Targeting the 18-kDa translocator protein: Recent perspectives for neuroprotection

Biochemical Society Transactions

Volumn 43, Issue , 2015, Pages 559-565

  Da Pozzo, Eleonora ^a   Giacomelli, Chiara ^a   Barresi, Elisabetta ^a   Costa, Barbara ^a   Taliani, Sabrina ^a   Da Settimo Passetti, Federico ^a   Martini, Claudia ^a  

^a UNIVERSITY OF PISA   (Italy)

Author keywords

Central nervous system diseases; Neuro inflammation; Neurodegeneration; Neurotrauma; Translocator protein; Translocator protein (TSPO) ligand

Indexed keywords

CARRIER PROTEIN; LIGAND; NEUROPROTECTIVE AGENT; 4 AMINOBUTYRIC ACID RECEPTOR; TSPO PROTEIN, HUMAN;

ARTICLE; BRAIN INJURY; CENTRAL NERVOUS SYSTEM; DRUG TARGETING; ENCEPHALITIS; GLIA CELL; GLIOMA; HUMAN; MITOCHONDRIAL MEMBRANE; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NERVOUS SYSTEM INJURY; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; STEROIDOGENESIS; TRAUMATIC BRAIN INJURY; UPREGULATION; ANIMAL; BRAIN DISEASES; CHEMISTRY; DRUG EFFECTS; GLIA; METABOLISM; MOLECULARLY TARGETED THERAPY; NERVE CELL; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN DISEASES; HUMANS; LIGANDS; MOLECULAR TARGETED THERAPY; NEUROGLIA; NEURONS; NEUROPROTECTIVE AGENTS; RECEPTORS, GABA; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84938676203     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20150028     Document Type: Article

References (50)

1. Papadopoulos, V., Baraldi, M., Guilarte, T.R., Knudsen, T.B., Lacapere, J.J., Lindemann, P., Norenberg, M.D., Nutt, D., Weizman, A., Zhang, M.R. and Gavish, M. (2006) Translocator protein (18 kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol. Sci. 27, 402-409 CrossRef PubMed
2. Olson, J.M., Ciliax, B.J., Mancini, W.R. and Young, A.B. (1988) Presence of peripheral-type benzodiazepine binding sites on human erythrocytemembranes. Eur. J. Pharmacol. 152, 47-53 CrossRef PubMed
3. O'Beirne, G.B., Woods, M.J. and Williams, D.C. (1990) Two subcellular locations for peripheral-type benzodiazepine acceptors in rat liver. Eur. J. Biochem. 188, 131-138 CrossRef PubMed
4. Woods, M.J., Zisterer, D.M. and Williams, D.C. (1996) Two cellular and subcellular locations for the peripheral-type benzodiazepine receptor in rat liver. Biochem. Pharmacol. 51, 1283-1292 CrossRef PubMed
5. Banati, R.B., Liu, G. and Middleton, R. (2013) Transgenic non-human organisms with non-functional TSPO genes. WO 2,014,138,791
6. Banati, R.B., Middleton, R.J., Chan, R., Hatty, C.R., Kam, W.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
7. Morohaku, K., Pelton, S.H., Daugherty, D.J., Butler, W.R., Deng, W. and Selvaraj, V. (2014) Translocator protein/peripheral benzodiazepine receptor is not required for steroid hormone biosynthesis. Endocrinology 155, 89-97 CrossRef PubMed
8. Šileikytė, J., Blachly-Dyson, E., Sewell, R., Carpi, A., Menabò, 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
9. Stocco, D.M. (2014) The role of PBR/TSPO in steroid biosynthesis challenged. Endocrinology 155, 6-9 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 knockout mice are viable with no effects on steroid hormone biosynthesis. J. Biol. Chem. 289, 27444-27454 CrossRef PubMed
11. Domazet-Loso, T. and Tautz, D. (2008) An ancient evolutionary origin of genes associated with human genetic diseases. Mol. Biol. Evol. 25, 2699-2707 CrossRef PubMed
12. 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 CrossRef PubMed
13. Rupprecht, R., Papadopoulos, V., Rammes, G., Baghai, T.C., Fan, J., Akula, N., Groyer, G., Adams, D. and Schumacher, M. (2010) Translocator protein (18 kDa) (TSPO) as a therapeutic target for neurological and psychiatric disorders. Nat. Rev. Drug. Discov. 9, 971-988 CrossRef PubMed
14. Da Pozzo, E., Costa, B. and Martini, C (2012) Translocator protein (TSPO) and neurosteroids: implications in psychiatric disorders. Curr. Mol. Med. 12, 426-442 PubMed
15. Batarseh, A. and Papadopoulos, V. (2010) Regulation of translocator protein 18 kDa (TSPO) expression in health and disease states. Mol. Cell. Endocrinol. 327, 1-12 CrossRef PubMed
16. Taliani, S., Pugliesi, I. and Da Settimo, F. (2011) Structural requirements to obtain highly potent and selective 18 kDa Translocator Protein (TSPO) Ligands. Curr. Top. Med. Chem. 11, 860-886 CrossRef PubMed
17. Owen, D.R. and Matthews, P.M. (2011) Imaging brain microglial activation using positron emission tomography and translocator protein-specific radioligands. Int. Rev. Neurobiol. 101, 19-39 CrossRef PubMed
18. Trapani, A., Palazzo, C., de Candia, M., Lasorsa, F.M. and Trapani, G. (2013) Targeting of the translocator protein 18 kDa (TSPO): a valuable approach for nuclear and optical imaging of activated microglia. Bioconjug. Chem. 24, 1415-1428 CrossRef PubMed
19. Benavides, J., Fage, D., Carter, C. and Scatton, B. (1987) Peripheral type benzodiazepine binding sites are a sensitive indirect index of neuronal damage. Brain Res. 421, 167-172 CrossRef PubMed
20. Girard, C., Liu, S., Adams, D., Lacroix, C., Sinéus, M., Boucher, C., Papadopoulos, V., Rupprecht, R., Schumacher, M. and Groyer, G. (2012) Axonal regeneration and neuroinflammation: roles for the translocator protein 18 kDa. J. Neuroendocrinol. 24, 71-81 CrossRef PubMed
21. Chen, M.K. and Guilarte, T.R. (2008) Translocator protein 18-kDa (TSPO): molecular sensor of brain injury and repair. Pharmacol. Ther. 118, 1-17 CrossRef PubMed
22. Bailey, S.L., Carpentier, P.A., McMahon, E.J., Begolka, W.S. and Miller, S.D. (2006) Innate and adaptive immune responses of the central nervous system. Crit. Rev. Immunol. 26, 149-188 CrossRef PubMed
23. Streit, W.J., Mrak, R.E. and Griffin, W.S.T. (2004) Microglia and neuroinflammation: a pathological perspective. J. Neuroinflammation 1, 1-4 CrossRef PubMed
24. Papadopoulos, V. and Lecanu, L. (2009) Translocator protein (18 kDa) TSPO: an emerging therapeutic target in neurotrauma. Exp. Neurol. 219, 53-57 CrossRef PubMed
25. Girard, C., Liu, S., Cadepond, F., Adams, D., Lacroix, C., Verleye, M., Gillardin, J.M., Baulieu, E.E., Schumacher, M. and Schweizer-Groyer, G. (2008) Etifoxine improves peripheral nerve regeneration and functional recovery. Proc. Natl. Acad. Sci. U.S.A. 105, 20505-20510 CrossRef PubMed
26. Soustiel, J.F., Zaaroor, M., Vlodavsky, E., Veenman, L., Weizman, A. and Gavish, M. (2008) Neuroprotective effect of Ro5-4864 following brain injury. Exp. Neurol. 214, 201-208 CrossRef PubMed
27. Zipp, F. and Aktas, O. (2006) The brain as a target of inflammation: common pathways link inflammatory and neurodegenerative diseases. Trends Neurosci. 29, 518-527 CrossRef PubMed
28. Ching, A.S., Kuhnast, B., Damont, A., Roeda, D., Tavitian, B. and Dollé, F. (2012) Current paradigm of the 18-kDa translocator protein (TSPO) as a molecular target for PET imaging in neuroinflammation and neurodegenerative diseases. Insights Imaging 3, 111-119 CrossRef PubMed
29. Chauveau, F., Boutin, H., Van Camp, N., Dollé, 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
30. Tarnok, K., kiss, E., Luiten, P.G.M., Nyakas, C., Tihanyi, K., Schlett, K. and Eisel, U.L.M. (2008) Effects of Vinpocetine on mitochondrial function and neuroprotection in primary cortical neurons. Neurochem. Int. 53, 289-295 CrossRef PubMed
31. Ferzaz, B., Brault, E., Bourliaud, G., Robert, J.P., Poughon, G., Claustre, Y., Marguet, F., Liere, P., Schumacher, M., Nowicki, J.P. et al. (2002) SSR180575 (7-chloro-N,N,5-trimethyl-4-oxo-3-phenyl-3,5-dihydro-4H-pyridazino[4,5-b]indole-1-acetamide), a peripheral benzodiazepine receptor ligand, promotes neuronal survival and repair. J. Pharmacol. Exp. Ther. 301, 1067-1078 CrossRef PubMed
32. Bordet, T., Buisson, B., Michaud, M., Drouot, C., Galéa, P., Delaage, P., Akentieva, N.P., Evers, A.S., Covey, D.F., Ostuni, M.A. et al. (2007) Identification and characterization of cholest-4-en-3-one, oxime (TRO19622), a novel drug candidate for amyotrophic lateral sclerosis. J. Pharmacol. Exp. Ther. 322, 709-720 CrossRef PubMed
33. Veiga, S., Azcoitia, I. and Garcia-Segura, L.M. (2005) Ro5-4864, a peripheral benzodiazepine receptor ligand, reduces reactive gliosis and protects hippocampal hilar neurons from kainic acid excitotoxicity. J. Neurosci. Res. 80, 129-137 CrossRef PubMed
34. Leaver, K.R., Reynolds, A., Bodard, S., Guilloteau, D., Chalon, S. and Kassiou, M. (2012) Effects of translocator protein (18 kDa) ligands on microglial activation and neuronal death in the quinolinic-acid-injected rat striatum. ACS Chem. Neurosci. 3, 114-119 CrossRef PubMed
35. Ryu, J.K., Choi, H.B. and McLarnon, J.G. (2005) Peripheral benzodiazepine receptor ligand PK11195 reduces microglial activation and neuronal death in quinolinic acid-injected rat striatum. Neurobiol. Dis. 20, 550-561 CrossRef PubMed
36. Daugherty, D.J., Selvaraj, V., Chechneva, O.V., Liu, X.B., Pleasure, D.E. and Deng, W. (2013) A TSPO ligand is protective in a mouse model of multiple sclerosis. EMBO Mol. Med. 5, 891-903 CrossRef PubMed
37. Sunyach, C., Michaud, M., Arnoux, T., Bernard-Marissal, N., Aebischer, J., Latyszenok, V., Gouarné, C., Raoul, C., Pruss, R.M., Bordet, T. and Pettmann, B. (2012) Olesoxime delays muscle denervation, astrogliosis, microglial activation and motoneuron death in an ALS mouse model. Neuropharmacology 62, 2346-2352 CrossRef PubMed
38. Lenglet, T., Lacomblez, L., Abitbol, J.L., Ludolph, A., Mora, J.S., Robberecht, W., Shaw, P.J., Pruss, R.M., Cuvier, V. and Meininger, V. (2014) Mitotarget study group. A phase II-III trial of olesoxime in subjects with amyotrophic lateral sclerosis. Eur. J. Neurol. 21, 529-536 CrossRef PubMed
39. Barron, A.M., Garcia-Segura, L.M., Caruso, D., Jayaraman, A., Lee, J.W., Melcangi, R.C. and Pike, C.J. (2013) Ligand for translocator protein reverses pathology in a mouse model of Alzheimer's disease. J. Neurosci. 33, 8891-8897 CrossRef PubMed
40. Choi, H.B., Khoo, C., Ryu, J.K., van Breemen, E., Kim, S.U. and McLarnon, J.G. (2002) Inhibition of lipopolysaccharide-induced cyclooxygenase-2, tumor necrosis factor-alpha and [Ca2+]i responses in human microglia by the peripheral benzodiazepine receptor ligand PK11195. J. Neurochem. 83, 546-555 CrossRef PubMed
41. Hong, S.H., Choi, H.B., Kim, S.U. and McLarnon, J.G. (2006) Mitochondrial ligand inhibits store-operated calcium influx and COX-2 production in human microglia. J. Neurosci. Res. 83, 1293-1298 CrossRef PubMed
42. Choi, J., Ifuku, M., Noda, M. and Guilarte, T.R. (2011) Translocator protein (18 kDa)/peripheral benzodiazepine receptor specific ligands induce microglia functions consistent with an activated state. Glia 59, 219-230 CrossRef PubMed
43. Wilms, H., Claasen, J., Röhl, C., Sievers, J., Deuschl, G. and Lucius, R. (2003) Involvement of benzodiazepine receptors in neuroinflammatory and neurodegenerative diseases: evidence from activated microglial cells in vitro. Neurobiol. Dis. 14, 417-424 CrossRef PubMed
44. Bae, K.R., Shim, H.J., Balu, D., Kim, S.R. and Yu, S.W. (2014) Translocator protein 18 kDa negatively regulates inflammation in microglia. J. Neuroimmune Pharmacol. 9, 424-437 CrossRef PubMed
45. Karlstetter, M., Nothdurfter, C., Aslanidis, A., Moeller, K., Horn, F., Scholz, R., Neumann, H., Weber, B.H., Rupprecht, R. and Langmann, T. (2014) Translocator protein (18 kDa) (TSPO) is expressed in reactive retinal microglia and modulates microglial inflammation and phagocytosis. J. Neuroinflammation 11, 3 CrossRef PubMed
46. Zhao, Y.Y., Yu, J.Z., Li, Q.Y., Ma, C.G., Lu, C.Z. and Xiao, B.G. (2011) TSPO-specific ligand vinpocetine exerts a neuroprotective effect by suppressing microglial inflammation. Neuron Glia Biol. 7, 187-197 CrossRef PubMed
47. Veiga, S., Carrero, P., Pernia, O., Azcoitia, I. and Garcia-Segura, L.M. (2007) Translocator protein 18 kDa is involved in the regulation of reactive gliosis. Glia 55, 1426-1436 CrossRef PubMed
48. Naseem, M. and Parvez, S. (2014) Role of melatonin in traumatic brain injury and spinal cord injury. Scientific World J. Article ID 586270
49. Corbett, D., Larsen, J. and Langdon, K.D. (2008) Diazepam delays the death of hippocampal CA1 neurons following global ischemia. Exp. Neurol. 214, 309-314 CrossRef PubMed
50. Sarnowska, A., Beresewicz, M., Zabłocka, B. and Domańska-Janik, K. (2009) Diazepam neuroprotection in excitotoxic and oxidative stress involves a mitochondrial mechanism additional to the GABAAR and hypothermic effects. Neurochem. Int. 55, 164-173 CrossRef PubMed