Drug screening identifies tazarotene and bexarotene as therapeutic agents in multiple sulfatase deficiency

Abstract Multiple sulfatase deficiency (MSD, MIM #272200) results from pathogenic variants in the SUMF1 gene that impair proper function of the formylglycine‐generating enzyme (FGE). FGE is essential for the posttranslational activation of cellular sulfatases. MSD patients display reduced or absent...

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Main Authors: Lars Schlotawa, Karolina Tyka, Matthias Kettwig, Rebecca C Ahrens‐Nicklas, Matthias Baud, Tea Berulava, Nicola Brunetti‐Pierri, Alyssa Gagne, Zackary M Herbst, Jean A Maguire, Jlenia Monfregola, Tonatiuh Pena, Karthikeyan Radhakrishnan, Sophie Schröder, Elisa A Waxman, Andrea Ballabio, Thomas Dierks, André Fischer, Deborah L French, Michael H Gelb, Jutta Gärtner
Format: Article
Language:English
Published: Springer Nature 2023-02-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.202114837
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author Lars Schlotawa
Karolina Tyka
Matthias Kettwig
Rebecca C Ahrens‐Nicklas
Matthias Baud
Tea Berulava
Nicola Brunetti‐Pierri
Alyssa Gagne
Zackary M Herbst
Jean A Maguire
Jlenia Monfregola
Tonatiuh Pena
Karthikeyan Radhakrishnan
Sophie Schröder
Elisa A Waxman
Andrea Ballabio
Thomas Dierks
André Fischer
Deborah L French
Michael H Gelb
Jutta Gärtner
author_facet Lars Schlotawa
Karolina Tyka
Matthias Kettwig
Rebecca C Ahrens‐Nicklas
Matthias Baud
Tea Berulava
Nicola Brunetti‐Pierri
Alyssa Gagne
Zackary M Herbst
Jean A Maguire
Jlenia Monfregola
Tonatiuh Pena
Karthikeyan Radhakrishnan
Sophie Schröder
Elisa A Waxman
Andrea Ballabio
Thomas Dierks
André Fischer
Deborah L French
Michael H Gelb
Jutta Gärtner
author_sort Lars Schlotawa
collection DOAJ
description Abstract Multiple sulfatase deficiency (MSD, MIM #272200) results from pathogenic variants in the SUMF1 gene that impair proper function of the formylglycine‐generating enzyme (FGE). FGE is essential for the posttranslational activation of cellular sulfatases. MSD patients display reduced or absent sulfatase activities and, as a result, clinical signs of single sulfatase disorders in a unique combination. Up to date therapeutic options for MSD are limited and mostly palliative. We performed a screen of FDA‐approved drugs using immortalized MSD patient fibroblasts. Recovery of arylsulfatase A activity served as the primary readout. Subsequent analysis confirmed that treatment of primary MSD fibroblasts with tazarotene and bexarotene, two retinoids, led to a correction of MSD pathophysiology. Upon treatment, sulfatase activities increased in a dose‐ and time‐dependent manner, reduced glycosaminoglycan content decreased and lysosomal position and size normalized. Treatment of MSD patient derived induced pluripotent stem cells (iPSC) differentiated into neuronal progenitor cells (NPC) resulted in a positive treatment response. Tazarotene and bexarotene act to ultimately increase the stability of FGE variants. The results lay the basis for future research on the development of a first therapeutic option for MSD patients. 
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spelling doaj-art-b678e69f8129428e87e0aebc0aa61cd42025-08-24T11:43:22ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842023-02-0115312110.15252/emmm.202114837Drug screening identifies tazarotene and bexarotene as therapeutic agents in multiple sulfatase deficiencyLars Schlotawa0Karolina Tyka1Matthias Kettwig2Rebecca C Ahrens‐Nicklas3Matthias Baud4Tea Berulava5Nicola Brunetti‐Pierri6Alyssa Gagne7Zackary M Herbst8Jean A Maguire9Jlenia Monfregola10Tonatiuh Pena11Karthikeyan Radhakrishnan12Sophie Schröder13Elisa A Waxman14Andrea Ballabio15Thomas Dierks16André Fischer17Deborah L French18Michael H Gelb19Jutta Gärtner20Department of Paediatrics and Adolescent Medicine, University Medical Centre GöttingenDepartment of Paediatrics and Adolescent Medicine, University Medical Centre GöttingenDepartment of Paediatrics and Adolescent Medicine, University Medical Centre GöttingenDivision of Human Genetics and Metabolism, The Children's Hospital of PhiladelphiaSchool of Chemistry and Institute for Life Sciences, University of SouthamptonDepartment for Epigenetics and Systems Medicine in Neurodegenerative Diseases, German Centre for Neurodegenerative DiseasesTelethon Institute of Genetics and MedicineCenter for Cellular and Molecular Therapeutics, The Children's Hospital of PhiladelphiaDepartment of Chemistry, University of WashingtonCenter for Cellular and Molecular Therapeutics, The Children's Hospital of PhiladelphiaTelethon Institute of Genetics and MedicineDepartment for Epigenetics and Systems Medicine in Neurodegenerative Diseases, German Centre for Neurodegenerative DiseasesFaculty of Chemistry, Biochemistry I, Bielefeld UniversityDepartment for Epigenetics and Systems Medicine in Neurodegenerative Diseases, German Centre for Neurodegenerative DiseasesCenter for Cellular and Molecular Therapeutics, The Children's Hospital of PhiladelphiaTelethon Institute of Genetics and MedicineFaculty of Chemistry, Biochemistry I, Bielefeld UniversityDepartment for Epigenetics and Systems Medicine in Neurodegenerative Diseases, German Centre for Neurodegenerative DiseasesCenter for Cellular and Molecular Therapeutics, The Children's Hospital of PhiladelphiaDepartment of Chemistry, University of WashingtonDepartment of Paediatrics and Adolescent Medicine, University Medical Centre GöttingenAbstract Multiple sulfatase deficiency (MSD, MIM #272200) results from pathogenic variants in the SUMF1 gene that impair proper function of the formylglycine‐generating enzyme (FGE). FGE is essential for the posttranslational activation of cellular sulfatases. MSD patients display reduced or absent sulfatase activities and, as a result, clinical signs of single sulfatase disorders in a unique combination. Up to date therapeutic options for MSD are limited and mostly palliative. We performed a screen of FDA‐approved drugs using immortalized MSD patient fibroblasts. Recovery of arylsulfatase A activity served as the primary readout. Subsequent analysis confirmed that treatment of primary MSD fibroblasts with tazarotene and bexarotene, two retinoids, led to a correction of MSD pathophysiology. Upon treatment, sulfatase activities increased in a dose‐ and time‐dependent manner, reduced glycosaminoglycan content decreased and lysosomal position and size normalized. Treatment of MSD patient derived induced pluripotent stem cells (iPSC) differentiated into neuronal progenitor cells (NPC) resulted in a positive treatment response. Tazarotene and bexarotene act to ultimately increase the stability of FGE variants. The results lay the basis for future research on the development of a first therapeutic option for MSD patients. https://doi.org/10.15252/emmm.202114837drug screeningformylglycine‐generating enzymelysosomal disorderretinoidssulfatase‐modifying factor 1
spellingShingle Lars Schlotawa
Karolina Tyka
Matthias Kettwig
Rebecca C Ahrens‐Nicklas
Matthias Baud
Tea Berulava
Nicola Brunetti‐Pierri
Alyssa Gagne
Zackary M Herbst
Jean A Maguire
Jlenia Monfregola
Tonatiuh Pena
Karthikeyan Radhakrishnan
Sophie Schröder
Elisa A Waxman
Andrea Ballabio
Thomas Dierks
André Fischer
Deborah L French
Michael H Gelb
Jutta Gärtner
Drug screening identifies tazarotene and bexarotene as therapeutic agents in multiple sulfatase deficiency
EMBO Molecular Medicine
drug screening
formylglycine‐generating enzyme
lysosomal disorder
retinoids
sulfatase‐modifying factor 1
title Drug screening identifies tazarotene and bexarotene as therapeutic agents in multiple sulfatase deficiency
title_full Drug screening identifies tazarotene and bexarotene as therapeutic agents in multiple sulfatase deficiency
title_fullStr Drug screening identifies tazarotene and bexarotene as therapeutic agents in multiple sulfatase deficiency
title_full_unstemmed Drug screening identifies tazarotene and bexarotene as therapeutic agents in multiple sulfatase deficiency
title_short Drug screening identifies tazarotene and bexarotene as therapeutic agents in multiple sulfatase deficiency
title_sort drug screening identifies tazarotene and bexarotene as therapeutic agents in multiple sulfatase deficiency
topic drug screening
formylglycine‐generating enzyme
lysosomal disorder
retinoids
sulfatase‐modifying factor 1
url https://doi.org/10.15252/emmm.202114837
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