Multifunctional carbon-coated magnetic sensing graphene oxide-cyclodextrin nanohybrid for potential cancer theranosis
Source abstract
Abstract
We functionalized graphene oxide (GO) with cyclodextrin (CD) to increase the drug loading and cellular uptake of GO, and bound the GO-CD to carbon-coated iron nanoparticles (Fe@C) with superparamagnetic properties for potential magnetic-directed drug delivery and as a diagnostic agent. The GO-CD/Fe@C was loaded with an anticancer drug, doxorubicin (DOX), to form a multifunctional GO-CD/Fe@C/DOX nanohybrid. A cumulative increase in DOX loading was observed probably due to DOX adsorption to the graphitic domains in Fe@C and also to the GO-CD. In acidic pH that resembles the pH of the tumor environment, a higher amount of DOX was released from the GO-CD/Fe@C/DOX nanohybrid when compared to the amount released at physiological pH. The signal intensity and the contrast enhancement in magnetic resonance imaging of Fe@C decreased with its concentration. Besides, the cellular uptake of GO-CD/Fe@C/DOX nanohybrid was significantly higher by 2.5-fold than that of Fe@C/DOX in MDA-MB-231 human breast cancer model. The nanohybrids were internalized into the tumor cells via an energy-dependent process and localized mainly in the nuclei, where it exerts its cytotoxic effect, and some in the lysosomes and mitochondria. This has resulted in significant cytotoxicity in tumor cells treated with GO-CD/Fe@C/DOX. These findings highlight the potential use of multifunctional GO-CD/Fe@C nanohybrid for magnetic sensing anticancer drug delivery to tumor cells.
Source: openaire · Quality: candidate unverified · Source record ↗
Research context
OpenAlex topics: Graphene and Nanomaterials Applications · Nanoparticle-Based Drug Delivery · Graphene research and applications
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (59)
Show source-provided references
1. Aguiló-Aguayo N, Inestrosa-Izurieta M, García-Céspedes J, Bertran E (2010) Morphological and magnetic properties of superparamagnetic carbon-coated Fe nanoparticles produced by arc discharge. J Nanosci Nanotechnol 10:2646–2649. https://doi.org/10.1166/jnn.2010.142010.1166/jnn.2010.1420 ↗
2. Alexiou C, Arnold W, Klein RJ, Parak FG, Hulin P, Bergemann C, Erhardt W, Wagenpfeil S, Lubbe AS (2000) Locoregional cancer treatment with magnetic drug targeting. Cancer Res 60:6641–6648
3. Aroui S, Ram N, Appaix F, Ronjat M, Kenani A, Pirollet F, De Waard M (2009) Maurocalcine as a non toxic drug carrier overcomes doxorubicin resistance in the cancer cell line MDA-MB 231. Pharm Res 26:836–845. https://doi.org/10.1007/s11095-008-9782-110.1007/s11095-008-9782-1 ↗
4. Bae H, Ahmad T, Rhee I, Chang Y, Jin SU, Hong S (2012) Carbon-coated iron oxide nanoparticles as contrast agents in magnetic resonance imaging. Nanoscale Res Lett 7:44. https://doi.org/10.1186/1556-276x-7-4410.1186/1556-276x-7-44 ↗
5. Bandara NA, Hansen MJ, Low PS (2014) Effect of receptor occupancy on folate receptor internalization. Mol Pharm 11:1007–1013. https://doi.org/10.1021/mp400659t10.1021/mp400659t ↗
6. Brumlik MJ, Daniel BJ, Waehler R, Curiel DT, Giles FJ, Curiel TJ (2008) Trends in immunoconjugate and ligand-receptor based targeting development for cancer therapy. Expert Opin Drug Deliv 5:87–103. https://doi.org/10.1517/17425247.5.1.8710.1517/17425247.5.1.87 ↗
7. Busquets J, Del Galdo F, Kissin EY, Jimenez SA (2010) Assessment of tissue fibrosis in skin biopsies from patients with systemic sclerosis employing confocal laser scanning microscopy: an objective outcome measure for clinical trials? Rheumatology (Oxford, England) 49:1069–1075. https://doi.org/10.1093/rheumatology/keq02410.1093/rheumatology/keq024 ↗
8. Chakraborty A, Jana NR (2015) Clathrin to lipid raft-endocytosis via controlled surface chemistry and efficient perinuclear targeting of nanoparticle. J Phys Chem Lett 6:3688–3697. https://doi.org/10.1021/acs.jpclett.5b0173910.1021/acs.jpclett.5b01739 ↗
9. Chomoucka J, Drbohlavova J, Huska D, Adam V, Kizek R, Hubalek J (2010) Magnetic nanoparticles and targeted drug delivering. Pharmacol Res 62:144–149. https://doi.org/10.1016/j.phrs.2010.01.01410.1016/j.phrs.2010.01.014 ↗
10. Cortés-Funes H, Coronado C (2007) Role of anthracyclines in the era of targeted therapy. Cardiovasc Toxicol 7:56–60. https://doi.org/10.1007/s12012-007-0015-310.1007/s12012-007-0015-3 ↗
11. Das M, Mohanty C, Sahoo SK (2009) Ligand-based targeted therapy for cancer tissue. Expert Opin Drug Deliv 6:285–304. https://doi.org/10.1517/1742524090278016610.1517/17425240902780166 ↗
12. Fan J, Park H, Tan S, Lee M (2013) Enhanced osteogenesis of adipose derived stem cells with Noggin suppression and delivery of BMP-2. PLoS One 8:e72474. https://doi.org/10.1371/journal.pone.007247410.1371/journal.pone.0072474 ↗
13. Fernández-Pacheco R, Ibarra MR, Valdivia JG, Marquina C, Serrate D, Romero MS (2005) Carbon coated magnetic nanoparticles for local drug delivery using magnetic implants. NanoBiotechnology 1:300–303. https://doi.org/10.1007/s12030-005-0051-710.1007/s12030-005-0051-7 ↗
14. Gouaze-Andersson V, Yu JY, Kreitenberg AJ, Bielawska A, Giuliano AE, Cabot MC (2007) Ceramide and glucosylceramide upregulate expression of the multidrug resistance gene MDR1 in cancer cells. Biochim Biophys Acta 1771:1407–1417. https://doi.org/10.1016/j.bbalip.2007.09.00510.1016/j.bbalip.2007.09.005 ↗
15. Himaja A, Karthik P, Singh SP (2015) Carbon dots: the newest member of the carbon nanomaterials family. Chem Rec 15:595–615. https://doi.org/10.1002/tcr.20140209010.1002/tcr.201402090 ↗
16. Hubbell JA, Chilkoti A (2012) Nanomaterials for drug delivery. Science 337:303–305. https://doi.org/10.1126/science.121965710.1126/science.1219657 ↗
17. Jusin JW, Aziz M, Sean GP, Jaafar J (2016) Preparation and characterization of graphene-based magnetic hybrid nanocomposite. Malaysian J Anal Sci 20:149–156. 10.17576/mjas-2016-2001-1610.17576/mjas-2016-2001-16 ↗
18. Kiew SF, Kiew LV, Lee HB, Imae T, Chung LY (2016) Assessing biocompatibility of graphene oxide-based nanocarriers: a review. J Control Release 226:217–228. https://doi.org/10.1016/j.jconrel.2016.02.01510.1016/j.jconrel.2016.02.015 ↗
19. Kobayashi T, Kakimi K, Nakayama E, Jimbow K (2014) Antitumor immunity by magnetic nanoparticle-mediated hyperthermia. Nanomed 9:1715–1726. https://doi.org/10.2217/nnm.14.10610.2217/nnm.14.106 ↗
20. Konkena B, Vasudevan S (2012a) Covalently linked, water-dispersible, cyclodextrin: reduced-graphene oxide sheets. Langmuir 28:12432–12437. https://doi.org/10.1021/la302078310.1021/la3020783 ↗
21. Konkena B, Vasudevan S (2012b) Understanding aqueous dispersibility of graphene oxide and reduced graphene oxide through pKa measurements. J Phys Chem Lett 3:867–872. https://doi.org/10.1021/jz300236w10.1021/jz300236w ↗
22. Kou L, Sun J, Zhai Y, He Z (2013) The endocytosis and intracellular fate of nanomedicines: implication for rational design. Asian J Pharm Sci 8:1–10. https://doi.org/10.1016/j.ajps.2013.07.00110.1016/j.ajps.2013.07.001 ↗
23. Krishnakumar B, Imae T, Miras J, Esquena J (2014) Synthesis and azo dye photodegradation activity of ZrS 2–ZnO nano-composites. Sep Purif Technol 132:281–288. https://doi.org/10.1016/j.seppur.2014.05.01810.1016/j.seppur.2014.05.018 ↗
24. Kue CS, Kamkaew A, Burgess K, Kiew LV, Chung LY, Lee HB (2016) Small molecules for active targeting in cancer. Med Res Rev 36:494–575. https://doi.org/10.1002/med.2138710.1002/med.21387 ↗
25. Liu G, Shen H, Mao J, Zhang L, Jiang Z, Sun T, Lan Q, Zhang Z (2013) Transferrin modified graphene oxide for glioma-targeted drug delivery: in vitro and in vivo evaluations. ACS Appl Mater Interfaces 5:6909–6914. https://doi.org/10.1021/am402128s10.1021/am402128s ↗
26. Liu Z, Robinson JT, Sun X, Dai H (2008) PEGylated nanographene oxide for delivery of water-insoluble cancer drugs. J Am Chem Soc 130:10876–10877. https://doi.org/10.1021/ja803688x10.1021/ja803688x ↗
27. Ma X, Tao H, Yang K, Feng L, Cheng L, Shi X, Li Y, Guo L, Liu Z (2012) A functionalized graphene oxide-iron oxide nanocomposite for magnetically targeted drug delivery, photothermal therapy, and magnetic resonance imaging. Nano Res 5:199–212. https://doi.org/10.1007/s12274-012-0200-y10.1007/s12274-012-0200-y ↗
28. Mahajan S, Koul V, Choudhary V, Shishodia G, Bharti AC (2013) Preparation and in vitro evaluation of folate-receptor-targeted SPION-polymer micelle hybrids for MRI contrast enhancement in cancer imaging. Nanotechnology 24:015603. https://doi.org/10.1088/0957-4484/24/1/01560310.1088/0957-4484/24/1/015603 ↗
29. Mody VV, Cox A, Shah S, Singh A, Bevins W, Parihar H (2013) Magnetic nanoparticle drug delivery systems for targeting tumor. Appl Nanosci 4:385–392. https://doi.org/10.1007/s13204-013-0216-y10.1007/s13204-013-0216-y ↗
30. Narayanan T, Liu Z, Lakshmy PR, Gao W, Nagaoka Y, Kumar DS, Lou J, Vajtai R, Ajayan PM (2012) Synthesis of reduced graphene oxide–Fe 3 O 4 multifunctional freestanding membranes and their temperature dependent electronic transport properties. Carbon 50:1338–1345. https://doi.org/10.1016/j.carbon.2011.11.00510.1016/j.carbon.2011.11.005 ↗
31. Nawara K, Romiszewski J, Kijewska K, Szczytko J, Twardowski A, Mazur M, Krysinski P (2012) Adsorption of doxorubicin onto citrate-stabilized magnetic nanoparticles. J Phys Chem C 116:5598–5609. https://doi.org/10.1021/jp209527810.1021/jp2095278 ↗
32. Ohashi H, Hiraoka Y, Yamaguchi T (2006) An autonomous phase transition−complexation/decomplexation polymer system with a molecular recognition property. Macromolecules 39:2614–2620. https://doi.org/10.1021/ma052509q10.1021/ma052509q ↗
33. Paredes JI, Villar-Rodil S, Martínez-Alonso A, Tascón JMD (2008) Graphene oxide dispersions in organic solvents. Langmuir 24:10560–10564. https://doi.org/10.1021/la801744a10.1021/la801744a ↗
34. Paulos CM, Reddy JA, Leamon CP, Turk MJ, Low PS (2004) Ligand binding and kinetics of folate receptor recycling in vivo: impact on receptor-mediated drug delivery. Mol Pharmacol 66:1406–1414. https://doi.org/10.1124/mol.104.00372310.1124/mol.104.003723 ↗
35. Popplewell J, Sakhnini L (1995) The dependence of the physical and magnetic properties of magnetic fluids on particle size. J Magn Magn Mater 149:72–78. https://doi.org/10.1016/0304-8853(95)00341-X10.1016/0304-8853(95)00341-X ↗
36. Prasannan A, Imae T (2013) One-pot synthesis of fluorescent carbon dots from orange waste peels. Ind Eng Chem Res 52:15673–15678. https://doi.org/10.1021/ie402421s10.1021/ie402421s ↗
37. Rosická D, Šembera J (2011) Influence of structure of iron nanoparticles in aggregates on their magnetic properties. Nanoscale Res Lett 6:527. https://doi.org/10.1186/1556-276X-6-52710.1186/1556-276X-6-527 ↗
38. Rudge SR, Kurtz TL, Vessely CR, Catterall LG, Williamson DL (2000) Preparation, characterization, and performance of magnetic iron–carbon composite microparticles for chemotherapy. Biomaterials 21:1411–1420. https://doi.org/10.1016/S0142-9612(00)00006-510.1016/S0142-9612(00)00006-5 ↗
39. Shen J, Hu Y, Shi M, Li N, Ma H, Ye M (2010) One step synthesis of graphene oxide−magnetic nanoparticle composite. J Phys Chem C 114:1498–1503. https://doi.org/10.1021/jp909756r10.1021/jp909756r ↗
40. Shi J, Wang L, Zhang J, Ma R, Gao J, Liu Y, Zhang C, Zhang Z (2014) A tumor-targeting near-infrared laser-triggered drug delivery system based on GO@Ag nanoparticles for chemo-photothermal therapy and X-ray imaging. Biomaterials 35:5847–5861. https://doi.org/10.1016/j.biomaterials.2014.03.04210.1016/j.biomaterials.2014.03.042 ↗
41. Shroff K, Kokkoli E (2012) PEGylated liposomal doxorubicin targeted to alpha5beta1-expressing MDA-MB-231 breast cancer cells. Langmuir 28:4729–4736. https://doi.org/10.1021/la204466g10.1021/la204466g ↗
42. Siriviriyanun A, Popova M, Imae T, Kiew LV, Looi CY, Wong WF, Lee HB, Chung LY (2015) Preparation of graphene oxide/dendrimer hybrid carriers for delivery of doxorubicin. Chem Eng J 281:771–781. https://doi.org/10.1016/j.cej.2015.07.02410.1016/j.cej.2015.07.024 ↗
43. Smith L, Watson MB, O'Kane SL, Drew PJ, Lind MJ, Cawkwell L (2006) The analysis of doxorubicin resistance in human breast cancer cells using antibody microarrays. Mol Cancer Ther 5:2115–2120. https://doi.org/10.1158/1535-7163.mct-06-019010.1158/1535-7163.mct-06-0190 ↗
44. Sun Y-P, Li X-q, Cao J, Zhang W-x, Wang HP (2006) Characterization of zero-valent iron nanoparticles. Adv Colloid Interf Sci 120:47–56. https://doi.org/10.1016/j.cis.2006.03.00110.1016/j.cis.2006.03.001 ↗
45. Tannock IF, Rotin D (1989) Acid pH in tumors and its potential for therapeutic exploitation. Cancer Res 49:4373–4384
46. Terzyk AP (2001) The influence of activated carbon surface chemical composition on the adsorption of acetaminophen (paracetamol) in vitro: part II. TG, FTIR, and XPS analysis of carbons and the temperature dependence of adsorption kinetics at the neutral pH. Colloids Surf Physicochem Eng Aspects 177:23–45. https://doi.org/10.1016/S0927-7757(00)00594-X10.1016/S0927-7757(00)00594-X ↗
47. Thomas RG, Moon MJ, Lee H, Sasikala AR, Kim CS, Park IK, Jeong YY (2015) Hyaluronic acid conjugated superparamagnetic iron oxide nanoparticle for cancer diagnosis and hyperthermia therapy. Carbohydr Polym 131:439–446. https://doi.org/10.1016/j.carbpol.2015.06.01010.1016/j.carbpol.2015.06.010 ↗
48. Thorn CF, Oshiro C, Marsh S, Hernandez-Boussard T, McLeod H, Klein TE, Altman RB (2011) Doxorubicin pathways: pharmacodynamics and adverse effects. Pharmacogenet Genomics 21:440–446. https://doi.org/10.1097/FPC.0b013e32833ffb5610.1097/FPC.0b013e32833ffb56 ↗
49. Thurn KT, Arora H, Paunesku T, Wu A, Brown EMB, Doty C, Kremer J, Woloschak G (2011) Endocytosis of titanium dioxide nanoparticles in prostate cancer PC-3M cells. Nanomed Nanotechnol 7:123–130. https://doi.org/10.1016/j.nano.2010.09.00410.1016/j.nano.2010.09.004 ↗
50. Tourinho F, Franck R, Massart R, Perzynski R (1989) Synthesis and mangeitc properties of managanese and cobalt ferrite ferrite ferrofluids. In: Bothorel P, Dufourc EJ (eds) Trends in colloid and Interface science III. Steinkopff, Darmstadt, pp 128–134. https://doi.org/10.1007/BFb011619810.1007/BFb0116198 ↗
51. Vermisoglou E, Devlin E, Giannakopoulou T, Romanos G, Boukos N, Psycharis V, Lei C, Lekakou C, Petridis D, Trapalis C (2014) Reduced graphene oxide/iron carbide nanocomposites for magnetic and supercapacitor applications. J Alloys Compd 590:102–109. https://doi.org/10.1016/j.jallcom.2013.11.08710.1016/j.jallcom.2013.11.087 ↗
52. Viswanathan G, Hsu Y-H, Voon SH, Imae T, Siriviriyanun A, Lee HB, Kiew LV, Chung LY, Yusa S-I (2016) A comparative study of cellular uptake and subcellular localization of doxorubicin loaded in self-assemblies of amphiphilic copolymers with pendant Dendron by MDA-MB-231 human breast cancer cells. Macromol Biosci 16:882–895. https://doi.org/10.1002/mabi.20150043510.1002/mabi.201500435 ↗
53. Voon SH, Kiew LV, Lee HB, Lim SH, Noordin MI, Kamkaew A, Burgess K, Chung LY (2014) In vivo studies of nanostructure-based photosensitizers for photodynamic cancer therapy. Small 10:4993–5013. https://doi.org/10.1002/smll.20140141610.1002/smll.201401416 ↗
54. Wang C, Li B, Niu W, Hong S, Saif B, Wang S, Dong C, Shuang S (2015a) β-Cyclodextrin modified graphene oxide–magnetic nanocomposite for targeted delivery and pH-sensitive release of stereoisomeric anti-cancer drugs. RSC Adv 5:89299–89308. https://doi.org/10.1039/C5RA13082D10.1039/C5RA13082D ↗
55. Wang Q, Zhou L, Qiu L, Lu D, Wu Y, Zhang X-B (2015b) An efficient ratiometric fluorescent probe for tracking dynamic changes in lysosomal pH. Analyst 140:5563–5569. https://doi.org/10.1039/C5AN00683J10.1039/C5AN00683J ↗
56. Wu A, Loutherback K, Lambert G, Estévez-Salmerón L, Tlsty TD, Austin RH, Sturm JC (2013) Cell motility and drug gradients in the emergence of resistance to chemotherapy. Proc Natl Acad Sci U S A 110:16103–16108. https://doi.org/10.1073/pnas.131438511010.1073/pnas.1314385110 ↗
57. Yang X, Wang Y, Huang X, Ma Y, Huang Y, Yang R, Duan H, Chen Y (2011) Multi-functionalized graphene oxide based anticancer drug-carrier with dual-targeting function and pH-sensitivity. J Mater Chem 21:3448–3454. https://doi.org/10.1039/C0JM02494E10.1039/C0JM02494E ↗
58. Yu D, Yang Y, Durstock M, Baek J-B, Dai L (2010) Soluble P3HT-grafted graphene for efficient bilayer−heterojunction photovoltaic devices. ACS Nano 4:5633–5640. https://doi.org/10.1021/nn101671t10.1021/nn101671t ↗
59. Zhang L, Xia J, Zhao Q, Liu L, Zhang Z (2010) Functional graphene oxide as a nanocarrier for controlled loading and targeted delivery of mixed anticancer drugs. Small 6:537–544. https://doi.org/10.1002/smll.20090168010.1002/smll.200901680 ↗