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Glycoconjugates can block such interactions and thereby prevent infection. The inhibition potency strongly depends on matching the spatial arrangement between the multivalent binding partners. However, the structural details of some key lectins remain unknown and different lectins may exhibit overlapping glycan specificity. This makes it difficult to design a glycoconjugate that can potently and specifically target a particular multimeric lectin for therapeutic interventions, especially under the challenging in vivo conditions. Conventional techniques such as surface plasmon resonance (SPR) and isothermal titration calorimetry (ITC) can provide quantitative binding thermodynamics and kinetics. However, they cannot reveal key structural information, e.g., lectin\u2019s binding site orientation, binding mode, and interbinding site spacing, which are critical to design specific multivalent inhibitors. Herein we report that gold nanoparticles (GNPs) displaying a dense layer of simple glycans are powerful mechanistic probes for multivalent lectin-glycan interactions. They can not only quantify the GNP-glycan-lectin binding affinities via a new fluorescence quenching method, but also reveal drastically different affinity enhancing mechanisms between two closely related tetrameric lectins, DC-SIGN (simultaneous binding to one GNP) and DC-SIGNR (intercross-linking with multiple GNPs), via a combined hydrodynamic size and electron microscopy analysis. Moreover, a new term, potential of assembly formation (PAF), has been proposed to successfully predict the assembly outcomes based on the binding mode between GNP-glycans and lectins. Finally, the GNP-glycans can potently and completely inhibit DC-SIGN-mediated augmentation of Ebola virus glycoprotein-driven cell entry (with IC50 values down to 95 pM), but only partially block DC-SIGNR-mediated virus infection. Our results suggest that the ability of a glycoconjugate to simultaneously block all binding sites of a target lectin is key to robust inhibition of viral infection.<\/jats:p>","DOI":"10.1021\/jacs.0c06793","type":"journal-article","created":{"date-parts":[[2020,9,16]],"date-time":"2020-09-16T13:34:45Z","timestamp":1600263285000},"page":"18022-18034","source":"Crossref","is-referenced-by-count":99,"title":["Glycan-Gold\nNanoparticles as Multifunctional Probes\nfor Multivalent Lectin\u2013Carbohydrate Binding: Implications for\nBlocking Virus Infection and Nanoparticle Assembly"],"prefix":"10.1021","volume":"142","author":[{"given":"Darshita","family":"Budhadev","sequence":"first","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emma","family":"Poole","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Inga","family":"Nehlmeier","sequence":"additional","affiliation":[{"name":"University of Go\u0308ttingen , , ,","place":["Go\u0308ttingen, Germany, 37073"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuanyuan","family":"Liu","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James","family":"Hooper","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth","family":"Kalverda","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Uchangi Satyaprasad","family":"Akshath","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicole","family":"Hondow","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7352-0360","authenticated-orcid":true,"given":"W. Bruce","family":"Turnbull","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefan","family":"Po\u0308hlmann","sequence":"additional","affiliation":[{"name":"University of Go\u0308ttingen , , ,","place":["Go\u0308ttingen, Germany, 37073"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4607-7356","authenticated-orcid":true,"given":"Yuan","family":"Guo","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3314-9242","authenticated-orcid":true,"given":"Dejian","family":"Zhou","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2020,9,16]]},"reference":[{"key":"2026090305221618600_cit1","doi-asserted-by":"publisher","first-page":"374","DOI":"10.1038\/s41577-018-0004-8","article-title":"C-type lectins in immunity and homeostasis","volume":"18","author":"Brown","year":"2018","journal-title":"Nat. Rev. Immunol."},{"key":"2026090305221618600_cit2","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1007\/s10719-019-09876-0","article-title":"Stuck on\nsugars - how carbohydrates regulate cell adhesion, recognition, and\nsignaling","volume":"36","author":"Cummings","year":"2019","journal-title":"Glycoconjugate J."},{"key":"2026090305221618600_cit3","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1038\/nri2569","article-title":"Signalling\nthrough C-type lectin receptors: shaping\nimmune responses","volume":"9","author":"Geijtenbeek","year":"2009","journal-title":"Nat. Rev. Immunol."},{"key":"2026090305221618600_cit4","doi-asserted-by":"publisher","first-page":"653","DOI":"10.1038\/nri3737","article-title":"Siglec-mediated\nregulation of immune\ncell function in disease","volume":"14","author":"Macauley","year":"2014","journal-title":"Nat. Rev. Immunol."},{"key":"2026090305221618600_cit5","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/j.1749-6632.2012.06492.x","article-title":"Glycobiology of immune responses","volume":"1253","author":"Rabinovich","year":"2012","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"2026090305221618600_cit6","doi-asserted-by":"publisher","first-page":"572","DOI":"10.1016\/j.ceb.2007.09.004","article-title":"Paradigms\nfor glycan-binding receptors in cell adhesion","volume":"19","author":"Taylor","year":"2007","journal-title":"Curr. Opin. Cell Biol."},{"key":"2026090305221618600_cit7","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1016\/j.coviro.2019.01.004","article-title":"Virus recognition\nof glycan receptors","volume":"34","author":"Thompson","year":"2019","journal-title":"Curr. Opin. Virol."},{"key":"2026090305221618600_cit8","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1016\/j.sbi.2017.04.002","article-title":"Recognition\nof microbial glycans\nby soluble human lectins","volume":"44","author":"Wesener","year":"2017","journal-title":"Curr. Opin. Struct.\nBiol."},{"key":"2026090305221618600_cit9","doi-asserted-by":"publisher","first-page":"6018","DOI":"10.1021\/jacs.7b01683","article-title":"Multivalent Glycosylated\nNanostructures To Inhibit Ebola Virus Infection","volume":"139","author":"Illescas","year":"2017","journal-title":"J. Am. Chem. Soc."},{"key":"2026090305221618600_cit10","doi-asserted-by":"publisher","first-page":"2754","DOI":"10.1002\/(SICI)1521-3773(19981102)37:20&lt;2754::AID-ANIE2754&gt;3.0.CO;2-3","article-title":"Polyvalent Interactions in Biological\nSystems: Implications for Design and Use of Multivalent Ligands and\nInhibitors","volume":"37","author":"Mammen","year":"1998","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026090305221618600_cit11","doi-asserted-by":"publisher","first-page":"669","DOI":"10.1038\/35001095","article-title":"Shiga-like\ntoxins are neutralized by tailored multivalent carbohydrate ligands","volume":"403","author":"Kitov","year":"2000","journal-title":"Nature"},{"key":"2026090305221618600_cit12","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1016\/S0065-2318(10)63005-3","article-title":"Multivalent lectin-carbohydrate interactions energetics\nand mechanisms of binding","volume":"63","author":"Dam","year":"2010","journal-title":"Adv. Carbohydr. Chem.\nBiochem."},{"key":"2026090305221618600_cit13","doi-asserted-by":"publisher","first-page":"8323","DOI":"10.1002\/anie.201404397","article-title":"A protein-based\npentavalent inhibitor of the cholera toxin B-subunit","volume":"53","author":"Branson","year":"2014","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026090305221618600_cit14","doi-asserted-by":"publisher","first-page":"4709","DOI":"10.1039\/C2CS35408J","article-title":"Multivalent glycoconjugates as anti-pathogenic\nagents","volume":"42","author":"Bernardi","year":"2013","journal-title":"Chem. Soc. Rev."},{"key":"2026090305221618600_cit15","doi-asserted-by":"publisher","first-page":"4202","DOI":"10.1074\/jbc.M609689200","article-title":"Multiple modes of binding enhance\nthe affinity of DC-SIGN\nfor high mannose N-linked glycans found on viral glycoproteins","volume":"282","author":"Feinberg","year":"2006","journal-title":"J. Biol. Chem."},{"key":"2026090305221618600_cit16","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms2302","article-title":"Virus-like glycodendrinanoparticles\ndisplaying quasi-equivalent nested polyvalency upon glycoprotein platforms\npotently block viral infection","volume":"3","author":"Ribeiro-Viana","year":"2012","journal-title":"Nat. Commun."},{"key":"2026090305221618600_cit17","doi-asserted-by":"publisher","first-page":"4746","DOI":"10.1039\/c2cs35424a","article-title":"Cyclodextrin-based multivalent glycodisplays:\ncovalent and supramolecular conjugates to assess carbohydrate-protein\ninteractions","volume":"42","author":"Martinez","year":"2013","journal-title":"Chem. Soc. Rev."},{"key":"2026090305221618600_cit18","doi-asserted-by":"publisher","first-page":"4358","DOI":"10.1039\/c2cs35427f","article-title":"Glyconanotechnology","volume":"42","author":"Reichardt","year":"2013","journal-title":"Chem. Soc.\nRev."},{"key":"2026090305221618600_cit19","doi-asserted-by":"publisher","first-page":"4557","DOI":"10.1039\/C2CS35406C","article-title":"Glycoclusters\non oligonucleotide\nand PNA scaffolds: synthesis and applications","volume":"42","author":"Spinelli","year":"2013","journal-title":"Chem. Soc. Rev."},{"key":"2026090305221618600_cit20","doi-asserted-by":"publisher","first-page":"3275","DOI":"10.1039\/C6CS00165C","article-title":"Organizing multivalency in carbohydrate\nrecognition","volume":"45","author":"Muller","year":"2016","journal-title":"Chem. Soc. Rev."},{"key":"2026090305221618600_cit21","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1038\/nchem.2387","article-title":"Synthesis of giant globular multivalent\nglycofullerenes as potent inhibitors in a model of Ebola virus infection","volume":"8","author":"Munoz","year":"2016","journal-title":"Nat. Chem."},{"key":"2026090305221618600_cit22","doi-asserted-by":"publisher","first-page":"9874","DOI":"10.1002\/chem.200900923","article-title":"Gold manno-glyconanoparticles: multivalent\nsystems to block HIV-1 gp120 binding to the lectin DC-SIGN","volume":"15","author":"Martinez-Avila","year":"2009","journal-title":"Chem. - Eur. J."},{"key":"2026090305221618600_cit23","doi-asserted-by":"publisher","first-page":"810","DOI":"10.1002\/anie.201307232","article-title":"Lactose\nas a \u2033Trojan horse\u2033 for quantum dot cell transport","volume":"53","author":"Benito-Alifonso","year":"2014","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026090305221618600_cit24","doi-asserted-by":"publisher","first-page":"8654","DOI":"10.1021\/jacs.5b12950","article-title":"Pathogen Inhibition by Multivalent\nLigand Architectures","volume":"138","author":"Bhatia","year":"2016","journal-title":"J. Am. Chem. Soc."},{"key":"2026090305221618600_cit25","doi-asserted-by":"publisher","first-page":"659","DOI":"10.1093\/protein\/gzr016","article-title":"Comparative analysis\nreveals selective recognition\nof glycans by the dendritic cell receptors DC-SIGN and Langerin","volume":"24","author":"Holla","year":"2011","journal-title":"Protein Eng., Des. Sel."},{"key":"2026090305221618600_cit26","doi-asserted-by":"publisher","first-page":"14577","DOI":"10.1021\/ja105852y","article-title":"Protein flexibility and conformational\nentropy in ligand design targeting the carbohydrate recognition domain\nof galectin-3","volume":"132","author":"Diehl","year":"2010","journal-title":"J. Am. Chem. Soc."},{"key":"2026090305221618600_cit27","doi-asserted-by":"publisher","first-page":"1047","DOI":"10.1021\/ja0378207","article-title":"Dissecting\nthe cholera toxin-ganglioside\nGM1 interaction by isothermal titration calorimetry","volume":"126","author":"Turnbull","year":"2004","journal-title":"J. Am. Chem. Soc."},{"key":"2026090305221618600_cit28","doi-asserted-by":"publisher","first-page":"3280","DOI":"10.1002\/anie.200904359","article-title":"Gold nanoparticles for biology and medicine","volume":"49","author":"Giljohann","year":"2010","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026090305221618600_cit29","doi-asserted-by":"publisher","first-page":"1547","DOI":"10.1021\/cr030067f","article-title":"Nanostructures in biodiagnostics","volume":"105","author":"Rosi","year":"2005","journal-title":"Chem. Rev."},{"key":"2026090305221618600_cit30","doi-asserted-by":"publisher","first-page":"1356","DOI":"10.1021\/ac061462j","article-title":"Glyconanoparticles for the colorimetric\ndetection of cholera toxin","volume":"79","author":"Schofield","year":"2007","journal-title":"Anal. Chem."},{"key":"2026090305221618600_cit31","doi-asserted-by":"publisher","first-page":"14044","DOI":"10.1021\/ja065223p","article-title":"Attomole microarray\ndetection of MicroRNAs by nanoparticle-amplified SPR imaging measurements\nof surface polyadenylation reactions","volume":"128","author":"Fang","year":"2006","journal-title":"J. Am.\nChem. Soc."},{"key":"2026090305221618600_cit32","doi-asserted-by":"publisher","first-page":"548","DOI":"10.1038\/nnano.2008.189","article-title":"Control of enhanced\nRaman scattering using a DNA-based assembly process of dye-coded nanoparticles","volume":"3","author":"Graham","year":"2008","journal-title":"Nat. Nanotechnol."},{"key":"2026090305221618600_cit33","doi-asserted-by":"publisher","first-page":"1536","DOI":"10.1126\/science.297.5586.1536","article-title":"Nanoparticles with Raman spectroscopic\nfingerprints for DNA and RNA detection","volume":"297","author":"Cao","year":"2002","journal-title":"Science"},{"key":"2026090305221618600_cit34","doi-asserted-by":"publisher","first-page":"4738","DOI":"10.1002\/anie.201600593","article-title":"Compact, Polyvalent\nMannose Quantum Dots as Sensitive, Ratiometric FRET Probes for Multivalent\nProtein-Ligand Interactions","volume":"55","author":"Guo","year":"2016","journal-title":"Angew. Chem., Int.\nEd."},{"key":"2026090305221618600_cit35","doi-asserted-by":"publisher","first-page":"11833","DOI":"10.1021\/jacs.7b05104","article-title":"Dissecting\nMultivalent\nLectin-Carbohydrate Recognition Using Polyvalent Multifunctional Glycan-Quantum\nDots","volume":"139","author":"Guo","year":"2017","journal-title":"J. Am. Chem. Soc."},{"key":"2026090305221618600_cit36","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1021\/bk-2020-1346.ch004","article-title":"Polyvalent\nGlycan-Quantum Dots as Multifunctional Structural\nProbes for Multivalent Lectin-Carbohydrate Interactions","volume":"1346","author":"Hooper","year":"2020","journal-title":"ACS Symp. Ser."},{"key":"2026090305221618600_cit37","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1016\/S0092-8674(00)80694-7","article-title":"DC-SIGN, a dendritic cell-specific HIV-1-binding protein\nthat enhances trans-infection of T cells","volume":"100","author":"Geijtenbeek","year":"2000","journal-title":"Cell"},{"key":"2026090305221618600_cit38","doi-asserted-by":"publisher","first-page":"591","DOI":"10.1038\/nsmb784","article-title":"Structural\nbasis for distinct ligand-binding and targeting properties of the\nreceptors DC-SIGN and DC-SIGNR","volume":"11","author":"Guo","year":"2004","journal-title":"Nat. Struct.\nMol. Biol."},{"key":"2026090305221618600_cit39","doi-asserted-by":"publisher","first-page":"2670","DOI":"10.1073\/pnas.051631398","article-title":"DC-SIGNR,\na DC-SIGN homologue expressed in endothelial cells, binds to human\nand simian immunodeficiency viruses and activates infection in trans","volume":"98","author":"Pohlmann","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2026090305221618600_cit40","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1016\/bs.mie.2017.06.012","article-title":"Probing Multivalent\nProtein-Carbohydrate\nInteractions by Quantum Dot-Forster Resonance Energy Transfer","volume":"598","author":"Guo","year":"2018","journal-title":"Methods Enzymol."},{"key":"2026090305221618600_cit41","doi-asserted-by":"publisher","first-page":"14862","DOI":"10.1073\/pnas.1820165116","article-title":"Antigen structure affects cellular\nrouting through\nDC-SIGN","volume":"116","author":"Jarvis","year":"2019","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2026090305221618600_cit42","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1038\/nri2569","article-title":"Signalling\nthrough C-type lectin receptors: shaping\nimmune responses","volume":"9","author":"Geijtenbeek","year":"2009","journal-title":"Nat. Rev. Immunol."},{"key":"2026090305221618600_cit43","doi-asserted-by":"publisher","first-page":"1081","DOI":"10.1038\/ni.1778","article-title":"Carbohydrate-specific\nsignaling through the DC-SIGN\nsignalosome tailors immunity to Mycobacterium tuberculosis, HIV-1\nand Helicobacter pylori","volume":"10","author":"Gringhuis","year":"2009","journal-title":"Nat. Immunol."},{"key":"2026090305221618600_cit44","doi-asserted-by":"publisher","first-page":"593","DOI":"10.1038\/ni.f.203","article-title":"Protein-glycan interactions in the\ncontrol of innate and adaptive immune responses","volume":"9","author":"van Kooyk","year":"2008","journal-title":"Nat. Immunol."},{"key":"2026090305221618600_cit45","doi-asserted-by":"publisher","first-page":"1043","DOI":"10.1126\/science.aad2450","article-title":"Cryo-EM structure of a native, fully\nglycosylated, cleaved HIV-1 envelope trimer","volume":"351","author":"Lee","year":"2016","journal-title":"Science"},{"key":"2026090305221618600_cit46","doi-asserted-by":"publisher","first-page":"813","DOI":"10.1016\/j.cell.2016.04.010","article-title":"l Trimeric HIV-1-Env Structures Define Glycan\nShields from Clades A, B, and G","volume":"165","author":"Stewart-Jones","year":"2016","journal-title":"Cell"},{"key":"2026090305221618600_cit47","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1038\/86762","article-title":"Single-mismatch\ndetection using gold-quenched\nfluorescent oligonucleotides","volume":"19","author":"Dubertret","year":"2001","journal-title":"Nat. Biotechnol."},{"key":"2026090305221618600_cit48","doi-asserted-by":"publisher","first-page":"13987","DOI":"10.1021\/ja0749744","article-title":"Enhancing\nthe stability and biological functionalities\nof quantum dots via compact multifunctional ligands","volume":"129","author":"Susumu","year":"2007","journal-title":"J. Am. Chem. Soc."},{"key":"2026090305221618600_cit49","doi-asserted-by":"publisher","first-page":"1517","DOI":"10.1021\/nl0345926","article-title":"Building three-dimensional\nsurface biological assemblies on the nanometer scale","volume":"3","author":"Zhou","year":"2003","journal-title":"Nano Lett."},{"key":"2026090305221618600_cit50","doi-asserted-by":"publisher","first-page":"15403","DOI":"10.1021\/jacs.9b08003","article-title":"Synthesis of Highly Efficient Multivalent Disaccharide\/\n60 Fullerene Nanoballs for Emergent Viruses","volume":"141","author":"Ramos-Soriano","year":"2019","journal-title":"J. Am. Chem. Soc."},{"key":"2026090305221618600_cit51","doi-asserted-by":"publisher","first-page":"15232","DOI":"10.1021\/acsami.6b13807","article-title":"Ultraefficient Cap-Exchange\nProtocol To Compact Biofunctional Quantum Dots for Sensitive Ratiometric\nBiosensing and Cell Imaging","volume":"9","author":"Wang","year":"2017","journal-title":"ACS Appl. Mater.\nInterfaces"},{"key":"2026090305221618600_cit52","doi-asserted-by":"publisher","first-page":"2648","DOI":"10.1021\/jo00008a014","article-title":"Selective\nReduction of Disulfides by Tris(2-Carboxyethyl)phosphine","volume":"56","author":"Burns","year":"1991","journal-title":"J. Org. Chem."},{"key":"2026090305221618600_cit53","doi-asserted-by":"publisher","first-page":"1103","DOI":"10.1021\/cr0300789","article-title":"Self-assembled\nmonolayers of thiolates on metals as a form of nanotechnology","volume":"105","author":"Love","year":"2005","journal-title":"Chem. Rev."},{"key":"2026090305221618600_cit54","doi-asserted-by":"publisher","first-page":"418","DOI":"10.1021\/nn800726e","article-title":"The Role Radius\nof Curvature Plays in Thiolated Oligonucleotide Loading on Gold Nanoparticles","volume":"3","author":"Hill","year":"2009","journal-title":"ACS Nano"},{"key":"2026090305221618600_cit55","doi-asserted-by":"publisher","first-page":"5462","DOI":"10.1021\/ja0583665","article-title":"Fluorescent lifetime quenching near\nd = 1.5 nm gold nanoparticles: Probing NSET validity","volume":"128","author":"Jennings","year":"2006","journal-title":"J. Am. Chem. 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