Microtubule inhibitors identified through nonbiased screening enhance DNA transfection efficiency by delaying p62‐dependent ubiquitin recruitment

Ectopic gene expression is an indispensable tool in biology and medicine, but is often limited by the low efficiency of DNA transfection. We previously reported that depletion of the autophagy receptor p62/SQSTM1 enhances DNA transfection efficiency by preventing the degradation of transfected DNA....

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Published inGenes to cells : devoted to molecular & cellular mechanisms Vol. 26; no. 9; pp. 739 - 751
Main Authors Tsuchiya, Megumi, Ogawa, Hidesato, Watanabe, Kento, Koujin, Takako, Mori, Chie, Nunomura, Kazuto, Lin, Bangzhong, Tani, Akiyoshi, Hiraoka, Yasushi, Haraguchi, Tokuko
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LanguageEnglish
Published England Wiley Subscription Services, Inc 01.09.2021
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Abstract Ectopic gene expression is an indispensable tool in biology and medicine, but is often limited by the low efficiency of DNA transfection. We previously reported that depletion of the autophagy receptor p62/SQSTM1 enhances DNA transfection efficiency by preventing the degradation of transfected DNA. Therefore, p62 is a potential target for drugs to increase transfection efficiency. To identify such drugs, a nonbiased high‐throughput screening was applied to over 4,000 compounds from the Osaka University compound library, and their p62 dependency was evaluated. The top‐scoring drugs were mostly microtubule inhibitors, such as colchicine and vinblastine, and all of them showed positive effects only in the presence of p62. To understand the p62‐dependent mechanisms, the time required for p62‐dependent ubiquitination, which is required for autophagosome formation, was examined using polystyrene beads that were introduced into cells as materials that mimicked transfected DNA. Microtubule inhibitors caused a delay in ubiquitination. Furthermore, the level of phosphorylated p62 at S405 was markedly decreased in the drug‐treated cells. These results suggest that microtubule inhibitors inhibit p62‐dependent autophagosome formation. Our findings demonstrate for the first time that microtubule inhibitors suppress p62 activation as a mechanism for increasing DNA transfection efficiency and provide solutions to increase efficiency. Non‐biased high‐throughput screening for over 4,000 compounds revealed microtubule inhibitors such as colchicine and vinblastine enhance transfection efficiency. These microtubule inhibitors increase transfection efficiency by suppressing p62 phosphorylation that leads to the degradation of transfected DNA.
AbstractList Ectopic gene expression is an indispensable tool in biology and medicine, but is often limited by the low efficiency of DNA transfection. We previously reported that depletion of the autophagy receptor p62/SQSTM1 enhances DNA transfection efficiency by preventing the degradation of transfected DNA. Therefore, p62 is a potential target for drugs to increase transfection efficiency. To identify such drugs, a nonbiased high‐throughput screening was applied to over 4,000 compounds from the Osaka University compound library, and their p62 dependency was evaluated. The top‐scoring drugs were mostly microtubule inhibitors, such as colchicine and vinblastine, and all of them showed positive effects only in the presence of p62. To understand the p62‐dependent mechanisms, the time required for p62‐dependent ubiquitination, which is required for autophagosome formation, was examined using polystyrene beads that were introduced into cells as materials that mimicked transfected DNA. Microtubule inhibitors caused a delay in ubiquitination. Furthermore, the level of phosphorylated p62 at S405 was markedly decreased in the drug‐treated cells. These results suggest that microtubule inhibitors inhibit p62‐dependent autophagosome formation. Our findings demonstrate for the first time that microtubule inhibitors suppress p62 activation as a mechanism for increasing DNA transfection efficiency and provide solutions to increase efficiency. Non‐biased high‐throughput screening for over 4,000 compounds revealed microtubule inhibitors such as colchicine and vinblastine enhance transfection efficiency. These microtubule inhibitors increase transfection efficiency by suppressing p62 phosphorylation that leads to the degradation of transfected DNA.
Ectopic gene expression is an indispensable tool in biology and medicine, but is often limited by the low efficiency of DNA transfection. We previously reported that depletion of the autophagy receptor p62/SQSTM1 enhances DNA transfection efficiency by preventing the degradation of transfected DNA. Therefore, p62 is a potential target for drugs to increase transfection efficiency. To identify such drugs, a nonbiased high‐throughput screening was applied to over 4,000 compounds from the Osaka University compound library, and their p62 dependency was evaluated. The top‐scoring drugs were mostly microtubule inhibitors, such as colchicine and vinblastine, and all of them showed positive effects only in the presence of p62. To understand the p62‐dependent mechanisms, the time required for p62‐dependent ubiquitination, which is required for autophagosome formation, was examined using polystyrene beads that were introduced into cells as materials that mimicked transfected DNA. Microtubule inhibitors caused a delay in ubiquitination. Furthermore, the level of phosphorylated p62 at S405 was markedly decreased in the drug‐treated cells. These results suggest that microtubule inhibitors inhibit p62‐dependent autophagosome formation. Our findings demonstrate for the first time that microtubule inhibitors suppress p62 activation as a mechanism for increasing DNA transfection efficiency and provide solutions to increase efficiency.
Author Haraguchi, Tokuko
Mori, Chie
Hiraoka, Yasushi
Watanabe, Kento
Koujin, Takako
Tani, Akiyoshi
Nunomura, Kazuto
Lin, Bangzhong
Ogawa, Hidesato
Tsuchiya, Megumi
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Issue 9
Keywords gene delivery
autophagy
ubiquitination
high-throughput screening
p62
phosphorylation
transfection efficiency
Language English
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Notes Megumi Tsuchiya and Hidesato Ogawa contributed equally to this manuscript.
Communicated by: Yoshihiro Yoneda
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Snippet Ectopic gene expression is an indispensable tool in biology and medicine, but is often limited by the low efficiency of DNA transfection. We previously...
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SubjectTerms Animals
Autophagy
Cells, Cultured
Colchicine
Colchicine - pharmacology
Deoxyribonucleic acid
DNA
Efficiency
Endocytosis
Fibroblasts - drug effects
Fibroblasts - metabolism
gene delivery
Gene expression
High-Throughput Screening Assays - methods
high‐throughput screening
Mice
Microtubules - drug effects
Microtubules - metabolism
p62
Phagocytosis
phosphorylation
Polystyrene
Sequestosome-1 Protein - metabolism
Small Molecule Libraries - pharmacology
Transfection
Transfection - methods
transfection efficiency
Tubulin Modulators - pharmacology
Ubiquitin
Ubiquitin - metabolism
Ubiquitination
Vinblastine
Vinblastine - pharmacology
Title Microtubule inhibitors identified through nonbiased screening enhance DNA transfection efficiency by delaying p62‐dependent ubiquitin recruitment
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fgtc.12881
https://www.ncbi.nlm.nih.gov/pubmed/34212463
https://www.proquest.com/docview/2570255880
https://search.proquest.com/docview/2548410200
Volume 26
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