Sorafenib Sensitizes Glioma Cells to the BH3 Mimetic ABT-737 by Targeting MCL1 in a STAT3-Dependent Manner

Neoplasia (United States)

Volumn 17, Issue 7, 2015, Pages 564-573

  Kiprianova, Irina ^a   Remy, Janina ^a   Milosch, Nelli ^a   Mohrenz, Isabelle V ^a   Seifert, Volker ^a   Aigner, Achim ^b   Kögel, Donat ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

3 (6 BROMO 2 PYRIDINYL) 2 CYANO N (1 PHENYLETHYL)ACRYLAMIDE; 4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; ACTIVATING TRANSCRIPTION FACTOR; ACTIVATING TRANSCRIPTION FACTOR 5; CASPASE 3; EFFECTOR CASPASE; LENTIVIRUS VECTOR; PROTEIN BAX; PROTEIN BCL 2; PROTEIN MCL 1; SORAFENIB; STAT3 PROTEIN; UNCLASSIFIED DRUG; ABT-737; ANTINEOPLASTIC AGENT; ATF5 PROTEIN, HUMAN; BIPHENYL DERIVATIVE; CARBANILAMIDE DERIVATIVE; CYTOCHROME C; DEVDASE; MCL1 PROTEIN, HUMAN; NICOTINAMIDE; NITROPHENOL; PEPTIDE HYDROLASE; PIPERAZINE DERIVATIVE; PROTEIN KINASE INHIBITOR; PYRIDINE DERIVATIVE; STAT3 PROTEIN, HUMAN; SULFONAMIDE; TYRPHOSTIN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG SENSITIZATION; ENZYME ACTIVITY; GENE SILENCING; GENETIC TRANSCRIPTION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; GENETICS; GLIOMA; METABOLISM; PATHOLOGY; SECRETION (PROCESS); TUMOR CELL LINE;

ACTIVATING TRANSCRIPTION FACTORS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BIPHENYL COMPOUNDS; CELL LINE, TUMOR; CELL SURVIVAL; CYTOCHROMES C; GENE KNOCKDOWN TECHNIQUES; GLIOMA; HUMANS; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; NIACINAMIDE; NITROPHENOLS; PEPTIDE HYDROLASES; PHENYLUREA COMPOUNDS; PIPERAZINES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRIDINES; STAT3 TRANSCRIPTION FACTOR; SULFONAMIDES; TYRPHOSTINS;

EID: 84963972084     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1016/j.neo.2015.07.003     Document Type: Article

References (37)

1. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007, 114:97-109.
2. Louis DN, Perry A, Burger P, Ellison DW, Reifenberger G, von Deimling A, Aldape K, Brat D, Collins VP, Eberhart C, et al. International Society of Neuropathology-Haarlem consensus guidelines for nervous system tumor classification and grading. Brain Pathol 2014, 24:429-435.
3. Claes A, Idema AJ, Wesseling P Diffuse glioma growth: a guerilla war. Acta Neuropathol 2007, 114:443-458.
4. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009, 10:459-466.
5. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005, 352:987-996.
6. Ziegler DS, Kung AL, Kieran MW Anti-apoptosis mechanisms in malignant gliomas. J Clin Oncol 2008, 26:493-500.
7. Bromberg J, Darnell JE The role of STATs in transcriptional control and their impact on cellular function. Oncogene 2000, 19:2468-2473.
8. Yu H, Jove R The STATs of cancer-new molecular targets come of age. Nat Rev Cancer 2004, 4:97-105.
9. Weissenberger J, Loeffler S, Kappeler A, Kopf M, Lukes A, Afanasieva TA, Aguzzi A, Weis J IL-6 is required for glioma development in a mouse model. Oncogene 2004, 23:3308-3316.
10. Gray GK, McFarland BC, Nozell SE, Benveniste EN NF-kappaB and STAT3 in glioblastoma: therapeutic targets coming of age. Expert Rev Neurother 2014, 14:1293-1306.
11. Birner P, Toumangelova-Uzeir K, Natchev S, Guentchev M STAT3 tyrosine phosphorylation influences survival in glioblastoma. J Neurooncol 2010, 100:339-343.
12. Priester M, Copanaki E, Vafaizadeh V, Hensel S, Bernreuther C, Glatzel M, Seifert V, Groner B, Kogel D, Weissenberger J STAT3 silencing inhibits glioma single cell infiltration and tumor growth. Neuro Oncol 2013, 15:840-852.
13. Weissenberger J, Priester M, Bernreuther C, Rakel S, Glatzel M, Seifert V, Kogel D Dietary curcumin attenuates glioma growth in a syngeneic mouse model by inhibition of the JAK1,2/STAT3 signaling pathway. Clin Cancer Res 2010, 16:5781-5795.
14. Chen F, Xu Y, Luo Y, Zheng D, Song Y, Yu K, Li H, Zhang L, Zhong W, Ji Y Down-regulation of Stat3 decreases invasion activity and induces apoptosis of human glioma cells. J Mol Neurosci 2010, 40:353-359.
15. Li GH, Wei H, Chen ZT, Lv SQ, Yin CL, Wang DL STAT3 silencing with lentivirus inhibits growth and induces apoptosis and differentiation of U251 cells. J Neurooncol 2009, 91:165-174.
16. Rahaman SO, Harbor PC, Chernova O, Barnett GH, Vogelbaum MA, Haque SJ Inhibition of constitutively active Stat3 suppresses proliferation and induces apoptosis in glioblastoma multiforme cells. Oncogene 2002, 21:8404-8413.
17. Kroemer G, Galluzzi L, Brenner C Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007, 87:99-163.
18. Adams JM, Cory S The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 2007, 26:1324-1337.
19. Cory S, Adams JM The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002, 2:647-656.
20. Chao DT, Korsmeyer SJ BCL-2 family: regulators of cell death. Annu Rev Immunol 1998, 16:395-419.
21. Lessene G, Czabotar PE, Colman PM BCL-2 family antagonists for cancer therapy. Nat Rev Drug Discov 2008, 7:989-1000.
22. Billard C BH3 mimetics: status of the field and new developments. Mol Cancer Ther 2013, 12:1691-1700.
23. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA, Bruncko M, Deckwerth TL, Dinges J, Hajduk PJ, et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005, 435:677-681.
24. Tse C, Shoemaker AR, Adickes J, Anderson MG, Chen J, Jin S, Johnson EF, Marsh KC, Mitten MJ, Nimmer P, et al. ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res 2008, 68:3421-3428.
25. Hetschko H, Voss V, Horn S, Seifert V, Prehn JH, Kogel D Pharmacological inhibition of Bcl-2 family members reactivates TRAIL-induced apoptosis in malignant glioma. J Neurooncol 2008, 86:265-272.
26. Voss V, Senft C, Lang V, Ronellenfitsch MW, Steinbach JP, Seifert V, Kogel D The pan-Bcl-2 inhibitor (-)-gossypol triggers autophagic cell death in malignant glioma. Mol Cancer Res 2010, 8:1002-1016.
27. Sheng Z, Li L, Zhu LJ, Smith TW, Demers A, Ross AH, Moser RP, Green MR A genome-wide RNA interference screen reveals an essential CREB3L2-ATF5-MCL1 survival pathway in malignant glioma with therapeutic implications. Nat Med 2010, 16:671-677.
28. Yoo JY, Wang W, Desiderio S, Nathans D Synergistic activity of STAT3 and c-Jun at a specific array of DNA elements in the alpha 2-macroglobulin promoter. J Biol Chem 2001, 276:26421-26429.
29. Iwamaru A, Szymanski S, Iwado E, Aoki H, Yokoyama T, Fokt I, Hess K, Conrad C, Madden T, Sawaya R, et al. A novel inhibitor of the STAT3 pathway induces apoptosis in malignant glioma cells both in vitro and in vivo. Oncogene 2007, 26:2435-2444.
30. Li J, Chen Y, Wan J, Liu X, Yu C, Li W ABT-263 enhances sorafenib-induced apoptosis associated with Akt activity and the expression of Bax and p21((CIP1/WAF1)) in human cancer cells. Br J Pharmacol 2014, 171:3182-3195.
31. Kharaziha P, Rodriguez P, Li Q, Rundqvist H, Bjorklund AC, Augsten M, Ullen A, Egevad L, Wiklund P, Nilsson S, et al. Targeting of distinct signaling cascades and cancer-associated fibroblasts define the efficacy of Sorafenib against prostate cancer cells. Cell Death Dis 2012, 3:e262.
32. Yang F, Brown C, Buettner R, Hedvat M, Starr R, Scuto A, Schroeder A, Jensen M, Jove R Sorafenib induces growth arrest and apoptosis of human glioblastoma cells through the dephosphorylation of signal transducers and activators of transcription 3. Mol Cancer Ther 2010, 9:953-962.
33. Konopleva M, Contractor R, Tsao T, Samudio I, Ruvolo PP, Kitada S, Deng X, Zhai D, Shi YX, Sneed T, et al. Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell 2006, 10:375-388.
34. Lucas KM, Mohana-Kumaran N, Lau D, Zhang XD, Hersey P, Huang DC, Weninger W, Haass NK, Allen JD Modulation of NOXA and MCL-1 as a strategy for sensitizing melanoma cells to the BH3-mimetic ABT-737. Clin Cancer Res 2012, 18:783-795.
35. Hikita H, Takehara T, Shimizu S, Kodama T, Shigekawa M, Iwase K, Hosui A, Miyagi T, Tatsumi T, Ishida H, et al. The Bcl-xL inhibitor, ABT-737, efficiently induces apoptosis and suppresses growth of hepatoma cells in combination with sorafenib. Hepatology 2010, 52:1310-1321.
36. Siegelin MD, Raskett CM, Gilbert CA, Ross AH, Altieri DC Sorafenib exerts anti-glioma activity in vitro and in vivo. Neurosci Lett 2010, 478:165-170.
37. Blechacz BR, Smoot RL, Bronk SF, Werneburg NW, Sirica AE, Gores GJ Sorafenib inhibits signal transducer and activator of transcription-3 signaling in cholangiocarcinoma cells by activating the phosphatase shatterproof 2. Hepatology 2009, 50:1861-1870.