oxides with or without pluronic F-127. Sci. Rep. 2016, 6, 38884. [Google Scholar] [CrossRef]
- Qu, G.; Liu, S.; Zhang, S.; Wang, L.; Wang, X.; Sun, B.; Yin, N.; Gao, X.; Xia, T.; Chen, J.-J. Graphene oxide induces toll-like receptor 4 (TLR4)-dependent necrosis in macrophages. ACS Nano 2013, 7, 5732–5745. [Google Scholar] [CrossRef]
- Ou, L.; Song, B.; Liang, H.; Liu, J.; Feng, X.; Deng, B.; Sun, T.; Shao, L. Toxicity of graphene-family nanoparticles: A general review of the origins and mechanisms. Part. Fibre Toxicol. 2016, 13, 57. [Google Scholar] [CrossRef]
- Fortini, P.; Pascucci, B.; Parlanti, E.; D’errico, M.; Simonelli, V.; Dogliotti, E. 8-Oxoguanine DNA damage: At the crossroad of alternative repair pathways. Mutat. Res.-Fundam. Mol. Mech. Mutagen. 2003, 531, 127–139. [Google Scholar] [CrossRef]
- Liu, Y.; Luo, Y.; Wu, J.; Wang, Y.; Yang, X.; Yang, R.; Wang, B.; Yang, J.; Zhang, N. Graphene oxide can induce in vitro and in vivo mutagenesis. Sci. Rep. 2013, 3, 3469. [Google Scholar] [CrossRef] [Green Version]
- Wang, D.; Zhu, L.; Chen, J.-F.; Dai, L. Can graphene quantum dots cause DNA damage in cells? Nanoscale 2015, 7, 9894–9901. [Google Scholar] [CrossRef]
- Lu, C.-J.; Jiang, X.-F.; Junaid, M.; Ma, Y.-B.; Jia, P.-P.; Wang, H.-B.; Pei, D.-S. Graphene oxide nanosheets induce DNA damage and activate the base excision repair (BER) signaling pathway both in vitro and in vivo. Chemosphere 2017, 184, 795–805. [Google Scholar] [CrossRef]
- Qin, Y.; Zhou, Z.-W.; Pan, S.-T.; He, Z.-X.; Zhang, X.; Qiu, J.-X.; Duan, W.; Yang, T.; Zhou, S.-F. Graphene quantum dots induce apoptosis, autophagy, and inflammatory response via p38 mitogen-activated protein kinase and nuclear factor-κB mediated signaling pathways in activated THP-1 macrophages. Toxicology 2015, 327, 62–76. [Google Scholar] [CrossRef]
- Tian, R.; Zhong, S.; Wu, J.; Jiang, W.; Wang, T. Facile hydrothermal method to prepare graphene quantum dots from graphene oxide with different photoluminescences. RSC Adv. 2016, 6, 40422–40426. [Google Scholar] [CrossRef]
- Cooke, M.S.; Evans, M.D.; Dizdaroglu, M.; Lunec, J. Oxidative DNA damage: Mechanisms, mutation, and disease. FASEB J. 2003, 17, 1195–1214. [Google Scholar] [CrossRef]
- Zhi, X.; Fang, H.; Bao, C.; Shen, G.; Zhang, J.; Wang, K.; Guo, S.; Wan, T.; Cui, D. The immunotoxicity of graphene oxides and the effect of PVP-coating. Biomaterials 2013, 34, 5254–5261. [Google Scholar] [CrossRef]
- Lategan, K.; Alghadi, H.; Bayati, M.; de Cortalezzi, M.F.; Pool, E. Effects of Graphene Oxide Nanoparticles on the Immune System Biomarkers Produced by RAW 264.7 and Human Whole Blood Cell Cultures. Nanomaterials 2018, 8, 125. [Google Scholar] [CrossRef]
- Lategan, K.; Fowler, J.; Bayati, M.; Fidalgo de Cortalezzi, M.; Pool, E. The Effects of Carbon Dots on Immune System Biomarkers, Using the Murine Macrophage Cell Line RAW 264.7 and Human Whole Blood Cell Cultures. Available online: http://hdl.handle.net/10566/3796 (accessed on 1 June 2018).
- Khatri, M.; Bello, D.; Gaines, P.; Martin, J.; Pal, A.K.; Gore, R.; Woskie, S. Nanoparticles from photocopiers induce oxidative stress and upper respiratory tract inflammation in healthy volunteers. Nanotoxicology 2013, 7, 1014–1027. [Google Scholar] [CrossRef]
- Mukherjee, S.P.; Gliga, A.R.; Lazzaretto, B.; Brandner, B.; Fielden, M.; Vogt, C.; Newman, L.; Rodrigues, A.F.; Shao, W.; Fournier, P.M. Graphene oxide is degraded by neutrophils and the degradation products are non-genotoxic. Nanoscale 2018, 10, 1180–1188. [Google Scholar] [CrossRef]
- Zhao, J.; Pei, S.; Ren, W.; Gao, L.; Cheng, H.-M. Efficient preparation of large-area graphene oxide sheets for transparent conductive films. ACS Nano 2010, 4, 5245–5252. [Google Scholar] [CrossRef]
- Zhang, H.; Peng, C.; Yang, J.; Lv, M.; Liu, R.; He, D.; Fan, C.; Huang, Q. Uniform ultrasmall graphene oxide nanosheets with low cytotoxicity and high cellular uptake. ACS Appl. Mater. Interfaces 2013, 5, 1761–1767. [Google Scholar] [CrossRef]
- Qi, X.; Zhou, T.; Deng, S.; Zong, G.; Yao, X.; Fu, Q. Size-specified graphene oxide sheets: Ultrasonication assisted preparation and characterization. J. Mater. Sci. 2014, 49, 1785–1793. [Google Scholar] [CrossRef]
- Gurunathan, S.; Qasim, M.; Park, C.; Yoo, H.; Kim, J.-H.; Hong, K. Cytotoxic Potential and Molecular Pathway Analysis of Silver Nanoparticles in Human Colon Cancer Cells HCT116. Int. J. Mol. Sci. 2018, 19, 2269. [Google Scholar] [CrossRef]
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Gurunathan, S.; Kang, M.-H.; Jeyaraj, M.; Kim, J.-H. Differential Immunomodulatory Effect of Graphene Oxide and Vanillin-Functionalized Graphene Oxide Nanoparticles in Human Acute Monocytic Leukemia Cell Line (THP-1). Int. J. Mol. Sci. 2019, 20, 247. https://doi.org/10.3390/ijms20020247
Gurunathan S, Kang M-H, Jeyaraj M, Kim J-H. Differential Immunomodulatory Effect of Graphene Oxide and Vanillin-Functionalized Graphene Oxide Nanoparticles in Human Acute Monocytic Leukemia Cell Line (THP-1). International Journal of Molecular Sciences. 2019; 20(2):247. https://doi.org/10.3390/ijms20020247
Chicago/Turabian StyleGurunathan, Sangiliyandi, Min-Hee Kang, Muniyandi Jeyaraj, and Jin-Hoi Kim. 2019. "Differential Immunomodulatory Effect of Graphene Oxide and Vanillin-Functionalized Graphene Oxide Nanoparticles in Human Acute Monocytic Leukemia Cell Line (THP-1)" International Journal of Molecular Sciences 20, no. 2: 247. https://doi.org/10.3390/ijms20020247