Low levels of graphene and graphene oxide inhibit cellular xenobiotic defense system mediated by efflux transporters

References

• Akhavan O, Ghaderi E. 2010. Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano 4:5731–6
   PubMed Web of Science ®Google Scholar
• Arias A, Rigalli JP, Villanueva SSM, Ruiz ML, Luquita MG, Perdomo VG, et al. 2014. Regulation of expression and activity of multidrug resistance proteins MRP2 and MDR1 by estrogenic compounds in Caco-2 cells. Role in prevention of xenobiotic-induced cytotoxicity. Toxicology 320:46–55
   PubMed Web of Science ®Google Scholar
• Auzmendi JA, Orozco-Suarez S, Banuelos-Cabrera I, Gonzalez-Trujano ME, Calixto Gonzalez E, Rocha L, et al. 2013. P-glycoprotein contributes to cell membrane depolarization of hippocampus and neocortex in a model of repetitive seizures induced by pentylenetetrazole in rats. Curr Pharm Des 19:6732–8
   PubMed Web of Science ®Google Scholar
• Buss DS, Callaghan A. 2008. Interaction of pesticides with p-glycoprotein and other ABC proteins: a survey of the possible importance to insecticide, herbicide and fungicide resistance. Pestic Biochem Physiol 90:141–53
   Web of Science ®Google Scholar
• Byrd TF, Hoang LT, Kim EG, Pfister ME, Werner EM, Arndt SE, et al. 2014. The microfluidic multitrap nanophysiometer for hematologic cancer cell characterization reveals temporal sensitivity of the calcein-AM efflux assay. Sci Rep 4:5117
   PubMed Web of Science ®Google Scholar
• Chang Y, Yang ST, Liu JH, Dong E, Wang Y, Cao A, et al. 2011. In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol Lett 200:201–10
   PubMed Web of Science ®Google Scholar
• Chung C, Kim YK, Shin D, Ryoo SR, Hong BH, Min DH. 2013. Biomedical applications of graphene and graphene oxide. Acc Chem Res 46:2211–24
   PubMed Web of Science ®Google Scholar
• Cole BJ, Hamdoun A, Epel D. 2013. Cost, effectiveness and environmental relevance of multidrug transporters in sea urchin embryos. J Exp Biol 216:3896–905
   PubMed Web of Science ®Google Scholar
• Csoboz B, Balogh GE, Kusz E, Gombos I, Peter M, Crul T, et al. 2013. Membrane fluidity matters: hyperthermia from the aspects of lipids and membranes. Int J Hyperthermia 29:491–9
   PubMed Web of Science ®Google Scholar
• Dean M, Rzhetsky A, Allikmets R. 2001. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11:1156–66
   PubMed Web of Science ®Google Scholar
• Drori S, Eytan GD, Assaraf YG. 1995. Potentiation of anticancer-drug cytotoxicity by multidrug-resistance chemosensitizers involves alterations in membrane fluidity leading to increased membrane permeability. Eur J Biochem 228:1020–9
   PubMedGoogle Scholar
• Epel D, Luckenbach T, Stevenson CN, Macmanus-Spencer LA, Hamdoun A, Smital T. 2008. Efflux transporters: newly appreciated roles in protection against pollutants. Environ Sci Technol 42:3914–20
   PubMed Web of Science ®Google Scholar
• George S, Lin S, Ji Z, Thomas CR, Li L, Mecklenburg M, et al. 2012. Surface defects on plate-shaped silver nanoparticles contribute to its hazard potential in a fish gill cell line and zebrafish embryos. ACS Nano 6:3745–59
   PubMed Web of Science ®Google Scholar
• Gokirmak T, Campanale JP, Shipp LE, Moy GW, Tao H, Hamdoun A. 2012. Localization and substrate selectivity of sea urchin multidrug (MDR) efflux transporters. J Biol Chem 287:43876–83
   PubMed Web of Science ®Google Scholar
• Gokirmak T, Shipp LE, Campanale JP, Nicklisch SCT, Hamdoun A. 2014. Transport in technicolor: mapping ATP-binding cassette transporters in sea urchin embryos. Mol Reprod Dev 81:778–93
   PubMed Web of Science ®Google Scholar
• Gottesman MM, Fojo T, Bates SE. 2002. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2:48–58
   PubMed Web of Science ®Google Scholar
• Guo X, Mei N. 2014. Assessment of the toxic potential of graphene family nanomaterials. J Food Drug Anal 22:105–15
   PubMed Web of Science ®Google Scholar
• Gurunathan S, Han JW, Eppakayala V, Kim JH. 2013. Green synthesis of graphene and its cytotoxic effects in human breast cancer cells. Int J Nanomedicine 8:1015–27
   PubMed Web of Science ®Google Scholar
• Hamdoun AM, Cherr GN, Roepke TA, Epel D. 2004. Activation of multidrug efflux transporter activity at fertilization in sea urchin embryos (Strongylocentrotus purpuratus). Dev Biol 276:452–62
   PubMed Web of Science ®Google Scholar
• Hu WB, Peng C, Luo WJ, Lv M, Li XM, Li D, et al. 2010. Graphene-based antibacterial paper. ACS Nano 4:4317–23
   PubMed Web of Science ®Google Scholar
• Huffer S, Clark ME, Ning JC, Blanch HW, Clark DS. 2011. Role of alcohols in growth, lipid composition, and membrane fluidity of yeasts, bacteria, and archaea. Appl Environ Microbiol 77:6400–8
   PubMed Web of Science ®Google Scholar
• Hummel I, Klappe K, Ercan C, Kok JW. 2011. Multidrug resistance-related protein 1 (MRP1) function and localization depend on cortical actin. Mol Pharmacol 79:229–40
   PubMed Web of Science ®Google Scholar
• Hussain S, Al-Nsour F, Rice AB, Marshburn J, Yingling B, Ji Z, et al. 2012. Cerium dioxide nanoparticles induce apoptosis and autophagy in human peripheral blood monocytes. ACS Nano 6:5820–9
   PubMed Web of Science ®Google Scholar
• Jaworski S, Sawosz E, Grodzik M, Winnicka A, Prasek M, Wierzbicki M, et al. 2013. In vitro evaluation of the effects of graphene platelets on glioblastoma multiforme cells. Int J Nanomedicine 8:413–20
   PubMed Web of Science ®Google Scholar
• Kemp KC, Seema H, Saleh M, Le NH, Mahesh K, Chandra V, et al. 2013. Environmental applications using graphene composites: water remediation and gas adsorption. Nanoscale 5:3149–71
   PubMed Web of Science ®Google Scholar
• Lammel T, Boisseaux P, Fernandez-Cruz ML, Navas JM. 2013. Internalization and cytotoxicity of graphene oxide and carboxyl graphene nanoplatelets in the human hepatocellular carcinoma cell line Hep G2. Part Fibre Toxicol 10:27
   PubMed Web of Science ®Google Scholar
• Leslie EM, Deeley RG, Cole SPC. 2005. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204:216–37
   PubMed Web of Science ®Google Scholar
• Li JL, Tang B, Yuan B, Sun L, Wang XG. 2013. A review of optical imaging and therapy using nanosized graphene and graphene oxide. Biomaterials 34:9519–34
   PubMed Web of Science ®Google Scholar
• Li Y, Feng L, Shi X, Wang X, Yang Y, Yang K, et al. 2014a. Surface coating-dependent cytotoxicity and degradation of graphene derivatives: towards the design of non-toxic, degradable nano-graphene. Small 10:1544–54
   PubMed Web of Science ®Google Scholar
• Li Y, Wu Q, Zhao Y, Bai Y, Chen P, Xia T, et al. 2014b. Response of microRNAs to in vitro treatment with graphene oxide. ACS Nano 8:2100–10
   PubMed Web of Science ®Google Scholar
• Liu JQ, Cui L, Losic D. 2013. Graphene and graphene oxide as new nanocarriers for drug delivery applications. Acta Biomater 9:9243–57
   PubMed Web of Science ®Google Scholar
• Liu SB, Zeng TH, Hofmann M, Burcombe E, Wei J, Jiang RR, et al. 2011. Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: membrane and oxidative stress. ACS Nano 5:6971–80
   PubMed Web of Science ®Google Scholar
• Lu PH, Liu RH, Sharom FJ. 2001. Drug transport by reconstituted P-glycoprotein in proteoliposomes. Effect of substrates and modulators, and dependence on bilayer phase state. Eur J Biochem 268:1687–97
   PubMedGoogle Scholar
• Luckenbach T, Epel D. 2005. Nitromusk and polycyclic musk compounds as long-term Inhibitors of cellular xenobiotic defense systems mediated by multidrug transporters. Environ Health Perspect 113:17–24
   PubMed Web of Science ®Google Scholar
• Meszaros P, Hummel I, Klappe K, Draghiciu O, Hoekstra D, Kok JW. 2013. The function of the ATP-binding cassette (ABC) transporter ABCB1 is not susceptible to actin disruption. Biochim Biophys Acta Biomembr 1828:340–51
   PubMed Web of Science ®Google Scholar
• Mullick Chowdhury S, Lalwani G, Zhang K, Yang JY, Neville K, Sitharaman B. 2013. Cell specific cytotoxicity and uptake of graphene nanoribbons. Biomaterials 34:283–93
   PubMed Web of Science ®Google Scholar
• Na J, Kim W, Yoon BJ. 2014. Development of a novel screening system for allatostatin receptor agonists in search of new candidate insect growth regulators. Biotechnol Lett 36:1439–46
   PubMed Web of Science ®Google Scholar
• Ochoa-Puentes C, Bauer S, Kuhnle M, Bernhard G, Buschauer A, Konig B. 2013. Benzanilide-biphenyl replacement: a bioisosteric approach to quinoline carboxamide-type ABCG2 modulators. ACS Med Chem Lett 4:393–6
   PubMed Web of Science ®Google Scholar
• Pavlidis IV, Patila M, Bornscheuer UT, Gournis D, Stamatis H. 2014. Graphene-based nanobiocatalytic systems: recent advances and future prospects. Trends Biotechnol 32:312–20
   PubMed Web of Science ®Google Scholar
• Picone P, Nuzzo D, Di Carlo M. 2013. Ferulic acid: a natural antioxidant against oxidative stress induced by oligomeric A-beta on sea urchin embryo. Biol Bull 224:18–28
   PubMed Web of Science ®Google Scholar
• Sasidharan A, Panchakarla LS, Sadanandan AR, Ashokan A, Chandran P, Girish CM, et al. 2012. Hemocompatibility and macrophage response of pristine and functionalized graphene. Small 8:1251–63
   PubMed Web of Science ®Google Scholar
• Schinwald A, Murphy FA, Jones A, MacNee W, Donaldson K. 2012. Graphene-based nanoplatelets: a new risk to the respiratory system as a consequence of their unusual aerodynamic properties. ACS Nano 6:736–46
   PubMed Web of Science ®Google Scholar
• Seabra AB, Paula AJ, de Lima R, Alves OL, Duran N. 2014. Nanotoxicity of graphene and graphene oxide. Chem Res Toxicol 27:159–68
   PubMed Web of Science ®Google Scholar
• Sharma V, Anderson D, Dhawan A. 2012. Zinc oxide nanoparticles induce oxidative DNA damage and ROS-triggered mitochondria mediated apoptosis in human liver cells (HepG2). Apoptosis 17:852–70
   PubMed Web of Science ®Google Scholar
• Sreeprasad TS, Pradeep T. 2012. Graphene for environmental and biological applications. Int J Mod Phys B 26:1242001
   Web of Science ®Google Scholar
• Stankovich S, Dikin DA, Dommett GHB, Kohlhaas KM, Zimney EJ, Stach EA, et al. 2006. Graphene-based composite materials. Nature 442:282–6
   PubMed Web of Science ®Google Scholar
• Stoloff DH, Wanunu M. 2013. Recent trends in nanopores for biotechnology. Curr Opin Biotechnol 24:699–704
   PubMed Web of Science ®Google Scholar
• Tu Y, Lv M, Xiu P, Huynh T, Zhang M, Castelli M, et al. 2013. Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets. Nat Nanotechnol 8:594–601
   PubMed Web of Science ®Google Scholar
• Varadi T, Roszik J, Lisboa D, Vereb G, Molina-Guijarro JM, Galmarini CM, et al. 2011. ErbB protein modifications are secondary to severe cell membrane alterations induced by elisidepsin treatment. Eur J Pharmacol 667:91–9
   PubMed Web of Science ®Google Scholar
• Vernhet L, Allain N, Bardiau C, Anger JP, Fardel O. 2000. Differential sensitivities of MRP1-overexpressing lung tumor cells to cytotoxic metals. Toxicology 142:127–34
   PubMed Web of Science ®Google Scholar
• Wang AX, Pu KF, Dong B, Liu Y, Zhang LM, Zhang ZJ, et al. 2013. Role of surface charge and oxidative stress in cytotoxicity and genotoxicity of graphene oxide towards human lung fibroblast cells. J Appl Toxicol 33:1156–64
   PubMed Web of Science ®Google Scholar
• Wang Y, Li ZH, Wang J, Li JH, Lin YH. 2011. Graphene and graphene oxide: biofunctionalization and applications in biotechnology. Trends Biotechnol 29:205–12
   PubMed Web of Science ®Google Scholar
• Watanabe T, Hirano S. 2013. Metabolism of arsenic and its toxicological relevance. Arch Toxicol 87:969–79
   PubMed Web of Science ®Google Scholar
• Wu B, Torres-Duarte C, Cole BJ, Cherr GN. 2015. Copper oxide and zinc oxide nanomaterials act as inhibitors of multidrug resistance transport in sea urchin embryos: their role as chemosensitizers. Environ Sci Technol 49:5760–70
   PubMed Web of Science ®Google Scholar
• Yang K, Li Y, Tan X, Peng R, Liu Z. 2013. Behavior and toxicity of graphene and its functionalized derivatives in biological systems. Small 9:1492–503
   PubMed Web of Science ®Google Scholar
• Yuan JF, Gao HC, Sui JJ, Duan HW, Chen WN, Ching CB. 2012. Cytotoxicity evaluation of oxidized single-walled carbon nanotubes and graphene oxide on human hepatoma HepG2 cells: an iTRAQ-coupled 2D LC-MS/MS proteome analysis. Toxicol Sci 126:149–61
   PubMed Web of Science ®Google Scholar
• Zastre J, Jackson JK, Wong W, Burt HM. 2007. Methoxypolyethylene glycol-block-polycaprolactone diblock copolymers reduce P-glycoprotein efflux in the absence of a membrane fluidization effect while stimulating P-glycoprotein ATPase activity. J Pharm Sci 96:864–75
   PubMed Web of Science ®Google Scholar
• Zhang Y, Ali SF, Dervishi E, Xu Y, Li Z, Casciano D, et al. 2010. Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived PC12 cells. ACS Nano 4:3181–6
   PubMed Web of Science ®Google Scholar
• Zhu B, Xia X, Xia N, Zhang S, Guo X. 2014. Modification of fatty acids in membranes of bacteria: implication for an adaptive mechanism to the toxicity of carbon nanotubes. Environ Sci Technol 48:4086–95
   PubMed Web of Science ®Google Scholar