A Reactive Oxygen Species-Scavenging 'Stealth' Polymer, Poly(thioglycidyl glycerol), Outperforms Poly(ethylene glycol) in Protein Conjugates and Nanocarriers and Enhances Protein Stability to Environmental and Biological Stressors.


Journal

Journal of the American Chemical Society
ISSN: 1520-5126
Titre abrégé: J Am Chem Soc
Pays: United States
ID NLM: 7503056

Informations de publication

Date de publication:
23 11 2022
Historique:
pubmed: 12 11 2022
medline: 25 11 2022
entrez: 11 11 2022
Statut: ppublish

Résumé

This study addresses well-known shortcomings of poly(ethylene glycol) (PEG)-based conjugates. PEGylation is by far the most common method employed to overcome immunogenicity and suboptimal pharmacokinetics of, for example, therapeutic proteins but has significant drawbacks. First, PEG offers no protection from denaturation during lyophilization, storage, or oxidation (e.g., by biological oxidants, reactive oxygen species); second, PEG's inherent immunogenicity, leading to hypersensitivity and accelerated blood clearance (ABC), is a growing concern. We have here developed an 'active-stealth' polymer, poly(thioglycidyl glycerol)(PTGG), which in human plasma is less immunogenic than PEG (35% less complement activation) and features a reactive oxygen species-scavenging and anti-inflammatory action (∼50% less TNF-α in LPS-stimulated macrophages at only 0.1 mg/mL). PTGG was conjugated to proteins via a one-pot process; molar mass- and grafting density-matched PTGG-lysozyme conjugates were superior to their PEG analogues in terms of enzyme activity and stability against freeze-drying or oxidation; the latter is due to sacrificial oxidation of methionine-mimetic PTGG chains. Both in mice and rats, PTGG-ovalbumin displayed circulation half-lives up to twice as long as PEG-ovalbumin, but most importantly─and differently from PEG─without any associated ABC effect seen either in the time dependency of blood concentration, in the liver/splenic accumulation, or in antipolymer IgM/IgG titers. Furthermore, similar pharmacokinetic results were obtained with PTGGylated/PEGylated liposomal nanocarriers. PTGG's 'active-stealth' character therefore makes it a highly promising alternative to PEG for conjugation to biologics or nanocarriers.

Identifiants

pubmed: 36367536
doi: 10.1021/jacs.2c09232
pmc: PMC9706570
doi:

Substances chimiques

Polyethylene Glycols 3WJQ0SDW1A
Polymers 0
Glycerol PDC6A3C0OX
Reactive Oxygen Species 0
Ovalbumin 9006-59-1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

21304-21317

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Auteurs

Richard d'Arcy (R)

Laboratory for Polymers and Biomaterials, Fondazione Istituto Italiano di Tecnologia, 16163 Genova, Italy.
Division of Pharmacy and Optometry, School of Health Sciences, University of Manchester, Oxford Road, Manchester M13 9PT, U.K.
Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee 37235, United States.

Farah El Mohtadi (F)

Division of Pharmacy and Optometry, School of Health Sciences, University of Manchester, Oxford Road, Manchester M13 9PT, U.K.

Nora Francini (N)

Laboratory for Polymers and Biomaterials, Fondazione Istituto Italiano di Tecnologia, 16163 Genova, Italy.
Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee 37235, United States.

Carlisle R DeJulius (CR)

Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee 37235, United States.

Hyunmoon Back (H)

Department of Pharmaceutics, Ernest Mario School of Pharmacy, Rutgers, The State University of New Jersey, 160 Frelinghuysen Road, Piscataway, New Jersey 08854, United States.
Center of Excellence for Pharmaceutical Translational Research and Education, Ernest Mario School of Pharmacy, Rutgers, The State University of New Jersey, 160 Frelinghuysen Road, Piscataway, New Jersey 08854, United States.

Arianna Gennari (A)

Laboratory for Polymers and Biomaterials, Fondazione Istituto Italiano di Tecnologia, 16163 Genova, Italy.

Mike Geven (M)

Laboratory for Polymers and Biomaterials, Fondazione Istituto Italiano di Tecnologia, 16163 Genova, Italy.

Maria Lopez-Cavestany (M)

Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee 37235, United States.

Zulfiye Yesim Turhan (ZY)

Laboratory for Polymers and Biomaterials, Fondazione Istituto Italiano di Tecnologia, 16163 Genova, Italy.
Division of Pharmacy and Optometry, School of Health Sciences, University of Manchester, Oxford Road, Manchester M13 9PT, U.K.

Fang Yu (F)

Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee 37235, United States.

Jong Bong Lee (JB)

Department of Pharmaceutics, Ernest Mario School of Pharmacy, Rutgers, The State University of New Jersey, 160 Frelinghuysen Road, Piscataway, New Jersey 08854, United States.

Michael R King (MR)

Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee 37235, United States.

Leonid Kagan (L)

Department of Pharmaceutics, Ernest Mario School of Pharmacy, Rutgers, The State University of New Jersey, 160 Frelinghuysen Road, Piscataway, New Jersey 08854, United States.
Center of Excellence for Pharmaceutical Translational Research and Education, Ernest Mario School of Pharmacy, Rutgers, The State University of New Jersey, 160 Frelinghuysen Road, Piscataway, New Jersey 08854, United States.

Craig L Duvall (CL)

Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee 37235, United States.

Nicola Tirelli (N)

Laboratory for Polymers and Biomaterials, Fondazione Istituto Italiano di Tecnologia, 16163 Genova, Italy.
Division of Pharmacy and Optometry, School of Health Sciences, University of Manchester, Oxford Road, Manchester M13 9PT, U.K.

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