{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T16:59:25Z","timestamp":1790614765656,"version":"4.1.0"},"reference-count":55,"publisher":"American Chemical Society (ACS)","issue":"9","license":[{"start":{"date-parts":[[2026,8,9]],"date-time":"2026-08-09T00:00:00Z","timestamp":1786233600000},"content-version":"vor","delay-in-days":10,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000054","name":"National Cancer Institute","doi-asserted-by":"publisher","award":["U24CA271079"],"award-info":[{"award-number":["U24CA271079"]}],"id":[{"id":"10.13039\/100000054","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,9,4]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Xenotransplantation using genetically engineered pig organs offers a promising solution to the shortage of donor organs for life-saving transplantations. However, human-preformed antibodies against unknown pig xenoantigens remain a significant barrier to successful xenotransplantation. Current methods for characterizing these antibodies or xenoantigens are limited to cellular-level cross-match assays. In this study, we developed a novel approach to identify pig xenoantigens, including peptide and glycopeptide epitopes, that react with human-preformed antibodies. First, human-preformed antibodies against xenoantigens were enriched from plasma using immobilized pig kidney proteins. The enriched antibodies were then immobilized and used to isolate pig kidney proteins, peptides, and intact glycopeptides, followed by liquid chromatography\u2013tandem mass spectrometry analysis. This dual-level approach identified 221 peptides corresponding to 153 proteins, with a significant enrichment of plasma membrane and extracellular proteins. Notably, 11 peptides were unique to pig sequences, suggesting their potential role in driving xenogeneic immune responses. Glycoproteomic analysis identified 122 intact glycopeptides, predominantly complex\/hybrid glycoforms, and Neu5Gc-containing glycans. Our method effectively identifies peptides and intact glycopeptides reactive to human-preformed antibodies, providing critical insights for discovering xenoantigens. These findings could guide genetic engineering strategies and enhance recipient candidate screening for xenotransplantation, ultimately increasing the feasibility and success of xenogeneic organ transplantation.<\/jats:p>","DOI":"10.1021\/acs.jproteome.5c01244","type":"journal-article","created":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T13:23:03Z","timestamp":1785849783000},"page":"4511-4523","source":"Crossref","is-referenced-by-count":1,"title":["Proteomic\nIdentification of Pig Xenoantigens for Clinical\nXenotransplantation"],"prefix":"10.1021","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9444-3632","authenticated-orcid":true,"given":"Hongyi","family":"Liu","sequence":"first","affiliation":[{"name":"Johns Hopkins University School of Medicine , , , ,","place":["Baltimore, Maryland, United States, 21231"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Trung","family":"Hoa\u0300ng","sequence":"additional","affiliation":[{"name":"Johns Hopkins University School of Medicine , , , ,","place":["Baltimore, Maryland, United States, 21231"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yingwei","family":"Hu","sequence":"additional","affiliation":[{"name":"Johns Hopkins University School of Medicine , , , ,","place":["Baltimore, Maryland, United States, 21231"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuanwei","family":"Xu","sequence":"additional","affiliation":[{"name":"Johns Hopkins University School of Medicine , , , ,","place":["Baltimore, Maryland, United States, 21231"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-5004-5904","authenticated-orcid":true,"given":"Zhenyu","family":"Sun","sequence":"additional","affiliation":[{"name":"Johns Hopkins University School of Medicine , , , ,","place":["Baltimore, Maryland, United States, 21231"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brandon J.","family":"Peiffer","sequence":"additional","affiliation":[{"name":"Johns Hopkins University School of Medicine , , , ,","place":["Baltimore, Maryland, United States, 21205"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-5930-8424","authenticated-orcid":true,"given":"Yuanyu","family":"Huang","sequence":"additional","affiliation":[{"name":"Johns Hopkins University School of Medicine , , , ,","place":["Baltimore, Maryland, United States, 21231"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhaoli","family":"Sun","sequence":"additional","affiliation":[{"name":"Johns Hopkins University School of Medicine , , , ,","place":["Baltimore, Maryland, United States, 21205"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8726-7098","authenticated-orcid":true,"given":"Hui","family":"Zhang","sequence":"additional","affiliation":[{"name":"Johns Hopkins University School of Medicine , , , ,","place":["Baltimore, Maryland, United States, 21231"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,7,30]]},"reference":[{"issue":"7220","key":"2026090409123303100_cit1","doi-asserted-by":"publisher","first-page":"1311","DOI":"10.1136\/bmj.319.7220.1311","article-title":"Xenotransplantation:\nProgress and Promise","volume":"319","author":"Vanderpool","year":"1999","journal-title":"BMJ"},{"issue":"7","key":"2026090409123303100_cit2","doi-asserted-by":"publisher","first-page":"519","DOI":"10.1038\/nri2099","article-title":"Xenotransplantation:\nCurrent Status and a Perspective on the Future","volume":"7","author":"Yang","year":"2007","journal-title":"Nat. Rev. Immunol."},{"issue":"6","key":"2026090409123303100_cit3","doi-asserted-by":"publisher","first-page":"513","DOI":"10.1097\/MOT.0000000000000463","article-title":"Xenotransplantation: Past, Present, and Future","volume":"22","author":"Ekser","year":"2017","journal-title":"Curr. Opin. Organ Transplant."},{"issue":"4","key":"2026090409123303100_cit4","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1016\/S1074-7613(01)00124-8","article-title":"The Immunological Barrier to Xenotransplantation","volume":"14","author":"Cascalho","year":"2001","journal-title":"Immunity"},{"issue":"3","key":"2026090409123303100_cit5","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1097\/MOT.0000000000001146","article-title":"Current Challenges in Xenotransplantation","volume":"29","author":"Vadori","year":"2024","journal-title":"Curr. Opin. Organ Transplant."},{"issue":"10","key":"2026090409123303100_cit6","doi-asserted-by":"publisher","first-page":"480","DOI":"10.1016\/0167-5699(93)90261-I","article-title":"Interaction\nof the Natural Anti-Gal Antibody with \u03b1-Galactosyl Epitopes:\nA Major Obstacle for Xenotransplantation in Humans","volume":"14","author":"Galili","year":"1993","journal-title":"Immunol. Today"},{"issue":"5","key":"2026090409123303100_cit7","doi-asserted-by":"publisher","DOI":"10.1111\/xen.12394","article-title":"B4GALNT2 and Xenotransplantation:\nA Newly Appreciated Xenogeneic Antigen","volume":"25","author":"Byrne","year":"2018","journal-title":"Xenotransplantation"},{"key":"2026090409123303100_cit8","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2020.00622","article-title":"The Possible Role\nof Anti-Neu5Gc as an Obstacle in Xenotransplantation","volume":"11","author":"Tector","year":"2020","journal-title":"Front. Immunol."},{"issue":"3","key":"2026090409123303100_cit9","doi-asserted-by":"publisher","first-page":"194","DOI":"10.1111\/xen.12161","article-title":"Evaluation of Human\nand Non-Human Primate Antibody\nBinding to Pig Cells Lacking GGTA1\/CMAH\/\u03b24GalNT2 Genes","volume":"22","author":"Estrada","year":"2015","journal-title":"Xenotransplantation"},{"issue":"1","key":"2026090409123303100_cit10","doi-asserted-by":"publisher","DOI":"10.1111\/ctr.14139","article-title":"Pig Kidney\nXenotransplantation: Progress\ntoward Clinical Trials","volume":"35","author":"Cooper","year":"2021","journal-title":"Clin. Transplant."},{"issue":"7893","key":"2026090409123303100_cit11","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1038\/d41586-022-00111-9","article-title":"First Pig-to-Human\nHeart Transplant: What Can Scientists Learn?","volume":"601","author":"Reardon","year":"2022","journal-title":"Nature"},{"issue":"8006","key":"2026090409123303100_cit12","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1038\/d41586-024-00879-y","article-title":"First Pig Kidney Transplant in a\nPerson: What It Means\nfor the Future","volume":"628","author":"Mallapaty","year":"2024","journal-title":"Nature"},{"issue":"8014","key":"2026090409123303100_cit13","doi-asserted-by":"publisher","first-page":"980","DOI":"10.1038\/d41586-024-01453-2","article-title":"Pig-Organ\nTransplants: What Three Human Recipients Have Taught Scientists","volume":"629","author":"Kozlov","year":"2024","journal-title":"Nature"},{"issue":"20","key":"2026090409123303100_cit14","doi-asserted-by":"publisher","first-page":"1889","DOI":"10.1056\/NEJMoa2120238","article-title":"Results of Two Cases\nof Pig-to-Human Kidney Xenotransplantation","volume":"386","author":"Montgomery","year":"2022","journal-title":"N. 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Immunol."},{"issue":"2","key":"2026090409123303100_cit17","doi-asserted-by":"publisher","first-page":"300","DOI":"10.1097\/TP.0000000000003303","article-title":"The Role of SLAs in Xenotransplantation","volume":"105","author":"Ladowski","year":"2021","journal-title":"Transplantation"},{"issue":"4","key":"2026090409123303100_cit18","doi-asserted-by":"publisher","DOI":"10.1111\/xen.12686","article-title":"Immunological\nSelection and Monitoring of Patients Undergoing Pig Kidney Transplantation","volume":"28","author":"Lucander","year":"2021","journal-title":"Xenotransplantation"},{"issue":"1","key":"2026090409123303100_cit19","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-020-66311-3","article-title":"Old World\nMonkeys Are Less than Ideal Transplantation Models for Testing Pig\nOrgans Lacking Three Carbohydrate Antigens (Triple-Knockout)","volume":"10","author":"Yamamoto","year":"2020","journal-title":"Sci. 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Smart Nano Mater."},{"issue":"1","key":"2026090409123303100_cit31","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-025-66469-2","article-title":"Straightforward\nConstruction of Functionalized \u03b3-Lactams via\nConjugated-Engineered Covalent Organic Framework Photocatalysed Cascade\nReactions","volume":"16","author":"Lin","year":"2025","journal-title":"Nat. Commun."},{"issue":"16","key":"2026090409123303100_cit32","doi-asserted-by":"publisher","first-page":"2833","DOI":"10.1002\/pmic.200700131","article-title":"Methods for\nthe Detection and Analysis\nof Protein-Protein Interactions","volume":"7","author":"Bergg\u00e5rd","year":"2007","journal-title":"Proteomics"},{"key":"2026090409123303100_cit33","doi-asserted-by":"publisher","DOI":"10.1002\/0471142301.ns0528s46","article-title":"Identifying Novel Protein-Protein\nInteractions Using Co-Immunoprecipitation and Mass Spectroscopy","volume":"46","author":"Free","year":"2009","journal-title":"Curr. Protoc. 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Biotechnol."},{"issue":"6","key":"2026090409123303100_cit41","doi-asserted-by":"publisher","first-page":"660","DOI":"10.1038\/nbt827","article-title":"Identification and Quantification\nof N-Linked Glycoproteins Using Hydrazide Chemistry, Stable Isotope\nLabeling and Mass Spectrometry","volume":"21","author":"Zhang","year":"2003","journal-title":"Nat. Biotechnol."},{"key":"2026090409123303100_cit42","first-page":"1","article-title":"Periodate Oxidation\nof Carbohydrates","volume-title":"Advances in Carbohydrate\nChemistry","author":"Bobbitt","year":"1956"},{"key":"2026090409123303100_cit43","doi-asserted-by":"publisher","first-page":"789","DOI":"10.3389\/fimmu.2019.00789","article-title":"Absence of Neu5Gc and\nPresence of Anti-Neu5Gc Antibodies\nin Humans\u2500An Evolutionary Perspective","volume":"10","author":"Altman","year":"2019","journal-title":"Front. Immunol."},{"issue":"20","key":"2026090409123303100_cit44","doi-asserted-by":"publisher","first-page":"5227","DOI":"10.1007\/s00216-021-03495-1","article-title":"In-Depth\nCharacterization of Non-Human Sialic Acid (Neu5Gc) in Human Serum\nUsing Label-Free ZIC-HILIC\/MRM-MS","volume":"413","author":"Seo","year":"2021","journal-title":"Anal. Bioanal.\nChem."},{"issue":"30","key":"2026090409123303100_cit45","doi-asserted-by":"publisher","first-page":"8114","DOI":"10.1021\/acs.jafc.8b01042","article-title":"Quantitation of Sialic Acids in Infant\nFormulas by\nLiquid Chromatography-Mass Spectrometry: An Assessment of Different\nProtein Sources and Discovery of New Analogues","volume":"66","author":"Wylie","year":"2018","journal-title":"J. Agric. Food Chem."},{"issue":"6","key":"2026090409123303100_cit46","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1038\/s41435-022-00182-8","article-title":"Immune Disguise:\nThe Mechanisms of\nNeu5Gc Inducing Autoimmune and Transplant Rejection","volume":"23","author":"Ding","year":"2022","journal-title":"Genes Immun."},{"issue":"14","key":"2026090409123303100_cit47","doi-asserted-by":"publisher","first-page":"814","DOI":"10.1089\/ars.2016.6793","article-title":"Haptoglobin","volume":"26","author":"Andersen","year":"2017","journal-title":"Antioxid. Redox\nSignal."},{"issue":"11","key":"2026090409123303100_cit48","doi-asserted-by":"publisher","first-page":"4168","DOI":"10.1073\/pnas.0508723103","article-title":"Haptoglobin, a Hemoglobin-Binding Plasma Protein, Is Present in Bony\nFish and Mammals but Not in Frog and Chicken","volume":"103","author":"Wicher","year":"2006","journal-title":"Proc. Natl. Acad. Sci. 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