17-allylamino-17-demethoxygeldanamycin and MEK1/2 inhibitors kill GI tumor cells via Ca2+-dependent suppression of GRP78/BiP and induction of ceramide and reactive oxygen species

Molecular Cancer Therapeutics

Volumn 9, Issue 5, 2010, Pages 1378-1395

  Walker, Teneille ^a   Mitchell, Clint ^a   Park, Margaret A ^a   Yacoub, Adly ^a   Rahmani, Mohamed ^b   Häussinger, Dieter ^d   Reinehr, Roland ^d   Voelkel Johnson, Christina ^c   Fisher, Paul B ^a,b   Grant, Steven ^a,b   Dent, Paul ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 CHLORO 4 IODOANILINO) N CYCLOPROPYLMETHOXY 3,4 DIFLUOROBENZAMIDE; CALCIUM; CASPASE 9; CERAMIDE; CERAMIDE SYNTHASE 6; FAS ANTIGEN; FLICE INHIBITORY PROTEIN; GLUCOSE REGULATED PROTEIN 78; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PROTEIN BCL XL; REACTIVE OXYGEN METABOLITE; SPHINGOSINE ACYLTRANSFERASE; TANESPIMYCIN; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM CELL LEVEL; CELL KILLING; CONTROLLED STUDY; CYTOSOL; ENZYME INHIBITION; GASTROINTESTINAL TUMOR; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BENZOQUINONES; CALCIUM; CARCINOMA; CERAMIDES; DOWN-REGULATION; DRUG EVALUATION, PRECLINICAL; DRUG INTERACTIONS; GASTROINTESTINAL NEOPLASMS; HCT116 CELLS; HEAT-SHOCK PROTEINS; HEP G2 CELLS; HUMANS; LACTAMS, MACROCYCLIC; MAP KINASE KINASE 1; MAP KINASE KINASE 2; PROTEIN KINASE INHIBITORS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 77952135961     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-09-1131     Document Type: Article

References (53)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005;55:74-108.
2. Bardeesy N, DePinho RA. Pancreatic cancer biology and genetics. Nat Rev Cancer 2002;2:897-909.
3. Dent P. MAP kinase pathways in the control of hepatocyte growth, metabolism and survival. In: Dufour JFP, Clavien A, editors. Signaling Pathways in Liver Diseases. Springer Press; 2005. p. 223-238
4. Dent P, Yacoub A, Fisher PB, Hagan MP, Grant S. MAPK pathways in radiation responses. Oncogene 2003;22:5885-5896
5. Valerie K, Yacoub A, Hagan MP, et al. Radiation-induced cell signaling: inside-out and outside-in. Mol Cancer Ther 2007;6:789-801. (Pubitemid 46554549)
6. Hamad NM, Elconin JH, Karnoub AE, et al. Distinct requirements for Ras oncogenesis in human versus mouse cells. Genes Dev 2002;16:2045-2057
7. Katz ME, McCormick F. Signal transduction from multiple Ras effectors. Curr Opin Genet Dev 1997;7:75-79 (Pubitemid 27092767)
8. Mori M, Uchida M, Watanabe T, et al. Activation of extracellular signal-regulated kinases ERK1 and ERK2 induces Bcl-xL up-regulation via inhibition of caspase activities in erythropoietin signaling. J Cell Physiol 2003;195:290-297 (Pubitemid 36384302)
9. Ley R, Balmanno K, Hadfield K, Weston C, Cook SJ. Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein, Bim. J Biol Chem 2003;278:18811-18816 (Pubitemid 36799262)
10. Wang YF, Jiang CC, Kiejda KA, Gillespie S, Zhang XD, Hersey P. Apoptosis induction in human melanoma cells by inhibition of MEK is caspase-independent and mediated by the Bcl-2 family members PUMA, Bim, and Mcl-1. Clin Cancer Res 2007;13:4934-4942 (Pubitemid 47294802)
11. Qiao L, Han SI, Fang Y, et al. Bile acid regulation of C/EBP β, CREB, c-Jun function, via the extracellular signal-regulated kinase and c-Jun NH2-terminal kinase pathways, modulates the apoptotic response of hepatocytes. Mol Cell Biol 2003;23:3052-3066
12. Li N, Batt D, Warmuth M. B-Raf kinase inhibitors for cancer treatment. Curr Opin Investig Drugs 2007;8:452-456 (Pubitemid 46868066)
13. Davies BR, Logie A, McKay JS, et al. AZD6244 (ARRY-142886), a potent inhibitor of mitogen-activated protein kinase/extracellular signal-regulated kinase kinase 1/2 kinases: mechanism of action in vivo, pharmacokinetic/ pharmacodynamic relationship, and potential for combination in preclinical models. Mol Cancer Ther 2007;6:2209-2219 (Pubitemid 47294749)
14. Bagatell R, Whitesell L. Altered Hsp90 function in cancer: a unique therapeutic opportunity. Mol Cancer Ther 2004;3:1021-1030 (Pubitemid 39199597)
15. Neckers L, Neckers K. Heat-shock protein 90 inhibitors as novel cancer chemotherapeutic agents. Expert Opin Emerg Drugs 2002;7:277-288 (Pubitemid 35291458)
16. DeBoer C, Meulman PA, Wnuk RJ, Peterson DH. Geldanamycin, a new antibiotic. J Antibiot (Tokyo) 1970;23:442-447
17. Isaacs JS, Xu W, Neckers L. Heat shock protein 90 as a molecular target for cancer therapeutics. Cancer Cell 2003;3:213-217 (Pubitemid 37443877)
18. Nimmanapalli R, O'Bryan E, Kuhn D, Yamaguchi H, Wang HG, Bhalla KN. Regulation of 17-AAG-induced apoptosis: role of Bcl-2, Bcl-XL, Bax downstream of 17-AAG-mediated down-regulation of Akt, Raf-1, and Src kinases. Blood 2003;102:269-275 (Pubitemid 36759664)
19. Stancato LF, Silverstein AM, Owens-Grillo JK, Chow YH, Jove R, Pratt WB. The hsp90-binding antibiotic geldanamycin decreases Raf levels and epidermal growth factor signaling without disrupting formation of signaling complexes or reducing the specific enzymatic activity of Raf kinase. J Biol Chem 1997;272:4013-4020 (Pubitemid 27078462)
20. Nimmanapalli R, O'Bryan E, Bhalla K. Geldanamycin and its analogue 17-allylamino-17-demethoxygeldanamycin lowers Bcr-Abl levels and induces apoptosis and differentiation of Bcr-Abl-positive human leukemic blasts. Cancer Res 2001;61:1799-1804 (Pubitemid 32691987)
21. RamanathanRK, TrumpDL, Eiseman JL, et al. Phase I pharmacokinetic- pharmacodynamic study of 17-(allylamino)-17-demethoxygeldanamycin (17AAG, NSC 330507), a novel inhibitor of heat shock protein 90, in patients with refractory advanced cancers. Clin Cancer Res 2005;11:3385-3391
22. Lane D, Robert V, Grondin R, Rancourt C, Piche A. Malignant ascites protect against TRAIL-induced apoptosis by activating the PI3K/Akt pathway in human ovarian carcinoma cells. Int J Cancer 2007;121:1227-1237 (Pubitemid 47293789)
23. Georgakis GV, Li Y, Rassidakis GZ, Martinez-Valdez H, Medeiros LJ, Younes A. Inhibition of heat shock protein 90 function by 17-allylamino-17-demethoxy- geldanamycin in Hodgkin's lymphoma cells down-regulates Akt kinase, dephosphorylates extracellular signal-regulated kinase, and induces cell cycle arrest and cell death. Clin Cancer Res 2006;12:584-590
24. Powers MV, Clarke PA, Workman P. Dual targeting of HSC70 and HSP72 inhibits HSP90 function and induces tumor-specific apoptosis. Cancer Cell 2008;14:250-262
25. Grem JL, Morrison G, Guo XD, et al. Phase I and pharmacologic study of 17-(allylamino)-17-demethoxygeldanamycin in adult patients with solid tumors. J Clin Oncol 2005;23:1885-1893.
26. Banerji U, O'Donnell A, Scurr M, et al. Phase I pharmacokinetic and pharmacodynamic study of 17-allylamino, 17-demethoxygeldanamycin in patients with advancedmalignancies. J Clin Oncol 2005;23:4152-4161
27. Park MA, Zhang G, Mitchell C, et al. Mitogen-activated protein kinase kinase 1/2 inhibitors and 17-allylamino-17-demethoxygeldanamycin synergize to kill human gastrointestinal tumor cells in vitro via suppression of c-FLIP-s levels and activation of CD95. Mol Cancer Ther 2008;7:2633-2648
28. Engelman JA, Chen L, Tan X, et al. Effective use of PI3K and MEK inhibitors to treat mutant K ras G12D and PIK3CA H1047R murine lung cancers. Nat Med 2008;14:1351-1356
29. Zhang G, Park M, Mitchell C, et al. Vorinostat and sorafenib synergistically kill tumor cells via FLIP suppression and CD95 activation. Clin Cancer Res 2008;14:5385-5399
30. Park MA, Zhang G, Martin AP, et al. Vorinostat and sorafenib increase ER stress, autophagy and apoptosis via ceramide-dependent CD95 and PERK activation. Cancer Biol Ther 2008;7:135-149
31. Park MA, Yacoub A, Rahmani M, et al. OSU-03012 stimulates PERK-dependent increases in HSP70 expression, attenuating its lethal actions in transformed cells. Mol Pharm 2008;73:1168-1184
32. Mitchell C, Park MA, Zhang G, et al. 17-Allylamino-17-demethoxy- geldanamycin enhances the lethality of deoxycholic acid in primary rodent hepatocytes and established cell lines. Mol Cancer Ther 2007;6:618-632
33. White-Gilbertson S, Mullen T, Senkal C, Lu P, Ogretmen B, Obeid L, Voelkel-Johnson C. Ceramide synthase 6 modulates TRAIL sensitivity and nuclear translocation of active caspase-3 in colon cancer cells. Oncogene 2009. [Epub ahead of print].
34. Martin AP, Miller A, Emad L, et al. Lapatinib resistance in HCT116 cells is mediated by elevated MCL-1 expression and decreased BAK activation and not by ERBB receptor kinase mutation. Mol Pharmacol 2008;74:807-822
35. Ihle N, Lemos R, Wipf P, et al. Activating PI-3-kinase mutation confers sensitivity, while oncogenic Ras mutation confers resistance to PI-3-kinase inhibition. Cancer Res 2008;69:143-150
36. Carpinteiro A, Dumitru C, Schenck M, Gulbins E. Ceramide-induced cell death in malignant cells. Cancer Lett 2008;264:1-10.
37. Fang Y, Han SI, Mitchell C, et al. Bile acids induce mitochondrial ROS, which promote activation of receptor tyrosine kinases and signaling pathways in rat hepatocytes. Hepatology 2004;40:961-971
38. Reinehr R, Sommerfeld A, Häussinger D. CD95 ligand is a proliferative and anti-apoptotic signal in quiescent hepatic stellate cells. Gastroenterology 2008;134:1494-1506
39. Reinehr R, Becker S, Eberle A, Grether-Beck S, Häussinger D. Involvement of NADPH oxidase isoforms and Src family kinases in CD95-dependent hepatocyte apoptosis. J Biol Chem 2005;280:27179-27194
40. Rodriguez-Viciana P, McCormick F. RalGDS comes of age. Cancer Cell 2005;7:205-206
41. Heigold S, Sers C, Bechtel W, Ivanovas B, Schäfer R, Bauer G. Nitric oxide mediates apoptosis induction selectively in transformed fibroblasts compared to nontransformed fibroblasts. Carcinogenesis 2002;23:929-941
42. Wang Y, Singh R, Massey AC, et al. Loss of macroautophagy promotes or prevents fibroblast apoptosis depending on the death stimulus. J Biol Chem 2008;283:4766-4777
43. Han J, Hou W, Goldstein LA, et al. Involvement of protective autophagy in TRAIL resistance of apoptosis-defective tumor cells. J Biol Chem 2008;283:19665-19677
44. Jin J, Hou Q, Mullen TD, et al. Ceramide generated by sphingomyelin hydrolysis and the salvage pathway is involved in hypoxia/reoxygenation-induced Bax redistribution to mitochondria in NT-2 cells. J Biol Chem 2008;283:26509-26517
45. Novgorodov SA, Gudz TI, Obeid LM. Long-chain ceramide is a potent inhibitor of the mitochondrial permeability transition pore. J Biol Chem 2008;283:24707-24717
46. Yan Y, Wei CL, Zhang WR, Cheng HP, Liu J. Cross-talk between calcium and reactive oxygen species signaling. Acta Pharmacol Sin 2006;27:821-826
47. Rao RV, Hermel E, Castro-Obregon S, et al. Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation. J Biol Chem 2001;276:33869-33874
48. Fu Y, Li J, Lee AS. GRP78/BiP inhibits endoplasmic reticulum BIK and protects human breast cancer cells against estrogen starvation-induced apoptosis. Cancer Res 2007;67:3734-3740
49. Fernandez PM, Tabbara SO, Jacobs LK, et al. Overexpression of the glucose-regulated stress gene GRP78 in malignant but not benign human breast lesions. Breast Cancer Res Treat 2000;59:15-26.
50. Lee E, Nichols P, Spicer D, Groshen S, Yu MC, Lee AS. GRP78 as a novel predictor of responsiveness to chemotherapy in breast cancer. Cancer Res 2006;66:7849-7853
51. Pootrakul L, Datar RH, Shi SR, et al. Expression of stress response protein Grp78 is associated with the development of castration-resistant prostate cancer. Clin Cancer Res 2006;12:5987-5993
52. Daneshmand S, Quek ML, Lin E, et al. Glucose-regulated protein GRP78 is up-regulated in prostate cancer and correlates with recurrence and survival. Hum Pathol 2007;38:1547-1552
53. Powers MV, Workman P. Targeting of multiple signalling pathways by heat shock protein 90 molecular chaperone inhibitors. Endocr Relat Cancer 2006;13 S1:S125-35.