Inhibition of 19S proteasome-associated deubiquitinases by metal-containing compounds

Oncoscience

Volumn 2, Issue 5, 2015, Pages 457-466

  Liu, Ningning ^a   Huang, Hongbiao ^a   Dou, Q Ping ^a,b,c   Liu, Jinbao ^a  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b WAYNE STATE UNIVERSITY   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

19S associated deubiquitinases; Copper complexes; Gold complexes

Indexed keywords

EID: 84958529561     PISSN: None     EISSN: 23314737     Source Type: Journal    
DOI: 10.18632/oncoscience.167     Document Type: Article

References (99)

1. Voges D, Zwickl P and Baumeister W. The 26S proteasome: a molecular machine designed for controlled proteolysis. Annual review of biochemistry. 1999; 68:1015-1068.
2. Glickman MH and Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiological reviews. 2002; 82(2):373-428.
3. Kish-Trier E and Hill CP. Structural biology of the proteasome. Annual review of biophysics. 2013; 42:29-49.
4. Yang H, Zhou P, Huang H, Chen D, Ma N, Cui QC, Shen S, Dong W, Zhang X, Lian W, Wang X, Dou QP and Liu J. Shikonin exerts antitumor activity via proteasome inhibition and cell death induction in vitro and in vivo. International journal of cancer Journal international du cancer. 2009; 124(10):2450-2459.
5. Huang H, Liu N, Zhao K, Zhu C, Lu X, Li S, Lian W, Zhou P, Dong X, Zhao C, Guo H, Zhang C, Yang C, Wen G, Lu L, Li X, et al. Sanggenon C decreases tumor cell viability associated with proteasome inhibition. Frontiers in bioscience (Elite edition). 2011; 3:1315-1325.
6. Li X, Liu S, Huang H, Liu N, Zhao C, Liao S, Yang C, Liu Y, Zhao C, Li S, Lu X, Liu C, Guan L, Zhao K, Shi X, Song W, et al. Gambogic acid is a tissue-specific proteasome inhibitor in vitro and in vivo. Cell reports. 2013; 3(1):211-222.
7. Shi X, Chen X, Li X, Lan X, Zhao C, Liu S, Huang H, Liu N, Liao S, Song W, Zhou P, Wang S, Xu L, Wang X, Dou QP and Liu J. Gambogic acid induces apoptosis in imatinib-resistant chronic myeloid leukemia cells via inducing proteasome inhibition and caspase-dependent Bcr-Abl downregulation. Clinical cancer research: an official journal of the American Association for Cancer Research. 2014; 20(1):151-163.
8. Daniel KG, Gupta P, Harbach RH, Guida WC and Dou QP. Organic copper complexes as a new class of proteasome inhibitors and apoptosis inducers in human cancer cells. Biochemical pharmacology. 2004; 67(6):1139-1151.
9. Chen D, Cui QC, Yang H and Dou QP. Disulfiram, a clinically used anti-alcoholism drug and copper-binding agent, induces apoptotic cell death in breast cancer cultures and xenografts via inhibition of the proteasome activity. Cancer research. 2006; 66(21):10425-10433.
10. Chen D, Cui QC, Yang H, Barrea RA, Sarkar FH, Sheng S, Yan B, Reddy GP and Dou QP. Clioquinol, a therapeutic agent for Alzheimer's disease, has proteasome-inhibitory, androgen receptor-suppressing, apoptosis-inducing, and antitumor activities in human prostate cancer cells and xenografts. Cancer research. 2007; 67(4):1636-1644.
11. Chen D, Frezza M, Shakya R, Cui QC, Milacic V, Verani CN and Dou QP. Inhibition of the proteasome activity by gallium(III) complexes contributes to their anti prostate tumor effects. Cancer research. 2007; 67(19):9258-9265.
12. Zhang Z, Bi C, Schmitt SM, Fan Y, Dong L, Zuo J and Dou QP. 1,10-Phenanthroline promotes copper complexes into tumor cells and induces apoptosis by inhibiting the proteasome activity. Journal of biological inorganic chemistry: JBIC: a publication of the Society of Biological Inorganic Chemistry. 2012; 17(8):1257-1267.
13. Milacic V, Chen D, Ronconi L, Landis-Piwowar KR, Fregona D and Dou QP. A novel anticancer gold(III) dithiocarbamate compound inhibits the activity of a purified 20S proteasome and 26S proteasome in human breast cancer cell cultures and xenografts. Cancer research. 2006; 66(21):10478-10486.
14. Milacic V and Dou QP. The tumor proteasome as a novel target for gold(III) complexes: implications for breast cancer therapy. Coordination chemistry reviews. 2009; 253(11-12):1649-1660.
15. Nardon C, Schmitt SM, Yang H, Zuo J, Fregona D and Dou QP. Gold(III)-dithiocarbamato peptidomimetics in the forefront of the targeted anticancer therapy: preclinical studies against human breast neoplasia. PloS one. 2014; 9(1):e84248.
16. Buac D, Schmitt S, Ventro G, Kona FR and Dou QP. Dithiocarbamate-based coordination compounds as potent proteasome inhibitors in human cancer cells. Mini reviews in medicinal chemistry. 2012; 12(12):1193-1201.
17. Pereira L, Igea A, Canovas B, Dolado I and Nebreda AR. Inhibition of p38 MAPK sensitizes tumour cells to cisplatin-induced apoptosis mediated by reactive oxygen species and JNK. EMBO molecular medicine. 2013; 5(11):1759-1774.
18. Kasparkova J, Thibault T, Kostrhunova H, Stepankova J, Vojtiskova M, Muchova T, Midoux P, Malinge JM and Brabec V. Different affinity of nuclear factor-kappa B proteins to DNA modified by antitumor cisplatin and its clinically ineffective trans isomer. The FEBS journal. 2014; 281(5):1393-1408.
19. Wang T and Guo Z. Copper in medicine: homeostasis, chelation therapy and antitumor drug design. Current medicinal chemistry. 2006; 13(5):525-537.
20. Arnesano F, Scintilla S, Calo V, Bonfrate E, Ingrosso C, Losacco M, Pellegrino T, Rizzarelli E and Natile G. Copper-triggered aggregation of ubiquitin. PloS one. 2009; 4(9):e7052.
21. Festa RA and Thiele DJ. Copper: an essential metal in biology. Current biology: CB. 2011; 21(21):R877-883.
22. Gandin V, Pellei M, Tisato F, Porchia M, Santini C and Marzano C. A novel copper complex induces paraptosis in colon cancer cells via the activation of ER stress signalling. Journal of cellular and molecular medicine. 2012; 16(1):142-151.
23. Bortolozzi R, Viola G, Porcu E, Consolaro F, Marzano C, Pellei M, Gandin V and Basso G. A novel copper(I) complex induces ER-stress-mediated apoptosis and sensitizes B-acute lymphoblastic leukemia cells to chemotherapeutic agents. Oncotarget. 2014; 5(15):5978-5991.
24. Karr JW and Szalai VA. Cu(II) binding to monomeric, oligomeric, and fibrillar forms of the Alzheimer's disease amyloid-beta peptide. Biochemistry. 2008; 47(17):5006-5016.
25. Tardito S, Bussolati O, Gaccioli F, Gatti R, Guizzardi S, Uggeri J, Marchio L, Lanfranchi M and Franchi-Gazzola R. Non-apoptotic programmed cell death induced by a copper(II) complex in human fibrosarcoma cells. Histochemistry and cell biology. 2006; 126(4):473-482.
26. Tardito S, Isella C, Medico E, Marchio L, Bevilacqua E, Hatzoglou M, Bussolati O and Franchi-Gazzola R. The thioxotriazole copper(II) complex A0 induces endoplasmic reticulum stress and paraptotic death in human cancer cells. The Journal of biological chemistry. 2009; 284(36):24306-24319.
27. Benedek TG. The history of gold therapy for tuberculosis. Journal of the history of medicine and allied sciences. 2004; 59(1):50-89.
28. Ronconi L, Giovagnini L, Marzano C, Bettio F, Graziani R, Pilloni G and Fregona D. Gold dithiocarbamate derivatives as potential antineoplastic agents: design, spectroscopic properties, and in vitro antitumor activity. Inorganic chemistry. 2005; 44(6):1867-1881.
29. Milacic V, Fregona D and Dou QP. Gold complexes as prospective metal-based anticancer drugs. Histology and histopathology. 2008; 23(1):101-108.
30. Norn S, Permin H, Kruse PR and Kruse E. [History of gold--with danish contribution to tuberculosis and rheumatoid arthritis]. Dansk medicinhistorisk arbog. 2011; 39:59-80.
31. Berners-Price SJ and Filipovska A. Gold compounds as therapeutic agents for human diseases. Metallomics: integrated biometal science. 2011; 3(9):863-873.
32. Han S, Kim K, Song Y, Kim H, Kwon J, Lee YH, Lee CK, Lee SJ, Ha N and Kim K. Auranofin, an immunosuppressive drug, inhibits MHC class I and MHC class II pathways of antigen presentation in dendritic cells. Archives of pharmacal research. 2008; 31(3):370-376.
33. Sannella AR, Casini A, Gabbiani C, Messori L, Bilia AR, Vincieri FF, Majori G and Severini C. New uses for old drugs. Auranofin, a clinically established antiarthritic metallodrug, exhibits potent antimalarial effects in vitro: Mechanistic and pharmacological implications. FEBS letters. 2008; 582(6):844-847.
34. Dai B, Yoo SY, Bartholomeusz G, Graham RA, Majidi M, Yan S, Meng J, Ji L, Coombes K, Minna JD, Fang B and Roth JA. KEAP1-dependent synthetic lethality induced by AKT and TXNRD1 inhibitors in lung cancer. Cancer research. 2013; 73(17):5532-5543.
35. Fiskus W, Saba N, Shen M, Ghias M, Liu J, Gupta SD, Chauhan L, Rao R, Gunewardena S, Schorno K, Austin CP, Maddocks K, Byrd J, Melnick A, Huang P, Wiestner A, et al. Auranofin induces lethal oxidative and endoplasmic reticulum stress and exerts potent preclinical activity against chronic lymphocytic leukemia. Cancer research. 2014; 74(9):2520-2532.
36. Park SH, Lee JH, Berek JS and Hu MC. Auranofin displays anticancer activity against ovarian cancer cells through FOXO3 activation independent of p53. International journal of oncology. 2014; 45(4):1691-1698.
37. Messori L, Marcon G and Orioli P. Gold(III) compounds as new family of anticancer drugs. Bioinorganic chemistry and applications. 2003:177-187.
38. Ronconi L, Marzano C, Zanello P, Corsini M, Miolo G, Macca C, Trevisan A and Fregona D. Gold(III) dithiocarbamate derivatives for the treatment of cancer: solution chemistry, DNA binding, and hemolytic properties. Journal of medicinal chemistry. 2006; 49(5):1648-1657.
39. Casini A, Hartinger C, Gabbiani C, Mini E, Dyson PJ, Keppler BK and Messori L. Gold(III) compounds as anticancer agents: relevance of gold-protein interactions for their mechanism of action. Journal of inorganic biochemistry. 2008; 102(3):564-575.
40. Aldinucci D, Lorenzon D, Stefani L, Giovagnini L, Colombatti A and Fregona D. Antiproliferative and apoptotic effects of two new gold(III) methylsarcosinedithiocarbamate derivatives on human acute myeloid leukemia cells in vitro. Anti-cancer drugs. 2007; 18(3):323-332.
41. Vela L, Contel M, Palomera L, Azaceta G and Marzo I. Iminophosphorane-organogold(III) complexes induce cell death through mitochondrial ROS production. Journal of inorganic biochemistry. 2011; 105(10):1306-1313.
42. Reyes-Turcu FE, Ventii KH and Wilkinson KD. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annual review of biochemistry. 2009; 78:363-397.
43. Komander D, Clague MJ and Urbe S. Breaking the chains: structure and function of the deubiquitinases. Nature reviews Molecular cell biology. 2009; 10(8):550-563.
44. Liang J, Saad Y, Lei T, Wang J, Qi D, Yang Q, Kolattukudy PE and Fu M. MCP-induced protein 1 deubiquitinates TRAF proteins and negatively regulates JNK and NF-kappaB signaling. The Journal of experimental medicine. 2010; 207(13):2959-2973.
45. Ardley HC, Scott GB, Rose SA, Tan NG and Robinson PA. UCH-L1 aggresome formation in response to proteasome impairment indicates a role in inclusion formation in Parkinson's disease. Journal of neurochemistry. 2004; 90(2):379-391.
46. Nijman SM, Huang TT, Dirac AM, Brummelkamp TR, Kerkhoven RM, D'Andrea AD and Bernards R. The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Molecular cell. 2005; 17(3):331-339.
47. Popov N, Wanzel M, Madiredjo M, Zhang D, Beijersbergen R, Bernards R, Moll R, Elledge SJ and Eilers M. The ubiquitin-specific protease USP28 is required for MYC stability. Nature cell biology. 2007; 9(7):765-774.
48. Shan J, Zhao W and Gu W. Suppression of cancer cell growth by promoting cyclin D1 degradation. Molecular cell. 2009; 36(3):469-476.
49. Schwickart M, Huang X, Lill JR, Liu J, Ferrando R, French DM, Maecker H, O'Rourke K, Bazan F, Eastham-Anderson J, Yue P, Dornan D, Huang DC and Dixit VM. Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature. 2010; 463(7277):103-107.
50. Bignell GR, Warren W, Seal S, Takahashi M, Rapley E, Barfoot R, Green H, Brown C, Biggs PJ, Lakhani SR, Jones C, Hansen J, Blair E, Hofmann B, Siebert R, Turner G, et al. Identification of the familial cylindromatosis tumour-suppressor gene. Nature genetics. 2000; 25(2):160-165.
51. Lee EG, Boone DL, Chai S, Libby SL, Chien M, Lodolce JP and Ma A. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science (New York, NY). 2000; 289(5488):2350-2354.
52. Hershko A and Rose IA. Ubiquitin-aldehyde: a general inhibitor of ubiquitin-recycling processes. Proceedings of the National Academy of Sciences of the United States of America. 1987; 84(7):1829-1833.
53. Borodovsky A, Kessler BM, Casagrande R, Overkleeft HS, Wilkinson KD and Ploegh HL. A novel active site-directed probe specific for deubiquitylating enzymes reveals proteasome association of USP14. The EMBO journal. 2001; 20(18):5187-5196.
54. Kapuria V, Peterson LF, Fang D, Bornmann WG, Talpaz M and Donato NJ. Deubiquitinase inhibition by small-molecule WP1130 triggers aggresome formation and tumor cell apoptosis. Cancer research. 2010; 70(22):9265-9276.
55. Perry JW, Ahmed M, Chang KO, Donato NJ, Showalter HD and Wobus CE. Antiviral activity of a small molecule deubiquitinase inhibitor occurs via induction of the unfolded protein response. PLoS pathogens. 2012; 8(7):e1002783.
56. Chauhan D, Tian Z, Nicholson B, Kumar KG, Zhou B, Carrasco R, McDermott JL, Leach CA, Fulcinniti M, Kodrasov MP, Weinstock J, Kingsbury WD, Hideshima T, Shah PK, Minvielle S, Altun M, et al. A small molecule inhibitor of ubiquitin-specific protease-7 induces apoptosis in multiple myeloma cells and overcomes bortezomib resistance. Cancer cell. 2012; 22(3):345-358.
57. Fan YH, Cheng J, Vasudevan SA, Dou J, Zhang H, Patel RH, Ma IT, Rojas Y, Zhao Y, Yu Y, Zhang H, Shohet JM, Nuchtern JG, Kim ES and Yang J. USP7 inhibitor P22077 inhibits neuroblastoma growth via inducing p53-mediated apoptosis. Cell death&disease. 2013; 4:e867.
58. Altun M, Kramer HB, Willems LI, McDermott JL, Leach CA, Goldenberg SJ, Kumar KG, Konietzny R, Fischer R, Kogan E, Mackeen MM, McGouran J, Khoronenkova SV, Parsons JL, Dianov GL, Nicholson B, et al. Activity-based chemical proteomics accelerates inhibitor development for deubiquitylating enzymes. Chemistry biology. 2011; 18(11):1401-1412.
59. Seiberlich V, Goldbaum O, Zhukareva V and Richter-Landsberg C. The small molecule inhibitor PR-619 of deubiquitinating enzymes affects the microtubule network and causes protein aggregate formation in neural cells: implications for neurodegenerative diseases. Biochim Biophys Acta. 2012; 1823(11):2057-2068.
60. Liu CW and Jacobson AD. Functions of the 19S complex in proteasomal degradation. Trends in biochemical sciences. 2013; 38(2):103-110.
61. Yao T and Cohen RE. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature. 2002; 419(6905):403-407.
62. Spataro V, Simmen K and Realini CA. The essential 26S proteasome subunit Rpn11 confers multidrug resistance to mammalian cells. Anticancer research. 2002; 22(6c):3905-3909.
63. Nabhan JF and Ribeiro P. The 19 S proteasomal subunit POH1 contributes to the regulation of c-Jun ubiquitination, stability, and subcellular localization. The Journal of biological chemistry. 2006; 281(23):16099-16107.
64. Gallery M, Blank JL, Lin Y, Gutierrez JA, Pulido JC, Rappoli D, Badola S, Rolfe M and Macbeth KJ. The JAMM motif of human deubiquitinase Poh1 is essential for cell viability. Molecular cancer therapeutics. 2007; 6(1):262-268.
65. Lee MJ, Lee BH, Hanna J, King RW and Finley D. Trimming of ubiquitin chains by proteasome-associated deubiquitinating enzymes. Molecular&cellular proteomics: MCP. 2011; 10(5):R110.003871.
66. Koulich E, Li X and De Martino GN. Relative structural and functional roles of multiple deubiquitylating proteins associated with mammalian 26S proteasome. Molecular biology of the cell. 2008; 19(3):1072-1082.
67. Hanna J, Hathaway NA, Tone Y, Crosas B, Elsasser S, Kirkpatrick DS, Leggett DS, Gygi SP, King RW and Finley D. Deubiquitinating enzyme Ubp6 functions noncatalytically to delay proteasomal degradation. Cell. 2006; 127(1):99-111.
68. Jin YN, Chen PC, Watson JA, Walters BJ, Phillips SE, Green K, Schmidt R, Wilson JA, Johnson GV, Roberson ED, Dobrunz LE and Wilson SM. Usp14 deficiency increases tau phosphorylation without altering tau degradation or causing tau-dependent deficits. PloS one. 2012; 7(10):e47884.
69. Chen PC, Bhattacharyya BJ, Hanna J, Minkel H, Wilson JA, Finley D, Miller RJ and Wilson SM. Ubiquitin homeostasis is critical for synaptic development and function. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2011; 31(48):17505-17513.
70. Jung H, Kim BG, Han WH, Lee JH, Cho JY, Park WS, Maurice MM, Han JK, Lee MJ, Finley D and Jho EH. Deubiquitination of Dishevelled by Usp14 is required for Wnt signaling. Oncogenesis. 2013; 2:e64.
71. Huranova M, Hnilicova J, Fleischer B, Cvackova Z and Stanek D. A mutation linked to retinitis pigmentosa in HPRP31 causes protein instability and impairs its interactions with spliceosomal snRNPs. Human molecular genetics. 2009; 18(11):2014-2023.
72. Wu N, Liu C, Bai C, Han YP, Cho WC and Li Q. Over-Expression of Deubiquitinating Enzyme USP14 in Lung Adenocarcinoma Promotes Proliferation through the Accumulation of beta-Catenin. International journal of molecular sciences. 2013; 14(6):10749-10760.
73. Wu N, Zhang C, Bai C, Han YP and Li Q. MiR-4782-3p inhibited non-small cell lung cancer growth via USP14. Cellular physiology and biochemistry: international journal of experimental cellular physiology, biochemistry, and pharmacology. 2014; 33(2):457-467.
74. Mialki RK, Zhao J, Wei J, Mallampalli DF and Zhao Y. Overexpression of USP14 protease reduces I-kappaB protein levels and increases cytokine release in lung epithelial cells. The Journal of biological chemistry. 2013; 288(22):15437-15441.
75. Yao T, Song L, Xu W, DeMartino GN, Florens L, Swanson SK, Washburn MP, Conaway RC, Conaway JW and Cohen RE. Proteasome recruitment and activation of the Uch37 deubiquitinating enzyme by Adrm1. Nature cell biology. 2006; 8(9):994-1002.
76. Schreiner P, Chen X, Husnjak K, Randles L, Zhang N, Elsasser S, Finley D, Dikic I, Walters KJ and Groll M. Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature. 2008; 453(7194):548-552.
77. Chen X, Lee BH, Finley D and Walters KJ. Structure of proteasome ubiquitin receptor hRpn13 and its activation by the scaffolding protein hRpn2. Molecular cell. 2010; 38(3):404-415.
78. Mazumdar T, Gorgun FM, Sha Y, Tyryshkin A, Zeng S, Hartmann-Petersen R, Jorgensen JP, Hendil KB and Eissa NT. Regulation of NF-kappaB activity and inducible nitric oxide synthase by regulatory particle non-ATPase subunit 13 (Rpn13). Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(31):13854-13859.
79. Wicks SJ, Haros K, Maillard M, Song L, Cohen RE, Dijke PT and Chantry A. The deubiquitinating enzyme UCH37 interacts with Smads and regulates TGF-beta signalling. Oncogene. 2005; 24(54):8080-8084.
80. Ko YM, Chang CY, Chiou SJ, Hsu FJ, Huang JS, Yang YL, Guh JY and Chuang LY. Ubiquitin C-terminal hydrolase-L5 is required for high glucose-induced transforming growth factor-beta receptor I expression and hypertrophy in mesangial cells. Archives of biochemistry and biophysics. 2013; 535(2):177-186.
81. Chen Z, Niu X, Li Z, Yu Y, Ye X, Lu S and Chen Z. Effect of ubiquitin carboxy-terminal hydrolase 37 on apoptotic in A549 cells. Cell biochemistry and function. 2011; 29(2):142-148.
82. Fang Y, Fu D, Tang W, Cai Y, Ma D, Wang H, Xue R, Liu T, Huang X, Dong L, Wu H and Shen X. Ubiquitin C-terminal Hydrolase 37, a novel predictor for hepatocellular carcinoma recurrence, promotes cell migration and invasion via interacting and deubiquitinating PRP19. Biochimica et biophysica acta. 2013; 1833(3):559-572.
83. Lee BH, Lee MJ, Park S, Oh DC, Elsasser S, Chen PC, Gartner C, Dimova N, Hanna J, Gygi SP, Wilson SM, King RW and Finley D. Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature. 2010; 467(7312):179-184.
84. Xu YH and Guo NL. USP14 inhibitor IU1 prevents ventilator-induced lung injury in rats. Cellular and molecular biology (Noisy-le-Grand, France). 2014; 60(2):50-54.
85. Nag DK and Finley D. A small-molecule inhibitor of deubiquitinating enzyme USP14 inhibits Dengue virus replication. Virus research. 2012; 165(1):103-106.
86. Finley DJ, King RK, Lee BH, Lee MJ and Gahman TC. Tricycle proteasome activity enhancing compounds. United States Patent NO 20130210845A1.
87. D'Arcy P, Brnjic S, Olofsson MH, Fryknas M, Lindsten K, De Cesare M, Perego P, Sadeghi B, Hassan M, Larsson R and Linder S. Inhibition of proteasome deubiquitinating activity as a new cancer therapy. Nature medicine. 2011; 17(12):1636-1640.
88. Tian Z, D'Arcy P, Wang X, Ray A, Tai YT, Hu Y, Carrasco RD, Richardson P, Linder S, Chauhan D and Anderson KC. A novel small molecule inhibitor of deubiquitylating enzyme USP14 and UCHL5 induces apoptosis in multiple myeloma and overcomes bortezomib resistance. Blood. 2014; 123(5):706-716.
89. Feng X, Holmlund T, Zheng C and Fadeel B. Proapoptotic effects of the novel proteasome inhibitor b-AP15 on multiple myeloma cells and natural killer cells. Experimental hematology. 2014; 42(3):172-182.
90. Sarhan D, D'Arcy P and Lundqvist A. Regulation of TRAIL-receptor expression by the ubiquitin-proteasome system. International journal of molecular sciences. 2014; 15(10):18557-18573.
91. Sarhan D, Wennerberg E, D'Arcy P, Gurajada D, Linder S and Lundqvist A. A novel inhibitor of proteasome deubiquitinating activity renders tumor cells sensitive to TRAIL-mediated apoptosis by natural killer cells and T cells. Cancer immunology, immunotherapy: CII. 2013; 62(8):1359-1368.
92. Wang X, Stafford W, Mazurkiewicz M, Fryknas M, Brjnic S, Zhang X, Gullbo J, Larsson R, Arner ES, D'Arcy P and Linder S. The 19S Deubiquitinase inhibitor b-AP15 is enriched in cells and elicits rapid commitment to cell death. Molecular pharmacology. 2014; 85(6):932-945.
93. Linder S and Larsson R. Method for inhibition of deubiquitinating actiity. United States Patent NO 201402283 54A1.
94. Zhou B, Zuo Y, Li B, Wang H, Liu H, Wang X, Qiu X, Hu Y, Wen S, Du J and Bu X. Deubiquitinase inhibition of 19S regulatory particles by 4-arylidene curcumin analog AC17 causes NF-kappaB inhibition and p53 reactivation in human lung cancer cells. Molecular cancer therapeutics. 2013; 12(8):1381-1392.
95. Zhang JJ, Ng KM, Lok CN, Sun RW and Che CM. Deubiquitinases as potential anti-cancer targets for gold(III) complexes. Chemical communications (Cambridge, England). 2013; 49(45):5153-5155.
96. Liu N, Liu C, Li X, Liao S, Song W, Yang C, Zhao C, Huang H, Guan L, Zhang P, Liu S, Hua X, Chen X, Zhou P, Lan X, Yi S, et al. A novel proteasome inhibitor suppresses tumor growth via targeting both 19S proteasome deubiquitinases and 20S proteolytic peptidases. Scientific reports. 2014; 4:5240.
97. Liu N, Li X, Huang H, Zhao C, Liao S, Yang C, Liu S, Song W, Lu X, Lan X, Chen X, Yi S, Xu L, Jiang L, Zhao C, Dong X, et al. Clinically used antirheumatic agent auranofin is a proteasomal deubiquitinase inhibitor and inhibits tumor growth. Oncotarget. 2014; 5(14):5453-5471.
98. Groth Petersen D, Dahllof I and Nielsen LP. Effects of zinc pyrithione and copper pyrithione on microbial community function and structure in sediments. Environmental toxicology and chemistry/SETAC. 2004; 23(4):921-928.
99. Chen X, Shi X, Zhao C, Li X, Lan X, Liu S, Huang H, Liu N, Liao S, Zang D, Song W, Liu Q, Carter BZ, Dou QP, Wang X and Liu J. Anti-rheumatic agent auranofin induced apoptosis in chronic myeloid leukemia cells resistant to imatinib through both Bcr/Abl-dependent and -independent mechanisms. Oncotarget. 2014; 5(19):9118-9132.