Loss of TC-PTP in keratinocytes leads to increased UVB-induced autophagy

Abstract Ultraviolet B (UVB) radiation can distort cellular homeostasis and predispose the skin to carcinogenesis. Amongst the deteriorating effects of the sun’s UVB radiation on cellular homeostasis is the formation of DNA photoproducts. These photoproducts can cause significant changes in the stru...

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Main Authors: Obed Asare, Lindsey Shim, Cheol-Jung Lee, Jose Delgado, Natasha Quailes, Klarissa Zavala, Junsoo Park, Bilal Bin Hafeez, Yong-Yeon Cho, Subhash C. Chauhan, Dae Joon Kim
Format: Article
Language:English
Published: Nature Publishing Group 2025-02-01
Series:Cell Death Discovery
Online Access:https://doi.org/10.1038/s41420-025-02353-8
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author Obed Asare
Lindsey Shim
Cheol-Jung Lee
Jose Delgado
Natasha Quailes
Klarissa Zavala
Junsoo Park
Bilal Bin Hafeez
Yong-Yeon Cho
Subhash C. Chauhan
Dae Joon Kim
author_facet Obed Asare
Lindsey Shim
Cheol-Jung Lee
Jose Delgado
Natasha Quailes
Klarissa Zavala
Junsoo Park
Bilal Bin Hafeez
Yong-Yeon Cho
Subhash C. Chauhan
Dae Joon Kim
author_sort Obed Asare
collection DOAJ
description Abstract Ultraviolet B (UVB) radiation can distort cellular homeostasis and predispose the skin to carcinogenesis. Amongst the deteriorating effects of the sun’s UVB radiation on cellular homeostasis is the formation of DNA photoproducts. These photoproducts can cause significant changes in the structure and conformation of DNA, inducing gene mutations which may accumulate to trigger the formation of skin cancer. Photoproducts are typically repaired by nucleotide excision repair. Notwithstanding, when the repair mechanism fails, apoptosis ensues to prevent the accumulation of mutations and to restore cellular homeostasis. This present study reports that T-cell protein tyrosine phosphatase (TC-PTP) can increase UVB-induced apoptosis by inhibiting autophagy-mediated cell survival of damaged keratinocytes. TC-PTP deficiency in 3PC mouse keratinocytes led to the formation of autophagic vacuoles and increased expression of LC3-II. We established human TC-PTP-deficient (TC-PTP/KO) HaCaT cells using the CRISPR/Cas9 system. TC-PTP/KO HaCaT cells exhibited increased cell survival upon UVB exposure, which was accompanied by increased expression of LC3-II and decreased expression of p62 compared to control cells. Pretreatment of TC-PTP/KO HaCaT cells with early-phase autophagy inhibitor, 3-methyladenine significantly decreased the expression of LC3-II and reduced cell survival in response to UVB irradiation in comparison with untreated TC-PTP/KO cells. Pretreatment of TC-PTP/KO HaCaT cells with late-phase inhibitor, chloroquine also significantly reduced cell viability with increased accumulation of LC3-II after UVB irradiation compared to untreated counterpart cells. While UVB significantly increased apoptosis in the engineered (Mock) cells, this was not observed in similarly treated TC-PTP/KO HaCaT cells. However, chloroquine treatment increased apoptosis in TC-PTP/KO HaCaT cells. Examination of human squamous cell carcinomas (SCCs) revealed that TC-PTP expression was inversely correlated with LC3 expression. Our findings suggest that TC-PTP negatively regulates autophagy-mediated survival of damaged cells following UVB exposure, which can contribute to remove damaged keratinocytes via apoptosis.
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spelling doaj-art-eb822cd1d4e34c4d9af9c84a9c51569d2025-08-20T03:04:01ZengNature Publishing GroupCell Death Discovery2058-77162025-02-0111111210.1038/s41420-025-02353-8Loss of TC-PTP in keratinocytes leads to increased UVB-induced autophagyObed Asare0Lindsey Shim1Cheol-Jung Lee2Jose Delgado3Natasha Quailes4Klarissa Zavala5Junsoo Park6Bilal Bin Hafeez7Yong-Yeon Cho8Subhash C. Chauhan9Dae Joon Kim10Department of Medicine and Oncology, School of Medicine, University of Texas Rio Grande ValleyDepartment of Medicine and Oncology, School of Medicine, University of Texas Rio Grande ValleyDepartment of Medicine and Oncology, School of Medicine, University of Texas Rio Grande ValleySchool of Medicine, University of Texas Rio Grande ValleySchool of Medicine, University of Texas Rio Grande ValleyDepartment of Health & Biomedical Sciences, College of Health Professions, University of Texas Rio Grande ValleyDivision of Biological Science and Technology, Yonsei UniversityDepartment of Medicine and Oncology, School of Medicine, University of Texas Rio Grande ValleyCollege of Pharmacy, The Catholic University of Korea, Bucheon-siDepartment of Medicine and Oncology, School of Medicine, University of Texas Rio Grande ValleyDepartment of Medicine and Oncology, School of Medicine, University of Texas Rio Grande ValleyAbstract Ultraviolet B (UVB) radiation can distort cellular homeostasis and predispose the skin to carcinogenesis. Amongst the deteriorating effects of the sun’s UVB radiation on cellular homeostasis is the formation of DNA photoproducts. These photoproducts can cause significant changes in the structure and conformation of DNA, inducing gene mutations which may accumulate to trigger the formation of skin cancer. Photoproducts are typically repaired by nucleotide excision repair. Notwithstanding, when the repair mechanism fails, apoptosis ensues to prevent the accumulation of mutations and to restore cellular homeostasis. This present study reports that T-cell protein tyrosine phosphatase (TC-PTP) can increase UVB-induced apoptosis by inhibiting autophagy-mediated cell survival of damaged keratinocytes. TC-PTP deficiency in 3PC mouse keratinocytes led to the formation of autophagic vacuoles and increased expression of LC3-II. We established human TC-PTP-deficient (TC-PTP/KO) HaCaT cells using the CRISPR/Cas9 system. TC-PTP/KO HaCaT cells exhibited increased cell survival upon UVB exposure, which was accompanied by increased expression of LC3-II and decreased expression of p62 compared to control cells. Pretreatment of TC-PTP/KO HaCaT cells with early-phase autophagy inhibitor, 3-methyladenine significantly decreased the expression of LC3-II and reduced cell survival in response to UVB irradiation in comparison with untreated TC-PTP/KO cells. Pretreatment of TC-PTP/KO HaCaT cells with late-phase inhibitor, chloroquine also significantly reduced cell viability with increased accumulation of LC3-II after UVB irradiation compared to untreated counterpart cells. While UVB significantly increased apoptosis in the engineered (Mock) cells, this was not observed in similarly treated TC-PTP/KO HaCaT cells. However, chloroquine treatment increased apoptosis in TC-PTP/KO HaCaT cells. Examination of human squamous cell carcinomas (SCCs) revealed that TC-PTP expression was inversely correlated with LC3 expression. Our findings suggest that TC-PTP negatively regulates autophagy-mediated survival of damaged cells following UVB exposure, which can contribute to remove damaged keratinocytes via apoptosis.https://doi.org/10.1038/s41420-025-02353-8
spellingShingle Obed Asare
Lindsey Shim
Cheol-Jung Lee
Jose Delgado
Natasha Quailes
Klarissa Zavala
Junsoo Park
Bilal Bin Hafeez
Yong-Yeon Cho
Subhash C. Chauhan
Dae Joon Kim
Loss of TC-PTP in keratinocytes leads to increased UVB-induced autophagy
Cell Death Discovery
title Loss of TC-PTP in keratinocytes leads to increased UVB-induced autophagy
title_full Loss of TC-PTP in keratinocytes leads to increased UVB-induced autophagy
title_fullStr Loss of TC-PTP in keratinocytes leads to increased UVB-induced autophagy
title_full_unstemmed Loss of TC-PTP in keratinocytes leads to increased UVB-induced autophagy
title_short Loss of TC-PTP in keratinocytes leads to increased UVB-induced autophagy
title_sort loss of tc ptp in keratinocytes leads to increased uvb induced autophagy
url https://doi.org/10.1038/s41420-025-02353-8
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