{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T21:56:54Z","timestamp":1790114214423,"version":"4.0.1"},"reference-count":46,"publisher":"Elsevier BV","issue":"1","license":[{"start":{"date-parts":[[2025,1,1]],"date-time":"2025-01-01T00:00:00Z","timestamp":1735689600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2025,1,1]],"date-time":"2025-01-01T00:00:00Z","timestamp":1735689600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2026,1,1]],"date-time":"2026-01-01T00:00:00Z","timestamp":1767225600000},"content-version":"vor","delay-in-days":365,"URL":"http:\/\/www.elsevier.com\/open-access\/userlicense\/1.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2021YFD1800404"],"award-info":[{"award-number":["2021YFD1800404"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2021YFD1800800"],"award-info":[{"award-number":["2021YFD1800800"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100013088","name":"Qinglan Project of Jiangsu Province of China","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100013088","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31973004"],"award-info":[{"award-number":["31973004"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32273009"],"award-info":[{"award-number":["32273009"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Microbes and Infection"],"published-print":{"date-parts":[[2025,1]]},"DOI":"10.1016\/j.micinf.2023.105209","type":"journal-article","created":{"date-parts":[[2023,8,17]],"date-time":"2023-08-17T03:22:44Z","timestamp":1692242564000},"page":"105209","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":2,"title":["The dual M protein systems have diverse biological characteristics, but both contribute to M18-type Group A Streptococcus pathogenicity"],"prefix":"10.1016","volume":"27","author":[{"given":"Xiaorui","family":"Zhou","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haoshuai","family":"Song","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fei","family":"Pan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chen","family":"Yuan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lu","family":"Jia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bing","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongjie","family":"Fan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhe","family":"Ma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.micinf.2023.105209_bib1","series-title":"Streptococcus pyogenes: Basic Biology to Clinical Manifestations","year":"2016"},{"key":"10.1016\/j.micinf.2023.105209_bib2","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1128\/CMR.00101-13","article-title":"Disease Manifestations and Pathogenic Mechanisms of Group A Streptococcus","volume":"27","author":"Walker","year":"2014","journal-title":"Clinical Microbiology Reviews"},{"key":"10.1016\/j.micinf.2023.105209_bib3","first-page":"3","article-title":"Catch Me if You Can: Streptococcus pyogenes Complement Evasion Strategies","volume":"11","author":"Laabei","year":"2019","journal-title":"J\u00a0Innate Immun"},{"key":"10.1016\/j.micinf.2023.105209_bib4","doi-asserted-by":"crossref","first-page":"2303","DOI":"10.1046\/j.1432-1033.2003.03600.x","article-title":"Interactions between M proteins of Streptococcus pyogenes and glycosaminoglycans promote bacterial adhesion to host cells","volume":"270","author":"Frick","year":"2003","journal-title":"Eur J Biochem"},{"key":"10.1016\/j.micinf.2023.105209_bib5","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1093\/infdis\/jiu260","article-title":"A\u00a0systematic and functional classification of Streptococcus pyogenes that serves as a new tool for molecular typing and vaccine development","volume":"210","author":"Sanderson-Smith","year":"2014","journal-title":"J\u00a0Infect Dis"},{"key":"10.1016\/j.micinf.2023.105209_bib6","doi-asserted-by":"crossref","first-page":"1429","DOI":"10.1093\/infdis\/jiz615","article-title":"Longitudinal Analysis of Group A Streptococcus emm Types and emm Clusters in a High-Prevalence Setting: Relationship between Past and Future Infections","volume":"221","author":"Campbell","year":"2020","journal-title":"J\u00a0Infect Dis"},{"key":"10.1016\/j.micinf.2023.105209_bib7","doi-asserted-by":"crossref","first-page":"1172","DOI":"10.1016\/j.cca.2010.04.032","article-title":"Streptococcal M proteins and their role as virulence determinants","volume":"411","author":"Oehmcke","year":"2010","journal-title":"Clin Chim Acta"},{"key":"10.1016\/j.micinf.2023.105209_bib8","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.tim.2010.02.007","article-title":"The streptococcal M protein: a highly versatile molecule","volume":"18","author":"Smeesters","year":"2010","journal-title":"Trend Microbiol"},{"key":"10.1016\/j.micinf.2023.105209_bib9","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1084\/jem.113.2.451","article-title":"The occurrence of two M antigens in certain group A streptococci related to type 14","volume":"113","author":"Wiley","year":"1961","journal-title":"J\u00a0Exp Med"},{"key":"10.1016\/j.micinf.2023.105209_bib10","doi-asserted-by":"crossref","first-page":"1185","DOI":"10.1111\/j.1365-2958.1992.tb01557.x","article-title":"Many group A streptococcal strains express two different immunoglobulin-binding proteins, encoded by closely linked genes: characterization of the proteins expressed by four strains of different M-type","volume":"6","author":"Stenberg","year":"1992","journal-title":"Mol Microbiol"},{"key":"10.1016\/j.micinf.2023.105209_bib11","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1128\/iai.60.1.124-135.1992","article-title":"Nucleotide sequences of two adjacent M or M-like protein genes of group A streptococci: different RNA transcript levels and identification of a unique immunoglobulin A-binding protein","volume":"60","author":"Bessen","year":"1992","journal-title":"Infect Immun"},{"key":"10.1016\/j.micinf.2023.105209_bib12","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1093\/femsre\/fux057","article-title":"Group A streptococcal M-like proteins: From pathogenesis to vaccine potential","volume":"42","author":"Frost","year":"2018","journal-title":"FEMS Microbiol Rev"},{"key":"10.1016\/j.micinf.2023.105209_bib13","doi-asserted-by":"crossref","first-page":"2943","DOI":"10.1128\/IAI.69.5.2943-2949.2001","article-title":"Spa Contributes to the Virulence of Type 18 Group A Streptococci","volume":"69","author":"McLellan","year":"2001","journal-title":"Infect Immun"},{"key":"10.1016\/j.micinf.2023.105209_bib14","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1016\/j.vetmic.2009.10.011","article-title":"Detection of Chlamydophila caviae and Streptococcus equi subsp. zooepidemicus in horses with signs of rhinitis and conjunctivitis","volume":"142","author":"Gaede","year":"2010","journal-title":"Vet Microbiol"},{"key":"10.1016\/j.micinf.2023.105209_bib15","first-page":"142","volume":"188","author":"Priestnall","year":"2011","journal-title":"Streptococcus zooepidemicus: an emerging canine pathogen Vet J"},{"key":"10.1016\/j.micinf.2023.105209_bib16","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.micpath.2013.02.006","article-title":"Identification of genes transcribed by Streptococcus equi ssp. zooepidemicus in infected porcine lung","volume":"59","author":"Yi","year":"2013","journal-title":"Microb Pathog"},{"key":"10.1016\/j.micinf.2023.105209_bib17","doi-asserted-by":"crossref","DOI":"10.1128\/mBio.02500-19","article-title":"A\u00a0Conserved Streptococcal Virulence Regulator Controls the Expression of a Distinct Class of M-Like Proteins","author":"D\u2019Gama","year":"2019","journal-title":"mBio"},{"key":"10.1016\/j.micinf.2023.105209_bib18","doi-asserted-by":"crossref","first-page":"1181","DOI":"10.1128\/CVI.00069-13","article-title":"Characterization and protective immunogenicity of the SzM protein of Streptococcus zooepidemicus NC78 from a clonal outbreak of equine respiratory disease","volume":"20","author":"Velineni","year":"2013","journal-title":"Clin Vaccine Immunol"},{"key":"10.1016\/j.micinf.2023.105209_bib19","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1003842","article-title":"RocA Truncation Underpins Hyper-Encapsulation, Carriage Longevity and Transmissibility of Serotype M18 Group A Streptococci","volume":"9","author":"Lynskey","year":"2013","journal-title":"PLoS Pathogens"},{"key":"10.1016\/j.micinf.2023.105209_bib20","doi-asserted-by":"crossref","first-page":"1805","DOI":"10.1128\/JCM.40.5.1805-1810.2002","article-title":"Molecular analysis of Group A Streptococcus type emm18 isolates temporally associated with acute rheumatic fever outbreaks in Salt Lake City, Utah","volume":"40","author":"Smoot","year":"2002","journal-title":"J\u00a0Clin Microbiol"},{"key":"10.1016\/j.micinf.2023.105209_bib21","doi-asserted-by":"crossref","first-page":"4011","DOI":"10.1128\/IAI.01921-14","article-title":"Role for streptococcal collagen-like protein 1 in M1T1 group A Streptococcus resistance to neutrophil extracellular traps","volume":"82","author":"D\u00f6hrmann","year":"2014","journal-title":"Infect Immun"},{"key":"10.1016\/j.micinf.2023.105209_bib22","doi-asserted-by":"crossref","first-page":"4244","DOI":"10.1074\/jbc.M116.749275","article-title":"Streptococcus pyogenes Endopeptidase O Contributes to Evasion from Complement-mediated Bacteriolysis via Binding to Human Complement Factor C1q","volume":"292","author":"Honda-Ogawa","year":"2017","journal-title":"J\u00a0Biol Chem"},{"key":"10.1016\/j.micinf.2023.105209_bib23","first-page":"88","article-title":"Prominent Binding of Human and Equine Fibrinogen to Streptococcus equi subsp. zooepidemicus Is Mediated by Specific SzM Types and Is a Distinct Phenotype of Zoonotic Isolates","author":"Bergmann","year":"2019","journal-title":"Infect Immun"},{"key":"10.1016\/j.micinf.2023.105209_bib24","doi-asserted-by":"crossref","first-page":"82","DOI":"10.3389\/fcimb.2015.00082","article-title":"Identification of Novel Laminin- and Fibronectin-binding Proteins by Far-Western Blot: Capturing the Adhesins of Streptococcus suis Type 2","volume":"5","author":"Li","year":"2015","journal-title":"Front Cell Infect Microbiol"},{"issue":"6","key":"10.1016\/j.micinf.2023.105209_bib25","doi-asserted-by":"crossref","DOI":"10.1128\/jb.00448-22","article-title":"CsbD, a novel group B streptococcal stress response factor that contributes to bacterial resistance against environmental bile salts","volume":"205","author":"Jia","year":"2023","journal-title":"J\u00a0Bacteriol"},{"key":"10.1016\/j.micinf.2023.105209_bib26","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1016\/j.meegid.2014.10.011","article-title":"Molecular epidemiology and genomics of group A Streptococcus","volume":"33","author":"Bessen","year":"2015","journal-title":"Infect Gene Evol"},{"key":"10.1016\/j.micinf.2023.105209_bib27","series-title":"Evolution in Health and Disease (Chapter 14. The Population Structure of Pathogenic Bacteria)","author":"Daniel","year":"2008"},{"key":"10.1016\/j.micinf.2023.105209_bib28","doi-asserted-by":"crossref","first-page":"1925","DOI":"10.1093\/bioinformatics\/btz848","article-title":"GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database","volume":"36","author":"Chaumeil","year":"2019","journal-title":"Bioinformatics"},{"key":"10.1016\/j.micinf.2023.105209_bib29","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1128\/CMR.15.4.613-630.2002","article-title":"What Happened to the Streptococci: Overview of Taxonomic and Nomenclature Changes","volume":"15","author":"Facklam","year":"2002","journal-title":"Clin Microbiol Rev"},{"key":"10.1016\/j.micinf.2023.105209_bib30","doi-asserted-by":"crossref","first-page":"10078","DOI":"10.1073\/pnas.152298499","article-title":"Genome sequence of a serotype M3 strain of group A Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence","volume":"99","author":"Beres","year":"2002","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.micinf.2023.105209_bib31","doi-asserted-by":"crossref","first-page":"5583","DOI":"10.1128\/JB.05700-11","article-title":"Complete genome sequence of Streptococcus equi subsp. zooepidemicus strain ATCC 35246","volume":"193","author":"Ma","year":"2011","journal-title":"J\u00a0Bacteriol"},{"key":"10.1016\/j.micinf.2023.105209_bib32","doi-asserted-by":"crossref","first-page":"1514","DOI":"10.1128\/JB.01132-06","article-title":"Proteomic Analysis and Identification of Streptococcus pyogenes Surface-Associated Proteins","volume":"189","author":"Severin","year":"2007","journal-title":"J\u00a0Bacteriol"},{"key":"10.1016\/j.micinf.2023.105209_bib33","doi-asserted-by":"crossref","first-page":"539","DOI":"10.2183\/pjab.91.539","article-title":"Molecular and genomic characterization of pathogenic traits of group A Streptococcus pyogenes","volume":"91","author":"Hamada","year":"2015","journal-title":"Proc Jpn Acad Ser B Phys Biol Sci"},{"key":"10.1016\/j.micinf.2023.105209_bib34","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1086\/653116","article-title":"Getting under the skin: the immunopathogenesis of Streptococcus pyogenes deep tissue infections","volume":"51","author":"Johansson","year":"2010","journal-title":"Clin Infect Dis"},{"key":"10.1016\/j.micinf.2023.105209_bib35","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1086\/515241","article-title":"Role of emm and mrp Genes in the Virulence of Group A Streptococcal Isolate 64\/14 in a Mouse Model of Skin Infection","volume":"177","author":"Boyle","year":"1998","journal-title":"J\u00a0Infect Dis"},{"key":"10.1016\/j.micinf.2023.105209_bib36","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1128\/iai.37.2.805-810.1982","article-title":"Fibronectin-mediated binding of group A streptococci to human polymorphonuclear leukocytes","volume":"37","author":"Simpson","year":"1982","journal-title":"Infect Immun"},{"key":"10.1016\/j.micinf.2023.105209_bib37","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1006\/mpat.2001.0467","article-title":"Genetic dissection of the Streptococcus pyogenes M1 protein: regions involved in fibronectin binding and intracellular invasion","volume":"31","author":"Cue","year":"2001","journal-title":"Microb Pathog"},{"key":"10.1016\/j.micinf.2023.105209_bib38","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1111\/j.1365-2958.2005.04527.x","article-title":"Human fibrinogen bound to Streptococcus pyogenes M protein inhibits complement deposition via the classical pathway","volume":"56","author":"Carlsson","year":"2005","journal-title":"Mol Microbiol"},{"key":"10.1016\/j.micinf.2023.105209_bib39","doi-asserted-by":"crossref","first-page":"105636","DOI":"10.1016\/j.micpath.2022.105636","article-title":"Contribution of Streptococcus pyogenes M87 protein to innate immune resistance and virulence","volume":"169","author":"Hirose","year":"2022","journal-title":"Microb Pathog"},{"key":"10.1016\/j.micinf.2023.105209_bib40","doi-asserted-by":"crossref","first-page":"1425","DOI":"10.1038\/s41564-017-0005-6","article-title":"Group A streptococcal M protein activates the NLRP3 inflammasome","volume":"2","author":"Valderrama","year":"2017","journal-title":"Nature Microbiol"},{"key":"10.1016\/j.micinf.2023.105209_bib41","doi-asserted-by":"crossref","first-page":"4668","DOI":"10.1073\/pnas.062526099","article-title":"Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks","volume":"99","author":"Smoot","year":"2002","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.micinf.2023.105209_bib42","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.1172\/JCI5118","article-title":"New protective antigen of group A streptococci","volume":"103","author":"Dale","year":"1999","journal-title":"J\u00a0Clin Invest"},{"key":"10.1016\/j.micinf.2023.105209_bib43","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1007\/s10096-009-0819-0","article-title":"Streptococcal protective antigens (Spa): a new family of type-specific proteins of group A streptococci","volume":"29","author":"Ahmed","year":"2010","journal-title":"Eur J Clin Microbiol Infect Dis"},{"key":"10.1016\/j.micinf.2023.105209_bib44","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1008169","article-title":"Structural determination of Streptococcus pyogenes M1 protein interactions with human immunoglobulin G using integrative structural biology","volume":"17","author":"Khakzad","year":"2021","journal-title":"PLoS Comput Biol"},{"key":"10.1016\/j.micinf.2023.105209_bib45","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1111\/j.1574-695X.1993.tb00392.x","article-title":"Multiple binding of type 3 streptococcal M protein to human fibrinogen, albumin and fibronectin","volume":"7","author":"Schmidt","year":"1993","journal-title":"FEMS Immunol Med Microbiol"},{"key":"10.1016\/j.micinf.2023.105209_bib46","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1016\/S0966-842X(03)00098-2","article-title":"Virulence factor regulation and regulatory networks in Streptococcus pyogenes and their impact on pathogen-host interactions","volume":"11","author":"Kreikemeyer","year":"2003","journal-title":"Trends Microbiol"}],"container-title":["Microbes and Infection"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1286457923001120?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1286457923001120?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2026,1,1]],"date-time":"2026-01-01T02:06:52Z","timestamp":1767233212000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S1286457923001120"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1]]},"references-count":46,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2025,1]]}},"alternative-id":["S1286457923001120"],"URL":"https:\/\/doi.org\/10.1016\/j.micinf.2023.105209","relation":{},"ISSN":["1286-4579"],"issn-type":[{"value":"1286-4579","type":"print"}],"subject":[],"published":{"date-parts":[[2025,1]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"The dual M protein systems have diverse biological characteristics, but both contribute to M18-type Group A Streptococcus pathogenicity","name":"articletitle","label":"Article Title"},{"value":"Microbes and Infection","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.micinf.2023.105209","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2023 Institut Pasteur. Published by Elsevier Masson SAS.","name":"copyright","label":"Copyright"}],"article-number":"105209"}}