Potential Biotoxicity of Fullerene C60 on Cell Membrane: Molecular Dynamics Simulation

Abstract

Abstract: Coarse-grained simulations were adopted to investigate interaction between fullerene C₆₀ cluster and lipid membranes. C₆₀ aggregates in water and their interaction with lipid membrane were investigated. It was found that the aggregate can penetrate the membrane directly instead of endocytosis and pinocytosis. The penetration caused transmembrane movement of lipid and water molecules. Interaction between C₆₀ molecules and small lipid vesicle was investigated and dependence on C₆₀ concentration was interpreted explicitly. Conflicting experimental observations due to different preparation methods and processes are also provided. Potential mechanism of the biotoxicity of fullerene was put forward. Our results are helpful in medical applications.

Key words: fullerene, lipid membrane, molecular simulation, biotoxicity

CLC Number:

O469
Q615

LIU Yongzhi, XIE Liqiang, LIANG Shengde, ZHU Kaili, XI Zhonghong, YUAN Fangqiang. Potential Biotoxicity of Fullerene C₆₀ on Cell Membrane: Molecular Dynamics Simulation[J]. CHINESE JOURNAL OF COMPUTATIONAL PHYSICS, 2020, 37(4): 479-487.

References

[1] KROTO H W, HEATH J R. C₆₀:Buck minster fullerene[J]. Nature, 1985, 318(6042):162-163.
[2] GAURAV L, BALAJI S. Multifunctional fullerene and metallofullerene based nanobiomaterials[J]. Nano Life, 2013, 03(03):1342003.
[3] CHEN C, XING G,WANG J, et al. Multihydroxylated[Gd@C₈₂(OH)₂₂]_<em>n nanoparticles:Antineoplastic activity of high efficiency and low toxicity[J]. Nano Letters, 2005, 5(10):2050-2057.
[4] BAKRY R, VALLANT R M, NAJAMULHAG M, et al. Medicinal applications of fullerenes[J]. International Journal of Nanomedicine, 2007, 2(4):639-649.
[5] MENG J, LIANG X, CHEN X, et al. Biological characterizations of[Gd@C₈₂(OH)₂₂]_<em>n nanoparticles as fullerene derivatives for cancer therapy[J]. Integrative Biology, 2013, 5(1):43-47.
[6] TEGOS G P, DEMIDOVA T N, ARCILALOPEZ D, et al. Cationic fullerenes are effective and selective antimicrobial photosensitizers[J]. Chem Biol, 2005, 12(10):1127-1135.
[7] DING H M, MA Y Q. Computational approaches to cell-nanomaterial interactions:Keeping balance between therapeutic efficiency and cytotoxicity[J]. Nanoscale Horiz, 2018, 3(1):6-27.
[8] MAGREZ A, KASAS S, SALICIO V, et al. Cellular toxicity of carbon based nanomaterials[J]. Nano Letters, 2006, 6(6):1121-1125.
[9] SAYES C M, FORTNER J D, GUO W, et al. The differential cytotoxicity of water-soluble fullerenes[J]. Nano Letters, 2004, 4(10):1881-1887.
[10] ANDRE E N, LUTZ M, DARRELL V, et al. Understanding biophysicochemical interactions at the nanobiointerface[J]. Nat Mater, 2009, 8(7):553-557.
[11] HA Y, KATZ L E, LILJESTRAND H M. Distribution of fullerene nanoparticles between water and solid supported lipid membranes:Thermodynamics and effects of membrane composition on distribution[J]. Environmental Science Technology, 2015, 49(24):14546-14553.
[12] FORTNER J D, LYON D Y, SAYES C M, et al. C₆₀ in water:Nanocrystal formation and microbial response[J]. Environmental Science Technolog, 2003, 9(11):4307-4316.
[13] LYON D Y, ADAMS L K, FALKNER C, et al. Antibacterial activity of fullerene water suspensions:Effects of preparation method and particle size[J]. Environmental Science Technology, 2006, 40(14):4360-4366.
[14] ANDRIEVSKY G, KLOCHKOV V, DEREVYANCHENKO L. Is the C₆₀ fullerene molecule toxic?[J]. Fullerenes Nanotubes and Carbon Nanostructures, 2005, 13(4):363-376.
[15] SAYES C M, GOBIN A M, AUSMAN K D, et al. Nano-C₆₀ cytotoxicity is due to lipid peroxidation[J]. Biomaterials, 2005, 20(36):7587-7595.
[16] ZUPANC J, DROBNE D, DRASLER B, et al. Experimental evidence for the interaction of C₆₀ fullerene with lipid vesicle membranes[J]. Carbon, 2012, 50(3):1170-1178.
[17] BARNOUD J, ROSSI G, MONTICELLI L. Lipid membranes as solvents for carbon nanoparticles[J]. Phys Rev Lett, 2014, 12(2):068102.
[18] JIRASAK W E, SVETLANA B, WANNAPONG T, et al. Computer simulation study of fullerene translocation through lipid membranes[J]. Nat Nano, 2008, 3(6):363-368.
[19] TIAN W D, MA Y Q. Theoretical and computational studies of dendrimers as delivery vectors[J]. Chem Soc Rev, 2013, 42:705-727.
[20] CHANG R, LEE J. Dynamics of C₆₀ molecules in biological membranes:Computer simulation studies[J]. Bulletin- Korean Chemical Society, 2010, 31(11):3195-3200.
[21] GUPTA R, RAI B. Molecular dynamics simulation study of translocation of fullerene C₆₀ through skin bilayer:Effect of concentration on barrier properties[J]. Nanoscale, 2017, 9(12):4114-4127.
[22] IKEDA A. An extremely effective DNA photocleavage utilizing functionalized liposomes with a fullerene-enriched lipid bilayer[J]. Journal of the American Chemical Society, 2007, 129(14):4140-4141.
[23] IKEDA A, KAWAI Y, KIKUCHI J, et al. Effect of phase transition temperature of liposomes on preparation of fullerene-encapsulated liposomes by the fullerene-exchange reaction[J]. Chem Commun, 2010, 46(16):2847-2849.
[24] IKEDA A, KAWAI Y, KIKUCHI JI, et al. Formation and regulation of fullerene-incorporation in liposomes under the phase transition temperature[J]. Org Biomol Chem, 2011,9(8):2622-2627.
[25] IKEDA A, MATSUMOTO M, AKIYAMA M, et al. Direct and short-time uptake of C₇₀ fullerene into the cell membrane using an exchange reaction from a C₇₀ fullerene-gamma-cyclodextrin complex and the resulting photodynamic activity[J]. Chem Commun, 2009, 5(12):1547-1549.
[26] LI L, DAVANDE H, BEDROV D, et al. A molecular dynamics simulation study of C₆₀ fullerenes inside a dimyristoyl phosphatidyl-choline lipid bilayer[J]. The Journal of Physical Chemistry B, 2007, 111(16):4067-4072.
[27] DEVANE R, JUSUFI A, SHINODA W, et al. Parametrization and application of a coarse grained force field for benzene/fullerene interactions with lipids[J]. The Journal of Physical Chemistry B, 2010, 114(49):16364-16372.
[28] JUSUFI A, DE VANE R H, SHINODA W, et al. Nanoscale carbon particles and the stability of lipid bilayers[J]. Soft Matter, 2011, 7(3):1139-1146.
[29] RUSS K A, ELVATI P, PARSONAGE T L, et al. C₆₀ fullerene localization and membrane interactions in raw 264.7 immortalized mouse macrophages[J]. Nanoscale, 2016,8(7):4134-4144.
[30] CHEN Y, BOTHUN G D. Lipid-assisted formation and dispersion of aqueous and bilayer-embedded nano-C₆₀[J]. Langmuir, 2009, 25(9):4875-4879.
[31] SALONEN E, LIN S, REID M L, et al. Real-time translocation of fullerene reveals cell contraction[J]. Small, 2008, 4(11):1986-1992.
[32] MARRINK S J, DE VRIES A H, MARK A E. Coarse grained model for semiquantitative lipid simulations[J]. The Journal of Physical Chemistry B, 2004, 108(2):750-760.
[33] MARRINK S J, RISSELADA H, YEFIMOV S,et al. The martini force field:Coarse grained model for biomolecular simulations[J]. The Journal of Physical Chemistry B, 2007, 111(27):7812-7824.
[34] BARNOUD J, URBINI L, MONTICELLI L. C₆₀ fullerene promotes lung monolayer collapse[J].Journal of The Royal Society Interface, 2015, 12(104):10.1098/rsif.2014.0931.
[35] MONTICELLI L. On atomistic and coarse-grained models for C₆₀ fullerene[J]. Journal of Chemical Theory and Computation, 2012, 8(4):1370-1378.
[36] BERENDSEN H C, POSTMA J, et al. Molecular dynamics with coupling to an external bath[J]. The Journal of Chemical Physics, 1984, 81(8):3684-3690.
[37] VAN DER SPOEL D, LINDAHL E, HESS B,et al. Gromacs:Fast, flexible, and free[J]. Journal of Computational Chemistry, 2005, 26(16):1701-1718.
[38] HUMPHREY W, DALKE A, SCHULTEN K. VMD-Visual molecular dynamics[J]. Journal of Molecular Graphics, 1996, 14(1):33-38.
[39] ZHANG S, MU Y, ZHANG J Z, et al. Effect of self-assembly of fullerene nano-particles on lipid membrane[J]. Plos One, 2013, 8(10):e77436.
[40] MARCUS Y, SMITH A L, KOROBOV M V, et al. Solubility of C₆₀ fullerene[J]. The Journal of Physical Chemistry B, 2001, 105(13):2499-2506.
[41] TU Y, LV M, XIU P, et al. Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets[J]. Nature Nanotechnology, 2013, 8(8):594-601.
[42] MANNO S, TAKAKUWA Y, MOHANDAS N. Identification of a functional role for lipid asymmetry in biological membranes phosphatidylserine-skeletal protein interactions modulate membrane stability[J]. Proceedings of the National Academy of Sciences, 2002, 99(4):1943-1948.
[43] RAMACHANDRAN S, KUMAR P S, LARADJI M. Lipid fip-flop driven mechanical and morphological changes in model membranes[J]. The Journal of Chemical Physics, 2008,129(12):125104.
[44] YANG K, YUAN B, MA Y Q. Curvature changes of bilayer membranes studied by computer simulations[J]. The Journal of Physical Chemistry B, 2012, 116(24):7196-7202.
[45] LIU J, CONBOY J C. 1,2-diacyl-phos phatidylcholine flip-flop measured directly by sum-frequency vibrational spectroscopy[J]. Biophysical Journal, 2005, 89(4):2522-2532.
[46] SARUKHANYAN E, NICOLA A D, ROCCATANO D, et al. Spontaneous insertion of carbon nanotube bundles inside biomembranes:A hybrid particle-field coarse-grained molecular dynamics study[J]. Chemical Physics Letters, 2014, 595:155-166.
[47] KRASZEWSKI S, TAREK M, RAMSEYER C. Uptake and translocation mechanisms of cationic amino derivatives functionalized on pristine C₆₀ by lipid membranes:A molecular dynamics simulation study[J]. ACS Nano, 2011, 5(11):8571-8578.
[48] YUE T, ZHANG X, HUANG F. Membrane monolayer protrusion mediates a new nanoparticle wrapping pathway[J]. Soft Matter, 2014, 10(12):2024-2034.
[49] GAO X, DONG J, ZHANG X. The effect of nanoparticle size on endocytosis dynamics depends on membrane-nanoparticle interaction[J]. Molecular Simulation, 2015, 41(7):531-537.
[50] ZHANG J, ZHAO X, LIU Q H. Interactions between C₆₀ and vesicles:A coarse-grained molecular dynamics simulation[J]. RSC Adv, 2016, 6:90388-90396.

Potential Biotoxicity of Fullerene C₆₀ on Cell Membrane: Molecular Dynamics Simulation

RichHTML

PDF

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 2

Recommended Articles

Metrics

Authors

Reviewers

Journal Online

About Journal

[1]	Renyi CAO, Tao HUANG, Linsong CHENG, Zhanwu GAO, Zhihao JIA. Influence of Polar Substance of Crude Oil on Adsorption and Wettability in Water Flooding Reservoir: Molecular Simulation [J]. Chinese Journal of Computational Physics, 2021, 38(5): 595-602.
[2]	LIU Hong. Electronic Structure and Nonlinear Properties of Charged Fullerenes C₆₀ [J]. CHINESE JOURNAL OF COMPUTATIONAL PHYSICS, 2005, 22(3): 256-260.