Dissolution of citrate-stabilized, polyethylene glycol–coated carboxyl and amine-functionalized gold nanoparticles in simulated biological fluids and environmental media

Abstract

Dissolution is an important property utilized to elucidate both short- and long-term effects of nanoparticles for their potential to cause harm to humans and the environment. Nanoparticles may therefore be classified based on their (bio)durability between those that are amenable and those that are resistant to dissolution, biodegradation and/or disintegration. The dissolution kinetics of uncoated citrate-stabilized, polyethylene glycol–coated (PEGylated) gold nanoparticles functionalized with carboxyl and amine functional groups in simulated biological and environmental fluids at physiological and room temperature, respectively, were studied using the static dialysis protocol to predict their (bio)durability. Citrate-stabilized gold nanoparticles showed high degrees of resistance to dissolution in the simulated media unlike those which were coated with polyethylene glycol and functionalized with carboxyl and amine functional groups. Generally, the extent of AuNP dissolution in acidic media (phagolysosomal fluid and gastric fluid) was greater than that in neutral or alkaline media such as Gamble’s fluid, blood plasma and intestinal fluids, freshwater and seawater. However, in all these experimental conditions, the particles did not completely dissolve. In the case of amine-functionalized AuNPs, the nanoparticles released a maximum of only 15% of their original concentration whereas carboxyl-functionalized and citrate-stabilized gold nanoparticles released 9% and 8.5% of gold ions, respectively. The rate and degree of dissolution depended on the surface functionalization, pH, ionic strength of the simulated fluid and particle aggregation. Therefore, the results indicate that gold nanoparticles with low dissolution rates are expected to be (bio)durable in biological and environmental surroundings; thus, they might impose long-term effects on humans and the environment. In contrast, those with high dissolution rate are not (bio)durable and hence may cause short-term effects.

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References

  1. Adeleye AS, Conway JR, Perez T, Rutten P, Keller A (2014) Influence of extracellular polymeric substances on the long-term fate, dissolution, and speciation of copper-based nanoparticles. Environ Sci Technol 48(21):12561–12568

    CAS  Google Scholar 

  2. Aiken GR, Hsu-Kim H, Ryan JN (2011) Influence of dissolved organic matter on the environmental fate of metals, nanoparticles, and colloids. Environ Sci Technol 45:3196–3201

    CAS  Google Scholar 

  3. Alkilany AM, Murphy CJ (2010) Toxicity and cellular uptake of gold nanoparticles: what we have learned so far? J Nanopart Res 12(7):2313–2333

    CAS  Google Scholar 

  4. Arnida MM, Ray A, Peterson CM, Ghandehari H (2011) Geometry and surface characteristics of gold nanoparticles influence their biodistribution and uptake by macrophages. Eur J Pharm Biopharm 77(3):417–423

    CAS  Google Scholar 

  5. Arts JH, Hadi M, Irfan MA, Keene AM, Kreiling R, Lyon D et al (2015) A decision-making framework for the grouping and testing of nanomaterials (DF4nanoGrouping). Regul Toxicol Pharmacol 71(2):S1–S27

    CAS  Google Scholar 

  6. Aryal S, Remant BK, Dharmaraj N, Bhattarai N, Kim CH, Kim HY (2006) Spectroscopic identification of SAu interaction in cysteine capped gold nanoparticles. Spectrochim Acta Part A Mol Biomol Spectrosc 63(1):160–163

    Google Scholar 

  7. Atkins P, de Paula J. Atkins’ physical chemistry. Oxford University Press. 2006. 8th Edition

  8. Auffan M, Rose J, Wiesner MR, Bottero JY (2009) Chemical stability of metallic nanoparticles: a parameter controlling their potential cellular toxicity in vitro. Environ Pollut 157(4):1127–1133

    CAS  Google Scholar 

  9. Avellan A, Simonin M, McGivney E, Bossa N, Spielman-Sun E, Rocca JD, Bernhardt ES, Geitner NK, Unrine JM, Wiesner MR, Lowry GV (2018) Gold nanoparticle biodissolution by a freshwater macrophyte and its associated microbiome. Nat Nanotechnol 13(11):1072–1077

    CAS  Google Scholar 

  10. Avramescu ML, Rasmussen PE, Chénier M, Gardner HD (2017) Influence of pH, particle size and crystal form on dissolution behaviour of engineered nanomaterials. Environ Sci Pollut Res 24(2):1553–1564

    CAS  Google Scholar 

  11. Bachler G, Losert S, Umehara Y, von Goetz N, Rodriguez-Lorenzo L, Petri-Fink A, Rothen-Rutishauser B, Hungerbuehler K (2015) Translocation of gold nanoparticles across the lung epithelial tissue barrier: combining in vitro and in silico methods to substitute in vivo experiments. Part Fibre Toxicol 12(1):18

    Google Scholar 

  12. Badawy AM, Luxton TP, Silva RG, Scheckel KG, Suidan MT, Tolaymat TM (2010) Impact of environmental conditions (pH, ionic strength, and electrolyte type) on the surface charge and aggregation of silver nanoparticles suspensions. Environ Sci Technol 44(4):1260–1266

    Google Scholar 

  13. Baker TJ, Tyler CR, Galloway TS (2014) Impacts of metal and metal oxide nanoparticles on marine organisms. Environ Pollut 186:257–271

    CAS  Google Scholar 

  14. Balasubramanian SK, Jittiwat J, Manikandan J, Ong CN, Liya EY, Ong WY (2010) Biodistribution of gold nanoparticles and gene expression changes in the liver and spleen after intravenous administration in rats. Biomaterials. 31(8):2034–2042

    CAS  Google Scholar 

  15. Bardaxoglou G, Rouleau C, Pelletier E (2017) High stability and very slow dissolution of bare and polymer coated silver nanoparticles dispersed in river and coastal waters. J Aquat Pollut Toxicol 1(2):1–15

    Google Scholar 

  16. Bian SW, Mudunkotuwa IA, Rupasinghe T, Grassian VH (2011) Aggregation and dissolution of 4 nm ZnO nanoparticles in aqueous environments: influence of pH, ionic strength, size, and adsorption of humic acid. Langmuir. 27(10):6059–6068

    CAS  Google Scholar 

  17. Botha TL, James TE, Wepener V (2015) Comparative aquatic toxicity of gold nanoparticles and ionic gold using a species sensitivity distribution approach. J Nanomater 2015:1–16

    Google Scholar 

  18. Bozich JS, Lohse SE, Torelli MD, Murphy CJ, Hamers RJ, Klaper RD (2014) Surface chemistry, charge and ligand type impact the toxicity of gold nanoparticles to Daphnia magna. Environ Sci Nano 1(3):260–270

    CAS  Google Scholar 

  19. Breitner EK, Hussain SM, Comfort KK (2015) The role of biological fluid and dynamic flow in the behavior and cellular interactions of gold nanoparticles. J Nanobiotechnol 13(1):56

    Google Scholar 

  20. Chambers BA, Afrooz AN, Bae S, Aich N, Katz L, Saleh NB et al (2014) Effects of chloride and ionic strength on physical morphology, dissolution, and bacterial toxicity of silver nanoparticles. Environ Sci Technol 48(1):761–769

    CAS  Google Scholar 

  21. Chen M, Jafvert CT (2018) Anion recovery from water by cross-linked cationic surfactant nanoparticles across dialysis membranes. Environ Sci Nano 5(6):1350–1360

    CAS  Google Scholar 

  22. Chen H, Wang Y, Wang Y, Dong S, Wang E (2006) One-step preparation and characterization of PDDA-protected gold nanoparticles. Polymer (Guildf) 47(2):763–766

    CAS  Google Scholar 

  23. Cherevko S, Zeradjanin A, Keeley GP, Mayrhofer K (2014) A comparative study on gold and platinum dissolution in acidic and alkaline media. J Electrochem Soc 161(12):H822–H830

    Google Scholar 

  24. Cohen JM, Teeguarden JG, Demokritou P (2014) An integrated approach for the in vitro dosimetry of engineered nanomaterials. Part Fibre Toxicol 11(1):20

    Google Scholar 

  25. Donovan AR, Adams CD, Ma Y, Stephan C, Eichholz T, Shi H (2016) Single particle ICP-MS characterization of titanium dioxide, silver, and gold nanoparticles during drinking water treatment. Chemosphere. 144:148–153

    CAS  Google Scholar 

  26. Ferry JL, Craig P, Hexel C, Sisco P, Frey R, Pennington PL, Fulton MH, Scott IG, Decho AW, Kashiwada S, Murphy CJ, Shaw TJ (2009) Transfer of gold nanoparticles from the water column to the estuarine food web. Nat Nanotechnol 4(7):441–444

    CAS  Google Scholar 

  27. Fratoddi I, Venditti I, Cametti C, Russo MV (2015) How toxic are gold nanoparticles? The state-of-the-art. Nano Res 8(6):1771–1799

    CAS  Google Scholar 

  28. Guerrini L, Alvarez-Puebla RA, Pazos-Perez N (2018) Surface modifications of nanoparticles for stability in biological fluids. Materials (Basel) 11(7):1145

    Google Scholar 

  29. Hitchman A, Sambrook Smith GH, Ju-Nam Y, Sterling M, Lead JR (2013) The effect of environmentally relevant conditions on PVP stabilised gold nanoparticles. Chemosphere. 90(2):410–416

    CAS  Google Scholar 

  30. Hong SC, Lee JH, Lee J, Kim HY, Park JY, Cho J, Lee J, Han DW (2011) Subtle cytotoxicity and genotoxicity differences in superparamagnetic iron oxide nanoparticles coated with various functional groups. Int J Nanomedicine 6:3219–3231

    CAS  Google Scholar 

  31. Hornos Carneiro MF, Barbosa F Jr (2016) Gold nanoparticles: a critical review of therapeutic applications and toxicological aspects. J Toxicol Environ Heal - Part B Crit Rev 19(3–4):129–148

    CAS  Google Scholar 

  32. Hosseini-Monfared H, Parchegani F, Alavi S (2015) Carboxylic acid effects on the size and catalytic activity of magnetite nanoparticles. J Colloid Interface Sci 437:1–9

    CAS  Google Scholar 

  33. Hull MS, Chaurand P, Rose J, Auffan M, Bottero JY, Jones JC, Schultz IR, Vikesland PJ (2011) Filter-feeding bivalves store and biodeposit colloidally stable gold nanoparticles. Environ Sci Technol 45(15):6592–6599

    CAS  Google Scholar 

  34. Islam NU, Jalil K, Shahid M, Rauf A, Muhammad N, Khan A, Shah MR, Khan MA (2019) Green synthesis and biological activities of gold nanoparticles functionalized with Salix alba. Arab J Chem 12(8):2914–2925

    Google Scholar 

  35. Kittler S, Greulich C, Diendorf J, Koller M, Epple M (2010) Toxicity of silver nanoparticles increases during storage because of slow dissolution under release of silver ions. Chem Mater 22(16):4548–4554

    CAS  Google Scholar 

  36. Kreyling WG, Fertsch-Gapp S, Schäffler M, Johnston BD, Haberl N, Pfeiffer C, Diendorf J, Schleh C, Hirn S, Semmler-Behnke M, Epple M, Parak WJ (2014) In vitro and in vivo interactions of selected nanoparticles with rodent serum proteins and their consequences in biokinetics. Beilstein J Nanotechnol 5(1):1699–1711

    Google Scholar 

  37. Laux P, Riebeling C, Booth AM, Brain JD, Brunner J, Cerrillo C, Creutzenberg O, Estrela-Lopis I, Gebel T, Johanson G, Jungnickel H, Kock H, Tentschert J, Tlili A, Schäffer A, Sips AJAM, Yokel RA, Luch A (2017) Nanoimpact biokinetics of nanomaterials : the role of biopersistence. NanoImpact. 6:69–80

    Google Scholar 

  38. Lemmerer A, Govindraju S, Johnston M, Motloung X, Savig KL (2015) Co-crystals and molecular salts of carboxylic acid/pyridine complexes: can calculated pKa’s predict proton transfer? A case study of nine complexes. CrystEngComm. 17(19):3591–3595

    CAS  Google Scholar 

  39. Li Y, Zhang W, Niu J, Chen Y (2013) Surface-coating-dependent dissolution, aggregation, and reactive oxygen species (ROS) generation of silver nanoparticles under different irradiation conditions. Environ Sci Technol 47(18):10293–10301

    CAS  Google Scholar 

  40. Libralato G, Galdiero E, Falanga A, Carotenuto R, De Alteriis E, Guida M (2017) Toxicity effects of functionalized quantum dots, gold and polystyrene nanoparticles on target aquatic biological models: a review. Molecules. 22(9):1439

    Google Scholar 

  41. Lin Z, Monteiro-Riviere NA, Kannan R, Riviere JE (2016) A computational framework for interspecies pharmacokinetics, exposure and toxicity assessment of gold nanoparticles. Nanomedicine. 11(2):107–119

    CAS  Google Scholar 

  42. Ludwig C, Devidal JL, Casey WH (1996) The effect of different functional groups on the ligand-promoted dissolution of NiO and other oxide minerals. Geochim Cosmochim Acta 60(2):213–224

    CAS  Google Scholar 

  43. Marchewka MK, Pietraszko A (2003) Structure and spectra of melaminium citrate. J Phys Chem Solids 64(11):2169–2181

    CAS  Google Scholar 

  44. Marques MR, Loebenberg R, Almukainzi M (2011) Simulated biological fluids with possible application in dissolution testing. Dissolution Technol 18(3):15–28

    CAS  Google Scholar 

  45. Oberdörster G, Kuhlbusch TAJ (2018) In vivo effects: methodologies and biokinetics of inhaled nanomaterials. NanoImpact. 10(April 2017):38–60

    Google Scholar 

  46. Oh N, Park JH (2014) Endocytosis and exocytosis of nanoparticles in mammalian cells. Int J Nanomedicine 9(Suppl 1):51

    Google Scholar 

  47. Oyabu T, Myojo T, Lee BW, Okada T, Izumi H, Yoshiura Y, Tomonaga T, Li YS, Kawai K, Shimada M, Kubo M, Yamamoto K, Kawaguchi K, Sasaki T, Morimoto Y (2017) Biopersistence of NiO and TiO2 nanoparticles following intratracheal instillation and inhalation. Int J Mol Sci 18(12):2757

    Google Scholar 

  48. Probst M, Schmidt M, Tietz K, Klein S, Weitschies W, Seidlitz A (2017) In vitro dissolution testing of parenteral aqueous solutions and oily suspensions of paracetamol and prednisolone. Int J Pharm 532(1):519–527

    CAS  Google Scholar 

  49. Rak MJ, Saadé NK, Friščić T, Moores A (2014) Mechanosynthesis of ultra-small monodisperse amine-stabilized gold nanoparticles with controllable size. Green Chem 16(1):86–89

    CAS  Google Scholar 

  50. Rouhana LL, Jaber JA, Schlenoff JB (2007) Aggregation-resistant water-soluble gold nanoparticles. Langmuir. 23(26):12799–12801

    CAS  Google Scholar 

  51. Sakka Y, Skjolding LM, Mackevica A, Filser J, Baun A (2016) Behavior and chronic toxicity of two differently stabilized silver nanoparticles to Daphnia magna. Aquat Toxicol 177:526–535

    CAS  Google Scholar 

  52. Simpson CA, Salleng KJ, Cliffel DE, Feldheim DL (2013) In vivo toxicity, biodistribution, and clearance of glutathione-coated gold nanoparticles. Nanomed Nanotechnol Biol Med 9(2):257–263

    CAS  Google Scholar 

  53. Sperling RA, Parak WJ (2010) Surface modification, functionalization and bioconjugation of colloidal inorganic nanoparticles. Philos Trans R Soc A Math Phys Eng Sci 368(1915):1333–1383

    CAS  Google Scholar 

  54. Stebounova LV, Guio E, Grassian VH (2011) Silver nanoparticles in simulated biological media: a study of aggregation, sedimentation, and dissolution. J Nanopart Res 13(1):233–244

    CAS  Google Scholar 

  55. Sun X, Dong S, Wang E (2005) One-step preparation of highly concentrated well-stable gold colloids by direct mix of polyelectrolyte and HAuCl4 aqueous solutions at room temperature. J Colloid Interface Sci 288(1):301–303

    CAS  Google Scholar 

  56. Tejamaya M, Römer I, Merrifield RC, Lead JR (2012) Stability of citrate, PVP, and PEG coated silver nanoparticles in ecotoxicology media. Environ Sci Technol 46(13):7011–7017

    CAS  Google Scholar 

  57. Tiwari PM, Vig K, Dennis VA, Singh SR (2011) Functionalized gold nanoparticles and their biomedical applications. Nanomaterials 1(1):31–63

    CAS  Google Scholar 

  58. Utembe W, Potgieter K, Stefaniak AB, Gulumian M (2015) Dissolution and biodurability: important parameters needed for risk assessment of nanomaterials. Part Fibre Toxicol 12(1):11

    Google Scholar 

  59. Vetten MA, Tlotleng N, Rascher DT, Skepu A, Keter FK, Boodhia K et al (2013) Label-free in vitro toxicity and uptake assessment of citrate stabilised gold nanoparticles in three cell lines. Part Fibre Toxicol 10(1):50

    Google Scholar 

  60. Wang A, Ng HP, Xu Y, Li Y, Zheng Y, Yu J, Han F, Peng F, Fu L (2014) Gold nanoparticles: synthesis, stability test, and application for the rice growth. J Nanomater 2014:1–6

    Google Scholar 

  61. Wang N, Tong T, Xie M, Gaillard JF (2016) Lifetime and dissolution kinetics of zinc oxide nanoparticles in aqueous media. Nanotechnology. 27(32):324001

    Google Scholar 

  62. Weber CI. Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms Fifth Edition October 2002. Environ Prot. 2002;232(October):266. Availabkle from: http://www.epa.gov/waterscience/WET/disk1/ctm.pdf

  63. Zeng S, Yong KT, Roy I, Dinh XQ, Yu X, Luan F (2011) A review on functionalized gold nanoparticles for biosensing applications. Plasmonics. 6(3):491–506

    CAS  Google Scholar 

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Funding

This work was funded by the South African Department of Science and Technology (DST) and the National Institute for Occupational Health (NIOH).

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Correspondence to Mary Gulumian.

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Mbanga, O., Cukrowska, E. & Gulumian, M. Dissolution of citrate-stabilized, polyethylene glycol–coated carboxyl and amine-functionalized gold nanoparticles in simulated biological fluids and environmental media. J Nanopart Res 23, 29 (2021). https://doi.org/10.1007/s11051-020-05132-x

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Keywords

  • Dissolution
  • (bio)durability
  • Gold nanoparticles
  • In vitro acellular
  • Dissolution kinetics
  • Health and environmental effects