Phase-separating peptide coacervates with programmable material properties for universal intracellular delivery of macromolecules

Abstract Phase-separating peptides (PSPs) self-assembling into coacervate microdroplets (CMs) are a promising class of intracellular delivery vehicles that can release macromolecular modalities deployed in a wide range of therapeutic treatments. However, the molecular grammar governing intracellular...

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Main Authors: Yue Sun, Xi Wu, Jianguo Li, Milad Radiom, Raffaele Mezzenga, Chandra Shekhar Verma, Jing Yu, Ali Miserez
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54463-z
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author Yue Sun
Xi Wu
Jianguo Li
Milad Radiom
Raffaele Mezzenga
Chandra Shekhar Verma
Jing Yu
Ali Miserez
author_facet Yue Sun
Xi Wu
Jianguo Li
Milad Radiom
Raffaele Mezzenga
Chandra Shekhar Verma
Jing Yu
Ali Miserez
author_sort Yue Sun
collection DOAJ
description Abstract Phase-separating peptides (PSPs) self-assembling into coacervate microdroplets (CMs) are a promising class of intracellular delivery vehicles that can release macromolecular modalities deployed in a wide range of therapeutic treatments. However, the molecular grammar governing intracellular uptake and release kinetics of CMs remains elusive. Here, we systematically manipulate the sequence of PSPs to unravel the relationships between their molecular structure, the physical properties of the resulting CMs, and their delivery efficacy. We show that a few amino acid alterations are sufficient to modulate the viscoelastic properties of CMs towards either a gel-like or a liquid-like state as well as their binding interaction with cellular membranes, collectively enabling to tune the kinetics of intracellular cargo release. We also demonstrate that the optimized PSPs CMs display excellent transfection efficiency in hard-to-transfect cells such as primary fibroblasts and immune cells. Our findings provide molecular guidelines to precisely program the material properties of PSP CMs and achieve tunable cellular uptake and release kinetics depending on the cargo modality, with broad implications for therapeutic applications such as protein, gene, and immune cell therapies.
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spelling doaj-art-025186c4a62443c190893e10c828c7cf2024-11-24T12:34:59ZengNature PortfolioNature Communications2041-17232024-11-0115111510.1038/s41467-024-54463-zPhase-separating peptide coacervates with programmable material properties for universal intracellular delivery of macromoleculesYue Sun0Xi Wu1Jianguo Li2Milad Radiom3Raffaele Mezzenga4Chandra Shekhar Verma5Jing Yu6Ali Miserez7Center for Sustainable Materials (SusMat), School of Materials Science and Engineering, Nanyang Technological UniversityCenter for Sustainable Materials (SusMat), School of Materials Science and Engineering, Nanyang Technological UniversityBioinformatics Institute, Agency for Science, Technology and ResearchDepartment of Health Sciences & Technology, ETH ZurichCenter for Sustainable Materials (SusMat), School of Materials Science and Engineering, Nanyang Technological UniversityBioinformatics Institute, Agency for Science, Technology and ResearchCenter for Sustainable Materials (SusMat), School of Materials Science and Engineering, Nanyang Technological UniversityCenter for Sustainable Materials (SusMat), School of Materials Science and Engineering, Nanyang Technological UniversityAbstract Phase-separating peptides (PSPs) self-assembling into coacervate microdroplets (CMs) are a promising class of intracellular delivery vehicles that can release macromolecular modalities deployed in a wide range of therapeutic treatments. However, the molecular grammar governing intracellular uptake and release kinetics of CMs remains elusive. Here, we systematically manipulate the sequence of PSPs to unravel the relationships between their molecular structure, the physical properties of the resulting CMs, and their delivery efficacy. We show that a few amino acid alterations are sufficient to modulate the viscoelastic properties of CMs towards either a gel-like or a liquid-like state as well as their binding interaction with cellular membranes, collectively enabling to tune the kinetics of intracellular cargo release. We also demonstrate that the optimized PSPs CMs display excellent transfection efficiency in hard-to-transfect cells such as primary fibroblasts and immune cells. Our findings provide molecular guidelines to precisely program the material properties of PSP CMs and achieve tunable cellular uptake and release kinetics depending on the cargo modality, with broad implications for therapeutic applications such as protein, gene, and immune cell therapies.https://doi.org/10.1038/s41467-024-54463-z
spellingShingle Yue Sun
Xi Wu
Jianguo Li
Milad Radiom
Raffaele Mezzenga
Chandra Shekhar Verma
Jing Yu
Ali Miserez
Phase-separating peptide coacervates with programmable material properties for universal intracellular delivery of macromolecules
Nature Communications
title Phase-separating peptide coacervates with programmable material properties for universal intracellular delivery of macromolecules
title_full Phase-separating peptide coacervates with programmable material properties for universal intracellular delivery of macromolecules
title_fullStr Phase-separating peptide coacervates with programmable material properties for universal intracellular delivery of macromolecules
title_full_unstemmed Phase-separating peptide coacervates with programmable material properties for universal intracellular delivery of macromolecules
title_short Phase-separating peptide coacervates with programmable material properties for universal intracellular delivery of macromolecules
title_sort phase separating peptide coacervates with programmable material properties for universal intracellular delivery of macromolecules
url https://doi.org/10.1038/s41467-024-54463-z
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