Insight into the interactions of fullerenes with biological membranes through molecular dynamics simulations

References

• Kroto HW, Heath JR, O’Brien SC, et al. C60: buckminsterfullerene. Nature. 1985;318:162–163. doi: 10.1038/318162a0
   Web of Science ®Google Scholar
• Holmannova D, Borsky P, Svadlakova T, et al. Carbon nanoparticles and their biomedical applications. Appl Sci. 2022;12:7865. doi: 10.3390/app12157865
   Google Scholar
• Alshehri MH. An analytical model for lithium storage in spherical fullerenes. Energies. 2022;15:7154. doi: 10.3390/en15197154
   Web of Science ®Google Scholar
• Riley PR, Narayan RJ. Recent advances in carbon nanomaterials for biomedical applications: a review. Curr Opin Biomed Eng. 2021;17:100262. doi: 10.1016/j.cobme.2021.100262
   PubMedGoogle Scholar
• Minami K, Song J, Shrestha LK, et al. Nanoarchitectonics for fullerene biology. Appl Mater Today. 2021;23:100989. doi: 10.1016/j.apmt.2021.100989
   Web of Science ®Google Scholar
• Kumar M, Raza K. C60-fullerenes as drug delivery carriers for anticancer agents: promises and hurdles. Pharm Nanotechnol. 2017;5:169–179. doi: 10.2174/2211738505666170301142232
   PubMedGoogle Scholar
• Anilkumar P, Lu F, Cao L, et al. Fullerenes for applications in biology and medicine. Curr Med Chem. 2011;18:2045–2059. doi: 10.2174/092986711795656225
   PubMed Web of Science ®Google Scholar
• Panwar N, Soehartono AM, Chan KK, et al. Nanocarbons for biology and medicine: sensing, imaging, and drug delivery. Chem Rev. 2019;119:9559–9656. doi: 10.1021/acs.chemrev.9b00099
   PubMed Web of Science ®Google Scholar
• Gharbi N, Pressac M, Hadchouel M, et al. Fullerene is a powerful antioxidant in vivo with no acute or subacute toxicity. Nano Lett. 2005 60;5:2578–2585. doi: 10.1021/nl051866b
   PubMed Web of Science ®Google Scholar
• Bundschuh M, Filser J, Lüderwald S, et al. Nanoparticles in the environment: where do we come from, where do we go to? Environ Sci Eur. 2018;30:1–17. doi: 10.1186/s12302-018-0132-6
   PubMed Web of Science ®Google Scholar
• Lespes G, Faucher S, Slaveykova VI. Natural nanoparticles, anthropogenic nanoparticles, where is the frontier? Front Environ Sci. 2020;8:71. doi: 10.3389/fenvs.2020.00071
   Web of Science ®Google Scholar
• Buzea C, Pacheco II, Robbie K. Nanomaterials and nanoparticles: sources and toxicity. Biointerphases. 2007;2:MR17–MR71. doi: 10.1116/1.2815690
   PubMed Web of Science ®Google Scholar
• Nielsen GD, Roursgaard M, Jensen KA, et al. In vivo biology and toxicology of fullerenes and their derivatives. Basic Clin Pharmacol Toxicol. 2008;103:197–208. doi: 10.1111/j.1742-7843.2008.00266.x
   PubMed Web of Science ®Google Scholar
• Dellinger A, Zhou Z, Norton SK, et al. Uptake and distribution of fullerenes in human mast cells. Nanomedicine. 2010;6:575–582. doi: 10.1016/j.nano.2010.01.008
   PubMed Web of Science ®Google Scholar
• Oberdörster G, Ferin J, Lehnert BE. Correlation between particle size, in vivo particle persistence, and lung injury. Environ Health Perspect. 1994;102:173–179. doi: 10.1289/ehp.102-1567252
   PubMed Web of Science ®Google Scholar
• Oberdörster G, Sharp Z, Atudorei V, et al. Translocation of inhaled ultrafine particles to the brain. Inhal Toxicol. 2004;16:437–445. doi: 10.1080/08958370490439597
   PubMed Web of Science ®Google Scholar
• Porter AE, Gass M, Muller K, et al. Visualizing the uptake of C60 to the cytoplasm and nucleus of human monocyte-derived macrophage cells using energy-filtered transmission electron microscopy and electron tomography. Environ Sci Technol. 2007;41:3012–3017. doi: 10.1021/es062541f
   PubMed Web of Science ®Google Scholar
• Muhlfeld C, Rothen-Rutishauser B, Blank F, et al. Interactions of nanoparticles with pulmonary structures and cellular responses. Am J Physiol Lung Cell Mol Physiol. 2008;294:L817–L829. doi: 10.1152/ajplung.00442.2007
   PubMed Web of Science ®Google Scholar
• Nisoh N, Jarerattanachat V, Karttunen M, et al. Fullerenes’ interactions with plasma membranes: insight from the MD simulations. Biomolecules. 2022;12:639. doi: 10.3390/biom12050639
   PubMed Web of Science ®Google Scholar
• Nisoh N, Jarerattanachat V, Karttunen M, et al. Formation of aggregates, icosahedral structures and percolation clusters of fullerenes in lipids bilayers: the key role of lipid saturation. Biochim Biophys Acta Biomembr. 2020;1862:183328. doi: 10.1016/j.bbamem.2020.183328
   PubMed Web of Science ®Google Scholar
• Pycke BF, Chao T-C, Herckes P, et al. Beyond nC60: strategies for identification of transformation products of fullerene oxidation in aquatic and biological samples. Anal Bioanal Chem. 2012;404:2583–2595. doi: 10.1007/s00216-012-6090-8
   PubMed Web of Science ®Google Scholar
• Aschberger K, Johnston HJ, Stone V, et al. Review of fullerene toxicity and exposure–appraisal of a human health risk assessment, based on open literature. Regul Toxicol Pharmacol. 2010;58:455–473. doi: 10.1016/j.yrtph.2010.08.017
   PubMed Web of Science ®Google Scholar
• Malhotra N, Audira G, Castillo AL, et al. An update report on the biosafety and potential toxicity of fullerene-based nanomaterials toward aquatic animals. Oxid Med Cell Longevity. 2021;2021:1–14. doi: 10.1155/2021/7995223
   Web of Science ®Google Scholar
• Russ K, Elvati P, Parsonage T, et al. C60 fullerene localization and membrane interactions in RAW 264.7 immortalized mouse macrophages. Nanoscale. 2016;8:4134–4144. doi: 10.1039/C5NR07003A
   PubMed Web of Science ®Google Scholar
• Franskevych D, Palyvoda K, Petukhov D, et al. Fullerene C60 penetration into leukemic cells and its photoinduced cytotoxic effects. Nanoscale Res Lett. 2017;12:1–9. doi: 10.1186/s11671-016-1819-5
   PubMed Web of Science ®Google Scholar
• Prylutska SV, Grebinyk AG, Lynchak OV, et al. In vitro and in vivo toxicity of pristine C60 fullerene aqueous colloid solution. Fuller Nanotub Carbon Nanostruct. 2019;27:715–728. doi: 10.1080/1536383X.2019.1634055
   Web of Science ®Google Scholar
• Qiao R, Roberts AP, Mount AS, et al. Translocation of C60 and its derivatives across a lipid bilayer. Nano Lett. 2007;7:614–619. doi: 10.1021/nl062515f
   PubMed Web of Science ®Google Scholar
• Li L, Davande H, Bedrov D, et al. A molecular dynamics simulation study of C60 fullerenes inside a dimyristoylphosphatidylcholine lipid bilayer. J Phys Chem B. 2007;111:4067–4072. doi: 10.1021/jp064982r
   PubMed Web of Science ®Google Scholar
• Jusufi A, DeVane RH, Shinoda W, et al. Nanoscale carbon particles and the stability of lipid bilayers. Soft Matter. 2011;7:1139–1146. doi: 10.1039/C0SM00963F
   Web of Science ®Google Scholar
• Wong-Ekkabut J, Baoukina S, Triampo W, et al. Computer simulation study of fullerene translocation through lipid membranes. Nat Nanotech. 2008;3:363–368. doi: 10.1038/nnano.2008.130
   PubMed Web of Science ®Google Scholar
• Bozdaganyan ME, Orekhov PS, Shaytan AK, et al. Comparative computational study of interaction of C60-fullerene and tris-malonyl-C60-fullerene isomers with lipid bilayer: relation to their antioxidant effect. PLOS ONE. 2014;9:e102487. doi: 10.1371/journal.pone.0102487
   PubMed Web of Science ®Google Scholar
• Sridhar A, Srikanth B, Kumar A, et al. Coarse-grain molecular dynamics study of fullerene transport across a cell membrane. J Chem Phys. 2015;143:024907. doi: 10.1063/1.4926668
   PubMed Web of Science ®Google Scholar
• Hsu P-C, Jefferies D, Khalid S. Molecular dynamics simulations predict the pathways via which pristine fullerenes penetrate bacterial membranes. J Phys Chem. 2016;120:11170–11179. doi: 10.1021/acs.jpcb.6b06615
   PubMed Web of Science ®Google Scholar
• Liang L, Kang Z, Shen J-W. Translocation mechanism of C60 and C60 derivations across a cell membrane. J Nanopart Res. 2016;18:333. doi: 10.1007/s11051-016-3647-z
   Web of Science ®Google Scholar
• Zhang S, Mu Y, Zhang JZ, et al. Effect of self-assembly of fullerene nano-particles on lipid membrane. PLOS ONE. 2013;8:e77436. doi: 10.1371/journal.pone.0077436
   PubMed Web of Science ®Google Scholar
• Sastre J, Mannelli I, Reigada R. Effects of fullerene on lipid bilayers displaying different liquid ordering: a coarse-grained molecular dynamics study. Biochim Biophys Acta. 2017;1861:2872–2882. doi: 10.1016/j.bbagen.2017.08.004
   Web of Science ®Google Scholar
• Gul G, Ileri-Ercan N. Fullerene translocation through peroxidized lipid membranes. RSC Adv. 2021;11:7575–7586. doi: 10.1039/D1RA00272D
   PubMed Web of Science ®Google Scholar
• Bedrov D, Smith GD, Davande H, et al. Passive transport of C60 fullerenes through a lipid membrane: a molecular dynamics simulation study. J Phys Chem. 2008;112:2078–2084. doi: 10.1021/jp075149c
   PubMed Web of Science ®Google Scholar
• Xie LQ, Liu YZ, Xi ZH, et al. Computer simulations of the interaction of fullerene clusters with lipid membranes. Mol Simul. 2017;43:1532–1538. doi: 10.1080/08927022.2017.1332410
   Web of Science ®Google Scholar
• Gupta R, Rai B. Molecular dynamics simulation study of translocation of fullerene C60 through skin bilayer: effect of concentration on barrier properties. Nanoscale. 2017;9:4114–4127. doi: 10.1039/C6NR09186E
   PubMed Web of Science ®Google Scholar
• Marrink SJ, de Vries AH, Mark AE. Coarse grained model for semiquantitative lipid simulations. J Phys Chem B. 2004;108:750–760. doi: 10.1021/jp036508g
   Web of Science ®Google Scholar
• Marrink SJ, Risselada HJ, Yefimov S, et al. The MARTINI force field: coarse grained model for biomolecular simulations. J Phys Chem B. 2007;111:7812–7824. doi: 10.1021/jp071097f
   PubMed Web of Science ®Google Scholar
• Ingólfsson HI, Melo MN, Van Eerden FJ, et al. Lipid organization of the plasma membrane. J Am Chem Soc. 2014;136:14554–14559. doi: 10.1021/ja507832e
   PubMed Web of Science ®Google Scholar
• Tian WD, Chen K, Ma YQ. Interaction of fullerene chains and a lipid membrane via computer simulations. RSC Adv. 2014;4:30215–30220. doi: 10.1039/C4RA04593A
   Web of Science ®Google Scholar
• Samal S, Choi BJ, Geckeler KE. The first water-soluble main-chain polyfullerene. Chem Commun. 2000;1373–1374. doi: 10.1039/b003881o
   Web of Science ®Google Scholar
• Spurlin TA, Gewirth AA. Effect of C60 on solid supported lipid bilayers. Nano Lett. 2007;7:531–535. doi: 10.1021/nl0622707
   PubMed Web of Science ®Google Scholar
• D’Rozario RS, Wee CL, Wallace EJ, et al. The interaction of C60 and its derivatives with a lipid bilayer via molecular dynamics simulations. Nanotechnology. 2009;20:115102. doi: 10.1088/0957-4484/20/11/115102
   PubMed Web of Science ®Google Scholar
• Kumar S, Rosenberg JM, Bouzida D, et al. The weighted histogram analysis method for free‐energy calculations on biomolecules. J Comput Chem. 1992;13:1011–1021. doi: 10.1002/jcc.540130812
   Web of Science ®Google Scholar
• Hub JS, De Groot BL, van der Spoel D. Van Der Spoel D. g_wham—A free weighted histogram analysis implementation including robust error and autocorrelation estimates. J Chem Theory Comput. 2010;6:3713–3720. doi: 10.1021/ct100494z
   Web of Science ®Google Scholar
• Verma A, Stellacci F. Effect of surface properties on nanoparticle–cell interactions. Small. 2010;6:12–21. doi: 10.1002/smll.200901158
   PubMed Web of Science ®Google Scholar
• Nalakarn P, Boonnoy P, Nisoh N, et al. Dependence of fullerene aggregation on lipid saturation due to a balance between entropy and enthalpy. Sci Rep. 2019;9:1037. doi: 10.1038/s41598-018-37659-4
   PubMed Web of Science ®Google Scholar
• Nisoh N, Karttunen M, Monticelli L, et al. Lipid monolayer disruption caused by aggregated carbon nanoparticles. RSC Adv. 2015;5:11676–11685. doi: 10.1039/C4RA17006G
   Web of Science ®Google Scholar
• Monticelli L. On atomistic and coarse-grained models for C60 fullerene. J Chem Theory Comput. 2012;8:1370–1378. doi: 10.1021/ct3000102
   PubMed Web of Science ®Google Scholar
• Fortner J, Lyon D, Sayes C, et al. C60 in water: nanocrystal formation and microbial response. Environ Sci Technol. 2005;39:4307–4316. doi: 10.1021/es048099n
   PubMed Web of Science ®Google Scholar
• Andrievsky G, Klochkov V, Derevyanchenko L. Is the C60 fullerene molecule toxic?! Fuller Nanotub Carbon Nanostruct. 2005;13:363–376. doi: 10.1080/15363830500237267
   Web of Science ®Google Scholar
• Brant J, Lecoanet H, Wiesner MR. Aggregation and deposition characteristics of fullerene nanoparticles in aqueous systems. J Nanopart Res. 2005;7:545–553. doi: 10.1007/s11051-005-4884-8
   Web of Science ®Google Scholar
• Ha Y, Katz LE, Liljestrand HM. Distribution of fullerene nanoparticles between water and solid supported lipid membranes: thermodynamics and effects of membrane composition on distribution. Environ Sci Technol. 2015;49:14546–14553. doi: 10.1021/acs.est.5b03339
   PubMed Web of Science ®Google Scholar
• Lyon DY, Adams LK, Falkner JC, et al. Antibacterial activity of fullerene water suspensions: effects of preparation method and particle size. Environ Sci Technol. 2006;40:4360–4366. doi: 10.1021/es0603655
   PubMed Web of Science ®Google Scholar
• Kitjanon J, Khuntawee W, Phongphanphanee S, et al. Nanocomposite of fullerenes and natural rubbers: MARTINI force field molecular dynamics simulations. Polymers. 2021;13:4044. doi: 10.3390/polym13224044
   PubMed Web of Science ®Google Scholar
• Khuntawee W, Sutthibutpong T, Phongphanphanee S, et al. Molecular dynamics study of natural rubber–fullerene composites: connecting microscopic properties to macroscopic behavior. Phys Chem Chem Phys. 2019;21:19403–19413. doi: 10.1039/C9CP03155C
   PubMed Web of Science ®Google Scholar
• Zupanc J, Drobne D, Drasler B, et al. Experimental evidence for the interaction of C-60 fullerene with lipid vesicle membranes. Carbon. 2012;50:1170–1178. doi: 10.1016/j.carbon.2011.10.030
   Web of Science ®Google Scholar
• Rossi G, Barnoud J, Monticelli L. Partitioning and solubility of C60 fullerene in lipid membranes. Phys Scr. 2013;87:058503. doi: 10.1088/0031-8949/87/05/058503
   Web of Science ®Google Scholar
• Chang RW, Lee JM. Dynamics of C60 molecules in biological membranes: computer simulation studies. Bull Korean Chem Soc. 2010;31:3195–3200. doi: 10.5012/bkcs.2010.31.11.3195
   Web of Science ®Google Scholar
• Barnoud J, Rossi G, Monticelli L. Lipid membranes as solvents for carbon nanoparticles. Phys Rev Lett. 2014;112:068102. doi: 10.1103/PhysRevLett.112.068102
   PubMed Web of Science ®Google Scholar
• Chen Y, Bothun GD. Lipid-assisted formation and dispersion of aqueous and bilayer-embedded nano-C60. Langmuir. 2009;25:4875–4879. doi: 10.1021/la804124q
   PubMed Web of Science ®Google Scholar
• Zhou J, Liang D, Contera S. Effect of intra-membrane C60 fullerenes on the modulus of elasticity and the mechanical resistance of gel and fluid lipid bilayers. Nanoscale. 2015;7:17102–17108. doi: 10.1039/C5NR04719F
   PubMed Web of Science ®Google Scholar
• Drasler B, Drobne D, Sadeghpour A, et al. Fullerene up-take alters bilayer structure and elasticity: a small angle X-ray study. Chem Phys Lipids. 2015;188:46–53. doi: 10.1016/j.chemphyslip.2015.04.001
   PubMed Web of Science ®Google Scholar
• Bortolus M, Parisio G, Maniero AL, et al. Monomeric fullerenes in lipid membranes: effects of molecular shape and polarity. Langmuir. 2011;27:12560–12568. doi: 10.1021/la202524r
   PubMed Web of Science ®Google Scholar
• Ikeda A, Doi Y, Hashizume M, et al. An extremely effective DNA photocleavage utilizing functionalized liposomes with a fullerene-enriched lipid bilayer. J Am Chem Soc. 2007;129:4140–4141. doi: 10.1021/ja070243s
   PubMed Web of Science ®Google Scholar
• DeVane R, Jusufi A, Shinoda W, et al. Parametrization and application of a coarse grained force field for benzene/fullerene interactions with lipids. J Phys Chem B. 2010;114:16364–16372. doi: 10.1021/jp1070264
   PubMed Web of Science ®Google Scholar
• Salonen E, Lin S, Reid ML, et al. Real‐time translocation of fullerene reveals cell contraction. Small. 2008;4:1986–1992. doi: 10.1002/smll.200701279
   PubMed Web of Science ®Google Scholar
• Lavagna E, Barnoud J, Rossi G, et al. Size-dependent aggregation of hydrophobic nanoparticles in lipid membranes. Nanoscale. 2020;12:9452–9461. doi: 10.1039/D0NR00868K
   PubMed Web of Science ®Google Scholar
• Wang Z, Yang S. Effects of fullerenes on phospholipid membranes: a langmuir monolayer study. Chemphyschem. 2009;10:2284–2289. doi: 10.1002/cphc.200900328
   PubMed Web of Science ®Google Scholar
• Ikeda A, Mori M, Kiguchi K, et al. Advantages and potential of lipid‐membrane‐incorporating fullerenes prepared by the fullerene‐exchange method. Chem Asian J. 2012;7:605–613. doi: 10.1002/asia.201100792
   PubMed Web of Science ®Google Scholar
• Kim H, Bedrov D, Smith GD. Molecular dynamics simulation study of the influence of cluster geometry on formation of C60 fullerene clusters in aqueous solution. Chem Theory Comput. 2008;4:335–340. doi: 10.1021/ct700211y
   PubMed Web of Science ®Google Scholar
• Mackay AL. A dense non-crystallographic packing of equal spheres. Acta Cryst. 1962;15:916–918. doi: 10.1107/S0365110X6200239X
   Web of Science ®Google Scholar
• Martin G, Remaud G, Martin GJ. Isotopic methods for control of natural flavours authenticity. Flavour Fragr J. 1993;8:97–107. doi: 10.1002/ffj.2730080206
   Google Scholar
• Baletto F, Ferrando R. Structural properties of nanoclusters: energetic, thermodynamic, and kinetic effects. Rev Mod Phys. 2005;77:371. doi: 10.1103/RevModPhys.77.371
   Web of Science ®Google Scholar
• Doye JP, Wales DJ. The structure of (C60) N clusters. Chem Phys Lett. 1996;262:167–174. doi: 10.1016/0009-2614(96)01039-1
   Web of Science ®Google Scholar
• Luo YH, Qiu ST, Wang G. Dependence between transport properties of gas phase C60 at low density and interfullerene interaction. J Chem Phys. 1999;110:9101–9103. doi: 10.1063/1.478831
   Web of Science ®Google Scholar
• Rey C, Garcia-Rodeja J, Gallego LJ. The structures of small clusters of C60 molecules. Mol Clusters. 1997;40:395–398. doi: 10.1007/s004600050235
   Google Scholar
• Garcia-Rodeja J, Rey C, Gallego LJ. Prediction of the structures of clusters of C60 molecules using an atom-atom interaction potential. Phys Rev B. 1997;56:6466. doi: 10.1103/PhysRevB.56.6466
   Web of Science ®Google Scholar
• Ikeda A, Kiguchi K, Shigematsu T, et al. Location of [60]fullerene incorporation in lipid membranes. Chem Commun. 2011;47:12095–12097. doi: 10.1039/c1cc14650e
   PubMed Web of Science ®Google Scholar
• Levi N, Hantgan RR, Lively MO, et al. C60-fullerenes: detection of intracellular photoluminescence and lack of cytotoxic effects. J Nanobiotechnol. 2006;4:1–11. doi: 10.1186/1477-3155-4-14
   PubMedGoogle Scholar
• Mori T, Takada H, Ito S, et al. Preclinical studies on safety of fullerene upon acute oral administration and evaluation for no mutagenesis. Toxicology. 2006;225:48–54. doi: 10.1016/j.tox.2006.05.001
   PubMed Web of Science ®Google Scholar
• Doktorova M, Harries D, Khelashvili G. Determination of bending rigidity and tilt modulus of lipid membranes from real-space fluctuation analysis of molecular dynamics simulations. Phys Chem Chem Phys. 2017;19:16806–16818. doi: 10.1039/C7CP01921A
   PubMed Web of Science ®Google Scholar
• Khelashvili G, Pabst G, Harries D. Cholesterol orientation and tilt modulus in DMPC bilayers. J Phys Chem B. 2010;114:7524–7534. doi: 10.1021/jp101889k
   PubMed Web of Science ®Google Scholar
• Lai K, Wang B, Zhang Y, et al. Computer simulation study of nanoparticle interaction with a lipid membrane under mechanical stress. Phys Chem Chem Phys. 2013;15:270–278. doi: 10.1039/C2CP42027A
   PubMed Web of Science ®Google Scholar
• Sumi N, Chitra KC. Possible role of C60 fullerene in the induction of reproductive toxicity in the freshwater fish, anabas testudineus (Bloch, 1792). Environ Sci Pollut Res Int. 2020;27:19603–19615. doi: 10.1007/s11356-020-08509-6
   PubMed Web of Science ®Google Scholar
• Zhou Z. Liposome formulation of fullerene-based molecular diagnostic and therapeutic agents. Pharmaceutics. 2013;5:525–541. doi: 10.3390/pharmaceutics5040525
   PubMedGoogle Scholar
• Fernandes NB, Shenoy RUK, Kajampady MK, et al. Fullerenes for the treatment of cancer: an emerging tool. Environ Sci Pollut Res. 2022;29:58607–58627. doi: 10.1007/s11356-022-21449-7
   PubMed Web of Science ®Google Scholar
• Gao W, Hu C-M, Fang RH, et al. Liposome-like nanostructures for drug delivery. J Mater Chem B. 2013;1:6569–6585. doi: 10.1039/c3tb21238f
   Web of Science ®Google Scholar
• Bozzuto G, Molinari A. Liposomes as nanomedical devices. Int J Nanomed. 2015;10:975. doi: 10.2147/IJN.S68861
   PubMed Web of Science ®Google Scholar