MSK1 promotes colorectal cancer metastasis by increasing Snail protein stability through USP5-mediated Snail deubiquitination

Abstract Mitogen- and stress-activated protein kinase 1 (MSK1), a Ser/Thr kinase, phosphorylates nuclear proteins to increase their stability and DNA-binding affinity. Despite the role of MSK1 in promoting cancer progression in colorectal cancer (CRC), the precise molecular mechanisms remain uneluci...

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Main Authors: Keun-Seok Hong, Ki-Jun Ryu, Hyemin Kim, Minju Kim, Seung-Ho Park, Taeyoung Kim, Jung Wook Yang, Cheol Hwangbo, Kwang Dong Kim, Young-Jun Park, Jiyun Yoo
Format: Article
Language:English
Published: Nature Publishing Group 2025-04-01
Series:Experimental and Molecular Medicine
Online Access:https://doi.org/10.1038/s12276-025-01433-0
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author Keun-Seok Hong
Ki-Jun Ryu
Hyemin Kim
Minju Kim
Seung-Ho Park
Taeyoung Kim
Jung Wook Yang
Cheol Hwangbo
Kwang Dong Kim
Young-Jun Park
Jiyun Yoo
author_facet Keun-Seok Hong
Ki-Jun Ryu
Hyemin Kim
Minju Kim
Seung-Ho Park
Taeyoung Kim
Jung Wook Yang
Cheol Hwangbo
Kwang Dong Kim
Young-Jun Park
Jiyun Yoo
author_sort Keun-Seok Hong
collection DOAJ
description Abstract Mitogen- and stress-activated protein kinase 1 (MSK1), a Ser/Thr kinase, phosphorylates nuclear proteins to increase their stability and DNA-binding affinity. Despite the role of MSK1 in promoting cancer progression in colorectal cancer (CRC), the precise molecular mechanisms remain unelucidated. Here we show that MSK1 expression induces the epithelial–mesenchymal transition (EMT) process and increases CRC cell metastasis. Furthermore, we discovered that MSK1 interacts with Snail, a key EMT regulator, and increases its stability by inhibiting ubiquitin-mediated proteasomal degradation. Importantly, MSK1 increased Snail protein stability by promoting deubiquitination rather than inhibiting its ubiquitination. Finally, we identified USP5 as an essential deubiquitinase that binds to Snail protein phosphorylated by MSK1. Based on the experimental data, in CRC, MSK1–Snail–USP5 axis can promote EMT and metastasis of CRC. Together, our findings provide potential biomarkers and novel therapeutic targets for further research in CRC.
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institution Kabale University
issn 2092-6413
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publishDate 2025-04-01
publisher Nature Publishing Group
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series Experimental and Molecular Medicine
spelling doaj-art-15130b40d99d4d15989329d75bce71ea2025-08-20T03:52:19ZengNature Publishing GroupExperimental and Molecular Medicine2092-64132025-04-0157482083510.1038/s12276-025-01433-0MSK1 promotes colorectal cancer metastasis by increasing Snail protein stability through USP5-mediated Snail deubiquitinationKeun-Seok Hong0Ki-Jun Ryu1Hyemin Kim2Minju Kim3Seung-Ho Park4Taeyoung Kim5Jung Wook Yang6Cheol Hwangbo7Kwang Dong Kim8Young-Jun Park9Jiyun Yoo10Department of Bio and Medical Bigdata (Brain Korea 21 Four), Gyeongsang National UniversityDepartment of Biochemistry and Institute of Health Sciences, Gyeongsang National University School of MedicineAnti-aging Bio Cell Factory Regional Leading Research Center, Gyeongsang National UniversityDivision of Applied Life Science (Brain Korea 21 Four), Research Institute of Life Sciences, Gyeongsang National UniversityEnvironmental Disease Research Center, Korea Research Institute of Bioscience and BiotechnologyDivision of Applied Life Science (Brain Korea 21 Four), Research Institute of Life Sciences, Gyeongsang National UniversityDepartment of Pathology, Gyeongsang National University Hospital, Gyeongsang National University College of MedicineDivision of Applied Life Science (Brain Korea 21 Four), Research Institute of Life Sciences, Gyeongsang National UniversityDivision of Applied Life Science (Brain Korea 21 Four), Research Institute of Life Sciences, Gyeongsang National UniversityEnvironmental Disease Research Center, Korea Research Institute of Bioscience and BiotechnologyDivision of Applied Life Science (Brain Korea 21 Four), Research Institute of Life Sciences, Gyeongsang National UniversityAbstract Mitogen- and stress-activated protein kinase 1 (MSK1), a Ser/Thr kinase, phosphorylates nuclear proteins to increase their stability and DNA-binding affinity. Despite the role of MSK1 in promoting cancer progression in colorectal cancer (CRC), the precise molecular mechanisms remain unelucidated. Here we show that MSK1 expression induces the epithelial–mesenchymal transition (EMT) process and increases CRC cell metastasis. Furthermore, we discovered that MSK1 interacts with Snail, a key EMT regulator, and increases its stability by inhibiting ubiquitin-mediated proteasomal degradation. Importantly, MSK1 increased Snail protein stability by promoting deubiquitination rather than inhibiting its ubiquitination. Finally, we identified USP5 as an essential deubiquitinase that binds to Snail protein phosphorylated by MSK1. Based on the experimental data, in CRC, MSK1–Snail–USP5 axis can promote EMT and metastasis of CRC. Together, our findings provide potential biomarkers and novel therapeutic targets for further research in CRC.https://doi.org/10.1038/s12276-025-01433-0
spellingShingle Keun-Seok Hong
Ki-Jun Ryu
Hyemin Kim
Minju Kim
Seung-Ho Park
Taeyoung Kim
Jung Wook Yang
Cheol Hwangbo
Kwang Dong Kim
Young-Jun Park
Jiyun Yoo
MSK1 promotes colorectal cancer metastasis by increasing Snail protein stability through USP5-mediated Snail deubiquitination
Experimental and Molecular Medicine
title MSK1 promotes colorectal cancer metastasis by increasing Snail protein stability through USP5-mediated Snail deubiquitination
title_full MSK1 promotes colorectal cancer metastasis by increasing Snail protein stability through USP5-mediated Snail deubiquitination
title_fullStr MSK1 promotes colorectal cancer metastasis by increasing Snail protein stability through USP5-mediated Snail deubiquitination
title_full_unstemmed MSK1 promotes colorectal cancer metastasis by increasing Snail protein stability through USP5-mediated Snail deubiquitination
title_short MSK1 promotes colorectal cancer metastasis by increasing Snail protein stability through USP5-mediated Snail deubiquitination
title_sort msk1 promotes colorectal cancer metastasis by increasing snail protein stability through usp5 mediated snail deubiquitination
url https://doi.org/10.1038/s12276-025-01433-0
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