<i>O</i>-GlcNAcylation of Focal Adhesion Kinase Regulates Cell Adhesion, Migration, and Proliferation via the FAK/AKT Pathway

Focal Adhesion Kinase (FAK) is a non-receptor tyrosine kinase pivotal in cellular signal transduction, regulating cell adhesion, migration, growth, and survival. However, the regulatory mechanisms of FAK during tumorigenesis and progression still need to be fully understood. Our previous study demon...

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Main Authors: Zhiwei Zhang, Tomoya Isaji, Yoshiyuki Oyama, Jianwei Liu, Zhiwei Xu, Yuhan Sun, Tomohiko Fukuda, Haojie Lu, Jianguo Gu
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Biomolecules
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Online Access:https://www.mdpi.com/2218-273X/14/12/1577
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author Zhiwei Zhang
Tomoya Isaji
Yoshiyuki Oyama
Jianwei Liu
Zhiwei Xu
Yuhan Sun
Tomohiko Fukuda
Haojie Lu
Jianguo Gu
author_facet Zhiwei Zhang
Tomoya Isaji
Yoshiyuki Oyama
Jianwei Liu
Zhiwei Xu
Yuhan Sun
Tomohiko Fukuda
Haojie Lu
Jianguo Gu
author_sort Zhiwei Zhang
collection DOAJ
description Focal Adhesion Kinase (FAK) is a non-receptor tyrosine kinase pivotal in cellular signal transduction, regulating cell adhesion, migration, growth, and survival. However, the regulatory mechanisms of FAK during tumorigenesis and progression still need to be fully understood. Our previous study demonstrated that <i>O</i>-GlcNAcylation regulates integrin-mediated cell adhesion. To further elucidate the underlying molecular mechanism, we focused on FAK in this study and purified it from 293T cells. Using liquid chromatography–mass spectrometry (LC-MS/MS), we identified the <i>O</i>-GlcNAcylation of FAK at Ser708, Thr739, and Ser886. Compared with wild-type FAK expressed in <i>FAK</i>-knockout 293T cells, the FAK mutant, in which Ser708, Thr739, and Ser886 were replaced with Ala, exhibited lower phosphorylation levels of Tyr397 and AKT. Cell proliferation and migration, assessed through MTT and wound healing assays, were significantly suppressed in the FAK mutant cells compared to the wild-type FAK cells. Additionally, the interaction among FAK, paxillin, and talin was enhanced, and cell adhesion was increased in the mutant cells. These data indicate that specific <i>O</i>-GlcNAcylation of FAK plays a critical regulatory role in integrin-mediated cell adhesion and migration. This further supports the idea that <i>O</i>-GlcNAcylation is essential for tumorigenesis and progression and that targeting the <i>O</i>-GlcNAcylation of FAK could offer a promising therapeutic strategy for cancer treatment.
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spelling doaj-art-48bd61905fc34d5c864e9686e994ca4b2025-08-20T02:43:29ZengMDPI AGBiomolecules2218-273X2024-12-011412157710.3390/biom14121577<i>O</i>-GlcNAcylation of Focal Adhesion Kinase Regulates Cell Adhesion, Migration, and Proliferation via the FAK/AKT PathwayZhiwei Zhang0Tomoya Isaji1Yoshiyuki Oyama2Jianwei Liu3Zhiwei Xu4Yuhan Sun5Tomohiko Fukuda6Haojie Lu7Jianguo Gu8Division of Regulatory Glycobiology, Graduate School of Pharmaceutical Sciences, Tohoku Medical and Pharmaceutical University, Sendai 980-0845, Miyagi, JapanDivision of Regulatory Glycobiology, Graduate School of Pharmaceutical Sciences, Tohoku Medical and Pharmaceutical University, Sendai 980-0845, Miyagi, JapanDivision of Regulatory Glycobiology, Graduate School of Pharmaceutical Sciences, Tohoku Medical and Pharmaceutical University, Sendai 980-0845, Miyagi, JapanDivision of Regulatory Glycobiology, Graduate School of Pharmaceutical Sciences, Tohoku Medical and Pharmaceutical University, Sendai 980-0845, Miyagi, JapanDivision of Regulatory Glycobiology, Graduate School of Pharmaceutical Sciences, Tohoku Medical and Pharmaceutical University, Sendai 980-0845, Miyagi, JapanDivision of Regulatory Glycobiology, Graduate School of Pharmaceutical Sciences, Tohoku Medical and Pharmaceutical University, Sendai 980-0845, Miyagi, JapanDivision of Regulatory Glycobiology, Graduate School of Pharmaceutical Sciences, Tohoku Medical and Pharmaceutical University, Sendai 980-0845, Miyagi, JapanShanghai Cancer Center and Institutes of Biomedical Sciences, Fudan University, Shanghai 200032, ChinaDivision of Regulatory Glycobiology, Graduate School of Pharmaceutical Sciences, Tohoku Medical and Pharmaceutical University, Sendai 980-0845, Miyagi, JapanFocal Adhesion Kinase (FAK) is a non-receptor tyrosine kinase pivotal in cellular signal transduction, regulating cell adhesion, migration, growth, and survival. However, the regulatory mechanisms of FAK during tumorigenesis and progression still need to be fully understood. Our previous study demonstrated that <i>O</i>-GlcNAcylation regulates integrin-mediated cell adhesion. To further elucidate the underlying molecular mechanism, we focused on FAK in this study and purified it from 293T cells. Using liquid chromatography–mass spectrometry (LC-MS/MS), we identified the <i>O</i>-GlcNAcylation of FAK at Ser708, Thr739, and Ser886. Compared with wild-type FAK expressed in <i>FAK</i>-knockout 293T cells, the FAK mutant, in which Ser708, Thr739, and Ser886 were replaced with Ala, exhibited lower phosphorylation levels of Tyr397 and AKT. Cell proliferation and migration, assessed through MTT and wound healing assays, were significantly suppressed in the FAK mutant cells compared to the wild-type FAK cells. Additionally, the interaction among FAK, paxillin, and talin was enhanced, and cell adhesion was increased in the mutant cells. These data indicate that specific <i>O</i>-GlcNAcylation of FAK plays a critical regulatory role in integrin-mediated cell adhesion and migration. This further supports the idea that <i>O</i>-GlcNAcylation is essential for tumorigenesis and progression and that targeting the <i>O</i>-GlcNAcylation of FAK could offer a promising therapeutic strategy for cancer treatment.https://www.mdpi.com/2218-273X/14/12/1577cell adhesioncellular signalingfocal adhesion kinase<i>O</i>-GlcNAcylationOGT
spellingShingle Zhiwei Zhang
Tomoya Isaji
Yoshiyuki Oyama
Jianwei Liu
Zhiwei Xu
Yuhan Sun
Tomohiko Fukuda
Haojie Lu
Jianguo Gu
<i>O</i>-GlcNAcylation of Focal Adhesion Kinase Regulates Cell Adhesion, Migration, and Proliferation via the FAK/AKT Pathway
Biomolecules
cell adhesion
cellular signaling
focal adhesion kinase
<i>O</i>-GlcNAcylation
OGT
title <i>O</i>-GlcNAcylation of Focal Adhesion Kinase Regulates Cell Adhesion, Migration, and Proliferation via the FAK/AKT Pathway
title_full <i>O</i>-GlcNAcylation of Focal Adhesion Kinase Regulates Cell Adhesion, Migration, and Proliferation via the FAK/AKT Pathway
title_fullStr <i>O</i>-GlcNAcylation of Focal Adhesion Kinase Regulates Cell Adhesion, Migration, and Proliferation via the FAK/AKT Pathway
title_full_unstemmed <i>O</i>-GlcNAcylation of Focal Adhesion Kinase Regulates Cell Adhesion, Migration, and Proliferation via the FAK/AKT Pathway
title_short <i>O</i>-GlcNAcylation of Focal Adhesion Kinase Regulates Cell Adhesion, Migration, and Proliferation via the FAK/AKT Pathway
title_sort i o i glcnacylation of focal adhesion kinase regulates cell adhesion migration and proliferation via the fak akt pathway
topic cell adhesion
cellular signaling
focal adhesion kinase
<i>O</i>-GlcNAcylation
OGT
url https://www.mdpi.com/2218-273X/14/12/1577
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