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Mini-Reviews in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

Mini-Review Article

Secretory Clusterin: A Promising Target for Chemoresistance of Hepatocellular Carcinoma

Author(s): Jie Zhang, Mengna Wu, Yuqing Xu, Qianqian Song and Wenjie Zheng*

Volume 20, Issue 12, 2020

Page: [1153 - 1165] Pages: 13

DOI: 10.2174/1389557520666200331072122

Price: $65

Abstract

Hepatocellular carcinoma (HCC) is a leading cause of cancer-related deaths worldwide. Chemoresistance remains the major factor for limited efficacy of the HCC treatment. Thus, exploring the mechanisms underlying drug resistance is of great importance. Secretory clusterin (sCLU), a stressactivated and ATP-independent molecular chaperone, is up-regulated in numerous tumors and correlated with malignant phenotypes. For HCC, the implication of sCLU was previously addressed in tumor growth, metastasis, as well as early diagnosis and poor prognosis. Notably, accumulating studies have emphasized its vital role in drug resistance of HCC. Depletion of sCLU synergistically could enhance the sensitivity of HCC cells to a variety of chemotherapy agents. Herein, we summarized the potential mechanisms accounting for the sCLU-induced chemoresistance, including promoting apoptosis evasion, facilitating epithelial-mesenchymal transition (EMT), maintaining the viability of cancer stem cell (CSC), enhancing drug efflux capacity, and regulating autophagic activities. The current evidence suggest that targeting sCLU might be a promising approach in overcoming chemoresistance of HCC.

Keywords: Hepatocellular carcinoma, secretory clusterin, drug resistance, molecular target, cancer, sCLU.

Graphical Abstract
[1]
Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2018, 68(6), 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[2]
Lange, N.; Dufour, J.F. Changing Epidemiology of HCC: How to Screen and Identify Patients at Risk? Dig. Dis. Sci., 2019, 64(4), 903-909.
[http://dx.doi.org/10.1007/s10620-019-05515-8] [PMID: 30863952]
[3]
Marengo, A.; Rosso, C.; Bugianesi, E. Liver Cancer: Connections with Obesity, Fatty Liver, and Cirrhosis. Annu. Rev. Med., 2016, 67, 103-117.
[http://dx.doi.org/10.1146/annurev-med-090514-013832] [PMID: 26473416]
[4]
Anstee, Q.M.; Reeves, H.L.; Kotsiliti, E.; Govaere, O.; Heikenwalder, M. From NASH to HCC: current concepts and future challenges. Nat. Rev. Gastroenterol. Hepatol., 2019, 16(7), 411-428.
[http://dx.doi.org/10.1038/s41575-019-0145-7] [PMID: 31028350]
[5]
Bruix, J.; Reig, M.; Sherman, M. Evidence-Based Diagnosis, Staging, and Treatment of Patients With Hepatocellular Carcinoma. Gastroenterology, 2016, 150(4), 835-853.
[http://dx.doi.org/10.1053/j.gastro.2015.12.041] [PMID: 26795574]
[6]
Roxburgh, P.; Evans, T.R. Systemic therapy of hepatocellular carcinoma: are we making progress? Adv. Ther., 2008, 25(11), 1089-1104.
[http://dx.doi.org/10.1007/s12325-008-0113-z] [PMID: 18972075]
[7]
Palmer, D.H. Sorafenib in advanced hepatocellular carcinoma. N. Engl. J. Med., 2008, 359(23), 2498.
[PMID: 19065750]
[8]
Kudo, M.; Finn, R.S.; Qin, S.; Han, K.H.; Ikeda, K.; Piscaglia, F.; Baron, A.; Park, J.W.; Han, G.; Jassem, J.; Blanc, J.F.; Vogel, A.; Komov, D.; Evans, T.R.J.; Lopez, C.; Dutcus, C.; Guo, M.; Saito, K.; Kraljevic, S.; Tamai, T.; Ren, M.; Cheng, A.L. Lenvatinib versus sorafenib in first-line treatment of patients with unresectable hepatocellular carcinoma: a randomised phase 3 non-inferiority trial. Lancet, 2018, 391(10126), 1163-1173.
[http://dx.doi.org/10.1016/S0140-6736(18)30207-1] [PMID: 29433850]
[9]
Shlomai, A.; Leshno, M.; Goldstein, D.A. Regorafenib treatment for patients with hepatocellular carcinoma who progressed on sorafenib-A cost-effectiveness analysis. PLoS One, 2018, 13(11) e0207132
[http://dx.doi.org/10.1371/journal.pone.0207132] [PMID: 30408106]
[10]
Abou-Alfa, G.K.; Meyer, T.; Cheng, A.L.; El-Khoueiry, A.B.; Rimassa, L.; Ryoo, B.Y.; Cicin, I.; Merle, P.; Chen, Y.; Park, J.W.; Blanc, J.F.; Bolondi, L.; Klümpen, H.J.; Chan, S.L.; Zagonel, V.; Pressiani, T.; Ryu, M.H.; Venook, A.P.; Hessel, C.; Borgman-Hagey, A.E.; Schwab, G.; Kelley, R.K. Cabozantinib in Patients with Advanced and Progressing Hepatocellular Carcinoma. N. Engl. J. Med., 2018, 379(1), 54-63.
[http://dx.doi.org/10.1056/NEJMoa1717002] [PMID: 29972759]
[11]
El-Khoueiry, A.B.; Sangro, B.; Yau, T.; Crocenzi, T.S.; Kudo, M.; Hsu, C.; Kim, T.Y.; Choo, S.P.; Trojan, J.; Welling, T.H.R.; Meyer, T.; Kang, Y.K.; Yeo, W.; Chopra, A.; Anderson, J.; Dela Cruz, C.; Lang, L.; Neely, J.; Tang, H.; Dastani, H.B.; Melero, I. Nivolumab in patients with advanced hepatocellular carcinoma (CheckMate 040): an open-label, non-comparative, phase 1/2 dose escalation and expansion trial. Lancet, 2017, 389(10088), 2492-2502.
[http://dx.doi.org/10.1016/S0140-6736(17)31046-2] [PMID: 28434648]
[12]
Zhu, A.X.; Finn, R.S.; Edeline, J.; Cattan, S.; Ogasawara, S.; Palmer, D.; Verslype, C.; Zagonel, V.; Fartoux, L.; Vogel, A.; Sarker, D.; Verset, G.; Chan, S.L.; Knox, J.; Daniele, B.; Webber, A.L.; Ebbinghaus, S.W.; Ma, J.; Siegel, A.B.; Cheng, A.L.; Kudo, M. KEYNOTE-224 investigators. Pembrolizumab in patients with advanced hepatocellular carcinoma previously treated with sorafenib (KEYNOTE-224): a non-randomised, open-label phase 2 trial. Lancet Oncol., 2018, 19(7), 940-952.
[http://dx.doi.org/10.1016/S1470-2045(18)30351-6] [PMID: 29875066]
[13]
Jia, H.; Liu, W.; Zhang, B.; Wang, J.; Wu, P.; Tandra, N.; Liang, Z.; Ji, C.; Yin, L.; Hu, X.; Yan, Y.; Mao, F.; Zhang, X.; Yu, J.; Xu, W.; Qian, H. HucMSC exosomes-delivered 14-3-3ζ enhanced autophagy via modulation of ATG16L in preventing cisplatin-induced acute kidney injury. Am. J. Transl. Res., 2018, 10(1), 101-113.
[PMID: 29422997]
[14]
Zhang, Y.; Jia, Q.A.; Kadel, D.; Zhang, X.F.; Zhang, Q.B. Targeting mTORC1/2 Complexes Inhibit Tumorigenesis and Enhance Sensitivity to 5-Flourouracil (5-FU) in Hepatocellular Carcinoma: A Preclinical Study of mTORC1/2-Targeted Therapy in Hepatocellular Carcinoma (HCC). Med. Sci. Monit., 2018, 24, 2735-2743.
[http://dx.doi.org/10.12659/MSM.907514] [PMID: 29720580]
[15]
Padhya, K.T.; Marrero, J.A.; Singal, A.G. Recent advances in the treatment of hepatocellular carcinoma. Curr. Opin. Gastroenterol., 2013, 29(3), 285-292.
[http://dx.doi.org/10.1097/MOG.0b013e32835ff1cf] [PMID: 23507917]
[16]
Breier, A.; Gibalova, L.; Seres, M.; Barancik, M.; Sulova, Z. New insight into p-glycoprotein as a drug target. Anticancer. Agents Med. Chem., 2013, 13(1), 159-170.
[http://dx.doi.org/10.2174/187152013804487380] [PMID: 22931413]
[17]
Ma, S.; Lee, T.K.; Zheng, B.J.; Chan, K.W.; Guan, X.Y. CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene, 2008, 27(12), 1749-1758.
[http://dx.doi.org/10.1038/sj.onc.1210811] [PMID: 17891174]
[18]
Chen, Z.; Shi, T.; Zhang, L.; Zhu, P.; Deng, M.; Huang, C.; Hu, T.; Jiang, L.; Li, J. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family in multidrug resistance: A review of the past decade. Cancer Lett., 2016, 370(1), 153-164.
[http://dx.doi.org/10.1016/j.canlet.2015.10.010] [PMID: 26499806]
[19]
Meena, A.S.; Sharma, A.; Kumari, R.; Mohammad, N.; Singh, S.V.; Bhat, M.K. Inherent and acquired resistance to paclitaxel in hepatocellular carcinoma: molecular events involved. PLoS One, 2013, 8(4) e61524
[http://dx.doi.org/10.1371/journal.pone.0061524] [PMID: 23613870]
[20]
Wakamatsu, T.; Nakahashi, Y.; Hachimine, D.; Seki, T.; Okazaki, K. The combination of glycyrrhizin and lamivudine can reverse the cisplatin resistance in hepatocellular carcinoma cells through inhibition of multidrug resistance-associated proteins. Int. J. Oncol., 2007, 31(6), 1465-1472.
[http://dx.doi.org/10.3892/ijo.31.6.1465] [PMID: 17982673]
[21]
Maehara, Y.; Fernandez-Checa, J.C. Augmenter of liver regeneration links mitochondrial function to steatohepatitis and hepatocellular carcinoma. Gastroenterology, 2015, 148(2), 285-288.
[http://dx.doi.org/10.1053/j.gastro.2014.12.013] [PMID: 25529802]
[22]
Yao, X.; Li, X.; Zhang, D.; Xie, Y.; Sun, B.; Li, H.; Sun, L.; Zhang, X. B-cell lymphoma 2 inhibitor ABT-737 induces Beclin1- and reactive oxygen species-dependent autophagy in Adriamycin-resistant human hepatocellular carcinoma cells. Tumour Biol., 2017, 39(3) 1010428317695965
[http://dx.doi.org/10.1177/1010428317695965] [PMID: 28351336]
[23]
Guo, Q.; Sui, Z.G.; Xu, W.; Quan, X.H.; Sun, J.L.; Li, X.; Ji, H.Y.; Jing, F.B. Ubenimex suppresses Pim-3 kinase expression by targeting CD13 to reverse MDR in HCC cells. Oncotarget, 2017, 8(42), 72652-72665.
[http://dx.doi.org/10.18632/oncotarget.20194] [PMID: 29069816]
[24]
Brozovic, A. The relationship between platinum drug resistance and epithelial-mesenchymal transition. Arch. Toxicol., 2017, 91(2), 605-619.
[http://dx.doi.org/10.1007/s00204-016-1912-7] [PMID: 28032148]
[25]
Wang, R.; Li, Y.; Hou, Y.; Yang, Q.; Chen, S.; Wang, X.; Wang, Z.; Yang, Y.; Chen, C.; Wang, Z.; Wu, Q. The PDGF-D/miR-106a/Twist1 pathway orchestrates epithelial-mesenchymal transition in gemcitabine resistance hepatoma cells. Oncotarget, 2015, 6(9), 7000-7010.
[http://dx.doi.org/10.18632/oncotarget.3193] [PMID: 25760076]
[26]
Wang, R.; Zhang, Q.; Peng, X.; Zhou, C.; Zhong, Y.; Chen, X.; Qiu, Y.; Jin, M.; Gong, M.; Kong, D.; Stellettin, B. Stellettin B Induces G1 Arrest, Apoptosis and Autophagy in Human Non-small Cell Lung Cancer A549 Cells via Blocking PI3K/Akt/mTOR Pathway. Sci. Rep., 2016, 6, 27071.
[http://dx.doi.org/10.1038/srep27071] [PMID: 27243769]
[27]
Abdul-Ghani, R.; Serra, V.; Györffy, B.; Jürchott, K.; Solf, A.; Dietel, M.; Schäfer, R. The PI3K inhibitor LY294002 blocks drug export from resistant colon carcinoma cells overexpressing MRP1. Oncogene, 2006, 25(12), 1743-1752.
[http://dx.doi.org/10.1038/sj.onc.1209201] [PMID: 16288223]
[28]
Barancík, M.; Bohácová, V.; Sedlák, J.; Sulová, Z.; Breier, A. LY294,002, a specific inhibitor of PI3K/Akt kinase pathway, antagonizes P-glycoprotein-mediated multidrug resistance. Eur. J. Pharm. Sci., 2006, 29(5), 426-434.
[http://dx.doi.org/10.1016/j.ejps.2006.08.006] [PMID: 17010577]
[29]
Kissinger, C.; Skinner, M.K.; Griswold, M.D. Analysis of Sertoli cell-secreted proteins by two-dimensional gel electrophoresis. Biol. Reprod., 1982, 27(1), 233-240.
[http://dx.doi.org/10.1095/biolreprod27.1.233] [PMID: 7115849]
[30]
Wong, P.; Borst, D.E.; Farber, D.; Danciger, J.S.; Tenniswood, M.; Chader, G.J.; van Veen, T. Increased TRPM-2/clusterin mRNA levels during the time of retinal degeneration in mouse models of retinitis pigmentosa. Biochem. Cell Biol., 1994, 72(9-10), 439-446.
[http://dx.doi.org/10.1139/o94-058] [PMID: 7605616]
[31]
Rizzi, F.; Bettuzzi, S. Targeting Clusterin in prostate cancer. J. Physiol. Pharmacol., 2008, 59(Suppl. 9), 265-274.
[PMID: 19261985]
[32]
Zhang, Q.; Zhou, W.; Kundu, S.; Jang, T.L.; Yang, X.; Pins, M.; Smith, N.; Jovanovic, B.; Xin, D.; Liang, L.; Guo, Y.; Lee, C. The leader sequence triggers and enhances several functions of clusterin and is instrumental in the progression of human prostate cancer in vivo and in vitro. BJU Int., 2006, 98(2), 452-460.
[http://dx.doi.org/10.1111/j.1464-410X.2006.06263.x] [PMID: 16879694]
[33]
Rizzi, F.; Coletta, M.; Bettuzzi, S. Chapter 2: Clusterin (CLU): From one gene and two transcripts to many proteins. Adv. Cancer Res., 2009, 104, 9-23.
[http://dx.doi.org/10.1016/S0065-230X(09)04002-0] [PMID: 19878770]
[34]
Trougakos, I.P.; Djeu, J.Y.; Gonos, E.S.; Boothman, D.A. Advances and challenges in basic and translational research on clusterin. Cancer Res., 2009, 69(2), 403-406.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-2912] [PMID: 19147550]
[35]
Trougakos, I.P.; Lourda, M.; Antonelou, M.H.; Kletsas, D.; Gorgoulis, V.G.; Papassideri, I.S.; Zou, Y.; Margaritis, L.H.; Boothman, D.A.; Gonos, E.S. Intracellular clusterin inhibits mitochondrial apoptosis by suppressing p53-activating stress signals and stabilizing the cytosolic Ku70-Bax protein complex. Clin. Cancer Res., 2009, 15(1), 48-59.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-1805] [PMID: 19118032]
[36]
Leskov, K.S.; Araki, S.; Lavik, J.P.; Gomez, J.A.; Gama, V.; Gonos, E.S.; Trougakos, I.P.; Matsuyama, S.; Boothman, D.A. CRM1 protein-mediated regulation of nuclear clusterin (nCLU), an ionizing radiation-stimulated, Bax-dependent pro-death factor. J. Biol. Chem., 2011, 286(46), 40083-40090.
[http://dx.doi.org/10.1074/jbc.M111.252957] [PMID: 21953454]
[37]
Leskov, K.S.; Klokov, D.Y.; Li, J.; Kinsella, T.J.; Boothman, D.A. Synthesis and functional analyses of nuclear clusterin, a cell death protein. J. Biol. Chem., 2003, 278(13), 11590-11600.
[http://dx.doi.org/10.1074/jbc.M209233200] [PMID: 12551933]
[38]
Essabbani, A.; Garcia, L.; Zonetti, M.J.; Fisco, T.; Pucci, S.; Chiocchia, G. Exon-skipping strategy by ratio modulation between cytoprotective versus pro-apoptotic clusterin forms increased sensitivity of LNCaP to cell death. PLoS One, 2013, 8(2) e54920
[http://dx.doi.org/10.1371/journal.pone.0054920] [PMID: 23418433]
[39]
Rosemblit, N.; Chen, C.L. Regulators for the rat clusterin gene: DNA methylation and cis-acting regulatory elements. J. Mol. Endocrinol., 1994, 13(1), 69-76.
[http://dx.doi.org/10.1677/jme.0.0130069] [PMID: 7999255]
[40]
Loison, F.; Debure, L.; Nizard, P.; le Goff, P.; Michel, D.; le Dréan, Y. Up-regulation of the clusterin gene after proteotoxic stress: implication of HSF1-HSF2 heterocomplexes. Biochem. J., 2006, 395(1), 223-231.
[http://dx.doi.org/10.1042/BJ20051190] [PMID: 16336210]
[41]
Michel, D.; Chatelain, G.; North, S.; Brun, G. Stress-induced transcription of the clusterin/apoJ gene. Biochem. J., 1997, 328(Pt 1), 45-50.
[http://dx.doi.org/10.1042/bj3280045] [PMID: 9359832]
[42]
Wong, P.; Pineault, J.; Lakins, J.; Taillefer, D.; Léger, J.; Wang, C.; Tenniswood, M. Genomic organization and expression of the rat TRPM-2 (clusterin) gene, a gene implicated in apoptosis. J. Biol. Chem., 1993, 268(7), 5021-5031.
[PMID: 7680346]
[43]
Cochrane, D.R.; Wang, Z.; Muramaki, M.; Gleave, M.E.; Nelson, C.C. Differential regulation of clusterin and its isoforms by androgens in prostate cells. J. Biol. Chem., 2007, 282(4), 2278-2287.
[http://dx.doi.org/10.1074/jbc.M608162200] [PMID: 17148459]
[44]
Schepeler, T.; Mansilla, F.; Christensen, L.L.; Orntoft, T.F.; Andersen, C.L. Clusterin expression can be modulated by changes in TCF1-mediated Wnt signaling. J. Mol. Signal., 2007, 2, 6.
[http://dx.doi.org/10.1186/1750-2187-2-6] [PMID: 17634137]
[45]
Cervellera, M.; Raschella, G.; Santilli, G.; Tanno, B.; Ventura, A.; Mancini, C.; Sevignani, C.; Calabretta, B.; Sala, A. Direct transactivation of the anti-apoptotic gene apolipoprotein J (clusterin) by B-MYB. J. Biol. Chem., 2000, 275(28), 21055-21060.
[http://dx.doi.org/10.1074/jbc.M002055200] [PMID: 10770937]
[46]
Shiota, M.; Zoubeidi, A.; Kumano, M.; Beraldi, E.; Naito, S.; Nelson, C.C.; Sorensen, P.H.; Gleave, M.E. Clusterin is a critical downstream mediator of stress-induced YB-1 transactivation in prostate cancer. Mol. Cancer Res., 2011, 9(12), 1755-1766.
[http://dx.doi.org/10.1158/1541-7786.MCR-11-0379] [PMID: 21987172]
[47]
Wang, Z.; Huang, J.; Zhong, J.; Wang, G. Molecular cloning, promoter analysis, SNP detection of Clusterin gene and their associations with mastitis in Chinese Holstein cows. Mol. Biol. Rep., 2012, 39(3), 2439-2445.
[http://dx.doi.org/10.1007/s11033-011-0994-9] [PMID: 21667239]
[48]
O’Sullivan, J.; Whyte, L.; Drake, J.; Tenniswood, M. Alterations in the post-translational modification and intracellular trafficking of clusterin in MCF-7 cells during apoptosis. Cell Death Differ., 2003, 10(8), 914-927.
[http://dx.doi.org/10.1038/sj.cdd.4401254] [PMID: 12867999]
[49]
Criswell, T.; Beman, M.; Araki, S.; Leskov, K.; Cataldo, E.; Mayo, L.D.; Boothman, D.A. Delayed activation of insulin-like growth factor-1 receptor/Src/MAPK/Egr-1 signaling regulates clusterin expression, a pro-survival factor. J. Biol. Chem., 2005, 280(14), 14212-14221.
[http://dx.doi.org/10.1074/jbc.M412569200] [PMID: 15689620]
[50]
Sallman, D.A.; Chen, X.; Zhong, B.; Gilvary, D.L.; Zhou, J.; Wei, S.; Djeu, J.Y. Clusterin mediates TRAIL resistance in prostate tumor cells. Mol. Cancer Ther., 2007, 6(11), 2938-2947.
[http://dx.doi.org/10.1158/1535-7163.MCT-07-0345] [PMID: 18025278]
[51]
Rizzi, F.; Bettuzzi, S. The clusterin paradigm in prostate and breast carcinogenesis. Endocr. Relat. Cancer, 2010, 17(1), R1-R17.
[http://dx.doi.org/10.1677/ERC-09-0140] [PMID: 19903745]
[52]
Sala, A.; Bettuzzi, S.; Pucci, S.; Chayka, O.; Dews, M.; Thomas-Tikhonenko, A. Regulation of CLU gene expression by oncogenes and epigenetic factors implications for tumorigenesis. Adv. Cancer Res., 2009, 105, 115-132.
[http://dx.doi.org/10.1016/S0065-230X(09)05007-6] [PMID: 19879426]
[53]
Zoubeidi, A.; Gleave, M. Small heat shock proteins in cancer therapy and prognosis. Int. J. Biochem. Cell Biol., 2012, 44(10), 1646-1656.
[http://dx.doi.org/10.1016/j.biocel.2012.04.010] [PMID: 22571949]
[54]
Trougakos, I.P.; Gonos, E.S. Chapter 9: Oxidative stress in malignant progression: The role of Clusterin, a sensitive cellular biosensor of free radicals. Adv. Cancer Res., 2009, 104, 171-210.
[http://dx.doi.org/10.1016/S0065-230X(09)04009-3] [PMID: 19878777]
[55]
Yerbury, J.J.; Stewart, E.M.; Wyatt, A.R.; Wilson, M.R. Quality control of protein folding in extracellular space. EMBO Rep., 2005, 6(12), 1131-1136.
[http://dx.doi.org/10.1038/sj.embor.7400586] [PMID: 16319958]
[56]
Redondo, M.; Villar, E.; Torres-Muñoz, J.; Tellez, T.; Morell, M.; Petito, C.K. Overexpression of clusterin in human breast carcinoma. Am. J. Pathol., 2000, 157(2), 393-399.
[http://dx.doi.org/10.1016/S0002-9440(10)64552-X] [PMID: 10934144]
[57]
Miyake, H.; Gleave, M.; Kamidono, S.; Hara, I. Overexpression of clusterin in transitional cell carcinoma of the bladder is related to disease progression and recurrence. Urology, 2002, 59(1), 150-154.
[http://dx.doi.org/10.1016/S0090-4295(01)01484-4] [PMID: 11796313]
[58]
Chen, X.; Halberg, R.B.; Ehrhardt, W.M.; Torrealba, J.; Dove, W.F. Clusterin as a biomarker in murine and human intestinal neoplasia. Proc. Natl. Acad. Sci. USA, 2003, 100(16), 9530-9535.
[http://dx.doi.org/10.1073/pnas.1233633100] [PMID: 12886021]
[59]
Steinberg, J.; Oyasu, R.; Lang, S.; Sintich, S.; Rademaker, A.; Lee, C.; Kozlowski, J.M.; Sensibar, J.A. Intracellular levels of SGP-2 (Clusterin) correlate with tumor grade in prostate cancer. Clin. Cancer Res., 1997, 3(10), 1707-1711.
[PMID: 9815554]
[60]
Burris, H.A., III Overcoming acquired resistance to anticancer therapy: focus on the PI3K/AKT/mTOR pathway. Cancer Chemother. Pharmacol., 2013, 71(4), 829-842.
[http://dx.doi.org/10.1007/s00280-012-2043-3] [PMID: 23377372]
[61]
Nitulescu, G.M.; Margina, D.; Juzenas, P.; Peng, Q.; Olaru, O.T.; Saloustros, E.; Fenga, C.; Spandidos, D.A.; Libra, M.; Tsatsakis, A.M. Akt inhibitors in cancer treatment: The long journey from drug discovery to clinical use (Review). Int. J. Oncol., 2016, 48(3), 869-885. [Review].
[http://dx.doi.org/10.3892/ijo.2015.3306] [PMID: 26698230]
[62]
Zhang, B.; Zhang, K.; Liu, Z.; Hao, F.; Wang, M.; Li, X.; Yin, Z.; Liang, H. Secreted clusterin gene silencing enhances chemosensitivity of a549 cells to cisplatin through AKT and ERK1/2 pathways in vitro. Cell. Physiol. Biochem., 2014, 33(4), 1162-1175.
[http://dx.doi.org/10.1159/000358685] [PMID: 24751980]
[63]
Jo, H.; Jia, Y.; Subramanian, K.K.; Hattori, H.; Luo, H.R. Cancer cell-derived clusterin modulates the phosphatidylinositol 3′-kinase-Akt pathway through attenuation of insulin-like growth factor 1 during serum deprivation. Mol. Cell. Biol., 2008, 28(13), 4285-4299.
[http://dx.doi.org/10.1128/MCB.01240-07] [PMID: 18458059]
[64]
Wang, C.; Jin, G.; Jin, H.; Wang, N.; Luo, Q.; Zhang, Y.; Gao, D.; Jiang, K.; Gu, D.; Shen, Q.; Huo, X.; Hu, F.; Ge, T.; Zhao, F.; Chu, W.; Shu, H.; Yao, M.; Cong, W.; Qin, W. Clusterin facilitates metastasis by EIF3I/Akt/MMP13 signaling in hepatocellular carcinoma. Oncotarget, 2015, 6(5), 2903-2916.
[http://dx.doi.org/10.18632/oncotarget.3093] [PMID: 25609201]
[65]
Wang, C.; Jiang, K.; Kang, X.; Gao, D.; Sun, C.; Li, Y.; Sun, L.; Zhang, S.; Liu, X.; Wu, W.; Yang, P.; Guo, K.; Liu, Y. Tumor-derived secretory clusterin induces epithelial-mesenchymal transition and facilitates hepatocellular carcinoma metastasis. Int. J. Biochem. Cell Biol., 2012, 44(12), 2308-2320.
[http://dx.doi.org/10.1016/j.biocel.2012.09.012] [PMID: 23010347]
[66]
Biroccio, A.; D’Angelo, C.; Jansen, B.; Gleave, M.E.; Zupi, G. Antisense clusterin oligodeoxynucleotides increase the response of HER-2 gene amplified breast cancer cells to Trastuzumab. J. Cell. Physiol., 2005, 204(2), 463-469.
[http://dx.doi.org/10.1002/jcp.20295] [PMID: 15685647]
[67]
July, L.V.; Beraldi, E.; So, A.; Fazli, L.; Evans, K.; English, J.C.; Gleave, M.E. Nucleotide-based therapies targeting clusterin chemosensitize human lung adenocarcinoma cells both in vitro and in vivo. Mol. Cancer Ther., 2004, 3(3), 223-232.
[PMID: 15026542]
[68]
Miyake, H.; Hara, I.; Hara, S.; Arakawa, S.; Kamidono, S. Synergistic chemosensitization and inhibition of tumor growth and metastasis by adenovirus-mediated P53 gene transfer in human bladder cancer model. Urology, 2000, 56(2), 332-336.
[http://dx.doi.org/10.1016/S0090-4295(00)00567-7] [PMID: 10925118]
[69]
Pucci, S.; Bonanno, E.; Pichiorri, F.; Angeloni, C.; Spagnoli, L.G. Modulation of different clusterin isoforms in human colon tumorigenesis. Oncogene, 2004, 23(13), 2298-2304.
[http://dx.doi.org/10.1038/sj.onc.1207404] [PMID: 14755245]
[70]
Bruix, J.; Sherman, M. Practice Guidelines Committee, American Association for the Study of Liver Diseases. Management of hepatocellular carcinoma. Hepatology, 2005, 42(5), 1208-1236.
[http://dx.doi.org/10.1002/hep.20933] [PMID: 16250051]
[71]
Zheng, W.; Yao, M.; Qian, Q.; Sai, W.; Qiu, L.; Yang, J.; Wu, W.; Dong, Z.; Yao, D. Oncogenic secretory clusterin in hepatocellular carcinoma: Expression at early staging and emerging molecular target. Oncotarget, 2016, 8(32), 52321-52332.
[PMID: 28881732]
[72]
Wang, C.; Jiang, K.; Gao, D.; Kang, X.; Sun, C.; Zhang, Q.; Li, Y.; Sun, L.; Zhang, S.; Guo, K.; Liu, Y. Clusterin protects hepatocellular carcinoma cells from endoplasmic reticulum stress induced apoptosis through GRP78. PLoS One, 2013, 8(2) e55981
[http://dx.doi.org/10.1371/journal.pone.0055981] [PMID: 23457489]
[73]
Lau, S.H.; Sham, J.S.; Xie, D.; Tzang, C.H.; Tang, D.; Ma, N.; Hu, L.; Wang, Y.; Wen, J.M.; Xiao, G.; Zhang, W.M.; Lau, G.K.; Yang, M.; Guan, X.Y. Clusterin plays an important role in hepatocellular carcinoma metastasis. Oncogene, 2006, 25(8), 1242-1250.
[http://dx.doi.org/10.1038/sj.onc.1209141] [PMID: 16247463]
[74]
Zhong, J.; Yu, X.; Dong, X.; Lu, H.; Zhou, W.; Li, L.; Li, Z.; Sun, P.; Shi, X. Therapeutic role of meloxicam targeting secretory clusterin-mediated invasion in hepatocellular carcinoma cells. Oncol. Lett., 2018, 15(5), 7191-7199.
[http://dx.doi.org/10.3892/ol.2018.8186] [PMID: 29731881]
[75]
Chen, D.; Wang, Y.; Zhang, K.; Jiao, X.; Yan, B.; Liang, J. Antisense oligonucleotide against clusterin regulates human hepatocellular carcinoma invasion through transcriptional regulation of matrix metalloproteinase-2 and E-cadherin. Int. J. Mol. Sci., 2012, 13(8), 10594-10607.
[http://dx.doi.org/10.3390/ijms130810594] [PMID: 22949882]
[76]
Wang, X.; Zou, F.; Zhong, J.; Yue, L.; Wang, F.; Wei, H.; Yang, G.; Jin, T.; Dong, X.; Li, J.; Xiu, P. Secretory Clusterin Mediates Oxaliplatin Resistance via the Gadd45a/PI3K/Akt Signaling Pathway in Hepatocellular Carcinoma. J. Cancer, 2018, 9(8), 1403-1413.
[http://dx.doi.org/10.7150/jca.23849] [PMID: 29721050]
[77]
Zhong, J.; Yu, X.; Dong, X.; Lu, H.; Zhou, W.; Li, L.; Li, Z.; Sun, P.; Shi, X. Downregulation of secreted clusterin potentiates the lethality of sorafenib in hepatocellular carcinoma in association with the inhibition of ERK1/2 signals. Int. J. Mol. Med., 2018, 41(5), 2893-2900.
[http://dx.doi.org/10.3892/ijmm.2018.3463] [PMID: 29436591]
[78]
Zheng, W.; Sai, W.; Yao, M.; Gu, H.; Yao, Y.; Qian, Q.; Yao, D. Silencing clusterin gene transcription on effects of multidrug resistance reversing of human hepatoma HepG2/ADM cells. Tumour Biol., 2015, 36(5), 3995-4003.
[http://dx.doi.org/10.1007/s13277-015-3043-9] [PMID: 25600802]
[79]
Xiu, P.; Xu, Z.; Liu, F.; Li, Z.; Li, T.; Zou, F.; Sun, X.; Li, J. Downregulating sCLU enhances the sensitivity of hepatocellular carcinoma cells to gemcitabine by activating the intrinsic apoptosis pathway. Dig. Dis. Sci., 2014, 59(8), 1798-1809.
[http://dx.doi.org/10.1007/s10620-014-3111-9] [PMID: 24671452]
[80]
Wang, Y.; Liu, Y.H.; Mai, S.J.; He, L.J.; Liao, Y.J.; Deng, H.X.; Guan, X.Y.; Zeng, Y.X.; Kung, H.F.; Xie, D. Evaluation of serum clusterin as a surveillance tool for human hepatocellular carcinoma with hepatitis B virus related cirrhosis. J. Gastroenterol. Hepatol., 2010, 25(6), 1123-1128.
[http://dx.doi.org/10.1111/j.1440-1746.2009.06205.x] [PMID: 20594228]
[81]
Nafee, A.M.; Pasha, H.F.; Abd El Aal, S.M.; Mostafa, N.A. Clinical significance of serum clusterin as a biomarker for evaluating diagnosis and metastasis potential of viral-related hepatocellular carcinoma. Clin. Biochem., 2012, 45(13-14), 1070-1074.
[http://dx.doi.org/10.1016/j.clinbiochem.2012.04.024] [PMID: 22580393]
[82]
Lai, J.P.; Chen, Z.M.; Lok, T.; Chan, O.T.; Himmelfarb, E.; Zhai, Q.; Lin, F.; Wang, H.L. Immunohistochemical stains of proliferating cell nuclear antigen, insulin-like growth factor 2 and clusterin help distinguish malignant from benign liver nodular lesions. J. Clin. Pathol., 2014, 67(6), 464-469.
[http://dx.doi.org/10.1136/jclinpath-2013-201907] [PMID: 24407433]
[83]
Kimura, A.; Sogawa, K.; Satoh, M.; Kodera, Y.; Yokosuka, O.; Tomonaga, T.; Nomura, F. The application of a three-step serum proteome analysis for the discovery and identification of novel biomarkers of hepatocellular carcinoma. Int. J. Proteomics, 2012, 2012, 623190
[http://dx.doi.org/10.1155/2012/623190] [PMID: 22957256]
[84]
Kuo, P.C.; Chau, I.Y.; Li, A.F.; Chauc, Y.P.; Hsia, C.Y.; Chau, G.Y. Clusterin expression in non-tumor tissue in patients with resectable hepatocellular carcinoma related with post-resectional survival. J. Chin. Med. Assoc., 2019.
[http://dx.doi.org/10.1097/JCMA.0000000000000195] [PMID: 31567651]
[85]
Chun, Y.J. Knockdown of clusterin expression increases the in vitro sensitivity of human prostate cancer cells to paclitaxel. J. Toxicol. Environ. Health A, 2014, 77(22-24), 1443-1450.
[http://dx.doi.org/10.1080/15287394.2014.951760] [PMID: 25343293]
[86]
So, A.; Sinnemann, S.; Huntsman, D.; Fazli, L.; Gleave, M. Knockdown of the cytoprotective chaperone, clusterin, chemosensitizes human breast cancer cells both in vitro and in vivo. Mol. Cancer Ther., 2005, 4(12), 1837-1849.
[http://dx.doi.org/10.1158/1535-7163.MCT-05-0178] [PMID: 16373699]
[87]
Cheng, C.Y.; Cherng, S.H.; Wu, W.J.; Yang, T.Y.; Huang, X.Y.; Liao, F.T.; Wu, M.F.; Sheu, G.T. Regulation of chemosensitivity and migration by clusterin in non-small cell lung cancer cells. Cancer Chemother. Pharmacol., 2012, 69(1), 145-154.
[http://dx.doi.org/10.1007/s00280-011-1682-0] [PMID: 21630085]
[88]
Hassan, M.K.; Watari, H.; Han, Y.; Mitamura, T.; Hosaka, M.; Wang, L.; Tanaka, S.; Sakuragi, N. Clusterin is a potential molecular predictor for ovarian cancer patient’s survival: targeting clusterin improves response to paclitaxel. J. Exp. Clin. Cancer Res., 2011, 30, 113.
[http://dx.doi.org/10.1186/1756-9966-30-113] [PMID: 22185350]
[89]
Koltai, T. Clusterin: a key player in cancer chemoresistance and its inhibition. OncoTargets Ther., 2014, 7, 447-456.
[http://dx.doi.org/10.2147/OTT.S58622] [PMID: 24672247]
[90]
Djeu, J.Y.; Wei, S. Clusterin and chemoresistance. Adv. Cancer Res., 2009, 105, 77-92.
[http://dx.doi.org/10.1016/S0065-230X(09)05005-2] [PMID: 19879424]
[91]
Zellweger, T.; Chi, K.; Miyake, H.; Adomat, H.; Kiyama, S.; Skov, K.; Gleave, M.E. Enhanced radiation sensitivity in prostate cancer by inhibition of the cell survival protein clusterin. Clin. Cancer Res., 2002, 8(10), 3276-3284.
[PMID: 12374699]
[92]
Gleave, M.; Chi, K.N. Knock-down of the cytoprotective gene, clusterin, to enhance hormone and chemosensitivity in prostate and other cancers. Ann. N. Y. Acad. Sci., 2005, 1058, 1-15.
[http://dx.doi.org/10.1196/annals.1359.001] [PMID: 16394121]
[93]
Xiu, P.; Dong, X.; Dong, X.; Xu, Z.; Zhu, H.; Liu, F.; Wei, Z.; Zhai, B.; Kanwar, J.R.; Jiang, H.; Li, J.; Sun, X. Secretory clusterin contributes to oxaliplatin resistance by activating Akt pathway in hepatocellular carcinoma. Cancer Sci., 2013, 104(3), 375-382.
[http://dx.doi.org/10.1111/cas.12088] [PMID: 23279642]
[94]
Zoubeidi, A.; Ettinger, S.; Beraldi, E.; Hadaschik, B.; Zardan, A.; Klomp, L.W.; Nelson, C.C.; Rennie, P.S.; Gleave, M.E. Clusterin facilitates COMMD1 and I-kappaB degradation to enhance NF-kappaB activity in prostate cancer cells. Mol. Cancer Res., 2010, 8(1), 119-130.
[http://dx.doi.org/10.1158/1541-7786.MCR-09-0277] [PMID: 20068069]
[95]
Shim, Y.J.; Kang, B.H.; Choi, B.K.; Park, I.S.; Min, B.H. Clusterin induces the secretion of TNF-α and the chemotactic migration of macrophages. Biochem. Biophys. Res. Commun., 2012, 422(1), 200-205.
[http://dx.doi.org/10.1016/j.bbrc.2012.04.162] [PMID: 22575505]
[96]
Sun, J.; Yeung, C.A.; Co, N.N.; Tsang, T.Y.; Yau, E.; Luo, K.; Wu, P.; Wa, J.C.; Fung, K.P.; Kwok, T.T.; Liu, F. Clitocine reversal of P-glycoprotein associated multi-drug resistance through down-regulation of transcription factor NF-κB in R-HepG2 cell line. PLoS One, 2012, 7(8) e40720
[http://dx.doi.org/10.1371/journal.pone.0040720] [PMID: 22927901]
[97]
Zinzi, L.; Capparelli, E.; Cantore, M.; Contino, M.; Leopoldo, M.; Colabufo, N.A. Small and Innovative Molecules as New Strategy to Revert MDR. Front. Oncol., 2014, 4, 2.
[http://dx.doi.org/10.3389/fonc.2014.00002] [PMID: 24478983]
[98]
Hoffmann, K.; Shibo, L.; Xiao, Z.; Longerich, T.; Büchler, M.W.; Schemmer, P. Correlation of gene expression of ATP-binding cassette protein and tyrosine kinase signaling pathway in patients with hepatocellular carcinoma. Anticancer Res., 2011, 31(11), 3883-3890.
[PMID: 22110214]
[99]
Beck, B.; Blanpain, C. Unravelling cancer stem cell potential. Nat. Rev. Cancer, 2013, 13(10), 727-738.
[http://dx.doi.org/10.1038/nrc3597] [PMID: 24060864]
[100]
Aguirre-Ghiso, J.A. Models, mechanisms and clinical evidence for cancer dormancy. Nat. Rev. Cancer, 2007, 7(11), 834-846.
[http://dx.doi.org/10.1038/nrc2256] [PMID: 17957189]
[101]
Brungs, D.; Aghmesheh, M.; Vine, K.L.; Becker, T.M.; Carolan, M.G.; Ranson, M. Gastric cancer stem cells: evidence, potential markers, and clinical implications. J. Gastroenterol., 2016, 51(4), 313-326.
[http://dx.doi.org/10.1007/s00535-015-1125-5] [PMID: 26428661]
[102]
Song, K.; Kwon, H.; Han, C.; Zhang, J.; Dash, S.; Lim, K.; Wu, T. Active glycolytic metabolism in CD133(+) hepatocellular cancer stem cells: regulation by MIR-122. Oncotarget, 2015, 6(38), 40822-40835.
[http://dx.doi.org/10.18632/oncotarget.5812] [PMID: 26506419]
[103]
Guan, D.X.; Shi, J.; Zhang, Y.; Zhao, J.S.; Long, L.Y.; Chen, T.W.; Zhang, E.B.; Feng, Y.Y.; Bao, W.D.; Deng, Y.Z.; Qiu, L.; Zhang, X.L.; Koeffler, H.P.; Cheng, S.Q.; Li, J.J.; Xie, D. Sorafenib enriches epithelial cell adhesion molecule-positive tumor initiating cells and exacerbates a subtype of hepatocellular carcinoma through TSC2-AKT cascade. Hepatology, 2015, 62(6), 1791-1803.
[http://dx.doi.org/10.1002/hep.28117] [PMID: 26257239]
[104]
Shan, J.; Shen, J.; Liu, L.; Xia, F.; Xu, C.; Duan, G.; Xu, Y.; Ma, Q.; Yang, Z.; Zhang, Q.; Ma, L.; Liu, J.; Xu, S.; Yan, X.; Bie, P.; Cui, Y.; Bian, X.W.; Qian, C. Nanog regulates self-renewal of cancer stem cells through the insulin-like growth factor pathway in human hepatocellular carcinoma. Hepatology, 2012, 56(3), 1004-1014.
[http://dx.doi.org/10.1002/hep.25745] [PMID: 22473773]
[105]
Zhou, W.; Guan, Q.; Kwan, C.C.; Chen, H.; Gleave, M.E.; Nguan, C.Y.; Du, C. Loss of clusterin expression worsens renal ischemia-reperfusion injury. Am. J. Physiol. Renal Physiol., 2010, 298(3), F568-F578.
[http://dx.doi.org/10.1152/ajprenal.00399.2009] [PMID: 20007348]
[106]
Dairi, G.; Guan, Q.; Roshan-Moniri, M.; Collins, C.C.; Ong, C.J.; Gleave, M.E.; Nguan, C.Y.; Du, C. Transcriptome-Based Analysis of Molecular Pathways for Clusterin Functions in Kidney Cells. J. Cell. Physiol., 2016, 231(12), 2628-2638.
[http://dx.doi.org/10.1002/jcp.25415] [PMID: 27155085]
[107]
Zhang, H.; Kim, J.K.; Edwards, C.A.; Xu, Z.; Taichman, R.; Wang, C.Y. Clusterin inhibits apoptosis by interacting with activated Bax. Nat. Cell Biol., 2005, 7(9), 909-915.
[http://dx.doi.org/10.1038/ncb1291] [PMID: 16113678]
[108]
Al Nakouzi, N.; Wang, C.K.; Beraldi, E.; Jager, W.; Ettinger, S.; Fazli, L.; Nappi, L.; Bishop, J.; Zhang, F.; Chauchereau, A.; Loriot, Y.; Gleave, M. Clusterin knockdown sensitizes prostate cancer cells to taxane by modulating mitosis. EMBO Mol. Med., 2016, 8(7), 761-778.
[http://dx.doi.org/10.15252/emmm.201506059] [PMID: 27198502]
[109]
Xiong, J.; Wang, S.; Chen, T.; Shu, X.; Mo, X.; Chang, G.; Chen, J.J.; Li, C.; Luo, H.; Lee, J.D. Verteporfin blocks Clusterin which is required for survival of gastric cancer stem cell by modulating HSP90 function. Int. J. Biol. Sci., 2019, 15(2), 312-324.
[http://dx.doi.org/10.7150/ijbs.29135] [PMID: 30745823]
[110]
Luo, B.; Lee, A.S. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene, 2013, 32(7), 805-818.
[http://dx.doi.org/10.1038/onc.2012.130] [PMID: 22508478]
[111]
Chen, D.; Bhat-Nakshatri, P.; Goswami, C.; Badve, S.; Nakshatri, H. ANTXR1, a stem cell-enriched functional biomarker, connects collagen signaling to cancer stem-like cells and metastasis in breast cancer. Cancer Res., 2013, 73(18), 5821-5833.
[http://dx.doi.org/10.1158/0008-5472.CAN-13-1080] [PMID: 23832666]
[112]
Majidzadeh-A, K.; Gharechahi, J. Plasma proteomics analysis of tamoxifen resistance in breast cancer. Med. Oncol., 2013, 30(4), 753.
[http://dx.doi.org/10.1007/s12032-013-0753-y] [PMID: 24158757]
[113]
Xu, F.; Yang, T.; Fang, D.; Xu, Q.; Chen, Y. An investigation of heat shock protein 27 and P-glycoprotein mediated multi-drug resistance in breast cancer using liquid chromatography-tandem mass spectrometry-based targeted proteomics. J. Proteomics, 2014, 108, 188-197.
[http://dx.doi.org/10.1016/j.jprot.2014.05.016] [PMID: 24882106]
[114]
Sipos, F.; Galamb, O. Epithelial-to-mesenchymal and mesenchymal-to-epithelial transitions in the colon. World J. Gastroenterol., 2012, 18(7), 601-608.
[http://dx.doi.org/10.3748/wjg.v18.i7.601] [PMID: 22363130]
[115]
Tiwari, N.; Gheldof, A.; Tatari, M.; Christofori, G. EMT as the ultimate survival mechanism of cancer cells. Semin. Cancer Biol., 2012, 22(3), 194-207.
[http://dx.doi.org/10.1016/j.semcancer.2012.02.013] [PMID: 22406545]
[116]
Das, V.; Bhattacharya, S.; Chikkaputtaiah, C.; Hazra, S.; Pal, M. The basics of epithelial-mesenchymal transition (EMT): A study from a structure, dynamics, and functional perspective. J. Cell. Physiol., 2019.
[http://dx.doi.org/10.1002/jcp.28160] [PMID: 30723913]
[117]
Thiery, J.P.; Acloque, H.; Huang, R.Y.; Nieto, M.A. Epithelial-mesenchymal transitions in development and disease. Cell, 2009, 139(5), 871-890.
[http://dx.doi.org/10.1016/j.cell.2009.11.007] [PMID: 19945376]
[118]
Uchibori, K.; Kasamatsu, A.; Sunaga, M.; Yokota, S.; Sakurada, T.; Kobayashi, E.; Yoshikawa, M.; Uzawa, K.; Ueda, S.; Tanzawa, H.; Sato, N. Establishment and characterization of two 5-fluorouracil-resistant hepatocellular carcinoma cell lines. Int. J. Oncol., 2012, 40(4), 1005-1010.
[http://dx.doi.org/10.3892/ijo.2011.1300] [PMID: 22179686]
[119]
Singh, A.; Settleman, J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene, 2010, 29(34), 4741-4751.
[http://dx.doi.org/10.1038/onc.2010.215] [PMID: 20531305]
[120]
Chin, V.L.; Lim, C.L. Epithelial-mesenchymal plasticity-engaging stemness in an interplay of phenotypes. Stem Cell Investig., 2019, 6, 25.
[http://dx.doi.org/10.21037/sci.2019.08.08] [PMID: 31559312]
[121]
Medema, J.P. Cancer stem cells: the challenges ahead. Nat. Cell Biol., 2013, 15(4), 338-344.
[http://dx.doi.org/10.1038/ncb2717] [PMID: 23548926]
[122]
Ren, W.W.; Li, D.D.; Chen, X.; Li, X.L.; He, Y.P.; Guo, L.H.; Liu, L.N.; Sun, L.P.; Zhang, X.P. MicroRNA-125b reverses oxaliplatin resistance in hepatocellular carcinoma by negatively regulating EVA1A mediated autophagy. Cell Death Dis., 2018, 9(5), 547.
[http://dx.doi.org/10.1038/s41419-018-0592-z] [PMID: 29749374]
[123]
Mani, S.A.; Guo, W.; Liao, M.J.; Eaton, E.N.; Ayyanan, A.; Zhou, A.Y.; Brooks, M.; Reinhard, F.; Zhang, C.C.; Shipitsin, M.; Campbell, L.L.; Polyak, K.; Brisken, C.; Yang, J.; Weinberg, R.A. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell, 2008, 133(4), 704-715.
[http://dx.doi.org/10.1016/j.cell.2008.03.027] [PMID: 18485877]
[124]
Yang, Y.; Yao, J.H.; Du, Q.Y.; Zhou, Y.C.; Yao, T.J.; Wu, Q.; Liu, J.; Ou, Y.R. Connexin 32 downregulation is critical for chemoresistance in oxaliplatin-resistant HCC cells associated with EMT. Cancer Manag. Res., 2019, 11, 5133-5146.
[http://dx.doi.org/10.2147/CMAR.S203656] [PMID: 31213923]
[125]
Xu, T.; Zhang, J.; Chen, W.; Pan, S.; Zhi, X.; Wen, L.; Zhou, Y.; Chen, B.W.; Qiu, J.; Zhang, Y.; Yang, Q.; Feng, X.; Bai, X.; Liang, T. ARK5 promotes doxorubicin resistance in hepatocellular carcinoma via epithelial-mesenchymal transition. Cancer Lett., 2016, 377(2), 140-148.
[http://dx.doi.org/10.1016/j.canlet.2016.04.026] [PMID: 27126361]
[126]
Ma, Z.; Guo, D.; Wang, Q.; Liu, P.; Xiao, Y.; Wu, P.; Wang, Y.; Chen, B.; Liu, Z.; Liu, Q. Lgr5-mediated p53 Repression through PDCD5 leads to doxorubicin resistance in Hepatocellular Carcinoma. Theranostics, 2019, 9(10), 2967-2983.
[http://dx.doi.org/10.7150/thno.30562] [PMID: 31244936]
[127]
Sreekumar, R.; Emaduddin, M.; Al-Saihati, H.; Moutasim, K.; Chan, J.; Spampinato, M.; Bhome, R.; Yuen, H.M.; Mescoli, C.; Vitale, A.; Cillo, U.; Rugge, M.; Primrose, J.; Hilal, M.A.; Thirdborough, S.; Tulchinsky, E.; Thomas, G.; Mirnezami, A.; Sayan, A.E. Protein kinase C inhibitors override ZEB1-induced chemoresistance in HCC. Cell Death Dis., 2019, 10(10), 703.
[http://dx.doi.org/10.1038/s41419-019-1885-6] [PMID: 31543517]
[128]
Tian, Y.; Wang, C.; Chen, S.; Liu, J.; Fu, Y.; Luo, Y. Extracellular Hsp90α and clusterin synergistically promote breast cancer epithelial-to-mesenchymal transition and metastasis via LRP1. J. Cell Sci., 2019, 132(15) jcs228213
[http://dx.doi.org/10.1242/jcs.228213] [PMID: 31273033]
[129]
Shiota, M.; Zardan, A.; Takeuchi, A.; Kumano, M.; Beraldi, E.; Naito, S.; Zoubeidi, A.; Gleave, M.E. Clusterin mediates TGF-β-induced epithelial-mesenchymal transition and metastasis via Twist1 in prostate cancer cells. Cancer Res., 2012, 72(20), 5261-5272.
[http://dx.doi.org/10.1158/0008-5472.CAN-12-0254] [PMID: 22896337]
[130]
Chou, T.Y.; Chen, W.C.; Lee, A.C.; Hung, S.M.; Shih, N.Y.; Chen, M.Y. Clusterin silencing in human lung adenocarcinoma cells induces a mesenchymal-to-epithelial transition through modulating the ERK/Slug pathway. Cell. Signal., 2009, 21(5), 704-711.
[http://dx.doi.org/10.1016/j.cellsig.2009.01.008] [PMID: 19166932]
[131]
Ho, C.J.; Gorski, S.M. Molecular Mechanisms Underlying Autophagy-Mediated Treatment Resistance in Cancer. Cancers (Basel), 2019, 11(11) E1775
[http://dx.doi.org/10.3390/cancers11111775] [PMID: 31717997]
[132]
Wu, M.; Zhang, P. EGFR-mediated autophagy in tumourigenesis and therapeutic resistance. Cancer Lett., 2019.
[PMID: 31639425]
[133]
Zhang, F.; Kumano, M.; Beraldi, E.; Fazli, L.; Du, C.; Moore, S.; Sorensen, P.; Zoubeidi, A.; Gleave, M.E. Clusterin facilitates stress-induced lipidation of LC3 and autophagosome biogenesis to enhance cancer cell survival. Nat. Commun., 2014, 5, 5775.
[http://dx.doi.org/10.1038/ncomms6775] [PMID: 25503391]
[134]
Lee, J.; Hong, S.W.; Kwon, H.; Park, S.E.; Rhee, E.J.; Park, C.Y.; Oh, K.W.; Park, S.W.; Lee, W.Y. Resveratrol, an activator of SIRT1, improves ER stress by increasing clusterin expression in HepG2 cells. Cell Stress Chaperones, 2019, 24(4), 825-833.
[http://dx.doi.org/10.1007/s12192-019-01012-z] [PMID: 31183612]
[135]
Peck-Radosavljevic, M. Drug therapy for advanced-stage liver cancer. Liver Cancer, 2014, 3(2), 125-131.
[http://dx.doi.org/10.1159/000343868] [PMID: 24945003]
[136]
Fornari, F.; Pollutri, D.; Patrizi, C.; La Bella, T.; Marinelli, S.; Casadei Gardini, A.; Marisi, G.; Baron Toaldo, M.; Baglioni, M.; Salvatore, V.; Callegari, E.; Baldassarre, M.; Galassi, M.; Giovannini, C.; Cescon, M.; Ravaioli, M.; Negrini, M.; Bolondi, L.; Gramantieri, L. In Hepatocellular Carcinoma miR-221 Modulates Sorafenib Resistance through Inhibition of Caspase-3-Mediated Apoptosis. Clin. Cancer Res., 2017, 23(14), 3953-3965.
[http://dx.doi.org/10.1158/1078-0432.CCR-16-1464] [PMID: 28096271]
[137]
Godin, C.; Bodeau, S.; Saidak, Z.; Louandre, C.; François, C.; Barbare, J.C.; Coriat, R.; Galmiche, A.; Sauzay, C. Early decrease in serum amphiregulin or vascular endothelial growth factor levels predicts sorafenib efficacy in hepatocellular carcinoma. Oncol. Rep., 2019, 41(3), 2041-2050.
[PMID: 30569112]
[138]
Gomes, A.S.; Monteleone, P.A.; Sayre, J.W.; Finn, R.S.; Sadeghi, S.; Tong, M.J.; Britten, C.D.; Busuttil, R.W. Comparison of Triple-Drug Transcatheter Arterial Chemoembolization (TACE) With Single-Drug TACE Using Doxorubicin-Eluting Beads: Long-Term Survival in 313 Patients. AJR Am. J. Roentgenol., 2017, 209(4), 722-732.
[http://dx.doi.org/10.2214/AJR.17.18219] [PMID: 28705059]
[139]
Gomes, A.S.; Rosove, M.H.; Rosen, P.J.; Amado, R.G.; Sayre, J.W.; Monteleone, P.A.; Busuttil, R.W. Triple-drug transcatheter arterial chemoembolization in unresectable hepatocellular carcinoma: assessment of survival in 124 consecutive patients. AJR Am. J. Roentgenol., 2009, 193(6), 1665-1671.
[http://dx.doi.org/10.2214/AJR.08.1806] [PMID: 19933662]
[140]
Ali, H.E.A.; Emam, A.A.; Zeeneldin, A.A.; Srour, R.; Tabashy, R.; El-Desouky, E.D.; Abd Elmageed, Z.Y.; Abdel-Wahab, A.A. Circulating miR-26a, miR-106b, miR-107 and miR-133b stratify hepatocellular carcinoma patients according to their response to transarterial chemoembolization. Clin. Biochem., 2019, 65, 45-52.
[http://dx.doi.org/10.1016/j.clinbiochem.2019.01.002] [PMID: 30653948]
[141]
Gleave, M.; Jansen, B. Clusterin and IGFBPs as antisense targets in prostate cancer. Ann. N. Y. Acad. Sci., 2003, 1002, 95-104.
[http://dx.doi.org/10.1196/annals.1281.020] [PMID: 14751827]
[142]
Zielinski, R.; Chi, K.N. Custirsen (OGX-011): a second-generation antisense inhibitor of clusterin in development for the treatment of prostate cancer. Future Oncol., 2012, 8(10), 1239-1251.
[http://dx.doi.org/10.2217/fon.12.129] [PMID: 23130925]
[143]
Laskin, J.J.; Nicholas, G.; Lee, C.; Gitlitz, B.; Vincent, M.; Cormier, Y.; Stephenson, J.; Ung, Y.; Sanborn, R.; Pressnail, B.; Nugent, F.; Nemunaitis, J.; Gleave, M.E.; Murray, N.; Hao, D. Phase I/II trial of custirsen (OGX-011), an inhibitor of clusterin, in combination with a gemcitabine and platinum regimen in patients with previously untreated advanced non-small cell lung cancer. J. Thorac. Oncol., 2012, 7(3), 579-586.
[http://dx.doi.org/10.1097/JTO.0b013e31823f459c] [PMID: 22198426]
[144]
Wang, X.; Xie, J.; Lu, X.; Li, H.; Wen, C.; Huo, Z.; Xie, J.; Shi, M.; Tang, X.; Chen, H.; Peng, C.; Fang, Y.; Deng, X.; Shen, B. Melittin inhibits tumor growth and decreases resistance to gemcitabine by downregulating cholesterol pathway gene CLU in pancreatic ductal adenocarcinoma. Cancer Lett., 2017, 399, 1-9.
[http://dx.doi.org/10.1016/j.canlet.2017.04.012] [PMID: 28428074]
[145]
Mustafi, S.; Sant, D.W.; Liu, Z.J.; Wang, G. Ascorbate induces apoptosis in melanoma cells by suppressing Clusterin expression. Sci. Rep., 2017, 7(1), 3671.
[http://dx.doi.org/10.1038/s41598-017-03893-5] [PMID: 28623268]

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