TSPO as a target for glioblastoma therapeutics

Biochemical Society Transactions

Volumn 43, Issue , 2015, Pages 531-536

  Werry, Eryn L ^a   Barron, Melissa L ^a   Kassiou, Michael ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Apoptosis; Drug design; Glioblastoma; Translocator protein

Indexed keywords

PROTEIN; TRANSLOCATOR PROTEIN; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; ANTINEOPLASTIC AGENT; TSPO PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CLINICAL ASSESSMENT; EXTRACELLULAR MATRIX; GLIOBLASTOMA; HUMAN; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN TARGETING; TUMOR INVASION; UPREGULATION; BRAIN NEOPLASMS; CLINICAL TRIAL (TOPIC); DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; MOLECULARLY TARGETED THERAPY;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BRAIN NEOPLASMS; CLINICAL TRIALS AS TOPIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MOLECULAR TARGETED THERAPY; RECEPTORS, GABA; UP-REGULATION;

EID: 84938811043     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20150015     Document Type: Article

References (52)

1. Wen, P.Y. and Kesari, S. (2008) Malignant gliomas in adults. N. Engl. J. Med. 359, 492-507 CrossRef PubMed
2. Holland, E.C. (2000) Glioblastoma multiforme: the terminator. Proc. Natl. Acad. Sci. U.S.A. 97, 6242-6244 CrossRef PubMed
3. Veenman, L., Gavish, M. and Kugler, W. (2014) Apoptosis induction by erucylphosphohomocholine via the 18 kDa mitochondrial translocator protein: implications for cancer treatment. Anticancer Agents Med. Chem. 14, 559-577 CrossRef PubMed
4. Jaremko, L., Jaremko, M., Giller, K., Becker, S. and Zweckstetter, M. (2014) Structure of the mitochondrial translocator protein in complex with a diagnostic ligand. Science 343, 1363-1366 CrossRef PubMed
5. Caballero, B., Veenman, L. and Gavish, M. (2013) Role of mitochondrial translocator protein (18 kDa) on mitochondrial- related cell death processes. Recent Pat. Endocr. Metab. Immune Drug Discov. 7, 86-101 CrossRef
6. Gatliff, J. and Campanella, M. (2012) The 18 kDa translocator protein (TSPO): a new perspective in mitochondrial biology. Curr. Mol. Med. 12, 356-368 PubMed
7. Verma, A., Nye, J.S. and Snyder, S.H. (1987) Porphyrins are endogenous ligands for the mitochondrial (peripheral-type) benzodiazepine receptor. Proc. Natl. Acad. Sci. U.S.A. 84, 2256-2260 CrossRef PubMed
8. Chua, S.W., Kassiou, M. and Ittner, L.M. (2014) The translocator protein as a drug target in Alzheimer's disease. Expert. Rev. Neurother. 14, 439-448 CrossRef PubMed
9. Papadopoulos, V., Amri, H., Boujrad, N., Cascio, C., Culty, M., Garnier, M., Hardwick, M., Li, H., Vidic, B., Brown, A.S. et al. (1997) Peripheral benzodiazepine receptor in cholesterol transport and steroidogenesis. Steroids 62, 21-28 CrossRef PubMed
10. Tu, L.N., Morohaku, K., Manna, P.R., Pelton, S.H., Butler, W.R., Stocco, D.M. and Selvaraj, V. (2014) Peripheral benzodiazepine receptor/translocator protein global knock-out mice are viable with no effects on steroid hormone biosynthesis. J. Biol. Chem. 289, 27444-27454 CrossRef PubMed
11. Banati, R.B., Middleton, R.J., Chan, R., Hatty, C.R., Wai-Ying Kam, W., Quin, C., Graeber, M.B., Parmar, A., Zahra, D., Callaghan, P. et al. (2014) Positron emission tomography and functional characterization of a complete PBR/TSPO knockout. Nat. Commun. 5, 5452 CrossRef PubMed
12. Liu, G.J., Middleton, R.J., Hatty, C.R., Kam, W.W., Chan, R., Pham, T., Harrison-Brown, M., Dodson, E., Veale, K. and Banati, R.B. (2014) The 18 kDa translocator protein, microglia and neuroinflammation. Brain Pathol. 24, 631-653 CrossRef PubMed
13. Cheung, Y.Y., Nickels, M.L., Tang, D., Buck, J.R. and Manning, H.C. (2014) Facile synthesis of SSR180575 and discovery of 7-chloro-N,N,5-trimethyl-4-oxo-3(6-[(18)F]fluoropyridin-2-yl)-3,5-dihydro-4H-pyri dazino[4,5-b]indole-1-acetamide, a potent pyridazinoindole ligand for PET imaging of TSPO in cancer. Bioorg Med. Chem. Lett. 24, 4466-4471 CrossRef PubMed
14. Miettinen, H., Kononen, J., Haapasalo, H., Helen, P., Sallinen, P., Harjuntausta, T., Helin, H. and Alho, H. (1995) Expression of peripheral-type benzodiazepine receptor and diazepam binding inhibitor in human astrocytomas: relationship to cell proliferation. Cancer Res. 55, 2691-2695 PubMed
15. Miyazawa, N., Hamel, E. and Diksic, M. (1998) Assessment of the peripheral benzodiazepine receptors in human gliomas by two methods. J. Neurooncol. 38, 19-26 CrossRef PubMed
16. Vlodavsky, E. and Soustiel, J.F. (2007) Immunohistochemical expression of peripheral benzodiazepine receptors in human astrocytomas and its correlation with grade of malignancy, proliferation, apoptosis and survival. J. Neurooncol. 81, 1-7 CrossRef PubMed
17. 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. Pharmacol. 68, 689-698 CrossRef PubMed
18. Tang, D., Hight, M.R., McKinley, E.T., Fu, A., Buck, J.R., Smith, R.A., Tantawy, M.N., Peterson, T.E., Colvin, D.C., Ansari, M.S. et al. (2012) Quantitative preclinical imaging of TSPO expression in glioma using N,N-diethyl-2-(2-(4-(2-18F-fluoroethoxy)phenyl)-5,7-dimethylpyrazolo[1,5-a]pyrimi din-3-yl)acetamide. J. Nucl. Med. 53, 287-294 CrossRef PubMed
19. Winkeler, A., Boisgard, R., Awde, A.R., Dubois, A., Theze, B., Zheng, J., Ciobanu, L., Dolle, F., Viel, T., Jacobs, A.H. and Tavitian, B. (2012) The translocator protein ligand [(1)(8)F]DPA-714 images glioma and activated microglia in vivo. Eur. J. Nucl. Med. Mol. Imaging 39, 811-823 CrossRef PubMed
20. Buck, J.R., McKinley, E.T., Hight, M.R., Fu, A., Tang, D., Smith, R.A., Tantawy, M.N., Peterson, T.E., Colvin, D., Ansari, M.S. et al. (2011) Quantitative, preclinical PET of translocator protein expression in glioma using 18F-N-fluoroacetyl-N-(2,5-dimethoxybenzyl)-2-phenoxyaniline. J. Nucl. Med. 52, 107-114 CrossRef PubMed
21. Junck, L., Olson, J.M., Ciliax, B.J., Koeppe, R.A., Watkins, G.L., Jewett, D.M., McKeever, P.E., Wieland, D.M., Kilbourn, M.R., Starosta-Rubinstein, S. et al. (1989) PET imaging of human gliomas with ligands for the peripheral benzodiazepine binding site. Ann. Neurol. 26, 752-758 CrossRef PubMed
22. Pappata, S., Cornu, P., Samson, Y., Prenant, C., Benavides, J., Scatton, B., Crouzel, C., Hauw, J.J. and Syrota, A. (1991) PET study of carbon-11-PK 11195 binding to peripheral type benzodiazepine sites in glioblastoma: a case report. J. Nucl. Med. 32, 1608-1610 PubMed
23. Su, Z., Herholz, K., Gerhard, A., Roncaroli, F., Du Plessis, D., Jackson, A., Turkheimer, F. and Hinz, R. (2013) [(1)(1)C]-(R)PK11195 tracer kinetics in the brain of glioma patients and a comparison of two referencing approaches. Eur. J. Nucl. Med. Mol. Imaging40, 1406-1419 CrossRef PubMed
24. Chauveau, F., Boutin, H., Van Camp, N., Dolle, F. and Tavitian, B. (2008) Nuclear imaging of neuroinflammation: a comprehensive review of [11C]PK11195 challengers. Eur. J. Nucl. Med. Mol. Imaging 35, 2304-2319 CrossRef PubMed
25. Endres, C.J., Pomper, M.G., James, M., Uzuner, O., Hammoud, D.A., Watkins, C.C., Reynolds, A., Hilton, J., Dannals, R.F. and Kassiou, M. (2009) Initial evaluation of 11C-DPA-713, a novel TSPO PET ligand, in humans. J. Nucl. Med. 50, 1276-1282 CrossRef PubMed
26. Corcia, P., Tauber, C., Vercoullie, J., Arlicot, N., Prunier, C., Praline, J., Nicolas, G., Venel, Y., Hommet, C., Baulieu, J.L. et al. (2012) Molecular imaging of microglial activation in amyotrophic lateral sclerosis. PLoS One 7, e52941 CrossRef PubMed
27. Kang, M.H. and Reynolds, C.P. (2009) Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy. Clin. Cancer Res. 15, 1126-1132 CrossRef PubMed
28. Daniele, S., Taliani, S., Da Pozzo, E., Giacomelli, C., Costa, B., Trincavelli, M.L., Rossi, L., La Pietra, V., Barresi, E., Carotenuto, A. et al. (2014) Apoptosis therapy in cancer: the first single-molecule co-activating p53 and the translocator protein in glioblastoma. Sci. Rep. 4, 4749 CrossRef PubMed
29. Placzek, W.J., Wei, J., Kitada, S., Zhai, D., Reed, J.C. and Pellecchia, M. (2010) A survey of the anti-apoptotic Bcl-2 subfamily expression in cancer types provides a platform to predict the efficacy of Bcl-2 antagonists in cancer therapy. Cell Death Dis. 1, e40 CrossRef PubMed
30. 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 CrossRef PubMed
31. Zamzami, N. and Kroemer, G. (2001) The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell Biol. 2, 67-71 CrossRef PubMed
32. Kugler, W., Veenman, L., Shandalov, Y., Leschiner, S., Spanier, I., Lakomek, M. and Gavish, M. (2008) Ligands of the mitochondrial 18 kDa translocator protein attenuate apoptosis of human glioblastoma cells exposed to erucylphosphohomocholine. Cell Oncol. 30, 435-450 PubMed
33. Veenman, L., Bode, J., Gaitner, M., Caballero, B., Pe'er, Y., Zeno, S., Kietz, S., Kugler, W., Lakomek, M. and Gavish, M. (2012) Effects of 18-kDa translocator protein knockdown on gene expression of glutamate receptors, transporters, and metabolism, and on cell viability affected by glutamate. Pharmacogenet. Genomics 22, 606-619 CrossRef PubMed
34. Castellano, S., Taliani, S., Viviano, M., Milite, C., Da Pozzo, E., Costa, B., Barresi, E., Bruno, A., Cosconati, S., Marinelli, L. et al. (2014) Structure-activity relationship refinement and further assessment of 4-phenylquinazoline-2-carboxamide translocator protein ligands as antiproliferative agents in human glioblastoma tumors. J. Med. Chem. 57, 2413-2428 CrossRef PubMed
35. Cosimelli, B., Simorini, F., Taliani, S., La Motta, C., Da Settimo, F., Severi, E., Greco, G., Novellino, E., Costa, B., Da Pozzo, E. et al. (2011) Tertiary amides with a five-membered heteroaromatic ring as new probes for the translocator protein. Eur. J. Med. Chem. 46, 4506-4520 CrossRef PubMed
36. Chelli, B., Salvetti, A., Da Pozzo, E., Rechichi, M., Spinetti, F., Rossi, L., Costa, B., Lena, A., Rainaldi, G., Scatena, F. et al. (2008) PK 11195 differentially affects cell survival in human wild-type and 18 kDa translocator protein-silenced ADF astrocytoma cells. J. Cell Biochem. 105, 712-723 CrossRef PubMed
37. Laquintana, V., Denora, N., Lopalco, A., Lopedota, A., Cutrignelli, A., Lasorsa, F.M., Agostino, G. and Franco, M. (2014) Translocator protein ligand-PLGA conjugated nanoparticles for 5-fluorouracil delivery to glioma cancer cells. Mol. Pharm. 11, 859-871 CrossRef PubMed
38. Zisterer, D.M., Hance, N., Campiani, G., Garofalo, A., Nacci, V. and Williams, D.C. (1998) Antiproliferative action of pyrrolobenzoxazepine derivatives in cultured cells: absence of correlation with binding to the peripheral-type benzodiazepine binding site. Biochem. Pharmacol. 55, 397-403 CrossRef PubMed
39. Farges, R., Joseph-Liauzun, E., Shire, D., Caput, D., Le Fur, G. and Ferrara, P. (1994) Site-directed mutagenesis of the peripheral benzodiazepine receptor: identification of amino acids implicated in the binding site of Ro5-4864. Mol. Pharmacol. 46, 1160-1167 PubMed
40. Scarf, A.M., Luus, C., Da Pozzo, E., Selleri, S., Guarino, C., Martini, C., Ittner, L.M. and Kassiou, M. (2012) Evidence for complex binding profiles and species differences at the translocator protein (TSPO) (18 kDa). Curr. Mol. Med. 12, 488-493 PubMed
41. Kreisl, W.C., Jenko, K.J., Hines, C.S., Lyoo, C.H., Corona, W., Morse, C.L., Zoghbi, S.S., Hyde, T., Kleinman, J.E., Pike, V.W. et al. (2013) A genetic polymorphism for translocator protein 18 kDa affects both in vitro and in vivo radioligand binding in human brain to this putative biomarker of neuroinflammation. J. Cereb. Blood Flow Metab. 33, 53-58 CrossRef PubMed
42. Tysnes, B.B. and Mahesparan, R. (2001) Biological mechanisms of glioma invasion and potential therapeutic targets. J. Neurooncol. 53, 129-147 CrossRef PubMed
43. Kuramochi, M., Fukuhara, H., Nobukuni, T., Kanbe, T., Maruyama, T., Ghosh, H.P., Pletcher, M., Isomura, M., Onizuka, M., Kitamura, T. et al. (2001) TSLC1 is a tumor-suppressor gene in human non-small-cell lung cancer. Nat. Genet. 27, 427-430 CrossRef PubMed
44. Bode, J., Veenman, L., Caballero, B., Lakomek, M., Kugler, W. and Gavish, M. (2012) The 18 kDa translocator protein influences angiogenesis, as well as aggressiveness, adhesion, migration, and proliferation of glioblastoma cells. Pharmacogenet. Genomics 22, 538-550 CrossRef PubMed
45. 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 CrossRef PubMed
46. Rechichi, M., Salvetti, A., Chelli, B., Costa, B., Da Pozzo, E., Spinetti, F., Lena, A., Evangelista, M., Rainaldi, G., Martini, C. et al. (2008) TSPO over-expression increases motility, transmigration and proliferation properties of C6 rat glioma cells. Biochim. Biophys. Acta 1782, 118-125 CrossRef PubMed
47. Kabat, G.C., Etgen, A.M. and Rohan, T.E. (2010) Do steroid hormones play a role in the etiology of glioma? Cancer Epidemiol. Biomarkers Prev. 19, 2421-2427 CrossRef
48. Shoukrun, R., Veenman, L., Shandalov, Y., Leschiner, S., Spanier, I., Karry, R., Katz, Y., Weisinger, G., Weizman, A. and Gavish, M. (2008) The 18-kDa translocator protein, formerly known as the peripheral-type benzodiazepine receptor, confers proapoptotic and antineoplastic effects in a human colorectal cancer cell line. Pharmacogenet. Genomics 18, 977-988 CrossRef PubMed
49. Xia, W., Spector, S., Hardy, L., Zhao, S., Saluk, A., Alemane, L. and Spector, N.L. (2000) Tumor selective G2/M cell cycle arrest and apoptosis of epithelial and hematological malignancies by BBL22, a benzazepine. Proc. Natl. Acad. Sci. U.S.A. 97, 7494-7499 CrossRef PubMed
50. Crossley, E.L., Issa, F., Scarf, A.M., Kassiou, M. and Rendina, L.M. (2011) Synthesis and cellular uptake of boron-rich pyrazolopyrimidines: exploitation of the translocator protein for the efficient delivery of boron into human glioma cells. Chem. Commun. 47, 12179-12181 CrossRef
51. Sileikyte, J., Blachly-Dyson, E., Sewell, R., Carpi, A., Menabo, R., Di Lisa, F., Ricchelli, F., Bernardi, P. and Forte, M. (2014) Regulation of the mitochondrial permeability transition pore by the outer membrane does not involve the peripheral benzodiazepine receptor (Translocator Protein of 18 kDa (TSPO)). J. Biol. Chem. 289, 13769-13781 CrossRef PubMed
52. Costa, B., Da Pozzo, E., Giacomelli, C., Taliani, S., Bendinelli, S., Barresi, E., Da Settimo, F. and Martini, C. (2015) TSPO ligand residence time influences human glioblastoma multiforme cell death/life balance. Apoptosis 20, 383-398 CrossRef PubMed