Pharmacological targeting of casein kinase 1δ suppresses oncogenic NRAS-driven melanoma

Abstract Activating mutations in NRAS account for 15–20% of melanoma, yet effective anti-NRAS therapies are still lacking. In this study, we unveil the casein kinase 1δ (CK1δ) as an uncharacterized regulator of oncogenic NRAS mutations, specifically Q61R and Q61K, which are the most prevalent NRAS m...

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Main Authors: Yalei Wen, Hui Wang, Xiao Yang, Yingjie Zhu, Mei Li, Xiuqing Ma, Lei Huang, Rui Wan, Caishi Zhang, Shengrong Li, Hongling Jia, Qin Guo, Xiaoyun Lu, Zhengqiu Li, Xiangchun Shen, Qiushi Zhang, Lu Si, Chengqian Yin, Tongzheng Liu
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54140-1
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author Yalei Wen
Hui Wang
Xiao Yang
Yingjie Zhu
Mei Li
Xiuqing Ma
Lei Huang
Rui Wan
Caishi Zhang
Shengrong Li
Hongling Jia
Qin Guo
Xiaoyun Lu
Zhengqiu Li
Xiangchun Shen
Qiushi Zhang
Lu Si
Chengqian Yin
Tongzheng Liu
author_facet Yalei Wen
Hui Wang
Xiao Yang
Yingjie Zhu
Mei Li
Xiuqing Ma
Lei Huang
Rui Wan
Caishi Zhang
Shengrong Li
Hongling Jia
Qin Guo
Xiaoyun Lu
Zhengqiu Li
Xiangchun Shen
Qiushi Zhang
Lu Si
Chengqian Yin
Tongzheng Liu
author_sort Yalei Wen
collection DOAJ
description Abstract Activating mutations in NRAS account for 15–20% of melanoma, yet effective anti-NRAS therapies are still lacking. In this study, we unveil the casein kinase 1δ (CK1δ) as an uncharacterized regulator of oncogenic NRAS mutations, specifically Q61R and Q61K, which are the most prevalent NRAS mutations in melanoma. The genetic ablation or pharmacological inhibition of CK1δ markedly destabilizes NRAS mutants and suppresses their oncogenic functions. Moreover, we identify USP46 as a bona fide deubiquitinase of NRAS mutants. Mechanistically, CK1δ directly phosphorylates USP46 and activates its deubiquitinase activity towards NRAS mutants, thus promoting oncogenic NRAS-driven melanocyte malignant transformation and melanoma progression in vitro and in vivo. Our findings underscore the significance of the CK1δ-USP46 axis in stabilizing oncogenic NRAS mutants and provide preclinical evidence that targeting this axis holds promise as a therapeutic strategy for human melanoma harboring NRAS mutations.
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record_format Article
series Nature Communications
spelling doaj-art-83e26542cf344856a8abf2d239e813902025-08-20T02:33:06ZengNature PortfolioNature Communications2041-17232024-11-0115111910.1038/s41467-024-54140-1Pharmacological targeting of casein kinase 1δ suppresses oncogenic NRAS-driven melanomaYalei Wen0Hui Wang1Xiao Yang2Yingjie Zhu3Mei Li4Xiuqing Ma5Lei Huang6Rui Wan7Caishi Zhang8Shengrong Li9Hongling Jia10Qin Guo11Xiaoyun Lu12Zhengqiu Li13Xiangchun Shen14Qiushi Zhang15Lu Si16Chengqian Yin17Tongzheng Liu18Research Institute for Maternal and Child Health, The Affiliated Guangdong Second Provincial General Hospital, Postdoctoral Research Station of Traditional Chinese Medicine, School of Pharmacy, Jinan UniversityInstitute of Cancer Research, Shenzhen Bay LaboratoryCollege of Pharmacy/International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Ministry of Education (MOE) of China, Jinan UniversityCollege of Pharmacy/International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Ministry of Education (MOE) of China, Jinan UniversityCollege of Pharmacy/International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Ministry of Education (MOE) of China, Jinan UniversityCollege of Pharmacy/International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Ministry of Education (MOE) of China, Jinan UniversityCollege of Pharmacy/International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Ministry of Education (MOE) of China, Jinan UniversityCollege of Pharmacy/International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Ministry of Education (MOE) of China, Jinan UniversityCollege of Pharmacy/International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Ministry of Education (MOE) of China, Jinan UniversityCollege of Pharmacy/International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Ministry of Education (MOE) of China, Jinan UniversityDepartment of Medical Biochemistry and Molecular Biology, School of Medicine, Jinan UniversityDepartment of Pathology, Shanxi Provincial People’s HospitalCollege of Pharmacy/International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Ministry of Education (MOE) of China, Jinan UniversityCollege of Pharmacy/International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Ministry of Education (MOE) of China, Jinan UniversityThe State Key Laboratory of Functions and Applications of Medicinal Plants, Guizhou Medical UniversityResearch Institute for Maternal and Child Health, The Affiliated Guangdong Second Provincial General Hospital, Postdoctoral Research Station of Traditional Chinese Medicine, School of Pharmacy, Jinan UniversityKey Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Department of Melanoma and Sarcoma, Peking University Cancer Hospital and Research InstituteInstitute of Cancer Research, Shenzhen Bay LaboratoryResearch Institute for Maternal and Child Health, The Affiliated Guangdong Second Provincial General Hospital, Postdoctoral Research Station of Traditional Chinese Medicine, School of Pharmacy, Jinan UniversityAbstract Activating mutations in NRAS account for 15–20% of melanoma, yet effective anti-NRAS therapies are still lacking. In this study, we unveil the casein kinase 1δ (CK1δ) as an uncharacterized regulator of oncogenic NRAS mutations, specifically Q61R and Q61K, which are the most prevalent NRAS mutations in melanoma. The genetic ablation or pharmacological inhibition of CK1δ markedly destabilizes NRAS mutants and suppresses their oncogenic functions. Moreover, we identify USP46 as a bona fide deubiquitinase of NRAS mutants. Mechanistically, CK1δ directly phosphorylates USP46 and activates its deubiquitinase activity towards NRAS mutants, thus promoting oncogenic NRAS-driven melanocyte malignant transformation and melanoma progression in vitro and in vivo. Our findings underscore the significance of the CK1δ-USP46 axis in stabilizing oncogenic NRAS mutants and provide preclinical evidence that targeting this axis holds promise as a therapeutic strategy for human melanoma harboring NRAS mutations.https://doi.org/10.1038/s41467-024-54140-1
spellingShingle Yalei Wen
Hui Wang
Xiao Yang
Yingjie Zhu
Mei Li
Xiuqing Ma
Lei Huang
Rui Wan
Caishi Zhang
Shengrong Li
Hongling Jia
Qin Guo
Xiaoyun Lu
Zhengqiu Li
Xiangchun Shen
Qiushi Zhang
Lu Si
Chengqian Yin
Tongzheng Liu
Pharmacological targeting of casein kinase 1δ suppresses oncogenic NRAS-driven melanoma
Nature Communications
title Pharmacological targeting of casein kinase 1δ suppresses oncogenic NRAS-driven melanoma
title_full Pharmacological targeting of casein kinase 1δ suppresses oncogenic NRAS-driven melanoma
title_fullStr Pharmacological targeting of casein kinase 1δ suppresses oncogenic NRAS-driven melanoma
title_full_unstemmed Pharmacological targeting of casein kinase 1δ suppresses oncogenic NRAS-driven melanoma
title_short Pharmacological targeting of casein kinase 1δ suppresses oncogenic NRAS-driven melanoma
title_sort pharmacological targeting of casein kinase 1δ suppresses oncogenic nras driven melanoma
url https://doi.org/10.1038/s41467-024-54140-1
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