{"id":"https://openalex.org/W1978807612","doi":"https://doi.org/10.1073/pnas.0903427106","title":"Differential neutralization efficiency of hemagglutinin epitopes, antibody interference, and the design of influenza vaccines","display_name":"Differential neutralization efficiency of hemagglutinin epitopes, antibody interference, and the design of influenza vaccines","publication_year":2009,"publication_date":"2009-05-13","ids":{"openalex":"https://openalex.org/W1978807612","doi":"https://doi.org/10.1073/pnas.0903427106","mag":"1978807612","pmid":"https://pubmed.ncbi.nlm.nih.gov/19439657","pmcid":"https://www.ncbi.nlm.nih.gov/pmc/articles/2688967"},"language":"en","primary_location":{"id":"doi:10.1073/pnas.0903427106","doi":"https://doi.org/10.1073/pnas.0903427106","is_oa":false,"landing_page_url":"https://doi.org/10.1073/pnas.0903427106","pdf_url":null,"source":{"id":"https://openalex.org/S125754415","display_name":"Proceedings of the National Academy of Sciences","issn_l":"0027-8424","issn":["0027-8424","1091-6490"],"is_oa":false,"is_in_doaj":false,"is_core":true,"listed_in":["anvur-class-a","anvur-scientific","cwts-core","dongbi-a","doyens","erih-plus","jufo-3","ki-jl-3","medline","norway-2","poland-200","russia-white-list-1","vabb-shw"],"host_organization":"https://openalex.org/P4310320052","host_organization_name":"National Academy of Sciences","host_organization_lineage":["https://openalex.org/P4310320052"],"host_organization_lineage_names":["National Academy of Sciences"],"type":"journal"},"license":null,"license_id":null,"version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":"Proceedings of the National Academy of Sciences","raw_type":"journal-article"},"volume":null,"type":"article","indexed_in":["crossref","pubmed"],"open_access":{"is_oa":true,"oa_status":"green","oa_url":"https://www.ncbi.nlm.nih.gov/pmc/articles/2688967","any_repository_has_fulltext":true},"authorships":[{"author_position":"first","author":{"id":"https://openalex.org/A5041306570","display_name":"Wilfred O. Ndifon","orcid":"https://orcid.org/0000-0001-6022-432X","observed_orcids":["https://orcid.org/0000-0001-6022-432X"]},"institutions":[{"id":"https://openalex.org/I20089843","display_name":"Princeton University","ror":"https://ror.org/00hx57361","country_code":"US","type":"education","lineage":["https://openalex.org/I20089843"]}],"countries":["US"],"is_corresponding":false,"raw_author_name":"Wilfred Ndifon","raw_affiliation_strings":["Departments of aEcology and Evolutionary Biology, and","Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, 08544, USA,"],"raw_orcid":null,"affiliations":[{"raw_affiliation_string":"Departments of aEcology and Evolutionary Biology, and","institution_ids":[]},{"raw_affiliation_string":"Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, 08544, USA,","institution_ids":["https://openalex.org/I20089843"]}]},{"author_position":"middle","author":{"id":"https://openalex.org/A5071133192","display_name":"Ned S. Wingreen","orcid":"https://orcid.org/0000-0001-7384-2821","observed_orcids":["https://orcid.org/0000-0001-7384-2821"]},"institutions":[{"id":"https://openalex.org/I20089843","display_name":"Princeton University","ror":"https://ror.org/00hx57361","country_code":"US","type":"education","lineage":["https://openalex.org/I20089843"]}],"countries":["US"],"is_corresponding":false,"raw_author_name":"Ned S. Wingreen","raw_affiliation_strings":["Molecular Biology, Princeton University, Princeton, NJ 08544"],"raw_orcid":null,"affiliations":[{"raw_affiliation_string":"Molecular Biology, Princeton University, Princeton, NJ 08544","institution_ids":["https://openalex.org/I20089843"]}]},{"author_position":"last","author":{"id":"https://openalex.org/A5077712228","display_name":"Simon A. Levin","orcid":"https://orcid.org/0000-0002-8216-5639","observed_orcids":["https://orcid.org/0000-0002-8216-5639","https://orcid.org/0000-0003-0895-0361"]},"institutions":[{"id":"https://openalex.org/I20089843","display_name":"Princeton University","ror":"https://ror.org/00hx57361","country_code":"US","type":"education","lineage":["https://openalex.org/I20089843"]},{"id":"https://openalex.org/I4405268937","display_name":"High Meadows Environmental Institute","ror":"https://ror.org/02hgay921","country_code":"US","type":"facility","lineage":["https://openalex.org/I4405268937"]}],"countries":["US"],"is_corresponding":false,"raw_author_name":"Simon A. Levin","raw_affiliation_strings":["Departments of aEcology and Evolutionary Biology, and","Princeton Environmental Institute"],"raw_orcid":null,"affiliations":[{"raw_affiliation_string":"Departments of aEcology and Evolutionary Biology, and","institution_ids":[]},{"raw_affiliation_string":"Princeton Environmental Institute","institution_ids":["https://openalex.org/I20089843","https://openalex.org/I4405268937"]}]}],"institutions":[],"countries_distinct_count":1,"institutions_distinct_count":2,"corresponding_author_ids":[],"corresponding_institution_ids":[],"apc_list":null,"apc_paid":null,"fwci":4.654,"has_fulltext":false,"cited_by_count":109,"citation_normalized_percentile":{"value":0.94972598,"is_in_top_1_percent":false,"is_in_top_10_percent":true},"cited_by_percentile_year":{"min":93,"max":99},"biblio":{"volume":"106","issue":"21","first_page":"8701","last_page":"8706"},"is_retracted":false,"is_paratext":false,"is_xpac":false,"primary_topic":{"id":"https://openalex.org/T10167","display_name":"Influenza Virus Research Studies","score":0.9994999766349792,"subfield":{"id":"https://openalex.org/subfields/2713","display_name":"Epidemiology"},"field":{"id":"https://openalex.org/fields/27","display_name":"Medicine"},"domain":{"id":"https://openalex.org/domains/4","display_name":"Health Sciences"}},"topics":[{"id":"https://openalex.org/T10167","display_name":"Influenza Virus Research Studies","score":0.9994999766349792,"subfield":{"id":"https://openalex.org/subfields/2713","display_name":"Epidemiology"},"field":{"id":"https://openalex.org/fields/27","display_name":"Medicine"},"domain":{"id":"https://openalex.org/domains/4","display_name":"Health Sciences"}},{"id":"https://openalex.org/T11764","display_name":"Evolution and Genetic Dynamics","score":9.999999747378752e-05,"subfield":{"id":"https://openalex.org/subfields/1311","display_name":"Genetics"},"field":{"id":"https://openalex.org/fields/13","display_name":"Biochemistry, Genetics and Molecular Biology"},"domain":{"id":"https://openalex.org/domains/1","display_name":"Life Sciences"}},{"id":"https://openalex.org/T12576","display_name":"vaccines and immunoinformatics approaches","score":9.999999747378752e-05,"subfield":{"id":"https://openalex.org/subfields/1312","display_name":"Molecular Biology"},"field":{"id":"https://openalex.org/fields/13","display_name":"Biochemistry, Genetics and Molecular Biology"},"domain":{"id":"https://openalex.org/domains/1","display_name":"Life Sciences"}}],"keywords":[{"id":"https://openalex.org/keywords/influenza-virus-hemagglutinin","display_name":"influenza virus hemagglutinin","score":0.824999988079071},{"id":"https://openalex.org/keywords/antibody-neutralization","display_name":"antibody neutralization","score":0.9070000052452087},{"id":"https://openalex.org/keywords/epitope-mutations","display_name":"epitope mutations","score":0.6690000295639038},{"id":"https://openalex.org/keywords/steric-interference","display_name":"steric interference","score":0.7429999709129333},{"id":"https://openalex.org/keywords/antibody-competition","display_name":"antibody competition","score":0.6510000228881836},{"id":"https://openalex.org/keywords/amino-acid-mutations","display_name":"amino acid mutations","score":0.5929999947547913},{"id":"https://openalex.org/keywords/h3n2","display_name":"H3N2","score":0.8309999704360962},{"id":"https://openalex.org/keywords/vaccine-design","display_name":"vaccine design","score":0.6740000247955322}],"concepts":[{"id":"https://openalex.org/C14086860","wikidata":"https://www.wikidata.org/wiki/Q337120","display_name":"Neutralization","level":3,"score":0.9577587842941284},{"id":"https://openalex.org/C159047783","wikidata":"https://www.wikidata.org/wiki/Q7215","display_name":"Virology","level":1,"score":0.755509614944458},{"id":"https://openalex.org/C2778692840","wikidata":"https://www.wikidata.org/wiki/Q9136673","display_name":"Hemagglutinin (influenza)","level":3,"score":0.7444849610328674},{"id":"https://openalex.org/C195616568","wikidata":"https://www.wikidata.org/wiki/Q128711","display_name":"Epitope","level":3,"score":0.6939740180969238},{"id":"https://openalex.org/C7842527","wikidata":"https://www.wikidata.org/wiki/Q575258","display_name":"Antigenic drift","level":4,"score":0.6446610689163208},{"id":"https://openalex.org/C159654299","wikidata":"https://www.wikidata.org/wiki/Q79460","display_name":"Antibody","level":2,"score":0.5863162875175476},{"id":"https://openalex.org/C2522874641","wikidata":"https://www.wikidata.org/wiki/Q808","display_name":"Virus","level":2,"score":0.5294368267059326},{"id":"https://openalex.org/C86803240","wikidata":"https://www.wikidata.org/wiki/Q420","display_name":"Biology","level":0,"score":0.5158645510673523},{"id":"https://openalex.org/C2909928835","wikidata":"https://www.wikidata.org/wiki/Q70684351","display_name":"Viral Interference","level":4,"score":0.469070166349411},{"id":"https://openalex.org/C515207424","wikidata":"https://www.wikidata.org/wiki/Q8066","display_name":"Amino acid","level":2,"score":0.4502800703048706},{"id":"https://openalex.org/C2777546802","wikidata":"https://www.wikidata.org/wiki/Q834390","display_name":"Influenza A virus","level":3,"score":0.4356768727302551},{"id":"https://openalex.org/C140704245","wikidata":"https://www.wikidata.org/wiki/Q3933202","display_name":"Viral replication","level":3,"score":0.14356744289398193},{"id":"https://openalex.org/C54355233","wikidata":"https://www.wikidata.org/wiki/Q7162","display_name":"Genetics","level":1,"score":0.10872915387153625}],"mesh":[{"descriptor_ui":"D000596","descriptor_name":"Amino Acids","qualifier_ui":"Q000276","qualifier_name":"immunology","is_major_topic":false},{"descriptor_ui":"D000914","descriptor_name":"Antibodies, Viral","qualifier_ui":"Q000276","qualifier_name":"immunology","is_major_topic":true},{"descriptor_ui":"D000914","descriptor_name":"Antibodies, Viral","qualifier_ui":"Q000737","qualifier_name":"chemistry","is_major_topic":false},{"descriptor_ui":"D000939","descriptor_name":"Epitopes","qualifier_ui":"Q000276","qualifier_name":"immunology","is_major_topic":true},{"descriptor_ui":"D000956","descriptor_name":"Antigens, Viral","qualifier_ui":"Q000276","qualifier_name":"immunology","is_major_topic":false},{"descriptor_ui":"D001665","descriptor_name":"Binding Sites","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false},{"descriptor_ui":"D007252","descriptor_name":"Influenza Vaccines","qualifier_ui":"Q000276","qualifier_name":"immunology","is_major_topic":true},{"descriptor_ui":"D008958","descriptor_name":"Models, Molecular","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false},{"descriptor_ui":"D017434","descriptor_name":"Protein Structure, Tertiary","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false},{"descriptor_ui":"D019267","descriptor_name":"Hemagglutinin Glycoproteins, Influenza Virus","qualifier_ui":"Q000276","qualifier_name":"immunology","is_major_topic":true},{"descriptor_ui":"D019267","descriptor_name":"Hemagglutinin Glycoproteins, Influenza Virus","qualifier_ui":"Q000737","qualifier_name":"chemistry","is_major_topic":false},{"descriptor_ui":"D053122","descriptor_name":"Influenza A Virus, H3N2 Subtype","qualifier_ui":"Q000276","qualifier_name":"immunology","is_major_topic":true}],"locations_count":3,"locations":[{"id":"doi:10.1073/pnas.0903427106","doi":"https://doi.org/10.1073/pnas.0903427106","is_oa":false,"landing_page_url":"https://doi.org/10.1073/pnas.0903427106","pdf_url":null,"source":{"id":"https://openalex.org/S125754415","display_name":"Proceedings of the National Academy of Sciences","issn_l":"0027-8424","issn":["0027-8424","1091-6490"],"is_oa":false,"is_in_doaj":false,"is_core":true,"listed_in":["anvur-class-a","anvur-scientific","cwts-core","dongbi-a","doyens","erih-plus","jufo-3","ki-jl-3","medline","norway-2","poland-200","russia-white-list-1","vabb-shw"],"host_organization":"https://openalex.org/P4310320052","host_organization_name":"National Academy of Sciences","host_organization_lineage":["https://openalex.org/P4310320052"],"host_organization_lineage_names":["National Academy of Sciences"],"type":"journal"},"license":null,"license_id":null,"version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":"Proceedings of the National Academy of Sciences","raw_type":"journal-article"},{"id":"pmh:oai:pubmedcentral.nih.gov:2688967","doi":null,"is_oa":true,"landing_page_url":"https://www.ncbi.nlm.nih.gov/pmc/articles/2688967","pdf_url":null,"source":{"id":"https://openalex.org/S2764455111","display_name":"PubMed Central","issn_l":null,"issn":null,"is_oa":true,"is_in_doaj":false,"is_core":false,"listed_in":[],"host_organization":"https://openalex.org/I1299303238","host_organization_name":"National Institutes of Health","host_organization_lineage":["https://openalex.org/I1299303238"],"host_organization_lineage_names":[],"type":"repository"},"license":null,"license_id":null,"version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":"Proc Natl Acad Sci U S A","raw_type":"Text"},{"id":"pmid:19439657","doi":null,"is_oa":false,"landing_page_url":"https://pubmed.ncbi.nlm.nih.gov/19439657","pdf_url":null,"source":{"id":"https://openalex.org/S4306525036","display_name":"PubMed","issn_l":null,"issn":null,"is_oa":false,"is_in_doaj":false,"is_core":false,"listed_in":[],"host_organization":"https://openalex.org/I1299303238","host_organization_name":"National Institutes of Health","host_organization_lineage":["https://openalex.org/I1299303238"],"host_organization_lineage_names":[],"type":"repository"},"license":null,"license_id":null,"version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":"Proceedings of the National Academy of Sciences of the United States of America","raw_type":"Journal Article"}],"best_oa_location":{"id":"pmh:oai:pubmedcentral.nih.gov:2688967","doi":null,"is_oa":true,"landing_page_url":"https://www.ncbi.nlm.nih.gov/pmc/articles/2688967","pdf_url":null,"source":{"id":"https://openalex.org/S2764455111","display_name":"PubMed Central","issn_l":null,"issn":null,"is_oa":true,"is_in_doaj":false,"is_core":false,"listed_in":[],"host_organization":"https://openalex.org/I1299303238","host_organization_name":"National Institutes of Health","host_organization_lineage":["https://openalex.org/I1299303238"],"host_organization_lineage_names":[],"type":"repository"},"license":null,"license_id":null,"version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":"Proc Natl Acad Sci U S A","raw_type":"Text"},"sustainable_development_goals":[{"score":0.46810001134872437,"display_name":"Good health and well-being","id":"https://metadata.un.org/sdg/3"}],"study_designs":[],"awards":[],"funders":[{"id":"https://openalex.org/F4320332815","display_name":"Advanced Research Projects Agency","ror":"https://ror.org/02caytj08"}],"has_content":{"pdf":false,"grobid_xml":false},"content_urls":null,"referenced_works_count":29,"referenced_works":["https://openalex.org/W1539294332","https://openalex.org/W1852389345","https://openalex.org/W1947752090","https://openalex.org/W1967195968","https://openalex.org/W1972843837","https://openalex.org/W1979158913","https://openalex.org/W1984412128","https://openalex.org/W1984670732","https://openalex.org/W2015635947","https://openalex.org/W2016452066","https://openalex.org/W2026763067","https://openalex.org/W2034314076","https://openalex.org/W2041108610","https://openalex.org/W2041646166","https://openalex.org/W2043259229","https://openalex.org/W2044253490","https://openalex.org/W2057349575","https://openalex.org/W2062083782","https://openalex.org/W2063490058","https://openalex.org/W2077845498","https://openalex.org/W2100397924","https://openalex.org/W2109541209","https://openalex.org/W2124935744","https://openalex.org/W2124941338","https://openalex.org/W2126430609","https://openalex.org/W2146961853","https://openalex.org/W2164807254","https://openalex.org/W2583369066","https://openalex.org/W4313376321"],"related_works":["https://openalex.org/W2899014127","https://openalex.org/W2146961853","https://openalex.org/W2124448263","https://openalex.org/W1974587421","https://openalex.org/W4319915658","https://openalex.org/W1852389345","https://openalex.org/W2030381656","https://openalex.org/W2071292211","https://openalex.org/W3029714937","https://openalex.org/W7116048895"],"abstract_inverted_index":{"It":[0],"is":[1,82],"generally":[2],"assumed":[3],"that":[4,36,63,99,155],"amino":[5,38,128,156],"acid":[6,39,129,157],"mutations":[7,130,158],"in":[8,67,138,178],"the":[9,45,50,57,101,124,145,165,179,182,193,196],"surface":[10],"protein,":[11],"hemagglutinin":[12],"(HA),":[13],"of":[14,47,49,103,119,164,167,181,198],"influenza":[15,33,168,203],"viruses":[16,19,34,170,204],"allow":[17],"these":[18],"to":[20,41,88,122,131,135,159,175],"circumvent":[21],"neutralization":[22,48,68,94,107,180],"by":[23,53,90],"antibodies":[24,54,91,104],"induced":[25],"during":[26],"infection.":[27],"However,":[28],"empirical":[29],"data":[30,187],"on":[31,173],"circulating":[32],"show":[35],"certain":[37],"changes":[40],"HA":[42,71,89,132,166],"actually":[43],"increase":[44,66,110,137,177],"efficiency":[46,69],"mutated":[51,183],"virus":[52],"raised":[55],"against":[56,202],"parent":[58],"virus.":[59],"Here,":[60],"we":[61,153],"suggest":[62],"this":[64,189],"surprising":[65],"after":[70],"mutation":[72,98],"could":[73,109,133,171],"reflect":[74],"steric":[75,84],"interference":[76],"between":[77],"antibodies.":[78],"Specifically,":[79],"if":[80],"there":[81],"a":[83,97,116],"competition":[85],"for":[86,195],"binding":[87,102],"with":[92,105,148],"different":[93],"efficiencies,":[95],"then":[96],"reduces":[100],"low":[106],"efficiencies":[108],"overall":[111],"viral":[112,139],"neutralization.":[113,140],"We":[114,185],"use":[115],"mathematical":[117],"model":[118],"virus-antibody":[120],"interaction":[121],"elucidate":[123],"conditions":[125],"under":[126],"which":[127],"lead":[134,172],"an":[136,176],"Using":[141],"insights":[142],"gained":[143],"from":[144],"model,":[146],"together":[147],"genetic":[149],"and":[150,162,191,205],"structural":[151],"data,":[152],"predict":[154],"epitopes":[160],"C":[161],"E":[163],"A/H3N2":[169],"average":[174],"viruses.":[184],"present":[186],"supporting":[188],"prediction":[190],"discuss":[192],"implications":[194],"design":[197],"more":[199],"effective":[200],"vaccines":[201],"other":[206],"pathogens.":[207]},"counts_by_year":[{"year":2026,"cited_by_count":4},{"year":2025,"cited_by_count":5},{"year":2024,"cited_by_count":3},{"year":2023,"cited_by_count":5},{"year":2022,"cited_by_count":2},{"year":2021,"cited_by_count":7},{"year":2020,"cited_by_count":13},{"year":2019,"cited_by_count":4},{"year":2018,"cited_by_count":8},{"year":2017,"cited_by_count":9},{"year":2016,"cited_by_count":5},{"year":2015,"cited_by_count":5},{"year":2014,"cited_by_count":7},{"year":2013,"cited_by_count":10},{"year":2012,"cited_by_count":8}],"updated_date":"2026-11-05T12:25:35.769452","created_date":"2016-06-24T00:00:00"}