Advertisement

In vivo toxicity and antimicrobial activity of AuPt bimetallic nanoparticles

  • Daniela Maria Ducatti Formaggio
  • Xisto Antonio de Oliveira Neto
  • Lina Dayse Alcântara Rodrigues
  • Vitor Martins de Andrade
  • Bruna C. Nunes
  • Mônica Lopes-Ferreira
  • Fabiana G. Ferreira
  • Cristiane C. Wachesk
  • Emerson R. Camargo
  • Katia Conceição
  • Dayane Batista TadaEmail author
Research Paper
  • 47 Downloads

Abstract

Despite the potential antimicrobial activity of metallic nanoparticles, the increasing concerns about nanosafety have been holding back the use of these materials in therapeutics and biomedical devices. In the last years, several studies called attention to metallic nanoparticles toxicity. In the most part of in vitro studies performed with mammalian cells, metallic NPs reduced cell viability and induced genotoxicity and inflammatory responses. Bimetallic NPs have attracted great attention because they present distinct and even more advanced characteristics when compared to nanoparticles formed by a single metal. Recently, bimetallic NPs have emerged as an alternative to improve the antimicrobial activity of metallic nanoparticles, aiming at the broadening of the action spectrum and the reduction of the toxicity. However, the biocompatibility of bimetallic nanoparticles has been demonstrated only by in vitro studies. In the present work, the toxicity of AuPt nanoparticles was addressed both in vitro and in vivo. In addition, the antimicrobial activity of AuPt bimetallic nanoparticles has been evaluated in comparison with Au and Ag nanoparticles. The nanoparticles were characterized by ultraviolet-visible spectroscopy, dynamic light scattering, transmission electron microscopy, inductively coupled plasma optical emission spectroscopy, and X-ray diffraction. The antimicrobial activity was studied against Candida albicans, Pseudomonas aeruginosa, and Staphylococcus aureus. The toxicity of nanoparticles was evaluated in vitro by analyzing their toxicity against human fibroblast cells (HS68 cell line) and in vivo by embryonic toxicity test in zebrafish (Danio rerio). The results confirmed the intrinsic antimicrobial activity of the three types of nanoparticles but different toxicity. Bimetallic nanoparticles showed enhanced antimicrobial activity in comparison with Au nanoparticles but lower antimicrobial activity compared with Ag nanoparticles. However, AuPt nanoparticles showed great advantage over Ag nanoparticles due to the absence of cytotoxicity and lower toxicity in vivo.

Keywords

Gold nanoparticles Silver nanoparticles Bimetallic nanoparticles Antimicrobial activity Toxicity Zebrafish Environmental and health effects 

Notes

Acknowledgements

The authors would like to thank Dr. João Paulo Barros Machado from INPE for the availability of the equipment and technical support on the X-ray diffractometry.

Funding information

This work had financial support from FAPESP (2011/23895-8, 2017/01697-6, 2017/0032-0), CNPQ (306874/2015-6), CAPES, and CeTICS CEPID (FAPESP).

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

References

  1. Aioub M, Panikkanvalappil SR, El-Sayed MA (2017) Platinum-coated gold nanorods: efficient reactive oxygen scavengers that prevent oxidative damage toward healthy, untreated cells during plasmonic photothermal therapy. ACS Nano 11:579–586CrossRefGoogle Scholar
  2. Arvizo R, Bhattacharya R, Mukherjee P (2010) Gold nanoparticles: opportunities and challenges in nanomedicine. Expert Opin Drug Deliv 7:753–763CrossRefGoogle Scholar
  3. Asharani P, Lianwu Y, Gong Z, Valiyaveettil S (2011) Comparison of the toxicity of silver, gold and platinum nanoparticles in developing zebrafish embryos. Nanotoxicology 5:43–54CrossRefGoogle Scholar
  4. Ávalos Fúnez A, Isabel Haza A, Mateo D, Morales P (2013) In vitro evaluation of silver nanoparticles on human tumoral and normal cells. Toxicol Mech Methods 23:153–160CrossRefGoogle Scholar
  5. Busquet F, Strecker R, Rawlings JM, Belanger SE, Braunbeck T, Carr GJ, Cenijn P, Fochtman P, Gourmelon A, Hübler N, Kleensang A, Knöbel M, Kussatz C, Legler J, Lillicrap A, Martínez-Jerónimo F, Polleichtner C, Rzodeczko H, Salinas E, Schneider KE, Scholz S, van den Brandhof EJ, van der Ven LTM, Walter-Rohde S, Weigt S, Witters H, Halder M (2014) OECD validation study to assess intra-and inter-laboratory reproducibility of the zebrafish embryo toxicity test for acute aquatic toxicity testing. Regul Toxicol Pharmacol 69:496–511CrossRefGoogle Scholar
  6. Conceição K, Monteiro-dos Santos J, Seibert CS, Silva PI Jr, Marques EE, Richardson M, Lopes-Ferreira M (2012) Potamotrygon cf. henlei stingray mucus: biochemical features of a novel antimicrobial protein. Toxicon 60:821–829CrossRefGoogle Scholar
  7. Dakal T.C.; Kumar A.; Majumdar R.S.; Yadav V. 2016 Mechanistic basis of antimicrobial actions of silver nanoparticles. Front Microbiol, 7.Google Scholar
  8. Enustun B, Turkevich J (1963) Coagulation of colloidal gold. J Am Chem Soc 85:3317–3328CrossRefGoogle Scholar
  9. Feng ZV, Gunsolus IL, Qiu TA, Hurley KR, Nyberg LH, Frew H, Johnson KP, Vartanian AM, Jacob LM, Lohse SE et al (2015) Impacts of gold nanoparticle charge and ligand type on surface binding and toxicity to Gram-negative and Gram-positive bacteria. Chem Sci 6:5186–5196CrossRefGoogle Scholar
  10. Gao X, Topping VD, Keltner Z, Sprando RL, Yourick JJ (2017) Toxicity of nano- and ionic silver to embryonic stem cells: a comparative toxicogenomic study. J Nanobiotechnol 15:31CrossRefGoogle Scholar
  11. Gorup LF, Longo E, Leite ER, Camargo ER (2011) Moderating effect of ammonia on particle growth and stability of quasi-monodisperse silver nanoparticles synthesized by the Turkevich method. J Colloid Interface Sci 360:355–358CrossRefGoogle Scholar
  12. Haiss W, Thanh NT, Aveyard J, Fernig DG (2007) Determination of size and concentration of gold nanoparticles from UV- Vis spectra. Anal Chem 79:4215–4221CrossRefGoogle Scholar
  13. Hinterwirth H, Lindner W, Lämmerhofer M (2012) Bioconjugation of trypsin onto gold nanoparticles: effect of surface chemistry on bioactivity. Anal Chim Acta 733:90–97CrossRefGoogle Scholar
  14. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498CrossRefGoogle Scholar
  15. Jung WK, Koo HC, Kim KW, Shin S, Kim SH, Park YH (2008) Antibacterial activity and mechanism of action of the silver ion in Staphylococcus aureus and Escherichia coli. Appl Environ Microbiol 74:2171–2178CrossRefGoogle Scholar
  16. Kaiser JP, Roesslein M, Diener L, Wichser A, Nowack B, Wick P (2017) Cytotoxic effects of nanosilver are highly dependent on the chloride concentration and the presence of organic compounds in the cell culture media. J Nanobiotechnology 15:5CrossRefGoogle Scholar
  17. Kim JS, Sung JH, Ji JH, Song KS, Lee JH, Kang CS, Yu IJ (2011) In vivo genotoxicity of silver nanoparticles after 90-day silver nanoparticle inhalation exposure. Saf Health Work 2:34–38CrossRefGoogle Scholar
  18. Kumar S.; Mukherjee M.M.; Varela M.F. 2013 Modulation of bacterial multidrug resistance efflux pumps of the major facilitator superfamily. Int J Bacteriol.Google Scholar
  19. Lai F, Chou H, Sarma LS, Wang D, Lin Y, Lee J, Hwang BJ, Chen C (2010) Tunable properties of PtxFe1-x electrocatalysts and their catalytic activity towards the oxygen reduction reaction. Nanoscale 2:573–581CrossRefGoogle Scholar
  20. Lapp AS, Duan Z, Marcella N, Luo L, Genc A, Ringnalda J, Frenkel AI, Henkelman G, Crooks RM (2018) Experimental and Theoretical Structural Investigation of AuPt Nanoparticles Synthesized Using a Direct Electrochemical Method. J Am Chem Soc 140, 20:6249–6259CrossRefGoogle Scholar
  21. Linic S, Aslam U, Boerigter C, Morabito M (2015) Photochemical transformations on plasmonic metal nanoparticles. Nat Mater 14:567–576CrossRefGoogle Scholar
  22. Ma Y, Song L, Lei Y, Jia P, Lu C, Wu J, Xi C, Strauss PR, Pei DS (2018) Sex dependent effects of silver nanoparticles on the zebrafish gut microbiota. Environ Sci: Nano 5:740–751Google Scholar
  23. McShan D, Ray PC, Yu H (2014) Molecular toxicity mechanism of nanosilver. J Food Drug Anal 22:116–127CrossRefGoogle Scholar
  24. Mott D, Luo J, Smith A, Njoki PN, Wang L, Zhong C (2007) Nanocrystal and Surface alloy properties of bimetallic Gold-Platinum nanoparticles. Nanoscale Res Lett 2:12–16CrossRefGoogle Scholar
  25. Murphy S, Murphy CJ, Leach A, Gall KA (2015) Possible oriented attachment growth mechanism for silver nanowire formation. Cryst Growth Des 15(4):1968–1974CrossRefGoogle Scholar
  26. Paramelle D, Sadovoy A, Gorelik S, Free P, Hobley J, Fernig DG (2014) A rapid method to estimate the concentration of citrate capped silver nanoparticles from UV-visible light spectra. Analyst 139:4855–4861CrossRefGoogle Scholar
  27. Park SB, Steadman CS, Chaudhari AA, Pillai SR, Singh SR, Ryan PL, Willard ST, Feugang JM (2018) Proteomic analysis of antimicrobial effects of pegylated silver coated carbon nanotubes in Salmonella enterica serovar Typhimurium. J Nanobiotechnol 16:31CrossRefGoogle Scholar
  28. Penn RL, Banfield JF (1998) Imperfect oriented attachment: dislocation generation in defect-free nanocrystals. Science 281:969–971CrossRefGoogle Scholar
  29. Petkov V, Wanjala BN, Loukrakpam R, Luo J, Yang L, Zhong C, Shastri S (2012) Pt-Au Alloying at the nanoscale. Nano Lett 12(8):4289–4299CrossRefGoogle Scholar
  30. Qian H, Zhao Q, Dai B, Guo L, Zhang J, Liu J, Zhang J (2015) Oriented attachment of nanoparticles to form micrometer-sized nanosheets/nanobelts by topotactic reaction on rigid/flexible substrates with improved electronic properties. NPG Asia Mater 7:e152CrossRefGoogle Scholar
  31. Qingbo Z, Jianping X, Yue Y, Jim Y (2010) L. Monodispersity control in the synthesis of monometallic and bimetallic quasi-spherical gold and silver nanoparticles. Nanoscale 2:1962–1975CrossRefGoogle Scholar
  32. Raju M, van Duin ACT, Fichthorn KA (2014) Mechanisms of oriented attachment of TiO2 nanocrystals in vacuum and humid environments: reactive molecular dynamics. Nano Lett. 14:1836–1842CrossRefGoogle Scholar
  33. Siddiqi KS, Husen A, Rao RAK (2018) A review on biosynthesis of silver nanoparticles and their biocidal properties. J Nanobiotechnol 16:14CrossRefGoogle Scholar
  34. Sieber S, Grossen P, Detampel P, Siegfried S, Witzigmann D, Huwyler J (2017) Zebrafish as an early stage screening tool to study the systemic circulation of nanoparticulate drug delivery systems in vivo. J Control Release 264:180–191CrossRefGoogle Scholar
  35. Singh J, Dutta T, Kim K, Rawat M, Samddar P, Kumar P (2018) "Green" synthesis of metals and their oxidenanoparticles: applications for environmental remediation. J. Nanobiotechnol. 16:84CrossRefGoogle Scholar
  36. Smith L, Kuncic Z, Ostrikov K, Kumar S (2012) Nanoparticles in cancer imaging and therapy. J Nanomater 2012:10CrossRefGoogle Scholar
  37. Song K, Xu P, Meng Y, Geng F, Li J, Li Z, Xing J, Chen J, Kong B (2013) Smart gold nanoparticles enhance killing effect on cancer cells. Int J Oncol 42:597–608CrossRefGoogle Scholar
  38. Srinoi P, Chen YT, Vittur V, Marquez MD, Lee TR (2018) Bimetallic nanoparticles: enhanced magnetic and optical properties for emerging biological applications. Appl Sci 8:1106CrossRefGoogle Scholar
  39. Tian X, Jiang X, Welch C, Croley TR, Wong TY, Chen C, Fan S, Chong Y, Li R, Ge C et al (2018) Bactericidal effects of silver nanoparticles on lactobacilli and the underlying mechanism. ACS Appl Mater Interfaces 10:8443–8450CrossRefGoogle Scholar
  40. Uson L, Sebastian V, Mayoral A, Hueso JL, Eguizabal A, Arruebo M, Santamaria J (2015) Spontaneous formation of Au–Pt alloyed nanoparticles using pure nano-counterparts as starters: a ligand and size dependent process. Nanoscale 7:10152–10161CrossRefGoogle Scholar
  41. Van Pomeren M, Brun N, Peijnenburg W, Vijver M (2017) Exploring uptake and biodistribution of polystyrene (nano) particles in zebrafish embryos at different developmental stages. Aquat Toxicol 190:40–45CrossRefGoogle Scholar
  42. Villiers CL, Freitas H, Couderc R, Villiers MB, Marche PN (2010) Analysis of the toxicity of gold nanoparticles on the immune system: effect on dendritic cell functions. J Nanopart Res 12:55–60CrossRefGoogle Scholar
  43. Wang L, Hu C, Shao L (2017) The antimicrobial activity of nanoparticles: present situation and prospects for the future. Int J Nanomed 12:1227CrossRefGoogle Scholar
  44. Westsson E, Koper GJ (2014) How to determine the core-shell nature in bimetallic catalyst particles? Catalysts 4:375–396CrossRefGoogle Scholar
  45. Xu Y, Chen L, Wang C, Yao W, Zhang Q (2015) Recent advances in noble metal based composite nanocatalysts: colloidal synthesis, properties, and catalytic applications. Nanoscale 7:10559–10583CrossRefGoogle Scholar
  46. Yao C, Zhang L, Wang J, He Y, Xin J, Wang S, Xu H, Zhang Z (2016) Gold nanoparticle mediated phototherapy for cancer. J Nanomater 2016Google Scholar
  47. Zhao L, Heinig N, Leung KT (2013) Formation of Au−Pt Alloy nanoparticles on a Si substrate by simple dip-coating at room temperature. Langmuir 29:927–931CrossRefGoogle Scholar
  48. Zhao Y, Ye C, Liu W, Chen R, Jiang X (2014) Tuning the composition of AuPt bimetallic nanoparticles for antibacterial application. Angew Chem Int Ed 53:8127–8131CrossRefGoogle Scholar
  49. Zhong C, Luo J, Njoki PN, Mott D, Wanjala B, Loukrakpam R, Lim S, Wang L, Fang N, Xu Z (2008) Fuel cell technology: nano-engineered multimetallic catalysts. Energy Environ Sci 1:454–466CrossRefGoogle Scholar
  50. Zhou Y, Kong Y, Kundu S, Cirillo JD, Liang H (2012) Antibacterial activities of gold and silver nanoparticles against Escherichia coli and bacillus Calmette-Guérin. J Nanobiotechnology 10:1CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Daniela Maria Ducatti Formaggio
    • 1
  • Xisto Antonio de Oliveira Neto
    • 2
  • Lina Dayse Alcântara Rodrigues
    • 1
  • Vitor Martins de Andrade
    • 2
  • Bruna C. Nunes
    • 1
  • Mônica Lopes-Ferreira
    • 3
  • Fabiana G. Ferreira
    • 1
  • Cristiane C. Wachesk
    • 1
  • Emerson R. Camargo
    • 4
  • Katia Conceição
    • 2
  • Dayane Batista Tada
    • 1
    Email author
  1. 1.Laboratory of Nanomaterials and NanotoxicologyUniversidade Federal de São PauloSão PauloBrasil
  2. 2.Laboratório de Bioquímica de PeptídeosUniversidade Federal de São PauloSão PauloBrazil
  3. 3.Immunoregulation Unit of the Special Laboratory of Applied Toxinology (CeTICS, CEPID/FAPESP)Instituto ButantanSão PauloBrazil
  4. 4.Department of ChemistryUFSCar–Federal University of São CarlosSão CarlosBrazil

Personalised recommendations