{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T02:14:10Z","timestamp":1790475250371,"version":"4.1.0"},"reference-count":24,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2023,4,25]],"date-time":"2023-04-25T00:00:00Z","timestamp":1682380800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"NIH","award":["S10OD028523"],"award-info":[{"award-number":["S10OD028523"]}]},{"name":"NIH","award":["R21AI156573"],"award-info":[{"award-number":["R21AI156573"]}]},{"name":"NIH","award":["1P20GM130460-01A1-7936"],"award-info":[{"award-number":["1P20GM130460-01A1-7936"]}]},{"name":"NIH","award":["1R03NS110996-01A1"],"award-info":[{"award-number":["1R03NS110996-01A1"]}]},{"name":"NIH","award":["DMR-1933525"],"award-info":[{"award-number":["DMR-1933525"]}]},{"name":"GlycoMIP","award":["S10OD028523"],"award-info":[{"award-number":["S10OD028523"]}]},{"name":"GlycoMIP","award":["R21AI156573"],"award-info":[{"award-number":["R21AI156573"]}]},{"name":"GlycoMIP","award":["1P20GM130460-01A1-7936"],"award-info":[{"award-number":["1P20GM130460-01A1-7936"]}]},{"name":"GlycoMIP","award":["1R03NS110996-01A1"],"award-info":[{"award-number":["1R03NS110996-01A1"]}]},{"name":"GlycoMIP","award":["DMR-1933525"],"award-info":[{"award-number":["DMR-1933525"]}]},{"name":"New York State Biodefense Commercialization Fund","award":["S10OD028523"],"award-info":[{"award-number":["S10OD028523"]}]},{"name":"New York State Biodefense Commercialization Fund","award":["R21AI156573"],"award-info":[{"award-number":["R21AI156573"]}]},{"name":"New York State Biodefense Commercialization Fund","award":["1P20GM130460-01A1-7936"],"award-info":[{"award-number":["1P20GM130460-01A1-7936"]}]},{"name":"New York State Biodefense Commercialization Fund","award":["1R03NS110996-01A1"],"award-info":[{"award-number":["1R03NS110996-01A1"]}]},{"name":"New York State Biodefense Commercialization Fund","award":["DMR-1933525"],"award-info":[{"award-number":["DMR-1933525"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Marine Drugs"],"abstract":"<jats:p>Sulfated glycans from marine organisms are excellent sources of naturally occurring glycosaminoglycan (GAG) mimetics that demonstrate therapeutic activities, such as antiviral\/microbial infection, anticoagulant, anticancer, and anti-inflammation activities. Many viruses use the heparan sulfate (HS) GAG on the surface of host cells as co-receptors for attachment and initiating cell entry. Therefore, virion\u2013HS interactions have been targeted to develop broad-spectrum antiviral therapeutics. Here we report the potential anti-monkeypox virus (MPXV) activities of eight defined marine sulfated glycans, three fucosylated chondroitin sulfates, and three sulfated fucans extracted from the sea cucumber species Isostichopus badionotus,\u00a0Holothuria floridana, and Pentacta pygmaea, and the sea urchin Lytechinus variegatus, as well as two chemically desulfated derivatives. The inhibitions of these marine sulfated glycans on MPXV A29 and A35 protein\u2013heparin interactions were evaluated using surface plasmon resonance (SPR). These results demonstrated that the viral surface proteins of MPXV A29 and A35 bound to heparin, which is a highly sulfated HS, and sulfated glycans from sea cucumbers showed strong inhibition of MPXV A29 and A35 interactions. The study of molecular interactions between viral proteins and host cell GAGs is important in developing therapeutics for the prevention and treatment of MPXV.<\/jats:p>","DOI":"10.3390\/md21050264","type":"journal-article","created":{"date-parts":[[2023,4,25]],"date-time":"2023-04-25T05:12:53Z","timestamp":1682399573000},"page":"264","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":25,"title":["SPR Sensor-Based Analysis of the Inhibition of Marine Sulfated Glycans on Interactions between Monkeypox Virus Proteins and Glycosaminoglycans"],"prefix":"10.3390","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7549-1890","authenticated-orcid":false,"given":"Peng","family":"He","sequence":"first","affiliation":[{"name":"Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"},{"name":"Department of Chemistry and Chemical Biology, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Deling","family":"Shi","sequence":"additional","affiliation":[{"name":"Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"},{"name":"Department of Chemistry and Chemical Biology, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yunran","family":"Li","sequence":"additional","affiliation":[{"name":"Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"},{"name":"Department of Biomedical Engineering, 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":"Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"},{"name":"Department of Chemistry and Chemical Biology, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8015-1404","authenticated-orcid":false,"given":"Seon Beom","family":"Kim","sequence":"additional","affiliation":[{"name":"Department of BioMolecular Sciences, Research Institute of Pharmaceutical Sciences, The University of Mississippi, Oxford, MS 38677, USA"},{"name":"Department of Food Science & Technology, College of Natural Resources and Life Science, Pusan National University, Miryang 46241, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rohini","family":"Dwivedi","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"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7104-3815","authenticated-orcid":false,"given":"Marwa","family":"Farrag","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"}]},{"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"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2219-5833","authenticated-orcid":false,"given":"Robert J.","family":"Linhardt","sequence":"additional","affiliation":[{"name":"Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"},{"name":"Department of Chemistry and Chemical Biology, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"},{"name":"Department of Biomedical Engineering, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"},{"name":"Departments 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":"Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"},{"name":"Departments 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":"Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"},{"name":"Departments of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY 12180, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1111\/j.1699-0463.1959.tb00328.x","article-title":"A pox-like disease in cynomolgus monkeys","volume":"46","author":"Magnus","year":"1959","journal-title":"Acta Pathol. Microbiolog. Scand."},{"key":"ref_2","first-page":"277","article-title":"Smallpox and monkeypox in non-human primates","volume":"39","author":"Arita","year":"1968","journal-title":"Bull. World Health Organ."},{"key":"ref_3","first-page":"593","article-title":"A human infection caused by monkeypox virus in Basankusu Territory, Democratic Republic of the Congo","volume":"46","author":"Ladnyj","year":"1972","journal-title":"Bull. World Health Organ."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1177\/216507990405200422","article-title":"Monkeypox in the United States: An occupational health look at the first cases","volume":"52","author":"Cunha","year":"2004","journal-title":"AAOHN J."},{"key":"ref_5","unstructured":"(2023, March 08). 2022 Monkeypox Outbreak Global Map, Available online: https:\/\/www.cdc.gov\/poxvirus\/monkeypox\/response\/2022\/worldmap.html."},{"key":"ref_6","first-page":"232","article-title":"Genomic variability of monkeypox virus among humans, Democratic Republic of the Congo","volume":"20","author":"Kugelman","year":"2014","journal-title":"Emerg. Infect. Disease J."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Bauer, S., Zhang, F., and Linhardt, R.J. (2021). Implications of glycosaminoglycans on viral zoonotic diseases. Diseases, 9.","DOI":"10.3390\/diseases9040085"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1038\/s41591-022-01907-y","article-title":"Phylogenomic characterization and signs of microevolution in the 2022 multi-country outbreak of monkeypox virus","volume":"28","author":"Isidro","year":"2022","journal-title":"Nat. Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"o2829","DOI":"10.1136\/bmj.o2829","article-title":"Monkeypox: Single dose of smallpox vaccine offers 78% protection, UKHSA reports","volume":"379","author":"Mahase","year":"2022","journal-title":"BMJ"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Freyn, A.W., Atyeo, C., Earl, P.L., Americo, J.L., Chuang, G.-Y., Natarajan, H., Frey, T., Gall, J., Moliva, J.I., and Hunegnaw, R. (2022). A monkeypox mRNA-lipid nanoparticle vaccine targeting virus binding, entry, and transmission drives protection against lethal orthopoxviral challenge. BioRxiv, BioRxiv:2022.12.17.520886.","DOI":"10.1101\/2022.12.17.520886"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Shi, D., He, P., Song, Y., Cheng, S., Linhardt, R.J., Dordick, J.S., Chi, L., and Zhang, F. (2022). Kinetic and structural aspects of glycosaminoglycan-monkeypox virus protein A29 interactions using surface plasmon resonance. Molecules, 27.","DOI":"10.3390\/molecules27185898"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Song, Y., He, P., Rodrigues, A.L., Datta, P., Tandon, R., Bates, J.T., Bierdeman, M.A., Chen, C., Dordick, J., and Zhang, F. (2021). Anti-SARS-CoV-2 Activity of Rhamnan Sulfate from Monostroma nitidum. Mar. Drugs, 19.","DOI":"10.3390\/md19120685"},{"key":"ref_13","first-page":"849","article-title":"Inhibition of SARS-CoV-2 wild-type (Wuhan-Hu-1) and Delta (B.1.617.2) strains by marine sulfated glycans","volume":"32","author":"Dwivedi","year":"2022","journal-title":"Glycobiology"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"101856","DOI":"10.1016\/j.jbc.2022.101856","article-title":"Fractionation of sulfated galactan from the red alga Botryocladia occidentalis separates its anticoagulant and anti-SARS-CoV-2 properties","volume":"298","author":"Kim","year":"2022","journal-title":"J Biol Chem."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1012207","DOI":"10.1016\/j.jbc.2021.101207","article-title":"Structural and kinetic analyses of holothurian sulfated glycans suggest potential treatment for SARS-CoV-2 infection","volume":"297","author":"Dwivedi","year":"2021","journal-title":"J Biol Chem."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"106869","DOI":"10.1016\/j.ijsu.2022.106869","article-title":"Monkeypox vaccines and vaccination strategies: Current knowledge and advances. An update\u2014Correspondence","volume":"105","author":"Chakraborty","year":"2022","journal-title":"Int. J. Surg."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Ahmed, S.F., Sohail, M.S., Quadeer, A.A., and McKay, M.R. (2022). Vaccinia-virus-based vaccines are expected to elicit highly cross-reactive immunity to the 2022 monkeypox virus. Viruses, 14.","DOI":"10.1101\/2022.06.23.497143"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"928","DOI":"10.1111\/brv.12034","article-title":"Glycosaminoglycans in infectious disease","volume":"88","author":"Kamhi","year":"2013","journal-title":"Biol. Rev."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"119818","DOI":"10.1016\/j.carbpol.2022.119818","article-title":"Heparin: An old drug for new clinical applications","volume":"295","author":"Wang","year":"2022","journal-title":"Carbohydr. Polym."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"7957","DOI":"10.1021\/acs.macromol.2c00675","article-title":"Polymers inspired by heparin and heparan sulfate for viral targeting","volume":"55","author":"Hoffmann","year":"2022","journal-title":"Macromolecules."},{"key":"ref_21","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. Biophys. Acta (BBA) Gen. Subj."},{"key":"ref_22","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_23","doi-asserted-by":"crossref","first-page":"18790","DOI":"10.1074\/jbc.M109.005702","article-title":"A Unique 2-Sulfated \u03b2-Galactan from the Egg Jelly of the Sea Urchin Glyptocidaris crenularis: Conformation Flexibility Versus Induction of the Sperm Acrosome Reaction*","volume":"284","author":"Castro","year":"2009","journal-title":"J Biol Chem."},{"key":"ref_24","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."}],"container-title":["Marine Drugs"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-3397\/21\/5\/264\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:23:01Z","timestamp":1760124181000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-3397\/21\/5\/264"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,25]]},"references-count":24,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,5]]}},"alternative-id":["md21050264"],"URL":"https:\/\/doi.org\/10.3390\/md21050264","relation":{},"ISSN":["1660-3397"],"issn-type":[{"value":"1660-3397","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,25]]}}}