Proteasome inhibition: A new therapeutic strategy to cancer treatment

Cancer Letters

Volumn 293, Issue 1, 2010, Pages 15-22

  Wu, William Ka Kei ^a   Cho, Chi Hin ^a   Lee, Chung Wa ^a   Wu, Kaichun ^b   Fan, Daiming ^b   Yu, Jun ^a   Yiu Sung, Joseph Jao ^a  

^a and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Autophagy; Cancer; Proliferation; Proteasome inhibitor; Signaling

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BONE MORPHOGENETIC PROTEIN; BORTEZOMIB; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEASOME; PROTEASOME INHIBITOR; PROTEIN BCL 2; PROTEIN BNIP3; PROTEIN NOXA; PROTEIN P53; UBIQUITIN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; AUTOPHAGY; AUTOREGULATION; BONE MARROW SUPPRESSION; CANCER CHEMOTHERAPY; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL PROLIFERATION; DRUG RESPONSE; ENZYME INHIBITION; GENE REPRESSION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MULTIPLE MYELOMA; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RNA INTERFERENCE; SENSITIZATION; SHORT SURVEY; SIGNAL TRANSDUCTION; SOLID TUMOR; UBIQUITINATION;

EID: 77952420148     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2009.12.002     Document Type: Review

References (119)

1. Schwartz A.L., Ciechanover A. The ubiquitin-proteasome pathway and pathogenesis of human diseases. Annu. Rev. Med. 1999, 50:57-74.
2. Rubinsztein D.C. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 2006, 443:780-786.
3. Cheng Y. Toward an atomic model of the 26S proteasome. Curr. Opin. Struct. Biol. 2009, 19:203-208.
4. Marques A.J., Palanimurugan R., Matias A.C., Ramos P.C., Dohmen R.J. Catalytic mechanism and assembly of the proteasome. Chem. Rev. 2009, 109:1509-1536.
5. Richardson P.G., Mitsiades C., Hideshima T., Anderson K.C. Bortezomib: proteasome inhibition as an effective anticancer therapy. Annu. Rev. Med. 2006, 57:33-47.
6. Yang Y., Kitagaki J., Dai R.M., Tsai Y.C., Lorick K.L., Ludwig R.L., Pierre S.A., Jensen J.P., Davydov I.V., Oberoi P., Li C.C., Kenten J.H., Beutler J.A., Vousden K.H., Weissman A.M. Inhibitors of ubiquitin-activating enzyme (E1), a new class of potential cancer therapeutics. Cancer Res. 2007, 67:9472-9481.
7. Grinkevich V.V., Nikulenkov F., Shi Y., Enge M., Bao W., Maljukova A., Gluch A., Kel A., Sangfelt O., Selivanova G. Ablation of key oncogenic pathways by RITA-reactivated p53 is required for efficient apoptosis. Cancer Cell 2009, 15:441-453.
8. Liu X., Yue P., Chen S., Hu L., Lonial S., Khuri F.R., Sun S.Y. The proteasome inhibitor PS-341 (bortezomib) up-regulates DR5 expression leading to induction of apoptosis and enhancement of TRAIL-induced apoptosis despite up-regulation of c-FLIP and survivin expression in human NSCLC cells. Cancer Res. 2007, 67:4981-4988.
9. Sun J., Nam S., Lee C.S., Li B., Coppola D., Hamilton A.D., Dou Q.P., Sebti S.M. CEP1612, a dipeptidyl proteasome, inhibitor, induces p21WAF1 and p27KIP1 expression and apoptosis and inhibits the growth of the human lung adenocarcinoma A-549 in nude mice. Cancer Res. 2001, 61:1280-1284.
10. Fribley A., Zeng Q., Wang C.Y. Proteasome inhibitor PS-341 induces apoptosis through induction of endoplasmic reticulum stress-reactive oxygen species in head and neck squamous cell carcinoma cells. Mol. Cell. Biol. 2004, 24:9695-9704.
11. Wu W.K., Sung J.J., Wu Y.C., Li Z.J., Yu L., Cho C.H. Bone morphogenetic protein signalling is required for the anti-mitogenic effect of the proteasome inhibitor MG-132 on colon cancer cells. Br. J. Pharmacol. 2008, 154:632-638.
12. Fan X.M., Wong B.C., Wang W.P., Zhou X.M., Cho C.H., Yuen S.T., Leung S.Y., Lin M.C., Kung H.F., Lam S.K. Inhibition of proteasome function induced apoptosis in gastric cancer. Int. J. Cancer 2001, 93:481-488.
13. Chen K.F., Yeh P.Y., Yeh K.H., Lu Y.S., Huang S.Y., Cheng A.L. Down-regulation of phospho-Akt is a major molecular determinant of bortezomib-induced apoptosis in hepatocellular carcinoma cells. Cancer Res. 2008, 68:6698-6707.
14. Ustundag Y., Bronk S.F., Gores GJ G.J. Proteasome inhibition-induces endoplasmic reticulum dysfunction and cell death of human cholangiocarcinoma cells. World J. Gastroenterol. 2007, 13:851-857.
15. Märten A., Zeiss N., Serba S., Mehrle S., von Lilienfeld-Toal M., Schmidt J J. Bortezomib is ineffective in an orthotopic mouse model of pancreatic adenocarcinoma. Mol. Cancer Ther. 2008, 7:3624-3631.
16. Mitsiades C.S., McMillin D., Kotoula V., Poulaki V., McMullan C., Negri J., Fanourakis G., Tseleni-Balafouta S., Ain K.B., Mitsiades N. Antitumor effects of the proteasome inhibitor bortezomib in medullary and anaplastic thyroid carcinoma cells in vitro. J. Clin. Endocrinol. Metab. 2006, 91:4013-4021.
17. An J., Rettig M.B. Epidermal growth factor receptor inhibition sensitizes renal cell carcinoma cells to the cytotoxic effects of bortezomib. Mol. Cancer Ther. 2007, 6:61-69.
18. Kamat A.M., Karashima T., Davis D.W., Lashinger L., Bar-Eli M., Millikan R., Shen Y., Dinney C.P., McConkey D.J. The proteasome inhibitor bortezomib synergizes with gemcitabine to block the growth of human 253JB-V bladder tumors in vivo. Mol. Cancer Ther. 2004, 3:279-290.
19. Bazzaro R.B., 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.
20. Cardoso F., Durbecq V., Laes J.F., Badran B., Lagneaux L., Bex F., Desmedt C., Willard-Gallo K., Ross J.S., Burny A., Piccart M., Sotiriou C. Bortezomib (PS-341, Velcade) increases the efficacy of trastuzumab (Herceptin) in HER-2-positive breast cancer cells in a synergistic manner. Mol. Cancer Ther. 2006, 5:3042-3051.
21. Birle D.C., Hedley D.W. Suppression of the hypoxia-inducible factor-1 response in cervical carcinoma xenografts by proteasome inhibitors. Cancer Res. 2007, 67:1735-1743.
22. Dolcet X., Llobet D., Encinas M., Pallares J., Cabero A., Schoenenberger J.A., Comella J.X., Matias-Guiu X. Proteasome inhibitors induce death but activate NF-kappaB on endometrial carcinoma cell lines and primary culture explants. J. Biol. Chem. 2006, 281:22118-22130.
23. Ikezoe T., Yang Y., Saito T., Koeffler H.P., Taguchi H. Proteasome inhibitor PS-341 down-regulates prostate-specific antigen (PSA) and induces growth arrest and apoptosis of androgen-dependent human prostate cancer LNCaP cells. Cancer Sci. 2004, 95:271-275.
24. Sun X., Gulyás M., Hjerpe A., Dobra K. Proteasome inhibitor PSI induces apoptosis in human mesothelioma cells. Cancer Lett. 2006, 232:161-169.
25. Brignole C., Marimpietri D., Pastorino F., Nico B., Di Paolo D., Cioni M., Piccardi F., Cilli M., Pezzolo A., Corrias M.V., Pistoia V., Ribatti D., Pagnan G., Ponzoni M. Effect of bortezomib on human neuroblastoma cell growth, apoptosis, and angiogenesis. J. Natl. Cancer Inst. 2006, 98:1142-1157.
26. Yin D., Zhou H., Kumagai T., Liu G., Ong J.M., Black K.L., Koeffler H.P. Proteasome inhibitor PS-341 causes cell growth arrest and apoptosis in human glioblastoma multiforme (GBM). Oncogene 2005, 24:344-354.
27. Taniguchi E., Cho M.J., Arenkiel B.R., Hansen M.S., Rivera O.J., McCleish A.T., Qualman S.J., Guttridge D.C., Scott M.P., Capecchi M.R., Keller C. Bortezomib reverses a post-translational mechanism of tumorigenesis for patched1 haplo insufficiency in medulloblastoma. Pediatr. Blood Cancer 2009, 53:136-144.
28. Poulaki V., Mitsiades C.S., Kotoula V., Negri J., McMillin D., Miller J.W., Mitsiades N. The proteasome inhibitor bortezomib induces apoptosis in human retinoblastoma cell lines in vitro. Invest. Ophthalmol. Vis. Sci. 2007, 48:4706-4719.
29. Størling J., Allaman-Pillet N., Karlsen A.E., Billestrup N., Bonny C., Mandrup-Poulsen T. Antitumorigenic effect of proteasome inhibitors on insulinoma cells. Endocrinology 2005, 146:1718-1726.
30. Młynarczuk-Biały I., Roeckmann H., Kuckelkorn U., Schmidt B., Umbreen S., Gołab J., Ludwig A., Montag C., Wiebusch L., Hagemeier C., Schadendorf D., Kloetzel P.M., Seifert U. Combined effect of proteasome and calpain inhibition on cisplatin-resistant human melanoma cells. Cancer Res. 2006, 66:7598-7605.
31. Bersani F., Taulli R., Accornero P., Morotti A., Miretti S., Crepaldi T., Ponzetto C. Bortezomib-mediated proteasome inhibition as a potential strategy for the treatment of rhabdomyosarcoma. Eur. J. Cancer 2008, 44:876-884.
32. Lu G., Punj V., Chaudhary P.M. Proteasome inhibitor bortezomib induces cell cycle arrest and apoptosis in cell lines derived from Ewing's sarcoma family of tumors and synergizes with TRAIL. Cancer Biol. Ther. 2008, 7:603-608.
33. Lauricella M., D'Anneo A., Giuliano M., Calvaruso G., Emanuele S., Vento R., Tesoriere G. Induction of apoptosis in human osteosarcoma Saos-2 cells by the proteasome inhibitor MG132 and the protective effect of pRb. Cell Death Differ. 2003, 10:930-932.
34. Chu S., Alexiadis M., Fuller P.J. Proteasome inhibition by bortezomib decreases proliferation and increases apoptosis in ovarian granulosa cell tumors. Reprod. Sci. 2009, 16:397-407.
35. Hideshima T., Mitsiades C., Akiyama M., Hayashi T., Chauhan D., Richardson P., Schlossman R., Podar K., Munshi N.C., Mitsiades N., Anderson K.C. Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341. Blood 2003, 101:1530-1534.
36. Pérez-Galán P., Roué G., Villamor N., Montserrat E., Campo E., Colomer D. The proteasome inhibitor bortezomib induces apoptosis in mantle-cell lymphoma through generation of ROS and noxa activation independent of p53 status. Blood 2006, 107:257-264.
37. Dunleavy K., Pittaluga S., Czuczman M.S., Dave S.S., Wright G., Grant N., Shovlin M., Jaffe E.S., Janik J.E., Staudt L.M., Wilson W.H. Differential efficacy of bortezomib plus chemotherapy within molecular subtypes of diffuse large B-cell lymphoma. Blood 2009, 113:6069-6076.
38. Zhang Q.L., Wang L., Zhang Y.W., Jiang X.X., Yang F., Wu W.L., Janin A., Chen Z., Shen Z.X., Chen S.J., Zhao W.L. The proteasome inhibitor bortezomib interacts synergistically with the histone deacetylase inhibitor suberoylanilide hydroxamic acid to induce T-leukemia/lymphoma cells apoptosis. Leukemia 2009, 23:1507-1514.
39. Shen L., Au W.Y., Guo T., Wong K.Y., Wong M.L., Tsuchiyama J., Yuen P.W., Kwong Y.L., Liang R.H., Srivastava G. Proteasome inhibitor bortezomib-induced apoptosis in natural killer (NK)-cell leukemia and lymphoma: an in vitro and in vivo preclinical evaluation. Blood 2007, 110:469-470.
40. Zhao X., Qiu W., Kung J., Zhao X., Peng X., Yegappan M., Yen-Lieberman B., Hsi ED E.D. Bortezomib induces caspase-dependent apoptosis in Hodgkin lymphoma cell lines and is associated with reduced c-FLIP expression: a gene expression profiling study with implications for potential combination therapies. Leuk. Res. 2008, 32:275-285.
41. Orlowski R.Z., Eswara J.R., Lafond-Walker A., Grever M.R., Orlowski M., Dang C.V. Tumor growth inhibition induced in a murine model of human Burkitt's lymphoma by a proteasome inhibitor. Cancer Res. 1998, 58:4328-4342.
42. Dimopoulos M.A., Anagnostopoulos A., Kyrtsonis M.C., Castritis E., Bitsaktsis A., Pangalis G.A. Treatment of relapsed or refractory Waldenström's macroglobulinemia with bortezomib. Haematologica 2005, 90:1655-1658.
43. Colado E., Alvarez-Fernández S., Maiso P., Martín-Sánchez J., Vidriales M.B., Garayoa M., Ocio E.M., Montero J.C., Pandiella A., San Miguel J.F. The effect of the proteasome inhibitor bortezomib on acute myeloid leukemia cells and drug resistance associated with the CD34+ immature phenotype. Haematologica 2008, 93:57-66.
44. Dou Q.P., McGuire T.F., Peng Y., An B. Proteasome inhibition leads to significant reduction of Bcr-Abl expression and subsequent induction of apoptosis in K562 human chronic myelogenous leukemia cells. J. Pharmacol. Exp. Ther. 1999, 289:781-790.
45. Ruiz S., Krupnik Y., Keating M., Chandra J., Palladino M., McConkey D. The proteasome inhibitor NPI-0052 is a more effective inducer of apoptosis than bortezomib in lymphocytes from patients with chronic lymphocytic leukemia. Mol. Cancer Ther. 2006, 5:1836-1843.
46. Mitsiades N., Mitsiades C.S., Richardson P.G., Poulaki V., Tai Y.T., Chauhan D., Fanourakis G., Gu X., Bailey C., Joseph M., Libermann T.A., Schlossman R., Munshi N.C., Hideshima T., Anderson K.C. The proteasome inhibitor PS-341 potentiates sensitivity of multiple myeloma cells to conventional chemotherapeutic agents: therapeutic applications. Blood 2003, 101:2377-2380.
47. Miller C.P., Ban K., Dujka M.E., McConkey D.J., Munsell M., Palladino M., Chandra J. NPI-0052, a novel proteasome inhibitor,induces caspase-8 and ROS-dependent apoptosis alone and in combination with HDAC inhibitors in leukemia cells. Blood 2007, 110:267-277.
48. Cascone T., Morelli M.P., Morgillo F., Kim W.Y., Rodolico G., Pepe S., Tortora G., Berrino L., Lee H.Y., Heymach J.V., Ciardiello F. Synergistic anti-proliferative and pro-apoptotic activity of combined therapy with bortezomib, a proteasome inhibitor, with anti-epidermal growth factor receptor (EGFR) drugs in human cancer cells. J. Cell. Physiol. 2008, 216:698-707.
49. Goel A., Dispenzieri A., Greipp P.R., Witzig T.E., Mesa R.A., Russell S.J. PS-341-mediated selective targeting of multiple myeloma cells by synergistic increase in ionizing radiation-induced apoptosis. Exp. Hematol. 2005, 33:784-795.
50. Orlowski R.Z., Kuhn D.J. Proteasome inhibitors in cancer therapy: lessons from the first decade. Clin. Cancer Res. 2008, 14:1649-1657.
51. Richardson P.G., Mitsiades C., Hideshima T., Anderson K.C. Proteasome inhibition in the treatment of cancer. Cell Cycle 2005, 4:290-296.
52. Cresta S., Sessa C., Catapano C.V., Gallerani E., Passalacqua D., Rinaldi A., Bertoni F., Viganò L., Maur M., Capri G., Maccioni E., Tosi D., Gianni L. Phase I study of bortezomib with weekly paclitaxel in patients with advanced solid tumours. Eur. J. Cancer 2008, 44:1829-1834.
53. Lashinger L.M., Zhu K., Williams S.A., Shrader M., Dinney C.P., McConkey D.J. Bortezomib abolishes tumor necrosis factor-related apoptosis-inducing ligand resistance via a p21-dependent mechanism in human bladder and prostate cancer cells. Cancer Res. 2005, 65:4902-4908.
54. Nickeleit I., Zender S., Sasse F., Geffers R., Brandes G., Sörensen I., Steinmetz H., Kubicka S., Carlomagno T., Menche D., Gütgemann I., Buer J., Gossler A., Manns M.P., Kalesse M., Frank R., Malek N.P. Argyrin a reveals a critical role for the tumor suppressor protein p27(kip1) in mediating antitumor activities in response to proteasome inhibition. Cancer Cell 2008, 14:23-35.
55. Lomonosova E., Ryerse J., Chinnadurai G. BAX/BAK-independent mitoptosis during cell death induced by proteasome inhibition. Mol. Cancer Res. 2009, 7:1268-1284.
56. Cao W., Shiverick K.T., Namiki K., Sakai Y., Porvasnik S., Urbanek C., Rosser C.J. Docetaxel and bortezomib downregulate Bcl-2 and sensitize PC-3-Bcl-2 expressing prostate cancer cells to irradiation. World J. Urol. 2008, 26:509-516.
57. Uddin S., Ahmed M., Bavi P., El-Sayed R., Al-Sanea N., AbdulJabbar A., Ashari L.H., Alhomoud S., Al-Dayel F., Hussain A.R., Al-Kuraya KS K.S. Bortezomib (Velcade) induces p27Kip1 expression through S-phase kinase protein 2 degradation in colorectal cancer. Cancer Res. 2008, 68:3379-3388.
58. Allen C., Saigal K., Nottingham L., Arun P., Chen Z., Van Waes C C. Bortezomib-induced apoptosis with limited clinical response is accompanied by inhibition of canonical but not alternative nuclear factor-{kappa}B subunits in head and neck cancer. Clin. Cancer Res. 2008, 14:4175-4185.
59. Kardosh A., Golden E.B., Pyrko P., Uddin J., Hofman F.M., Chen T.C., Louie S.G., Petasis N.A., Schönthal A.H. Aggravated endoplasmic reticulum stress as a basis for enhanced glioblastoma cell killing by bortezomib in combination with celecoxib or its non-coxib analogue, 2,5-dimethyl-celecoxib. Cancer Res. 2008, 68:843-851.
60. Miller C.P., Ban K., Dujka M.E., McConkey D.J., Munsell M., Palladino M., Chandra J. NPI-0052, a novel proteasome inhibitor, induces caspase-8 and ROS-dependent apoptosis alone and in combination with HDAC inhibitors in leukemia cells. Blood 2007, 110:267-277.
61. Wu W.K., Volta V., Cho C.H., Wu Y.C., Li H.T., Yu L., Li Z.J., Sung J.J. Repression of protein translation and mTOR signaling by proteasome inhibitor in colon cancer cells. Biochem. Biophys. Res. Commun. 2009, 386:598-601.
62. Zhang W., Tong Q., Li S., Wang X., Wang Q. MG-132 inhibits telomerase activity, induces apoptosis and G(1) arrest associated with upregulated p27kip1 expression and downregulated survivin expression in gastric carcinoma cells. Cancer Invest. 2008, 26:1032-1036.
63. Chen K.F., Yeh P.Y., Hsu C., Hsu C.H., Lu Y.S., Hsieh H.P., Chen P.J., Cheng A.L. Bortezomib overcomes tumor necrosis factor-related apoptosis-inducing ligand resistance in hepatocellular carcinoma cells in part through the inhibition of the phosphatidylinositol 3-kinase/Akt pathway. J. Biol. Chem. 2009, 284:11121-11133.
64. He Q., Huang Y., Sheikh M.S. Proteasome inhibitor MG132 upregulates death receptor 5 and cooperates with Apo2L/TRAIL to induce apoptosis in Bax-proficient and -deficient cells. Oncogene 2004, 23:2554-2558.
65. Miller C.P., Rudra S., Keating M.J., Wierda W.G., Palladino M., Chandra J. Caspase-8 dependent histone acetylation by a novel proteasome inhibitor, NPI-0052: a mechanism for synergy in leukemia cells. Blood 2009, 113:4289-4299.
66. Lim J.H., Chang Y.C., Park Y.B., Park J.W., Kwon T.K. Transcriptional repression of E2F gene by proteasome inhibitors in human osteosarcoma cells. Biochem. Biophys. Res. Commun. 2004, 318:868-872.
67. Hideshima T., Chauhan D., Hayashi T., Akiyama M., Mitsiades N., Mitsiades C., Podar K., Munshi N.C., Richardson P.G., Anderson K.C. Proteasome inhibitor PS-341 abrogates IL-6 triggered signaling cascades via caspase-dependent downregulation of gp130 in multiple myeloma. Oncogene 2003, 22:8386-8393.
68. Jagani Z., Song K., Kutok J.L., Dewar M.R., Melet A., Santos T., Grassian A., Ghaffari S., Wu C., Ren R., Rodin H.Y., Miller K., Khosravi-Far R. Proteasome inhibition causes regression of leukemia and abrogates BCR-ABL-induced evasion of apoptosis in part through regulation of forkhead tumor suppressors. Cancer Res. 2009, 69:6546-6555.
69. Bhat U.G., Halasi M., Gartel A.L. FoxM1 is a general target for proteasome inhibitors. PLoS ONE 2009, 4:e6593.
70. Poruchynsky M.S., Sackett D.L., Robey R.W., Ward Y., Annunziata C., Fojo T. Proteasome inhibitors increase tubulin polymerization and stabilization in tissue culture cells: a possible mechanism contributing to peripheral neuropathy and cellular toxicity following proteasome inhibition. Cell Cycle 2008, 7:940-949.
71. Shen L., Au W.Y., Wong K.Y., Shimizu N., Tsuchiyama J., Kwong Y.L., Liang R.H., Srivastava G. Cell death by bortezomib-induced mitotic catastrophe in natural killer lymphoma cells. Mol. Cancer Ther. 2008, 7:3807-3815.
72. Baritaki S., Chapman A., Yeung K., Spandidos D.A., Palladino M., Bonavida B. Inhibition of epithelial to mesenchymal transition in metastatic prostate cancer cells by the novel proteasome inhibitor, NPI-0052: pivotal roles of Snail repression and RKIP induction. Oncogene 2009, 28:3573-3585.
73. Meissner M., Reichenbach G., Stein M., Hrgovic I., Kaufmann R., Gille J. Down-regulation of vascular endothelial growth factor receptor 2 is a major molecular determinant of proteasome inhibitor-mediated antiangiogenic action in endothelial cells. Cancer Res. 2009, 69:1976-1984.
74. Schumacher L.Y., Vo D.D., Garban H.J., Comin-Anduix B., Owens S.K., Dissette V.B., Glaspy J.A., McBride W.H., Bonavida B., Economou J.S., Ribas A. Immunosensitization of tumor cells to dendritic cell-activated immune responses with the proteasome inhibitor bortezomib (PS-341, Velcade). J. Immunol. 2006, 176:4757-4765.
75. Blickwedehl J., Agarwal M., Seong C., Pandita R.K., Melendy T., Sung P., Pandita T.K., Bangia N. Role for proteasome activator PA200 and postglutamyl proteasome activity in genomic stability. Proc. Natl. Acad. Sci. USA 2008, 105:16165-16170.
76. Fujita T., Washio K., Takabatake D., Takahashi H., Yoshitomi S., Tsukuda K., Ishibe Y., Ogasawara Y., Doihara H., Shimizu N. Proteasome inhibitors can alter the signaling pathways and attenuate the P-glycoprotein-mediated multidrug resistance. Int. J. Cancer 2005, 117:670-682.
77. Milani M., Rzymski T., Mellor H.R., Pike L., Bottini A., Generali D., Harris A.L. The role of ATF4 stabilization and autophagy in resistance of breast cancer cells treated with bortezomib. Cancer Res. 2009, 69:4415-4423.
78. Hideshima T., Ikeda H., Chauhan D., Okawa Y., Raje N., Podar K., Mitsiades C., Munshi N.C., Richardson P.G., Carrasco R.D., Anderson K.C. Bortezomib induces canonical nuclear factor-kappaB activation in multiple myeloma cells. Blood 2009, 114:1046-1052.
79. Sloss C.M., Wang F., Liu R., Xia L., Houston M., Ljungman D., Palladino M.A., Cusack J.C. Proteasome inhibition activates epidermal growth factor receptor (EGFR) and EGFR-independent mitogenic kinase signaling pathways in pancreatic cancer cells. Clin. Cancer Res. 2008, 14:5116-5123.
80. Li C., Zang Y., Sen M., Leeman-Neill R.J., Man D.S., Grandis J.R., Johnson D.E. Bortezomib up-regulates activated signal transducer and activator of transcription-3 and synergizes with inhibitors of signal transducer and activator of transcription-3 to promote head and neck squamous cell carcinoma cell death. Mol. Cancer Ther. 2009, 8:2211-2220.
81. Ayala G., Yan J., Li R., Ding Y., Thompson T.C., Mims M.P., Hayes T.G., MacDonnell V., Lynch P.G., Frolov A., Miles B.J., Wheeler T.M., Harper J.W., Tsai M.J., Ittmann M.M., Kadmon D. Bortezomib-mediated inhibition of steroid receptor coactivator-3 degradation leads to activated Akt. Clin. Cancer Res. 2008, 14:7511-7518.
82. Loeffler-Ragg J., Mueller D., Gamerith G., Auer T., Skvortsov S., Sarg B., Skvortsova I., Schmitz K.J., Martin H.J., Krugmann J., Alakus H., Maser E., Menzel J., Hilbe W., Lindner H., Schmid K.W., Zwierzina H. Proteomic identification of aldo-keto reductase AKR1B10 induction after treatment of colorectal cancer cells with the proteasome inhibitor bortezomib. Mol. Cancer Ther. 2009, 8:1995-2006.
83. Du Z.X., Zhang H.Y., Meng X., Guan Y., Wang H.Q. Role of oxidative stress and intracellular glutathione in the sensitivity to apoptosis induced by proteasome inhibitor in thyroid cancer cells. BMC Cancer 2009, 9:56.
84. Maki C.G., Huibregtse J.M., Howley P.M. In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res. 1996, 56:2649-2654.
85. P. Roth, M. Kissel, C. Herrmann, G. Eisele, J. Leban, M. Weller, F. Schmidt, SC68896, A novel small molecule proteasome inhibitor, exerts antiglioma activity in vitro and in vivo, Clin. Cancer Res. doi: 10.1158/1078-0432.CCR-09-0548.
86. Ling Y.H., Liebes L., Jiang J.D., Holland J.F., Elliott P.J., Adams J., Muggia F.M., Perez-Soler R. Mechanisms of proteasome inhibitor PS-341-induced G(2)-M-phase arrest and apoptosis in human non-small cell lung cancer cell lines. Clin. Cancer Res. 2003, 9:145-154.
87. Blagosklonny M.V., Wu G.S., Omura S., el-Deiry W.S. Proteasome-dependent regulation of p21WAF1/CIP1 expression. Biochem. Biophys. Res. Commun. 1996, 227:564-569.
88. Pagano M., Tam S.W., Theodoras A.M., Beer-Romero P., Del Sal G., Chau V., Yew P.R., Draetta G.F., Rolfe M. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 1995, 269:682-685.
89. Green D.R., Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004, 305:626-629.
90. Podar K., Gouill S.L., Zhang J., Opferman J.T., Zorn E., Tai Y.T., Hideshima T., Amiot M., Chauhan D., Harousseau J.L., Anderson K.C. A pivotal role for Mcl-1 in bortezomib-induced apoptosis. Oncogene 2008, 27:721-731.
91. Iijima M., Momose I., Ikeda D. TP-110, a new proteasome inhibitor, down-regulates IAPs in human multiple myeloma cells. Anticancer Res. 2009, 29:977-985.
92. Liu A., Niswander L.A. Bone morphogenetic protein signalling and vertebrate nervous system development. Nat. Rev. Neurosci. 2005, 6:945-954.
93. Bleuming S.A., He X.C., Kodach L.L., Hardwick J.C., Koopman F.A., Ten Kate F.J., van Deventer S.J., Hommes D.W., Peppelenbosch M.P., Offerhaus G.J., Li L., van den Brink G.R. Bone morphogenetic protein signaling suppresses tumorigenesis at gastric epithelial transition zones in mice. Cancer Res. 2007, 67:8149-8155.
94. Howe J.R., Bair J.L., Sayed M.G., Anderson M.E., Mitros F.A., Petersen G.M., Velculescu V.E., Traverso G., Vogelstein B. Germline mutations of the gene encoding bone morphogenetic protein receptor 1A in juvenile polyposis. Nat. Genet. 2001, 28:184-187.
95. Garrett I.R., Chen D., Gutierrez G., Zhao M., Escobedo A., Rossini G., Harris S.E., Gallwitz W., Kim K.B., Hu S., Crews C.M., Mundy G.R. Selective inhibitors of the osteoblast proteasome stimulate bone formation in vivo and in vitro. J. Clin. Invest. 2003, 111:1771-1782.
96. Aza-Blanc P., Ramírez-Weber F.A., Laget M.P., Schwartz C., Kornberg T.B. Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 1997, 89:1043-1053.
97. Ingham P.W. Transducing Hedgehog: the story so far. EMBO J. 1998, 17:3505-3511.
98. Jiang J., Struhl G. Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 1998, 391:493-496.
99. Chen C.H., von Kessler D.P., Park W., Wang B., Ma Y., Beachy P.A. Nuclear trafficking of cubitus interruptus in the transcriptional regulation of hedgehog target gene expression. Cell 1999, 98:305-316.
100. Wu W.K., Sung J.J., Yu L., Cho C.H. Proteasome inhibitor MG-132 lowers gastric adenocarcinoma TMK1 cell proliferation via bone morphogenetic protein signaling. Biochem. Biophys. Res. Commun. 2008, 371:209-214.
101. Mamane Y., Petroulakis E., LeBacquer O., Sonenberg N. mTOR, translation initiation and cancer. Oncogene 2006, 25:6416-6422.
102. Ghosh P., Wu M., Zhang H., Sun H. mTORC1 signaling requires proteasomal function and the involvement of CUL4-DDB1 ubiquitin E3 ligase. Cell Cycle 2008, 7:373-381.
103. Mazroui R., Di Marco S., Kaufman R.J., Gallouzi I.E. Inhibition of the ubiquitin-proteasome system induces stress granule formation. Mol. Biol. Cell 2007, 18:2603-2618.
104. Schewe D.M., Aguirre-Ghiso J.A. Inhibition of eIF2alpha dephosphorylation maximizes bortezomib efficiency and eliminates quiescent multiple myeloma cells surviving proteasome inhibitor therapy. Cancer Res. 2009, 69:1545-1552.
105. Nawrocki S.T., Carew J.S., Jr Dunner K., Boise L.H., Chiao P.J., Huang P., Abbruzzese J.L., McConkey D.J. Bortezomib inhibits PKR-like endoplasmic reticulum (ER) kinase and induces apoptosis via ER stress in human pancreatic cancer cells. Cancer Res. 2005, 65:11510-11519.
106. Chen J.J., Chou C.W., Chang Y.F., Chen C.C. Proteasome inhibitors enhance TRAIL-induced apoptosis through the intronic regulation of DR5: involvement of NF-kappa B and reactive oxygen species-mediated p53 activation. J. Immunol. 2008, 180:8030-8039.
107. Baritaki S., Suzuki E., Umezawa K., Spandidos D.A., Berenson J., Daniels T.R., Penichet M.L., Jazirehi A.R., Palladino M., Bonavida B. Inhibition of Yin Yang 1-dependent repressor activity of DR5 transcription and expression by the novel proteasome inhibitor NPI-0052 contributes to its TRAIL-enhanced apoptosis in cancer cells. J. Immunol. 2008, 180:6199-6210.
108. Kandasamy K., Kraft A.S. Proteasome inhibitor PS-341 (Velcade) induces stabilization of the TRAIL receptor DR5 mRNA through the 3′-untranslated region. Mol. Cancer Ther. 2008, 7:1091-1100.
109. Butler J.E., Moore M.B., Presnell S.R., Chan H.W., Chalupny N.J., Lutz C.T. Proteasome regulation of ULBP1 transcription. J. Immunol. 2009, 182:6600-6609.
110. Mizushima N., Levine B., Cuervo A.M., Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
111. Kang M.R., Kim M.S., Oh J.E., Kim Y.R., Song S.Y., Kim S.S., Ahn C.H., Yoo N.J., Lee S.H. Frameshift mutations of autophagy-related genes, ATG2B, ATG5, ATG9B and ATG12 in gastric and colorectal cancers with microsatellite instability. J. Pathol. 2009, 217:702-706.
112. Scarlatti F., Granata R., Meijer A.J., Codogno P. Does autophagy have a license to kill mammalian cells?. Cell Death Differ. 2009, 16:12-20.
113. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
114. Fung C., Lock R., Gao S., Salas E., Debnath J. Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol. Biol. Cell 2008, 19:797-806.
115. Abedin M.J., Wang D., McDonnell M.A., Lehmann U., Kelekar A. Autophagy delays apoptotic death in breast cancer cells following DNA damage. Cell Death Differ. 2007, 14:500-510.
116. Wu W.K., Wu Y.C., Yu L., Li Z.J., Sung J.J., Cho C.H. Induction of autophagy by proteasome inhibitor is associated with proliferative arrest in colon cancer cells. Biochem. Biophys. Res. Commun. 2008, 374:258-263.
117. Ge P.F., Zhang J.Z., Wang X.F., Meng F.K., Li W.C., Luan Y.X., Ling F., Luo Y.N. Inhibition of autophagy induced by proteasome inhibition increases cell death in human SHG-44 glioma cells. Acta Pharmacol. Sin. 2009, 30:1046-1052.
118. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006, 441:431-436.
119. Rodriguez M.S., Wright J., Thompson J., Thomas D., Baleux F., Virelizier J.L., Hay R.T., Arenzana-Seisdedos F. Identification of lysine residues required for signal-induced ubiquitination and degradation of I kappa B-alpha in vivo. Oncogene 1996, 12:2425-2435.