Environmental Chemistry Letters

, Volume 11, Issue 2, pp 105–118 | Cite as

Fullerenes toxicity and electronic properties

  • Manzetti Sergio
  • Hadi Behzadi
  • Andersen Otto
  • David van der Spoel
Review

Abstract

Nanotechnology globally represents a new direction within scientific development, where the atomic and electronic properties of molecules are used in a unique fashion to produce and construct new and exotic materials and products. Fullerenes (Bucky balls, C60) constitute a particular group within the field of nanotechnology. Fullerenes find applications in medicine, industrial chemistry and electronics. However, there are several unanswered questions about fullerenes and their toxicological properties. Most toxicological studies on fullerenes evolve around the in vitro and in vivo aspects of pristine C60 along with chemically modified C60 molecules. We reviewed toxicology reports on C60. We bring a critical and challenging evaluation of the electronic and quantum properties of C60 molecules in context with the implications on cellular factors and metabolites. The evaluation shows that the reactivity and quantum chemical properties of C60 can have unexpected effects in the cell, by principally absorbing metabolites, such as OH and H+ ions and alter its reactivity. We thus challenge the present view of C60 solely based on empirical studies, based on the electronic properties of C60 that vary considerably with their size and reaction path. A further example of this is the absorption of divalent zinc ions, which shows an increase in reactivity of the C60 that presents an important pattern of chemical state, reactivity and toxicological potential. The results evaluate the toxicological potential of C60 from a different angle than conventional, by applying a blend of critical review of the findings on C60 toxicity, their chemical and electronic properties.

Keywords

Fullerenes Chemical modifications Toxicity prediction Electronic properties Quantum chemistry Mutagenicity 

References

  1. Allouche A (2011) Gabedit—a graphical user interface for computational chemistry softwares. J Comput Chem 32:174–182CrossRefGoogle Scholar
  2. Anctil A, Babbitt C, Raffaelle R, Landi B (2011) Material and energy intensity of fullerene production. Environ Sci Technol 45:2353–2359CrossRefGoogle Scholar
  3. Bakry R, Vallant R, Najam-ul-Haq M et al (2007) Medicinal applications of fullerenes. Int J Nanomed 2:639Google Scholar
  4. Becke A (1993) Density-functional thermochemistry. III. The role of exact exchange. J Chem Phys 98:5648–5652CrossRefGoogle Scholar
  5. Cagle D, Kenmnel S, Mirzadeh S et al (1999) In vivo studies of materials using endohedral metallofullerene radiotracers. Proc Natl Acad Sci USA 96:5182–5187CrossRefGoogle Scholar
  6. Chen Z, King R (2005) Spherical aromaticity: recent work on fullerenes, polyhedral boranes, and related structures. Chem Rev 105:3613–3642CrossRefGoogle Scholar
  7. Chen Z, Heine T, Jiao H et al (2004) Theoretical studies on the smallest fullerene: from monomer to oligomers and solid States. Chemistry 10:963–970CrossRefGoogle Scholar
  8. Da Ros T (2008) Twenty years of promises: fullerene in medicinal chemistry. Medicinal chemistry and pharmacological potential of fullerenes and carbon nanotubes. Springer, Netherlands, pp 1–21. doi: 10.1007/978-1-4020-6845-4_1
  9. Dekant W (2009) The role of biotransformation and bioactivation in toxicity. EXS 99:57–86Google Scholar
  10. Dhawan A, Taurozzi J, Pandey A et al (2006) Stable colloidal dispersions of C60 fullerenes in water: evidence for genotoxicity. Environ Sci Technol 40:7394–7401CrossRefGoogle Scholar
  11. Drug E, Landesman-Milo D, Belgorodsky B et al (2011) Enhanced bioavailability of polyaromatic hydrocarbons in the form of mucin complexes. Chem Res Toxicol 24:314–320CrossRefGoogle Scholar
  12. Eilmes A, Munn R (2004) A test of the method of images at the surface of molecular materials. J Chem Phys 120:3887–3892CrossRefGoogle Scholar
  13. Elliot K (2011) Nanomaterials and the precautionary principle. Environ Health Perspect 119:A240. doi: 10.1289/ehp.1103687 CrossRefGoogle Scholar
  14. Filella M, Rellestab C, Chanudet V, Spaak P (2008) Effect of the filter feeder Daphnia on the particle size distribution of inorganic colloids in freshwaters. Water Res 42:1919–1924CrossRefGoogle Scholar
  15. Fortner J, Lyon D, Sayes C et al (2005) C60 in water: nanocrystal formation and microbial response. Environ Sci Technol 39:4307–4316CrossRefGoogle Scholar
  16. Frisch M, Trucks G, Schlegel H et al (2003) Gaussian 03. Gaussian, Inc., WallingfordGoogle Scholar
  17. Fujita K, Morimoto Y, Ogami A et al (2009) Gene expression profiles in rat lung after inhalation exposure to C60 fullerene particles. Toxicol 258:47–55CrossRefGoogle Scholar
  18. Gonzalez-Parra E, Gonzalez-Casaus M, Galán A et al (2011) Lanthanum carbonate reduces FGF23 in chronic kidney disease stage 3 patients. Nephrol Dial Transplant 26:2567–2571CrossRefGoogle Scholar
  19. Haddon R, Pasquarello A (1994) Magnetism of carbon clusters. Phys Rev B 50:16459–16463CrossRefGoogle Scholar
  20. Henry T, Menn F, Fleming J et al (2007) Attributing effects of aqueous C60 nano-aggregates to tetrahydrofuran decomposition products in larval zebrafish by assessment of gene expression. Environ Health Perspect 115:1059–1065CrossRefGoogle Scholar
  21. Henry T, Petersen E, Compton R (2011) Aqueous fullerene aggregates (nC60) generate minimal reactive oxygen species and are of low toxicity in fish: a revision of previous reports. Curr Opin Biotechnol 22:533–537CrossRefGoogle Scholar
  22. Hosseini A, Sharifzadeh M, Rezayat S et al (2010) Benefit of magnesium-25 carrying porphyrin-fullerene nanoparticles in experimental diabetic neuropathy. Int J Nanomed 5:517–523Google Scholar
  23. Hummelen J, Knight B, Pepeq F et al (1995) Preparation and characterization of fulleroid and methanofullerene derivatives. J Org Chem 60:532–538CrossRefGoogle Scholar
  24. Hyung H, Fortner J, Hughes J, Kim J (2007) Natural organic matter stabilizes carbon nanotubes in the aqueous phase. Environ Sci Technol 41:179–184CrossRefGoogle Scholar
  25. Jakubov T, Mainwaring S (2009) Interaction between C60 fullerene and alkali metals demonstrating superconductivity. Procedia Chem 1:1584–1589CrossRefGoogle Scholar
  26. JCrystalSoft (2012) Nanotube modeler. J Crystal Soft. http://www.jcrystal.com/
  27. Jehoulet C, Obeng Y, Kim Y et al (1992) Electrochemistry and langmuir trough studies of fullerene C60 and C70 films. J Am Chem Soc 114:4237–4247CrossRefGoogle Scholar
  28. Jensen A, Wilson S, Schuster D (1996) Biological applications of fullerenes. Bioorg Med Chem 4:1–20CrossRefGoogle Scholar
  29. Jiao F, Qu Y, Zhou G et al (2010) Modulation of oxidative stress by functionalized fullerene materials in the lung tissues of female C57/BL mice with a metastatic Lewis lung carcinoma. J Nanosci Nanotechnol 10:8632–8637CrossRefGoogle Scholar
  30. Jovanović B, Anastasova L, Rowe E, Palić D (2011) Hydroxylated fullerenes inhibit neutrophil function in fathead minnow (Pimephales promelas Rafinesque, 1820). Aquat Toxicol 101:474–482CrossRefGoogle Scholar
  31. Kashiwada S (2006) Distribution of nanoparticles in the see-through medaka (Oryzias latipes). Environ Health Persp 114:1697–1702Google Scholar
  32. Khairullin I, Chen Y, Hwang L (1997a) Evidence for electron charge transfer in the polyvinylpyrrolidone-c60 system as seen from ESR spectra. Chem Phys Lett 275:1CrossRefGoogle Scholar
  33. Khairullin I, Tsao Z, Hwang L (1997b) Characterization of KC60 obtained via a potassium carbonate route. Fuller Sci Tech 5:1507CrossRefGoogle Scholar
  34. Kim K, Jang M, Kim JY, Kim S (2010) Effect of preparation methods on toxicity of fullerene water suspensions to Japanese medaka embryos. Sci Tot Environ 408:5606–5612CrossRefGoogle Scholar
  35. Knupfer M, Knauff O, Golden M et al (1996) Electronic structure of the two C78 isomers with C2v symmetry. Chem Phys Lett 258:513CrossRefGoogle Scholar
  36. Lee C, Yang W, Parr R (1988) Development of the Colle-Salvetti conelation energy formula into a functional of the electron density. Phys Rev B 37:785–789CrossRefGoogle Scholar
  37. Lee J, Jung J, Emrick T et al (2010) Morphology control of a polythiophene-fullerene bulk heterojunction for enhancement of the high-temperature stability of solar cell performance by a new donor-acceptor diblock copolymer. Nanotechnology 21:105201CrossRefGoogle Scholar
  38. Levin W, Wood A, Chang R et al (1982) Oxidative metabolism of polycyclic aromatic hydrocarbons to ultimate carcinogens. Drug Metab Rev 13:555–580CrossRefGoogle Scholar
  39. Li Q, Xie B, Hwang Y, Xu Y (2009) Kinetics of C60 fullerene dispersion in water enhanced by natural organic matter and sunlight. Environ Sci Technol 43:3574–3579CrossRefGoogle Scholar
  40. Liang C, Xie H, Schwartz V et al (2009) Open-cage fullerene-like graphitic carbons as catalysts for oxidative dehydrogenation of isobutane. J Am Chem Soc 131:7735–7741CrossRefGoogle Scholar
  41. Lin C, Zhang M, Liu S et al (2011) High photoelectric conversion efficiency of metal phthalocyanine/fullerene heterojunction photovoltaic device. Int J Mol Sci 12:476–505CrossRefGoogle Scholar
  42. Lyon D, Fortner J, Sayes C et al (2005) Bacterial cell association and antimicrobial activity of a C60 water suspension. Environ Toxicol Chem 24:2757–2762CrossRefGoogle Scholar
  43. Manzetti S (2011) Quantum toxicology—a potential perspective in toxicology? Toxicology 288:56–57CrossRefGoogle Scholar
  44. Markovic Z, Todorovic-Markovic B, Kleut D et al (2007) The mechanism of cell-damaging reactive oxygen generation by colloidal fullerenes. Biomaterials 28:5437–5448CrossRefGoogle Scholar
  45. Mauter EM (2008) Environmental applications of carbon-based nanomaterials. Environ Sci Technol 42:5843–5859CrossRefGoogle Scholar
  46. Miles R, Hynes K, Forbes I (2005) Photovoltaic solar cells: an overview of state-of-the-art cell development and environmental issues. Progr Cryst Growth Charact Mater 51:1–42CrossRefGoogle Scholar
  47. Mori T et al (2006) Preclinical studies on safety of fullerene upon acute oral administration and evaluation for no mutagenesis. Toxicology 225:48–54CrossRefGoogle Scholar
  48. Nakagawa Y, Suzuki T, Ishii H et al (2011) Cytotoxic effects of hydroxylated fullerenes on isolated rat hepatocytes via mitochondrial dysfunction. Arch Toxicol. doi: 10.1007/s00204-011-0688-z Google Scholar
  49. Oberdörster E (2004a) Manufactured nanomaterials (fullerenes, C60) induce oxidative stress in the brain of juvenile largemouth bass. Environ Health Perspect 112:1058–1062CrossRefGoogle Scholar
  50. Oberdörster E (2004b) Toxicity of nC60 fullerenes to two aquatic species: Daphnia and largemouth bass [Abstract]. In: 227th American Chemical Society National Meeting, 27 March–1 April 2004, Anaheim, CAGoogle Scholar
  51. Oberdörster G, Oberdörster E, Oberdörster J (2005) Nanotoxicology: an emerging discipline evolving from 116 studies of ultrafine particles. Environ Health Persp 113:823–839CrossRefGoogle Scholar
  52. Oberdörster E, Zhu S, Blickley T et al (2006) Ecotoxicology of carbon-based engineered nanoparticles: effects of fullerene (C60) on aquatic organisms. Carbon 44:1112–1120CrossRefGoogle Scholar
  53. Park J, Henry T, Menn F et al (2010) No bioavailability of 17α-ethinylestradiol when associated with nC60 aggregates during dietary exposure in adult male zebrafish (Danio rerio). Chemosphere 81:1227–1232CrossRefGoogle Scholar
  54. Qiao R, Roberts A, Mount A et al (2007) Translocation of C60 and its derivatives across a lipid bilayer. Nano Lett 7:614–619CrossRefGoogle Scholar
  55. Raghavachari K, Binkley J, Seeger R, Pople J (1980) Self-consistent molecular orbital methods. 20. Basis set for correlated wave-functions. J Chem Phys 72:650–654CrossRefGoogle Scholar
  56. Rassolov V, Pople J, Ratner M, Windus T (1998) 6–31G* basis set for atoms K through Zn. J Chem Phys 109:1223–1229. doi: 10.1063/1.476673 CrossRefGoogle Scholar
  57. Rodríguez-Fortea A, Irle S, Poblet J (2011) Fullerenes: formation, stability, and reactivity. Adv Rev. doi:  10.1002/wcms
  58. Sadauskas E, Wallin H, Stoltenberg M et al (2007) Kupffer cells are central in the removal of nanoparticles from the organism. Part Fibre Toxicol 4:10CrossRefGoogle Scholar
  59. Sayes C et al (2007) Comparative pulmonary toxicity assessments of C60 water suspensions in rats: few differences in fullerene toxicity in vivo in contrast to in vitro profiles. Nano Lett 7:2399–2406CrossRefGoogle Scholar
  60. Shrotriya V, Yao Y, Li G, Yang Y (2006) Effect of self-organization in polymer/fullerene bulk heterojunctions on solar cell performance. Appl Phys Lett 89:063505CrossRefGoogle Scholar
  61. Stephens P, Devlin F, Chabalowski C, Frisch M (1994) Ab initio calculation of vibrational absorption and circular dichroism spectra using density functional force fields. J Phys Chem 98:11623–11627CrossRefGoogle Scholar
  62. Subach F, Malashkevich V, Zencheck W et al (2009) Photoactivation mechanism of PAmCherry based on crystal structures of the protein in the dark and fluorescent states. Proc Natl Acad Sci USA 106:21097–21102CrossRefGoogle Scholar
  63. Tanaka A (2004) Toxicity of indium arsenide, gallium arsenide, and aluminium gallium arsenide. Toxicol Appl Pharmacol 198:405–411CrossRefGoogle Scholar
  64. Thompson M (2004) ArgusLab. Planaria Software LLC, SeattleGoogle Scholar
  65. Tokuyama H, Yamago S, Nakamura E et al (1993) Photoinduced biochemical activity of fullerene carboxylic acid. J Am Chem Soc 115:7918–7919CrossRefGoogle Scholar
  66. Tong J, Zimmerman M, Li S et al (2011) Neuronal uptake and intracellular superoxide scavenging of a fullerene (C60)-poly(2-oxazoline)s nanoformulation. Biomaterials 32:3654–3665CrossRefGoogle Scholar
  67. Tsuchiya T, Oguri I, Yamakoshi Y, Miyata N (1996) Novel harmful effects of [60] fullerene on mouse embryos in vitro and in vivo. FEBS Lett 393:139–145CrossRefGoogle Scholar
  68. Voet D, Voet J (2010) Biochemistry, 4th edn. Wiley, New YorkGoogle Scholar
  69. Vosko S, Wilk L, Nusair M (1980) Accurate spin-dependent electron liquid correlation energies for local spin density calculations: a critical analysis. Can J Phys 58:1200–1211CrossRefGoogle Scholar
  70. Walsh B (2010) The perils of plastic. Time Magazine, USGoogle Scholar
  71. Willner I, Willner B (2010) Biomolecule-based nanomaterials and nanostructures. Nano Lett 10:3805–3815CrossRefGoogle Scholar
  72. Yamago S, Tokuyama H, Nakamura E et al (1995) In vivo biological behavior of a water-miscible fullerene: 14C labeling, absorption, distribution, excretion and acute toxicity. Chem Biol 2:385–389CrossRefGoogle Scholar
  73. Yamakoshi Y, Umezawa N, Ryu A et al (2003) Active oxygen species generated from photoexcited fullerene (C60) as potential medicines: O2− versus 1O2. J Am Chem Soc 125:12803–12809CrossRefGoogle Scholar
  74. Yang D, Park C, Min J et al (2009) Fullerene nanohybrid metal oxide ultrathin films. Curr Appl Phys 9:132–135CrossRefGoogle Scholar
  75. Yuan Y, Reece T, Sharma P et al (2011) Efficiency enhancement in organic solar cells with ferroelectric polymer. Nat Mater 10:296–302CrossRefGoogle Scholar
  76. Zhang L, Yang J, Barron A, Monteiro-Riviere N (2009) Endocytic mechanisms and toxicity of a functionalized fullerene in human cells. Toxicol Lett 191:149–157CrossRefGoogle Scholar
  77. Zhang M, Xing G, Yuan H et al (2010) Transmembrane delivery of aggregated [Gd@C82(OH)22]n nanoparticles. J Nanosci Nanotechnol 10:8556–85661CrossRefGoogle Scholar
  78. Zhou Z, Joslin S, Dellinger A et al (2010) A novel class of compounds with cutaneous wound healing properties. J Biomed Nanotechnol 6:605–611CrossRefGoogle Scholar
  79. Zhu X, Zhu L, Lang Y, Chen Y (2008) Oxidative stress and growth inhibition in the freshwater fish Carpassius auratus induced by chronic exposure to sublethal fullerene aggregates. Environ Toxicol 27:1979–1985CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Manzetti Sergio
    • 1
  • Hadi Behzadi
    • 2
  • Andersen Otto
    • 3
  • David van der Spoel
    • 4
  1. 1.FJORDFORSK Health and Environmental SciencesFlåmNorway
  2. 2.Department of ChemistryTarbiat Moallem UniversityTehranIran
  3. 3.Western Norway Research InstituteSogndalNorway
  4. 4.Department of Cell and Molecular BiologyUppsala UniversityUppsalaSweden

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