USP22 mediates the multidrug resistance of hepatocellular carcinoma via the SIRT1/AKT/MRP1 signaling pathway

Molecular Oncology

Volumn 11, Issue 6, 2017, Pages 682-695

  Ling, S ^a,b,c,d   Li, Jie ^a,b,c   Shan, Qiaonan ^a,b,c   Dai, Haojiang ^a,b,c   Lu, Di ^a,b,c   Wen, Xue ^e   Song, Penghong ^a,b,c   Xie, Haiyang ^a,b,c   Zhou, Lin ^a,b,c   Liu, Jimin ^f   Xu, Xiao ^a,b,c   Zheng, Shusen ^a,b,c  

^a ZHEJIANG UNIVERSITY   (China)

^b BEIJING HOSPITAL   (China)

^c KEY LABORATORY OF ORGAN TRANSPLANTATION   (China)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^f MCMASTER UNIVERSITY   (Canada)

Author keywords

Hepatocellular carcinoma; MRP1; Multidrug resistance; SIRT1; USP22

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CASPASE 3; DEUBIQUITINASE; FLUOROURACIL; GLYCOGEN SYNTHASE KINASE 3BETA; MESSENGER RNA; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 1; PROTEIN KINASE B; SIRTUIN 1; TUMOR MARKER; UBIQUITIN SPECIFIC PROTEASE 22; UNCLASSIFIED DRUG; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; ABC TRANSPORTER SUBFAMILY B; ABCB1 PROTEIN, HUMAN; AKTIP PROTEIN, HUMAN; APOPTOSIS REGULATORY PROTEIN; CHROMONE DERIVATIVE; ENZYME INHIBITOR; MORPHOLINE DERIVATIVE; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN; MULTIDRUG RESISTANCE-ASSOCIATED PROTEIN 1; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SIRT1 PROTEIN, HUMAN; THIOL ESTER HYDROLASE; USP22 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER STEM CELL; CELL PROLIFERATION; CHEMOSENSITIVITY; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MALE; MOUSE; MULTIDRUG RESISTANCE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANALYSIS OF VARIANCE; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; DRUG RESISTANCE; DRUG SCREENING; GENETICS; LIVER TUMOR; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS REGULATORY PROTEINS; ATP BINDING CASSETTE TRANSPORTER, SUB-FAMILY B; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CHROMONES; DISEASE MODELS, ANIMAL; DOWN-REGULATION; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; ENZYME INHIBITORS; HUMANS; LIVER NEOPLASMS; MALE; MICE; MICE, NUDE; MORPHOLINES; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; SIRTUIN 1; THIOLESTER HYDROLASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85025626937     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1002/1878-0261.12067     Document Type: Article

References (42)

1. Armour SM, Bennett EJ, Braun CR, Zhang XY, McMahon SB, Gygi SP, Harper JW and Sinclair DA (2013) A high-confidence interaction map identifies SIRT1 as a mediator of acetylation of USP22 and the SAGA coactivator complex. Mol Cell Biol 33, 1487-1502.
2. Atanassov BS, Evrard YA, Multani AS, Zhang Z, Tora L, Devys D, Chang S and Dent SY (2009) Gcn5 and SAGA regulate shelterin protein turnover and telomere maintenance. Mol Cell 35, 352-364.
3. Azim HA Jr, Peccatori FA, Brohee S, Branstetter D, Loi S, Viale G, Piccart M, Dougall WC, Pruneri G and Sotiriou C (2015) RANK-ligand (RANKL) expression in young breast cancer patients and during pregnancy. Breast Cancer Res 17, 24.
4. Bellet MM, Masri S, Astarita G, Sassone-Corsi P, Della Fazia MA and Servillo G (2016) Histone deacetylase SIRT1 controls proliferation, circadian rhythm, and lipid metabolism during liver regeneration in mice. J Biol Chem 291, 23318-23329.
5. Bhattacharya B, Mohd Omar MF and Soong R (2016) The Warburg effect and drug resistance. Br J Pharmacol 173, 970-979.
6. Chan LH, Luk ST and Ma S (2015) Turning hepatic cancer stem cells inside out - a deeper understanding through multiple perspectives. Mol Cells 38, 202-209.
7. Chan SL, Wong AM, Lee K, Wong N and Chan AK (2016) Personalized therapy for hepatocellular carcinoma: where are we now? Cancer Treat Rev 45,77-86.
8. Chen HC, Jeng YM, Yuan RH, Hsu HC and Chen YL (2012) SIRT1 promotes tumorigenesis and resistance to chemotherapy in hepatocellular carcinoma and its expression predicts poor prognosis. Ann Surg Oncol 19, 2011-2019.
9. Cheng AL, Kang YK, Chen Z, Tsao CJ, Qin S, Kim JS, Luo R, Feng J, Ye S, Yang TS et al. (2009) Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 10,25-34.
10. Cheng L, Luo S, Jin C, Ma H, Zhou H and Jia L (2013) FUT family mediates the multidrug resistance of human hepatocellular carcinoma via the P13K/Akt signaling pathway. Cell Death Dis 4, e923.
11. Ge S and Huang D (2015) Systemic therapies for hepatocellular carcinoma. Drug Discov Ther 9, 352-362.
12. Glinsky GV (2005) Death-from-cancer signatures and stem cell contribution to metastatic cancer. Cell Cycle 4, 1171-1175.
13. Glinsky GV (2006) Genomic models of metastatic cancer: functional analysis of death-from-cancer signature genes reveals aneuploid, anoikis-resistant, metastasis-enabling phenotype with altered cell cycle control and activated Polycomb Group (PcG) protein chromatin silencing pathway. Cell Cycle 5, 1208-1216.
14. Glinsky GV, Berezovska O and Glinskii AB (2005) Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. J Clin Invest 115, 1503-1521.
15. He Y, Jin YJ, Zhang YH, Meng HX, Zhao BS, Jiang Y, Zhu JW, Liang GY, Kong D and Jin XM (2015) Ubiquitin-specific peptidase 22 overexpression may promote cancer progression and poor prognosis in human gastric carcinoma. Transl Res 165, 407-416.
16. Kathawala RJ, Gupta P, Ashby CR Jr and Chen ZS (2015) The modulation of ABC transporter-mediated multidrug resistance in cancer: a review of the past decade. Drug Resist Updat 18,1-17.
17. Li L, Wei XH, Pan YP, Li HC, Yang H, He QH, Pang Y, Shan Y, Xiong FX, Shao GZ et al. (2010) LAPTM4B: a novel cancer-associated gene motivates multidrug resistance through efflux and activating P13K/AKT signaling. Oncogene 29, 5785-5795.
18. Lin DY, Lin SM and Liaw YF (1997) Non-surgical treatment of hepatocellular carcinoma. J Gastroenterol Hepatol 12, S319-S328.
19. Lin Z, Tan C, Qiu Q, Kong S, Yang H, Zhao F, Liu Z, Li J, Kong Q, Gao B et al. (2015) Ubiquitin-specific protease 22 is a deubiquitinase of CCNB1. Cell Discov 1, pii: 15028.
20. Lin Z, Yang H, Kong Q, Li J, Lee SM, Gao B, Dong H, Wei J, Song J, Zhang DD et al. (2012) USP22 antagonizes p53 transcriptional activation by deubiquitinating Sirt1 to suppress cell apoptosis and is required for mouse embryonic development. Mol Cell 46, 484-494.
21. Ling S, Feng T, Ke Q, Fan N, Li L, Li Z, Dong C, Wang C, Xu F, Li Y et al. (2014a) Metformin inhibits proliferation and enhances chemosensitivity of intrahepatic cholangiocarcinoma cell lines. Oncol Rep 31, 2611-2618.
22. Ling X, He Y, Zhang G, Zhou Y and Yan B (2012b) Increased P-glycoprotein expression in mitochondria is related to acquired multidrug resistance in human hepatoma cells depleted of mitochondrial DNA. Int J Oncol 40, 109-118.
23. Ling SB, Sun DG, Tang B, Guo C, Zhang Y, Liang R, Wang LM (2012a) Knock-down of USP22 by small interfering RNA interference inhibits HepG2 cell proliferation and induces cell cycle arrest. Cell Mol Biol (Noisy-le-grand) 58(Suppl), OL1803-OL1808.
24. Ling S, Tian Y, Zhang H, Jia K, Feng T, Sun D, Gao Z, Xu F, Hou Z, Li Y et al. (2014b) Metformin reverses multidrug resistance in human hepatocellular carcinoma Be17402/5-fluorouracil cells. Mol Med Rep 10, 2891-2897.
25. Liu YL, Jiang SX, Yang YM, Xu H, Liu JL and Wang XS (2012) USP22 acts as an oncogene by the activation of BMI-1-mediated INK4a/ARF pathway and Akt pathway. Cell Biochem Biophys 62, 229-235.
26. Melo-Cardenas J, Zhang Y, Zhang DD and Fang D (2016) Ubiquitin-specific peptidase 22 functions and its involvement in disease. Oncotarget 7, 44848-44856.
27. Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM, Sixma TK and Bernards R (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786.
28. Ou X, Lee MR, Huang X, Messina-Graham S and Broxmeyer HE (2014) SIRT1 positively regulates autophagy and mitochondria function in embryonic stem cells under oxidative stress. Stem Cells 32, 1183-1194.
29. Pinton G, Manente AG, Murer B, De Marino E, Mutti L and Moro L (2013) PARP1 inhibition affects pleural mesothelioma cell viability and uncouples AKT/mTOR axis via SIRT1. J Cell Mol Med 17, 233-241.
30. Qian JQ, Sun P, Pan ZY and Fang ZZ (2015) Annonaceous acetogenins reverses drug resistance of human hepatocellular carcinoma BEL-7402/5-FU and HepG2/ADM cell lines. Int J Clin Exp Pathol 8, 11934-11944.
31. Qin S, Bai Y, Lim HY, Thongprasert S, Chao Y, Fan J, Yang TS, Bhudhisawasdi V, Kang WK, Zhou Y et al. (2013) Randomized, multicenter, open-label study of oxaliplatin plus fluorouracil/leucovorin versus doxorubicin as palliative chemotherapy in patients with advanced hepatocellular carcinoma from Asia. J Clin Oncol 31, 3501-3508.
32. Reyes-Turcu FE, Ventii KH and Wilkinson KD (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 78, 363-397.
33. Sundaresan NR, Pillai VB, Wolfgeher D, Samant S, Vasudevan P, Parekh V, Raghuraman H, Cunningham JM, Gupta M, Gupta MP (2011) The deacetylase SIRT1 promotes membrane localization and activation of Akt and PDK1 during tumorigenesis and cardiac hypertrophy. Sci Signal 4, ra46.
34. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J and Jemal A (2015) Global cancer statistics, 2012. CA Cancer J Clin 65,87-108.
35. Wang H, Jia XH, Chen JR, Yi YJ, Wang JY, Li YJ, Xie SY (2016b) HOXB4 knockdown reverses multidrug resistance of human myelogenous leukemia K562/ ADM cells by downregulating P-gp, MRP1 and BCRP expression via P13K/Akt signaling pathway. Int J Oncol 49, 2529-2537.
36. Wang B, Wang D, Yan T and Yuan H (2016a) MiR-138-5p promotes TNF-alpha-induced apoptosis in human intervertebral disc degeneration by targeting SIRT1 through PTEN/P13K/Akt signaling. Exp Cell Res 345, 199-205.
37. Wolking S, Schaeffeler E, Lerche H, Schwab M and Nies AT (2015) Impact of genetic polymorphisms of ABCB1 (MDR1, P-Glycoprotein) on drug disposition and potential clinical implications: update of the literature. Clin Pharmacokinet 54, 709-735.
38. Zaanan A, Williet N, Hebbar M, Dabakuyo TS, Fartoux L, Mansourbakht T, Dubreuil O, Rosmorduc O, Cattan S, Bonnetain F et al. (2013) Gemcitabine plus oxaliplatin in advanced hepatocellular carcinoma: a large multicenter AGEO study. J Hepatol 58,81-88.
39. Zhang XY, Varthi M, Sykes SM, Phillips C, Warzecha C, Zhu W, Wyce A, Thorne AW, Berger SL and McMahon SB (2008) The putative cancer stem cell marker USP22 is a subunit of the human SAGA complex required for activated transcription and cell-cycle progression. Mol Cell 29, 102-111.
40. Zhou A, Lin K, Zhang S, Chen Y, Zhang N, Xue J, Wang Z, Aldape KD, Xie K, Woodgett JR et al. (2016) Nuclear GSK3beta promotes tumorigenesis by phosphorylating KDM1A and inducing its deubiquitylation by USP22. Nat Cell Biol 18, 954-966.
41. Zhuang YJ, Liao ZW, Yu HW, Song XL, Liu Y, Shi XY, Lin XD and Zhou TC (2015) ShRNA-mediated silencing of the ubiquitin-specific protease 22 gene restrained cell progression and affected the Akt pathway in nasopharyngeal carcinoma. Cancer Biol Ther 16,88-96.
42. van Zijl F, Mall S, Machat G, Pirker C, Zeillinger R, Weinhaeusel A, Bilban M, Berger W and Mikulits W (2011) A human model of epithelial to mesenchymal transition to monitor drug efficacy in hepatocellular carcinoma progression. Mol Cancer Ther 10, 850-860.