Repression of GRIM19 expression potentiates cisplatin chemoresistance in advanced bladder cancer cells via disrupting ubiquitination-mediated Bcl-xL degradation
Objective The mainstay of treatment for advanced bladder cancer (BC) is cisplatin (CDDP)-based systematic chemotherapy. However, acquired chemoresistance induced by as yet unidentified mechanisms is encountered frequently and often results in treatment failure and disease progression. The present st...
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Published in | Cancer chemotherapy and pharmacology Vol. 82; no. 4; pp. 593 - 605 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
Berlin/Heidelberg
Springer Berlin Heidelberg
01.10.2018
Springer Nature B.V |
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Abstract | Objective
The mainstay of treatment for advanced bladder cancer (BC) is cisplatin (CDDP)-based systematic chemotherapy. However, acquired chemoresistance induced by as yet unidentified mechanisms is encountered frequently and often results in treatment failure and disease progression. The present study was designed to elucidate the expression and potential role of the gene associated with retinoid-interferon-induced mortality-19 (GRIM19) in the pathogenesis of CDDP resistance in BC.
Methods
RT-qPCR and immunoblotting were employed to evaluate the expression profile of GRIM19 in clinical BC samples and in different BC cells. Using cell viability assay, apoptotic ELISA, xenografts mouse model, and Transwell assay, the effects of GRIM19 inhibition or GRIM19 overexpression on CDDP resistance were determined in different BC cells. Lastly, using co-immunoprecipitation, we provided the molecular evidence for the interaction between GRIM19 and Bcl-xL.
Results
Expression levels of GRIM19 were significantly down-regulated in recurrent BC specimens, and in experimentally induced CDDP-resistant BC cells. Functionally, overexpression of the exogenous GRIM19 potentiated CDDP sensitivity and suppressed the survival and invasion of BC cells in the presence of CDDP challenge. Mechanistically, the compromised CDDP chemosensitization induced by GRIM19 loss was at least partially attributed to the attenuation of Bcl-xL polyubiquitination and subsequent degradation, because (1) GRIM19 colocalized with Bcl-xL in the mitochondria of BC cells and (2) GRIM19 overexpression promoted the ubiquitination of Bcl-xL, and this event could be effectively reversed by pretreatment with inhibitors of p38-MAPK and JNK pathways, indicating that GRIM19 overexpression-induced Bcl-xL ubiquitination may achieve in a p38/JNK-dependent manner. Using the UMUC-3 cells stably depleted of endogenous GRIM19, we further show that inhibition of Bcl-xL rectified GRIM19 deficiency-caused CDDP resistance in BC cells. In addition,
BCL2L1
mRNA levels were negatively correlated with GRIM19 mRNA levels in CDDP-associated clinical BC tissues.
Conclusions
Disruption of GRIM19/Bcl-xL is a key mechanism of CDDP resistance in advanced BC. Therapeutically, enhancement of GRIM19 expression or employment of p38/JNK inhibitors may serve as resensitizing therapies for subgroups of CDDP-resistant or refractory BC patients. |
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AbstractList | OBJECTIVEThe mainstay of treatment for advanced bladder cancer (BC) is cisplatin (CDDP)-based systematic chemotherapy. However, acquired chemoresistance induced by as yet unidentified mechanisms is encountered frequently and often results in treatment failure and disease progression. The present study was designed to elucidate the expression and potential role of the gene associated with retinoid-interferon-induced mortality-19 (GRIM19) in the pathogenesis of CDDP resistance in BC. METHODSRT-qPCR and immunoblotting were employed to evaluate the expression profile of GRIM19 in clinical BC samples and in different BC cells. Using cell viability assay, apoptotic ELISA, xenografts mouse model, and Transwell assay, the effects of GRIM19 inhibition or GRIM19 overexpression on CDDP resistance were determined in different BC cells. Lastly, using co-immunoprecipitation, we provided the molecular evidence for the interaction between GRIM19 and Bcl-xL. RESULTSExpression levels of GRIM19 were significantly down-regulated in recurrent BC specimens, and in experimentally induced CDDP-resistant BC cells. Functionally, overexpression of the exogenous GRIM19 potentiated CDDP sensitivity and suppressed the survival and invasion of BC cells in the presence of CDDP challenge. Mechanistically, the compromised CDDP chemosensitization induced by GRIM19 loss was at least partially attributed to the attenuation of Bcl-xL polyubiquitination and subsequent degradation, because (1) GRIM19 colocalized with Bcl-xL in the mitochondria of BC cells and (2) GRIM19 overexpression promoted the ubiquitination of Bcl-xL, and this event could be effectively reversed by pretreatment with inhibitors of p38-MAPK and JNK pathways, indicating that GRIM19 overexpression-induced Bcl-xL ubiquitination may achieve in a p38/JNK-dependent manner. Using the UMUC-3 cells stably depleted of endogenous GRIM19, we further show that inhibition of Bcl-xL rectified GRIM19 deficiency-caused CDDP resistance in BC cells. In addition, BCL2L1 mRNA levels were negatively correlated with GRIM19 mRNA levels in CDDP-associated clinical BC tissues. CONCLUSIONSDisruption of GRIM19/Bcl-xL is a key mechanism of CDDP resistance in advanced BC. Therapeutically, enhancement of GRIM19 expression or employment of p38/JNK inhibitors may serve as resensitizing therapies for subgroups of CDDP-resistant or refractory BC patients. The mainstay of treatment for advanced bladder cancer (BC) is cisplatin (CDDP)-based systematic chemotherapy. However, acquired chemoresistance induced by as yet unidentified mechanisms is encountered frequently and often results in treatment failure and disease progression. The present study was designed to elucidate the expression and potential role of the gene associated with retinoid-interferon-induced mortality-19 (GRIM19) in the pathogenesis of CDDP resistance in BC. RT-qPCR and immunoblotting were employed to evaluate the expression profile of GRIM19 in clinical BC samples and in different BC cells. Using cell viability assay, apoptotic ELISA, xenografts mouse model, and Transwell assay, the effects of GRIM19 inhibition or GRIM19 overexpression on CDDP resistance were determined in different BC cells. Lastly, using co-immunoprecipitation, we provided the molecular evidence for the interaction between GRIM19 and Bcl-xL. Expression levels of GRIM19 were significantly down-regulated in recurrent BC specimens, and in experimentally induced CDDP-resistant BC cells. Functionally, overexpression of the exogenous GRIM19 potentiated CDDP sensitivity and suppressed the survival and invasion of BC cells in the presence of CDDP challenge. Mechanistically, the compromised CDDP chemosensitization induced by GRIM19 loss was at least partially attributed to the attenuation of Bcl-xL polyubiquitination and subsequent degradation, because (1) GRIM19 colocalized with Bcl-xL in the mitochondria of BC cells and (2) GRIM19 overexpression promoted the ubiquitination of Bcl-xL, and this event could be effectively reversed by pretreatment with inhibitors of p38-MAPK and JNK pathways, indicating that GRIM19 overexpression-induced Bcl-xL ubiquitination may achieve in a p38/JNK-dependent manner. Using the UMUC-3 cells stably depleted of endogenous GRIM19, we further show that inhibition of Bcl-xL rectified GRIM19 deficiency-caused CDDP resistance in BC cells. In addition, BCL2L1 mRNA levels were negatively correlated with GRIM19 mRNA levels in CDDP-associated clinical BC tissues. Disruption of GRIM19/Bcl-xL is a key mechanism of CDDP resistance in advanced BC. Therapeutically, enhancement of GRIM19 expression or employment of p38/JNK inhibitors may serve as resensitizing therapies for subgroups of CDDP-resistant or refractory BC patients. Objective The mainstay of treatment for advanced bladder cancer (BC) is cisplatin (CDDP)-based systematic chemotherapy. However, acquired chemoresistance induced by as yet unidentified mechanisms is encountered frequently and often results in treatment failure and disease progression. The present study was designed to elucidate the expression and potential role of the gene associated with retinoid-interferon-induced mortality-19 (GRIM19) in the pathogenesis of CDDP resistance in BC. Methods RT-qPCR and immunoblotting were employed to evaluate the expression profile of GRIM19 in clinical BC samples and in different BC cells. Using cell viability assay, apoptotic ELISA, xenografts mouse model, and Transwell assay, the effects of GRIM19 inhibition or GRIM19 overexpression on CDDP resistance were determined in different BC cells. Lastly, using co-immunoprecipitation, we provided the molecular evidence for the interaction between GRIM19 and Bcl-xL. Results Expression levels of GRIM19 were significantly down-regulated in recurrent BC specimens, and in experimentally induced CDDP-resistant BC cells. Functionally, overexpression of the exogenous GRIM19 potentiated CDDP sensitivity and suppressed the survival and invasion of BC cells in the presence of CDDP challenge. Mechanistically, the compromised CDDP chemosensitization induced by GRIM19 loss was at least partially attributed to the attenuation of Bcl-xL polyubiquitination and subsequent degradation, because (1) GRIM19 colocalized with Bcl-xL in the mitochondria of BC cells and (2) GRIM19 overexpression promoted the ubiquitination of Bcl-xL, and this event could be effectively reversed by pretreatment with inhibitors of p38-MAPK and JNK pathways, indicating that GRIM19 overexpression-induced Bcl-xL ubiquitination may achieve in a p38/JNK-dependent manner. Using the UMUC-3 cells stably depleted of endogenous GRIM19, we further show that inhibition of Bcl-xL rectified GRIM19 deficiency-caused CDDP resistance in BC cells. In addition, BCL2L1 mRNA levels were negatively correlated with GRIM19 mRNA levels in CDDP-associated clinical BC tissues. Conclusions Disruption of GRIM19/Bcl-xL is a key mechanism of CDDP resistance in advanced BC. Therapeutically, enhancement of GRIM19 expression or employment of p38/JNK inhibitors may serve as resensitizing therapies for subgroups of CDDP-resistant or refractory BC patients. |
Author | Yu, Jin Hu, Xiao-jian Zhou, Sheng Ni, Feng Yan, Chang-you Hui, Peng-yu Du, Yong-hui Zhang, Zhi-gang Zheng, Liang |
Author_xml | – sequence: 1 givenname: Feng surname: Ni fullname: Ni, Feng organization: Department of Urology, The 2nd Affiliated Hospital of Xi’an Medical University – sequence: 2 givenname: Chang-you surname: Yan fullname: Yan, Chang-you organization: Family Planning Service Stations of Health and Family Planning Commission of Chengcheng County – sequence: 3 givenname: Sheng surname: Zhou fullname: Zhou, Sheng email: 997196691@qq.com organization: Department of Anorectal Surgery, The 2nd Affiliated Hospital of Xi’an Medical University – sequence: 4 givenname: Peng-yu surname: Hui fullname: Hui, Peng-yu organization: Department of Urology, The 2nd Affiliated Hospital of Xi’an Medical University – sequence: 5 givenname: Yong-hui surname: Du fullname: Du, Yong-hui organization: Department of Urology, The 2nd Affiliated Hospital of Xi’an Medical University – sequence: 6 givenname: Liang surname: Zheng fullname: Zheng, Liang organization: Department of Urology, The 2nd Affiliated Hospital of Xi’an Medical University – sequence: 7 givenname: Jin surname: Yu fullname: Yu, Jin organization: Department of Urology, The 2nd Affiliated Hospital of Xi’an Medical University – sequence: 8 givenname: Xiao-jian surname: Hu fullname: Hu, Xiao-jian organization: Department of Urology, The 2nd Affiliated Hospital of Xi’an Medical University – sequence: 9 givenname: Zhi-gang surname: Zhang fullname: Zhang, Zhi-gang organization: Department of Urology, The 2nd Affiliated Hospital of Xi’an Medical University |
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CitedBy_id | crossref_primary_10_3390_ijms21020418 crossref_primary_10_2174_2589977512666200220122650 crossref_primary_10_1016_j_drup_2023_100938 crossref_primary_10_3389_fimmu_2023_1202633 crossref_primary_10_1007_s13205_020_02237_x crossref_primary_10_1002_advs_202302002 |
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Keywords | Bcl-xL GRIM19 Bladder cancer Cisplatin Chemoresistance |
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The mainstay of treatment for advanced bladder cancer (BC) is cisplatin (CDDP)-based systematic chemotherapy. However, acquired chemoresistance... The mainstay of treatment for advanced bladder cancer (BC) is cisplatin (CDDP)-based systematic chemotherapy. However, acquired chemoresistance induced by as... ObjectiveThe mainstay of treatment for advanced bladder cancer (BC) is cisplatin (CDDP)-based systematic chemotherapy. However, acquired chemoresistance... OBJECTIVEThe mainstay of treatment for advanced bladder cancer (BC) is cisplatin (CDDP)-based systematic chemotherapy. However, acquired chemoresistance... |
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SubjectTerms | Apoptosis Attenuation Bcl-x protein Bladder Bladder cancer Cancer Cancer Research Chemoresistance Chemosensitization Chemotherapy Cisplatin Degradation Enzyme-linked immunosorbent assay Gene expression Immunoblotting Immunoprecipitation Inhibition Inhibitors Interferon MAP kinase Medical treatment Medicine Medicine & Public Health Mitochondria Molecular chains mRNA Oncology Original Article Pathogenesis Pharmacology/Toxicology Subgroups Ubiquitination Xenografts Xenotransplantation |
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Title | Repression of GRIM19 expression potentiates cisplatin chemoresistance in advanced bladder cancer cells via disrupting ubiquitination-mediated Bcl-xL degradation |
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