Cell-Based Small-Molecule Screening Identifying Proteostasis Regulators Enhancing Factor VIII Missense Mutant Secretion

Missense mutations are the most prevalent alterations in genetic disorders such as hemophilia A (HA), which results from coagulation factor VIII (FVIII) deficiencies. These mutations disrupt protein biosynthesis, folding, secretion, and function. Current treatments for HA are extremely expensive and...

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Main Authors: Vishal Srivastava, Zhigang Liu, Wei Wei, Yuan Zhang, James C. Paton, Adrienne W. Paton, Tingwei Mu, Bin Zhang
Format: Article
Language:English
Published: MDPI AG 2025-03-01
Series:Biomolecules
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Online Access:https://www.mdpi.com/2218-273X/15/4/458
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author Vishal Srivastava
Zhigang Liu
Wei Wei
Yuan Zhang
James C. Paton
Adrienne W. Paton
Tingwei Mu
Bin Zhang
author_facet Vishal Srivastava
Zhigang Liu
Wei Wei
Yuan Zhang
James C. Paton
Adrienne W. Paton
Tingwei Mu
Bin Zhang
author_sort Vishal Srivastava
collection DOAJ
description Missense mutations are the most prevalent alterations in genetic disorders such as hemophilia A (HA), which results from coagulation factor VIII (FVIII) deficiencies. These mutations disrupt protein biosynthesis, folding, secretion, and function. Current treatments for HA are extremely expensive and inconvenient for patients. Small molecule drugs offer a promising alternative or adjunctive strategy due to their lower cost and ease of administration, enhancing accessibility and patient compliance. By screening drug/chemical libraries with cells stably expressing FVIII–Gaussia luciferase fusion proteins, we identified compounds that enhance FVIII secretion and activity. Among these, suberoylanilide hydroxamic acid (SAHA) improved the secretion and activity of wild-type FVIII and common HA-associated missense mutants, especially mild and moderate ones. SAHA increased FVIII interaction with the endoplasmic reticulum chaperone BiP/GRP78 but not with calreticulin. Lowering cellular BiP levels decreased SAHA-induced FVIII secretion and enhancing BiP expression increased FVIII secretion. SAHA also enhanced secretion and BiP interactions with individual domains of FVIII. In vivo, treating mice with SAHA or a BiP activator boosted endogenous FVIII activity. These findings suggest that SAHA serves as a proteostasis regulator, providing a novel therapeutic approach to improve the secretion and functionality of FVIII missense mutants prone to misfolding.
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spelling doaj-art-d9bfdc97ef5f4afeaa4bed1ddebfcdb32025-08-20T03:14:15ZengMDPI AGBiomolecules2218-273X2025-03-0115445810.3390/biom15040458Cell-Based Small-Molecule Screening Identifying Proteostasis Regulators Enhancing Factor VIII Missense Mutant SecretionVishal Srivastava0Zhigang Liu1Wei Wei2Yuan Zhang3James C. Paton4Adrienne W. Paton5Tingwei Mu6Bin Zhang7Genomic Medicine Institute, Cleveland Clinic Lerner Research Institute, Cleveland, OH 44195, USAGenomic Medicine Institute, Cleveland Clinic Lerner Research Institute, Cleveland, OH 44195, USAGenomic Medicine Institute, Cleveland Clinic Lerner Research Institute, Cleveland, OH 44195, USAGenomic Medicine Institute, Cleveland Clinic Lerner Research Institute, Cleveland, OH 44195, USAResearch Centre for Infectious Diseases, Department of Molecular and Biomedical Science, University of Adelaide, Adelaide, SA 5005, AustraliaResearch Centre for Infectious Diseases, Department of Molecular and Biomedical Science, University of Adelaide, Adelaide, SA 5005, AustraliaDepartment of Physiology and Biophysics, Case Western Reserve University School of Medicine, Cleveland, OH 44106, USAGenomic Medicine Institute, Cleveland Clinic Lerner Research Institute, Cleveland, OH 44195, USAMissense mutations are the most prevalent alterations in genetic disorders such as hemophilia A (HA), which results from coagulation factor VIII (FVIII) deficiencies. These mutations disrupt protein biosynthesis, folding, secretion, and function. Current treatments for HA are extremely expensive and inconvenient for patients. Small molecule drugs offer a promising alternative or adjunctive strategy due to their lower cost and ease of administration, enhancing accessibility and patient compliance. By screening drug/chemical libraries with cells stably expressing FVIII–Gaussia luciferase fusion proteins, we identified compounds that enhance FVIII secretion and activity. Among these, suberoylanilide hydroxamic acid (SAHA) improved the secretion and activity of wild-type FVIII and common HA-associated missense mutants, especially mild and moderate ones. SAHA increased FVIII interaction with the endoplasmic reticulum chaperone BiP/GRP78 but not with calreticulin. Lowering cellular BiP levels decreased SAHA-induced FVIII secretion and enhancing BiP expression increased FVIII secretion. SAHA also enhanced secretion and BiP interactions with individual domains of FVIII. In vivo, treating mice with SAHA or a BiP activator boosted endogenous FVIII activity. These findings suggest that SAHA serves as a proteostasis regulator, providing a novel therapeutic approach to improve the secretion and functionality of FVIII missense mutants prone to misfolding.https://www.mdpi.com/2218-273X/15/4/458factor VIIIsecretionVorinostatproteostasis regulatorsBiP/GRP78
spellingShingle Vishal Srivastava
Zhigang Liu
Wei Wei
Yuan Zhang
James C. Paton
Adrienne W. Paton
Tingwei Mu
Bin Zhang
Cell-Based Small-Molecule Screening Identifying Proteostasis Regulators Enhancing Factor VIII Missense Mutant Secretion
Biomolecules
factor VIII
secretion
Vorinostat
proteostasis regulators
BiP/GRP78
title Cell-Based Small-Molecule Screening Identifying Proteostasis Regulators Enhancing Factor VIII Missense Mutant Secretion
title_full Cell-Based Small-Molecule Screening Identifying Proteostasis Regulators Enhancing Factor VIII Missense Mutant Secretion
title_fullStr Cell-Based Small-Molecule Screening Identifying Proteostasis Regulators Enhancing Factor VIII Missense Mutant Secretion
title_full_unstemmed Cell-Based Small-Molecule Screening Identifying Proteostasis Regulators Enhancing Factor VIII Missense Mutant Secretion
title_short Cell-Based Small-Molecule Screening Identifying Proteostasis Regulators Enhancing Factor VIII Missense Mutant Secretion
title_sort cell based small molecule screening identifying proteostasis regulators enhancing factor viii missense mutant secretion
topic factor VIII
secretion
Vorinostat
proteostasis regulators
BiP/GRP78
url https://www.mdpi.com/2218-273X/15/4/458
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