A novel proteasome inhibitor suppresses tumor growth via targeting both 19S proteasome deubiquitinases and 20S proteolytic peptidases

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Liu, Ningning ^a   Liu, Chunjiao ^a   Li, Xiaofen ^a   Liao, Siyan ^a   Song, Wenbin ^a   Yang, Changshan ^a   Zhao, Chong ^a   Huang, Hongbiao ^a   Guan, Lixia ^a   Zhang, Peiquan ^a   Liu, Shouting ^a   Hua, Xianliang ^a   Chen, Xin ^a   Zhou, Ping ^a   Lan, Xiaoying ^a   Yi, Songgang ^a   Wang, Shunqing ^a   Wang, Xuejun ^a,b   Dou, Q Ping ^a,c   Liu, Jinbao ^a  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BORONIC ACID DERIVATIVE; BORTEZOMIB; COPPER PYRITHIONE; DEUBIQUITINASE; ORGANOMETALLIC COMPOUND; PEPTIDE HYDROLASE; PROTEASOME; PROTEASOME INHIBITOR; PROTEINASE INHIBITOR; PYRAZINE DERIVATIVE; PYRIDINE DERIVATIVE; UBIQUITIN;

ANIMAL; BAGG ALBINO MOUSE; CELL LINE; DRUG EFFECTS; HEK293 CELL LINE; HEPG2 CELL LINE; HUMAN; MALE; METABOLISM; MOUSE; MULTIPLE MYELOMA; NUDE MOUSE; PROTEIN DEGRADATION; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; BORONIC ACIDS; CELL LINE; CELL LINE, TUMOR; HEK293 CELLS; HEP G2 CELLS; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MULTIPLE MYELOMA; ORGANOMETALLIC COMPOUNDS; PEPTIDE HYDROLASES; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; PROTEOLYSIS; PYRAZINES; PYRIDINES; UBIQUITIN; UBIQUITIN-SPECIFIC PROTEASES;

EID: 84902257060     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep05240     Document Type: Article

References (43)

1. Richardson, P. G. et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N. Engl. J. Med. 348, 2609-2617 (2003). (Pubitemid 36741588)
2. Adams, J. The development of proteasome inhibitors as anticancer drugs. Cancer Cell 5, 417-421 (2004). (Pubitemid 38610244)
3. Richardson, P. G. et al. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N. Engl. J. Med. 352, 2487-2498 (2005). (Pubitemid 41007864)
4. Galanski, M., Arion, V. B., Jakupec, M. A. & Keppler, B. K. Recent developments in the field of tumor-inhibiting metal complexes. Curr. Pharm. Des. 9, 2078-2089 (2003). (Pubitemid 37142439)
5. Galanski, M., Jakupec, M. A. & Keppler, B. K. Update of the preclinical situation of anticancer platinum complexes: novel design strategies and innovative analytical approaches. Curr. Med. Chem. 12, 2075-2094 (2005). (Pubitemid 41093559)
6. Daniel, K. G., Gupta, P., Harbach, R. H., Guida, W. C. & Dou, Q. P. Organic copper complexes as a new class of proteasome inhibitors and apoptosis inducers in human cancer cells. Biochem. Pharmacol. 67, 1139-1151 (2004). (Pubitemid 38296793)
7. Cvek, B., Milacic, V., Taraba, J. & Dou, Q. P. Ni(II), Cu(II), and Zn(II) diethyldithiocarbamate complexes show various activities against the proteasome in breast cancer cells. J. Med. Chem. 51, 6256-6258 (2008).
8. Verani, C. N. Metal complexes as inhibitors of the 26S proteasome in tumor cells. J. Inorg. Biochem. 106, 59-67 (2012).
9. Chen, D., Cui, Q. C., Yang, H. & Dou, Q. P. Disulfiram, a clinically used antialcoholism drug and copper-binding agent, induces apoptotic cell death in breast cancer cultures and xenografts via inhibition of the proteasome activity. Cancer Res. 66, 10425-10433 (2006). (Pubitemid 44799763)
10. Chen, D. et al. 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 Res. 67, 1636-1644 (2007). (Pubitemid 46383389)
11. Skrott, Z. & Cvek, B. Diethyldithiocarbamate complex with copper: the mechanism of action in cancer cells. Mini. Rev. Med. Chem. 12, 1184-1192 (2012).
12. Daniel, K. G. et al. Clioquinol and pyrrolidine dithiocarbamate complex with copper to form proteasome inhibitors and apoptosis inducers in human breast cancer cells. Breast Cancer Res. 7, R897-908 (2005).
13. Milacic, V. et al. Pyrrolidine dithiocarbamate-zinc(II) and -copper(II) complexes induce apoptosis in tumor cells by inhibiting the proteasomal activity. Toxicol. Appl. Pharmacol. 231, 24-33 (2008).
14. Fraile, J. M., Quesada, V., Rodriguez, D., Freije, J. M. & Lopez-Otin, C. Deubiquitinases in cancer: new functions and therapeutic options. Oncogene 31, 2373-2388 (2012).
15. Yao, T. et al. Proteasome recruitment and activation of the Uch37 deubiquitinating enzyme by Adrm1. Nat. Cell Biol. 8, 994-1002 (2006). (Pubitemid 44314731)
16. Verma, R. et al. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298, 611-615 (2002). (Pubitemid 35215317)
17. Lam, Y. A., Xu, W., DeMartino, G. N. & Cohen, R. E. Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature 385, 737-740 (1997). (Pubitemid 27098096)
18. Lee, M. J., Lee, B. H., Hanna, J., King, R. W. & Finley, D. Trimming of ubiquitin chains by proteasome-associated deubiquitinating enzymes. Mol. Cell Proteomics 10, R110 003871 (2011).
19. Chandler, C. J. & Segel, I. H. Mechanism of the antimicrobial action of pyrithione: effects on membrane transport, ATP levels, and protein synthesis. Antimicrob. Agents Chemother. 14, 60-68 (1978). (Pubitemid 8370708)
20. Davies, T. W. The dissolution rate of zinc pyrithione. Int. J. Cosmet. Sci. 7, 153-156 (1985). (Pubitemid 16169565)
21. Fenn, R. V. & Alexander, M. T. Determination of zinc pyrithione in hair care products by normal phase liquid chromatography. J. Liq. Chromatogr. 11, 3403-3413 (1988). (Pubitemid 19099016)
22. Hu, M. et al. Structure and mechanisms of the proteasome-associated deubiquitinating enzyme USP14. Embo. J. 24, 3747-3756 (2005). (Pubitemid 41581691)
23. Maiti, T. K. et al. Crystal structure of the catalytic domain of UCHL5, a proteasome-associated human deubiquitinating enzyme, reveals an unproductive form of the enzyme. Febs. J. 278, 4917-4926 (2011).
24. Koulich, E., Li, X. & DeMartino, G. N. Relative structural and functional roles of multiple deubiquitylating proteins associated with mammalian 26S proteasome. Mol. Biol. Cell 19, 1072-1082 (2008). (Pubitemid 351481820)
25. Milacic, V. & Dou, Q. P. The tumor proteasome as a novel target for gold(III) complexes: implications for breast cancer therapy. Coord. Chem. Rev. 253, 1649-1660 (2009).
26. Mochida, K. et al. Inhibition of acetylcholinesterase by metabolites of copper pyrithione (CuPT) and its possible involvement in vertebral deformity of a CuPTexposed marine teleostean fish. Comp Biochem Physiol C Toxicol Pharmacol. 149, 624-30 (2009).
27. Mochida, K., Amano, H., Onduka, T., Kakuno, A. & Fujii, K. Toxicity and metabolism of copper pyrithione and its degradation product, 2,2′- dipyridyldisulfide in a marine polychaete. Chemosphere. 82, 390-397 (2011).
28. Milacic, V., Jiao, P., Zhang, B., Yan, B. & Dou, Q. P. Novel 8-hydroxylquinoline analogs induce copper-dependent proteasome inhibition and cell death in human breast cancer cells. Int. J. Oncol. 35, 1481-1491 (2009).
29. Zuo, J. et al. Cellular and computational studies of proteasome inhibition and apoptosis induction in human cancer cells by amino acid Schiff base-copper complexes. J. Inorg. Biochem. 118, 83-93 (2012).
30. Qiu, M. et al. Zinc ionophores pyrithione inhibits herpes simplex virus replication through interfering with proteasome function and NF-kappaB activation. Antiviral Res. 100, 44-53 (2013).
31. Lindskog, S. & Malmstrom, B. G. Metal binding and catalytic activity in bovine carbonic anhydrase. J. Biol. Chem. 237, 1129-1137 (1962).
32. Lee, B. H. et al. Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature 467, 179-184 (2010).
33. Faergemann, J. Management of seborrheic dermatitis and pityriasis versicolor. Am. J. Clin. Dermatol. 1, 75-80 (2000).
34. Groth Petersen, D., Dahllof, I. & Nielsen, L. P. Effects of zinc pyrithione and copper pyrithione on microbial community function and structure in sediments. Environ. Toxicol. Chem. 23, 921-928 (2004). (Pubitemid 38418641)
35. Tailler, M. et al. Antineoplastic activity of ouabain and pyrithione zinc in acute myeloid leukemia. Oncogene 31, 3536-3546 (2012).
36. Carraway, R. E. & Dobner, P. R. Zinc pyrithione induces ERK- and PKCdependent necrosis distinct from TPEN-induced apoptosis in prostate cancer cells. Biochim. Biophys. Acta 1823, 544-557 (2012).
37. Li, X. et al. Gambogic acid is a tissue-specific proteasome inhibitor in vitro and in vivo. Cell Rep. 3, 211-222 (2013).
38. Huang, H. et al. Physiological levels of ATP negatively regulate proteasome function. Cell Res. 20, 1372-1385 (2010).
39. Huang, H. et al. L-carnitine is an endogenous HDAC inhibitor selectively inhibiting cancer cell growth in vivo and in vitro. PLoS One 7, e49062 (2012).
40. D'Arcy, P. et al. Inhibition of proteasome deubiquitinating activity as a new cancer therapy. Nat. Med. 17, 1636-1640 (2011).
41. Dayal, S. et al. Suppression of the deubiquitinating enzyme USP5 causes the accumulation of unanchored polyubiquitin and the activation of p53. J. Biol. Chem. 284, 5030-5041 (2009).
42. Borodovsky, A. et al. A novel active site-directed probe specific for deubiquitylating enzymes reveals proteasome association of USP14. Embo. J. 20, 5187-5196 (2001). (Pubitemid 32910913)
43. Shi, X. et al. Gambogic acid induces apoptosis in imatinib-resistant chronic myeloid leukemia cells via inducing proteasome inhibition and caspasedependent Bcr-Abl downregulation. Clin. Cancer Res. 20,151-163 (2014).