PET Imaging Expedites Detection of Aberration in the Humanization of an Annexin A1 Targeting Antibody

<b>Objectives</b>: Annexin-A1 is a 37 kDa phospholipid-binding protein which is concentrated in a truncated 34 kDa form (AnnA1) in caveolae on the tumor vascular endothelial cell surface with expression in many tumor types. PRISM developed the monoclonal mouse antibody mAnnA1 against Ann...

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Main Authors: Hailey A. Houson, Brian D. Wright, Solana R. Fernandez, Tim Buss, Sharon L. White, Brittany Cederstrom, James M. Omweri, Jonathan E. McConathy, Jan E. Schnitzer, Suzanne E. Lapi
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Language:English
Published: MDPI AG 2025-02-01
Series:Pharmaceuticals
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Online Access:https://www.mdpi.com/1424-8247/18/3/295
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author Hailey A. Houson
Brian D. Wright
Solana R. Fernandez
Tim Buss
Sharon L. White
Brittany Cederstrom
James M. Omweri
Jonathan E. McConathy
Jan E. Schnitzer
Suzanne E. Lapi
author_facet Hailey A. Houson
Brian D. Wright
Solana R. Fernandez
Tim Buss
Sharon L. White
Brittany Cederstrom
James M. Omweri
Jonathan E. McConathy
Jan E. Schnitzer
Suzanne E. Lapi
author_sort Hailey A. Houson
collection DOAJ
description <b>Objectives</b>: Annexin-A1 is a 37 kDa phospholipid-binding protein which is concentrated in a truncated 34 kDa form (AnnA1) in caveolae on the tumor vascular endothelial cell surface with expression in many tumor types. PRISM developed the monoclonal mouse antibody mAnnA1 against AnnA1 for evaluation of AnnA1 as a potential target for imaging and therapy in oncology. mAnnA1 was humanized to make hAnnA1 for translation to clinical studies. Both PRISM-produced mAnnA1 and cGMP contractor-produced hAnnA1 were investigated using noninvasive PET/CT imaging, and dosimetry was evaluated to enable clinical translation of this strategy and to investigate in vivo behavior of hAnnA1. <b>Methods</b>: Antibodies mAnnA1 and hAnnA1 (PRISM “hAnnA1-P” or contractor generated “hAnnA1-C”) were conjugated with the chelator deferoxamine and evaluated for immunoreactivity with ELISA. Conjugated antibodies were radiolabeled with zirconium-89. Naïve mice, rats, and non-human primates (NHP) were injected with [<sup>89</sup>Zr]mAnnA1 or [<sup>89</sup>Zr]hAnnA1 and imaged with PET/CT up to 10 days post injection. After imaging, mice and rats were euthanized and organs were collected, weighed, and radioactivity was quantified using a gamma counter. Dosimetry in mice and NHPs were calculated using OLINDA. <b>Results</b>: [<sup>89</sup>Zr]mAnnA1 showed similar biodistribution to other antibodies with slow clearance through the liver. Transition to [<sup>89</sup>Zr]hAnnA1-C during the dosimetry studies revealed substantial uptake in the spleen (130 ± 48% ID/g at day 5 post injection in female BALB/c), which was not observed with [<sup>89</sup>Zr]mAnnA1 (5.6 ± 1.7% ID/g at day 7 PI). Further studies in multiple strains of mice showed variable elevated splenic uptake of [<sup>89</sup>Zr]hAnnA1-C across mouse strains, with the highest uptake observed in female BALB/c mice (118.4 ± 23.1% ID/g) and the lowest uptake observed in male CD1 mice (34.7 ± 10.2% ID/g). Additionally, splenic uptake of hAnnA1-C was observed in Fischer rats (2.8 ± 0.6% ID/organ) and NHPs (1.6 ± 0.6% ID/organ), although at lower levels than what was observed in BALB/c mice (8.8 ± 1.8% ID/organ). Dosimetry results showed similar values between estimates based on mouse and NHP data, with the largest difference seen in the spleen (5.2 vs. 2.6 mSv/MBq in females respectively). Sequencing of hAnnA1-C revealed a frameshift mutation in the antibody sequence introduced during cGMP manufacture. Restoration of the antibody sequence by PRISM returned the antibody distribution into alignment with mAnnA1. <b>Conclusions</b>: An aberration introduced during cGMP production of hAnnA1-C resulted in increased splenic uptake and alteration of the biodistribution in mice. PET imaging enabled quantitative detection of the immunogenic behavior of hAnnA1, which led to detection of the sequence error. Restoration of the sequence resulted in an antibody which was non-immunogenic to mice.
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spelling doaj-art-9b7b30ec4c2e4c7cb5def3339873856c2025-08-20T02:42:28ZengMDPI AGPharmaceuticals1424-82472025-02-0118329510.3390/ph18030295PET Imaging Expedites Detection of Aberration in the Humanization of an Annexin A1 Targeting AntibodyHailey A. Houson0Brian D. Wright1Solana R. Fernandez2Tim Buss3Sharon L. White4Brittany Cederstrom5James M. Omweri6Jonathan E. McConathy7Jan E. Schnitzer8Suzanne E. Lapi9Department of Radiology, University of Alabama at Birmingham, Birmingham, AL 35294, USADepartment of Radiology, University of Alabama at Birmingham, Birmingham, AL 35294, USADepartment of Radiology, University of Alabama at Birmingham, Birmingham, AL 35294, USAProteogenomics Research Institute for Systems Medicine (PRISM), La Jolla, CA 92037, USADepartment of Radiology, University of Alabama at Birmingham, Birmingham, AL 35294, USAProteogenomics Research Institute for Systems Medicine (PRISM), La Jolla, CA 92037, USADepartment of Radiology, University of Alabama at Birmingham, Birmingham, AL 35294, USADepartment of Radiology, University of Alabama at Birmingham, Birmingham, AL 35294, USAProteogenomics Research Institute for Systems Medicine (PRISM), La Jolla, CA 92037, USADepartment of Radiology, University of Alabama at Birmingham, Birmingham, AL 35294, USA<b>Objectives</b>: Annexin-A1 is a 37 kDa phospholipid-binding protein which is concentrated in a truncated 34 kDa form (AnnA1) in caveolae on the tumor vascular endothelial cell surface with expression in many tumor types. PRISM developed the monoclonal mouse antibody mAnnA1 against AnnA1 for evaluation of AnnA1 as a potential target for imaging and therapy in oncology. mAnnA1 was humanized to make hAnnA1 for translation to clinical studies. Both PRISM-produced mAnnA1 and cGMP contractor-produced hAnnA1 were investigated using noninvasive PET/CT imaging, and dosimetry was evaluated to enable clinical translation of this strategy and to investigate in vivo behavior of hAnnA1. <b>Methods</b>: Antibodies mAnnA1 and hAnnA1 (PRISM “hAnnA1-P” or contractor generated “hAnnA1-C”) were conjugated with the chelator deferoxamine and evaluated for immunoreactivity with ELISA. Conjugated antibodies were radiolabeled with zirconium-89. Naïve mice, rats, and non-human primates (NHP) were injected with [<sup>89</sup>Zr]mAnnA1 or [<sup>89</sup>Zr]hAnnA1 and imaged with PET/CT up to 10 days post injection. After imaging, mice and rats were euthanized and organs were collected, weighed, and radioactivity was quantified using a gamma counter. Dosimetry in mice and NHPs were calculated using OLINDA. <b>Results</b>: [<sup>89</sup>Zr]mAnnA1 showed similar biodistribution to other antibodies with slow clearance through the liver. Transition to [<sup>89</sup>Zr]hAnnA1-C during the dosimetry studies revealed substantial uptake in the spleen (130 ± 48% ID/g at day 5 post injection in female BALB/c), which was not observed with [<sup>89</sup>Zr]mAnnA1 (5.6 ± 1.7% ID/g at day 7 PI). Further studies in multiple strains of mice showed variable elevated splenic uptake of [<sup>89</sup>Zr]hAnnA1-C across mouse strains, with the highest uptake observed in female BALB/c mice (118.4 ± 23.1% ID/g) and the lowest uptake observed in male CD1 mice (34.7 ± 10.2% ID/g). Additionally, splenic uptake of hAnnA1-C was observed in Fischer rats (2.8 ± 0.6% ID/organ) and NHPs (1.6 ± 0.6% ID/organ), although at lower levels than what was observed in BALB/c mice (8.8 ± 1.8% ID/organ). Dosimetry results showed similar values between estimates based on mouse and NHP data, with the largest difference seen in the spleen (5.2 vs. 2.6 mSv/MBq in females respectively). Sequencing of hAnnA1-C revealed a frameshift mutation in the antibody sequence introduced during cGMP manufacture. Restoration of the antibody sequence by PRISM returned the antibody distribution into alignment with mAnnA1. <b>Conclusions</b>: An aberration introduced during cGMP production of hAnnA1-C resulted in increased splenic uptake and alteration of the biodistribution in mice. PET imaging enabled quantitative detection of the immunogenic behavior of hAnnA1, which led to detection of the sequence error. Restoration of the sequence resulted in an antibody which was non-immunogenic to mice.https://www.mdpi.com/1424-8247/18/3/295zirconium-89antibody imagingdosimetrytranslation
spellingShingle Hailey A. Houson
Brian D. Wright
Solana R. Fernandez
Tim Buss
Sharon L. White
Brittany Cederstrom
James M. Omweri
Jonathan E. McConathy
Jan E. Schnitzer
Suzanne E. Lapi
PET Imaging Expedites Detection of Aberration in the Humanization of an Annexin A1 Targeting Antibody
Pharmaceuticals
zirconium-89
antibody imaging
dosimetry
translation
title PET Imaging Expedites Detection of Aberration in the Humanization of an Annexin A1 Targeting Antibody
title_full PET Imaging Expedites Detection of Aberration in the Humanization of an Annexin A1 Targeting Antibody
title_fullStr PET Imaging Expedites Detection of Aberration in the Humanization of an Annexin A1 Targeting Antibody
title_full_unstemmed PET Imaging Expedites Detection of Aberration in the Humanization of an Annexin A1 Targeting Antibody
title_short PET Imaging Expedites Detection of Aberration in the Humanization of an Annexin A1 Targeting Antibody
title_sort pet imaging expedites detection of aberration in the humanization of an annexin a1 targeting antibody
topic zirconium-89
antibody imaging
dosimetry
translation
url https://www.mdpi.com/1424-8247/18/3/295
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