Skip to main content

Ferritin as a photocatalyst and scaffold for gold nanoparticle synthesis

Abstract

The ferrihydrite mineral core of ferritin is a semi-conductor capable of catalyzing oxidation/reduction reactions. This report shows that ferritin can photoreduce AuCl4 to form gold nanoparticles (AuNPs). An important goal was to identify innocent reaction conditions that prevented formation of AuNPs unless the sample was illuminated in the presence of ferritin. TRIS buffer satisfied this requirement and produced AuNPs with spherical morphology with diameters of 5.7 ± 1.6 nm and a surface plasmon resonance (SPR) peak at 530 nm. Size-exclusion chromatography of the AuNP–ferritin reaction mixture produced two fractions containing both ferritin and AuNPs. TEM analysis of the fraction close to where native ferritin normally elutes showed that AuNPs form inside ferritin. The other peak eluted at a volume indicating a particle size much larger than ferritin. TEM analysis revealed AuNPs adjacent to ferritin molecules suggesting that a dimeric ferritin–AuNP species forms. We propose that the ferritin protein shell acts as a nucleation site for AuNP formation leading to the AuNP-ferritin dimeric species. Ferrihydrite nanoparticles (~10 nm diameter) were unable to produce soluble AuNPs under identical conditions unless apo ferritin was present indicating that the ferritin protein shell was essential for stabilizing AuNPs in aqueous solution.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

References

  • Arosio P, Ingrassia R, Cavadini P (2009) Ferritins: a family of molecules for iron storage, antioxidation and more. Biochim Biophys Acta 1790(7):589–599. doi:10.1016/j.bbagen.2008.09.004

    CAS  Google Scholar 

  • Bhaviripudi S, Mile E, Steiner SA, Zare AT, Dresselhaus MS, Belcher AM, Kong J (2007) Cvd synthesis of single-walled carbon nanotubes from gold nanoparticle catalysts. J Am Chem Soc 129(6):1516–1517. doi:10.1021/ja0673332

    Article  CAS  Google Scholar 

  • Butts CA, Swift J, Kang SG, Di Costanzo L, Christianson DW, Saven JG, Dmochowski IJ (2008) Directing noble metal ion chemistry within a designed ferritin protein. Biochemistry 47(48):12729–12739. doi:10.1021/bi8016735

    Article  CAS  Google Scholar 

  • Cao YWC, Jin RC, Mirkin CA (2002) Nanoparticles with Raman spectroscopic fingerprints for DNA and RNA detection. Science 297(5586):1536–1540

    Article  CAS  Google Scholar 

  • Cherry RJ, Bjornsen AJ, Zapien DC (1998) Direct electron transfer of ferritin adsorbed at tin-doped indium oxide electrodes. Langmuir 14(8):1971–1973. doi:10.1021/la970685p

    Article  CAS  Google Scholar 

  • Chikae M, Fukuda T, Kerman K, Idegami K, Miura Y, Tamiya E (2008) Amyloid-[beta] detection with saccharide immobilized gold nanoparticle on carbon electrode. Bioelectrochemistry 74(1):118–123

    Article  CAS  Google Scholar 

  • Daniel M-C, Astruc D (2003) Gold nanoparticles: assembly, supramolecular chemistry, quantum-size-related properties, and applications toward biology, catalysis, and nanotechnology. Chem Rev 104(1):293–346. doi:10.1021/cr030698+

    Article  Google Scholar 

  • Domìnguez-Vera JM, Gálvez N, Sánchez P, Mota AJ, Trasobares S, Hernández JC, Calvino JJ (2007) Size-controlled water-soluble Ag nanoparticles. Eur J Inorg Chem 2007(30):4823–4826

    Article  Google Scholar 

  • Douglas T, Stark VT (2000) Nanophase cobalt oxyhydroxide mineral synthesized within the protein cage of ferritin. Inorg Chem 39(8):1828–1830

    Article  CAS  Google Scholar 

  • Douglas T, Dickson DPE, Betteridge S, Charnock J, Garner CD, Mann S (1995) Synthesis and structure of an iron (iii) sulfide-ferritin bioinorganic nanocomposite. Science 269(5220):54–57

    Article  CAS  Google Scholar 

  • Ensign D, Young M, Douglas T (2004) Photocatalytic synthesis of copper colloids from Cu(II) by the ferrihydrite core of ferritin. Inorg Chem 43(11):3441–3446

    Article  CAS  Google Scholar 

  • Esumi K, Matsuhisa K, Torigoe K (1995) Preparation of rodlike gold particles by UV irradiation using cationic micelles as a template. Langmuir 11(9):3285–3287. doi:10.1021/la00009a002

    Article  CAS  Google Scholar 

  • Eustis S, Hsu H-Y, El-Sayed MA (2005) Gold nanoparticle formation from photochemical reduction of Au3+ by continuous excitation in colloidal solutions. A proposed molecular mechanism. J Phys Chem B 109(11):4811–4815. doi:10.1021/jp0441588

    Article  CAS  Google Scholar 

  • Fan RL, Chew SW, Cheong VV, Orner BP (2010) Fabrication of gold nanoparticles inside unmodified horse spleen apoferritin. Small 6(14):1483–1487. doi:10.1002/smll.201000457

    Article  CAS  Google Scholar 

  • Galvez N, Sanchez P, Dominguez-Vera JM (2005) Preparation of Cu and CuFe Prussian blue derivative nanoparticles using the apoferritin cavity as nanoreactor. Dalton Trans 7(15):2492–2494. doi:10.1039/b506290j

    Article  Google Scholar 

  • Galvez N, Sanchez P, Dominguez-Vera JM, Soriano-Portillo A, Clemente-Leon M, Coronado E (2006) Apoferritin-encapsulated Ni and Co superparamagnetic nanoparticles. J Mater Chem 16(26):2757–2761

    Article  CAS  Google Scholar 

  • Habib A, Tabata M, Wu YG (2005) Formation of gold nanoparticles by good’s buffers. Bull Chem Soc Jpn 78:262–269

    Article  CAS  Google Scholar 

  • Hainfeld JF (1992) Uranium-loaded apoferritin with antibodies attached: molecular design for uranium neutron-capture therapy. Proc Natl Acad Sci USA 89(22):11064–11068

    Article  CAS  Google Scholar 

  • Harrison PM, Arosio P (1996) The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1275(3):161–203

    Article  Google Scholar 

  • Hilton RJ, Keyes JD, Watt RK (2010a) Maximizing the efficiency of ferritin as a photocatalyst for applications in an artificial photosynthesis system. In: Varadan VK (ed) SPIE smart structures/NDE 2010, San Diego, CA. SPIE nanosensors, biosensors and info-tech sensors and systems. Proc. of SPIE, p 76460J

  • Hilton RJ, Keyes JD, Watt RK (2010b) Photoreduction of Au(III) to form Au(0) nanoparticles using ferritin as a photocatalyst. In: Varadan VK (ed) SPIE smart structures/NDE 2010, San Diego, CA. SPIE nanosensors, biosensors and info-tech sensors and systems. Proc. of SPIE, pp 764601–764607

  • Huang WC, Chen YC (2008) Photochemical synthesis of polygonal gold nanoparticles. J Nanopart Res 10(4):697–702. doi:10.1007/s11051-007-9293-8

    Article  CAS  Google Scholar 

  • Iwahori K, Yoshizawa K, Muraoka M, Yamashita I (2005) Fabrication of ZnSe nanoparticles in the apoferritin cavity by designing a slow chemical reaction system. Inorg Chem 44(18):6393–6400. doi:10.1021/ic0502426

    Article  CAS  Google Scholar 

  • Kasyutich O, Ilari A, Fiorillo A, Tatchev D, Hoell A, Ceci P (2010) Silver ion incorporation and nanoparticle formation inside the cavity of pyrococcus furiosus ferritin: structural and size-distribution analyses. J Am Chem Soc 132(10):3621–3627. doi:10.1021/ja910918b

    Article  CAS  Google Scholar 

  • Katz E, Willner I (2004) Integrated nanoparticle-biomolecule hybrid systems: synthesis, properties, and applications. Angew Chem Int Ed 43(45):6042–6108

    Article  CAS  Google Scholar 

  • Kim I, Hosein HA, Strongin DR, Douglas T (2002) Photochemical reactivity of ferritin for Cr(VI) reduction. Chem Mater 14(11):4874–4879

    Article  CAS  Google Scholar 

  • Kim JW, Posey AE, Watt GD, Choi SH, Lillehei PT (2010) Gold nanoshell assembly on a ferritin protein employed as a bio-template. J Nanosci Nanotechnol 10(3):1771–1777

    Article  CAS  Google Scholar 

  • Klem MT, Mosolf J, Young M, Douglas T (2008) Photochemical mineralization of europium, titanium, and iron oxyhydroxide nanoparticles in the ferritin protein cage. Inorg Chem 47(7):2237–2239

    Article  CAS  Google Scholar 

  • Kuong C-L, Chen W-Y, Chen Y-C (2007) Semi-quantitative determination of cationic surfactants in aqueous solutions using gold nanoparticles as reporter probes. Anal Bioanal Chem 387(6):2091–2099

    Article  CAS  Google Scholar 

  • Lee J-S, Ulmann PA, Han MS, Mirkin CA (2008) A DNA–gold nanoparticle-based colorimetric competition assay for the detection of cysteine. Nano Lett 8(2):529–533. doi:10.1021/nl0727563

    Article  CAS  Google Scholar 

  • Liu J, Lu Y (2003) A colorimetric lead biosensor using DNAzyme-directed assembly of gold nanoparticles. J Am Chem Soc 125(22):6642–6643. doi:10.1021/ja034775u

    Article  CAS  Google Scholar 

  • Liu J, Lu Y (2006) Fast colorimetric sensing of adenosine and cocaine based on a general sensor design involving aptamers and nanoparticles. Angew Chem Int Ed 45(1):90–94

    Article  CAS  Google Scholar 

  • Liu SF, Liu QY, Boerio-Goates J, Woodfield BF (2007) Preparation of a wide array of ultra-high purity metals, metal oxides, and mixed metal oxides with uniform particle sizes from 1 nm to bulk. J Adv Mater 39(2):18–23

    CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193(1):265–275

    CAS  Google Scholar 

  • Mallick K, Witcomb MJ, Scurrell MS (2005) Polymer-stabilized colloidal gold: a convenient method for the synthesis of nanoparticles by a UV-irradiation approach. Appl Phys A 80(2):395–398

    Article  CAS  Google Scholar 

  • Marken F, Patel D, Madden CE, Millward RC, Fletcher S (2002) The direct electrochemistry of ferritin compared with the direct electrochemistry of nanoparticulate hydrous ferric oxide. New J Chem 26(2):259–263

    Article  CAS  Google Scholar 

  • Meldrum FC, Wade VJ, Nimmo DL, Heywood BR, Mann S (1991) Synthesis of inorganic nanophase materials in supramolecular protein cages. Nature 349(6311):684–687

    Article  CAS  Google Scholar 

  • Meldrum FC, Douglas T, Levi S, Arosio P, Mann S (1995) Reconstitution of manganese oxide cores in horse spleen and recombinant ferritins. J Inorg Biochem 58(1):59–68

    Article  CAS  Google Scholar 

  • Niemeyer CM (2001) Nanoparticles, proteins, and nucleic acids: biotechnology meets materials science. Angew Chem Int Ed 40(22):4128–4158

    Article  CAS  Google Scholar 

  • Nikandrov VV, Gratzel CK, Moser JE, Gratzel M (1997) Light induced redox reactions involving mammalian ferritin as photocatalyst. J Photochem Photobiol B 41(1–2):83–89

    Article  CAS  Google Scholar 

  • Okuda M, Iwahori K, Yamashita I, Yoshimura H (2003) Fabrication of nickel and chromium nanoparticles using the protein cage of apoferritin. Biotechnol Bioeng 84(2):187–194

    Article  CAS  Google Scholar 

  • Sau TK, Pal A, Jana NR, Wang ZL, Pal T (2001) Size controlled synthesis of gold nanoparticles using photochemically prepared seed particles. J Nanopart Res 3(4):257–261

    Article  CAS  Google Scholar 

  • Shankar SS, Rai A, Ankamwar B, Singh A, Ahmad A, Sastry M (2004) Biological synthesis of triangular gold nanoprisms. Nat Mater 3(7):482–488

    Article  CAS  Google Scholar 

  • Shin Y, Dohnalkova A, Lin Y (2010) Preparation of homogeneous gold‚ and silver alloy nanoparticles using the apoferritin cavity as a nanoreactor. J Phys Chem C 114(13):5985–5989. doi:10.1021/jp911004a

    Article  CAS  Google Scholar 

  • Skrabalak SE, Chen J, Au L, Lu X, Li X, Xia Y (2007) Gold nanocages for biomedical applications. Adv Mater Deerfield 19(20):3177–3184. doi:10.1002/adma.200701972

    Article  CAS  Google Scholar 

  • Taton TA, Mirkin CA, Letsinger RL (2000) Scanometric DNA array detection with nanoparticle probes. Science 289(5485):1757–1760

    Article  CAS  Google Scholar 

  • Turner M, Golovko VB, Vaughan OPH, Abdulkin P, Berenguer-Murcia A, Tikhov MS, Johnson BFG, Lambert RM (2008) Selective oxidation with dioxygen by gold nanoparticle catalysts derived from 55-atom clusters. Nature 454(7207):981–983

    Article  CAS  Google Scholar 

  • Turyanska L, Bradshaw TD, Sharpe J, Li M, Mann S, Thomas NR, Patane A (2009) The biocompatibility of apoferritin-encapsulated PbS quantum dots. Small 5(15):1738–1741. doi:10.1002/smll.200900017

    Article  CAS  Google Scholar 

  • Uchida M, Klem MT, Allen M, Suci P, Flenniken M, Gillitzer E, Varpness Z, Liepold LO, Young M, Douglas T (2007) Biological containers: protein cages as multifunctional nanoplatforms. Adv Mater 19(8):1025–1042

    Article  CAS  Google Scholar 

  • Ueno T, Suzuki M, Goto T, Matsumoto T, Nagayama K, Watanabe Y (2004) Size-selective olefin hydrogenation by a Pd nanocluster provided in an apo-ferritin cage. Angew Chem Int Ed 43(19):2527–2530

    Article  CAS  Google Scholar 

  • Watt GD, Jacobs D, Frankel RB (1988) Redox reactivity of bacterial and mammalian ferritin: is reductant entry into the ferritin interior a necessary step for iron release? Proc Natl Acad Sci USA 85(20):7457–7461

    Article  CAS  Google Scholar 

  • Watt RK, Frankel RB, Watt GD (1992) Redox reactions of apo mammalian ferritin. Biochemistry 31(40):9673–9679

    Article  CAS  Google Scholar 

  • Whaley SR, English DS, Hu EL, Barbara PF, Belcher AM (2000) Selection of peptides with semiconductor binding specificity for directed nanocrystal assembly. Nature 405(6787):665–668

    Article  CAS  Google Scholar 

  • Wong KKW, Mann S (1996) Biomimetic synthesis of cadmium sulfide-ferritin nanocomposites. Adv Mater 8(11):928–932

    Article  CAS  Google Scholar 

  • Xie J, Lee JY, Wang DIC (2007) Seedless, surfactantless, high-yield synthesis of branched gold nanocrystals in hepes buffer solution. Chem Mater 19(11):2823–2830. doi:10.1021/cm0700100

    Article  CAS  Google Scholar 

  • Yamashita I, Hayashi J, Hara M (2004) Bio-template synthesis of uniform CdSe nanoparticles using cage-shaped protein, apoferritin. Chem Lett 33(9):1158–1159

    Article  CAS  Google Scholar 

  • Yang M, Kostov Y, Bruck HA, Rasooly A (2009) Gold nanoparticle-based enhanced chemiluminescence immunosensor for detection of staphylococcal enterotoxin b (SEB) in food. Int J Food Microbiol 133(3):265–271

    Article  CAS  Google Scholar 

  • Yeh CH, Hung CY, Chang TC, Lin HP, Lin YC (2009) An immunoassay using antibody-gold nanoparticle conjugate, silver enhancement and flatbed scanner. Microfluid Nanofluid 6(1):85–91. doi:10.1007/s10404-008-0298-0

    Article  CAS  Google Scholar 

  • Yoshizawa K, Iwahori K, Sugimoto K, Yamashita I (2006) Fabrication of gold sulfide nanoparticles using the protein cage of apoferritin. Chem Lett 35(10):1192–1193

    Article  CAS  Google Scholar 

  • Zhang B, Watt GD (2007) Anaerobic iron deposition into horse spleen, recombinant human heavy and light and bacteria ferritins by large oxidants. J Inorg Biochem 101(11–12):1676–1685

    Article  CAS  Google Scholar 

  • Zhang B, Harb JN, Davis RC, Kim JW, Chu SH, Choi S, Miller T, Watt GD (2005) Kinetic and thermodynamic characterization of the cobalt and manganese oxyhydroxide cores formed in horse spleen ferritin. Inorg Chem 44(10):3738–3745. doi:10.1021/ic049085l

    Article  CAS  Google Scholar 

  • Zhang L, Swift J, Butts CA, Yerubandi V, Dmochowski IJ (2007) Structure and activity of apoferritin-stabilized gold nanoparticles. J Inorg Biochem 101(11–12):1719–1729. doi:10.1016/j.jinorgbio.2007.07.023

    Article  CAS  Google Scholar 

  • Zhou Y, Wang CY, Zhu YR, Chen ZY (1999) A novel ultraviolet irradiation technique for shape-controlled synthesis of gold nanoparticles at room temperature. Chem Mater 11(9):2310–2312. doi:10.1021/cm990315h

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard K. Watt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 90 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Keyes, J.D., Hilton, R.J., Farrer, J. et al. Ferritin as a photocatalyst and scaffold for gold nanoparticle synthesis. J Nanopart Res 13, 2563–2575 (2011). https://doi.org/10.1007/s11051-010-0149-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11051-010-0149-2

Keywords

  • Gold nanoparticles
  • Ferritin
  • Nanoparticle synthesis
  • Photochemistry
  • Photoreduction