Identification of tyrosine sulfation in the variable region of a bispecific antibody and its effect on stability and biological activity

Despite tyrosine sulfation being a relatively common post-translational modification (PTM) on the secreted proteins of higher eukaryotic organisms, there have been surprisingly few reports of this modification occurring in recombinant monoclonal antibodies (mAbs) expressed by mammalian cell lines an...

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Main Authors: Christopher B. Lietz, Ekaterina Deyanova, Younhee Cho, Jon Cordia, Sarah Franc, Sally Kabro, Steven Wang, David Mikolon, Douglas D. Banks
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:mAbs
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Online Access:https://www.tandfonline.com/doi/10.1080/19420862.2023.2259289
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author Christopher B. Lietz
Ekaterina Deyanova
Younhee Cho
Jon Cordia
Sarah Franc
Sally Kabro
Steven Wang
David Mikolon
Douglas D. Banks
author_facet Christopher B. Lietz
Ekaterina Deyanova
Younhee Cho
Jon Cordia
Sarah Franc
Sally Kabro
Steven Wang
David Mikolon
Douglas D. Banks
author_sort Christopher B. Lietz
collection DOAJ
description Despite tyrosine sulfation being a relatively common post-translational modification (PTM) on the secreted proteins of higher eukaryotic organisms, there have been surprisingly few reports of this modification occurring in recombinant monoclonal antibodies (mAbs) expressed by mammalian cell lines and even less information regarding its potential impact on mAb efficacy and stability. This discrepancy is likely due to the extreme lability of this modification using many of the mass spectrometry methods typically used within the biopharmaceutical industry for PTM identification, as well as the possible misidentification as phosphorylation. Here, we identified sulfation on a single tyrosine residue located within the identical variable region sequence of a 2 + 1 bispecific mAbs heavy and heavy-heavy chains using a multi-enzymatic approach in combination with mass spectrometry analysis and examined its impact on binding, efficacy, and physical stability. Unlike previous reports, we found that tyrosine sulfation modestly decreased the mAb cell binding and T cell-mediated killing, primarily by increasing the rate of antigen disassociation as determined from surface plasmon resonance-binding experiments. We also found that, while this acidic modification had no significant impact on the mAb thermal stability, sulfation did modestly increase its rate of aggregation, presumably by lowering the mAb’s colloidal stability as indicated by polyethylene glycol induced liquid–liquid phase separation experiments.
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spelling doaj-art-4708d09120bb4b4ebcea29f7c90344fa2025-08-20T02:47:49ZengTaylor & Francis GroupmAbs1942-08621942-08702023-12-0115110.1080/19420862.2023.2259289Identification of tyrosine sulfation in the variable region of a bispecific antibody and its effect on stability and biological activityChristopher B. Lietz0Ekaterina Deyanova1Younhee Cho2Jon Cordia3Sarah Franc4Sally Kabro5Steven Wang6David Mikolon7Douglas D. Banks8Department of Pharmaceutical Candidate Optimization - DMPK, Bristol Myers Squibb, San Diego, CA, USADepartment of Pharmaceutical Candidate Optimization - DPAS, Bristol Myers Squibb, Lawrenceville, NJ, USADepartment of Pharmaceutical Candidate Optimization - DPAS, Bristol Myers Squibb, San Diego, CA, USADepartment of Pharmaceutical Candidate Optimization - DPAS, Bristol Myers Squibb, San Diego, CA, USADepartment of Pharmaceutical Candidate Optimization - DPAS, Bristol Myers Squibb, San Diego, CA, USADepartment of Pharmaceutical Candidate Optimization - DPAS, Bristol Myers Squibb, San Diego, CA, USADepartment of Pharmaceutical Candidate Optimization - DPAS, Bristol Myers Squibb, San Diego, CA, USADepartment of Biotherapeutics, Bristol Myers Squibb, San Diego, CA, USADepartment of Pharmaceutical Candidate Optimization - DPAS, Bristol Myers Squibb, San Diego, CA, USADespite tyrosine sulfation being a relatively common post-translational modification (PTM) on the secreted proteins of higher eukaryotic organisms, there have been surprisingly few reports of this modification occurring in recombinant monoclonal antibodies (mAbs) expressed by mammalian cell lines and even less information regarding its potential impact on mAb efficacy and stability. This discrepancy is likely due to the extreme lability of this modification using many of the mass spectrometry methods typically used within the biopharmaceutical industry for PTM identification, as well as the possible misidentification as phosphorylation. Here, we identified sulfation on a single tyrosine residue located within the identical variable region sequence of a 2 + 1 bispecific mAbs heavy and heavy-heavy chains using a multi-enzymatic approach in combination with mass spectrometry analysis and examined its impact on binding, efficacy, and physical stability. Unlike previous reports, we found that tyrosine sulfation modestly decreased the mAb cell binding and T cell-mediated killing, primarily by increasing the rate of antigen disassociation as determined from surface plasmon resonance-binding experiments. We also found that, while this acidic modification had no significant impact on the mAb thermal stability, sulfation did modestly increase its rate of aggregation, presumably by lowering the mAb’s colloidal stability as indicated by polyethylene glycol induced liquid–liquid phase separation experiments.https://www.tandfonline.com/doi/10.1080/19420862.2023.2259289Biotherapeuticmass spectrometrymonoclonal antibodypeptide mappost-translational modificationsulfotyrosine
spellingShingle Christopher B. Lietz
Ekaterina Deyanova
Younhee Cho
Jon Cordia
Sarah Franc
Sally Kabro
Steven Wang
David Mikolon
Douglas D. Banks
Identification of tyrosine sulfation in the variable region of a bispecific antibody and its effect on stability and biological activity
mAbs
Biotherapeutic
mass spectrometry
monoclonal antibody
peptide map
post-translational modification
sulfotyrosine
title Identification of tyrosine sulfation in the variable region of a bispecific antibody and its effect on stability and biological activity
title_full Identification of tyrosine sulfation in the variable region of a bispecific antibody and its effect on stability and biological activity
title_fullStr Identification of tyrosine sulfation in the variable region of a bispecific antibody and its effect on stability and biological activity
title_full_unstemmed Identification of tyrosine sulfation in the variable region of a bispecific antibody and its effect on stability and biological activity
title_short Identification of tyrosine sulfation in the variable region of a bispecific antibody and its effect on stability and biological activity
title_sort identification of tyrosine sulfation in the variable region of a bispecific antibody and its effect on stability and biological activity
topic Biotherapeutic
mass spectrometry
monoclonal antibody
peptide map
post-translational modification
sulfotyrosine
url https://www.tandfonline.com/doi/10.1080/19420862.2023.2259289
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