Skip to main content

Advertisement

Log in

Molecular Interactions Between Silver Nanoparticles and Model Cell Membranes

  • Original Paper
  • Published:
Topics in Catalysis Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  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):1073–1080

    Article  CAS  Google Scholar 

  2. De Jong WH, Borm PJ (2008) Drug delivery and nanoparticles: applications and hazards. Int J Nanomed 3(2):133

    Article  Google Scholar 

  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):583–593

    Article  CAS  Google Scholar 

  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):6516–6526

    Article  CAS  PubMed  Google Scholar 

  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 146:162–172

    Article  CAS  PubMed  Google Scholar 

  6. Zhao X, Tapec-Dytioco R, Tan W (2003) Ultrasensitive DNA detection using highly fluorescent bioconjugated nanoparticles. J Am Chem Soc 125(38):11474–11475

    Article  CAS  PubMed  Google Scholar 

  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):1253–1271

    Article  CAS  PubMed  Google Scholar 

  8. Biju V (2014) Chemical modifications and bioconjugate reactions of nanomaterials for sensing, imaging, drug delivery and therapy. Chem Soc Rev 43(3):744–764

    Article  CAS  PubMed  Google Scholar 

  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):130–136

    Article  CAS  PubMed  Google Scholar 

  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):570–574

    Article  CAS  Google Scholar 

  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):30–46

    Article  CAS  Google Scholar 

  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):396–409

    Article  CAS  PubMed  Google Scholar 

  13. Walser T, Demou E, Lang DJ, Hellweg S (2011) Prospective environmental life cycle assessment of nanosilver T-shirts. Environ Sci Technol 45(10):4570–4578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Lansdown AB (2004) A review of the use of silver in wound care: facts and fallacies. Br J Nurs 13(6):S6–S19

    Article  PubMed  Google Scholar 

  15. Cao H, Liu X (2010) Silver nanoparticles-modified films versus biomedical device-associated infections. Wiley Interdiscip Rev 2(6):670–684

    CAS  Google Scholar 

  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):2295–2350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 9:2399

    Google Scholar 

  18. Galdiero S, Falanga A, Vitiello M, Cantisani M, Marra V, Galdiero M (2011) Silver nanoparticles as potential antiviral agents. Molecules 16(10):8894–8918

    Article  CAS  PubMed  Google Scholar 

  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 2015:5

    Article  CAS  Google Scholar 

  20. Wong KK, Liu X (2010) Silver nanoparticles—the real “silver bullet” in clinical medicine? MedChemComm 1(2):125–131

    Article  CAS  Google Scholar 

  21. Choi O, Hu Z (2008) Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ Sci Technol 42(12):4583–4588

    Article  CAS  PubMed  Google Scholar 

  22. Ovington LG (2004) The truth about silver. Ostomy/Wound Manag 50(9A Suppl):1S–10S

    Google Scholar 

  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):95–101

    Article  CAS  Google Scholar 

  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):279–290

    Article  CAS  Google Scholar 

  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):7285–7290

    Article  CAS  PubMed  Google Scholar 

  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):1

    Article  CAS  Google Scholar 

  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):249–265

    Article  Google Scholar 

  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):177–182

    Article  CAS  PubMed  Google Scholar 

  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):581–592

    Article  CAS  PubMed  Google Scholar 

  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):1004–1013

    Article  CAS  PubMed  Google Scholar 

  31. Kaba SI, Egorova EM (2015) In vitro studies of the toxic effects of silver nanoparticles on HeLa and U937 cells. Nanotechnol Sci Appl 8:19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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):e105359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 2015:6

    Google Scholar 

  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):103–145

    Article  CAS  Google Scholar 

  35. Chen X, Chen Z (2006) SFG studies on interactions between antimicrobial peptides and supported lipid bilayers. Biochim Biophys Acta 1758(9):1257–1273

    Article  CAS  PubMed  Google Scholar 

  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):61–77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Zhu X, Suhr H, Shen Y (1987) Surface vibrational spectroscopy by infrared-visible sum frequency generation. Phys Rev B 35(6):3047

    Article  CAS  Google Scholar 

  38. Eisenthal K (1996) Liquid interfaces probed by second-harmonic and sum-frequency spectroscopy. Chem Rev 96(4):1343–1360

    Article  CAS  PubMed  Google Scholar 

  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):930–940

    Article  CAS  Google Scholar 

  40. Chen Z, Shen Y, Somorjai GA (2002) Studies of polymer surfaces by sum frequency generation vibrational spectroscopy. Annu Rev Phys Chem 53(1):437–465

    Article  CAS  PubMed  Google Scholar 

  41. Richmond G (2002) Molecular bonding and interactions at aqueous surfaces as probed by vibrational sum frequency spectroscopy. Chem Rev 102(8):2693–2724

    Article  CAS  PubMed  Google Scholar 

  42. Vidal F, Tadjeddine A (2005) Sum-frequency generation spectroscopy of interfaces. Rep Prog Phys 68(5):1095

    Article  CAS  Google Scholar 

  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):6528–6529

    Article  CAS  PubMed  Google Scholar 

  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):3436–3442

    Article  CAS  PubMed  Google Scholar 

  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):8201–8205

    Article  CAS  Google Scholar 

  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):15114–15117

    Article  CAS  PubMed  Google Scholar 

  47. Shen Y-R (2016) Fundamentals of sum-frequency spectroscopy. Cambridge University Press, Cambridge

    Book  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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):12195–12205

    Article  CAS  Google Scholar 

  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):17538–17548

    Article  CAS  Google Scholar 

  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):9873–9884

    Article  CAS  PubMed  Google Scholar 

  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 894712–894712-8

    Google Scholar 

  53. Liu J, Conboy JC (2005) 1, 2-diacyl-phosphatidylcholine flip-flop measured directly by sum-frequency vibrational spectroscopy. Biophys J 89(4):2522–2532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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):10220–10234

    Article  CAS  PubMed  Google Scholar 

  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):13639–13645

    Article  CAS  PubMed  Google Scholar 

  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):8376–8377

    Article  CAS  PubMed  Google Scholar 

  57. Yang P, Ramamoorthy A, Chen Z (2011) Membrane orientation of MSI-78 measured by sum frequency generation vibrational spectroscopy. Langmuir 27(12):7760–7767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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):866–875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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):775–788

    Article  CAS  Google Scholar 

  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):1506–1513

    Article  CAS  PubMed  Google Scholar 

  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):392–396

    Article  CAS  PubMed  Google Scholar 

  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):2275–2292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Chen Z, Zhang Z (1991) Enhanced surface sum frequency generation from LB layer covered silver film. J Appl Phys 69(11):7406–7410

    Article  CAS  Google Scholar 

  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):609–613

    Article  Google Scholar 

  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):5868–5874

    Article  CAS  PubMed  Google Scholar 

  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):7729–7737

    Article  CAS  PubMed  Google Scholar 

  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):517–531

    Article  CAS  PubMed  Google Scholar 

  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):162–168

    Article  CAS  PubMed  Google Scholar 

  69. Gao H, Shi W, Freund LB (2005) Mechanics of receptor-mediated endocytosis. Proc Natl Acad Sci USA 102(27):9469–9474

    Article  CAS  PubMed  Google Scholar 

  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):22718–22729

    Article  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhan Chen.

Ethics declarations

Conflict of interest

The authors declare no competing financial interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1360 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hu, P., Zhang, X., Li, Y. et al. Molecular Interactions Between Silver Nanoparticles and Model Cell Membranes. Top Catal 61, 1148–1162 (2018). https://doi.org/10.1007/s11244-018-0926-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11244-018-0926-1

Keywords

Navigation