A bis-Benzylidine Piperidone Targeting Proteasome Ubiquitin Receptor RPN13/ADRM1 as a Therapy for Cancer

Cancer Cell

Volumn 24, Issue 6, 2013, Pages 791-805

  Anchoori, RaviK ^a   Karanam, Balasubramanyam ^a   Peng, Shiwen ^a   Wang, JoshuaW ^a   Jiang, Rosie ^a   Tanno, Toshihiko ^a   Orlowski, RobertZ ^b   Matsui, William ^a   Zhao, Ming ^a   Rudek, MichelleA ^a   Hung, Chien fu ^a   Chen, Xiang ^c,d   Walters, KylieJ ^c,d   Roden, RichardB S ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BORTEZOMIB; PIPERIDONE DERIVATIVE; PROTEASOME; PROTEIN ADRM1; PROTEIN E6; PROTEIN RPN13; RA 190; RECEPTOR PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG DISTRIBUTION; DRUG TARGETING; ENDOPLASMIC RETICULUM STRESS; FEMALE; HUMAN PAPILLOMAVIRUS TYPE 16; MOUSE; MULTIPLE MYELOMA; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; TUMOR GROWTH; TUMOR XENOGRAFT;

EID: 84891913291     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2013.11.001     Document Type: Article

References (39)

1. Al-Shami A., Jhaver K.G., Vogel P., Wilkins C., Humphries J., Davis J.J., Xu N., Potter D.G., Gerhardt B., Mullinax R., et al. Regulators of the proteasome pathway, Uch37 and Rpn13, play distinct roles in mouse development. PLoS ONE 2010, 5:e13654.
2. Anchoori R.K., Khan S.R., Sueblinvong T., Felthauser A., Iizuka Y., Gavioli R., Destro F., Isaksson Vogel R., Peng S., Roden R.B., Bazzaro M. Stressing the ubiquitin-proteasome system without 20S proteolytic inhibition selectively kills cervical cancer cells. PLoS ONE 2011, 6:e23888.
3. Arastu-Kapur S., Anderl J.L., Kraus M., Parlati F., Shenk K.D., Lee S.J., Muchamuel T., Bennett M.K., Driessen C., Ball A.J., et al. Nonproteasomal targets of the proteasome inhibitors bortezomib and carfilzomib: a link to clinical adverse events. Clin. Cancer Res. 2011, 17:2734-2743.
4. Bazzaro M., Lee M.K., Zoso A., Stirling W.L., Santillan A., Shih IeM., Roden R.B. Ubiquitin-proteasome system stress sensitizes ovarian cancer to proteasome inhibitor-induced apoptosis. Cancer Res. 2006, 66:3754-3763.
5. Bazzaro M., Lin Z., Santillan A., Lee M.K., Wang M.C., Chan K.C., Bristow R.E., Mazitschek R., Bradner J., Roden R.B. Ubiquitin proteasome system stress underlies synergistic killing of ovarian cancer cells by bortezomib and a novel HDAC6 inhibitor. Clin. Cancer Res. 2008, 14:7340-7347.
6. Bazzaro M., Anchoori R.K., Mudiam M.K., Issaenko O., Kumar S., Karanam B., Lin Z., Isaksson Vogel R., Gavioli R., Destro F., et al. α,β-Unsaturated carbonyl system of chalcone-based derivatives is responsible for broad inhibition of proteasomal activity and preferential killing of human papilloma virus (HPV) positive cervical cancer cells. J.Med. Chem. 2011, 54:449-456.
7. Bedford L., Lowe J., Dick L.R., Mayer R.J., Brownell J.E. Ubiquitin-like protein conjugation and the ubiquitin-proteasome system as drug targets. Nat. Rev. Drug Discov. 2011, 10:29-46.
8. + Tcell immune responses compared to intramuscular injection and intradermal gene gun delivery. Vaccine 2009, 27:5450-5459.
9. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 1998, 54:905-921.
10. Chauhan D., Catley L., Li G., Podar K., Hideshima T., Velankar M., Mitsiades C., Mitsiades N., Yasui H., Letai A., et al. A novel orally active proteasome inhibitor induces apoptosis in multiple myeloma cells with mechanisms distinct from Bortezomib. Cancer Cell 2005, 8:407-419.
11. Chen W., Hu X.T., Shi Q.L., Zhang F.B., He C. Knockdown of the novel proteasome subunit Adrm1 located on the 20q13 amplicon inhibits colorectal cancer cell migration, survival and tumorigenicity. Oncol. Rep. 2009, 21:531-537.
12. Chen S., Blank J.L., Peters T., Liu X.J., Rappoli D.M., Pickard M.D., Menon S., Yu J., Driscoll D.L., Lingaraj T., et al. Genome-wide siRNA screen for modulators of cell death induced by proteasome inhibitor bortezomib. Cancer Res. 2010, 70:4318-4326.
13. Chen X., Lee B.H., Finley D., Walters K.J. Structure of proteasome ubiquitin receptor hRpn13 and its activation by the scaffolding protein hRpn2. Mol. Cell 2010, 38:404-415.
14. Ciechanover A. The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J. 1998, 17:7151-7160.
15. Deveraux Q., Ustrell V., Pickart C., Rechsteiner M. A 26S protease subunit that binds ubiquitin conjugates. J.Biol. Chem. 1994, 269:7059-7061.
16. Dominguez C., Boelens R., Bonvin A.M. HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J.Am. Chem. Soc. 2003, 125:1731-1737.
17. Fejzo M.S., Anderson L., von Euw E.M., Kalous O., Avliyakulov N.K., Haykinson M.J., Konecny G.E., Finn R.S., Slamon D.J. Amplification Target ADRM1: Role as an Oncogene and Therapeutic Target for Ovarian Cancer. Int. J. Mol. Sci. 2013, 14:3094-3109.
18. Gandhi T.K., Zhong J., Mathivanan S., Karthick L., Chandrika K.N., Mohan S.S., Sharma S., Pinkert S., Nagaraju S., Periaswamy B., et al. Analysis of the human protein interactome and comparison with yeast, worm and fly interaction datasets. Nat. Genet. 2006, 38:285-293.
19. Hamazaki J., Iemura S., Natsume T., Yashiroda H., Tanaka K., Murata S. A novel proteasome interacting protein recruits the deubiquitinating enzyme UCH37 to 26S proteasomes. EMBO J. 2006, 25:4524-4536.
20. Hideshima T., Bradner J.E., Wong J., Chauhan D., Richardson P., Schreiber S.L., Anderson K.C. Small-molecule inhibition of proteasome and aggresome function induces synergistic antitumor activity in multiple myeloma. Proc. Natl. Acad. Sci. USA 2005, 102:8567-8572.
21. Husnjak K., Elsasser S., Zhang N., Chen X., Randles L., Shi Y., Hofmann K., Walters K.J., Finley D., Dikic I. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 2008, 453:481-488.
22. Ito T., Chiba T., Ozawa R., Yoshida M., Hattori M., Sakaki Y. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA 2001, 98:4569-4574.
23. Koulich E., Li X., DeMartino G.N. Relative structural and functional roles of multiple deubiquitylating proteins associated with mammalian 26S proteasome. Mol. Biol. Cell 2008, 19:1072-1082.
24. Kuhn D.J., Berkova Z., Jones R.J., Woessner R., Bjorklund C.C., Ma W., Davis R.E., Lin P., Wang H., Madden T.L., et al. Targeting the insulin-like growth factor-1 receptor to overcome bortezomib resistance in preclinical models of multiple myeloma. Blood 2012, 120:3260-3270.
25. Lin Z., Bazzaro M., Wang M.C., Chan K.C., Peng S., Roden R.B. Combination of proteasome and HDAC inhibitors for uterine cervical cancer treatment. Clin. Cancer Res. 2009, 15:570-577.
26. Luker G.D., Pica C.M., Song J., Luker K.E., Piwnica-Worms D. Imaging 26S proteasome activity and inhibition in living mice. Nat. Med. 2003, 9:969-973.
27. Moody C.A., Laimins L.A. Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer 2010, 10:550-560.
28. Qiu X.B., Ouyang S.Y., Li C.J., Miao S., Wang L., Goldberg A.L. hRpn13/ADRM1/GP110 is a novel proteasome subunit that binds the deubiquitinating enzyme, UCH37. EMBO J. 2006, 25:5742-5753.
29. Ri M., Iida S., Nakashima T., Miyazaki H., Mori F., Ito A., Inagaki A., Kusumoto S., Ishida T., Komatsu H., et al. Bortezomib-resistant myeloma cell lines: a role for mutated PSMB5 in preventing the accumulation of unfolded proteins and fatal ER stress. Leukemia 2010, 24:1506-1512.
30. Ruschak A.M., Slassi M., Kay L.E., Schimmer A.D. Novel proteasome inhibitors to overcome bortezomib resistance. J.Natl. Cancer Inst. 2011, 103:1007-1017.
31. Sakata E., Bohn S., Mihalache O., Kiss P., Beck F., Nagy I., Nickell S., Tanaka K., Saeki Y., Förster F., Baumeister W. Localization of the proteasomal ubiquitin receptors Rpn10 and Rpn13 by electron cryomicroscopy. Proc. Natl. Acad. Sci. USA 2012, 109:1479-1484.
32. Scheffner M., Huibregtse J.M., Vierstra R.D., Howley P.M. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993, 75:495-505.
33. Schreiner P., Chen X., Husnjak K., Randles L., Zhang N., Elsasser S., Finley D., Dikic I., Walters K.J., Groll M. Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 2008, 453:548-552.
34. Schwartz A.L., Ciechanover A. Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annu. Rev. Pharmacol. Toxicol. 2009, 49:73-96.
35. Spisek R., Dhodapkar M.V. Towards a better way to die with chemotherapy: role of heat shock protein exposure on dying tumor cells. Cell Cycle 2007, 6:1962-1965.
36. + Tcell responses and antitumor effects generated by DNA vaccine administered through gene gun, biojector, and syringe. Vaccine 2003, 21:4036-4042.
37. Vousden K.H., Lu X. Live or let die: the cell's response to p53. Nat. Rev. Cancer 2002, 2:594-604.
38. + T-cell immunity in cervical cancer patients by a human papillomavirus type 16 E6 and E7 long peptides vaccine. Clin. Cancer Res. 2008, 14:178-187.
39. Yao T., Song L., Xu W., DeMartino G.N., Florens L., Swanson S.K., Washburn M.P., Conaway R.C., Conaway J.W., Cohen R.E. Proteasome recruitment and activation of the Uch37 deubiquitinating enzyme by Adrm1. Nat. Cell Biol. 2006, 8:994-1002.