{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T20:01:51Z","timestamp":1792008111789,"version":"4.4.0"},"reference-count":29,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2023,4,21]],"date-time":"2023-04-21T00:00:00Z","timestamp":1682035200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc\/4.0"},{"start":{"date-parts":[[2023,4,21]],"date-time":"2023-04-21T00:00:00Z","timestamp":1682035200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc\/4.0"}],"funder":[{"name":"Biosidus"},{"name":"Vriendenloterij"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Drugs R D"],"published-print":{"date-parts":[[2023,6]]},"DOI":"10.1007\/s40268-023-00421-x","type":"journal-article","created":{"date-parts":[[2023,4,21]],"date-time":"2023-04-21T15:11:34Z","timestamp":1682089894000},"page":"141-153","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Development of a Biosimilar of Agalsidase Beta for the Treatment of Fabry Disease: Preclinical Evaluation"],"prefix":"10.1007","volume":"23","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7989-4910","authenticated-orcid":false,"given":"Andr\u00e9 B. P.","family":"van Kuilenburg","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carla E. M.","family":"Hollak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana","family":"Travella","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melisa","family":"Jacobs","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lucas D.","family":"Gentilini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ren\u00e9","family":"Leen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karen M. M. Ghauharali-van","family":"der Vlugt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Femke S. Beers","family":"Stet","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Susan M. I.","family":"Goorden","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sanne","family":"van der Veen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcelo","family":"Criscuolo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mariana","family":"Papouchado","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,4,21]]},"reference":[{"key":"421_CR1","volume-title":"The Online Metabolic and Molecular Bases of Inherited Disease","author":"RJ Desnick","year":"2019","unstructured":"Desnick RJ, Ioannou YA, Eng CM. \u03b1-Galactosidase A deficiency: Fabry disease. In: Valle DL, Antonarakis S, Ballabio A, Beaudet\u00a0AL, Mitchell GA, editors. The Online Metabolic and Molecular Bases of Inherited Disease. New York: McGraw-Hill Education; 2019."},{"key":"421_CR2","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1016\/B978-0-444-62702-5.00017-2","volume":"132","author":"R Schiffmann","year":"2015","unstructured":"Schiffmann R. Fabry disease. Handb Clin Neurol. 2015;132:231\u201348.","journal-title":"Handb Clin Neurol"},{"issue":"5","key":"421_CR3","doi-asserted-by":"publisher","first-page":"1631","DOI":"10.1681\/ASN.2016090964","volume":"28","author":"M Arends","year":"2017","unstructured":"Arends M, Wanner C, Hughes D, Mehta A, Oder D, Watkinson OT, et\u00a0al. Characterization of classical and nonclassical Fabry disease: A multicenter study. J Am Soc Nephrol. 2017;28(5):1631\u201341.","journal-title":"J Am Soc Nephrol"},{"issue":"5","key":"421_CR4","doi-asserted-by":"publisher","first-page":"1139","DOI":"10.33594\/000000077","volume":"52","author":"F Braun","year":"2019","unstructured":"Braun F, Blomberg L, Brodesser S, Liebau MC, Schermer B, Benzing T, et\u00a0al. Enzyme replacement therapy clears Gb3 deposits from a podocyte cell culture model of Fabry disease but fails to restore altered cellular signaling. Cell Physiol Biochem. 2019;52(5):1139\u201350.","journal-title":"Cell Physiol Biochem"},{"issue":"1","key":"421_CR5","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1056\/NEJM200107053450102","volume":"345","author":"CM Eng","year":"2001","unstructured":"Eng CM, Guffon N, Wilcox WR, Germain DP, Lee P, Waldek S, et\u00a0al. Safety and efficacy of recombinant human alpha-galactosidase A replacement therapy in Fabry\u2019s disease. N Engl J Med. 2001;345(1):9\u201316.","journal-title":"N Engl J Med"},{"issue":"6","key":"421_CR6","doi-asserted-by":"publisher","first-page":"1933","DOI":"10.1046\/j.1523-1755.2002.00675.x","volume":"62","author":"BL Thurberg","year":"2002","unstructured":"Thurberg BL, Rennke H, Colvin RB, Dikman S, Gordon RE, Collins AB, et\u00a0al. Globotriaosylceramide accumulation in the Fabry kidney is cleared from multiple cell types after enzyme replacement therapy. Kidney Int. 2002;62(6):1933\u201346.","journal-title":"Kidney Int"},{"issue":"5","key":"421_CR7","doi-asserted-by":"publisher","first-page":"1547","DOI":"10.1681\/ASN.2006080816","volume":"18","author":"DP Germain","year":"2007","unstructured":"Germain DP, Waldek S, Banikazemi M, Bushinsky DA, Charrow J, Desnick RJ, et\u00a0al. Sustained, long-term renal stabilization after 54 months of agalsidase beta therapy in patients with Fabry disease. J Am Soc Nephrol. 2007;18(5):1547\u201357.","journal-title":"J Am Soc Nephrol"},{"issue":"8","key":"421_CR8","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0182379","volume":"12","author":"M Arends","year":"2017","unstructured":"Arends M, Biegstraaten M, Hughes DA, Mehta A, Elliott PM, Oder D, et\u00a0al. Retrospective study of long-term outcomes of enzyme replacement therapy in Fabry disease: analysis of prognostic factors. PLoS\u00a0One. 2017;12(8): e0182379.","journal-title":"PLoS\u00a0One"},{"issue":"5","key":"421_CR9","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1136\/jmedgenet-2017-104863","volume":"55","author":"M Arends","year":"2018","unstructured":"Arends M, Biegstraaten M, Wanner C, Sirrs S, Mehta A, Elliott PM, et\u00a0al. Agalsidase alfa versus agalsidase beta for the treatment of Fabry disease: an international cohort study. J Med Genet. 2018;55(5):351\u20138.","journal-title":"J Med Genet"},{"issue":"2","key":"421_CR10","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1016\/j.ymgme.2018.11.008","volume":"126","author":"SJ van der Veen","year":"2019","unstructured":"van der Veen SJ, van Kuilenburg ABP, Hollak CEM, Kaijen PHP, Voorberg J, Langeveld M. Antibodies against recombinant alpha-galactosidase A in Fabry disease: subclass analysis and impact on response to treatment. Mol Genet Metab. 2019;126(2):162\u20138.","journal-title":"Mol Genet Metab"},{"issue":"12","key":"421_CR11","doi-asserted-by":"publisher","first-page":"2879","DOI":"10.1681\/ASN.2018070740","volume":"29","author":"M Lenders","year":"2018","unstructured":"Lenders M, Neu\u00dfer LP, Rudnicki M, Nordbeck P, Canaan-K\u00fchl S, Nowak A, et\u00a0al. Dose-dependent effect of enzyme replacement therapy on neutralizing antidrug antibody titers and clinical outcome in patients with Fabry disease. J Am Soc Nephrol. 2018;29(12):2879\u201389.","journal-title":"J Am Soc Nephrol"},{"issue":"3","key":"421_CR12","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1002\/jimd.12080","volume":"42","author":"R Schiffmann","year":"2019","unstructured":"Schiffmann R, Goker-Alpan O, Holida M, Giraldo P, Barisoni L, Colvin RB, et\u00a0al. Pegunigalsidase alfa, a novel PEGylated enzyme replacement therapy for Fabry disease, provides sustained plasma concentrations and favorable pharmacodynamics: a 1-year Phase 1\/2 clinical trial. J Inherit Metab Dis. 2019;42(3):534\u201344.","journal-title":"J Inherit Metab Dis"},{"issue":"3","key":"421_CR13","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1016\/j.ymgme.2020.04.003","volume":"130","author":"K Nakamura","year":"2020","unstructured":"Nakamura K, Kawashima S, Tozawa H, Yamaoka M, Yamamoto T, Tanaka N, et\u00a0al. Pharmacokinetics and pharmacodynamics of JR-051, a biosimilar of agalsidase beta, in healthy adults and patients with Fabry disease: Phase I and II\/III clinical studies. Mol Genet Metab. 2020;130(3):215\u201324.","journal-title":"Mol Genet Metab"},{"issue":"2","key":"421_CR14","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1016\/0009-8981(81)90384-3","volume":"112","author":"JS Mayes","year":"1981","unstructured":"Mayes JS, Scheerer JB, Sifers RN, Donaldson ML. Differential assay for lysosomal alpha-galactosidases in human tissues and its application to Fabry\u2019s disease. Clin Chim Acta. 1981;112(2):247\u201351.","journal-title":"Clin Chim Acta"},{"issue":"8","key":"421_CR15","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0136442","volume":"10","author":"YJ Jeon","year":"2015","unstructured":"Jeon YJ, Jung N, Park JW, Park HY, Jung SC. Epithelial-mesenchymal transition in kidney tubular epithelial cells induced by globotriaosylsphingosine and globotriaosylceramide. PLoS ONE. 2015;10(8): e0136442.","journal-title":"PLoS ONE"},{"issue":"24","key":"421_CR16","doi-asserted-by":"publisher","first-page":"10395","DOI":"10.1007\/s00253-016-7689-z","volume":"100","author":"HJ Lee","year":"2016","unstructured":"Lee HJ, Park HH, Sohn Y, Ryu J, Park JH, Rhee WJ, et\u00a0al. \u03b1-Galactosidase delivery using 30Kc19-human serum albumin nanoparticles for effective treatment of Fabry disease. Appl Microbiol Biotechnol. 2016;100(24):10395\u2013402.","journal-title":"Appl Microbiol Biotechnol"},{"issue":"8","key":"421_CR17","doi-asserted-by":"publisher","first-page":"911","DOI":"10.1139\/o59-099","volume":"37","author":"EG Bligh","year":"1959","unstructured":"Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37(8):911\u20137.","journal-title":"Can J Biochem Physiol"},{"issue":"4","key":"421_CR18","doi-asserted-by":"publisher","first-page":"742","DOI":"10.1373\/clinchem.2006.079012","volume":"53","author":"JE Groener","year":"2007","unstructured":"Groener JE, Poorthuis BJ, Kuiper S, Helmond MT, Hollak CE, Aerts JM. HPLC for simultaneous quantification of total ceramide, glucosylceramide, and ceramide trihexoside concentrations in plasma. Clin Chem. 2007;53(4):742\u20137.","journal-title":"Clin Chem"},{"issue":"3","key":"421_CR19","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1373\/clinchem.2012.192138","volume":"59","author":"H Gold","year":"2013","unstructured":"Gold H, Mirzaian M, Dekker N, Joao Ferraz M, Lugtenburg J, Cod\u00e9e JD, et\u00a0al. Quantification of globotriaosylsphingosine in plasma and urine of Fabry patients by stable isotope ultraperformance liquid chromatography-tandem mass spectrometry. Clin Chem. 2013;59(3):547\u201356.","journal-title":"Clin Chem"},{"issue":"2","key":"421_CR20","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1016\/j.jmb.2004.01.035","volume":"337","author":"SC Garman","year":"2004","unstructured":"Garman SC, Garboczi DN. The molecular defect leading to Fabry disease: structure of human alpha-galactosidase. J Mol Biol. 2004;337(2):319\u201335.","journal-title":"J Mol Biol"},{"issue":"4","key":"421_CR21","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1093\/glycob\/cwg034","volume":"13","author":"K Lee","year":"2003","unstructured":"Lee K, Jin X, Zhang K, Copertino L, Andrews L, Baker-Malcolm J, et\u00a0al. A biochemical and pharmacological comparison of enzyme replacement therapies for the glycolipid storage disorder Fabry disease. Glycobiology. 2003;13(4):305\u201313.","journal-title":"Glycobiology"},{"issue":"1","key":"421_CR22","doi-asserted-by":"publisher","first-page":"1785","DOI":"10.1038\/s41467-019-09809-3","volume":"10","author":"W Tian","year":"2019","unstructured":"Tian W, Ye Z, Wang S, Schulz MA, Van Coillie J, Sun L, et\u00a0al. The glycosylation design space for recombinant lysosomal replacement enzymes produced in CHO cells. Nat Commun. 2019;10(1):1785.","journal-title":"Nat Commun"},{"key":"421_CR23","doi-asserted-by":"publisher","first-page":"941","DOI":"10.2147\/DDDT.S188171","volume":"13","author":"JM Teare","year":"2019","unstructured":"Teare JM, Kates DS, Shah A, Garger S. Increased branching and sialylation of N-linked glycans correlate with an improved pharmacokinetic profile for BAY 81\u20138973 compared with other full-length rFVIII products. Drug Des Dev Ther. 2019;13:941\u20138.","journal-title":"Drug Des Dev Ther"},{"issue":"1","key":"421_CR24","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1086\/316953","volume":"68","author":"YA Ioannou","year":"2001","unstructured":"Ioannou YA, Zeidner KM, Gordon RE, Desnick RJ. Fabry disease: preclinical studies demonstrate the effectiveness of alpha-galactosidase A replacement in enzyme-deficient mice. Am J Hum Genet. 2001;68(1):14\u201325.","journal-title":"Am J Hum Genet"},{"issue":"8","key":"421_CR25","doi-asserted-by":"publisher","first-page":"2812","DOI":"10.1073\/pnas.0712309105","volume":"105","author":"JM Aerts","year":"2008","unstructured":"Aerts JM, Groener JE, Kuiper S, Donker-Koopman WE, Strijland A, Ottenhoff R, et\u00a0al. Elevated globotriaosylsphingosine is a hallmark of Fabry disease. Proc Natl Acad Sci U S A. 2008;105(8):2812\u20137.","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"1\u20132","key":"421_CR26","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1016\/j.ymgme.2018.07.009","volume":"125","author":"H Morimoto","year":"2018","unstructured":"Morimoto H, Ito Y, Yoden E, Horie M, Tanaka N, Komurasaki Y, et\u00a0al. Non-clinical evaluation of JR-051 as a biosimilar to agalsidase beta for the treatment of Fabry disease. Mol Genet Metab. 2018;125(1\u20132):153\u201360.","journal-title":"Mol Genet Metab"},{"issue":"3","key":"421_CR27","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1016\/j.ymgme.2013.12.296","volume":"111","author":"T Togawa","year":"2014","unstructured":"Togawa T, Takada M, Aizawa Y, Tsukimura T, Chiba Y, Sakuraba H. Comparative study on mannose 6-phosphate residue contents of recombinant lysosomal enzymes. Mol Genet Metab. 2014;111(3):369\u201373.","journal-title":"Mol Genet Metab"},{"issue":"12","key":"421_CR28","doi-asserted-by":"publisher","first-page":"2025","DOI":"10.1021\/bc400365a","volume":"24","author":"Q Zhou","year":"2013","unstructured":"Zhou Q, Avila LZ, Konowicz PA, Harrahy J, Finn P, Kim J, et\u00a0al. Glycan structure determinants for cation-independent mannose 6-phosphate receptor binding and cellular uptake of a recombinant protein. Bioconjug Chem. 2013;24(12):2025\u201335.","journal-title":"Bioconjug Chem"},{"issue":"38","key":"421_CR29","doi-asserted-by":"publisher","first-page":"12472","DOI":"10.1021\/jacs.6b05762","volume":"138","author":"T Yamaguchi","year":"2016","unstructured":"Yamaguchi T, Amin MN, Toonstra C, Wang LX. Chemoenzymatic synthesis and receptor binding of mannose-6-phosphate (M6P)-containing glycoprotein ligands reveal unusual structural requirements for M6P receptor recognition. J Am Chem Soc. 2016;138(38):12472\u201385.","journal-title":"J Am Chem Soc"}],"container-title":["Drugs in R&D"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s40268-023-00421-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s40268-023-00421-x\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s40268-023-00421-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,12,11]],"date-time":"2023-12-11T06:00:55Z","timestamp":1702274455000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s40268-023-00421-x"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,21]]},"references-count":29,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2023,6]]}},"alternative-id":["421"],"URL":"https:\/\/doi.org\/10.1007\/s40268-023-00421-x","relation":{},"ISSN":["1174-5886","1179-6901"],"issn-type":[{"value":"1174-5886","type":"print"},{"value":"1179-6901","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,21]]},"assertion":[{"value":"29 March 2023","order":1,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 April 2023","order":2,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"This work is funded by Biosidus in collaboration with Pharmagister and the platform Medicine for Society for which funding is provided by the Vriendenloterij. None of the funders had any influence on the analysis and interpretation of the data.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Funding"}},{"value":"Ana Travella, Melisa Jacobs, Lucas D. Gentillini, Marcelo Criscuolo, and Mariana Papouchado are employed by Biosidus, which manufactures AGABIO. The remaining authors declare no conflict of interest.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflicts of interest"}},{"value":"The datasets generated during and\/or analyzed during the current study are available from the corresponding author on reasonable request.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Availability of data and material"}},{"value":"Written informed consent was obtained to use patients fibroblasts for the study as part of our biobanking protocol, approved by the Ethics Committee.","order":5,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}},{"value":"Not applicable.","order":6,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to participate"}},{"value":"Not applicable.","order":7,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"Not applicable.","order":8,"name":"Ethics","group":{"name":"EthicsHeading","label":"Code availability"}},{"value":"Andr\u00e9 B. P. van Kuilenburg, Carla E. M. Hollak, Marcelo Criscuolo and Mariana Papouchado designed the study. Ana Travella, Melisa Jacobs, Lucas D. Gentillini, Ren\u00e9 Leen, Karen M. M. Ghauharali-van der Vlugt, Femke S. Beers Stet, Sanne van der Veen, and Mariana Papouchado gathered the data. Andr\u00e9 B. P. van Kuilenburg, Ren\u00e9 Leen, Karen M. M. Ghauharali-van der Vlugt, Femke S. Beers Stet, Susan. M. I. Goorden, Sanne van der Veen, and Mariana Papouchado analyzed the data. Andr\u00e9 B. P. van Kuilenburg, Carla E. M. Hollak, Ren\u00e9 Leen, Karen M. M. Ghauharali-van der Vlugt, Susan. M. I. Goorden, Sanne van der Veen, Marcelo Criscuolo, and Mariana Papouchado wrote the publication. All authors read and approved the final version","order":9,"name":"Ethics","group":{"name":"EthicsHeading","label":"Author contributions"}}]}}