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Research Article

D-α-tocopheryl polyethylene glycol 1000 succinate functionalized nanographene oxide for cancer therapy

    Duarte de Melo-Diogo

    CICS-UBI – Centro de Investigação em Ciências da Saúde, Universidade da Beira Interior, 6200-506 Covilhã, Portugal

    ,
    Cleide Pais-Silva

    CICS-UBI – Centro de Investigação em Ciências da Saúde, Universidade da Beira Interior, 6200-506 Covilhã, Portugal

    ,
    Elisabete C Costa

    CICS-UBI – Centro de Investigação em Ciências da Saúde, Universidade da Beira Interior, 6200-506 Covilhã, Portugal

    ,
    Ricardo O Louro

    ITQB – Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, 2780-157 Oeiras, Portugal

    &
    Ilídio J Correia

    *Author for correspondence:

    E-mail Address: icorreia@ubi.pt

    CICS-UBI – Centro de Investigação em Ciências da Saúde, Universidade da Beira Interior, 6200-506 Covilhã, Portugal

    Published Online:https://doi.org/10.2217/nnm-2016-0384

    Aim: To evaluate the therapeutic capacity of D-α-tocopheryl polyethylene glycol 1000 succinate (TPGS)-functionalized nanographene oxide (nGO) in breast cancer cells. Methods: TPGS-functionalized nGO-based materials were obtained through two different approaches: a simple sonication method and a one-pot hydrothermal treatment. Results: TPGS coating successfully improved the stability of the nGO-based materials. The nanomaterials that underwent the hydrothermal procedure generated a 1.4- to 1.6-fold higher temperature variation under near infrared laser irradiation than those prepared only by sonication. In vitro, the TPGS/nGO derivatives reduced breast cancer cells’ viability and had an insignificant effect on healthy cells. Furthermore, the combined application of TPGS/nGO derivatives and near infrared light generated an improved therapeutic effect. Conclusion: TPGS/nGO derivatives are promising materials for breast cancer phototherapy.

    Papers of special note have been highlighted as: • of interest

    References

    • 1 Cheng L, Wang C, Feng L, Yang K, Liu Z. Functional nanomaterials for phototherapies of cancer. Chem. Rev. 114(21), 10869–10939 (2014). • Comprehensive review covering the utilization of nanomaterials for cancer photothermal and photodynamic therapies.
    • 2 Vogel A, Venugopalan V. Mechanisms of pulsed laser ablation of biological tissues. Chem. Rev. 103(2), 577–644 (2003).
    • 3 Dreaden EC, Mackey MA, Huang X, Kang B, El-Sayed MA. Beating cancer in multiple ways using nanogold. Chem. Soc. Rev. 40(7), 3391–3404 (2011).
    • 4 Cheng L, Yang K, Chen Q, Liu Z. Organic stealth nanoparticles for highly effective in vivo near-infrared photothermal therapy of cancer. ACS Nano 6(6), 5605–5613 (2012).
    • 5 Wang Y, Black KC, Luehmann H et al. Comparison study of gold nanohexapods, nanorods, and nanocages for photothermal cancer treatment. ACS Nano 7(3), 2068–2077 (2013).
    • 6 Zhang B, Wang H, Shen S et al. Fibrin-targeting peptide CREKA-conjugated multi-walled carbon nanotubes for self-amplified photothermal therapy of tumor. Biomaterials 79, 46–55 (2016).
    • 7 Liu Z, Liu J, Wang R, Du Y, Ren J, Qu X. An efficient nano-based theranostic system for multi-modal imaging-guided photothermal sterilization in gastrointestinal tract. Biomaterials 56, 206–218 (2015).
    • 8 Liu Z, Liu X, Ran X, Ju E, Ren J, Qu X. Single-layer tungsten oxide as intelligent photo-responsive nanoagents for permanent male sterilization. Biomaterials 69, 56–64 (2015).
    • 9 Liu Z, Liu X, Du Y, Ren J, Qu X. Using plasmonic copper sulfide nanocrystals as smart light-driven sterilants. ACS Nano 9(10), 10335–10346 (2015).
    • 10 Jang C, Lee JH, Sahu A, Tae G. The synergistic effect of folate and RGD dual ligand of nanographene oxide on tumor targeting and photothermal therapy in vivo. Nanoscale 7(44), 18584–18594 (2015).
    • 11 Dreyer DR, Todd AD, Bielawski CW. Harnessing the chemistry of graphene oxide. Chem. Soc. Rev. 43(15), 5288–5301 (2014).
    • 12 Fazaeli Y, Akhavan O, Rahighi R, Aboudzadeh MR, Karimi E, Afarideh H. In vivo SPECT imaging of tumors by 198,199Au-labeled graphene oxide nanostructures. Mater. Sci. Eng. C 45, 196–204 (2014).
    • 13 Yang K, Zhang S, Zhang G, Sun X, Lee S-T, Liu Z. Graphene in mice: ultrahigh in vivo tumor uptake and efficient photothermal therapy. Nano Lett. 10(9), 3318–3323 (2010). • Pioneering work describing the in vivo photothermal capacity of PEGylated nanographene oxide.
    • 14 Bitounis D, Ali-Boucetta H, Hong BH, Min DH, Kostarelos K. Prospects and challenges of graphene in biomedical applications. Adv. Mater. 25(16), 2258–2268 (2013).
    • 15 Sun X, Liu Z, Welsher K et al. Nano-graphene oxide for cellular imaging and drug delivery. Nano Res. 1(3), 203–212 (2008).
    • 16 Shen H, Liu M, He H et al. PEGylated graphene oxide-mediated protein delivery for cell function regulation. ACS Appl. Mater. Interfaces 4(11), 6317–6323 (2012).
    • 17 Krishna KV, Ménard-Moyon C, Verma S, Bianco A. Graphene-based nanomaterials for nanobiotechnology and biomedical applications. Nanomedicine 8(10), 1669–1688 (2013). • Comprehensive review detailing the application of graphene-based nanomaterials in tissue engineering, cancer therapy, sensing and imaging.
    • 18 Yang K, Wan J, Zhang S, Tian B, Zhang Y, Liu Z. The influence of surface chemistry and size of nanoscale graphene oxide on photothermal therapy of cancer using ultra-low laser power. Biomaterials 33(7), 2206–2214 (2012).
    • 19 Xu H, Fan M, Elhissi AMA et al. PEGylated graphene oxide for tumor-targeted delivery of paclitaxel. Nanomedicine 10(8), 1247–1262 (2015).
    • 20 Lee JH, Sahu A, Jang C, Tae G. The effect of ligand density on in vivo tumor targeting of nanographene oxide. J. Control. Release 209, 219–228 (2015).
    • 21 Robinson JT, Tabakman SM, Liang Y et al. Ultrasmall reduced graphene oxide with high near-infrared absorbance for photothermal therapy. J. Am. Chem. Soc. 133(17), 6825–6831 (2011). • Research article describing the therapeutic potential of reduced nanographene oxide.
    • 22 Akhavan O, Ghaderi E, Emamy H. Nontoxic concentrations of PEGylated graphene nanoribbons for selective cancer cell imaging and photothermal therapy. J. Mater. Chem. 22(38), 20626–20633 (2012).
    • 23 Zhang L, Wang Z, Lu Z et al. PEGylated reduced graphene oxide as a superior ssRNA delivery system. J. Mater. Chem. B 1(6), 749–755 (2013).
    • 24 Akhavan O, Ghaderi E. Graphene nanomesh promises extremely efficient in vivo photothermal therapy. Small 9(21), 3593–3601 (2013).
    • 25 Akhavan O, Meidanchi A, Ghaderi E, Khoei S. Zinc ferrite spinel-graphene in magneto-photothermal therapy of cancer. J. Mater. Chem. B 2(21), 3306–3314 (2014).
    • 26 Zhang Z, Tan S, Feng S-S, Vitamin E. TPGS as a molecular biomaterial for drug delivery. Biomaterials 33(19), 4889–4906 (2012). • Comprehensive review describing the diverse applications of D-α-tocopheryl polyethylene glycol 1000 succinate in cancer therapy.
    • 27 Zhu D, Tao W, Zhang H et al. Docetaxel (DTX)-loaded polydopamine-modified TPGS-PLA nanoparticles as a targeted drug delivery system for the treatment of liver cancer. Acta Biomater. 30, 144–154 (2016).
    • 28 Kutty RV, Chia SL, Setyawati MI, Muthu MS, Feng S-S, Leong DT. In vivo and ex vivo proofs of concept that cetuximab conjugated vitamin E TPGS micelles increases efficacy of delivered docetaxel against triple negative breast cancer. Biomaterials 63, 58–69 (2015).
    • 29 Tao W, Zhang J, Zeng X et al. Blended nanoparticle system based on miscible structurally similar polymers: a safe, simple, targeted, and surprisingly high efficiency vehicle for cancer therapy. Adv. Healthcare Mater. 4(8), 1203–1214 (2015).
    • 30 Mi Y, Zhao J, Feng S-S. Targeted co-delivery of docetaxel, cisplatin and herceptin by vitamin E TPGS-cisplatin prodrug nanoparticles for multimodality treatment of cancer. J. Control. Release 169(3), 185–192 (2013).
    • 31 Zhao J, Mi Y, Feng S-S. Targeted co-delivery of docetaxel and siPlk1 by herceptin-conjugated vitamin E TPGS-based immunomicelles. Biomaterials 34(13), 3411–3421 (2013).
    • 32 De Melo-Diogo D, Gaspar VM, Costa EC et al. Combinatorial delivery of crizotinib–palbociclib–sildenafil using TPGS-PLA micelles for improved cancer treatment. Eur. J. Pharm. Biopharm. 88(3), 718–729 (2014).
    • 33 Muthu MS, Avinash Kulkarni S, Liu Y, Feng S-S. Development of docetaxel-loaded vitamin E TPGS micelles: formulation optimization, effects on brain cancer cells and biodistribution in rats. Nanomedicine 7(3), 353–364 (2012).
    • 34 Gaspar VM, Moreira AF, Costa EC et al. Gas-generating TPGS-PLGA microspheres loaded with nanoparticles (NIMPS) for co-delivery of minicircle DNA and anti-tumoral drugs. Colloids Surf. B 134, 287–294 (2015).
    • 35 Tian G, Zheng X, Zhang X et al. TPGS-stabilized NaYbF4: Er upconversion nanoparticles for dual-modal fluorescent/CT imaging and anticancer drug delivery to overcome multi-drug resistance. Biomaterials 40, 107–116 (2015).
    • 36 Singh RP, Sharma G, Singh S et al. Vitamin E TPGS conjugated carbon nanotubes improved efficacy of docetaxel with safety for lung cancer treatment. Colloids Surf. B 141, 429–442 (2016).
    • 37 Duhem N, Danhier F, Préat V. Vitamin E-based nanomedicines for anti-cancer drug delivery. J. Control. Release 182, 33–44 (2014).
    • 38 Neophytou CM, Constantinou C, Papageorgis P, Constantinou AI. D-alpha-tocopheryl polyethylene glycol succinate (TPGS) induces cell cycle arrest and apoptosis selectively in survivin-overexpressing breast cancer cells. Biochem. Pharmacol. 89(1), 31–42 (2014). • Research article describing the effect of D-α-tocopheryl polyethylene glycol 1000 succinate in breast cancer cells.
    • 39 Huang NM, Lim HN, Chia CH, Yarmo MA, Muhamad MR. Simple room-temperature preparation of high-yield large-area graphene oxide. Int. J. Nanomed. 6, 3443–3448 (2011).
    • 40 Thomas HR, Day SP, Woodruff WE et al. Deoxygenation of graphene oxide: reduction or cleaning? Chem. Mater. 25(18), 3580–3588 (2013).
    • 41 Antaris AL, Robinson JT, Yaghi OK et al. Ultra-low doses of chirality sorted (6, 5) carbon nanotubes for simultaneous tumor imaging and photothermal therapy. ACS Nano 7(4), 3644–3652 (2013).
    • 42 Chen J, Wang X, Chen T. Facile and green reduction of covalently PEGylated nanographene oxide via a ‘water-only'route for high-efficiency photothermal therapy. Nanoscale Res. Lett. 9(1), 86 (2014).
    • 43 Gaspar VM, Baril P, Costa EC et al. Bioreducible poly(2-ethyl-2-oxazoline)–PLA–PEI-SS triblock copolymer micelles for co-delivery of DNA minicircles and Doxorubicin. J. Control. Release 213, 175–191 (2015).
    • 44 Gaspar VM, Gonçalves C, De Melo-Diogo D et al. Poly(2-ethyl-2-oxazoline)–PLA-g–PEI amphiphilic triblock micelles for co-delivery of minicircle DNA and chemotherapeutics. J. Control. Release 189, 90–104 (2014).
    • 45 Mou J, Li P, Liu C et al. Ultrasmall Cu2-xS nanodots for highly efficient photoacoustic imaging-guided photothermal therapy. Small 11(19), 2275–2283 (2015).
    • 46 Coluci VR, Martinez DSFT, HonóRio JG et al. Noncovalent interaction with graphene oxide: the crucial role of oxidative debris. J. Phys. Chem. C 118(4), 2187–2193 (2014).
    • 47 Ma D, Dong L, Zhou M, Zhu L. The influence of oxidation debris containing in graphene oxide on the adsorption and electrochemical properties of 1,10-phenanthroline-5,6-dione. Analyst 141(9), 2761–2766 (2016).
    • 48 Kulkarni SA, Feng S-S. Effects of particle size and surface modification on cellular uptake and biodistribution of polymeric nanoparticles for drug delivery. Pharm. Res. 30(10), 2512–2522 (2013).
    • 49 Chu KF, Dupuy DE. Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat. Rev. Cancer 14(3), 199–208 (2014).
    • 50 Kiew SF, Kiew LV, Lee HB, Imae T, Chung LY. Assessing biocompatibility of graphene oxide-based nanocarriers: a review. J. Control. Release 226, 217–228 (2016).
    • 51 Akhavan O, Ghaderi E, Emamy H, Akhavan F. Genotoxicity of graphene nanoribbons in human mesenchymal stem cells. Carbon 54, 419–431 (2013).
    • 52 Akhavan O, Ghaderi E, Akhavan A. Size-dependent genotoxicity of graphene nanoplatelets in human stem cells. Biomaterials 33(32), 8017–8025 (2012).
    • 53 Zhang H, Peng C, Yang J et al. Uniform ultrasmall graphene oxide nanosheets with low cytotoxicity and high cellular uptake. ACS Appl. Mater. Interfaces 5(5), 1761–1767 (2013).
    • 54 Chang Y, Yang S-T, Liu J-H et al. In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol. Lett. 200(3), 201–210 (2011).
    • 55 Pattammattel A, Williams CL, Pande P, Tsui WG, Basu AK, Kumar CV. Biological relevance of oxidative debris present in as-prepared graphene oxide. RSC Adv. 5(73), 59364–59372 (2015).
    • 56 Cheng C, Nie S, Li S et al. Biopolymer functionalized reduced graphene oxide with enhanced biocompatibility via mussel inspired coatings/anchors. J. Mater. Chem. B 1(3), 265–275 (2013).
    • 57 Akhavan O, Ghaderi E, Aghayee S, Fereydooni Y, Talebi A. The use of a glucose-reduced graphene oxide suspension for photothermal cancer therapy. J. Mater. Chem. 22(27), 13773–13781 (2012).
    • 58 Khare V, Sakarchi WA, Gupta PN, Curtis AD, Hoskins C. Synthesis and characterization of TPGS–gemcitabine prodrug micelles for pancreatic cancer therapy. RSC Adv. 6(65), 60126–60137 (2016).
    • 59 Yu P, Yu H, Guo C et al. Reversal of doxorubicin resistance in breast cancer by mitochondria-targeted pH-responsive micelles. Acta Biomater. 14, 115–124 (2015).
    • 60 Bernabeu E, Gonzalez L, Cagel M, Gergic EP, Moretton MA, Chiappetta DA. Novel Soluplus®–TPGS mixed micelles for encapsulation of paclitaxel with enhanced in vitro cytotoxicity on breast and ovarian cancer cell lines. Colloids Surf. B 140, 403–411 (2016).
    • 61 Bao Y, Yin M, Hu X et al. A safe, simple and efficient doxorubicin prodrug hybrid micelle for overcoming tumor multidrug resistance and targeting delivery. J. Control. Release 235, 182–194 (2016).
    • 62 Salvati A, Pitek AS, Monopoli MP et al. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat. Nanotechnol. 8(2), 137–143 (2013).
    • 63 Bani F, Adeli M, Movahedi S, Sadeghizadeh M. Graphene-polyglycerol-curcumin hybrid as a near-infrared (NIR) laser stimuli-responsive system for chemo-photothermal cancer therapy. RSC Adv. 6(66), 61141–61149 (2016).
    • 64 Kim SH, Lee JE, Sharker SM, Jeong JH, In I, Park SY. In vitro and in vivo tumor targeted photothermal cancer therapy using functionalized graphene nanoparticles. Biomacromolecules 16(11), 3519–3529 (2015).
    • 65 Tran TH, Nguyen HT, Pham TT et al. Development of a graphene oxide nanocarrier for dual-drug chemo-phototherapy to overcome drug resistance in cancer. ACS Appl. Mater. Interfaces 7(51), 28647–28655 (2015).
    • 66 Markovic ZM, Harhaji-Trajkovic LM, Todorovic-Markovic BM et al. In vitro comparison of the photothermal anticancer activity of graphene nanoparticles and carbon nanotubes. Biomaterials 32(4), 1121–1129 (2011).
    • 67 Qin X, Guo Z, Liu Z, Zhang W, Wan M, Yang B. Folic acid-conjugated graphene oxide for cancer targeted chemo-photothermal therapy. J. Photochem. Photobiol., B 120, 156–162 (2013).
    • 68 Zhang W, Guo Z, Huang D, Liu Z, Guo X, Zhong H. Synergistic effect of chemo-photothermal therapy using PEGylated graphene oxide. Biomaterials 32(33), 8555–8561 (2011).
    • 69 Yang H-W, Lu Y-J, Lin K-J et al. EGRF conjugated PEGylated nanographene oxide for targeted chemotherapy and photothermal therapy. Biomaterials 34(29), 7204–7214 (2013).