Efficacy and Molecular Effects of a Reduced Graphene Oxide/Fe₃O₄ Nanocomposite in Photothermal Therapy Against Cancer

References

• IARC Global Cancer Observatory. Press release N° 263; 2018 Available from: http://gco.iarc.fr/. Accessed 1021, 2019
   Google Scholar
• Lepisto AJ, Mckolanis JR, Finn OJ. Chapter 10 – cancer Immunotherapy: challenges and opportunities In: Cancer Immunotherapy; 2007:167–181. doi:10.1016/B978-012372551-6/50074-2
   Google Scholar
• Yoo CB, Jones PA. Epigenetic therapy of cancer: past, present and future. Nat Rev Drug Discov. 2006;5(1):37–50. doi:10.1038/nrd193016485345
   PubMed Web of Science ®Google Scholar
• Pereira DM, Rodrigues PM, Borralho PM, Rodrigues CMP. Delivering the promise of miRNA cancer therapeutics. Drug Discov Today. 2013;18(5):282–289. doi:10.1016/j.drudis.2012.10.00223064097
   PubMed Web of Science ®Google Scholar
• Yang X, Zhang X, Ma Y, Huang Y, Wang Y, Chen Y. Superparamagnetic graphene oxide–Fe3O4 nanoparticles hybrid for controlled targeted drug carriers. J Mater Chem. 2009;19(18):2710. doi:10.1039/b821416f
   Web of Science ®Google Scholar
• Pérez-Hernández M, Del Pino P, Mitchell SG, et al. Dissecting the molecular mechanism of apoptosis during photothermal therapy using gold nanoprisms. ACS Nano. 2015;9(1):52–61. doi:10.1021/nn505468v25493329
   PubMed Web of Science ®Google Scholar
• Huang X, El-Sayed MA. Plasmonic photo-thermal therapy (PPTT). Alexandria J Med. 2011;47(1):1–9. doi:10.1016/j.ajme.2011.01.001
   Google Scholar
• Shi X, Gong H, Li Y, Wang C, Cheng L, Liu Z. Graphene-based magnetic plasmonic nanocomposite for dual bioimaging and photothermal therapy. Biomaterials. 2013;34(20):4786–4793. doi:10.1016/j.biomaterials.2013.03.02323557860
   PubMed Web of Science ®Google Scholar
• Yang L, Tseng YT, Suo G, et al. Photothermal therapeutic response of cancer cells to aptamer-gold nanoparticle-hybridized graphene oxide under NIR illumination. ACS Appl Mater Interfaces. 2015;7(9):5097–5106. doi:10.1021/am508117e25705789
   PubMed Web of Science ®Google Scholar
• Lal S, Clare SE, Halas NJ. Photothermal therapy: impending clinical impact. Acc Chem Res. 2008;41(12):1842–1851. doi:10.1021/ar800150g19053240
   PubMed Web of Science ®Google Scholar
• Liu Y, Li N, Li Y, Li H, Wang X. HSP70 is associated with endothelial activation in placental vascular diseases. Mol Med. 2008;14(9–10):1. doi:10.2119/2008-00009.Liu
   Web of Science ®Google Scholar
• Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Molecular Biology of the Cell. Vol. 1 Fifth ed. Anderson M, Granum S eds.Garland Science, Taylor & Francis Group; 2008. doi:10.1017/CBO9781107415324.004
   Google Scholar
• Geim AK, Novoselov KS, The rise of graphene. Nat Mater. 2007;6(3):183–191. doi:10.1038/nmat184917330084
   PubMed Web of Science ®Google Scholar
• Lotya M, Hernandez Y, King PJ, et al. Liquid phase production of graphene by exfoliation of graphite in surfactant/water solutions liquid phase production of graphene by exfoliation of graphite in surfactant/water solutions. J Am Chem Soc. 2009;131(11):3611–3620. doi:10.1021/ja807449u19227978
   PubMedGoogle Scholar
• Zhang Y, Zhang L, Zhou C. Review of chemical vapor deposition of graphene and related applications. Acc Chem Res. 2013;46(10):2329–2339. doi:10.1021/ar300203n23480816
   PubMed Web of Science ®Google Scholar
• Coleman JN. Liquid exfoliation of defect-free graphene. Acc Chem Res. 2012;6(1):14–22. doi:10.1021/ar300009f
   Google Scholar
• Paton KR, Varrla E, Backes C, et al. Scalable production of large quantities of defect-free few-layer graphene by shear exfoliation in liquids. Nat Mater. 2014;13(6):624–630. doi:10.1038/nmat394424747780
   PubMed Web of Science ®Google Scholar
• Hummers WS, Offeman RE. Preparation of graphitic oxide. J Am Chem Soc. 1958;80(6):1339. doi:10.1021/ja01539a017
   Web of Science ®Google Scholar
• Sun Z, James DK, Tour JM. Graphene chemistry: synthesis and manipulation. J Phys Chem Lett. 2011;2(19):2425–2432. doi:10.1021/jz201000a
   Web of Science ®Google Scholar
• Jahanbani S, Benvidi A. A novel electrochemical DNA biosensor based on a modified magnetic bar carbon paste electrode with Fe3O4NPs-reduced graphene oxide/PANHS nanocomposite. Mater Sci Eng C. 2016;68:1–8. doi:10.1016/j.msec.2016.05.056
   PubMed Web of Science ®Google Scholar
• Gollavelli G, Chang CC, Ling YC. Facile synthesis of smart magnetic graphene for safe drinking water: heavy metal removal and disinfection control. ACS Sustain Chem Eng. 2013;1(5):462–472. doi:10.1021/sc300112z
   Web of Science ®Google Scholar
• Ma X, Tao H, Yang K, et al. A functionalized graphene oxide-iron oxide nanocomposite for magnetically targeted drug delivery, photothermal therapy, and magnetic resonance imaging. Nano Res. 2012;5(3):199–212. doi:10.1007/s12274-012-0200-y
   Web of Science ®Google Scholar
• Tian T, Shi X, Cheng L, et al. Graphene-based nanocomposite as an effective, multifunctional, and recyclable antibacterial agent. ACS Appl Mater Interfaces. 2014;6(11):8542–8548. doi:10.1021/am502291424806506
   PubMed Web of Science ®Google Scholar
• Amjadi M, Manzoori JL, Hallaj T. Chemiluminescence of graphene quantum dots and its application to the determination of uric acid. J Lumin. 2014;153:73–78. doi:10.1016/j.jlumin.2014.03.020
   Web of Science ®Google Scholar
• Chen ML, He YJ, Chen XW, Wang JH. Quantum-dot-conjugated graphene as a probe for simultaneous cancer-targeted fluorescent imaging, tracking, and monitoring drug delivery. Bioconjug Chem. 2013;24(3):387–397. doi:10.1021/bc300480923425155
   PubMed Web of Science ®Google Scholar
• Patil AJ, Vickery JL, Scott TB, Mann S. Aqueous stabilization and self-assembly of craphene sheets into layered bio-nanocomposites using DNA. Adv Mater. 2009;21(31):3159–3164. doi:10.1002/adma.200803633
   Web of Science ®Google Scholar
• Paul-Samojedny M, Kokocińska D, Samojedny A, et al. Expression of cell survival/death genes: bcl-2 and bax at the rate of colon cancer prognosis. Biochim Biophys Acta Mol Basis Dis. 2005;1741(1):25–29. doi:10.1016/j.bbadis.2004.11.021
   Web of Science ®Google Scholar
• Sun X, Liu Z, Welsher K, et al. Nano-graphene oxide for cellular imaging and drug delivery. Nano Res. 2008;1(3):203–212. doi:10.1007/s12274-008-8021-820216934
   PubMed Web of Science ®Google Scholar
• Chandra V, Park J, Chun Y, Lee JW, Hwang I, Kim KS. Water-dispersible magnetite-reduced graphene oxide composites for arsenic removal. ACS Nano. 2010;4(7):3979–3986. doi:10.1021/nn100889720552997
   PubMed Web of Science ®Google Scholar
• Haimes J, Kelley M Demonstration of a ΔΔCq calculation method to compute relative gene expression from qPCR data. GE Healthc; 2010 Available from: http://dharmacon.gelifesciences.com/uploadedfiles/resources/delta-cq-solaris-technote.pdf.
   Google Scholar
• Ramakrishnan Minitha C, Suresh R, Kumar Maity U, et al. Magnetite nanoparticle decorated reduced graphene oxide composite as an efficient and recoverable adsorbent for the removal of cesium and strontium ions. Ind Eng Chem Res. 2018;57:58. doi:10.1021/acs.iecr.7b05340
   Web of Science ®Google Scholar
• Liu Y, Chen Z, Zhang Y, et al. Broadband and lightweight microwave absorber constructed by in situ growth of hierarchical CoFe 2 O 4/reduced graphene oxide porous nanocomposites. ACS Appl Mater Interfaces. 2018;10(16):13860–13868. doi:10.1021/acsami.8b0213729589899
   PubMed Web of Science ®Google Scholar
• Gurbani N, Han C-P, Marumoto K, et al. Biogenic reduction of graphene oxide: an efficient superparamagnetic material for photocatalytic hydrogen production. ACS Appl Energy Mater. 2018;1(11):5907–5918. doi:10.1021/acsaem.8b00552
   Web of Science ®Google Scholar
• Jabbar A, Yasin G, Khan WQ, et al. Electrochemical deposition of nickel graphene composite coatings effect of deposition temperature on its surface morphology and corrosion resistance. RSC Adv. 2017;7(49):31100–31109. doi:10.1039/c6ra28755g
   Web of Science ®Google Scholar
• Ferrari AC, Meyer JC, Scardaci V, et al. Raman spectrum of graphene and graphene layers. Phys Rev Lett. 2006;97(18). doi:10.1103/PhysRevLett.97.187401.
   Web of Science ®Google Scholar
• Wall M. The Raman spectroscopy of graphene and the determination of layer thickness. Thermo Sci. 2011;5.
   Google Scholar
• Malard LM, Pimenta MA, Dresselhaus G, Dresselhaus MS. Raman spectroscopy in graphene. Phys Rep. 2009;473(5–6):51–87. doi:10.1016/j.physrep.2009.02.003
   Web of Science ®Google Scholar
• Zong M, Huang Y, Zhang N. Reduced graphene oxide-CoFe2O4 composite: synthesis and electromagnetic absorption properties. Appl Surf Sci. 2015;345:272–278. doi:10.1016/j.apsusc.2015.03.203
   Web of Science ®Google Scholar
• Liu Y, Guo H, Sun K, Jiang J. Magnetic CoOx@C-reduced graphene oxide composite with catalytic activity towards hydrogen generation. Int J Hydrogen Energy. 2019;44(52):28163–28172. doi:10.1016/j.ijhydene.2019.09.034
   Web of Science ®Google Scholar
• Wahajuddin AS. Superparamagnetic iron oxide nanoparticles: magnetic nanoplatforms as drug carriers. Int J Nanomedicine. 2012;7:3445–3471. doi:10.2147/IJN.S3032022848170
   PubMed Web of Science ®Google Scholar
• Szymczyk A, Paszkiewicz S, Typek J, et al. Magnetic properties of poly(trimethylene terephthalate‐block‐poly(tetramethylene oxide) copolymer nanocomposites reinforced by graphene oxide–Fe3O4 hybrid nanoparticles. Phys Status Solidi. 2019;216(23):1900402. doi:10.1002/pssa.201900402
   Google Scholar
• Vinodhkumar G, Wilson J, Inbanathan SSR, Potheher IV, Ashokkumar M, Peter AC. Solvothermal synthesis of magnetically separable reduced graphene oxide/Fe3O4 hybrid nanocomposites with enhanced photocatalytic properties. Phys Rev B Condens Matter. 2020;580:411752. doi:10.1016/j.physb.2019.411752
   Web of Science ®Google Scholar
• Hakimi M, Alimard P, Yousefi M. Green synthesis of reduced graphene oxide/Sr2CuMgFe 28O46 nanocomposite with tunable magnetic properties. Ceram Int. 2014;40(8PART A):11957–11961. doi:10.1016/j.ceramint.2014.04.032
   Google Scholar
• Guo X, Mei N. Assessment of the toxic potential of graphene family nanomaterials. J Food Drug Anal. 2014;22(1):105–115. doi:10.1016/j.jfda.2014.01.00924673908
   PubMed Web of Science ®Google Scholar
• Liao KH, Lin YS, MacOsko CW, Haynes CL. Cytotoxicity of graphene oxide and graphene in human erythrocytes and skin fibroblasts. ACS Appl Mater Interfaces. 2011;3(7):2607–2615. doi:10.1021/am200428v21650218
   PubMed Web of Science ®Google Scholar
• Jiao G, He X, Li X, et al. Limitations of MTT and CCK-8 assay for evaluation of graphene cytotoxicity. RSC Adv. 2015;5(66):53240–53244. doi:10.1039/C5RA08958A
   Web of Science ®Google Scholar
• Li R, Guiney LM, Chang CH, et al. Surface oxidation of graphene oxide determines membrane damage, lipid peroxidation, and cytotoxicity in macrophages in a pulmonary toxicity model. ACS Nano. 2018;12(2):1390–1402. doi:10.1021/acsnano.7b0773729328670
   PubMed Web of Science ®Google Scholar
• Das S, Singh S, Singh V, et al. Oxygenated functional group density on graphene oxide: its effect on cell toxicity. Part Part Syst Char. 2013;30(2):148–157. doi:10.1002/ppsc.201200066
   Web of Science ®Google Scholar
• Bonaccorso F, Sun Z, Hasan T, Ferrari AC. Graphene photonics and optoelectronics. Nat Photonics. 2010;4(9):611–622. doi:10.1038/nphoton.2010.186
   Web of Science ®Google Scholar
• Gurunathan S, Han JW, Eppakayala V, Kim JH. Biocompatibility of microbially reduced graphene oxide in primary mouse embryonic fibroblast cells. Colloids Surf B Biointerfaces. 2013;105:58–66. doi:10.1016/j.colsurfb.2012.12.03623352948
   PubMed Web of Science ®Google Scholar
• Lingaraju K, Raja Naika H, Nagaraju G, Nagabhushana H. Biocompatible synthesis of reduced graphene oxide from Euphorbia heterophylla (L.) and their in-vitro cytotoxicity against human cancer cell lines. Biotechnol Rep. 2019;24:e00376. doi:10.1016/j.btre.2019.e00376
   Google Scholar
• Luo L, Xu L, Zhao H. Biosynthesis of reduced graphene oxide and its in-vitro cytotoxicity against cervical cancer (HeLa) cell lines. Mater Sci Eng C. 2017;78:198–202. doi:10.1016/j.msec.2017.04.031
   PubMed Web of Science ®Google Scholar
• Li Y, Yuan H, von Dem Bussche A, et al. Graphene microsheets enter cells through spontaneous membrane penetration at edge asperities and corner sites. Proc Natl Acad Sci U S A. 2013;110(30):12295–12300. doi:10.1073/pnas.122227611023840061
   PubMed Web of Science ®Google Scholar
• Duan G, Zhang Y, Luan B, et al. Graphene-induced pore formation on cell membranes. Sci Rep. 2017;7. doi:10.1038/srep42767
   Web of Science ®Google Scholar
• Badrigilan S, Shaabani B, Gharehaghaji N, Mesbahi A. Iron oxide/bismuth oxide nanocomposites coated by graphene quantum dots: “three-in-one” theranostic agents for simultaneous CT/MR imaging-guided in vitro photothermal therapy. Photodiagnosis Photodyn Ther. 2018;25:504–514. doi:10.1016/j.pdpdt.2018.10.02130385298
   PubMed Web of Science ®Google Scholar
• Xie M, Zhang F, Peng H, et al. Layer-by-layer modification of magnetic graphene oxide by chitosan and sodium alginate with enhanced dispersibility for targeted drug delivery and photothermal therapy. Colloids Surf B Biointerfaces. 2019;176:462–470. doi:10.1016/j.colsurfb.2019.01.02830682619
   PubMed Web of Science ®Google Scholar
• Geng B, Yang D, Pan D, et al. NIR-responsive carbon dots for efficient photothermal cancer therapy at low power densities. Carbon. 2018;134:153–162. doi:10.1016/j.carbon.2018.03.084
   Web of Science ®Google Scholar
• Zhang F, Xie M, Zhao Y, et al. Chitosan and dextran stabilized GO-iron oxide nanosheets with high dispersibility for chemotherapy and photothermal ablation. Ceram Int. 2019;45(5):5996–6003. doi:10.1016/j.ceramint.2018.12.070
   Web of Science ®Google Scholar
• Chang X, Zhang Y, Xu P, Zhang M, Wu H, Yang S. Graphene oxide/MnWO 4 nanocomposite for magnetic resonance/photoacoustic dual-model imaging and tumor photothermo-chemotherapy. Carbon. 2018;138:397–409. doi:10.1016/j.carbon.2018.07.058
   Web of Science ®Google Scholar
• Zhen SJ, Wang TT, Liu YX, Wu ZL, Zou HY, Huang CZ. Reduced graphene oxide coated Cu2−xSe nanoparticles for targeted chemo-photothermal therapy. J Photochem Photobiol B Biol. 2018;180:9–16. doi:10.1016/j.jphotobiol.2018.01.020
   PubMed Web of Science ®Google Scholar
• Su Y, Wang N, Liu B, et al. A phototheranostic nanoparticle for cancer therapy fabricated by BODIPY and graphene to realize photo-chemo synergistic therapy and fluorescence/photothermal imaging. Dyes Pigm. 2020;177:108262. doi:10.1016/j.dyepig.2020.108262
   Web of Science ®Google Scholar
• Liu J, Yuan X, Deng L, et al. Graphene oxide activated by 980 nm laser for cascading two-photon photodynamic therapy and photothermal therapy against breast cancer. Appl Mater Today. 2020;20:100665. doi:10.1016/j.apmt.2020.100665
   Web of Science ®Google Scholar
• Liu H, Li C, Qian Y, et al. Magnetic-induced graphene quantum dots for imaging-guided photothermal therapy in the second near-infrared window. Biomaterials. 2020;232:119700. doi:10.1016/j.biomaterials.2019.11970031881379
   PubMed Web of Science ®Google Scholar
• Chang X, Zhang M, Wang C, Zhang J, Wu H, Yang S. Graphene oxide/BaHoF5/PEG nanocomposite for dual-modal imaging and heat shock protein inhibitor-sensitized tumor photothermal therapy. Carbon. 2020;158:372–385. doi:10.1016/j.carbon.2019.10.105
   Web of Science ®Google Scholar
• Marangon I, Ménard-Moyon C, Silva AKA, Bianco A, Luciani N, Gazeau F. Synergic mechanisms of photothermal and photodynamic therapies mediated by photosensitizer/carbon nanotube complexes. Carbon. 2016;97:110–123. doi:10.1016/j.carbon.2015.08.023
   Web of Science ®Google Scholar
• Salaheldin TA, Loutfy SA, Ramadan MA, Youssef T, Mousa SA. Ir-enhanced photothermal therapeutic effect of graphene magnetite nanocomposite on human liver cancer HepG2 cell model. Int J Nanomedicine. 2019;14:4397–4412. doi:10.2147/IJN.S19625631417251
   PubMed Web of Science ®Google Scholar
• Schmitt E, Gehrmann M, Brunet M, Multhoff G, Garrido C. Intracellular and extracellular functions of heat shock proteins: repercussions in cancer therapy. J Leukoc Biol. 2007;81(1):15–27. doi:10.1189/jlb.030616716931602
   PubMed Web of Science ®Google Scholar
• Rizwan Younis M, Bing An R, Yin Y-C, Wang S, Ye D, Xia X-H. Plasmonic nanohybrid with high photothermal conversion efficiency for simultaneously effective antibacterial/anticancer photothermal therapy. ACS Appl Bio Mater. 2019;2(9):3942–3953. doi:10.1021/acsabm.9b00521
   PubMedGoogle Scholar
• Tang X, Tan L, Shi K, et al. Gold nanorods together with HSP inhibitor-VER-155008 micelles for colon cancer mild-temperature photothermal therapy. Acta Pharm Sin B. 2018;8(4):587–601. doi:10.1016/j.apsb.2018.05.01130109183
   PubMed Web of Science ®Google Scholar
• 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(2):247. doi:10.3390/ijms20020247
   PubMed Web of Science ®Google Scholar
• Choi YJ, Gurunathan S, Kim JH. Graphene oxide-silver nanocomposite enhances cytotoxic and apoptotic potential of salinomycin in human ovarian cancer stem cells (OvCSCs): a novel approach for cancer therapy. Int J Mol Sci. 2018;19(710):710. doi:10.3390/ijms19030710
   PubMedGoogle Scholar
• Adams JM, Cory S. The Bcl-2-regulated apoptosis switch: mechanism and therapeutic potential. Curr Opin Immunol. 2009;19(5):488–496. doi:10.1016/j.coi.2007.05.004.The
   Web of Science ®Google Scholar
• Thapa RK, Byeon JH, Choi HG, Yong CS, Kim JO. PEGylated lipid bilayer-wrapped nano-graphene oxides for synergistic co-delivery of doxorubicin and rapamycin to prevent drug resistance in cancers. Nanotechnology. 2017;28(29):295101. doi:10.1088/1361-6528/aa799728614069
   PubMed Web of Science ®Google Scholar
• Placzek WJ, Wei J, Kitada S, Zhai D, Reed JC, Pellecchia M. A survey of the anti-apoptotic Bcl-2 subfamily expression in cancer types provides a platform to predict the efficacy of Bcl-2 antagonists in cancer therapy. Cell Death Dis. 2010;1(5):e40. doi:10.1038/cddis.2010.1821364647
   PubMedGoogle Scholar