The peripheral-type benzodiazepine receptor and tumorigenicity: Isoquinoline binding protein (IBP) antisense knockdown in the C6 glioma cell line

Biochemistry

Volumn 44, Issue 29, 2005, Pages 9924-9935

  Levin, Evgeny ^a   Premkumar, Arumugam ^b   Veenman, Leo ^a   Kugler, Wilfried ^c   Leschiner, Svetlana ^a   Spanier, Ilana ^a   Weisinger, Gary ^d   Lakomek, Max ^c   Weizman, Abraham ^e   Snyder, Solomon H ^f   Pasternak, Gavril W ^b   Gavish, Moshe ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^e TEL AVIV UNIVERSITY   (Israel)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOASSAY; CELLS; DNA; GENES; TUMORS;

CANCER CELLS; CELL CYCLE ANALYSIS; GLIOMA CELLS; PERIPHERAL-TYPE BENZODIAZEPINE RECEPTORS (PBR);

PROTEINS;

ADENINE NUCLEOTIDE TRANSLOCASE; ANION CHANNEL; ANTINEOPLASTIC AGENT; BENZODIAZEPINE RECEPTOR; BINDING PROTEIN; DNA FRAGMENT; ERUCYLPHOSPHO N,N,N TRIMETHYLAMMONIUM; ERUCYLPHOSPHOCHOLINE; ISOQUINOLINE; ISOQUINOLINE BINDING PROTEIN; TRIMETHYLAMMONIUM SALT DERIVATIVE; UNCLASSIFIED DRUG;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER; CARCINOGENICITY; CELL COUNT; CELL CYCLE; CELL DEATH; CONTROLLED STUDY; DNA MODIFICATION; GLIOMA CELL; IN VITRO STUDY; LIGAND BINDING; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CARRIER PROTEINS; CASPASE 3; CASPASES; CELL COUNT; CELL LINE, TUMOR; CLONE CELLS; DNA, ANTISENSE; PHOSPHORYLCHOLINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RECEPTORS, GABA-A; TRANSFECTION; TRYPAN BLUE;

EID: 22744450362     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050150s     Document Type: Article

References (74)

1. McEnery, M. W., Snowman, A. M., Trifiletti, R. R., and Snyder, S. H. (1992) Isolation of the mitochondrial benzodiazepine receptor: association with the voltage-dependent anion channel and the adenine nucleotide carrier, Proc. Natl. Acad. Sci. U.S.A. 89, 3170-3174.
2. 3H]diazepam binding, Proc. Natl. Acad. Sci. U.S.A. 74, 3805-3809.
3. Verma, A., and Snyder, S. H. (1989) Peripheral type benzodiazepine receptors, Annu. Rev. Pharmacol. Toxicol. 29, 307-322.
4. Syapin, P. J., and Skolnick, P. (1979) Characterization of benzodiazepine binding sites in cultured cells of neural origin, J. Neurochem. 32, 1047-1051.
5. 3H]Ro 5-4864 in rat brain and kidney, J. Pharmacol. Exp. Ther. 225, 61-69.
6. Anholt, R. R. H., Pedersen, P. L., De Souza, E. B., and Snyder, S. H. (1986) The peripheral-type benzodiazepine receptor: localization to the mitochondrial outer membrane, J. Biol. Chem. 261, 576-583.
7. Antkiewicz-Michaluk, L., Guidotti, A., and Krueger, K. E. (1988a) Molecular characterization and mitochondrial density of a recognition site for peripheral-type benzodiazepine ligands, Mol. Pharmacol. 34, 272-278.
8. Antkiewicz-Michaluk, L., Mukhin, A. G., Guidotti, A., and Krueger, K. E. (1988b) Purification and characterization of a protein associated with peripheral-type benzodiazepine binding sites, J. Biol. Chem. 263, 17317-17321.
9. 3H]Ro5-4864 in guinea pig lung. Localization to the mitochondrial inner membrane, J. Biol. Chem. 264, 16713-16718.
10. Papadopoulos, V., Boujrad, N., Ikonomovic, M. D., Ferrara, P., and Vidic, B. (1994) Topography of the Leydig cell mitochondrial peripheral-type benzodiazepine receptor, Mol. Cell. Endocrinol. 104, R5-9.
11. Culty, M., Li, H., Boujrad, N., Amri, H., Vidic, B., Bernassau, J. M., Reversat, J. L., and Papadopoulos, V. (1999) In vitro studies on the role of the peripheral-type benzodiazepine receptor in steroidogenesis, J. Steroid Biochem. Mol. Biol. 69, 123-130.
12. Golani, I., Weizman, A., Leschiner, S., Spanier, I., Eckstein, N., Limor, R., Yanai, J., Weisinger, G., and Gavish, M. (2001) Hormonal regulation of peripheral benzodiazepine receptor binding properties is mediated by subunit interaction, Biochemistry 40, 10213-10222.
13. Veenman, L., Leschiner, S., Spanier, I., Weisinger, G., Weizman, A., and Gavish, M. (2002) PK11195 attenuates kainic acid-induced seizures and alterations in peripheral-type benzodiazepine receptor (PBR) components in the rat brain, J. Neurochem. 80, 917-927.
14. Papadopoulos, V., Dharmarajan, A. M., Li, H., Culty, M., Lemay, M., and Sridaran, R. (1999) Mitochondrial peripheral-type benzodiazepine receptor expression. Correlation with gonadotropin-releasing hormone (GnRH) agonist-induced apoptosis in the corpus luteum, Biochem. Pharmacol. 58, 1389-1393.
15. Tsujimoto, Y., and Shimizu, S. (2000) VDAC regulation by the Bcl-2 family of proteins, Cell Death Differ. 7, 1174-1181.
16. Dolder, M., Wendt, S., and Wallimann, T. (2001) Mitochondrial creatine kinase in contact sites: interaction with porin and adenine nucleotide translocase, role in permeability transition and sensitivity to oxidative damage, Biol. Signals Recept. 10, 93-111.
17. Papadopoulos, V., Guarneri, P., Krueger, K. E., Guidotti, A., and Costa, E. (1992) Pregnenolone biosynthesis in C6 glioma cell mitochondria: regulation by diazepam-binding inhibitor mitochondrial receptor, Proc. Natl. Acad. Sci. U.S.A. 89, 5118-5122.
18. Papadopoulos, V., Amri, H., Boujrad, N., Cascio, C, Culty, M., Garnier, M., Hardwick, M., Li, H., Vidic, B., Brown, A. S., Reversa, J. L., Bernassau, J. M., and Drieu, K. (1997) Peripheral benzodiazepine receptor in cholesterol transport and steroidogenesis, Steroids 62, 21-28.
19. Weizman, R., Dagan, E., Snyder, S. H., and Gavish, M. (1997) Impact of pregnancy and lactation on GABAA receptor and central-type and peripheral-type benzodiazepine receptors, Brain Res. 752, 307-314.
20. Weizman, R., Leschiner, S., Schlegel, W., and Gavish, M. (1997) Peripheral-type benzodiazepine receptor ligands and serum steroid hormones, Brain Res. 772, 203-208.
21. Kelly-Hershkovitz, E., Weizman, R., Spanier, I., Leschiner, S., Lahav, M., Weisinger, G., and Gavish, M. (1998) Effects of peripheral-type benzodiazepine receptor antisense knockout on MA-10 Leydig cell proliferation and steroidogenesis, J. Biol. Chem. 273, 5478-5483.
22. Wang, J. K. T., Morgan, J. I., and Spector, S. (1984) Benzodiazepines that bind at peripheral sites inhibit cell proliferation, Proc. Natl. Acad. Sci. U.S.A. 81, 753-756.
23. Landau, M., Weizman, A., Zoref-Shani, E., Beery, E., Wasseman, L., Landau, O., Gavish, M., Brenner, S., and Nordenberg, J. (1998) Antiproliferative and differentiating effects of benzodiazepine receptor ligands on B16 melanoma cells, Biochem. Pharmacol. 56, 1029-1034.
24. Nordenberg, J., Fenig, E., Landau, M., Weizman, R., and Weizman, A. (1999) Effect of psychotropic drugs on cell proliferation and differentiation, Biochem. Pharmacol. 58, 1229-1236.
25. Carmel, I., Fares, F. A., Leschiner, S., Scherubl, H., Weisinger, G., and Gavish, M. (1999) Peripheral-type benzodiazepine receptors in the regulation of proliferation of MCF-7 human breast carcinoma cell line, Biochem. Pharmacol. 58, 273-278.
26. Hirsch, J. D., Beyer, C. F., Malkowitz, L., Beer, B., and Blume, A. J. (1989) Mitochondrial benzodiazepine receptors mediate inhibition of mitochondrial respiratory control, Mol. Pharmacol. 35, 157-163.
27. Zisterer, D. M., Gorman, A. M., Williams, D. C., and Murphy, M. P. (1992) The effects of the peripheral-type benzodiazepine acceptor ligands, Ro 5-4864 and PK 11195, on mitochondrial respiration, Methods Find. Exp. Clin. Pharmacol. 14, 85-90.
28. Ruff, M. R., Pert, C. B., Weber, R. J., Wahl, L. M., Wahl, S. M., and Paul, S. M. (1985) Benzodiazepine receptor-mediated chemotaxis of human monocytes, Science 229, 1281-1283.
29. Bessler, H., Caspi, B., Gavish, M., Rehavi, M., and Weizman, A. (1997) Significant inhibition of spontaneous IgA secretion by selective peripheral-type benzodiazepine receptor ligands, Clin. Neuropharmacol. 20, 215-223.
30. Krueger, K. E. (1995) Molecular and functional properties of mitochondrial benzodiazepine receptors, Biochim. Biophys. Acta 1241, 453-470.
31. Weizman, R., Burgin, R., and Gavish, M. (1993) Modulatory effect of antidepressants on peripheral-type benzodiazepine receptors, Eur. J. Pharmacol. 250, 289-294.
32. Avital, A., Richter-Levin, G., Leschiner, S., Spanier, I., Veenman, L., Weizman, A., and Gavish, M. (2001) Acute and repeated swim stress effects on peripheral benzodiazepine receptors in the rat hippocampus, adrenal, and kidney, Neuropsychopharmacology 25, 669-678.
33. 3H]PK-11195 as a marker for gliosis, Acta Neurochir. 137, 207-216.
34. Veenman, L., and Gavish, M. (2000) Peripheral-type benzodiazepine receptors: their implication in brain disease, Drug Dev. Res. 50, 355-370.
35. Pubill, D., Verdaguer, E., Canudas, A. M., Sureda, F. X., Escubedo, E., Camarasa, J., Pallas, M., and Camins, A. (2001) Orphenadrine prevents 3-nitropropionic acid-induced neurotoxicity in vitro and in vivo, Br. J. Pharmacol. 132, 693-702.
36. Gavish, M., Bachman, I., Shoukrun, R., Katz, Y., Veenman, L., Weisinger, G., and Weizman, A. (1999) Enigma of the peripheral benzodiazepine receptor, Pharmacol. Rev. 51, 629-650.
37. 6 glioma, Neurology 38, 1255-1262.
38. Ikezaki, K., Black, K. L., Santori, E. M., Smith, M. L., Becker, D. P., Payne, B. A., and Toga, A. W. (1990) Three-dimensional comparison of peripheral benzodiazepine binding and histological findings in rat brain tumor, Neurosurgery 27, 78-82.
39. Kletsas, D., Li, W., Han, Z., and Papadopoulos, V. (2004) Peripheral-type benzodiazepine receptor (PBR) and PBR drug ligands in fibroblast and fibrosarcoma cell proliferation: role of ERK, c-Jun and ligand-activated PBR-independent pathways, Biochem. Pharmacol. 67, 1927-1932.
40. Ferrarese, C., Appollonio, I., Frigo, M., Gaini, S. M., Piolti, R., and Frattola, L. (1989) Benzodiazepine receptors and diazepam-binding inhibitor in human cerebral tumors, Ann. Neurol. 26, 564-568.
41. Black, K. L., Ikezaki, K., Santori, E., Becker, D. P., and Vinters, H. V. (1990) Specific high-affinity binding of peripheral benzodiazepine receptor ligands to brain tumors in rat and man, Cancer 65, 93-97.
42. Marcian, E., Van Dort, M. E., Ciliax, B. J., Gildersleeve, D. L., Sherman, P. S., Rosenspire, K. C., Young, A. B., Junck, L., and Wieland, D. M. (1988) Radioiodinated benzodiazepines: agents for mapping glial tumors, J. Med. Chem. 31, 2081-2086.
43. Takada, A., Mitsuka, S., Diksic, M., and Yamamoto, Y. L. (1992) Autoradiographic study of peripheral benzodiazepine receptors in animal brain tumor models and human gliomas, Eur. J. Pharmacol. 228, 131-139.
44. Olson, J. M., Junck, L., Young, A. B., Penney, J. B., and Mancini, W. R. (1988) Isoquinoline and peripheral-type benzodiazepine binding in gliomas: implications for diagnostic imaging, Cancer Res. 48, 5837-5841.
45. Miyazawa, N., Hamel, E., and Diksic, M. (1998) Assessment of the peripheral benzodiazepine receptors in human gliomas by two methods, J. Neuro-Oncol. 38, 19-26.
46. Shiraishi, T., Black, K. L., Ikezaki, K., and Becker, D. P. (1991) Peripheral benzodiazepine induces morphological changes and proliferation of mitochondria in glioma cells, J. Neurosci. Res. 30, 463-474.
47. Ikezaki, K., and Black, K. L. (1990) Stimulation of cell growth and DNA synthesis by peripheral benzodiazepine, Cancer Lett. 49, 115-120.
48. Veenman, L., Levin, E., Weisinger, G., Leschiner, S., Spanier, I., Snyder, S. H., Weizman, A., and Gavish, M. (2004) Peripheral-type benzodiazepine receptor density and in vitro tumorigenicity of glioma cell lines, Biochem. Pharm. 68, 689-698.
49. Weisinger, G., Kelly-Hershkovitz, E., Veenman, L., Spanier, I., Leschiner, S., and Gavish, M. (2004) Peripheral benzodiazepine receptor antisense knockout increases tumorigenicity of MA-10 Leydig cells in vivo and in vitro, Biochemistry 43, 12315-12321.
50. Jendrossek, V., Erdlenbruch, B., Hunold, A., Kugler, W., Eibl, H., and Lakomek, M. (1999) Erucylphosphocholine, a novel antineoplastic ether lipid, blocks growth and induces apoptosis in brain tumor cell lines in vitro, Int. J. Oncol. 14, 15-22.
51. Jendrossek, V., Kugler, W., Erdlenbruch, B., Eibl, H., Lang, F., and Lakomek, M. (2001) Erucylphosphocholine-induced apoptosis in chemoresistant glioblastoma cell lines: involvement of caspase activation and mitochondrial alterations, Anticancer Res. 21, 3389-3396.
52. Kugler, W., Erdlenbruch, B., Jünemann, A., Heinemann, D., Eibl, H., and Lakomek, M. (2002) Erucylphosphocholine-induced apoptosis in glioma cells: involvement of death receptor signaling and caspase activation, J. Neurochem. 82, 1160-1170.
53. Gorman, C. M., Moffat, L. R, and Howard, B. H. (1982) Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells, Mol. Cell Biol. 2, 1044-1051.
54. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72, 248-54.
55. 3H]PK 11195 to cerebral cortex and peripheral tissues of various species: species differences and heterogeneity in peripheral benzodiazepine binding sites, J. Neurochem. 49, 1407-1414.
56. Vindelov, L. L., Christensen, I. J., and Nissen, N. I. (1983) A detergent-trypsin method for the preparation of nuclei for flow cytometric DNA analysis, Cytometry 3, 323-327.
57. Zar, J. M. (1974) Biostatistical Analysis, pp 101-162, Prentice-Hall, Englewood Cliffs, NJ.
58. Lacapere, J. J., and Papadopoulos, V. (2003) Peripheral-type benzodiazepine receptor: structure and function of a cholesterol-binding protein in steroid and bile acid biosynthesis, Steroids 68, 569-585.
59. Katz, Y., Ben-Baruch, G., Kloog, Y., Menczer, J., and Gavish, M. (1990) Increased density of peripheral benzodiazepine-binding sites in ovarian carcinomas as compared with benign ovarian tumours and normal ovaries, Clin. Sci. 78, 155-158.
60. Katz, Y., Eitan, A., and Gavish M. (1990) Increase in peripheral benzodiazepine binding sites in colonie adenocarcinoma, Oncology 47, 139-142.
61. Verrier, F., Mignotte, B., Jan, G., and Brenner, C. (2003) Study of PTPC composition during apoptosis for identification of viral protein target, Ann. N.Y. Acad. Sci. 1010, 126-142.
62. Kunduzova, O. R., Escourrou, G., De La Farge, F., Salvayre, R., Seguelas, M. H., Leducq, N., Bono, F., Herbert, J. M., and Parini, A. (2004) Involvement of peripheral benzodiazepine receptor in the oxidative stress, death-signaling pathways, and renal injury induced by ischemia-reperfusion, J. Am. Soc. Nephrol. 15, 2152-2160.
63. Maaser, K., Hopfner, M., Jansen, A., Weisinger, G., Gavish, M., Kozikowski, A. P., Weizman, A., Carayon, P., Riecken, E. O., Zeitz, M., and Scherubl, H. (2001) Specific ligands of the peripheral benzodiazepine receptor induce apoptosis and cell cycle arrest in human colorectal cancer cells, Br. J. Cancer. 85, 1771-1780.
64. Chelli, B., Lena, A., Vanacore, R., Pozzo, E. D., Costa, B., Rossi, L., Salvetti, A., Scatena, F., Ceruti, S., Abbracchio, M. P., Gremigni, V., and Martini, C. (2004) Peripheral benzodiazepine receptor ligands: mitochondrial transmembrane potential depolarization and apoptosis induction in rat C6 glioma cells, Biochem. Pharmacol. 68, 125-134.
65. Jorda, E. G., Jimenez, A., Verdaguer, E., Canudas, A. M., Folch, J., Sureda, F. X., Camins, A., and Pallas, M. (2005) Evidence in favour of a role for peripheral-type benzodiazepine receptor ligands in amplification of neuronal apoptosis, Apoptosis. 10, 91-104.
66. Gavish, M., and Weizman, R. (1997) Role of peripheral-type benzodiazepine receptors in steroidogenesis, Clin. Neuropharmacol. 20, 473-481.
67. Baudet, C., Chevalier, G., Chassevent, A., Canova, C., Filmon, R., Larra, F., Brachet, P., and Wion, D. (1996) 1,25-Dihydroxyvitamin D3 induces programmed cell death in a rat glioma cell line, J. Neurosci. Res. 46, 540-550.
68. Elias, J., Marian, B., Edling, C., Lachmann, B., Noe, C. R., Rolf, S. H., and Schuster, I. (2003) Induction of apoptosis by vitamin D metabolites and analogs in a glioma cell line, Recent Results Cancer Res. 164, 319-332.
69. Ansquer, Y., Legrand, A., Bringuier, A. F., Vadrot, N., Lardeux, B., Mandelbrot, L., and Feldmann, G. (2005) Progesterone induces BRCA1 mRNA decrease, cell cycle alterations and apoptosis in the MCF7 breast cancer cell line, Anticancer Res. 25, 243-248.
70. Syed, V., Mukherjee, K., Lyons-Weiler, J., Lau, K. M., Mashima, T., Tsuruo, T., and Ho, S. M. (2005) Identification of ATF-3, caveolin-1, DLC-1, and NM23-H2 as putative antitumorigenic, progesterone-regulated genes for ovarian cancer cells by gene profiling, Oncogene 24, 1774-1787.
71. Cascio, C., Guarneri, R., Russo, D., De Leo, G., Guarneri, M., Piccoli, F., and Guarneri, P. (2002) A caspase-3-dependent pathway is predominantly activated by the excitotoxin pregnenolone sulfate and requires early and late cytochrome c release and cell-specific caspase-2 activation in the retinal cell death, J. Neurochem. 83, 1358-1371.
72. 3H]-PK 11195 distribution in dunning AT-1 tumor-bearing rats, Oncol. Res. 6, 603-609.
73. Hardwick, M., Fertikh, D., Culti, M., Li, H., Vidic, B., and Papadopoulos, V. (1999) Peripheral-type benzodiazepine receptor (PBR) in human breast cancer: correlation of breast cancer cell aggressive phenotype with PBR expression, nuclear localization, and PBR-mediated cell proliferation and nuclear transport of cholesterol, Cancer Res. 59, 831-842.
74. Brown, R. C., Degenhardt, B., Kotoula, M., and Papadopoulous, V. (2000) Location-dependent role of the human glioma cell peripheral-type benzodiazepine receptor in proliferation and steroid biosynthesis, Cancer Lett. 156, 125-132.