{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T02:59:40Z","timestamp":1760151580838,"version":"build-2065373602"},"reference-count":42,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2022,3,29]],"date-time":"2022-03-29T00:00:00Z","timestamp":1648512000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000277","name":"Department for Environment Food and Rural Affairs","doi-asserted-by":"publisher","award":["SE1130"],"award-info":[{"award-number":["SE1130"]}],"id":[{"id":"10.13039\/501100000277","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/S506680\/1"],"award-info":[{"award-number":["BB\/S506680\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Foot-and-mouth disease (FMD) is a disease of cloven-hoofed livestock caused by FMD virus (FMDV). FMD can be controlled through the use of inactivated vaccines, and it is well established that the protection afforded by FMD vaccines correlates strongly with neutralising antibody titres. However, the overall strength of binding, referred to as avidity, is also an important parameter with respect to the ability of antibodies to neutralise virus infection, and there is evidence that avidity can affect the level of protection afforded by FMDV vaccines. Here, as an alternative to modified enzyme-linked immunosorbent assays (avidity ELISAs) incorporating a chaotropic wash step, we used bio-layer interferometry (BLI) to measure the avidity of bovine polyclonal antibodies against FMDV capsids. We conducted preliminary experiments using recombinant FMDV capsids, as well as peptides representing antigenic loops, to demonstrate that the binding of monoclonal antibodies targeting specific antigenic sites could be detected using BLI. Subsequent experiments using polyclonal sera derived from FMD vaccinated cattle provided evidence of a positive correlation between the neutralising titre of the serum and the avidity as measured by BLI. Furthermore, we observed an increase in BLI avidity, as well as in the titre, in vaccinated animals upon challenge with the live virus.<\/jats:p>","DOI":"10.3390\/v14040714","type":"journal-article","created":{"date-parts":[[2022,3,29]],"date-time":"2022-03-29T21:45:51Z","timestamp":1648590351000},"page":"714","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Avidity of Polyclonal Antibodies to Foot-and-Mouth Disease Virus in Bovine Serum Measured Using Bio-Layer Interferometry"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5761-9769","authenticated-orcid":false,"given":"Andrew E.","family":"Shaw","sequence":"first","affiliation":[{"name":"The Pirbright Institute, Pirbright, Woking GU24 0NF, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alison","family":"Burman","sequence":"additional","affiliation":[{"name":"The Pirbright Institute, Pirbright, Woking GU24 0NF, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Amin","family":"Asfor","sequence":"additional","affiliation":[{"name":"The Pirbright Institute, Pirbright, Woking GU24 0NF, UK"},{"name":"Department of Pathology and Infectious Diseases, Faculty of Health and Medical Sciences, School of Veterinary Medicine, University of Surrey, Guilford GU2 7AL, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1864-080X","authenticated-orcid":false,"given":"Emiliana","family":"Brocchi","sequence":"additional","affiliation":[{"name":"Istituto Zooprofilattico Sperimentale della Lombardia e Dell\u2019Emilia Romagna \u201cBruno Ubertini\u201d, 25124 Brescia, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Santina","family":"Grazioli","sequence":"additional","affiliation":[{"name":"Istituto Zooprofilattico Sperimentale della Lombardia e Dell\u2019Emilia Romagna \u201cBruno Ubertini\u201d, 25124 Brescia, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Clare","family":"Browning","sequence":"additional","affiliation":[{"name":"The Pirbright Institute, Pirbright, Woking GU24 0NF, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anna","family":"Ludi","sequence":"additional","affiliation":[{"name":"The Pirbright Institute, Pirbright, Woking GU24 0NF, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6582-388X","authenticated-orcid":false,"given":"Tobias J.","family":"Tuthill","sequence":"additional","affiliation":[{"name":"The Pirbright Institute, Pirbright, Woking GU24 0NF, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6959-2708","authenticated-orcid":false,"given":"Donald P.","family":"King","sequence":"additional","affiliation":[{"name":"The Pirbright Institute, Pirbright, Woking GU24 0NF, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,3,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.prevetmed.2013.07.013","article-title":"The economic impacts of foot and mouth disease\u2014What are they, how big are they and where do they occur?","volume":"112","author":"Rushton","year":"2013","journal-title":"Prev. Vet. Med."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"veab009","DOI":"10.1093\/ve\/veab009","article-title":"The history of foot-and-mouth disease virus serotype C: The first known extinct serotype?","volume":"7","author":"Paton","year":"2021","journal-title":"Virus Evol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"5515","DOI":"10.1016\/j.vaccine.2019.07.102","article-title":"Estimating the protection afforded by foot-and-mouth disease vaccines in the laboratory","volume":"37","author":"Paton","year":"2019","journal-title":"Vaccine"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1099\/0022-1317-70-3-639","article-title":"Evidence for at least four antigenic sites on type O foot-and-mouth disease virus involved in neutralization; identification by single and multiple site monoclonal antibody-resistant mutants","volume":"70","author":"McCahon","year":"1989","journal-title":"J. Gen. Virol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1099\/vir.0.048249-0","article-title":"Mapping of antigenic sites of foot-and-mouth disease virus serotype Asia 1 and relationships with sites described in other serotypes","volume":"94","author":"Grazioli","year":"2013","journal-title":"J. Gen. Virol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1099\/0022-1317-74-8-1547","article-title":"Identification of a fifth neutralizable site on type O foot-and-mouth disease virus following characterization of single and quintuple monoclonal antibody escape mutants","volume":"74","author":"Crowther","year":"1993","journal-title":"J. Gen. Virol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1016\/0264-410X(92)90092-X","article-title":"Foot and mouth disease vaccine potency test in cattle: The interrelationship of antigen dose, serum neutralizing antibody response and protection from challenge","volume":"10","author":"Pay","year":"1992","journal-title":"Vaccine"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1681","DOI":"10.1016\/j.vaccine.2008.01.038","article-title":"High potency vaccines induce protection against heterologous challenge with foot-and-mouth disease virus","volume":"26","author":"Brehm","year":"2008","journal-title":"Vaccine"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"938","DOI":"10.1016\/j.cell.2018.07.033","article-title":"Systematic Analysis of Monoclonal Antibodies against Ebola Virus GP Defines Features that Contribute to Protection","volume":"174","author":"Saphire","year":"2018","journal-title":"Cell"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1038\/nri.2017.106","article-title":"Beyond binding: Antibody effector functions in infectious diseases","volume":"18","author":"Lu","year":"2017","journal-title":"Nat. Rev. Immunol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"6845","DOI":"10.1016\/j.vaccine.2012.09.011","article-title":"Avidity and subtyping of specific antibodies applied to the indirect assessment of heterologous protection against Foot-and-Mouth Disease Virus in cattle","volume":"30","author":"Lavoria","year":"2012","journal-title":"Vaccine"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1016\/j.vaccine.2013.12.007","article-title":"Accuracy of traditional and novel serology tests for predicting cross-protection in foot-and-mouth disease vaccinated cattle","volume":"32","author":"Brito","year":"2014","journal-title":"Vaccine"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"5981","DOI":"10.1128\/JVI.00320-15","article-title":"What Do Chaotrope-Based Avidity Assays for Antibodies to HIV-1 Envelope Glycoproteins Measure?","volume":"89","author":"Alexander","year":"2015","journal-title":"J. Virol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Kimuda, S.G., Biraro, I.A., Bagaya, B.S., Raynes, J.G., and Cose, S. (2018). Characterising antibody avidity in individuals of varied Mycobacterium tuberculosis infection status using surface plasmon resonance. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0205102"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1315","DOI":"10.4049\/jimmunol.1800323","article-title":"Qualified Biolayer Interferometry Avidity Measurements Distinguish the Heterogeneity of Antibody Interactions with Plasmodium falciparum Circumsporozoite Protein Antigens","volume":"201","author":"Dennison","year":"2018","journal-title":"J. Immunol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1586\/14760584.2016.1128831","article-title":"How to assess the binding strength of antibodies elicited by vaccination against HIV and other viruses","volume":"15","author":"Klasse","year":"2016","journal-title":"Expert Rev. Vaccines"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1637","DOI":"10.1099\/0022-1317-68-6-1637","article-title":"Neutralization of foot-and-mouth disease virus can be mediated through any of at least three separate antigenic sites","volume":"68","author":"Xie","year":"1987","journal-title":"J. Gen. Virol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2761","DOI":"10.1016\/j.vaccine.2017.02.047","article-title":"Efficacy of a high potency O1 Manisa foot-and-mouth disease vaccine in cattle against heterologous challenge with a field virus from the O\/ME-SA\/Ind-2001 lineage collected in North Africa","volume":"35","author":"Fishbourne","year":"2017","journal-title":"Vaccine"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Shimmon, G., Wood, B.A., Morris, A., Mioulet, V., Grazioli, S., Brocchi, E., Berryman, S., Tuthill, T., King, D.P., and Burman, A. (2016). Truncated bovine integrin alpha-V\/beta-6 as a universal capture ligand for FMD diagnosis. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0160696"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"e01527-19","DOI":"10.1128\/JCM.01527-19","article-title":"Detection of Bovine Antibodies against a Conserved Capsid Epitope as the Basis of a Novel Universal Serological Test for Foot-and-Mouth Disease","volume":"58","author":"Asfor","year":"2020","journal-title":"J. Clin. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Porta, C., Kotecha, A., Burman, A., Jackson, T., Ren, J., Loureiro, S., Jones, I.M., Fry, E.E., Stuart, D.I., and Charleston, B. (2013). Rational engineering of recombinant picornavirus capsids to produce safe, protective vaccine antigen. PLoS Pathog., 9.","DOI":"10.1371\/journal.ppat.1003255"},{"key":"ref_22","unstructured":"R Core Team (2016). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"4949","DOI":"10.1128\/JVI.74.11.4949-4956.2000","article-title":"The epithelial integrin alphavbeta6 is a receptor for foot-and-mouth disease virus","volume":"74","author":"Jackson","year":"2000","journal-title":"J. Virol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"694","DOI":"10.1038\/306694a0","article-title":"Chemical basis of antigenic variation in foot-and-mouth disease virus","volume":"306","author":"Rowlands","year":"1983","journal-title":"Nature"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1104","DOI":"10.1099\/vir.0.060939-0","article-title":"Novel antibody binding determinants on the capsid surface of serotype O foot-and-mouth disease virus","volume":"95","author":"Asfor","year":"2014","journal-title":"J. Gen. Virol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1099\/vir.0.000051","article-title":"Prediction and characterization of novel epitopes of serotype A foot-and-mouth disease viruses circulating in East Africa using site-directed mutagenesis","volume":"96","author":"Bari","year":"2015","journal-title":"J. Gen. Virol."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Soria, I., Quattrocchi, V., Langellotti, C., Gammella, M., Digiacomo, S., and Garcia de la Torre, B. (2017). Andreu, D.; Montoya, M.; Sobrino, F.; Blanco, B.; et al. Dendrimeric peptides can confer protection against foot-and-mouth disease virus in cattle. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0185184"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"7223","DOI":"10.1128\/JVI.00401-08","article-title":"Enhanced Mucosal Immunoglobulin A Response and Solid Protection against Foot-and-Mouth Disease Virus Challenge Induced by a Novel Dendrimeric Peptide","volume":"82","author":"Cubillos","year":"2008","journal-title":"J. Virol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1038\/298030a0","article-title":"Protection against foot-and-mouth disease by immunization with a chemically synthesized peptide predicted from the viral nucleotide sequence","volume":"298","author":"Bittle","year":"1982","journal-title":"Nature"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2606","DOI":"10.1128\/jvi.71.4.2606-2614.1997","article-title":"A large-scale evaluation of peptide vaccines against foot-and-mouth disease: Lack of solid protection in cattle and isolation of escape mutants","volume":"71","author":"Taboga","year":"1997","journal-title":"J. Virol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Ca\u00f1as-Arranz, R., Forner, M., Defaus, S., de Le\u00f3n, P., Bustos, M.J., Torres, E., Sobrino, F., Andreu, D., and Blanco, E. (2020). A Single Dose of Dendrimer B 2 T Peptide Vaccine Partially Protects Pigs against Foot-and-Mouth Disease Virus Infection. Vaccines, 8.","DOI":"10.3390\/vaccines8010019"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"3751","DOI":"10.1016\/S0264-410X(03)00364-5","article-title":"A synthetic peptide containing the consensus sequence of the G\u2013H loop region of foot-and-mouth disease virus type-O VP1 and a promiscuous T-helper epitope induces peptide-specific antibodies but fails to protect cattle against viral challenge","volume":"21","author":"Rodriguez","year":"2003","journal-title":"Vaccine"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"749","DOI":"10.4049\/jimmunol.146.2.749","article-title":"A T cell epitope in VP1 of foot-and-mouth disease virus is immunodominant for vaccinated cattle","volume":"146","author":"Collen","year":"1991","journal-title":"J. Immunol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"475960","DOI":"10.1155\/2013\/475960","article-title":"B epitope multiplicity and B\/T epitope orientation influence immunogenicity of foot-and-mouth disease peptide vaccines","volume":"2013","author":"Blanco","year":"2013","journal-title":"Clin. Dev. Immunol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2870","DOI":"10.3389\/fimmu.2019.02870","article-title":"Development of Foot-and-Mouth Disease Virus-Neutralizing Monoclonal Antibodies Derived From Plasmablasts of Infected Cattle and Their Germline Gene Usage","volume":"10","author":"Li","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"He, Y., Li, K., Cao, Y., Sun, Z., Li, P., Bao, H., Wang, S., Zhu, G., Bai, X., and Sun, P. (2021). Structures of Foot-and-mouth disease virus with neutralizing antibodies derived from recovered natural host reveal a mechanism for cross-serotype neutralization. PLoS Pathog., 17.","DOI":"10.1371\/journal.ppat.1009507"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.coi.2020.06.003","article-title":"Dissecting the antibody-OME: Past, present, and future","volume":"65","author":"Loos","year":"2020","journal-title":"Curr. Opin. Immunol."},{"key":"ref_38","first-page":"187","article-title":"Opsonization-enhanced phagocytosis of foot-and-mouth disease virus","volume":"65","author":"Mccullough","year":"1988","journal-title":"Immunology"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jim.2017.07.001","article-title":"Enhanced sensitivity in detection of antiviral antibody responses using biotinylation of foot-and-mouth disease virus (FMDV) capsids","volume":"450","author":"Kenney","year":"2017","journal-title":"J. Immunol. Methods"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1016\/S0264-410X(96)00284-8","article-title":"Total and isotype humoral responses in cattle vaccinated with foot and mouth disease virus (FMDV) immunogen produced either in bovine tongue tissue or in BHK-21 cell suspension cultures","volume":"15","author":"Capozzo","year":"1997","journal-title":"Vaccine"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"21738","DOI":"10.1038\/s41598-020-78895-x","article-title":"Rapid and sensitive detection of SARS-CoV-2 antibodies by biolayer interferometry","volume":"10","author":"Dzimianski","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1016\/j.snb.2015.06.088","article-title":"Rapid and sensitive detection of norovirus antibodies in human serum with a biolayer interferometry biosensor","volume":"221","author":"Auer","year":"2015","journal-title":"Sens. Actuators B Chem."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/14\/4\/714\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:46:05Z","timestamp":1760136365000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/14\/4\/714"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,29]]},"references-count":42,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2022,4]]}},"alternative-id":["v14040714"],"URL":"https:\/\/doi.org\/10.3390\/v14040714","relation":{},"ISSN":["1999-4915"],"issn-type":[{"type":"electronic","value":"1999-4915"}],"subject":[],"published":{"date-parts":[[2022,3,29]]}}}