{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T18:49:47Z","timestamp":1792003787751,"version":"4.4.0"},"reference-count":66,"publisher":"American Chemical Society (ACS)","issue":"40","license":[{"start":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T00:00:00Z","timestamp":1790640000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/na","name":"Academia Sinica Core Facility and Innovative Instrument Project","doi-asserted-by":"publisher","award":["AS-CFII-114-A13"],"award-info":[{"award-number":["AS-CFII-114-A13"]}],"id":[{"id":"10.13039\/na","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/na","name":"Rock Biomedical, Inc. and the NIH","doi-asserted-by":"publisher","award":["NA"],"award-info":[{"award-number":["NA"]}],"id":[{"id":"10.13039\/na","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/na","name":"Rock Biomedical, Inc. and the NIH","doi-asserted-by":"publisher","award":["NIH-AI130227"],"award-info":[{"award-number":["NIH-AI130227"]}],"id":[{"id":"10.13039\/na","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,10,14]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Immune checkpoints are key regulators of the immune system that cancer cells exploit to evade immune surveillance. While these pathways have been targeted with antibody therapies such as PD-1\/PD-L1 inhibitors, other inhibitory receptors, like sialic acid-binding immunoglobulin-type lectins (Siglecs), remain clinically underexplored. Among the many Siglecs on immune cells that interact with sialosides on cancer cells, Siglec-9 and Siglec-10 are prominently expressed on macrophages within the tumor microenvironment, functioning as key inhibitory immune checkpoints that suppress macrophage-mediated phagocytosis and cytotoxicity. Similarly, Siglec-7 and Siglec-9 are expressed on NK cells, acting as primary immune checkpoints that inhibit cellular cytotoxicity. Since all Siglecs recognize sialic acids, we sought to identify a common small-molecule inhibitor to target these receptors for immunotherapy. We first chemoenzymatically synthesized more than 60 glycans, including multiantennary glycans with terminal sialic acids, and assembled them onto a glycan microarray to screen for high-affinity binders to these Siglecs. We identified several strong binders in these array assays; among them, a truncated glycolyl sialoside (R3) was found to strongly inhibit the interaction of Siglec-10 with HER2-low MCF-7 cells, substantially enhancing macrophage-mediated phagocytosis and cytotoxicity. Notably, R3 also interacts significantly with other inhibitory immune checkpoint receptors, including Siglec-5, -7, -9, -11, and -15, thereby relieving Siglec-mediated suppression and enhancing NK cell-mediated cytotoxicity in cell-based assays. Structural studies are underway to investigate the binding mode of R3 with these Siglecs to guide further optimization toward a common small-molecule inhibitor targeting multiple inhibitory glyco-immune checkpoints for cancer immunotherapy.<\/jats:p>","DOI":"10.1021\/jacs.6c15475","type":"journal-article","created":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T19:03:07Z","timestamp":1790708587000},"page":"43743-43753","source":"Crossref","is-referenced-by-count":0,"title":["A Common Small-Molecule\nInhibitor Targeting Multiple\nSiglecs Associated with Immune Checkpoint Suppression of Cytotoxicity\nand Phagocytosis"],"prefix":"10.1021","volume":"148","author":[{"given":"Cinya","family":"Chung","sequence":"first","affiliation":[{"name":"Academia Sinica , , 128 Academia Rd., Sec, 2 , ,","place":["Taipei, Taiwan, 11529"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8060-897X","authenticated-orcid":true,"given":"Ruofan","family":"Li","sequence":"additional","affiliation":[{"name":"The Scripps Research Institute , , 10550 North Torrey Pines Rd. , , ,","place":["La Jolla, California, United States, 92037"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6187-288X","authenticated-orcid":true,"given":"Li-Chun","family":"Cheng","sequence":"additional","affiliation":[{"name":"Academia Sinica , , 128 Academia Rd., Sec, 2 , ,","place":["Taipei, Taiwan, 11529"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chen-Yo","family":"Fan","sequence":"additional","affiliation":[{"name":"Academia Sinica , , 128 Academia Rd., Sec, 2 , ,","place":["Taipei, Taiwan, 11529"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-3039-7570","authenticated-orcid":true,"given":"Kuo-Shiang","family":"Liao","sequence":"additional","affiliation":[{"name":"Academia Sinica , , 128 Academia Rd., Sec, 2 , ,","place":["Taipei, Taiwan, 11529"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chih-Chuan","family":"Kung","sequence":"additional","affiliation":[{"name":"Academia Sinica , , 128 Academia Rd., Sec, 2 , ,","place":["Taipei, Taiwan, 11529"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9961-7865","authenticated-orcid":true,"given":"Chi-Huey","family":"Wong","sequence":"additional","affiliation":[{"name":"Academia Sinica , , 128 Academia Rd., Sec, 2 , ,","place":["Taipei, Taiwan, 11529"]},{"name":"The Scripps Research Institute , , 10550 North Torrey Pines Rd. , , ,","place":["La Jolla, California, United States, 92037"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,9,29]]},"reference":[{"issue":"11","key":"2026101414074176100_cit1","doi-asserted-by":"publisher","first-page":"3887","DOI":"10.1002\/j.1460-2075.1992.tb05481.x","article-title":"Induced expression\nof PD-1, a novel member of the immunoglobulin gene superfamily, upon\nprogrammed cell death","volume":"11","author":"Ishida","year":"1992","journal-title":"EMBO J."},{"issue":"2","key":"2026101414074176100_cit2","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/j.cell.2015.03.030","article-title":"Immune checkpoint targeting in cancer therapy: toward\ncombination strategies with curative potential","volume":"161","author":"Sharma","year":"2015","journal-title":"Cell"},{"key":"2026101414074176100_cit3","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2022.964442","article-title":"The role of\nPD-1\/PD-L1\nand application of immune-checkpoint inhibitors in human cancers","volume":"13","author":"Tang","year":"2022","journal-title":"Front. 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Immunother."},{"issue":"2","key":"2026101414074176100_cit22","doi-asserted-by":"publisher","first-page":"489","DOI":"10.1042\/bj3550489","article-title":"Identification, characterization and leucocyte expression\nof Siglec-10, a novel human sialic acid-binding receptor","volume":"355","author":"Munday","year":"2001","journal-title":"Biochem. J."},{"issue":"10","key":"2026101414074176100_cit23","doi-asserted-by":"publisher","first-page":"3779","DOI":"10.4049\/jimmunol.136.10.3779","article-title":"The human B cell-associated antigen CD24 is a single\nchain sialoglycoprotein","volume":"136","author":"Pirruccello","year":"1986","journal-title":"J. Immunol."},{"issue":"2","key":"2026101414074176100_cit24","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1038\/cmi.2009.119","article-title":"CD24: from A to Z","volume":"7","author":"Fang","year":"2010","journal-title":"Cell. Mol. 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Immunol."},{"issue":"6","key":"2026101414074176100_cit29","doi-asserted-by":"publisher","first-page":"3962","DOI":"10.4049\/jimmunol.134.6.3962","article-title":"Monoclonal antibody BA-1 recognizes\na novel human leukocyte\ncell surface sialoglycoprotein complex","volume":"134","author":"Pirruccello","year":"1985","journal-title":"J. Immunol."},{"issue":"5","key":"2026101414074176100_cit30","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1007\/s00418-016-1531-7","article-title":"Expression of CD24 and Siglec-10 in first trimester\nplacenta: implications for immune tolerance at the fetal\u2013maternal\ninterface","volume":"147","author":"Sammar","year":"2017","journal-title":"Histochem. Cell Biol."},{"issue":"12","key":"2026101414074176100_cit31","doi-asserted-by":"publisher","first-page":"1376","DOI":"10.1038\/s41589-020-0622-x","article-title":"Targeted glycan degradation potentiates the anticancer\nimmune response in vivo","volume":"16","author":"Gray","year":"2020","journal-title":"Nat. Chem. Biol."},{"issue":"11","key":"2026101414074176100_cit32","doi-asserted-by":"publisher","DOI":"10.3390\/molecules30112264","article-title":"Chemical and Enzymatic Synthesis\nof DisialylGb5 and Other Sialosides for Glycan Array Assembly and\nEvaluation of Siglec-Mediated Immune Checkpoint Inhibition","volume":"30","author":"Liao","year":"2025","journal-title":"Molecules"},{"issue":"38","key":"2026101414074176100_cit33","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2517415122","article-title":"Improving the efficacy\nof anti-SSEA4 antibody in pancreatic cancer immunotherapy with glyco-optimization\nand immune checkpoint blockade","volume":"122","author":"Chuang","year":"2025","journal-title":"Proc. Natl.\nAcad. Sci. U.S.A."},{"issue":"41","key":"2026101414074176100_cit34","doi-asserted-by":"publisher","first-page":"15382","DOI":"10.1021\/ja409097c","article-title":"Efficient\nconvergent synthesis of bi-, tri-, and tetra-antennary complex type\nN-glycans and their HIV-1 antigenicity","volume":"135","author":"Shivatare","year":"2013","journal-title":"J. Am.\nChem. Soc."},{"issue":"42","key":"2026101414074176100_cit35","doi-asserted-by":"publisher","first-page":"14849","DOI":"10.1021\/ja104657b","article-title":"Differential\nreceptor binding affinities of influenza hemagglutinins on glycan\narrays","volume":"132","author":"Liao","year":"2010","journal-title":"J. Am. Chem. Soc."},{"issue":"15","key":"2026101414074176100_cit36","doi-asserted-by":"publisher","first-page":"12937","DOI":"10.1021\/jacs.5c02356","article-title":"Expedient\nAssembly of Multiantennary\nN-Glycans from Common N-Glycan Cores with Orthogonal Protection for\nthe Profiling of Glycan-Binding Proteins","volume":"147","author":"Li","year":"2025","journal-title":"J.\nAm. Chem. Soc."},{"issue":"44","key":"2026101414074176100_cit37","doi-asserted-by":"publisher","first-page":"10909","DOI":"10.1021\/ja011382r","article-title":"Microbial glycosyltransferases\nfor carbohydrate synthesis:\nalpha-2,3-sialyltransferase from Neisseria gonorrheae","volume":"123","author":"Izumi","year":"2001","journal-title":"J. Am. Chem. 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U.S.A."},{"issue":"6","key":"2026101414074176100_cit40","doi-asserted-by":"publisher","first-page":"752","DOI":"10.1093\/glycob\/cwq030","article-title":"Extensive\nenrichment of N-glycolylneuraminic\nacid in extracellular sialoglycoproteins abundantly synthesized and\nsecreted by human cancer cells","volume":"20","author":"Inoue","year":"2010","journal-title":"Glycobiology"},{"key":"2026101414074176100_cit41","doi-asserted-by":"publisher","DOI":"10.1016\/j.tranon.2023.101643","article-title":"N-glycolylneuraminic\nacid as a carbohydrate cancer biomarker","volume":"31","author":"Wang","year":"2023","journal-title":"Transl.\nOncol."},{"issue":"3\u20134","key":"2026101414074176100_cit42","doi-asserted-by":"publisher","first-page":"412","DOI":"10.1002\/ijch.201400141","article-title":"Rapid Identification\nof Terminal\nSialic Acid Linkage Isomers by Pseudo-MS3 Mass Spectrometry","volume":"55","author":"Chen","year":"2015","journal-title":"Isr. J. Chem."},{"key":"2026101414074176100_cit43","doi-asserted-by":"publisher","DOI":"10.3389\/fmolb.2021.645999","article-title":"Terminal Epitope-Dependent Branch\nPreference of Siglecs Toward N-Glycans","volume":"8","author":"Wang","year":"2021","journal-title":"Front.\nMol. Biosci."},{"issue":"12","key":"2026101414074176100_cit44","doi-asserted-by":"publisher","first-page":"8633","DOI":"10.1074\/jbc.275.12.8633","article-title":"Loss of N-glycolylneuraminic acid\nin human evolution Implications for sialic acid recognition by siglecs","volume":"275","author":"Brinkman-Van der Linden","year":"2000","journal-title":"J. Biol. 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Invest."},{"issue":"1","key":"2026101414074176100_cit47","doi-asserted-by":"publisher","DOI":"10.1128\/mbio.03393-22","article-title":"Siglec-9 Restrains\nAntibody-Dependent Natural Killer Cell Cytotoxicity against SARS-CoV-2","volume":"14","author":"Saini","year":"2023","journal-title":"mBio"},{"issue":"3","key":"2026101414074176100_cit48","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1093\/intimm\/dxu090","article-title":"IL-10 enhances\nthe phenotype of M2 macrophages induced by IL-4 and confers the ability\nto increase eosinophil migration","volume":"27","author":"Makita","year":"2015","journal-title":"Int. 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