Drugs targeting the mitochondrial pore act as citotoxic and cytostatic agents in temozolomide-resistant glioma cells

Journal of Translational Medicine

Volumn 7, Issue , 2009, Pages

  Lena, Annalisa ^a   Rechichi, Mariarosa ^a   Salvetti, Alessandra ^a   Bartoli, Barbara ^a   Vecchio, Donatella ^a   Scarcelli, Vittoria ^a   Amoroso, Rosina ^b   Benvenuti, Lucia ^b   Gagliardi, Rolando ^b   Gremigni, Vittorio ^a   Rossi, Leonardo ^a,c  

^a UNIVERSITY OF PISA   (Italy)

^b Livorno Hospital   (Italy)

^c ISTITUTO TOSCANO TUMORI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

6 [3 (1 ADAMANTYL) 4 HYDROXYPHENYL] 2 NAPHTHOIC ACID; ACRIDINE ORANGE; BETULIC ACID; CALCEIN; CYTOSTATIC AGENT; CYTOTOXIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR; HOE 33342; LIPOCORTIN 5; LONIDAMINE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; TEMOZOLOMIDE; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CARRIER PROTEIN; CYCLOSPORIN; DACARBAZINE; DRUG DERIVATIVE; EPIDERMAL GROWTH FACTOR RECEPTOR VIII; INDAZOLE DERIVATIVE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; RETINOID; TRITERPENE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BINDING ASSAY; CANCER CELL CULTURE; CANCER INHIBITION; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG TARGETING; GENE AMPLIFICATION; GENE DELETION; GLIOBLASTOMA; GLIOMA CELL; HEMIZYGOSITY; HUMAN; HUMAN CELL; HUMAN TISSUE; MITOCHONDRIAL PERMEABILITY; MITOSIS INDEX; MOLECULAR GENETICS; MUTATIONAL ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; CELL DEATH; CELL SURVIVAL; DRUG ANTAGONISM; DRUG EFFECT; DRUG RESISTANCE; GENETICS; GLIOMA; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; PATHOLOGY; POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

ACRIDINE ORANGE; CARBONYL CYANIDE M-CHLOROPHENYL HYDRAZONE; CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; CYCLOSPORINE; CYTOSTATIC AGENTS; DACARBAZINE; DRUG RESISTANCE, NEOPLASM; GLIOMA; HUMANS; INDAZOLES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; POLYMERASE CHAIN REACTION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RETINOIDS; TRITERPENES;

EID: 63649110495     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-7-13     Document Type: Article

References (51)

1. Kleihues P Cavenee W WHO classification of tumours. Pathology and genetics: Tumours of the nervous system Lyon, France: IARC Press 2000.
2. Stupp R Mason WP Bent van den MJ Weller M Fisher B Taphoorn MJ Belanger K Brandes AA Marosi C Bogdahn U Curschmann J Janzer RC Ludwin SK Gorlia T Allgeier A Lacombe D Cairncross JG Eisenhauer E Mirimanoff RO European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy, Groups, National Cancer Institute of Canada Clinical Trials Group Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma N Engl J Med 2005, 352:987-96. 10.1056/NEJMoa043330 15758009
3. Nagane M Kobayashi K Ohnishi A Shimizu S Shiokawa Y Prognostic significance of O6-methylguanine-DNA methyltransferase protein expression in patients with recurrent glioblastoma treated with temozolomide Jpn J Clin Oncol 2007, 37:897-906. 10.1093/jjco/hym132 18156172
4. Wong ET Hess KR Gleason MJ Jaeckle KA Kyritsis AP Prados MD Levin VA Yung WK Outcomes and prognostic factors in recurrent glioma patients enrolled onto phase II clinical trials J Clin Oncol 1999, 17:2572-8. 10561324
5. Ohgaki H Kleihues P Genetic pathways to primary and secondary glioblastoma Am J Pathol 2007, 170:1445-53. 1854940 17456751 10.2353/ ajpath.2007.070011
6. Wong AJ Bigner SH Bigner DD Kinzler KW Hamilton SR Vogelstein B Increased expression of the epidermal growth factor receptor gene in malignant gliomas is invariably associated with gene amplification Proc Natl Acad Sci USA 1987, 84:6899-903. 299192 3477813 10.1073/ pnas.84.19.6899
7. de Groot JF Gilbert MR New molecular targets in malignant gliomas Curr Opin Neurol 2007, 20:712-8. 17992095
8. Prados MD Lamborn KR Chang S Burton E Butowski N Malec M Kapadia A Rabbitt J Page MS Fedoroff A Xie D Kelley SK Phase 1 study of erlotinib HCl alone and combined with temozolomide in patients with stable or recurrent malignant glioma Neuro Oncol 2006, 8:67-78. 1871925 16443950 10.1215/S1522851705000451
9. Rich JN Reardon DA Peery T Dowell JM Quinn JA Penne KL Wikstrand CJ Van Duyn LB Dancey JE McLendon RE Kao JC Stenzel TT Ahmed Rasheed BK Tourt-Uhlig SE Herndon JE 2nd Vredenburgh JJ Sampson JH Friedman AH Bigner DD Friedman HS Phase II trial of gefitinib in recurrent glioblastoma J Clin Oncol 2004, 22:133-42. 10.1200/JCO.2004.08.110 14638850
10. Armstrong JS Mitochondria: A target for cancer therapy Br J Pharmacol 2006, 147:239-48. 1751297 16331284 10.1038/sj.bjp.0706556
11. Bernardi P Krauskopf A Basso E Petronilli V Blachly-Dyson E Di Lisa F Forte MA The mitochondrial permeability transition from in vitro artifact to disease target FEBS J 2006, 273:2077-99. 10.1111/ j.1742-4658.2006.05213.x 16649987
12. Brenner C Grimm S The permeability transition pore complex in cancer cell death Oncogene 2006, 25:4744-56. 10.1038/sj.onc.1209609 16892087
13. Kroemer G Galluzzi L Brenner C Mitochondrial membrane permeabilization in cell death Physiol Rev 2007, 87:99-163. 10.1152/physrev.00013.2006 17237344
14. Zoratti M Szabò I The mitochondrial permeability transition Biochim Biophys Acta 1995, 1241:139-76. 7640294
15. Galiegue S Tinel N Casellas P The peripheral benzodiazepine receptor: A promising therapeutic drug target Curr Med Chem 2003, 10:1563-72. 10.2174/0929867033457223 12871127
16. Giraud S Bonod-Bidaud C Wesolowski-Louvel M Stepien G Expression of human ANT2 gene in highly proliferative cells: GRBOX, a new transcriptional element, is involved in the regulation of glycolytic ATP import into mitochondria J Mol Biol 1998, 281:409-18. 10.1006/ jmbi.1998.1955 9698557
17. Lunardi J Attardi G Differential regulation of expression of the multiple ADP/ATP translocase genes in human cells J Biol Chem 1991, 266:16534-40. 1885585
18. Baráth P Albert-Fournier B Luciaková K Nelson BD Characterization of a silencer element and purification of a silencer protein that negatively regulates the human adenine nucleotide translocator 2 promoter J Biol Chem 1999, 274:3378-84. 10.1074/ jbc.274.6.3378 9920880
19. Chelli B Lena A Vanacore R Da Pozzo E Costa B Rossi L Salvetti A Scatena F Ceruti S Abbracchio MP Gremigni V Martini C Peripheral benzodiazepine receptor ligands: Mitochondrial transmembrane potential depolarization and apoptosis induction in rat C6 glioma cells Biochem Pharmacol 2004, 68:125-34. 10.1016/j.bcp.2004.03.008 15183124
20. Chelli B Rossi L Da Pozzo E Costa B Spinetti F Rechichi M Salvetti A Lena A Simorini F Vanacore R Scatena F Da Settimo F Gremigni V Martini C PIGA (N,N-Di-n-butyl-5-chloro-2-(4-chlorophenyl)indol-3-ylglyoxylamide), a new mitochondrial benzodiazepine-receptor ligand, induces apoptosis in C6 glioma cells Chembiochem 2005, 6:1082-8. 10.1002/cbic.200400350 15883977
21. Kanzawa T Zhang L Xiao L Germano IM Kondo Y Kondo S Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3 Oncogene 2005, 24:980-91. 10.1038/sj.onc.1208095 15592527
22. Fulda S Jeremias I Steiner HH Pietsch T Debatin KM Betulinic acid: A new cytotoxic agent against malignant brain-tumor cells Int J Cancer 1999, 82:435-41. 10.1002/ (SICI)1097-0215(19990730)82:3<435::AID-IJC18>3.0.CO;2-1 10399962
23. Del Bufalo D Biroccio A Soddu S Laudonio N D'Angelo C Sacchi A Zupi G Lonidamine induces apoptosis in drug-resistant cells independently of the p53 gene J Clin Invest 1996, 98:1165-73. 507539 8787680 10.1172/ JCI118900
24. Costantini P Jacotot E Decaudin D Kroemer G Mitochondrion as a novel target of anticancer chemotherapy J Natl Cancer Inst 2000, 92:1042-53. 10.1093/jnci/92.13.1042 10880547
25. Eiznhamer DA Xu ZQ Betulinic acid: A promising anticancer candidate IDrugs 2004, 7:359-73. 15057642
26. Fulda S Debatin KM Betulinic acid induces apoptosis through a direct effect on mitochondria in neuroectodermal tumors Med Pediatr Oncol 2000, 35:616-8. 10.1002/ 1096-911X(20001201)35:6<616::AID-MPO27>3.0.CO;2-N 11107130
27. Zuco V Supino R Righetti SC Cleris L Marchesi E Gambacorti-Passerini C Formelli F Selective cytotoxicity of betulinic acid on tumor cell lines, but not on normal cells Cancer Lett 2002, 175:17-25. 10.1016/ S0304-3835(01)00718-2 11734332
28. Ben-Yoseph O Lyons JC Song CW Ross BD Mechanism of action of lonidamine in the 9L brain tumor model involves inhibition of lactate efflux and intracellular acidification J Neurooncol 1998, 36:149-57. 10.1023/ A:1005819604858 9525814
29. Paggi MG Carapella CM Fanciulli M Del Carlo C Giorno S Zupi G Silvestrini B Caputo A Floridi A Effect of lonidamine on human malignant gliomas: Biochemical studies J Neurooncol 1988, 6:203-9. 10.1007/ BF00163702 3225640
30. Belzacq AS El Hamel C Vieira HL Cohen I Haouzi D Métivier D Marchetti P Brenner C Kroemer G Adenine nucleotide translocator mediates the mitochondrial membrane permeabilization induced by lonidamine, arsenite and CD437 Oncogene 2001, 20:7579-87. 10.1038/sj.onc.1204953 11753636
31. Fontana JA Rishi AK Classical and novel retinoids: Their targets in cancer therapy Leukemia 2002, 16:463-72. 10.1038/sj.leu.2402414 11960323
32. Rishi AK Zhang L Boyanapalli M Wali A Mohammad RM Yu Y Fontana JA Hatfield JS Dawson MI Majumdar AP Reichert U Identification and characterization of a cell cycle and apoptosis regulatory protein-1 as a novel mediator of apoptosis signaling by retinoid CD437 J Biol Chem 2003, 278:33422-35. 10.1074/jbc.M303173200 12816952
33. Kim HJ Lotan R Identification of protein modulation by the synthetic retinoid CD437 in lung carcinoma cells using high throughput immunoblotting Int J Oncol 2005, 26:483-91. 15645134
34. Fabrizi C Colasanti M Persichini T Businaro R Starace G Lauro GM Interferon gamma up-regulates alpha 2 macroglobulin expression in human astrocytoma cells J Neuroimmunol 1994, 53:31-7. 10.1016/ 0165-5728(94)90061-2 7519632
35. Ji H Zhao X Yuza Y Shimamura T Li D Protopopov A Jung BL McNamara K Xia H Glatt KA Thomas RK Sasaki H Horner JW Eck M Mitchell A Sun Y Al-Hashem R Bronson RT Rabindran SK Discafani CM Maher E Shapiro GI Meyerson M Wong KK Epidermal growth factor receptor variant III mutations in lung tumorigenesis and sensitivity to tyrosine kinase inhibitors Proc Natl Acad Sci USA 2006, 103:7817-22. 1456806 16672372 10.1073/pnas.0510284103
36. Abramoff MD Magelhaes PJ Ram SJ Image Processing with ImageJ Biophotonics International 2004, 11:36-42.
37. Szilágyi G Simon L Koska P Telek G Nagy Z Visualization of mitochondrial membrane potential and reactive oxygen species via double staining Neurosci Lett 2006, 399:206-9. 10.1016/j.neulet.2006.01.071 16530963
38. Schmid I Uittenbogaart C Jamieson BD Live-cell assay for detection of apoptosis by dual-laser flow cytometry using Hoechst 33342 and 7-amino-actinomycin D Nat Protoc 2007, 2:187-90. 10.1038/nprot.2006.458 17401329
39. Paglin S Hollister T Delohery T Hackett N McMahill M Sphicas E Domingo D Yahalom J A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles Cancer Res 2001, 61:439-44. 11212227
40. Biroccio A Bufalo DD Ricca A D'Angelo C D'Orazi G Sacchi A Soddu S Zupi G Increase of BCNU sensitivity by wt-p53 gene therapy in glioblastoma lines depends on the administration schedule Gene Ther 1999, 6:1064-72. 10.1038/sj.gt.3300935 10455409
41. Wick W Grimmel C Wagenknecht B Dichgans J Weller M Betulinic acid-induced apoptosis in glioma cells: A sequential requirement for new protein synthesis, formation of reactive oxygen species, and caspase processing J Pharmacol Exp Ther 1999, 289:1306-12. 10336521
42. Watanabe Y Tsuchiya H Sakabe T Matsuoka S Akechi Y Fujimoto Y Yamane K Ikeda R Nishio R Terabayashi K Ishii K Gonda K Matsumi Y Ashla AA Okamoto H Takubo K Tomita A Hoshikawa Y Kurimasa A Itamochi H Harada T Terakawa N Shiota G CD437 induces apoptosis in ovarian adenocarcinoma cells via ER stress signaling Biochem Biophys Res Commun 2008, 366:840-7. 10.1016/j.bbrc.2007.12.028 18082618
43. Jiang T Soprano DR Soprano KJ GADD45A is a mediator of CD437 induced apoptosis in ovarian carcinoma cells J Cell Physiol 2007, 212:771-9. 10.1002/jcp.21073 17474084
44. Boisvieux-Ulrich E Sourdeval M Marano F CD437, a synthetic retinoid, induces apoptosis in human respiratory epithelial cells via caspase-independent mitochondrial and caspase-8-dependent pathways both up-regulated by JNK signaling pathway Exp Cell Res 2005, 307:76-90. 10.1016/j.yexcr.2005.02.005 15922728
45. Floridi A Paggi MG D'Atri S De Martino C Marcante ML Silvestrini B Caputo A Effect of lonidamine on the energy metabolism of Ehrlich ascites tumor cells Cancer Res 1981, 41:4661-6. 7306982
46. Carapella CM Paggi MG Calvosa F Cattani F Jandolo B Mastrostefano R Raus L Riccio A Lonidamine in the combined treatment of malignant gliomas. A randomized study J Neurosurg Sci 1990, 34:261-4. 2098504
47. Oudard S Carpentier A Banu E Fauchon F Celerier D Poupon MF Dutrillaux B Andrieu JM Delattre JY Phase II study of lonidamine and diazepam in the treatment of recurrent glioblastoma multiforme J Neurooncol 2003, 63:81-6. 10.1023/A:1023756707900 12814259
48. Costa SL Paillaud E Fages C Rochette-Egly C Plassat JL Jouault H Perzelova A Tardy M Effects of a novel synthetic retinoid on malignant glioma in vitro: Inhibition of cell proliferation, induction of apoptosis and differentiation Eur J Cancer 2001, 37:520-30. 10.1016/ S0959-8049(00)00430-5 11267863
49. Jeremias I Steiner HH Benner A Debatin KM Herold-Mende C Cell death induction by betulinic acid, ceramide and TRAIL in primary glioblastoma multiforme cells Acta Neurochir (Wien) 2004, 146:721-9. 10.1007/ s00701-004-0286-4 15197616
50. Fulda S Jeremias I Debatin KM Cooperation of betulinic acid and TRAIL to induce apoptosis in tumor cells Oncogene 2004, 23:7611-20. 10.1038/ sj.onc.1207970 15361826
51. Rzeski W Stepulak A Szymañski M Sifringer M Kaczor J Wejksza K Zdzisiñska B Kandefer-Szerszeñ M Betulinic acid decreases expression of bcl-2 and cyclin D1, inhibits proliferation, migration and induces apoptosis in cancer cells Naunyn Schmiedebergs Arch Pharmacol 2006, 374:11-20. 10.1007/s00210-006-0090-1 16964520