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

Author

Listed:
  • Yue Sun

    (Nanyang Technological University)

  • Xi Wu

    (Nanyang Technological University)

  • Jianguo Li

    (Technology and Research
    Singapore Eye Research Institute)

  • Milad Radiom

    (ETH Zurich)

  • Raffaele Mezzenga

    (Nanyang Technological University
    ETH Zurich
    ETH Zurich)

  • Chandra Shekhar Verma

    (Technology and Research
    National University of Singapore
    Nanyang Technological University)

  • Jing Yu

    (Nanyang Technological University
    Nanyang Technological University)

  • Ali Miserez

    (Nanyang Technological University
    Nanyang Technological University)

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.

Suggested Citation

  • Yue Sun & Xi Wu & Jianguo Li & Milad Radiom & Raffaele Mezzenga & Chandra Shekhar Verma & Jing Yu & Ali Miserez, 2024. "Phase-separating peptide coacervates with programmable material properties for universal intracellular delivery of macromolecules," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54463-z
    DOI: 10.1038/s41467-024-54463-z
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    References listed on IDEAS

    as
    1. Yuri Hong & Saeed Najafi & Thomas Casey & Joan-Emma Shea & Song-I Han & Dong Soo Hwang, 2022. "Hydrophobicity of arginine leads to reentrant liquid-liquid phase separation behaviors of arginine-rich proteins," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Bartosz Gabryelczyk & Hao Cai & Xiangyan Shi & Yue Sun & Piet J. M. Swinkels & Stefan Salentinig & Konstantin Pervushin & Ali Miserez, 2019. "Hydrogen bond guidance and aromatic stacking drive liquid-liquid phase separation of intrinsically disordered histidine-rich peptides," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    3. Rachel S. Fisher & Shana Elbaum-Garfinkle, 2020. "Tunable multiphase dynamics of arginine and lysine liquid condensates," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
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