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Heterogeneous oxidization of graphene nanosheets damages membrane

  • QianChun Wang
  • XiaoBo Zhai
  • Michael Crowe
  • Lu Gou
  • YinFeng Li
  • DeChang LiEmail author
  • Lei ZhangEmail author
  • JiaJie DiaoEmail author
  • BaoHua JiEmail author
Article

Abstract

Graphene-based materials exhibit unique properties that have been sought to utilize for various potential applications. Many studies suggest that graphene-based materials can be cytotoxic, which may be attributed to destructive effects on cell membranes. However, there still are conflicting results regarding interactions between graphene-based materials and lipid membranes. Here, through cryo-electron microscopy (Cryo-EM) and dye-leakage experiments along with in silico methods, we found that graphene oxide nanosheets induce significant membrane damage, while the effect of pristine graphene is negligible. We revealed the importance of heterogeneous oxidization of graphene-based nanosheets in damaging vesicle membranes. Moreover, that not only the oxidization degree but also the oxidization loci and membrane tension play important roles in the cytotoxicity of the graphene-based nanosheets.

Keywords

graphene graphene oxide heterogeneous oxidization cytotoxicity lipid membrane 

Supplementary material

11433_2018_9317_MOESM1_ESM.docx (11.8 mb)
Heterogeneous oxidization of graphene nanosheets damages membrane

References

  1. 1.
    Y. Wang, Z. Li, J. Wang, J. Li, and Y. Lin, Trends Biotech. 29, 205 (2011).CrossRefGoogle Scholar
  2. 2.
    C. Chung, Y. K. Kim, D. Shin, S. R. Ryoo, B. H. Hong, and D. H. Min, Acc. Chem. Res. 46, 2211 (2013).CrossRefGoogle Scholar
  3. 3.
    H. Y. Mao, S. Laurent, W. Chen, O. Akhavan, M. Imani, A. A. Ashkarran, and M. Mahmoudi, Chem. Rev. 113, 3407 (2013).CrossRefGoogle Scholar
  4. 4.
    G. Reina, J. M. González-Domínguez, A. Criado, E. Vázquez, A. Bianco, and M. Prato, Chem. Soc. Rev. 46, 4400 (2017).CrossRefGoogle Scholar
  5. 5.
    D. Kim, J. M. Yoo, H. Hwang, J. Lee, S. H. Lee, S. P. Yun, M. J. Park, M. J. Lee, S. Choi, S. H. Kwon, S. Lee, S. H. Kwon, S. Kim, Y. J. Park, M. Kinoshita, Y. H. Lee, S. Shin, S. R. Paik, S. J. Lee, S. Lee, B. H. Hong, and H. S. Ko, Nat. Nanotech. 13, 812 (2018), arXiv: 1710.07213.ADSCrossRefGoogle Scholar
  6. 6.
    Z. Liu, J. T. Robinson, X. Sun, and H. Dai, J. Am. Chem. Soc. 130, 10876 (2008).CrossRefGoogle Scholar
  7. 7.
    X. Sun, Z. Liu, K. Welsher, J. T. Robinson, A. Goodwin, S. Zaric, and H. Dai, Nano Res. 1, 203 (2008).CrossRefGoogle Scholar
  8. 8.
    K. Yang, S. Zhang, G. Zhang, X. Sun, S. T. Lee, and Z. Liu, Nano Lett. 10, 3318 (2010).ADSCrossRefGoogle Scholar
  9. 9.
    X. Yang, Y. Wang, X. Huang, Y. Ma, Y. Huang, R. Yang, H. Duan, and Y. Chen, J. Mater. Chem. 21, 3448 (2011).CrossRefGoogle Scholar
  10. 10.
    A. Servant, A. Bianco, M. Prato, and K. Kostarelos, Bioorg. Med. Chem. Lett. 24, 1638 (2014).CrossRefGoogle Scholar
  11. 11.
    L. Feng, S. Zhang, and Z. Liu, Nanoscale 3, 1252 (2011).ADSCrossRefGoogle Scholar
  12. 12.
    M. Kalbacova, A. Broz, J. Kong, and M. Kalbac, Carbon 48, 4323 (2010).CrossRefGoogle Scholar
  13. 13.
    H. Yuan, C. Huang, J. Li, G. Lykotrafitis, and S. Zhang, Phys. Rev. E 82, 011905 (2010).ADSCrossRefGoogle Scholar
  14. 14.
    A. Bianco, Angew. Chem. Int. Ed. 52, 4986 (2013).CrossRefGoogle Scholar
  15. 15.
    R. Zhou, and H. Gao, WIREs Nanomed Nanobiotech. 6, 452 (2014).CrossRefGoogle Scholar
  16. 16.
    X. Zou, L. Zhang, Z. Wang, and Y. Luo, J. Am. Chem. Soc. 138, 2064 (2016).CrossRefGoogle Scholar
  17. 17.
    Q. Zhang, Z. Wu, N. Li, Y. Pu, B. Wang, T. Zhang, and J. Tao, Mater. Sci. Eng.-C 77, 1363 (2017).CrossRefGoogle Scholar
  18. 18.
    O. Akhavan, and E. Ghaderi, ACS Nano 4, 5731 (2010).CrossRefGoogle Scholar
  19. 19.
    W. Hu, C. Peng, W. Luo, M. Lv, X. Li, D. Li, Q. Huang, and C. Fan, ACS Nano 4, 4317 (2010).CrossRefGoogle Scholar
  20. 20.
    S. Liu, T. H. Zeng, M. Hofmann, E. Burcombe, J. Wei, R. Jiang, J. Kong, and Y. Chen, ACS Nano 5, 6971 (2011).CrossRefGoogle Scholar
  21. 21.
    S. Liu, M. Hu, T. H. Zeng, R. Wu, R. Jiang, J. Wei, L. Wang, J. Kong, and Y. Chen, Langmuir 28, 12364 (2012).CrossRefGoogle Scholar
  22. 22.
    V. T. H. Pham, V. K. Truong, M. D. J. Quinn, S. M. Notley, Y. Guo, V. A. Baulin, M. Al Kobaisi, R. J. Crawford, and E. P. Ivanova, ACS Nano 9, 8458 (2015).CrossRefGoogle Scholar
  23. 23.
    G. Duan, Y. Zhang, B. Luan, J. K. Weber, R. W. Zhou, Z. Yang, L. Zhao, J. Xu, J. Luo, and R. Zhou, Sci. Rep. 7, 42767 (2017).ADSCrossRefGoogle Scholar
  24. 24.
    M. C. Duch, G. R. S. Budinger, Y. T. Liang, S. Soberanes, D. Urich, S. E. Chiarella, L. A. Campochiaro, A. Gonzalez, N. S. Chandel, M. C. Hersam, and G. M. Mutlu, Nano Lett. 11, 5201 (2011).ADSCrossRefGoogle Scholar
  25. 25.
    K. H. Liao, Y. S. Lin, C. W. Macosko, and C. L. Haynes, ACS Appl. Mater. Interfaces 3, 2607 (2011).CrossRefGoogle Scholar
  26. 26.
    R. Li, L. M. Guiney, C. H. Chang, N. D. Mansukhani, Z. Ji, X. Wang, Y. P. Liao, W. Jiang, B. Sun, M. C. Hersam, A. E. Nel, and T. Xia, ACS Nano 12, 1390 (2018).CrossRefGoogle Scholar
  27. 27.
    Y. Tu, M. Lv, P. Xiu, T. Huynh, M. Zhang, M. Castelli, Z. Liu, Q. Huang, C. Fan, H. Fang, and R. Zhou, Nat. Nanotech. 8, 594 (2013).ADSCrossRefGoogle Scholar
  28. 28.
    A. C. F. Ip, B. Liu, P. J. J. Huang, and J. Liu, Small 9, 1030 (2013).CrossRefGoogle Scholar
  29. 29.
    M. Crowe, Y. Lai, Y. Wang, J. Lu, M. Zhao, Z. Tian, J. Long, P. Zhang, and J. Diao, Small Methods 1, 1700207 (2017).CrossRefGoogle Scholar
  30. 30.
    I. Zucker, J. R. Werber, Z. S. Fishman, S. M. Hashmi, U. R. Gabinet, X. Lu, C. O. Osuji, L. D. Pfefferle, and M. Elimelech, Environ. Sci. Technol. Lett. 4, 404 (2017).CrossRefGoogle Scholar
  31. 31.
    J. Mao, R. Guo, and L. T. Yan, Biomaterials 35, 6069 (2014).CrossRefGoogle Scholar
  32. 32.
    R. Guo, J. Mao, and L. T. Yan, Biomaterials 34, 4296 (2013).CrossRefGoogle Scholar
  33. 33.
    J. Chen, G. Zhou, L. Chen, Y. Wang, X. Wang, and S. Zeng, J. Phys. Chem. C 120, 6225 (2016).CrossRefGoogle Scholar
  34. 34.
    W. Yang, H. T. Wang, T. F. Li, and S. X. Qu, Sci. China-Phys. Mech. Astron. 62, 014601 (2019).CrossRefGoogle Scholar
  35. 35.
    J. Chen, B. Yao, C. Li, and G. Shi, Carbon 64, 225 (2013).CrossRefGoogle Scholar
  36. 36.
    A. Dato, V. Radmilovic, Z. Lee, J. Phillips, and M. Frenklach, Nano Lett. 8, 2012 (2008).ADSCrossRefGoogle Scholar
  37. 37.
    M. Kyoung, A. Srivastava, Y. Zhang, J. Diao, M. Vrljic, P. Grob, E. Nogales, S. Chu, and A. T. Brunger, Proc. Natl. Acad. Sci. USA 108, E304 (2011).Google Scholar
  38. 38.
    Y. Lai, J. Diao, Y. Liu, Y. Ishitsuka, Z. Su, K. Schulten, T. Ha, and Y. K. Shin, Proc. Natl. Acad. Sci. USA 110, 1333 (2013).ADSCrossRefGoogle Scholar
  39. 39.
    J. Gong, Y. Lai, X. Li, M. Wang, J. Leitz, Y. Hu, Y. Zhang, U. B. Choi, D. Cipriano, R. A. Pfuetzner, T. C. Südhof, X. Yang, A. T. Brunger, and J. Diao, Proc. Natl. Acad. Sci. USA 113, E7590 (2016).Google Scholar
  40. 40.
    Y. Lai, U. B. Choi, Y. Zhang, M. Zhao, R. A. Pfuetzner, A. L. Wang, J. Diao, and A. T. Brunger, Proc. Natl. Acad. Sci. USA 113, E4698 (2016).Google Scholar
  41. 41.
    Y. Li, H. Yuan, A. von dem Bussche, M. Creighton, R. H. Hurt, A. B. Kane, and H. Gao, Proc. Natl. Acad. Sci. USA 110, 12295 (2013).ADSCrossRefGoogle Scholar
  42. 42.
    Y. Li, X. Li, Z. Li, and H. Gao, Nanoscale 4, 3768 (2012).ADSCrossRefGoogle Scholar
  43. 43.
    L. Zhang, M. Becton, and X. Wang, J. Phys. Chem. B 119, 3786 (2015).CrossRefGoogle Scholar
  44. 44.
    X. Qiang, X. Wang, Y. Ji, S. Li, and L. He, Polymer 115, 1 (2017).CrossRefGoogle Scholar
  45. 45.
    M. Venturoli, B. Smit, and M. M. Sperotto, Biophys. J. 88, 1778 (2005).CrossRefGoogle Scholar
  46. 46.
    L. Martínez, R. Andrade, E. G. Birgin, and J. M. Martínez, J. Comput. Chem. 30, 2157 (2009).CrossRefGoogle Scholar
  47. 47.
    L. T. Yan, and X. Yu, Nanoscale 3, 3812 (2011).ADSCrossRefGoogle Scholar
  48. 48.
    J. C. Shillcock, and R. Lipowsky, Nat. Mater. 4, 225 (2005).ADSCrossRefGoogle Scholar
  49. 49.
    P. J. Hoogerbrugge, and J. M. V. A. Koelman, Europhys. Lett. 19, 155 (1992).ADSCrossRefGoogle Scholar
  50. 50.
    R. D. Groot, and P. B. Warren, J. Chem. Phys. 107, 4423 (1997).ADSCrossRefGoogle Scholar
  51. 51.
    K. A. Smith, D. Jasnow, and A. C. Balazs, J. Chem. Phys. 127, 084703 (2007).ADSCrossRefGoogle Scholar
  52. 52.
    X. Li, Y. Liu, L. Wang, M. Deng, and H. Liang, Phys. Chem. Chem. Phys. 11, 4051 (2009).CrossRefGoogle Scholar
  53. 53.
    N. Arai, K. Yasuoka, and X. C. Zeng, Nanoscale 5, 9089 (2013).ADSCrossRefGoogle Scholar
  54. 54.
    A. Maiti, and S. McGrother, J. Chem. Phys. 120, 1594 (2004).ADSCrossRefGoogle Scholar
  55. 55.
    A. Alexeev, W. E. Uspal, and A. C. Balazs, ACS Nano 2, 1117 (2008).CrossRefGoogle Scholar
  56. 56.
    H. M. Ding, and Y. Q. Ma, Nanoscale 4, 1116 (2012).ADSCrossRefGoogle Scholar
  57. 57.
    S. Plimpton, J Comput Phys 117, 1 (1995).ADSCrossRefGoogle Scholar
  58. 58.
    A. Lerf, H. He, M. Forster, and J. Klinowski, J. Phys. Chem. B 102, 4477 (1998).CrossRefGoogle Scholar
  59. 59.
    K. Erickson, R. Erni, Z. Lee, N. Alem, W. Gannett, and A. Zettl, Adv. Mater. 22, 4467 (2010).CrossRefGoogle Scholar
  60. 60.
    C. Gomez-Navarro, J. C. Meyer, R. S. Sundaram, A. Chuvilin, S. Kurasch, M. Burghard, K. Kern, and U. Kaiser, Nano Lett. 10, 1144 (2010).ADSCrossRefGoogle Scholar
  61. 61.
    D. Pacilé, J. C. Meyer, A. Fraile Rodríguez, M. Papagno, C. Gómez- Navarro, R. S. Sundaram, M. Burghard, K. Kern, C. Carbone, and U. Kaiser, Carbon 49, 966 (2011).CrossRefGoogle Scholar
  62. 62.
    J. Yang, G. Shi, Y. Tu, and H. Fang, Angew. Chem. Int. Ed. 53, 10190 (2014).CrossRefGoogle Scholar
  63. 63.
    S. Pei, and H. M. Cheng, Carbon 50, 3210 (2012).CrossRefGoogle Scholar
  64. 64.
    A. V. Titov, P. Král, and R. Pearson, ACS Nano 4, 229 (2009).CrossRefGoogle Scholar
  65. 65.
    M. Dallavalle, M. Calvaresi, A. Bottoni, M. Melle-Franco, and F. Zerbetto, ACS Appl. Mater. Interfaces 7, 4406 (2015).CrossRefGoogle Scholar
  66. 66.
    J. Wang, Y. Wei, X. Shi, and H. Gao, RSC Adv. 3, 15776 (2013).CrossRefGoogle Scholar
  67. 67.
    W. Zhu, A. von dem Bussche, X. Yi, Y. Qiu, Z. Wang, P. Weston, R. H. Hurt, A. B. Kane, and H. Gao, Proc. Natl. Acad. Sci. USA 113, 12374 (2016).ADSCrossRefGoogle Scholar
  68. 68.
    A. A. Gurtovenko, and I. Vattulainen, J. Phys. Chem. B 111, 13554 (2007).CrossRefGoogle Scholar
  69. 69.
    W. F. D. Bennett, J. L. MacCallum, M. J. Hinner, S. J. Marrink, and D. P. Tieleman, J. Am. Chem. Soc. 131, 12714 (2009).CrossRefGoogle Scholar
  70. 70.
    M. Nakano, M. Fukuda, T. Kudo, N. Matsuzaki, T. Azuma, K. Sekine, H. Endo, and T. Handa, J. Phys. Chem. B 113, 6745 (2009).CrossRefGoogle Scholar
  71. 71.
    Q. Hu, B. Jiao, X. Shi, R. P. Valle, Y. Y. Zuo, and G. Hu, Nanoscale 7, 18025 (2015).ADSCrossRefGoogle Scholar
  72. 72.
    T. Szabó, O. Berkesi, P. Forgó, K. Josepovits, Y. Sanakis, D. Petridis, and I. Dékány, Chem. Mater. 18, 2740 (2006).CrossRefGoogle Scholar
  73. 73.
    O. C. Compton, and S. B. T. Nguyen, Small 6, 711 (2010).CrossRefGoogle Scholar
  74. 74.
    K. Andre Mkhoyan, A. W. Contryman, J. Silcox, D. A. Stewart, G. Eda, C. Mattevi, S. Miller, and M. Chhowalla, Nano Lett. 9, 1058 (2009).ADSCrossRefGoogle Scholar
  75. 75.
    D. Luo, G. Zhang, J. Liu, and X. Sun, J. Phys. Chem. C 115, 11327 (2011).CrossRefGoogle Scholar
  76. 76.
    S. Kim, S. Zhou, Y. Hu, M. Acik, Y. J. Chabal, C. Berger, W. de Heer, A. Bongiorno, and E. Riedo, Nat. Mater. 11, 544 (2012).ADSCrossRefGoogle Scholar
  77. 77.
    R. Raj, S. C. Maroo, and E. N. Wang, Nano Lett. 13, 1509 (2013).ADSCrossRefGoogle Scholar
  78. 78.
    Q. Mu, G. Su, L. Li, B. O. Gilbertson, L. H. Yu, Q. Zhang, Y. P. Sun, and B. Yan, ACS Appl. Mater. Interfaces 4, 2259 (2012).CrossRefGoogle Scholar
  79. 79.
    L. Hui, J. G. Piao, J. Auletta, K. Hu, Y. Zhu, T. Meyer, H. Liu, and L. Yang, ACS Appl. Mater. Interfaces 6, 13183 (2014).CrossRefGoogle Scholar
  80. 80.
    B. G. Monasterio, B. Alonso, J. Sot, A. B. García-Arribas, D. Gil- Cartón, M. Valle, A. Zurutuza, and F. M. Goñi, Langmuir 33, 8181 (2017).CrossRefGoogle Scholar
  81. 81.
    A. D. Petelska, and Z. A. Figaszewski, Biophys. J. 78, 812 (2000).CrossRefGoogle Scholar
  82. 82.
    M. A. Idiart, and Y. Levin, Phys. Rev. E 69, 061922 (2004).ADSCrossRefGoogle Scholar
  83. 83.
    A. D. Petelska, Cent. Eur. J. Chem. 10, 16 (2012).CrossRefGoogle Scholar
  84. 84.
    E. Evans, and V. Heinrich, C. R. Physique 4, 265 (2003).ADSCrossRefGoogle Scholar
  85. 85.
    E. Evans, V. Heinrich, F. Ludwig, and W. Rawicz, Biophys. J. 85, 2342 (2003).CrossRefGoogle Scholar
  86. 86.
    H. Leontiadou, A. E. Mark, and S. J. Marrink, Biopshys. J. 86, 2156 (2004).CrossRefGoogle Scholar
  87. 87.
    B. Bu, Z. Tian, D. Li, and B. Ji, Front. Mol. Neurosci. 9, 136 (2016).CrossRefGoogle Scholar
  88. 88.
    L. T. Yan, and X. Yu, ACS Nano 3, 2171 (2009).CrossRefGoogle Scholar
  89. 89.
    C. E. Morris, and U. Homann, J. Membr. Biol. 179, 79 (2001).CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Biomechanics and Biomaterials Laboratory, Department of Applied MechanicsBeijing Institute of TechnologyBeijingChina
  2. 2.College of ScienceXi’an University of Science and TechnologyXi’anChina
  3. 3.Department of Cancer BiologyUniversity of Cincinnati College of MedicineCincinnatiUSA
  4. 4.MOE Key Laboratory for Nonequilibrium Synthesis and Modulation of Condensed Matter, School of ScienceXi’an Jiaotong UniversityXi’anChina
  5. 5.Department of Engineering Mechanics, School of Naval Architecture, Ocean and Civil Engineering, and Key Laboratory of HydrodynamicsShanghai Jiao Tong UniversityShanghaiChina
  6. 6.Institute of Applied Mechanics, Department of Engineering MechanicsZhejiang UniversityHangzhouChina

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