Diltiazem enhances the apoptotic effects of proteasome inhibitors to induce prostate cancer cell death

Journal of Pharmacology and Experimental Therapeutics

Volumn 341, Issue 3, 2012, Pages 646-655

  Kaddour Djebbar, Ismail ^a,b   Choudhary, Vivek ^a,b   Lakshmikanthan, Vijayabaskar ^a,b,d   Shirley, Robert ^a,b   El Gaish, Manal ^a   Al Shabrawey, Mohamed ^b   Al Husein, Belal ^a,c   Zhong, Roger ^a   Davis, Michael ^a   Dong, Zheng ^a,b   Bollag, Wendy B ^a,b   Kumar, M Vijay ^a,b,e  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

^d UNIVERSITY OF LOUISIANA   (United States)

^e VA WESTERN NEW YORK HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BORTEZOMIB; DILTIAZEM; GLUCOSE REGULATED PROTEIN 78; LACTACYSTIN; PEPTIDES AND PROTEINS; PROTEASOME INHIBITOR; PROTEIN BAK; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BIK; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CANCER CELL; CELL FUNCTION; CELL STRAIN LNCAP; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE RESPONSE; DRUG APPROVAL; DRUG POTENTIATION; ENDOPLASMIC RETICULUM STRESS; INTRACELLULAR SIGNALING; MITOCHONDRION; MONOTHERAPY; MULTIPLE MYELOMA; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN FUNCTION; PROTEIN SECRETION; UPREGULATION;

ACETYLCYSTEINE; APOPTOSIS; BLOTTING, WESTERN; BORONIC ACIDS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CLINICAL TRIALS AS TOPIC; DILTIAZEM; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; DRUG SYNERGISM; HUMANS; MALE; PROSTATIC NEOPLASMS; PROTEASE INHIBITORS; PYRAZINES; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 84861537604     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.111.188151     Document Type: Article

References (41)

1. Autret A and Martin SJ (2009) Emerging role for members of the Bcl-2 family in mitochondrial morphogenesis. Mol Cell 36:355-363.
2. Bae VL, Jackson-Cook CK, Brothman AR, Maygarden SJ, and Ware JL (1994) Tumorigenicity of SV40 T antigen immortalized human prostate epithelial cells: association with decreased epidermal growth factor receptor (EGFR) expression. Int J Cancer 58:721-729. (Pubitemid 24279437)
3. Bakhshi J, Weinstein L, Poksay KS, Nishinaga B, Bredesen DE, and Rao RV (2008) Coupling endoplasmic reticulum stress to the cell death program in mouse melanoma cells: effect of curcumin. Apoptosis 13:904-914.
4. Cornwell MM, Pastan I, and Gottesman MM (1987) Certain calcium channel blockers bind specifically to multidrug-resistant human KB carcinoma membrane vesicles and inhibit drug binding to P-glycoprotein. J Biol Chem 262:2166-2170. (Pubitemid 17102655)
5. Choudhary V, Kaddour-Djebbar I, Lakshmikanthan V, Ghazaly T, Thangjam GS, Sreekumar A, Lewis RW, Mills IG, Bollag WB, and Kumar MV (2011) Novel role of androgens in mitochondrial fission and apoptosis. Mol Cancer Res 9:1067-1077.
6. Cummings J, Hodgkinson C, Odedra R, Sini P, Heaton SP, Mundt KE, Ward TH, Wilkinson RW, Growcott J, Hughes A, et al. (2008) Preclinical evaluation of M30 and M65 ELISAs as biomarkers of drug induced tumor cell death and antitumor activity. Mol Cancer Ther 7:455-463. (Pubitemid 351482128)
7. Debes JD, Roberts RO, Jacobson DJ, Girman CJ, Lieber MM, Tindall DJ, and Jacobsen SJ (2004) Inverse association between prostate cancer and the use of calcium channel blockers. Cancer Epidemiol Biomarkers Prev 13:255-259. (Pubitemid 38222557)
8. Egger L, Madden DT, Rhême C, Rao RV, and Bredesen DE (2007) Endoplasmic reticulum stress-induced cell death mediated by the proteasome. Cell Death Differ 14:1172-1180. (Pubitemid 46785108)
9. Ferreiro E, Oliveira CR, and Pereira CM (2008) The release of calcium from the endoplasmic reticulum induced by amyloid-β and prion peptides activates the mitochondrial apoptotic pathway. Neurobiol Dis 30:331-342.
10. Fribley A, Zeng Q, and Wang CY (2004) 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 24:9695-9704. (Pubitemid 39458799)
11. Ghosh TK, Bian JH, Short AD, Rybak SL, and Gill DL (1991) Persistent intracellular calcium pool depletion by thapsigargin and its influence on cell growth. J Biol Chem 266:24690-24697. (Pubitemid 21908997)
12. Gill DL, Waldron RT, Rys-Sikora KE, Ufret-Vincenty CA, Graber MN, Favre CJ, and Alfonso A (1996) Calcium pools, calcium entry, and cell growth. Biosci Rep 16: 139-157. (Pubitemid 26199713)
13. Goldberg AL and Rock K (2002) Not just research tools-proteasome inhibitors offer therapeutic promise. Nat Med 8:338-340. (Pubitemid 34407027)
14. Greystoke A, Cummings J, Ward T, Simpson K, Renehan A, Butt F, Moore D, Gietema J, Blackhall F, Ranson M, et al. (2008) Optimisation of circulating biomarkers of cell death for routine clinical use. Ann Oncol 19:990-995. (Pubitemid 351627319)
15. Hom JR, Gewandter JS, Michael L, Sheu SS, and Yoon Y (2007) Thapsigargin induces biphasic fragmentation of mitochondria through calcium-mediated mitochondrial fission and apoptosis. J Cell Physiol 212:498-508. (Pubitemid 47025640)
16. Jambrina E, Alonso R, Alcalde M, del Carmen Rodríguez M, Serrano A, Martínez-A C, García-Sancho J, and Izquierdo M (2003) Calcium influx through receptoroperated channel induces mitochondria-triggered paraptotic cell death. J Biol Chem 278:14134-14145. (Pubitemid 36799960)
17. Kaddour-Djebbar I, Choudhary V, Brooks C, Ghazaly T, Lakshmikanthan V, Dong Z, and Kumar MV (2010) Specific mitochondrial calcium overload induces mitochondrial fission in prostate cancer cells. Int J Oncol 36:1437-1444.
18. Kaddour-Djebbar I, Lakshmikanthan V, Shirley RB, Ma Y, Lewis RW, and Kumar MV (2006) Therapeutic advantage of combining calcium channel blockers and TRAIL in prostate cancer. Mol Cancer Ther 5:1958-1966. (Pubitemid 44336567)
19. Lakshmikanthan V, Kaddour-Djebbar I, Lewis RW, and Kumar MV (2006) SAHA-sensitized prostate cancer cells to TNFα-related apoptosis-inducing ligand (TRAIL): mechanisms leading to synergistic apoptosis. Int J Cancer 119:221-228.
20. 2+ is a critical determinant of Velcade (PS-341/bortezomib) cytotoxicity in myeloma cell lines. Cancer Res 65:3828-3836.
21. Li J, Lee B, and Lee AS (2006) Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J Biol Chem 281:7260-7270. (Pubitemid 43847494)
22. Lomonosova E, Ryerse J, and Chinnadurai G (2009) BAX/BAK-independent mitoptosis during cell death induced by proteasome inhibition? Mol Cancer Res 7:1268-1284.
23. Madeo F and Kroemer G (2009) Intricate links between ER stress and apoptosis. Mol Cell 33:669-670.
24. Mattson MP and Chan SL (2003) Calcium orchestrates apoptosis. Nat Cell Biol 5:1041-1043. (Pubitemid 37509106)
25. Meister S, Frey B, Lang VR, Gaipl US, Schett G, Schlötzer-Schrehardt U, and Voll RE (2010) Calcium channel blocker verapamil enhances endoplasmic reticulum stress and cell death induced by proteasome inhibition in myeloma cells. Neoplasia 12:550-561.
26. Mussche S, Leybaert L, and D'Herde K (2000) First and second messenger role of calcium. Survival versus apoptosis in serum-free cultured granulosa explants. Ann NY Acad Sci 926:101-115. (Pubitemid 32050147)
27. Nikrad M, Johnson T, Puthalalath H, Coultas L, Adams J, and Kraft AS (2005) The proteasome inhibitor bortezomib sensitizes cells to killing by death receptor ligand TRAIL via BH3-only proteins Bik and Bim. Mol Cancer Ther 4:443-449. (Pubitemid 40443929)
28. Olsen JH, Sørensen HT, Friis S, McLaughlin JK, Steffensen FH, Nielsen GL, Andersen M, Fraumeni JF Jr, and Olsen J (1997) Cancer risk in users of calcium channel blockers. Hypertension 29:1091-1094. (Pubitemid 27198215)
29. Papandreou CN, Daliani DD, Nix D, Yang H, Madden T, Wang X, Pien CS, Millikan RE, Tu SM, Pagliaro L, et al. (2004) Phase I trial of the proteasome inhibitor bortezomib in patients with advanced solid tumors with observations in androgenindependent prostate cancer. J Clin Oncol 22:2108-2121. (Pubitemid 41095144)
30. Papandreou CN and Logothetis CJ (2004) Bortezomib as a potential treatment for prostate cancer. Cancer Res 64:5036-5043. (Pubitemid 39006513)
31. Paschen W, Hotop S, and Aufenberg C (2003) Loading neurons with BAPTA-AM activates xbp1 processing indicative of induction of endoplasmic reticulum stress. Cell Calcium 33:83-89. (Pubitemid 36221692)
32. Puthalakath H, O'Reilly LA, Gunn P, Lee L, Kelly PN, Huntington ND, Hughes PD, Michalak EM, McKimm-Breschkin J, Motoyama N, et al. (2007) ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129:1337-1349. (Pubitemid 46962086)
33. 2+ for cancer cell proliferation and survival. Nat Rev Cancer 8:361-375.
34. Rodriguez C, Jacobs EJ, Deka A, Patel AV, Bain EB, Thun MJ, and Calle EE (2009) Use of blood-pressure-lowering medication and risk of prostate cancer in the Cancer Prevention Study II Nutrition Cohort. Cancer Causes Control 20:671-679.
35. Sareen D, Darjatmoko SR, Albert DM, and Polans AS (2007) Mitochondria, calcium, and calpain are key mediators of resveratrol-induced apoptosis in breast cancer. Mol Pharmacol 72:1466-1475. (Pubitemid 350146084)
36. Scorrano L and Korsmeyer SJ (2003) Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem Biophys Res Commun 304:437-444. (Pubitemid 36506515)
37. Shirley RB, Kaddour-Djebbar I, Patel DM, Lakshmikanthan V, Lewis RW, and Kumar MV (2005) Combination of proteasomal inhibitors lactacystin and MG132 induced synergistic apoptosis in prostate cancer cells. Neoplasia 7:1104-1111. (Pubitemid 44430989)
38. 2+ depletion suppresses protein synthesis and induces activation-enhanced cell death in mast cells. J Biol Chem 277:13812-13820.
39. 2+ in the cytosol. Biochem J 344 (Pt 1):39-46.
40. Tagliarino C, Pink JJ, Dubyak GR, Nieminen AL, and Boothman DA (2001) Calcium is a key signaling molecule in β-lapachone-mediated cell death. J Biol Chem 276:19150-19159.
41. Yoshinaga A, Hayashi T, Yoshida S, Ohno R, Ishii N, Terao T, Watanabe T, and Yamada T (2006) [Comparison and outcome of prevalence of concurrent diseases in patients with urological malignant diseases]. Hinyokika Kiyo 52:537-541.