Molecular Interactions Between Silver Nanoparticles and Model Cell Membranes

  • Peipei Hu
  • Xiaoxian Zhang
  • Yaoxin Li
  • Cayla Pichan
  • Zhan Chen
Original Paper
  • 12 Downloads

Abstract

Silver (Ag) nanoparticles (NPs) are well known for their antibacterial properties. However, concerns have been raised on their possible toxicity to humans. This work is aimed to understand molecular interactions between Ag NPs and model mammalian cell membranes. Sum frequency generation (SFG) vibrational spectroscopy was used to study such interactions, supplemented by attenuated total reflectance–Fourier transform infrared spectroscopy (ATR–FTIR). Based on the SFG and ATR–FTIR results, it was found that Ag NPs could induce flip-flop of substrate supported lipid bilayers serving as model mammalian cell membranes. The Ag NPs could accumulate onto the model cell membrane and may aggregate. The Ag NP–model cell membrane interactions depend on the Ag NP solution concentration. At low Ag NP solution concentration, lipid flip-flop was observed. At higher Ag NP concentrations, Ag NPs caused lipid flip-flop faster and might aggregate. Therefore, the lipid flip-flop rates and Ag NP accumulation/aggregation rates are directly related to the Ag NP concentration of the subphase in contact with the lipid bilayer.

Keywords

Silver nanoparticle Sum frequency generation (SFG) vibrational spectroscopy ATR–FTIR Model cell membrane Lipid flip-flop 

Notes

Acknowledgements

This research is supported by the University of Michigan. P.H thanks for University of Michigan Rackham Graduate School for the Rackham Merit Fellowship.

Compliance with Ethical Standards

Conflict of interest

The authors declare no competing financial interest.

Supplementary material

11244_2018_926_MOESM1_ESM.docx (1.3 mb)
Supplementary material 1 (DOCX 1360 KB)

References

  1. 1.
    Kuo C-W, Chueh D-Y, Singh N, Chien F-C, Chen P (2011) Targeted nuclear delivery using peptide-coated quantum dots. Bioconjugate Chem 22(6):1073–1080CrossRefGoogle Scholar
  2. 2.
    De Jong WH, Borm PJ (2008) Drug delivery and nanoparticles: applications and hazards. Int J Nanomed 3(2):133CrossRefGoogle Scholar
  3. 3.
    Fang B, Luo J, Chen Y, Wanjala BN, Loukrakpam R, Hong J, Yin J, Hu X, Hu P, Zhong CJ (2011) Nanoengineered PtVFe/C cathode electrocatalysts in PEM fuel cells: catalyst activity and stability. ChemCatChem 3(3):583–593CrossRefGoogle Scholar
  4. 4.
    Yin J, Hu P, Luo J, Wang L, Cohen MF, Zhong C-J (2011) Molecularly mediated thin film assembly of nanoparticles on flexible devices: electrical conductivity versus device strains in different gas/vapor environment. ACS Nano 5(8):6516–6526CrossRefGoogle Scholar
  5. 5.
    Yu F, Ma J, Wang J, Zhang M, Zheng J (2016) Magnetic iron oxide nanoparticles functionalized multi-walled carbon nanotubes for toluene, ethylbenzene and xylene removal from aqueous solution. Chemosphere 146:162–172CrossRefGoogle Scholar
  6. 6.
    Zhao X, Tapec-Dytioco R, Tan W (2003) Ultrasensitive DNA detection using highly fluorescent bioconjugated nanoparticles. J Am Chem Soc 125(38):11474–11475CrossRefGoogle Scholar
  7. 7.
    Bamrungsap S, Zhao Z, Chen T, Wang L, Li C, Fu T, Tan W (2012) Nanotechnology in therapeutics: a focus on nanoparticles as a drug delivery system. Nanomedicine 7(8):1253–1271CrossRefGoogle Scholar
  8. 8.
    Biju V (2014) Chemical modifications and bioconjugate reactions of nanomaterials for sensing, imaging, drug delivery and therapy. Chem Soc Rev 43(3):744–764CrossRefGoogle Scholar
  9. 9.
    Zhang L, Xu J, Mi L, Gong H, Jiang S, Yu Q (2012) Multifunctional magnetic–plasmonic nanoparticles for fast concentration and sensitive detection of bacteria using SERS. Biosens. Bioelectron 31(1):130–136CrossRefGoogle Scholar
  10. 10.
    Kokura S, Handa O, Takagi T, Ishikawa T, Naito Y, Yoshikawa T (2010) Silver nanoparticles as a safe preservative for use in cosmetics. Nanomed Nanotechnol Biol Med 6(4):570–574CrossRefGoogle Scholar
  11. 11.
    Cushen M, Kerry J, Morris M, Cruz-Romero M, Cummins E (2012) Nanotechnologies in the food industry—recent developments, risks and regulation. Trends Food Sci Technol 24(1):30–46CrossRefGoogle Scholar
  12. 12.
    Blaser SA, Scheringer M, MacLeod M, Hungerbühler K (2008) Estimation of cumulative aquatic exposure and risk due to silver: contribution of nano-functionalized plastics and textiles. Sci Total Environ 390(2):396–409CrossRefGoogle Scholar
  13. 13.
    Walser T, Demou E, Lang DJ, Hellweg S (2011) Prospective environmental life cycle assessment of nanosilver T-shirts. Environ Sci Technol 45(10):4570–4578CrossRefGoogle Scholar
  14. 14.
    Lansdown AB (2004) A review of the use of silver in wound care: facts and fallacies. Br J Nurs 13(6):S6–S19CrossRefGoogle Scholar
  15. 15.
    Cao H, Liu X (2010) Silver nanoparticles-modified films versus biomedical device-associated infections. Wiley Interdiscip Rev 2(6):670–684Google Scholar
  16. 16.
    Reidy B, Haase A, Luch A, Dawson KA, Lynch I (2013) Mechanisms of silver nanoparticle release, transformation and toxicity: a critical review of current knowledge and recommendations for future studies and applications. Materials 6(6):2295–2350CrossRefGoogle Scholar
  17. 17.
    Ge L, Li Q, Wang M, Ouyang J, Li X, Xing MM (2014) Nanosilver particles in medical applications: synthesis, performance, and toxicity. Int J Nanomed 9:2399Google Scholar
  18. 18.
    Galdiero S, Falanga A, Vitiello M, Cantisani M, Marra V, Galdiero M (2011) Silver nanoparticles as potential antiviral agents. Molecules 16(10):8894–8918CrossRefGoogle Scholar
  19. 19.
    Murphy M, Ting K, Zhang X, Soo C, Zheng Z (2015) Current development of silver nanoparticle preparation, investigation, and application in the field of medicine. J Nanomater 2015:5CrossRefGoogle Scholar
  20. 20.
    Wong KK, Liu X (2010) Silver nanoparticles—the real “silver bullet” in clinical medicine? MedChemComm 1(2):125–131CrossRefGoogle Scholar
  21. 21.
    Choi O, Hu Z (2008) Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ Sci Technol 42(12):4583–4588CrossRefGoogle Scholar
  22. 22.
    Ovington LG (2004) The truth about silver. Ostomy/Wound Manag 50(9A Suppl):1S–10SGoogle Scholar
  23. 23.
    Kim JS, Kuk E, Yu KN, Kim J-H, Park SJ, Lee HJ, Kim SH, Park YK, Park YH, Hwang C-Y (2007) Antimicrobial effects of silver nanoparticles. Nanomed Nanotechnol Biol Med 3(1):95–101CrossRefGoogle Scholar
  24. 24.
    AshaRani P, Low Kah Mun G, Hande MP, Valiyaveettil S (2008) Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3(2):279–290CrossRefGoogle Scholar
  25. 25.
    Fabrega J, Fawcett SR, Renshaw JC, Lead JR (2009) Silver nanoparticle impact on bacterial growth: effect of pH, concentration, and organic matter. Environ Sci Technol 43(19):7285–7290CrossRefGoogle Scholar
  26. 26.
    Gliga AR, Skoglund S, Wallinder IO, Fadeel B, Karlsson HL (2014) Size-dependent cytotoxicity of silver nanoparticles in human lung cells: the role of cellular uptake, agglomeration and Ag release. Part Fibre Toxicol 11(1):1CrossRefGoogle Scholar
  27. 27.
    Santra TS, Tseng F-GK, Barik TK (2014) Biosynthesis of silver and gold nanoparticles for potential biomedical applications—a brief review. J Nanopharm Drug Deliv 2(4):249–265CrossRefGoogle Scholar
  28. 28.
    Sondi I, Salopek-Sondi B (2004) Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J Colloid Interface Sci 275(1):177–182CrossRefGoogle Scholar
  29. 29.
    Milić M, Leitinger G, Pavičić I, Zebić Avdičević M, Dobrović S, Goessler W, Vinković Vrček I (2015) Cellular uptake and toxicity effects of silver nanoparticles in mammalian kidney cells. J Appl Toxicol 35(6):581–592CrossRefGoogle Scholar
  30. 30.
    Genter MB, Newman NC, Shertzer HG, Ali SF, Bolon B (2012) Distribution and systemic effects of intranasally administered 25 nm silver nanoparticles in adult mice. Toxicol Pathol 40(7):1004–1013CrossRefGoogle Scholar
  31. 31.
    Kaba SI, Egorova EM (2015) In vitro studies of the toxic effects of silver nanoparticles on HeLa and U937 cells. Nanotechnol Sci Appl 8:19CrossRefGoogle Scholar
  32. 32.
    Söderstjerna E, Bauer P, Cedervall T, Abdshill H, Johansson F, Johansson UE (2014) Silver and gold nanoparticles exposure to in vitro cultured retina—studies on nanoparticle internalization, apoptosis, oxidative stress, glial-and microglial activity. PLoS ONE 9(8):e105359CrossRefGoogle Scholar
  33. 33.
    Sambale F, Wagner S, Stahl F, Khaydarov R, Scheper T, Bahnemann D (2015) Investigations of the toxic effect of silver nanoparticles on mammalian cell lines. J Nanomater 2015:6Google Scholar
  34. 34.
    Lambert AG, Davies PB, Neivandt DJ (2005) Implementing the theory of sum frequency generation vibrational spectroscopy: a tutorial review. Appl Spectrosc Rev 40(2):103–145CrossRefGoogle Scholar
  35. 35.
    Chen X, Chen Z (2006) SFG studies on interactions between antimicrobial peptides and supported lipid bilayers. Biochim Biophys Acta 1758(9):1257–1273CrossRefGoogle Scholar
  36. 36.
    Ye S, Nguyen KT, Le Clair SV, Chen Z (2009) In situ molecular level studies on membrane related peptides and proteins in real time using sum frequency generation vibrational spectroscopy. J Struct Biol 168(1):61–77CrossRefGoogle Scholar
  37. 37.
    Zhu X, Suhr H, Shen Y (1987) Surface vibrational spectroscopy by infrared-visible sum frequency generation. Phys Rev B 35(6):3047CrossRefGoogle Scholar
  38. 38.
    Eisenthal K (1996) Liquid interfaces probed by second-harmonic and sum-frequency spectroscopy. Chem Rev 96(4):1343–1360CrossRefGoogle Scholar
  39. 39.
    Gracias D, Chen Z, Shen Y, Somorjai G (1999) Molecular characterization of polymer and polymer blend surfaces. Combined sum frequency generation surface vibrational spectroscopy and scanning force microscopy studies. Acc Chem Res 32(11):930–940CrossRefGoogle Scholar
  40. 40.
    Chen Z, Shen Y, Somorjai GA (2002) Studies of polymer surfaces by sum frequency generation vibrational spectroscopy. Annu Rev Phys Chem 53(1):437–465CrossRefGoogle Scholar
  41. 41.
    Richmond G (2002) Molecular bonding and interactions at aqueous surfaces as probed by vibrational sum frequency spectroscopy. Chem Rev 102(8):2693–2724CrossRefGoogle Scholar
  42. 42.
    Vidal F, Tadjeddine A (2005) Sum-frequency generation spectroscopy of interfaces. Rep Prog Phys 68(5):1095CrossRefGoogle Scholar
  43. 43.
    Ye H, Abu-Akeel A, Huang J, Katz HE, Gracias DH (2006) Probing organic field effect transistors in situ during operation using SFG. J Am Chem Soc 128(20):6528–6529CrossRefGoogle Scholar
  44. 44.
    Li Q, Kuo CW, Yang Z, Chen P, Chou KC (2009) Surface-enhanced IR–visible sum frequency generation vibrational spectroscopy. Phys Chem Chem Phys 11(18):3436–3442CrossRefGoogle Scholar
  45. 45.
    Yang Z, Li Q, Chou KC (2009) Structures of water molecules at the interfaces of aqueous salt solutions and silica: cation effects. J Phys Chem C 113(19):8201–8205CrossRefGoogle Scholar
  46. 46.
    Hu D, Chou KC (2014) Re-evaluating the surface tension analysis of polyelectrolyte-surfactant mixtures using phase-sensitive sum frequency generation spectroscopy. J Am Chem Soc 136(43):15114–15117CrossRefGoogle Scholar
  47. 47.
    Shen Y-R (2016) Fundamentals of sum-frequency spectroscopy. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  48. 48.
    Xiao M, Jasensky J, Zhang X, Li Y, Pichan C, Lu X, Chen Z (2016) Influences of side chain and substrate on polythiophene thin film surface, bulk, and buried interfacial structures. Phys Chem Chem Phys.  https://doi.org/10.1039/c6cp04155h Google Scholar
  49. 49.
    Zhang C, Wu F-G, Hu P, Chen Z (2014) Interaction of polyethylenimine with model cell membranes studied by linear and nonlinear spectroscopic techniques. J Phys Chem C 118(23):12195–12205CrossRefGoogle Scholar
  50. 50.
    Wu F-G, Yang P, Zhang C, Han X, Song M, Chen Z (2014) Investigation of drug-model cell membrane interactions using sum frequency generation vibrational spectroscopy: a case study of chlorpromazine. J Phys Chem C 118(31):17538–17548CrossRefGoogle Scholar
  51. 51.
    Hu P, Zhang X, Zhang C, Chen Z (2015) Molecular interactions between gold nanoparticles and model cell membranes. Phys Chem Chem Phys 17(15):9873–9884CrossRefGoogle Scholar
  52. 52.
    Zhang C, Jasensky J, Wu J, Chen Z (2014) Combining surface sensitive vibrational spectroscopy and fluorescence microscopy to study biological interfaces. SPIE BiOS, International Society for Optics and Photonics, pp 894712–894712-8Google Scholar
  53. 53.
    Liu J, Conboy JC (2005) 1, 2-diacyl-phosphatidylcholine flip-flop measured directly by sum-frequency vibrational spectroscopy. Biophys J 89(4):2522–2532CrossRefGoogle Scholar
  54. 54.
    Anglin TC, Conboy JC (2009) Kinetics and thermodynamics of flip-flop in binary phospholipid membranes measured by sum-frequency vibrational spectroscopy. Biochemistry 48(43):10220–10234CrossRefGoogle Scholar
  55. 55.
    Nam J, Won N, Jin H, Chung H, Kim S (2009) pH-induced aggregation of gold nanoparticles for photothermal cancer therapy. J Am Chem Soc 131(38):13639–13645CrossRefGoogle Scholar
  56. 56.
    Liu J, Conboy JC (2004) Direct measurement of the transbilayer movement of phospholipids by sum-frequency vibrational spectroscopy. J Am Chem Soc 126(27):8376–8377CrossRefGoogle Scholar
  57. 57.
    Yang P, Ramamoorthy A, Chen Z (2011) Membrane orientation of MSI-78 measured by sum frequency generation vibrational spectroscopy. Langmuir 27(12):7760–7767CrossRefGoogle Scholar
  58. 58.
    Chen X, Wang J, Kristalyn CB, Chen Z (2007) Real-time structural investigation of a lipid bilayer during its interaction with melittin using sum frequency generation vibrational spectroscopy. Biophys J 93(3):866–875CrossRefGoogle Scholar
  59. 59.
    Parveen A, Rao S (2015) Cytotoxicity and genotoxicity of biosynthesized gold and silver nanoparticles on human cancer cell lines. J Cluster Sci 26(3):775–788CrossRefGoogle Scholar
  60. 60.
    Pascarelli NA, Moretti E, Terzuoli G, Lamboglia A, Renieri T, Fioravanti A, Collodel G (2013) Effects of gold and silver nanoparticles in cultured human osteoarthritic chondrocytes. J Appl Toxicol 33(12):1506–1513CrossRefGoogle Scholar
  61. 61.
    Moretti E, Terzuoli G, Renieri T, Iacoponi F, Castellini C, Giordano C, Collodel G (2013) In vitro effect of gold and silver nanoparticles on human spermatozoa. Andrologia 45(6):392–396CrossRefGoogle Scholar
  62. 62.
    Lis D, Cecchet F (2014) Localized surface plasmon resonances in nanostructures to enhance nonlinear vibrational spectroscopies: towards an astonishing molecular sensitivity. Beilstein J Nanotechnol 5(1):2275–2292CrossRefGoogle Scholar
  63. 63.
    Chen Z, Zhang Z (1991) Enhanced surface sum frequency generation from LB layer covered silver film. J Appl Phys 69(11):7406–7410CrossRefGoogle Scholar
  64. 64.
    Alieva E, Petrov YE, Yakovlev V, Eliel E, Van Der Ham E, Vrehen Q, Van Der Meer A, Sychugov V (1997) Giant enhancement of sum-frequency generation upon excitation of a surface plasmon-polariton. J Exp Theor Phys Lett 66(9):609–613CrossRefGoogle Scholar
  65. 65.
    Goreham RV, Thompson VC, Samura Y, Gibson CT, Shapter JG, Köper I (2015) Interaction of silver nanoparticles with tethered bilayer lipid membranes. Langmuir 31(21):5868–5874CrossRefGoogle Scholar
  66. 66.
    Pluchery O, Humbert C, Valamanesh M, Lacaze E, Busson B (2009) Enhanced detection of thiophenol adsorbed on gold nanoparticles by SFG and DFG nonlinear optical spectroscopy. Phys Chem Chem Phys 11(35):7729–7737CrossRefGoogle Scholar
  67. 67.
    Fabrega J, Luoma SN, Tyler CR, Galloway TS, Lead JR (2011) Silver nanoparticles: behaviour and effects in the aquatic environment. Environ Int 37(2):517–531CrossRefGoogle Scholar
  68. 68.
    Park E-J, Bae E, Yi J, Kim Y, Choi K, Lee SH, Yoon J, Lee BC, Park K (2010) Repeated-dose toxicity and inflammatory responses in mice by oral administration of silver nanoparticles. Environ Toxicol Pharmacol 30(2):162–168CrossRefGoogle Scholar
  69. 69.
    Gao H, Shi W, Freund LB (2005) Mechanics of receptor-mediated endocytosis. Proc Natl Acad Sci USA 102(27):9469–9474CrossRefGoogle Scholar
  70. 70.
    Hu P, Quan W, Liu B, Pichan C, Chen Z (2016) Molecular interactions between gold nanoparticles and model cell membranes: a study of nanoparticle surface charge effect. J Phys Chem C 120(39):22718–22729CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Peipei Hu
    • 1
  • Xiaoxian Zhang
    • 2
  • Yaoxin Li
    • 1
  • Cayla Pichan
    • 1
  • Zhan Chen
    • 1
  1. 1.Department of ChemistryUniversity of MichiganAnn ArborUSA
  2. 2.CAS Key Laboratory of Standardization and Measurement for Nanotechnology, CAS Center for Excellence in NanoscienceNational Center for Nanoscience and TechnologyBeijingChina

Personalised recommendations