Novel Endogenous Engineering Platform for Robust Loading and Delivery of Functional mRNA by Extracellular Vesicles

Abstract Messenger RNA (mRNA) has emerged as an attractive therapeutic molecule for a plethora of clinical applications. For in vivo functionality, mRNA therapeutics require encapsulation into effective, stable, and safe delivery systems to protect the cargo from degradation and reduce immunogenicit...

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Main Authors: Antje M. Zickler, Xiuming Liang, Dhanu Gupta, Doste R. Mamand, Mariacristina De Luca, Giulia Corso, Lorenzo Errichelli, Justin Hean, Titash Sen, Omnia M. Elsharkasy, Noriyasu Kamei, Zheyu Niu, Guannan Zhou, Houze Zhou, Samantha Roudi, Oscar P. B. Wiklander, André Görgens, Joel Z. Nordin, Virginia Castilla‐Llorente, Samir EL Andaloussi
Format: Article
Language:English
Published: Wiley 2024-11-01
Series:Advanced Science
Subjects:
Online Access:https://doi.org/10.1002/advs.202407619
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author Antje M. Zickler
Xiuming Liang
Dhanu Gupta
Doste R. Mamand
Mariacristina De Luca
Giulia Corso
Lorenzo Errichelli
Justin Hean
Titash Sen
Omnia M. Elsharkasy
Noriyasu Kamei
Zheyu Niu
Guannan Zhou
Houze Zhou
Samantha Roudi
Oscar P. B. Wiklander
André Görgens
Joel Z. Nordin
Virginia Castilla‐Llorente
Samir EL Andaloussi
author_facet Antje M. Zickler
Xiuming Liang
Dhanu Gupta
Doste R. Mamand
Mariacristina De Luca
Giulia Corso
Lorenzo Errichelli
Justin Hean
Titash Sen
Omnia M. Elsharkasy
Noriyasu Kamei
Zheyu Niu
Guannan Zhou
Houze Zhou
Samantha Roudi
Oscar P. B. Wiklander
André Görgens
Joel Z. Nordin
Virginia Castilla‐Llorente
Samir EL Andaloussi
author_sort Antje M. Zickler
collection DOAJ
description Abstract Messenger RNA (mRNA) has emerged as an attractive therapeutic molecule for a plethora of clinical applications. For in vivo functionality, mRNA therapeutics require encapsulation into effective, stable, and safe delivery systems to protect the cargo from degradation and reduce immunogenicity. Here, a bioengineering platform for efficient mRNA loading and functional delivery using bionormal nanoparticles, extracellular vesicles (EVs), is established by expressing a highly specific RNA‐binding domain fused to CD63 in EV producer cells stably expressing the target mRNA. The additional combination with a fusogenic endosomal escape moiety, Vesicular Stomatitis Virus Glycoprotein, enables functional mRNA delivery in vivo at doses substantially lower than currently used clinically with synthetic lipid‐based nanoparticles. Importantly, the application of EVs loaded with effective cancer immunotherapy proves highly effective in an aggressive melanoma mouse model. This technology addresses substantial drawbacks currently associated with EV‐based nucleic acid delivery systems and is a leap forward to clinical EV applications.
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spelling doaj-art-57285ee9b4914259979d9194d408bdbc2025-08-20T01:51:14ZengWileyAdvanced Science2198-38442024-11-011142n/an/a10.1002/advs.202407619Novel Endogenous Engineering Platform for Robust Loading and Delivery of Functional mRNA by Extracellular VesiclesAntje M. Zickler0Xiuming Liang1Dhanu Gupta2Doste R. Mamand3Mariacristina De Luca4Giulia Corso5Lorenzo Errichelli6Justin Hean7Titash Sen8Omnia M. Elsharkasy9Noriyasu Kamei10Zheyu Niu11Guannan Zhou12Houze Zhou13Samantha Roudi14Oscar P. B. Wiklander15André Görgens16Joel Z. Nordin17Virginia Castilla‐Llorente18Samir EL Andaloussi19Division of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenEvox Therapeutics Ltd. Oxford Science Park Medawar Centre Robert Robinson Avenue Oxford OX4 4HG UKDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenEvox Therapeutics Ltd. Oxford Science Park Medawar Centre Robert Robinson Avenue Oxford OX4 4HG UKEvox Therapeutics Ltd. Oxford Science Park Medawar Centre Robert Robinson Avenue Oxford OX4 4HG UKEvox Therapeutics Ltd. Oxford Science Park Medawar Centre Robert Robinson Avenue Oxford OX4 4HG UKDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenEvox Therapeutics Ltd. Oxford Science Park Medawar Centre Robert Robinson Avenue Oxford OX4 4HG UKDivision of Biomolecular and Cellular Medicine Department of Laboratory Medicine Karolinska Institutet ANA Futura Alfred‐Nobels‐Allé 8, Huddinge Stockholm 14152 SwedenAbstract Messenger RNA (mRNA) has emerged as an attractive therapeutic molecule for a plethora of clinical applications. For in vivo functionality, mRNA therapeutics require encapsulation into effective, stable, and safe delivery systems to protect the cargo from degradation and reduce immunogenicity. Here, a bioengineering platform for efficient mRNA loading and functional delivery using bionormal nanoparticles, extracellular vesicles (EVs), is established by expressing a highly specific RNA‐binding domain fused to CD63 in EV producer cells stably expressing the target mRNA. The additional combination with a fusogenic endosomal escape moiety, Vesicular Stomatitis Virus Glycoprotein, enables functional mRNA delivery in vivo at doses substantially lower than currently used clinically with synthetic lipid‐based nanoparticles. Importantly, the application of EVs loaded with effective cancer immunotherapy proves highly effective in an aggressive melanoma mouse model. This technology addresses substantial drawbacks currently associated with EV‐based nucleic acid delivery systems and is a leap forward to clinical EV applications.https://doi.org/10.1002/advs.202407619bioengineeringcancer immunotherapydrug deliveryextracellular vesiclesnanotechnologynucleic acid therapeutics
spellingShingle Antje M. Zickler
Xiuming Liang
Dhanu Gupta
Doste R. Mamand
Mariacristina De Luca
Giulia Corso
Lorenzo Errichelli
Justin Hean
Titash Sen
Omnia M. Elsharkasy
Noriyasu Kamei
Zheyu Niu
Guannan Zhou
Houze Zhou
Samantha Roudi
Oscar P. B. Wiklander
André Görgens
Joel Z. Nordin
Virginia Castilla‐Llorente
Samir EL Andaloussi
Novel Endogenous Engineering Platform for Robust Loading and Delivery of Functional mRNA by Extracellular Vesicles
Advanced Science
bioengineering
cancer immunotherapy
drug delivery
extracellular vesicles
nanotechnology
nucleic acid therapeutics
title Novel Endogenous Engineering Platform for Robust Loading and Delivery of Functional mRNA by Extracellular Vesicles
title_full Novel Endogenous Engineering Platform for Robust Loading and Delivery of Functional mRNA by Extracellular Vesicles
title_fullStr Novel Endogenous Engineering Platform for Robust Loading and Delivery of Functional mRNA by Extracellular Vesicles
title_full_unstemmed Novel Endogenous Engineering Platform for Robust Loading and Delivery of Functional mRNA by Extracellular Vesicles
title_short Novel Endogenous Engineering Platform for Robust Loading and Delivery of Functional mRNA by Extracellular Vesicles
title_sort novel endogenous engineering platform for robust loading and delivery of functional mrna by extracellular vesicles
topic bioengineering
cancer immunotherapy
drug delivery
extracellular vesicles
nanotechnology
nucleic acid therapeutics
url https://doi.org/10.1002/advs.202407619
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