Site-specific Targeting of Enterovirus Capsid by Functionalized Monodisperse Gold Nanoclusters

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2014 Jan 30

PMID 24474748

Citations 14

Authors

Varpu Marjomaki

Tanja Lahtinen

Mari Martikainen

Jaakko Koivisto

Sami Malola

Kirsi Salorinne

Mika Pettersson

Hannu Hakkinen

Affiliations

Soon will be listed here.

Abstract

Development of precise protocols for accurate site-specific conjugation of monodisperse inorganic nanoparticles to biological material is one of the challenges in contemporary bionanoscience and nanomedicine. We report here a successful site-specific covalent conjugation of functionalized atomically monodisperse gold clusters with 1.5-nm metal cores to viral surfaces. Water-soluble Au102(para-mercaptobenzoic acid)44 clusters, functionalized by maleimide linkers to target cysteines of viral capsid proteins, were synthesized and conjugated to enteroviruses echovirus 1 and coxsackievirus B3. Quantitative analysis of transmission electron microscopy images and the known virus structures showed high affinity and mutual ordering of the bound gold clusters on the viral surface and a clear correlation between the clusters and the targeted cysteine sites close to the viral surface. Infectivity of the viruses was not compromised by loading of several tens of gold clusters per virus. These advances allow for future investigations of the structure-function relations of enteroviruses and enterovirus-related virus-like particles, including their entry mechanisms into cells and uncoating in cellular endosomes.

Citing Articles

Buckling cluster-based H-bonded icosahedral capsules and their propagation to a robust zeolite-like supramolecular framework.

Zhao Z, Han B, Su H, Guo Q, Wang W, Zhuo J Nat Commun. 2024; 15(1):9401.

PMID: 39477935 PMC: 11525653. DOI: 10.1038/s41467-024-53640-4.

Thermodynamic Characterization of the Interaction of Biofunctionalized Gold Nanoclusters with Serum Albumin Using Two- and Three-Dimensional Methods.

Juhasz A, Gombar G, F Varkonyi E, Wojnicki M, Ungor D, Csapo E Int J Mol Sci. 2023; 24(23).

PMID: 38069083 PMC: 10706308. DOI: 10.3390/ijms242316760.

Covalent and non-covalent coupling of a Au nanocluster with a fluorophore: energy transfer, quenching and intracellular pH sensing.

Hulkko E, Lahtinen T, Marjomaki V, Pohjolainen E, Saarnio V, Sokolowska K Nanoscale Adv. 2022; 3(23):6649-6658.

PMID: 36132657 PMC: 9417352. DOI: 10.1039/d1na00368b.

Assembly of gold nanoparticles using turnip yellow mosaic virus as an in-solution SERS sensor.

Nguyen H, Jupin I, Decorse P, Lau-Truong S, Ammar S, Ha-Duong N RSC Adv. 2022; 9(55):32296-32307.

PMID: 35530810 PMC: 9072845. DOI: 10.1039/c9ra08015e.

Nanotechnology-based approaches for emerging and re-emerging viruses: Special emphasis on COVID-19.

Saravanan M, Mostafavi E, Vincent S, Negash H, Andavar R, Perumal V Microb Pathog. 2021; 156:104908.

PMID: 33932543 PMC: 8079947. DOI: 10.1016/j.micpath.2021.104908.

References

Kostiainen M, Hiekkataipale P, Laiho A, Lemieux V, Seitsonen J, Ruokolainen J . Electrostatic assembly of binary nanoparticle superlattices using protein cages. Nat Nanotechnol. 2012; 8(1):52-6. DOI: 10.1038/nnano.2012.220. View

Yoder J, Cifuente J, Pan J, Bergelson J, Hafenstein S . The crystal structure of a coxsackievirus B3-RD variant and a refined 9-angstrom cryo-electron microscopy reconstruction of the virus complexed with decay-accelerating factor (DAF) provide a new footprint of DAF on the virus surface. J Virol. 2012; 86(23):12571-81. PMC: 3497627. DOI: 10.1128/JVI.01592-12. View

DeVries G, Brunnbauer M, Hu Y, Jackson A, Long B, Neltner B . Divalent metal nanoparticles. Science. 2007; 315(5810):358-61. DOI: 10.1126/science.1133162. View

Filman D, Wien M, Cunningham J, Bergelson J, Hogle J . Structure determination of echovirus 1. Acta Crystallogr D Biol Crystallogr. 1999; 54(Pt 6 Pt 2):1261-72. DOI: 10.1107/s0907444998002790. View

Lewis J, Bothner B, Smith T, Siuzdak G . Antiviral agent blocks breathing of the common cold virus. Proc Natl Acad Sci U S A. 1998; 95(12):6774-8. PMC: 22631. DOI: 10.1073/pnas.95.12.6774. View

Heinecke C, Ni T, Malola S, Makinen V, Wong O, Hakkinen H . Structural and theoretical basis for ligand exchange on thiolate monolayer protected gold nanoclusters. J Am Chem Soc. 2012; 134(32):13316-22. PMC: 4624284. DOI: 10.1021/ja3032339. View

Walter M, Akola J, Lopez-Acevedo O, Jadzinsky P, Calero G, Ackerson C . A unified view of ligand-protected gold clusters as superatom complexes. Proc Natl Acad Sci U S A. 2008; 105(27):9157-62. PMC: 2442568. DOI: 10.1073/pnas.0801001105. View

Hainfeld J, Furuya F . A 1.4-nm gold cluster covalently attached to antibodies improves immunolabeling. J Histochem Cytochem. 1992; 40(2):177-84. DOI: 10.1177/40.2.1552162. View

Lin J, Lee L, Roivainen M, Filman D, Hogle J, Belnap D . Structure of the Fab-labeled "breathing" state of native poliovirus. J Virol. 2012; 86(10):5959-62. PMC: 3347258. DOI: 10.1128/JVI.05990-11. View

10.

Hober D, Sauter P . Pathogenesis of type 1 diabetes mellitus: interplay between enterovirus and host. Nat Rev Endocrinol. 2010; 6(5):279-89. DOI: 10.1038/nrendo.2010.27. View

11.

Hainfeld J . Gold cluster-labelled antibodies. Nature. 1988; 333(6170):281-2. DOI: 10.1038/333281a0. View

12.

Bostina M, Levy H, Filman D, Hogle J . Poliovirus RNA is released from the capsid near a twofold symmetry axis. J Virol. 2010; 85(2):776-83. PMC: 3020038. DOI: 10.1128/JVI.00531-10. View

13.

Sexton J, Ackerson C . Determination of Rigidity of Protein Bound Au(144) Clusters by Electron Cryomicroscopy. J Phys Chem C Nanomater Interfaces. 2010; 114(38):16037-16042. PMC: 2992337. DOI: 10.1021/jp101970x. View

14.

Karjalainen M, Rintanen N, Lehkonen M, Kallio K, Maki A, Hellstrom K . Echovirus 1 infection depends on biogenesis of novel multivesicular bodies. Cell Microbiol. 2011; 13(12):1975-95. DOI: 10.1111/j.1462-5822.2011.01685.x. View

15.

Tuthill T, Groppelli E, Hogle J, Rowlands D . Picornaviruses. Curr Top Microbiol Immunol. 2010; 343:43-89. PMC: 3018333. DOI: 10.1007/82_2010_37. View

16.

Jadzinsky P, Calero G, Ackerson C, Bushnell D, Kornberg R . Structure of a thiol monolayer-protected gold nanoparticle at 1.1 A resolution. Science. 2007; 318(5849):430-3. DOI: 10.1126/science.1148624. View

17.

Abraham G, Colonno R . Many rhinovirus serotypes share the same cellular receptor. J Virol. 1984; 51(2):340-5. PMC: 254443. DOI: 10.1128/JVI.51.2.340-345.1984. View

18.

Ackerson C, Powell R, Hainfeld J . Site-specific biomolecule labeling with gold clusters. Methods Enzymol. 2010; 481:195-230. PMC: 3568671. DOI: 10.1016/S0076-6879(10)81009-2. View

19.

Smyth M, Martin J . Picornavirus uncoating. Mol Pathol. 2002; 55(4):214-9. PMC: 1187181. DOI: 10.1136/mp.55.4.214. View

20.

Kankaanpaa P, Paavolainen L, Tiitta S, Karjalainen M, Paivarinne J, Nieminen J . BioImageXD: an open, general-purpose and high-throughput image-processing platform. Nat Methods. 2012; 9(7):683-9. DOI: 10.1038/nmeth.2047. View