Carfilzomib and oprozomib synergize with histone deacetylase inhibitors in head and neck squamous cell carcinoma models of acquired resistance to proteasome inhibitors

Cancer Biology and Therapy

Volumn 15, Issue 9, 2014, Pages 1142-1152

  Zang, Yan ^a   Kirk, Christopher J ^b   Johnson, Daniel E ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b ONYX PHARMACEUTICALS   (United States)

Author keywords

Acquired resistance; Bortezomib; Carfilzomib; Entinostat; MDR 1 P gp; Oprozomib; Vorinostat

Indexed keywords

ABCB1 PROTEIN, HUMAN; ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN; BIK PROTEIN, HUMAN; BORONIC ACID DERIVATIVE; BORTEZOMIB; CARFILZOMIB; CISPLATIN; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; MEMBRANE PROTEIN; MULTIDRUG RESISTANCE PROTEIN; OLIGOPEPTIDE; OPROZOMIB; PROTEASOME INHIBITOR; PYRAZINE DERIVATIVE; REVERSIN 121; VORINOSTAT;

APOPTOSIS; DRUG EFFECTS; DRUG POTENTIATION; DRUG RESISTANCE; HEAD AND NECK TUMOR; HUMAN; METABOLISM; PATHOLOGY; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BORONIC ACIDS; BORTEZOMIB; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CISPLATIN; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; HEAD AND NECK NEOPLASMS; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; MEMBRANE PROTEINS; OLIGOPEPTIDES; P-GLYCOPROTEIN; P-GLYCOPROTEINS; PROTEASOME INHIBITORS; PYRAZINES;

EID: 84906828490     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.29452     Document Type: Article

References (49)

1. Adams J, Kauffman M. Development of the proteasome inhibitor Velcade (Bortezomib). Cancer Invest 2004; 22:304-11; PMID:15199612; http://dx.doi.org/ 10.1081/CNV-120030218
2. Bross PF, Kane R, Farrell AT, Abraham S, Benson K, Brower ME, Bradley S, Gobburu JV, Goheer A, Lee SL, et al. Approval summary for bortezomib for injection in the treatment of multiple myeloma. Clin Cancer Res 2004; 10:3954-64; PMID:15217925; http://dx.doi.org/10.1158/1078-0432.CCR-03-0781
3. Richardson PG, Barlogie B, Berenson J, Singhal S, Jagannath S, Irwin D, Rajkumar SV, Srkalovic G, Alsina M, Alexanian R, et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med 2003; 348:2609-17; PMID:12826635; http://dx.doi.org/10.1056/NEJMoa030288
4. Richardson PG, Sonneveld P, Schuster MW, Irwin D, Stadtmauer EA, Facon T, Harousseau JL, Ben-Yehuda D, Lonial S, Goldschmidt H, et al.; Assessment of Proteasome Inhibition for Extending Remissions (APEX) Investigators. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N Engl J Med 2005; 352:2487-98; PMID:15958804; http://dx.doi.org/10.1056/NEJMoa043445
5. Fisher RI, Bernstein SH, Kahl BS, Djulbegovic B, Robertson MJ, de Vos S, Epner E, Krishnan A, Leonard JP, Lonial S, et al. Multicenter phase II study of bortezomib in patients with relapsed or refractory mantle cell lymphoma. J Clin Oncol 2006; 24:4867-74; PMID:17001068; http://dx.doi.org/10.1200/JCO.2006.07. 9665
6. Sunwoo JB, Chen Z, Dong G, Yeh N, Crowl Bancroft C, Sausville E, Adams J, Elliott P, Van Waes C. Novel proteasome inhibitor PS-341 inhibits activation of nuclear factor-kappa B, cell survival, tumor growth, and angiogenesis in squamous cell carcinoma. Clin Cancer Res 2001; 7:1419-28; PMID:11350913
7. Fribley A, Zeng Q, Wang CY. 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; 24:9695-704; PMID:15509775; http://dx.doi.org/10.1128/MCB.24.22.9695-9704.2004
8. Li C, Li R, Grandis JR, Johnson DE. Bortezomib induces apoptosis via Bim and Bik up-regulation and synergizes with cisplatin in the killing of head and neck squamous cell carcinoma cells. Mol Cancer Ther 2008; 7:1647-55; PMID:18566236; http://dx.doi.org/10.1158/1535-7163.MCT-07-2444
9. Li C, Johnson DE. Liberation of functional p53 by proteasome inhibition in human papilloma viruspositive head and neck squamous cell carcinoma cells promotes apoptosis and cell cycle arrest. Cell Cycle 2013; 12:923-34; PMID:23421999; http://dx.doi.org/10.4161/cc.23882
10. Lorch JH, Thomas TO, Schmoll HJ. Bortezomib inhibits cell-cell adhesion and cell migration and enhances epidermal growth factor receptor inhibitor-induced cell death in squamous cell cancer. Cancer Res 2007; 67:727-34; PMID:17234784; http://dx.doi.org/10.1158/0008-5472.CAN-06-2162
11. Allen C, Saigal K, Nottingham L, Arun P, Chen Z, Van Waes C. Bortezomib-induced apoptosis with limited clinical response is accompanied by inhibition of canonical but not alternative nuclear factor-kappaB subunits in head and neck cancer. Clin Cancer Res 2008; 14:4175-85; PMID:18593997; http://dx.doi.org/10.1158/1078-0432.CCR-07-4470
12. Van Waes C, Chang AA, Lebowitz PF, Druzgal CH, Chen Z, Elsayed YA, Sunwoo JB, Rudy SF, Morris JC, Mitchell JB, et al. Inhibition of nuclear factor-kappaB and target genes during combined therapy with proteasome inhibitor bortezomib and reirradiation in patients with recurrent head-and-neck squamous cell carcinoma. Int J Radiat Oncol Biol Phys 2005; 63:1400-12; PMID:16005577; http://dx.doi.org/10.1016/j.ijrobp.2005.05.007
13. Kubicek GJ, Axelrod RS, Machtay M, Ahn PH, Anne PR, Fogh S, Cognetti D, Myers TJ, Curran WJ Jr., Dicker AP. Phase I trial using the proteasome inhibitor bortezomib and concurrent chemoradiotherapy for head-and-neck malignancies. Int J Radiat Oncol Biol Phys 2012; 83:1192-7; PMID:22245208; http://dx.doi.org/10. 1016/j.ijrobp.2011.09.023
14. Gilbert J, Lee JW, Argiris A, Haigentz M Jr., Feldman LE, Jang M, Arun P, Van Waes C, Forastiere AA. Phase II 2-arm trial of the proteasome inhibitor, PS-341 (bortezomib) in combination with irinotecan or PS-341 alone followed by the addition of irinotecan at time of progression in patients with locally recurrent or metastatic squamous cell carcinoma of the head and neck (E1304): a trial of the Eastern Cooperative Oncology Group. Head Neck 2013; 35:942-8; PMID:22791234; http://dx.doi.org/10.1002/hed.23046
15. Chung CH, Aulino J, Muldowney NJ, Hatakeyama H, Baumann J, Burkey B, Netterville J, Sinard R, Yarbrough WG, Cmelak AJ, et al. Nuclear factor-kappa B pathway and response in a phase II trial of bortezomib and docetaxel in patients with recurrent and/or metastatic head and neck squamous cell carcinoma. Ann Oncol 2010; 21:864-70; PMID:19850643; http://dx.doi.org/10.1093/annonc/mdp390
16. Dudek AZ, Lesniewski-Kmak K, Shehadeh NJ, Pandey ON, Franklin M, Kratzke RA, Greeno EW, Kumar P. Phase I study of bortezomib and cetuximab in patients with solid tumours expressing epidermal growth factor receptor. Br J Cancer 2009; 100:1379-84; PMID:19401697; http://dx.doi.org/10.1038/sj.bjc.6605043
17. Argiris A, Duffy AG, Kummar S, Simone NL, Arai Y, Kim SW, Rudy SF, Kannabiran VR, Yang X, Jang M, et al. Early tumor progression associated with enhanced EGFR signaling with bortezomib, cetuximab, and radiotherapy for head and neck cancer. Clin Cancer Res 2011; 17:5755-64; PMID:21750205; http://dx.doi.org/10.1158/1078-0432.CCR-11-0861
18. Arastu-Kapur S, Anderl JL, Kraus M, Parlati F, Shenk KD, Lee SJ, Muchamuel T, Bennett MK, Driessen C, Ball AJ, et al. Nonproteasomal targets of the proteasome inhibitors bortezomib and carfilzomib: a link to clinical adverse events. Clin Cancer Res 2011; 17:2734-43; PMID:21364033; http://dx.doi.org/10. 1158/1078-0432.CCR-10-1950
19. Orlowski RZ, Nagler A, Sonneveld P, Bladé J, Hajek R, Spencer A, San Miguel J, Robak T, Dmoszynska A, Horvath N, et al. Randomized phase III study of pegylated liposomal doxorubicin plus bortezomib compared with bortezomib alone in relapsed or refractory multiple myeloma: combination therapy improves time to progression. J Clin Oncol 2007; 25:3892-901; PMID:17679727; http://dx.doi.org/10.1200/JCO.2006.10.5460
20. Richardson PG, Briemberg H, Jagannath S, Wen PY, Barlogie B, Berenson J, Singhal S, Siegel DS, Irwin D, Schuster M, et al. Frequency, characteristics, and reversibility of peripheral neuropathy during treatment of advanced multiple myeloma with bortezomib. J Clin Oncol 2006; 24:3113-20; PMID:16754936; http://dx.doi.org/10.1200/JCO.2005.04.7779
21. Cavaletti G, Jakubowiak AJ. Peripheral neuropathy during bortezomib treatment of multiple myeloma: a review of recent studies. Leuk Lymphoma 2010; 51:1178-87; PMID:20497001; http://dx.doi.org/10.3109/10428194.2010.483303
22. Corso A, Mangiacavalli S, Varettoni M, Pascutto C, Zappasodi P, Lazzarino M. Bortezomib-induced peripheral neuropathy in multiple myeloma: a comparison between previously treated and untreated patients. Leuk Res 2010; 34:471-4; PMID:19674790; http://dx.doi.org/10.1016/j.leukres.2009.07.022
23. O'Connor OA, Wright J, Moskowitz C, Muzzy J, MacGregor-Cortelli B, Stubblefield M, Straus D, Portlock C, Hamlin P, Choi E, et al. Phase II clinical experience with the novel proteasome inhibitor bortezomib in patients with indolent non-Hodgkin's lymphoma and mantle cell lymphoma. J Clin Oncol 2005; 23:676-84; PMID:15613699; http://dx.doi.org/10.1200/JCO.2005.02.050
24. Oerlemans R, Franke NE, Assaraf YG, Cloos J, van Zantwijk I, Berkers CR, Scheffer GL, Debipersad K, Vojtekova K, Lemos C, et al. Molecular basis of bortezomib resistance: proteasome subunit beta5 (PSMB5) gene mutation and overexpression of PSMB5 protein. Blood 2008; 112:2489-99; PMID:18565852; http://dx.doi.org/10.1182/blood-2007-08-104950
25. Ruschak AM, Slassi M, Kay LE, Schimmer AD. Novel proteasome inhibitors to overcome bortezomib resistance. J Natl Cancer Inst 2011; 103:1007-17; PMID:21606441; http://dx.doi.org/10.1093/jnci/djr160
26. Kuhn DJ, Chen Q, Voorhees PM, Strader JS, Shenk KD, Sun CM, Demo SD, Bennett MK, van Leeuwen FW, Chanan-Khan AA, et al. Potent activity of carfilzomib, a novel, irreversible inhibitor of the ubiquitin-proteasome pathway, against preclinical models of multiple myeloma. Blood 2007; 110:3281-90; PMID:17591945; http://dx.doi.org/10.1182/blood-2007-01-065888
27. Demo SD, Kirk CJ, Aujay MA, Buchholz TJ, Dajee M, Ho MN, Jiang J, Laidig GJ, Lewis ER, Parlati F, et al. Antitumor activity of PR-171, a novel irreversible inhibitor of the proteasome. Cancer Res 2007; 67:6383-91; PMID:17616698; http://dx.doi.org/10.1158/0008-5472.CAN-06-4086
28. O'Connor OA, Stewart AK, Vallone M, Molineaux CJ, Kunkel LA, Gerecitano JF, Orlowski RZ. A phase 1 dose escalation study of the safety and pharmacokinetics of the novel proteasome inhibitor carfilzomib (PR-171) in patients with hematologic malignancies. Clin Cancer Res 2009; 15:7085-91; PMID:19903785; http://dx.doi.org/10.1158/1078-0432.CCR-09-0822
29. Siegel D, Martin T, Nooka A, Harvey RD, Vij R, Niesvizky R, Badros AZ, Jagannath S, McCulloch L, Rajangam K, et al. Integrated safety profile of single-agent carfilzomib: experience from 526 patients enrolled in 4 phase II clinical studies. Haematologica 2013; 98:1753-61; PMID:23935022; http://dx.doi.org/10.3324/haematol.2013.089334
30. Vij R, Siegel DS, Jagannath S, Jakubowiak AJ, Stewart AK, McDonagh K, Bahlis N, Belch A, Kunkel LA, Wear S, et al. An open-label, single-arm, phase 2 study of single-agent carfilzomib in patients with relapsed and/or refractory multiple myeloma who have been previously treated with bortezomib. Br J Haematol 2012; 158:739-48; PMID:22845873; http://dx.doi.org/10.1111/j.1365-2141.2012. 09232.x
31. Siegel DS, Martin T, Wang M, Vij R, Jakubowiak AJ, Lonial S, Trudel S, Kukreti V, Bahlis N, Alsina M, et al. A phase 2 study of single-agent carfilzomib (PX-171-003-A1) in patients with relapsed and refractory multiple myeloma. Blood 2012; 120:2817-25; PMID:22833546; http://dx.doi.org/10.1182/ blood-2012-05-425934
32. Zhou HJ, Aujay MA, Bennett MK, Dajee M, Demo SD, Fang Y, Ho MN, Jiang J, Kirk CJ, Laidig GJ, et al. Design and synthesis of an orally bioavailable and selective peptide epoxyketone proteasome inhibitor (PR-047). J Med Chem 2009; 52:3028-38; PMID:19348473; http://dx.doi.org/10.1021/jm801329v
33. Chauhan D, Singh AV, Aujay M, Kirk CJ, Bandi M, Ciccarelli B, Raje N, Richardson P, Anderson KC. A novel orally active proteasome inhibitor ONX 0912 triggers in vitro and in vivo cytotoxicity in multiple myeloma. Blood 2010; 116:4906-15; PMID:20805366; http://dx.doi.org/10.1182/blood-2010-04-276626
34. Zang Y, Thomas SM, Chan ET, Kirk CJ, Freilino ML, DeLancey HM, Grandis JR, Li C, Johnson DE. Carfilzomib and ONX 0912 inhibit cell survival and tumor growth of head and neck cancer and their activities are enhanced by suppression of Mcl-1 or autophagy. Clin Cancer Res 2012; 18:5639-49; PMID:22929803; http://dx.doi.org/10.1158/1078-0432.CCR-12-1213
35. Yu C, Rahmani M, Conrad D, Subler M, Dent P, Grant S. The proteasome inhibitor bortezomib interacts synergistically with histone deacetylase inhibitors to induce apoptosis in Bcr/Abl+ cells sensitive and resistant to STI571. Blood 2003; 102:3765-74; PMID:12893773; http://dx.doi.org/10.1182/blood- 2003-03-0737
36. Pei XY, Dai Y, Grant S. Synergistic induction of oxidative injury and apoptosis in human multiple myeloma cells by the proteasome inhibitor bortezomib and histone deacetylase inhibitors. Clin Cancer Res 2004; 10:3839-52; PMID:15173093; http://dx.doi.org/10.1158/1078-0432.CCR-03-0561
37. Kim J, Guan J, Chang I, Chen X, Han D, Wang CY. PS-341 and histone deacetylase inhibitor synergistically induce apoptosis in head and neck squamous cell carcinoma cells. Mol Cancer Ther 2010; 9:1977-84; PMID:20571067; http://dx.doi.org/10.1158/1535-7163.MCT-10-0141
38. Dasmahapatra G, Lembersky D, Kramer L, Fisher RI, Friedberg J, Dent P, Grant S. The pan-HDAC inhibitor vorinostat potentiates the activity of the proteasome inhibitor carfilzomib in human DLBCL cells in vitro and in vivo. Blood 2010; 115:4478-87; PMID:20233973; http://dx.doi.org/10.1182/blood-2009-12- 257261
39. Dasmahapatra G, Lembersky D, Son MP, Attkisson E, Dent P, Fisher RI, Friedberg JW, Grant S. Carfilzomib interacts synergistically with histone deacetylase inhibitors in mantle cell lymphoma cells in vitro and in vivo. Mol Cancer Ther 2011; 10:1686-97; PMID:21750224; http://dx.doi.org/10.1158/1535- 7163.MCT-10-1108
40. Stessman HA, Baughn LB, Sarver A, Xia T, Deshpande R, Mansoor A, Walsh SA, Sunderland JJ, Dolloff NG, Linden MA, et al. Profiling bortezomib resistance identifies secondary therapies in a mouse myeloma model. Mol Cancer Ther 2013; 12:1140-50; PMID:23536725; http://dx.doi.org/10.1158/1535-7163.MCT-12-1151
41. Li C, Zang Y, Sen M, Leeman-Neill RJ, Man DS, Grandis JR, Johnson DE. 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; 8:2211-20; PMID:19638453; http://dx.doi.org/ 10.1158/1535-7163.MCT-09-0327
42. Pérez-Galán P, Roué G, Villamor N, Campo E, Colomer D. The BH3-mimetic GX15-070 synergizes with bortezomib in mantle cell lymphoma by enhancing Noxa-mediated activation of Bak. Blood 2007; 109:4441-9; PMID:17227835; http://dx.doi.org/10.1182/blood-2006-07-034173
43. Li C, Johnson DE. Bortezomib induces autophagy in head and neck squamous cell carcinoma cells via JNK activation. Cancer Lett 2012; 314:102-7; PMID:21993018; http://dx.doi.org/10.1016/j.canlet.2011.09.020
44. Kale AJ, Moore BS. Molecular mechanisms of acquired proteasome inhibitor resistance. J Med Chem 2012; 55:10317-27; PMID:22978849; http://dx.doi.org/10. 1021/jm300434z
45. Verbrugge SE, Assaraf YG, Dijkmans BA, Scheffer GL, Al M, den Uyl D, Oerlemans R, Chan ET, Kirk CJ, Peters GJ, et al. Inactivating PSMB5 mutations and P-glycoprotein (multidrug resistance-associated protein/ATP-binding cassette B1) mediate resistance to proteasome inhibitors: ex vivo efficacy of (immuno) proteasome inhibitors in mononuclear blood cells from patients with rheumatoid arthritis. J Pharmacol Exp Ther 2012; 341:174-82; PMID:22235146; http://dx.doi.org/10.1124/jpet.111.187542
46. Ao L, Wu Y, Kim D, Jang ER, Kim K, Lee DM, Kim KB, Lee W. Development of peptide-based reversing agents for p-glycoprotein-mediated resistance to carfilzomib. Mol Pharm 2012; 9:2197-205; PMID:22734651
47. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984; 22:27-55; PMID:6382953; http://dx.doi.org/10.1016/0065-2571(84)90007-4
48. Mehanna H, Paleri V, West CM, Nutting C. Head and neck cancer - Part 1: Epidemiology, presentation, and prevention. BMJ 2010; 341:c4684; PMID:20855405; http://dx.doi.org/10.1136/bmj.c4684
49. Fribley AM, Evenchik B, Zeng Q, Park BK, Guan JY, Zhang H, Hale TJ, Soengas MS, Kaufman RJ, Wang CY. Proteasome inhibitor PS-341 induces apoptosis in cisplatin-resistant squamous cell carcinoma cells by induction of Noxa. J Biol Chem 2006; 281:31440-7; PMID:16928686; http://dx.doi.org/10.1074/jbc. M604356200