SAMHD1-induced endosomal FAK signaling promotes human renal clear cell carcinoma metastasis by activating Rac1-mediated lamellipodia protrusion

Abstract Human sterile α motif and HD domain-containing protein 1 (SAMHD1) has deoxyribonucleoside triphosphohydrolase (dNTPase) activity that allows it to defend against human immunodeficiency virus type I (HIV-1) infections and regulate the cell cycle. Although SAMHD1 mutations have been identifie...

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Main Authors: Sunho An, Tam Thuy Lu Vo, Taekwon Son, Hoon Choi, Jinyoung Kim, Juyeon Lee, Byung Hoon Kim, Misun Choe, Eunyoung Ha, Young-Joon Surh, Kyu-Won Kim, Ji Hae Seo
Format: Article
Language:English
Published: Nature Publishing Group 2023-04-01
Series:Experimental and Molecular Medicine
Online Access:https://doi.org/10.1038/s12276-023-00961-x
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author Sunho An
Tam Thuy Lu Vo
Taekwon Son
Hoon Choi
Jinyoung Kim
Juyeon Lee
Byung Hoon Kim
Misun Choe
Eunyoung Ha
Young-Joon Surh
Kyu-Won Kim
Ji Hae Seo
author_facet Sunho An
Tam Thuy Lu Vo
Taekwon Son
Hoon Choi
Jinyoung Kim
Juyeon Lee
Byung Hoon Kim
Misun Choe
Eunyoung Ha
Young-Joon Surh
Kyu-Won Kim
Ji Hae Seo
author_sort Sunho An
collection DOAJ
description Abstract Human sterile α motif and HD domain-containing protein 1 (SAMHD1) has deoxyribonucleoside triphosphohydrolase (dNTPase) activity that allows it to defend against human immunodeficiency virus type I (HIV-1) infections and regulate the cell cycle. Although SAMHD1 mutations have been identified in various cancer types, their role in cancer is unclear. Here, we aimed to investigate the oncogenic role of SAMHD1 in human clear cell renal cell carcinoma (ccRCC), particularly as a core molecule promoting cancer cell migration. We found that SAMHD1 participated in endocytosis and lamellipodia formation. Mechanistically, SAMHD1 contributed to the formation of the endosomal complex by binding to cortactin. Thereafter, SAMHD1-stimulated endosomal focal adhesion kinase (FAK) signaling activated Rac1, which promoted lamellipodia formation on the plasma membrane and enhanced the motility of ccRCC cells. Finally, we observed a strong correlation between SAMHD1 expression and the activation of FAK and cortactin in tumor tissues obtained from patients with ccRCC. In brief, these findings reveal that SAMHD1 is an oncogene that plays a pivotal role in ccRCC cell migration through the endosomal FAK-Rac1 signaling pathway.
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spelling doaj-art-d4ce04dbbcdb4b258bd7cb70076861a52025-08-20T03:04:15ZengNature Publishing GroupExperimental and Molecular Medicine2092-64132023-04-0155477979310.1038/s12276-023-00961-xSAMHD1-induced endosomal FAK signaling promotes human renal clear cell carcinoma metastasis by activating Rac1-mediated lamellipodia protrusionSunho An0Tam Thuy Lu Vo1Taekwon Son2Hoon Choi3Jinyoung Kim4Juyeon Lee5Byung Hoon Kim6Misun Choe7Eunyoung Ha8Young-Joon Surh9Kyu-Won Kim10Ji Hae Seo11College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National UniversityDepartment of Biochemistry, School of Medicine, Keimyung UniversityKorea Brain Bank, Korea Brain Research InstituteCollege of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National UniversityDepartment of Internal Medicine, School of Medicine, Keimyung UniversityDepartment of Biochemistry, School of Medicine, Keimyung UniversityDepartment of Urology, School of Medicine, Keimyung UniversityDepartment of Pathology, School of Medicine, Keimyung UniversityDepartment of Biochemistry, School of Medicine, Keimyung UniversityCollege of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National UniversityCollege of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National UniversityDepartment of Biochemistry, School of Medicine, Keimyung UniversityAbstract Human sterile α motif and HD domain-containing protein 1 (SAMHD1) has deoxyribonucleoside triphosphohydrolase (dNTPase) activity that allows it to defend against human immunodeficiency virus type I (HIV-1) infections and regulate the cell cycle. Although SAMHD1 mutations have been identified in various cancer types, their role in cancer is unclear. Here, we aimed to investigate the oncogenic role of SAMHD1 in human clear cell renal cell carcinoma (ccRCC), particularly as a core molecule promoting cancer cell migration. We found that SAMHD1 participated in endocytosis and lamellipodia formation. Mechanistically, SAMHD1 contributed to the formation of the endosomal complex by binding to cortactin. Thereafter, SAMHD1-stimulated endosomal focal adhesion kinase (FAK) signaling activated Rac1, which promoted lamellipodia formation on the plasma membrane and enhanced the motility of ccRCC cells. Finally, we observed a strong correlation between SAMHD1 expression and the activation of FAK and cortactin in tumor tissues obtained from patients with ccRCC. In brief, these findings reveal that SAMHD1 is an oncogene that plays a pivotal role in ccRCC cell migration through the endosomal FAK-Rac1 signaling pathway.https://doi.org/10.1038/s12276-023-00961-x
spellingShingle Sunho An
Tam Thuy Lu Vo
Taekwon Son
Hoon Choi
Jinyoung Kim
Juyeon Lee
Byung Hoon Kim
Misun Choe
Eunyoung Ha
Young-Joon Surh
Kyu-Won Kim
Ji Hae Seo
SAMHD1-induced endosomal FAK signaling promotes human renal clear cell carcinoma metastasis by activating Rac1-mediated lamellipodia protrusion
Experimental and Molecular Medicine
title SAMHD1-induced endosomal FAK signaling promotes human renal clear cell carcinoma metastasis by activating Rac1-mediated lamellipodia protrusion
title_full SAMHD1-induced endosomal FAK signaling promotes human renal clear cell carcinoma metastasis by activating Rac1-mediated lamellipodia protrusion
title_fullStr SAMHD1-induced endosomal FAK signaling promotes human renal clear cell carcinoma metastasis by activating Rac1-mediated lamellipodia protrusion
title_full_unstemmed SAMHD1-induced endosomal FAK signaling promotes human renal clear cell carcinoma metastasis by activating Rac1-mediated lamellipodia protrusion
title_short SAMHD1-induced endosomal FAK signaling promotes human renal clear cell carcinoma metastasis by activating Rac1-mediated lamellipodia protrusion
title_sort samhd1 induced endosomal fak signaling promotes human renal clear cell carcinoma metastasis by activating rac1 mediated lamellipodia protrusion
url https://doi.org/10.1038/s12276-023-00961-x
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