{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,20]],"date-time":"2026-10-20T23:48:54Z","timestamp":1792540134751,"version":"4.5.0"},"reference-count":76,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,11,28]],"date-time":"2022-11-28T00:00:00Z","timestamp":1669593600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>Pathogenic species of <jats:italic>Leptospira<\/jats:italic> are etiologic agents of leptospirosis, an emerging zoonotic disease of worldwide extent and endemic in tropical regions. The growing number of identified leptospiral species sheds light to their genetic diversity and unique virulence mechanisms, many of them still remain unknown. Toxins and adhesins are important virulence factors in several pathogens, constituting promising antigens for the development of vaccines with cross-protection and long-lasting effect against leptospirosis. For this aim, we used the shotgun phage display technique to unravel new proteins with adhesive properties. A shotgun library was constructed using fragmented genomic DNA from <jats:italic>Leptospira interrogans<\/jats:italic> serovar Copenhageni strain Fiocruz L1-130 and pG8SAET phagemid vector. Selection of phages bearing new possible cell-binding antigens was performed against VERO cells, using BRASIL biopanning methodology. Analysis of selected clones revealed the hypothetical protein LIC10778, a potentially exposed virulence factor that belongs to the virulence-modifying (VM) protein family (PF07598), composed of 13 members in the leptospiral strain Fiocruz L1-130. Prediction of LIC10778 tertiary structure indicates that the protein contains a cellular-binding domain (N-terminal portion) and an unknown domain of no assigned activity (C-terminal portion). The predicted N-terminal domain shared structural similarities with the cell-binding and internalization domain of toxins like Ricin and Abrin, as well as to the Community-Acquired Respiratory Distress Syndrome (CARDS) toxin in <jats:italic>Mycoplasma pneumoniae<\/jats:italic>. Interestingly, recombinant portions of the N-terminal region of LIC10778 protein showed binding to laminin, collagens I and IV, vitronectin, and plasma and cell fibronectins using overlay blotting technique, especially regarding the binding site identified by phage display. These data validate our preliminary phage display biopanning and support the predicted three-dimensional models of LIC10778 protein and other members of PF07598 protein family, confirming the identification of the N-terminal cell-binding domains that are similar to ricin-like toxins. Moreover, fluorescent fused proteins also confirmed that N-terminal region of LIC10778 is capable of binding to VERO and A549 cell lines, further highlighting its virulence role during host-pathogen interaction in leptospirosis probably mediated by its C-terminal domain. Indeed, recent results in the literature confirmed this assumption by demonstrating the cytotoxicity of a closely related PF07598 member.<\/jats:p>","DOI":"10.3389\/fmicb.2022.1051698","type":"journal-article","created":{"date-parts":[[2022,11,28]],"date-time":"2022-11-28T05:01:45Z","timestamp":1669611705000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":6,"title":["Characterization of a virulence-modifying protein of Leptospira interrogans identified by shotgun phage display"],"prefix":"10.3389","volume":"13","author":[{"given":"Fabiana","family":"Lauretti-Ferreira","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andr\u00e9 Azevedo Reis","family":"Teixeira","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ricardo Jos\u00e9","family":"Giordano","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Josefa Bezerra","family":"da Silva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patricia Antonia Estima","family":"Abreu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angela Silva","family":"Barbosa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Milena Apetito","family":"Akamatsu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paulo Lee","family":"Ho","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,11,28]]},"reference":[{"key":"ref1","first-page":"251","article-title":"Vaccines Against Leptospirosis","volume-title":"Current Topics in Microbiology and Immunology","author":"Adler","year":"2015"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1126\/science.181.4096.223","article-title":"Principles that govern the folding of protein chains","volume":"1979","author":"Anfinsen","year":"1973","journal-title":"Science"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"262","DOI":"10.1111\/j.1365-2958.2007.05924.x","article-title":"Borrelia burgdorferi adhesins identified using in vivo phage display","volume":"66","author":"Antonara","year":"2007","journal-title":"Mol. Microbiol."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1126\/science.abj8754","article-title":"Accurate prediction of protein structures and interactions using a three-track neural network","volume":"1979","author":"Baek","year":"2021","journal-title":"Science"},{"key":"ref6","volume-title":"Phage Display: A Laboratory Manual","author":"Barbas","year":"2001"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"6356","DOI":"10.1128\/IAI.00460-06","article-title":"A newly identified leptospiral adhesin mediates attachment to laminin","volume":"74","author":"Barbosa","year":"2006","journal-title":"Infect. Immun."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"3207","DOI":"10.1128\/IAI.00279-10","article-title":"Functional characterization of LcpA, a surface-exposed protein of Leptospira spp. that binds the human complement regulator C4BP","volume":"78","author":"Barbosa","year":"2010","journal-title":"Infect. Immun."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"5165","DOI":"10.1073\/pnas.1420308112","article-title":"Structure of CARDS toxin, a unique ADP-ribosylating and vacuolating cytotoxin from mycoplasma pneumoniae","volume":"112","author":"Becker","year":"2015","journal-title":"PNAS"},{"key":"ref10","year":"2022"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1016\/j.toxicon.2005.04.003","article-title":"Molecular engineering of an EGFP\/disintegrin-based integrin marker","volume":"46","author":"Butera","year":"2005","journal-title":"Toxicon"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"11146","DOI":"10.1073\/pnas.95.19.11146","article-title":"Unexpected frameshifts from gene to expressed protein in a phage-displayed peptide library","volume":"95","author":"C\u00e1rcamo","year":"1998","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref13","first-page":"995","article-title":"Leptospiral immunoglobulin-like proteins interact with human complement regulators factor H, FHL-1, FHR-1, and C4BP","volume-title":"J. Infect. Dis.","author":"Castiblanco-Valencia","year":"2012"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1016\/j.vetmic.2011.04.030","article-title":"Identification of candidate host proteins that interact with LipL32, the major outer membrane protein of pathogenic Leptospira, by random phage display peptide library","volume":"153","author":"Chaemchuen","year":"2011","journal-title":"Vet. Microbiol."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"859680","DOI":"10.3389\/fmicb.2022.859680","article-title":"Pathogenic Leptospira evolved a unique gene family comprised of ricin B-like lectin domain-containing Cytotoxins","volume":"13","author":"Chaurasia","year":"","journal-title":"Front. Microbiol."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"926994","DOI":"10.3389\/fcimb.2022.926994","article-title":"Vaccination with Leptospira interrogans PF07598 gene family-encoded virulence modifying proteins protects mice from severe leptospirosis and reduces bacterial load in the liver and kidney","volume":"12","author":"Chaurasia","year":"","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"1065","DOI":"10.1099\/mic.0.000976","article-title":"Cytotoxicity of the 42 kda smase c sphingomyelinase secreted by leptospira interrogans serovar Pomona on vero cells","volume":"166","author":"Chaurasia","year":"2020","journal-title":"Microbiology (United Kingdom)"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"774","DOI":"10.1016\/j.bbrc.2012.09.137","article-title":"Leptospira interrogans shotgun phage display identified LigB as a heparin-binding protein","volume":"427","author":"Ching","year":"2012","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1007\/s12275-011-1405-6","article-title":"Bacteria-based in vivo peptide library screening using biopanning approach","volume":"49","author":"Choi","year":"2011","journal-title":"J. Microbiol."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"e82","DOI":"10.1038\/emi.2014.78","article-title":"Potential impact on kidney infection: a whole-genome analysis of Leptospira santarosai serovar Shermani","volume":"3","author":"Chou","year":"2014","journal-title":"Emerg. Microbes Infect."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"2441","DOI":"10.1128\/IAI.01635-06","article-title":"Physiological osmotic induction of Leptospira interrogans adhesion: LigA and LigB bind extracellular matrix proteins and fibrinogen","volume":"75","author":"Choy","year":"2007","journal-title":"Infect. Immun."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"926","DOI":"10.1046\/j.1365-2958.1999.01654.x","article-title":"Characterization of a candidate Borrella burgdorferi \u03b23-chain integrin ligand identified using a phage display library","volume":"34","author":"Coburn","year":"1999","journal-title":"Mol. Microbiol."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"e0003898","DOI":"10.1371\/journal.pntd.0003898","article-title":"Global morbidity and mortality of leptospirosis: a systematic review","volume":"9","author":"Costa","year":"2015","journal-title":"PLoS Negl. Trop. Dis."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"206","DOI":"10.1016\/j.micpath.2012.01.002","article-title":"Induction of TNF-alfa and CXCL-2 mRNAs in different organs of mice infected with pathogenic Leptospira","volume":"52","author":"Da Silva","year":"2012","journal-title":"Microb. Pathog."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"509","DOI":"10.3389\/fphar.2016.00509","article-title":"Peptides derived from a phage display library inhibit adhesion and protect the host against infection by Paracoccidioides brasiliensis and Paracoccidioides lutzii","volume":"7","author":"De Oliveira","year":"2016","journal-title":"Front. Pharmacol."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"3000605211019665","DOI":"10.1177\/03000605211019665","article-title":"Leptospirosis with pulmonary haemorrhage and multiple organ failure: a case report and literature review","volume":"49","author":"Dong","year":"2021","journal-title":"J. Int. Med. Res."},{"key":"ref27","first-page":"39","article-title":"Nutrition of Leptospira pomona and growth of 13 other serotypes: a serum-free medium employing oleic albumin complex","volume":"26","author":"Ellinghausen","year":"1965","journal-title":"Am. J. Vet. Res."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"1413","DOI":"10.2217\/fmb.10.102","article-title":"Leptospira as an emerging pathogen: a review of its biology, pathogenesis and host immune responses","volume":"5","author":"Evangelista","year":"2010","journal-title":"Future Microbiol."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"e3215","DOI":"10.1371\/journal.pntd.0003215","article-title":"Identification of cell-binding Adhesins of Leptospira interrogans","volume":"8","author":"Evangelista","year":"2014","journal-title":"PLoS Negl. Trop. Dis."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1016\/S1380-2933(98)00018-9","article-title":"Cross-reactive epitope mimics in a fragmented-genome phage display library derived from the rickettsia, Cowdria ruminantium","volume":"4","author":"Fehrsen","year":"1999","journal-title":"Immunotechnology"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"3679","DOI":"10.1128\/IAI.00474-12","article-title":"Ompl1 is an extracellular matrix- and plasminogen-interacting protein of Leptospira spp","volume":"80","author":"Fernandes","year":"2012","journal-title":"Infect. Immun."},{"key":"ref32","author":"Ferreira","year":"2015"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pntd.0004403","article-title":"What makes a bacterial species pathogenic?:comparative genomic analysis of the genus Leptospira","volume":"10","author":"Fouts","year":"2016","journal-title":"PLoS Negl. Trop. Dis."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"1249","DOI":"10.1038\/nm1101-1249","article-title":"Biopanning and rapid analysis of selective interactive ligands","volume":"7","author":"Giordano","year":"2001","journal-title":"Nat. Med."},{"key":"ref35","first-page":"65","article-title":"Leptospirosis in humans","volume-title":"Current Topics in Microbiology and Immunology","author":"Haake","year":"2015"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1007\/978-1-4939-2425-7_24","article-title":"Studying protein-protein interactions via blot overlay\/far western blot","volume":"1278","author":"Hall","year":"2015","journal-title":"Methods Mol. Biol."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"2642","DOI":"10.1128\/IAI.01639-07","article-title":"In LipL32, the major leptospiral lipoprotein, the C terminus is the primary immunogenic domain and mediates interaction with collagen IV and plasma fibronectin","volume":"76","author":"Hauk","year":"2008","journal-title":"Infect. Immun."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"1490","DOI":"10.1002\/pro.5560050805","article-title":"The (QxW)3 domain: a flexible lectin scaffold","volume":"5","author":"Hazes","year":"1996","journal-title":"Protein Sci."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1251\/bpo54","article-title":"Shotgun phage display - selection for bacterial Receptins or other exported proteins","volume":"5","author":"Jacobsson","year":"2003","journal-title":"Biol. Proced. Online"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1146\/annurev.biochem.72.121801.161459","article-title":"Protein disulfide bond formation in prokaryotes","volume":"72","author":"Kadokura","year":"2003","journal-title":"Annu. Rev. Biochem."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"568","DOI":"10.1111\/mmi.12680","article-title":"Functional mapping of community-acquired respiratory distress syndrome (CARDS) toxin of mycoplasma pneumoniae defines regions with ADP-ribosyltransferase, vacuolating and receptor-binding activities","volume":"93","author":"Kannan","year":"2014","journal-title":"Mol. Microbiol."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"580","DOI":"10.1016\/j.chom.2009.05.011","article-title":"Bacterial Adhesins in host-microbe interactions","volume":"5","author":"Kline","year":"2009","journal-title":"Cell Host Microbe"},{"key":"ref44","doi-asserted-by":"publisher","first-page":"736","DOI":"10.1038\/nrmicro2208","article-title":"Leptospira: the dawn of the molecular genetics era for an emerging zoonotic pathogen","volume":"7","author":"Ko","year":"2009","journal-title":"Nat. Rev. Microbiol."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"270","DOI":"10.1038\/s41564-017-0106-2","article-title":"Disulfide bond formation in prokaryotes","volume":"3","author":"Landeta","year":"2018","journal-title":"Nat. Microbiol."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1128\/IAI.70.1.315-322.2002","article-title":"Cytotoxic activities of Leptospira interrogans hemolysin SphH as a pore-forming protein on mammalian cells","volume":"70","author":"Lee","year":"2002","journal-title":"Infect. Immun."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pntd.0002468","article-title":"Pathogenomic inference of virulence-associated genes in Leptospira interrogans","volume":"7","author":"Lehmann","year":"2013","journal-title":"PLoS Negl. Trop. Dis."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"280","DOI":"10.3390\/pathogens3020280","article-title":"Leptospiral pathogenomics","volume":"3","author":"Lehmann","year":"2014","journal-title":"Pathogens"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"296","DOI":"10.1128\/CMR.14.2.296","article-title":"Leptospirosis. Clinical","volume":"14","author":"Levett","year":"2001","journal-title":"Microbiology"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"342","DOI":"10.1016\/j.bbrc.2012.12.095","article-title":"Adhesin activity of Leptospira interrogans lipoprotein identified by in vivo and in vitro shotgun phage display","volume":"431","author":"Lima","year":"2013","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"7747","DOI":"10.1128\/IAI.73.11.7747-7758.2005","article-title":"Development of a ligand-directed approach to study the pathogenesis of invasive aspergillosis","volume":"73","author":"Lionakis","year":"2005","journal-title":"Infect. Immun."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2-\u0394\u0394CT method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref53","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s00408-010-9273-0","article-title":"Clinical and imaging manifestations of hemorrhagic pulmonary leptospirosis: a state-of-the-art review","volume":"189","author":"Marchiori","year":"2011","journal-title":"Lung"},{"key":"ref54","doi-asserted-by":"publisher","first-page":"1601","DOI":"10.1099\/jmm.0.058586-0","article-title":"Use of a high-throughput screen to identify Leptospira mutants unable to colonize the carrier host or cause disease in the acute model of infection","volume":"62","author":"Marcsisin","year":"2013","journal-title":"J. Med. Microbiol."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"2864","DOI":"10.1128\/IAI.01619-06","article-title":"Response of Leptospira interrogans to physiologic osmolarity: relevance in signaling the environment-to-host transition","volume":"75","author":"Matsunaga","year":"2007","journal-title":"Infect. Immun."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1016\/j.tim.2006.01.006","article-title":"Phage display in the study of infectious diseases","volume":"14","author":"Mullen","year":"2006","journal-title":"Trends Microbiol."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1093\/dnares\/dsu029","article-title":"The genome landscape of the African green monkey kidney-derived vero cell line","volume":"21","author":"Naoki","year":"2014","journal-title":"DNA Res."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"2164","DOI":"10.1128\/JB.186.7.2164","article-title":"Comparative genomics of two Leptospira interrogans Serovars reveals novel insights into physiology and pathogenesis","volume":"186","author":"Nascimento","year":"2004","journal-title":"J. Bacteriol."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"294","DOI":"10.1126\/science.aah4043","article-title":"Protein structure determination using metagenome sequence data","volume":"1979","author":"Ovchinnikov","year":"2017","journal-title":"Science"},{"key":"ref60","doi-asserted-by":"publisher","first-page":"906","DOI":"10.3390\/pathogens9110906","article-title":"Characterization of a novel peptide from pathogenic leptospira and its cytotoxic effect","volume":"9","author":"Paratsaphan","year":"2020","journal-title":"Pathogens"},{"key":"ref61","doi-asserted-by":"publisher","first-page":"e45","DOI":"10.1093\/nar\/29.9.e45","article-title":"A new mathematical model for relative quantification in real-time RT\u2013PCR","volume":"29","author":"Pfaffl","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1038\/nrmicro.2017.5","article-title":"Virulence of the zoonotic agent of leptospirosis: still terra incognita?","volume":"15","author":"Picardeau","year":"2017","journal-title":"Nat. Rev. Microbiol."},{"key":"ref63","author":"Plotkin","year":"2018"},{"key":"ref64","doi-asserted-by":"publisher","first-page":"e0009320","DOI":"10.1371\/journal.pntd.0009320","article-title":"Distinct transcriptional profiles of Leptospira borgpetersenii serovar hardjo strains jb197 and hb203 cultured at different temperatures","volume":"15","author":"Putz","year":"2021","journal-title":"PLoS Negl. Trop. Dis."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"1103","DOI":"10.1590\/S0100-879X2004000800001","article-title":"A high-copy T7 Escherichia coli expression vector for the production of recombinant proteins with a minimal N-terminal his-tagged fusion peptide","volume":"37","author":"Ramos","year":"2004","journal-title":"Braz. J. Med. Biol. Res."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pntd.0003712","article-title":"Evaluation of cell binding activities of Leptospira ECM Adhesins","volume":"9","author":"Robbins","year":"2015","journal-title":"PLoS Negl. Trop. Dis."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1016\/j.vetmic.2011.06.005","article-title":"Identification of immunogenic proteins in Treponema phagedenis-like strain V1 from digital dermatitis lesions by phage display","volume":"153","author":"Rosander","year":"2011","journal-title":"Vet. Microbiol."},{"key":"ref68","doi-asserted-by":"publisher","first-page":"624","DOI":"10.1038\/326624a0","article-title":"Structure and evolution of ricin B chain","volume":"326","author":"Rutenber","year":"1987","journal-title":"Nature"},{"key":"ref69","doi-asserted-by":"publisher","first-page":"260","DOI":"10.1002\/prot.340100310","article-title":"Structure of ricin B-chain at 2.5 \u00c5 resolution","volume":"10","author":"Rutenber","year":"1991","journal-title":"Proteins"},{"key":"ref70","doi-asserted-by":"publisher","first-page":"145","DOI":"10.3390\/pathogens10020145","article-title":"Leptospiral infection, pathogenesis and its diagnosis\u2014a review","volume":"10","author":"Samrot","year":"2021","journal-title":"Pathogens"},{"key":"ref71","first-page":"1","volume-title":"History and characterization of the Vero cell line","author":"Sheets","year":"2000"},{"key":"ref72","doi-asserted-by":"publisher","first-page":"119","DOI":"10.3181\/00379727-125-32029","article-title":"Characterization of the Tacaribe Group of Arboviruses. 1. Propagation and plaque assay of Tacaribe virus in a line of African green monkey kidney cells (Vero)","volume":"125","author":"Simizu","year":"1967","journal-title":"Proc. Soc. Exp. Biol. Med."},{"key":"ref73","first-page":"1","article-title":"Annexin A2 mediates mycoplasma pneumoniae community-acquired respiratory distress syndrome toxin binding to eukaryotic cells","author":"Somarajan","year":"2014"},{"key":"ref74","doi-asserted-by":"publisher","first-page":"712","DOI":"10.1038\/nri2852","article-title":"The impact of the extracellular matrix on inflammation","volume":"10","author":"Sorokin","year":"2010","journal-title":"Nat. Rev. Immunol."},{"key":"ref75","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0001188","article-title":"Leptospira interrogans endostatin-like outer membrane proteins bind host fibronectin, laminin and regulators of complement","volume":"2","author":"Stevenson","year":"2007","journal-title":"PLoS One"},{"key":"ref77","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1016\/j.isci.2021.102540","article-title":"A refined genome phage display methodology delineates the human antibody response in patients with Chagas disease","author":"Teixeira","year":"2021","journal-title":"iScience"},{"key":"ref78","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1111\/1574-6968.12349","article-title":"Leptospiral extracellular matrix adhesins as mediators of pathogen-host interactions","volume":"352","author":"Vieira","year":"2014","journal-title":"FEMS Microbiol. Lett."},{"key":"ref79","doi-asserted-by":"publisher","first-page":"3278","DOI":"10.1038\/nprot.2007.459","article-title":"Detecting protein-protein interactions by far western blotting","volume":"2","author":"Wu","year":"2007","journal-title":"Nat. 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