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The role of glycosaminoglycans, especially heparan sulfate, is critical in facilitating pathogen\u2013host interactions, presenting a strategic target for therapeutic intervention. In this study, we assembled a glycan library comprising heparin, its oligosaccharide derivatives, and a variety of marine-derived sulfated glycans to screen the potential inhibitors for the pathogen\u2013host interactions. By using Surface Plasmon Resonance spectroscopy, we evaluated the library\u2019s efficacy in inhibiting the interaction between M. pneumoniae adhesion proteins and heparin. Our findings offer a promising avenue for developing novel therapeutic strategies against M. pneumoniae infections.<\/jats:p>","DOI":"10.3390\/md22050232","type":"journal-article","created":{"date-parts":[[2024,5,20]],"date-time":"2024-05-20T06:31:58Z","timestamp":1716186718000},"page":"232","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Marine-Derived Sulfated Glycans Inhibit the Interaction of Heparin with Adhesion Proteins of Mycoplasma pneumoniae"],"prefix":"10.3390","volume":"22","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9713-7032","authenticated-orcid":false,"given":"Jiyuan","family":"Yang","sequence":"first","affiliation":[{"name":"The Key Laboratory of Molecular Microbiology and Technology, Ministry of Education, College of Life Sciences, Nankai University, Tianjin 300071, China"},{"name":"Department of Chemistry and Chemical Biology, Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0151-2046","authenticated-orcid":false,"given":"Yuefan","family":"Song","sequence":"additional","affiliation":[{"name":"Department of Chemistry and Chemical Biology, Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9699-9901","authenticated-orcid":false,"given":"Ke","family":"Xia","sequence":"additional","affiliation":[{"name":"Department of Chemistry and Chemical Biology, Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5015-8880","authenticated-orcid":false,"given":"Vitor H.","family":"Pomin","sequence":"additional","affiliation":[{"name":"Department of BioMolecular Sciences, Research Institute of Pharmaceutical Sciences, The University of Mississippi, Oxford, MS 38677, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunyu","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Chemistry and Chemical Biology, Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mingqiang","family":"Qiao","sequence":"additional","affiliation":[{"name":"The Key Laboratory of Molecular Microbiology and Technology, Ministry of Education, College of Life Sciences, Nankai University, Tianjin 300071, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2219-5833","authenticated-orcid":false,"given":"Robert J.","family":"Linhardt","sequence":"additional","affiliation":[{"name":"Department of Chemistry and Chemical Biology, Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"},{"name":"Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonathan S.","family":"Dordick","sequence":"additional","affiliation":[{"name":"Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2803-3704","authenticated-orcid":false,"given":"Fuming","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,5,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Parrott, G.L., Kinjo, T., and Fujita, J. (2016). A Compendium for Mycoplasma Pneumoniae. Front. Microbiol., 7.","DOI":"10.3389\/fmicb.2016.00513"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1128\/CMR.00114-16","article-title":"Mycoplasma Pneumoniae from the Respiratory Tract and Beyond","volume":"30","author":"Waites","year":"2017","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_3","first-page":"000817","article-title":"Immune Thrombocytopenia Associated with Mycoplasma Pneumoniae Infection","volume":"5","author":"Gouveia","year":"2018","journal-title":"Eur. J. Case Rep. Intern. Med."},{"key":"ref_4","first-page":"15666","article-title":"Effects of Bacterial and Viral Co-Infections of Mycoplasma Pneumoniae Pneumonia in Children: Analysis Report from Beijing Children\u2019s Hospital between 2010 and 2014","volume":"8","author":"Song","year":"2015","journal-title":"Int. J. Clin. Exp. Med."},{"key":"ref_5","first-page":"2100746","article-title":"Mycoplasma Pneumoniae Detections before and during the COVID-19 Pandemic: Results of a Global Survey, 2017 to 2021","volume":"27","author":"Beeton","year":"2022","journal-title":"Eurosurveillance"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1508","DOI":"10.1080\/22221751.2022.2078228","article-title":"Mycoplasma pneumoniae Triggers Pneumonia Epidemic in Autumn and Winter in Beijing: A Multicentre, Population-Based Epidemiological Study between 2015 and 2020","volume":"11","author":"Wang","year":"2022","journal-title":"Emerg. Microbes Infect."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1111\/crj.13584","article-title":"Thromboembolic Complications of Mycoplasma pneumoniae Pneumonia in Children","volume":"17","author":"Chen","year":"2023","journal-title":"Clin. Respir. J."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Shin, S., Koo, S., Yang, Y.-J., and Lim, H.-J. (2023). Characteristics of the Mycoplasma pneumoniae Epidemic from 2019 to 2020 in Korea: Macrolide Resistance and Co-Infection Trends. Antibiotics, 12.","DOI":"10.3390\/antibiotics12111623"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Jiang, Z., Li, S., Zhu, C., Zhou, R., and Leung, P.H.M. (2021). Mycoplasma pneumoniae Infections: Pathogenesis and Vaccine Development. Pathogens, 10.","DOI":"10.3390\/pathogens10020119"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e00392-20","DOI":"10.1128\/IAI.00392-20","article-title":"Distinct Mycoplasma pneumoniae Interactions with Sulfated and Sialylated Receptors","volume":"88","author":"Williams","year":"2020","journal-title":"Infect Immun."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1111\/mmi.13997","article-title":"Sialylated Receptor Setting Influences Mycoplasma pneumoniae Attachment and Gliding Motility","volume":"109","author":"Williams","year":"2018","journal-title":"Mol. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1128\/JB.188.2.569-575.2006","article-title":"Synthesis, Stability, and Function of Cytadhesin P1 and Accessory Protein B\/C Complex of Mycoplasma pneumoniae","volume":"188","author":"Waldo","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1128\/JB.187.2.747-751.2005","article-title":"Identification and Complementation of a Mutation Associated with Loss of Mycoplasma pneumoniae Virulence-Specific Proteins B and C","volume":"187","author":"Waldo","year":"2005","journal-title":"J. Bacteriol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"3061","DOI":"10.1128\/JB.184.11.3061-3068.2002","article-title":"Characterization of a Mycoplasma pneumoniae Hmw3 Mutant: Implications for Attachment Organelle Assembly","volume":"184","author":"Willby","year":"2002","journal-title":"J. Bacteriol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"6384","DOI":"10.1038\/s41598-020-63136-y","article-title":"Cell Surface Processing of the P1 Adhesin of Mycoplasma pneumoniae Identifies Novel Domains That Bind Host Molecules","volume":"10","author":"Widjaja","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.micres.2018.09.006","article-title":"Organization of Multi-Binding to Host Proteins: The Glyceraldehyde-3-Phosphate Dehydrogenase (GAPDH) of Mycoplasma pneumoniae","volume":"218","author":"Grimmer","year":"2019","journal-title":"Microbiol. Res."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Miyata, M., and Hamaguchi, T. (2016). Integrated Information and Prospects for Gliding Mechanism of the Pathogenic Bacterium Mycoplasma pneumoniae. Front. Microbiol., 7.","DOI":"10.3389\/fmicb.2016.00960"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1726","DOI":"10.1128\/JB.01228-10","article-title":"Domain Analysis of Protein P30 in Mycoplasma pneumoniae Cytadherence and Gliding Motility","volume":"193","author":"Chang","year":"2011","journal-title":"J. Bacteriol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"De Pasquale, V., Quiccione, M.S., Tafuri, S., Avallone, L., and Pavone, L.M. (2021). Heparan Sulfate Proteoglycans in Viral Infection and Treatment: A Special Focus on SARS-CoV-2. IJMS, 22.","DOI":"10.3390\/ijms22126574"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"C605","DOI":"10.1152\/ajpcell.00028.2022","article-title":"Is Heparan Sulfate a Target for Inhibition of RNA Virus Infection?","volume":"322","author":"Ling","year":"2022","journal-title":"Am. J. Physiol.-Cell Physiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1128\/IAI.74.1.481-487.2006","article-title":"Two Domains within the Mycoplasma Hyopneumoniae Cilium Adhesin Bind Heparin","volume":"74","author":"Jenkins","year":"2006","journal-title":"Infect Immun."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1086\/322009","article-title":"Heparan Sulfate\u2013like Glycosaminoglycan Is a Cellular Receptor for Chlamydia pneumoniae","volume":"184","author":"Wuppermann","year":"2001","journal-title":"J. Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Vasconcelos, A., and Pomin, V. (2017). The Sea as a Rich Source of Structurally Unique Glycosaminoglycans and Mimetics. Microorganisms, 5.","DOI":"10.3390\/microorganisms5030051"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Pav\u00e3o, M.S.G. (2011). Glycans in Diseases and Therapeutics, Springer.","DOI":"10.1007\/978-3-642-16833-8"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1265","DOI":"10.1007\/s10096-018-3243-5","article-title":"Clinical Characteristics of Infections Caused by Mycoplasma pneumoniae P1 Genotypes in Children","volume":"37","author":"Krivec","year":"2018","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1128\/JCM.43.1.321-325.2005","article-title":"Expression and Immunological Characterization of the Carboxy-Terminal Region of the P1 Adhesin Protein of Mycoplasma pneumoniae","volume":"43","author":"Chaudhry","year":"2005","journal-title":"J. Clin. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1016\/j.etap.2017.01.001","article-title":"The Effect of Platycodin D on the Expression of Cytoadherence Proteins P1 and P30 in Mycoplasma pneumoniae Models","volume":"49","author":"Meng","year":"2017","journal-title":"Environ. Toxicol. Pharmacol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1128\/CVI.00283-07","article-title":"Cloning, Expression, and Immunological Characterization of the P30 Protein of Mycoplasma pneumoniae","volume":"15","author":"Varshney","year":"2008","journal-title":"Clin. Vaccine Immunol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.carres.2017.10.008","article-title":"Characterization of Structural Motifs for Interactions between Glycosaminoglycans and Proteins","volume":"452","author":"Yang","year":"2017","journal-title":"Carbohydr. Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"688","DOI":"10.1016\/j.carbpol.2010.08.040","article-title":"Comparison of Structures and Anticoagulant Activities of Fucosylated Chondroitin Sulfates from Different Sea Cucumbers","volume":"83","author":"Chen","year":"2011","journal-title":"Carbohydr. Polym."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"989","DOI":"10.1016\/j.bbagen.2012.03.002","article-title":"Sequence Determination and Anticoagulant and Antithrombotic Activities of a Novel Sulfated Fucan Isolated from the Sea Cucumber Isostichopus Badionotus","volume":"1820","author":"Chen","year":"2012","journal-title":"Biochim. Et Biophys. Acta (BBA)-Gen. Subj."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Yang, J., Song, Y., Jin, W., Xia, K., Burnett, G.C., Qiao, W., Bates, J.T., Pomin, V.H., Wang, C., and Qiao, M. (2024). Sulfated Glycans Inhibit the Interaction of MERS-CoV Receptor Binding Domain with Heparin. Viruses, 16.","DOI":"10.3390\/v16020237"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"738","DOI":"10.1016\/j.ijbiomac.2019.03.127","article-title":"Comparison of Hydrothermal Depolymerization and Oligosaccharide Profile of Fucoidan and Fucosylated Chondroitin Sulfate from Holothuria Floridana","volume":"132","author":"Shi","year":"2019","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1093\/glycob\/cwi021","article-title":"Selective Cleavage and Anticoagulant Activity of a Sulfated Fucan: Stereospecific Removal of a 2-Sulfate Ester from the Polysaccharide by Mild Acid Hydrolysis, Preparation of Oligosaccharides, and Heparin Cofactor II\u2013Dependent Anticoagulant Activity","volume":"15","author":"Pomin","year":"2005","journal-title":"Glycobiology"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Dwivedi, R., Samanta, P., Sharma, P., Zhang, F., Mishra, S.K., Kucheryavy, P., Kim, S.B., Aderibigbe, A.O., Linhardt, R.J., and Tandon, R. (2021). Structural and Kinetic Analyses of Holothurian Sulfated Glycans Suggest Potential Treatment for SARS-CoV-2 Infection. J. Biol. Chem., 297.","DOI":"10.1016\/j.jbc.2021.101207"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"122156","DOI":"10.1016\/j.carbpol.2024.122156","article-title":"Seaweed-Derived Fucoidans and Rhamnan Sulfates Serve as Potent Anti-SARS-CoV-2 Agents with Potential for Prophylaxis","volume":"337","author":"Song","year":"2024","journal-title":"Carbohydr. Polym."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Dwivedi, R., Sharma, P., Farrag, M., Kim, S.B., Fassero, L.A., Tandon, R., and Pomin, V.H. (2022). Inhibition of SARS-CoV-2 Wild-Type (Wuhan-Hu-1) and Delta (B.1.617.2) Strains by Marine Sulfated Glycans. 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