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Cytosolic Protein Delivery Using Modular Biotin–Streptavidin Assembly of Nanocomposites

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    Cytosolic Protein Delivery Using Modular Biotin–Streptavidin Assembly of Nanocomposites
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    • David C. Luther
      David C. Luther
      Department of Chemistry, University of Massachusetts Amherst, 710 North Pleasant Street, Amherst, Massachusetts 01003, United States
      More by David C. Luther
      Orcidhttps://orcid.org/0000-0002-4697-8683
    • Yi-Wei Lee
      Yi-Wei Lee
      Department of Chemistry, University of Massachusetts Amherst, 710 North Pleasant Street, Amherst, Massachusetts 01003, United States
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    • Harini Nagaraj
      Harini Nagaraj
      Department of Chemistry, University of Massachusetts Amherst, 710 North Pleasant Street, Amherst, Massachusetts 01003, United States
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      Orcidhttps://orcid.org/0000-0002-1615-9126
    • Vincent Clark
      Vincent Clark
      Department of Chemistry, University of Massachusetts Amherst, 710 North Pleasant Street, Amherst, Massachusetts 01003, United States
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      Orcidhttps://orcid.org/0000-0001-9707-8004
    • Taewon Jeon
      Taewon Jeon
      Molecular and Cellular Biology Graduate Program, University of Massachusetts Amherst, 710 North Pleasant Street, Amherst, Massachusetts 01003, United States
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      Orcidhttps://orcid.org/0000-0003-3840-5129
    • Ritabrita Goswami
      Ritabrita Goswami
      Department of Chemistry, University of Massachusetts Amherst, 710 North Pleasant Street, Amherst, Massachusetts 01003, United States
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      Orcidhttps://orcid.org/0000-0003-3812-6322
    • Sanjana Gopalakrishnan
      Sanjana Gopalakrishnan
      Department of Chemistry, University of Massachusetts Amherst, 710 North Pleasant Street, Amherst, Massachusetts 01003, United States
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    • Stefano Fedeli
      Stefano Fedeli
      Department of Chemistry, University of Massachusetts Amherst, 710 North Pleasant Street, Amherst, Massachusetts 01003, United States
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    • William Jerome
      William Jerome
      Department of Chemistry, University of Massachusetts Amherst, 710 North Pleasant Street, Amherst, Massachusetts 01003, United States
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    • James L. Elia
      James L. Elia
      Department of Chemistry, University of Massachusetts Amherst, 710 North Pleasant Street, Amherst, Massachusetts 01003, United States
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      Orcidhttps://orcid.org/0000-0003-3962-7452
    • Vincent M. Rotello*
      Vincent M. Rotello
      Department of Chemistry, University of Massachusetts Amherst, 710 North Pleasant Street, Amherst, Massachusetts 01003, United States
      *Address correspondence to [email protected]
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      Orcidhttps://orcid.org/0000-0002-5184-5439
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    ACS Nano

    Cite this: ACS Nano 2022, 16, 5, 7323–7330
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    https://doi.org/10.1021/acsnano.1c06768
    Published April 18, 2022
    Copyright © 2022 American Chemical Society
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    Abstract

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    Current strategies for the delivery of proteins into cells face general challenges of endosomal entrapment and concomitant degradation of protein cargo. Efficient delivery directly to the cytosol overcomes this obstacle: we report here the use of biotin–streptavidin tethering to provide a modular approach to the generation of nanovectors capable of a cytosolic delivery of biotinylated proteins. This strategy uses streptavidin to organize biotinylated protein and biotinylated oligo(glutamate) peptide into modular complexes that are then electrostatically self-assembled with a cationic guanidinium-functionalized polymer. The resulting polymer–protein nanocomposites demonstrate efficient cytosolic delivery of six biotinylated protein cargos of varying size, charge, and quaternary structure. Retention of protein function was established through efficient cell killing via delivery of the chemotherapeutic enzyme granzyme A. This platform represents a versatile and modular approach to intracellular delivery through the noncovalent tethering of multiple components into a single delivery vector.

    Copyright © 2022 American Chemical Society

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    Supporting Information

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    • Polymer synthesis and characterization; additional experimental details and related figures (PDF)

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    Cited By

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    This article is cited by 18 publications.

    1. Dheeraj K. Agrohia, Ritabrita Goswami, Teerapong Jantarat, Yağız Anil Çiçek, Korndanai Thongsukh, Taewon Jeon, Jonathan M. Bell, Vincent M. Rotello, Richard W. Vachet. Suborgan Level Quantitation of Proteins in Tissues Delivered by Polymeric Nanocarriers. ACS Nano 2024, 18 (26) , 16808-16818. https://doi.org/10.1021/acsnano.4c02344
    2. Maximilian A. Beach, Umeka Nayanathara, Yanting Gao, Changhe Zhang, Yijun Xiong, Yufu Wang, Georgina K. Such. Polymeric Nanoparticles for Drug Delivery. Chemical Reviews 2024, 124 (9) , 5505-5616. https://doi.org/10.1021/acs.chemrev.3c00705
    3. Santanu Shaw, Ankan Kumar Sarkar, Nikhil R. Jana. Protein Delivery to the Cytosol and Cell Nucleus via Micellar Nanocarrier-Based Nonendocytic Uptake. ACS Applied Bio Materials 2023, 6 (10) , 4200-4207. https://doi.org/10.1021/acsabm.3c00431
    4. Ankan Kumar Sarkar, Santanu Shaw, Himali Arora, Pankaj Seth, Nikhil R. Jana. Nuclear Transport of the Molecular Drug via Nanocarrier-Based Nonendocytic Cellular Uptake. ACS Applied Materials & Interfaces 2023, 15 (33) , 39176-39185. https://doi.org/10.1021/acsami.3c09241
    5. Xiang Li, Chao Pan, Caixia Li, Kangfeng Wang, Jingqin Ye, Peng Sun, Yan Guo, Jun Wu, Hengliang Wang, Li Zhu. Self-Assembled Proteinaceous Nanoparticles for Co-Delivery of Antigens and Cytosine Phosphoguanine (CpG) Adjuvants: Implications for Nanovaccines. ACS Applied Nano Materials 2023, 6 (9) , 7637-7648. https://doi.org/10.1021/acsanm.3c00787
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    7. Naomi M. Hamelmann, Sjoerd Uijttewaal, Sry D. Hujaya, Jos M. J. Paulusse. Enhancing Cellular Internalization of Single-Chain Polymer Nanoparticles via Polyplex Formation. Biomacromolecules 2022, 23 (12) , 5036-5042. https://doi.org/10.1021/acs.biomac.2c00858
    8. Kohei Shiomi, Keita Hayashi, Haruyuki Ishii, Toshiyuki Kamei, Toshinori Shimanouchi, Hidemi Nakamura, Sosaku Ichikawa. Phase-separated cationic giant unilamellar vesicles as templates for the polymerization of tetraethyl orthosilicate (TEOS). Biochimica et Biophysica Acta (BBA) - Biomembranes 2025, 1867 (2) , 184403. https://doi.org/10.1016/j.bbamem.2024.184403
    9. Lijia Liang, Xia Zhang, Feng Wang, Fengxian Wang, Xiaokang Chen, Qiao Liao, Yao Xiong, Jianjie Ma, Jing Wang, Chunyu Zeng. MG53 Protein-Mediated biomimetic nanotherapeutics for the treatment of acute myocardial infarction by driving the impaired plasma membrane resealing. Chemical Engineering Journal 2024, 500 , 157091. https://doi.org/10.1016/j.cej.2024.157091
    10. Yanwen Li, Xin Yu, Qianqian Chen, Hui Wang, Jia Lv, Yiyun Cheng. Polyresorcinols for intracellular protein delivery. Nano Today 2024, 56 , 102287. https://doi.org/10.1016/j.nantod.2024.102287
    11. Nayana Mukherjee, Ankan Kumar Sarkar, Prasanta Panja, Nikhil R. Jana. Guanidinium-terminated gold nanoparticles for protein delivery to the cell nucleus. New Journal of Chemistry 2024, 48 (15) , 6553-6556. https://doi.org/10.1039/D4NJ00370E
    12. Subhamoy Banerjee, Ruchira Mukherjee. Two-Dimensional Material-Based Novel Drug Delivery System. 2024, 259-278. https://doi.org/10.1007/978-981-99-8010-9_9
    13. Alexander Chan, Andrew Tsourkas. Intracellular Protein Delivery: Approaches, Challenges, and Clinical Applications. BME Frontiers 2024, 5 https://doi.org/10.34133/bmef.0035
    14. Yifan Yang, Haichao Zhu, Dingkang Liu, Hong Luo, Ruilong Chang, Yue Ji, Wenbing Yao, Jun Yin, Xiangdong Gao. A Versatile Platform for the Tumor‐Targeted Intracellular Delivery of Peptides, Proteins, and siRNA. Advanced Functional Materials 2023, 33 (30) https://doi.org/10.1002/adfm.202301011
    15. David C. Luther, Ritabrita Goswami, Yi-Wei Lee, Taewon Jeon, Rui Huang, James L. Elia, Harini Nagaraj, Jetta J. E. Bijlsma, Martin Piest, Martijn A. Langereis, Vincent M. Rotello. Non-viral vaccination through cationic guanidium polymer-pDNA polyplex mediated gene transfer. Nanoscale 2023, 15 (24) , 10351-10359. https://doi.org/10.1039/D2NR06428F
    16. Hangyu Son, Jeongsu Shin, Joonhyuck Park. Recent progress in nanomedicine-mediated cytosolic delivery. RSC Advances 2023, 13 (15) , 9788-9799. https://doi.org/10.1039/D2RA07111H
    17. Ritabrita Goswami, Victor Lehot, Yağız Anıl Çiçek, Harini Nagaraj, Taewon Jeon, Terry Nguyen, Stefano Fedeli, Vincent M. Rotello. Direct Cytosolic Delivery of Citraconylated Proteins. Pharmaceutics 2023, 15 (1) , 218. https://doi.org/10.3390/pharmaceutics15010218
    18. Won Ho Jung, Gayeon You, Hyejung Mok. Different Influences of Biotinylation and PEGylation on Cationic and Anionic Proteins for Spheroid Penetration and Intracellular Uptake to Cancer Cells. Journal of Microbiology and Biotechnology 2022, 32 (9) , 1209-1216. https://doi.org/10.4014/jmb.2207.07058
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    ACS Nano

    Cite this: ACS Nano 2022, 16, 5, 7323–7330
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsnano.1c06768
    Published April 18, 2022
    Copyright © 2022 American Chemical Society
    Request reuse permissions

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