Design and screening of novel endosomal escape compounds that enhance functional delivery of oligonucleotides in vitro

Antisense oligonucleotides (ASOs), including splice-switching oligonucleotides (SSOs), are promising therapeutic approaches for targeting genetic defects. ASOs act in the nucleus and the cytosol to cleave mRNAs via the RNaseH1 mechanism (e.g., gapmers), while SSOs alter transcript splicing to restor...

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Main Authors: H. Yesid Estupiñán, Tom Baladi, Samantha Roudi, Michael J. Munson, Jeremy Bost, Oskar Gustafsson, Daniel Velásquez-Ramírez, Deepak Kumar Bhatt, Daniel Hagey, Dennis Hekman, Shalini Andersson, Samir EL Andaloussi, Anders Dahlén
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Molecular Therapy: Nucleic Acids
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Online Access:http://www.sciencedirect.com/science/article/pii/S2162253125000769
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author H. Yesid Estupiñán
Tom Baladi
Samantha Roudi
Michael J. Munson
Jeremy Bost
Oskar Gustafsson
Daniel Velásquez-Ramírez
Deepak Kumar Bhatt
Daniel Hagey
Dennis Hekman
Shalini Andersson
Samir EL Andaloussi
Anders Dahlén
author_facet H. Yesid Estupiñán
Tom Baladi
Samantha Roudi
Michael J. Munson
Jeremy Bost
Oskar Gustafsson
Daniel Velásquez-Ramírez
Deepak Kumar Bhatt
Daniel Hagey
Dennis Hekman
Shalini Andersson
Samir EL Andaloussi
Anders Dahlén
author_sort H. Yesid Estupiñán
collection DOAJ
description Antisense oligonucleotides (ASOs), including splice-switching oligonucleotides (SSOs), are promising therapeutic approaches for targeting genetic defects. ASOs act in the nucleus and the cytosol to cleave mRNAs via the RNaseH1 mechanism (e.g., gapmers), while SSOs alter transcript splicing to restore or inhibit protein function. RNA interference (RNAi) is another approach to down-regulate gene expression via the RISC complex. However, a major challenge is the effective delivery of these nucleic acid-based therapeutics. Recent developments focus on enhancing cellular uptake and endosomal release, including the use of small-molecule endosomal escape enhancers (EEEs) such as chloroquine. Here, we disclose a next generation of EEEs, which efficiently enhance SSOs and gapmers in vitro activity. We identify proton sponge-mediated endosomal leakage as a mechanism of action and observe, by Gene Ontology analysis on bulk RNA sequencing, that EEE treatment increased gene expression of markers associated with vesicle organization. Additionally, using primary human hepatocytes, we demonstrate that EEEs enhance small interfering RNA (siRNA) activity. Unconjugated siRNA reached similar levels of mRNA knockdown to the observed GalNAc-conjugated siRNA. Substantial GalNAc conjugated siRNA enhancement was also observed when used together with EEE. Our results indicate that these EEEs constitute a promising strategy to enhance the activity of multimodal oligonucleotide therapeutics.
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spelling doaj-art-4d9300e28e8d4152814712e1daf8deb22025-08-20T01:55:11ZengElsevierMolecular Therapy: Nucleic Acids2162-25312025-06-0136210252210.1016/j.omtn.2025.102522Design and screening of novel endosomal escape compounds that enhance functional delivery of oligonucleotides in vitroH. Yesid Estupiñán0Tom Baladi1Samantha Roudi2Michael J. Munson3Jeremy Bost4Oskar Gustafsson5Daniel Velásquez-Ramírez6Deepak Kumar Bhatt7Daniel Hagey8Dennis Hekman9Shalini Andersson10Samir EL Andaloussi11Anders Dahlén12Department of Laboratory Medicine, Karolinska Institutet, ANA Futura, Huddinge, Sweden; Departamento de Ciencias Básicas, Universidad Industrial de Santander, Bucaramanga, Colombia; Karolinska ATMP Center, ANA Futura, Huddinge, Sweden; Department of Cellular Therapy and Allogeneic Stem Cell Transplantation (CAST), Karolinska University Hospital, Huddinge, Sweden; Corresponding author: H. Yesid Estupiñán, Department of Laboratory Medicine, Karolinska Institutet, ANA Futura, Huddinge, Sweden.Discovery Sciences, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, SwedenDepartment of Laboratory Medicine, Karolinska Institutet, ANA Futura, Huddinge, Sweden; Karolinska ATMP Center, ANA Futura, Huddinge, Sweden; Department of Cellular Therapy and Allogeneic Stem Cell Transplantation (CAST), Karolinska University Hospital, Huddinge, SwedenAdvanced Drug Delivery, Pharmaceutical Sciences, BioPharmaceuticals R&D, AstraZeneca, Mölndal, SwedenDepartment of Laboratory Medicine, Karolinska Institutet, ANA Futura, Huddinge, Sweden; Karolinska ATMP Center, ANA Futura, Huddinge, Sweden; Department of Cellular Therapy and Allogeneic Stem Cell Transplantation (CAST), Karolinska University Hospital, Huddinge, SwedenDepartment of Laboratory Medicine, Karolinska Institutet, ANA Futura, Huddinge, Sweden; Karolinska ATMP Center, ANA Futura, Huddinge, Sweden; Department of Cellular Therapy and Allogeneic Stem Cell Transplantation (CAST), Karolinska University Hospital, Huddinge, SwedenDepartment of Laboratory Medicine, Karolinska Institutet, ANA Futura, Huddinge, Sweden; Karolinska ATMP Center, ANA Futura, Huddinge, Sweden; Department of Cellular Therapy and Allogeneic Stem Cell Transplantation (CAST), Karolinska University Hospital, Huddinge, SwedenDMPK, Research and Early Development Cardiovascular Renal and Metabolism, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, SwedenDepartment of Laboratory Medicine, Karolinska Institutet, ANA Futura, Huddinge, Sweden; Karolinska ATMP Center, ANA Futura, Huddinge, Sweden; Department of Cellular Therapy and Allogeneic Stem Cell Transplantation (CAST), Karolinska University Hospital, Huddinge, SwedenDMPK, Research and Early Development Cardiovascular Renal and Metabolism, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, SwedenDiscovery Sciences, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, SwedenDepartment of Laboratory Medicine, Karolinska Institutet, ANA Futura, Huddinge, Sweden; Karolinska ATMP Center, ANA Futura, Huddinge, Sweden; Department of Cellular Therapy and Allogeneic Stem Cell Transplantation (CAST), Karolinska University Hospital, Huddinge, Sweden; Corresponding author: Samir EL Andaloussi, Department of Laboratory Medicine, Karolinska Institutet, ANA Futura, Huddinge, Sweden.Discovery Sciences, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, Sweden; Corresponding author: Anders Dahlén, Discovery Sciences, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, Sweden.Antisense oligonucleotides (ASOs), including splice-switching oligonucleotides (SSOs), are promising therapeutic approaches for targeting genetic defects. ASOs act in the nucleus and the cytosol to cleave mRNAs via the RNaseH1 mechanism (e.g., gapmers), while SSOs alter transcript splicing to restore or inhibit protein function. RNA interference (RNAi) is another approach to down-regulate gene expression via the RISC complex. However, a major challenge is the effective delivery of these nucleic acid-based therapeutics. Recent developments focus on enhancing cellular uptake and endosomal release, including the use of small-molecule endosomal escape enhancers (EEEs) such as chloroquine. Here, we disclose a next generation of EEEs, which efficiently enhance SSOs and gapmers in vitro activity. We identify proton sponge-mediated endosomal leakage as a mechanism of action and observe, by Gene Ontology analysis on bulk RNA sequencing, that EEE treatment increased gene expression of markers associated with vesicle organization. Additionally, using primary human hepatocytes, we demonstrate that EEEs enhance small interfering RNA (siRNA) activity. Unconjugated siRNA reached similar levels of mRNA knockdown to the observed GalNAc-conjugated siRNA. Substantial GalNAc conjugated siRNA enhancement was also observed when used together with EEE. Our results indicate that these EEEs constitute a promising strategy to enhance the activity of multimodal oligonucleotide therapeutics.http://www.sciencedirect.com/science/article/pii/S2162253125000769MT: Oligonucleotides: Therapies and Applicationsoligonucleotidesantisensetherapeuticsmall moleculesenhancers
spellingShingle H. Yesid Estupiñán
Tom Baladi
Samantha Roudi
Michael J. Munson
Jeremy Bost
Oskar Gustafsson
Daniel Velásquez-Ramírez
Deepak Kumar Bhatt
Daniel Hagey
Dennis Hekman
Shalini Andersson
Samir EL Andaloussi
Anders Dahlén
Design and screening of novel endosomal escape compounds that enhance functional delivery of oligonucleotides in vitro
Molecular Therapy: Nucleic Acids
MT: Oligonucleotides: Therapies and Applications
oligonucleotides
antisense
therapeutic
small molecules
enhancers
title Design and screening of novel endosomal escape compounds that enhance functional delivery of oligonucleotides in vitro
title_full Design and screening of novel endosomal escape compounds that enhance functional delivery of oligonucleotides in vitro
title_fullStr Design and screening of novel endosomal escape compounds that enhance functional delivery of oligonucleotides in vitro
title_full_unstemmed Design and screening of novel endosomal escape compounds that enhance functional delivery of oligonucleotides in vitro
title_short Design and screening of novel endosomal escape compounds that enhance functional delivery of oligonucleotides in vitro
title_sort design and screening of novel endosomal escape compounds that enhance functional delivery of oligonucleotides in vitro
topic MT: Oligonucleotides: Therapies and Applications
oligonucleotides
antisense
therapeutic
small molecules
enhancers
url http://www.sciencedirect.com/science/article/pii/S2162253125000769
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