O-GlcNAc modification is essential for the regulation of autophagy in Drosophila melanogaster

Sujin Park; Yangsin Lee; Jin Won Pak; Hanbyeol Kim; Hyeonjin Choi; Jae Woo Kim; Jürgen Roth; Jin Won Cho

doi:10.1007/s00018-015-1889-z

O-GlcNAc modification is essential for the regulation of autophagy in Drosophila melanogaster

Sujin Park, Yangsin Lee, Jin Won Pak, Hanbyeol Kim, Hyeonjin Choi, Jae Woo Kim, Jürgen Roth, Jin Won Cho

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31 Citations (Scopus)

Abstract

O-GlcNAcylation is a dynamic post-translational modification that takes place on ser/thr residues of nucleocytoplasmic proteins. O-GlcNAcylation regulates almost all cellular events as a nutrient sensor, a transcriptional and translational regulator, and a disease-related factor. Although the role of O-GlcNAcylation in insulin signaling and metabolism are well established, the relationship between O-GlcNAcylation and autophagy is largely unknown. Here, we manipulated O-GlcNAcylation in Drosophila and found that it regulates autophagy through Akt/dFOXO signaling. We demonstrate that O-GlcNAcylation and the levels of O-GlcNAc transferase (OGT) are increased during starvation. Furthermore, Atg proteins and autolysosomes are increased in OGT-reduced flies without fasting. Atg proteins and autophagosomes are reduced in OGT-overexpressing flies. Our results suggest that not only autophagy gene expression but also autophagic structures are regulated by OGT through Akt and dFOXO. These data imply that O-GlcNAcylation is important in modulating autophagy as well as insulin signaling in Drosophila.

Original language	English
Pages (from-to)	3173-3183
Number of pages	11
Journal	Cellular and Molecular Life Sciences
Volume	72
Issue number	16
DOIs	https://doi.org/10.1007/s00018-015-1889-z
Publication status	Published - 2015 Aug 25

Bibliographical note

Funding Information:
We thank K. M. Choe, and K. Yu for fly stocks and DNA clones, and O. Puig and K. Yu for providing the anti dFOXO antibody. We are also grateful to other members of the Cho and Choe laboratories for helpful discussions. This work is partly supported by the Graduate School of Yonsei University. This work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (NRF-2013R1A2A1A01008067) to J. W. C.

Publisher Copyright:
© 2015 Springer Basel.

All Science Journal Classification (ASJC) codes

Molecular Medicine
Molecular Biology
Pharmacology
Cellular and Molecular Neuroscience
Cell Biology

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10.1007/s00018-015-1889-z

Cite this

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title = "O-GlcNAc modification is essential for the regulation of autophagy in Drosophila melanogaster",

abstract = "O-GlcNAcylation is a dynamic post-translational modification that takes place on ser/thr residues of nucleocytoplasmic proteins. O-GlcNAcylation regulates almost all cellular events as a nutrient sensor, a transcriptional and translational regulator, and a disease-related factor. Although the role of O-GlcNAcylation in insulin signaling and metabolism are well established, the relationship between O-GlcNAcylation and autophagy is largely unknown. Here, we manipulated O-GlcNAcylation in Drosophila and found that it regulates autophagy through Akt/dFOXO signaling. We demonstrate that O-GlcNAcylation and the levels of O-GlcNAc transferase (OGT) are increased during starvation. Furthermore, Atg proteins and autolysosomes are increased in OGT-reduced flies without fasting. Atg proteins and autophagosomes are reduced in OGT-overexpressing flies. Our results suggest that not only autophagy gene expression but also autophagic structures are regulated by OGT through Akt and dFOXO. These data imply that O-GlcNAcylation is important in modulating autophagy as well as insulin signaling in Drosophila.",

author = "Sujin Park and Yangsin Lee and Pak, {Jin Won} and Hanbyeol Kim and Hyeonjin Choi and Kim, {Jae Woo} and J{\"u}rgen Roth and Cho, {Jin Won}",

note = "Funding Information: We thank K. M. Choe, and K. Yu for fly stocks and DNA clones, and O. Puig and K. Yu for providing the anti dFOXO antibody. We are also grateful to other members of the Cho and Choe laboratories for helpful discussions. This work is partly supported by the Graduate School of Yonsei University. This work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (NRF-2013R1A2A1A01008067) to J. W. C. Publisher Copyright: {\textcopyright} 2015 Springer Basel.",

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AU - Park, Sujin

AU - Lee, Yangsin

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AU - Choi, Hyeonjin

AU - Kim, Jae Woo

AU - Roth, Jürgen

AU - Cho, Jin Won

N1 - Funding Information: We thank K. M. Choe, and K. Yu for fly stocks and DNA clones, and O. Puig and K. Yu for providing the anti dFOXO antibody. We are also grateful to other members of the Cho and Choe laboratories for helpful discussions. This work is partly supported by the Graduate School of Yonsei University. This work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (NRF-2013R1A2A1A01008067) to J. W. C. Publisher Copyright: © 2015 Springer Basel.

PY - 2015/8/25

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N2 - O-GlcNAcylation is a dynamic post-translational modification that takes place on ser/thr residues of nucleocytoplasmic proteins. O-GlcNAcylation regulates almost all cellular events as a nutrient sensor, a transcriptional and translational regulator, and a disease-related factor. Although the role of O-GlcNAcylation in insulin signaling and metabolism are well established, the relationship between O-GlcNAcylation and autophagy is largely unknown. Here, we manipulated O-GlcNAcylation in Drosophila and found that it regulates autophagy through Akt/dFOXO signaling. We demonstrate that O-GlcNAcylation and the levels of O-GlcNAc transferase (OGT) are increased during starvation. Furthermore, Atg proteins and autolysosomes are increased in OGT-reduced flies without fasting. Atg proteins and autophagosomes are reduced in OGT-overexpressing flies. Our results suggest that not only autophagy gene expression but also autophagic structures are regulated by OGT through Akt and dFOXO. These data imply that O-GlcNAcylation is important in modulating autophagy as well as insulin signaling in Drosophila.

AB - O-GlcNAcylation is a dynamic post-translational modification that takes place on ser/thr residues of nucleocytoplasmic proteins. O-GlcNAcylation regulates almost all cellular events as a nutrient sensor, a transcriptional and translational regulator, and a disease-related factor. Although the role of O-GlcNAcylation in insulin signaling and metabolism are well established, the relationship between O-GlcNAcylation and autophagy is largely unknown. Here, we manipulated O-GlcNAcylation in Drosophila and found that it regulates autophagy through Akt/dFOXO signaling. We demonstrate that O-GlcNAcylation and the levels of O-GlcNAc transferase (OGT) are increased during starvation. Furthermore, Atg proteins and autolysosomes are increased in OGT-reduced flies without fasting. Atg proteins and autophagosomes are reduced in OGT-overexpressing flies. Our results suggest that not only autophagy gene expression but also autophagic structures are regulated by OGT through Akt and dFOXO. These data imply that O-GlcNAcylation is important in modulating autophagy as well as insulin signaling in Drosophila.

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O-GlcNAc modification is essential for the regulation of autophagy in Drosophila melanogaster

Abstract

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