Myc regulates aggresome formation, the induction of Noxa, and apoptosis in response to the combination of bortezomib and SAHA

Blood

Volumn 112, Issue 7, 2008, Pages 2917-2926

  Nawrocki, Steffan T ^a   Carew, Jennifer S ^a   Maclean, Kirsteen H ^b   Courage, James F ^a   Huang, Peng ^c   Houghton, Janet A ^d   Cleveland, John L ^e   Giles, Francis J ^a   McConkey, David J ^c  

^a CTRC Institute for Drug Development   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c UNIVERSITY OF TEXAS   (United States)

^d LERNER RESEARCH INSTITUTE   (United States)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BORTEZOMIB; CALCIUM; CASPASE 4; CYCLOHEXIMIDE; HISTONE DEACETYLASE 6; MYC PROTEIN; PROTEIN NOXA; SMALL INTERFERING RNA; VORINOSTAT; BORONIC ACID DERIVATIVE; HDAC6 PROTEIN, HUMAN; HISTONE DEACETYLASE; HYDROXAMIC ACID; PMAIP1 PROTEIN, HUMAN; PROTEIN BCL 2; PYRAZINE DERIVATIVE;

AGGRESOME; APOPTOSIS; ARTICLE; CALCIUM HOMEOSTASIS; CONTROLLED STUDY; DIPLOIDY; DRUG SENSITIVITY; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; FIBROBLAST; HUMAN; HUMAN CELL; MULTIPLE MYELOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; STRESS; CELL NUCLEUS; DRUG EFFECT; DRUG POTENTIATION; METABOLISM; PATHOLOGY; TUMOR CELL LINE; ULTRASTRUCTURE;

APOPTOSIS; BORONIC ACIDS; CELL LINE, TUMOR; CELL NUCLEUS STRUCTURES; CYCLOHEXIMIDE; DIPLOIDY; DRUG SYNERGISM; ENDOPLASMIC RETICULUM; FIBROBLASTS; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; MULTIPLE MYELOMA; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-MYC; PYRAZINES; RNA, SMALL INTERFERING;

EID: 53049110009     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-12-130823     Document Type: Article

References (42)

1. Adams J. The proteasome: a suitable antineoplastic target. Nat Rev Cancer. 2004;4:349-360.
2. Lashinger LM, Zhu K, Williams SA, Shrader M, Dinney GP. McConkey DJ. 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.
3. Nawrocki ST. Bruns CJ, Harbison MT, et al. Effects of the proteasome inhibitor PS-341 on apoptosis and angiogenesis in orthotopic human pancreatic tumor xenografts. Mol CancerTher. 2002;1:1243-1253.
4. Pérez-Galán P. Roue 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.
5. Qin JZ, Ziffra J, Stennett L. et al. Proteasome inhibitors trigger NOXA-mediated apoptosis in melanoma and myeloma cells. Cancer Res. 2005;65:6282-6293.
6. Williams S, Pettaway C, Song R, Papandreou C, Logothetis C. McConkey DJ. Differential effects of the proteasome inhibitor bortezomib on apoptosis and angiogenesis in human prostate tumor xenografts. Mol Cancer Ther. 2003;2:835-843.
7. Carew JS, Giles FJ, Nawrocki ST. Histone deacetylase inhibitors: Mechanisms of cell death and promise in combination cancer therapy. Cancer Lett. 2008;269:7-17.
8. Mitsiades CS, Mitsiades NS, McMullan CJ, et al. Transcriptional signature of histone deacetylase inhibition in multiple myeloma: biological and clinical implications. Proc Natl Acad Sci U S A. 2004:101:540-545.
9. Nawrocki ST, Carew JS, Douglas L, Cleveland JL, Humphreys R, Houghton JA. Histone deacetylase inhibitors enhance lexatumumabinduced apoptosis via a p21 Cip1-dependent decrease in survivin levels. Cancer Res. 2007;67: 6987-6994.
10. Nawrocki ST, Carew JS, Pino MS, et al. Aggresome disruption: a novel strategy to enhance bortezomib-induced apoptosis in pancreatic cancer cells. Cancer Res. 2006;66:3773-3781.
11. Nawrocki ST, Carew JS, Pino MS, et al. Bortezomib sensitizes pancreatic cancer cells to endoplasmic reticulum stress-mediated apoptosis. Cancer Res. 2005;65:11658-11666.
12. Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A, Yao TP. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell. 2003; 115:727-738.
13. Adachi M. Zhang Y, Zhao X. et al. Synergistic effect of histone deacetylase inhibitors FK228 and m-carboxycinnamic acid bis-hydroxamide with proteasome inhibitors PSI and PS-341 against gastrointestinal adenocarcinoma cells. Clin Cancer Res. 2004;10:3853-3862.
14. Drexler HC, Euler M. Synergistic apoptosis induction by proteasome and histone deacetylase inhibitors is dependent on protein synthesis. Apoptosis. 2005;10:743-758.
15. 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;10:3839-3852.
16. 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; 102:3765-3774.
17. Nawrocki ST. Carew JS, Dunner K Jr. et al. 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.
18. Nilsson JA, Cleveland JL. Myc pathways provoking cell suicide and cancer. Oncogene. 2003;22: 9007-9021.
19. Schmidt EV. The role of c-myc in regulation of translation initiation. Oncogene. 2004;23:3217-3221.
20. Littlewood TD, Hancock DC, Danielian PS, Parker MG, Evan Gl. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 1995;23:1686-1690.
21. Maclean KH, Keller UB, Rodriguez-Galindo C, Nilsson JA, Cleveland JL. c-Myc augments gamma irradiation-induced apoptosis by suppressing Bcl-XL. Mol Cell Biol. 2003;23:7256-7270.
22. Carew JS, Nawrocki ST, Krupnik YV, et al. Targeting endoplasmic reticulum protein transport: a novel strategy to kill malignant B cells and overcome fludarabine resistance in CLL. Blood. 2006; 107:222-231.
23. Carew JS, Nawrocki ST. Kahue CN, et al. Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHA to overcome Bcr-Abl-mediated drug resistance. Blood. 2007;110:313-322.
24. Hideshima T, Bradner JE. Wong J, et al. Smallmolecule inhibition of proteasome and aggresome function induces synergistic antitumor activity in multiple myeloma. Proc Natl Acad Sci U S A. 2005;102:8567-8572.
25. Li Z, Van Calcar S, Qu C, Cavenee WK. Zhang MQ, Ren B. A global transcriptional regulatory role for c-Myc in Burkitt's lymphoma cells. Proc Natl Acad Sci U S A. 2003; 100:8164-8169.
26. Jones RM, Branda J, Johnston KA, et al. An essential E box in the promoter of the gene encoding the mRNA cap-binding protein (eukaryotic initiation factor 4E) is a target for activation by c-myc. Mol Cell Biol. 1996;16:4754-4764.
27. LandowskiTH, Megli CJ, Nullmeyer KD, Lynch RM, Dorr RT. Mitochondrial-mediated disregulation of Ca2+ is a critical determinant of Velcade (PS-341/bortezomib) cytotoxicity in myeloma cell lines. Cancer Res. 2005;65:3828-3836.
28. Lee AH, Iwakoshi NN, Anderson KC, Glimcher LH. Proteasome inhibitors disrupt the unfolded protein response in myeloma cells. Proc Natl Acad Sci U S A. 2003;100:9946-9951.
29. Obeng EA, Carlson LM, Gutman DM, Harrington WJ Jr, Lee KP, Boise LH. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood. 2006;107:4907-4916.
30. Nowis D, McConnell EJ, Dierlam L, Palamarchuk A, Lass A, Wojcik C. TNF potentiates anticancer activity of bortezomib (Velcade) through reduced expression of proteasome subunits and dysregulation of unfolded protein response. Int J Cancer. 2007;121:431-441.
31. Fernandez Y, Verhaegen M, Miller TP, et al. Differential regulation of noxa in normal melanocytes and melanoma cells by proteasome inhibition: therapeutic implications. Cancer Res. 2005; 65:6294-6304.
32. Fribley AM, Evenchik B, Zeng Q, et al. Proteasome inhibitor PS-341 induces apoptosis in cisplatin-resistant squamous cell carcinoma cells by induction of Noxa. J Biol Chem. 2006;281:31440-31447.
33. Qin JZ, Xin H, Sitailo LA, Denning MF, Nickoloff BJ. Enhanced killing of melanoma cells by simultaneously targeting Mcl-1 and NOXA. Cancer Res. 2006;66:9636-9645.
34. Iritani BM, Eisenman RN. c-Myc enhances protein synthesis and cell size during B lymphocyte development. Proc Natl Acad Sci U SA. 1999;96: 13180-13185.
35. Schmidt EV. The role of c-myc in cellular growth control. Oncogene. 1999;18:2988-2996.
36. Orlowski RZ, Eswara JR, Lafond-Walker A, Grever MR, Orlowski M, Dang CV. Tumor growth inhibition induced in a murine model of human Burkitt's lymphoma by a proteasome inhibitor. Cancer Res. 1998;58:4342-4348.
37. Hitomi J, KatayamaT, Eguchi Y, et al. Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Abeta-induced cell death. J Cell Biol. 2004;165:347-356.
38. Nikiforov MA, Riblett M, Tang WH, et al. Tumor cell-selective regulation of NOXA by c-MYC in response to proteasome inhibition. Proc Natl Acad Sci U S A. 2007;104:19488-19493.
39. Li J, Lee B, Lee AS. Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J Biol Chem. 2006;281:7260-7270.
40. Meister S, Schubert U, Neubert K, et al. Extensive immunoglobulin production sensitizes myeloma cells for proteasome inhibition. Cancer Res. 2007;67:1783-1792.
41. Avet-Loiseau H, Gerson F, Magrangeas F. Minvielle S, Harousseau JL, Bataille R. Rearrangements of the c-myc oncogene are present in 15% of primary human multiple myeloma tumors. Blood. 2001;98:3082-3086.
42. Shou Y, Martelli ML, Gabrea A, et al. Diverse karyotypic abnormalities of the c-myc locus associated with c-myc dysregulation and tumor progression in multiple myeloma. Proc Natl Acad Sci U S A. 2000;97:228-233.