Guwiyang Wurra - 'Fire Mouse': A global gene knockout model for TSPO/PBR drug development, loss-of-function and mechanisms of compensation studies

Biochemical Society Transactions

Volumn 43, Issue , 2015, Pages 553-558

  Middleton, Ryan J ^a   Liu, Guo Jun ^a,b   Banati, Richard B ^a,b  

^a AUSTRALIAN NUCLEAR SCIENCE AND TECHNOLOGY ORGANISATION   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Compound development; Energy; Knockout; Metabolism; Mitochondria; TSPO PBR

Indexed keywords

BENZODIAZEPINE RECEPTOR; CARRIER PROTEIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PERIPHERAL BENZODIAZEPINE RECEPTOR; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; 6-CHLORO-2-(4'-IODOPHENYL)-3-(N,N-DIETHYL)IMIDAZO(1,2-A)PYRIDINE-3-ACETAMIDE; BZRP PROTEIN, MOUSE; FUSED HETEROCYCLIC RINGS; ISOQUINOLINE DERIVATIVE; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; STEROID;

DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG DEVELOPMENT; ENERGY METABOLISM; GENE INACTIVATION; GUWIYANG WURRA; KNOCKOUT MOUSE; LOSS OF FUNCTION MUTATION; MITOCHONDRIAL PERMEABILITY; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; STEROIDOGENESIS; ANIMAL; BIOSYNTHESIS; DISEASE MODEL; GENETICS; INFLAMMATION; METABOLISM; MITOCHONDRION; MUTATION; NEURODEGENERATIVE DISEASES;

MUS;

ANIMALS; BRIDGED BICYCLO COMPOUNDS, HETEROCYCLIC; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; INFLAMMATION; ISOQUINOLINES; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MUTATION; NEURODEGENERATIVE DISEASES; RECEPTORS, GABA; STEROIDS;

EID: 84938810813     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20150039     Document Type: Review

References (46)

1. 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
2. Gut, P., Baeza-Raja, B., Andersson, O., Hasenkamp, L., Hsiao, J., Hesselson, D., Akassoglou, K., Verdin, E., Hirschey, M.D. and Stainier, D.Y. (2013) Whole-organism screening for gluconeogenesis identifies activators of fasting metabolism. Nat. Chem. Biol. 9, 97-104 CrossRef PubMed
3. 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
4. Krueger, K.E. and Papadopoulos, V. (1990) Peripheral-type benzodiazepine receptors mediate translocation of cholesterol from outer to inner mitochondrial membranes in adrenocortical cells. J. Biol. Chem. 265, 15015-15022 PubMed
5. 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
6. 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
7. 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
8. 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
9. Scarf, A.M., Auman, K.M. and Kassiou, M. (2012) Is there any correlation between binding and functional effects at the translocator protein (TSPO) (18 kDa)? Curr. Mol. Med. 12, 387-397 PubMed
10. 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
11. Halestrap, A.P. (2009) What is the mitochondrial permeability transition pore? J. Mol. Cell Cardiol. 46, 821-831 CrossRef PubMed
12. Bernardi, P. (2013) The mitochondrial permeability transition pore: a mystery solved? Front. Physiol. 4, 95
13. 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
14. Pastorino, J.G., Simbula, G., Gilfor, E., Hoek, J.B. and Farber, J.L. (1994) Protoporphyrin IX, an endogenous ligand of the peripheral benzodiazepine receptor, potentiates induction of the mitochondrial permeability transition and the killing of cultured hepatocytes by rotenone. J. Biol. Chem. 269, 31041-31046 PubMed
15. Chelli, B., Falleni, A., Salvetti, F., Gremigni, V., Lucacchini, A. and Martini, C. (2001) Peripheral-type benzodiazepine receptor ligands: mitochondrial permeability transition induction in rat cardiac tissue. Biochem. Pharmacol. 61, 695-705 CrossRef PubMed
16. Li, J., Wang, J. and Zeng, Y. (2007) Peripheral benzodiazepine receptor ligand, PK11195 induces mitochondria cytochrome c release and dissipation of mitochondria potential via induction of mitochondria permeability transition. Eur. J. Pharmacol. 560, 117-122 CrossRef PubMed
17. Azarashvili, T., Grachev, D., Krestinina, O., Evtodienko, Y., Yurkov, I., Papadopoulos, V. and Reiser, G. (2007) The peripheral-type benzodiazepine receptor is involved in control of Ca2 + -induced permeability transition pore opening in rat brain mitochondria. Cell Calcium 42, 27-39 CrossRef PubMed
18. Krauskopf, A., Eriksson, O., Craigen, W.J., Forte, M.A. and Bernardi, P. (2006) Properties of the permeability transition in VDAC1(-/-) mitochondria. Biochim. Biophys. Acta 1757, 590-595 CrossRef PubMed
19. Baines, C.P., Kaiser, R.A., Sheiko, T., Craigen, W.J. and Molkentin, J.D. (2007) Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat. Cell Biol. 9, 550-555 CrossRef PubMed
20. Kokoszka, J.E., Waymire, K.G., Levy, S.E., Sligh, J.E., Cai, J., Jones, D.P., MacGregor, G.R. and Wallace, D.C. (2004) The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427, 461-465 CrossRef PubMed
21. Giorgio, V., von Stockum, S., Antoniel, M., Fabbro, A., Fogolari, F., Forte, M., Glick, G.D., Petronilli, V., Zoratti, M., Szabo, I. et al. (2013) Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc. Natl. Acad. Sci. U.S.A. 110, 5887-5892 CrossRef PubMed
22. Okuno, D., Iino, R. and Noji, H. (2011) Rotation and structure of FoF1-ATP synthase. J. Biochem. 149, 655-664 CrossRef PubMed
23. Cleary, J., Johnson, K.M., Opipari, Jr, A.W. and Glick, G.D. (2007) Inhibition of the mitochondrial F1F0-ATPase by ligands of the peripheral benzodiazepine receptor. Bioorg. Med. Chem. Lett. 17, 1667-1670 CrossRef PubMed
24. Seneviratne, M.S., Faccenda, D., De Biase, V. and Campanella, M. (2012) PK11195 inhibits mitophagy targeting the F1Fo-ATPsynthase in Bcl-2 knock-down cells. Curr. Mol. Med. 12, 476-482 PubMed
25. Krestinina, O.V., Grachev, D.E., Odinokova, I.V., Reiser, G., Evtodienko, Y.V. and Azarashvili, T.S. (2009) Effect of peripheral benzodiazepine receptor (PBR/TSPO) ligands on opening of Ca2 + -induced pore and phosphorylation of 3.5-kDa polypeptide in rat brain mitochondria. Biochem. Mosc. 74, 421-429 CrossRef
26. Veenman, L., Alten, J., Linnemannstons, K., Shandalov, Y., Zeno, S., Lakomek, M., Gavish, M. and Kugler, W. (2010) Potential involvement of F0F1-ATP(synth)ase and reactive oxygen species in apoptosis induction by the antineoplastic agent erucylphosphohomocholine in glioblastoma cell lines : a mechanism for induction of apoptosis via the 18 kDa mitochondrial translocator protein. Apoptosis 15, 753-768 CrossRef PubMed
27. 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 PubMed
28. Li, H. and Papadopoulos, V. (1998) Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern. Endocrinology 139, 4991-4997 PubMed
29. Papadopoulos, V., Amri, H., Li, H., Boujrad, N., Vidic, B. and Garnier, M. (1997) Targeted disruption of the peripheral-type benzodiazepine receptor gene inhibits steroidogenesis in the R2C Leydig tumor cell line. J. Biol. Chem. 272, 32129-32135 CrossRef PubMed
30. 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 CrossRef PubMed
31. Hauet, T., Yao, Z.X., Bose, H.S., Wall, C.T., Han, Z., Li, W., Hales, D.B., Miller, W.L., Culty, M. and Papadopoulos, V. (2005) Peripheral-type benzodiazepine receptor-mediated action of steroidogenic acute regulatory protein on cholesterol entry into leydig cell mitochondria. Mol. Endocrinol. 19, 540-554 CrossRef PubMed
32. Tu, L.N., Zhao, A.H., Stocco, D.M. and Selvaraj, V. (2014) PK11195 effect on steroidogenesis is not mediated through the translocator protein (TSPO). Endocrinology en20141707
33. Le Fur, G., Perrier, M.L., Vaucher, N., Imbault, F., Flamier, A., Benavides, J., Uzan, A., Renault, C., Dubroeucq, M.C. and Gueremy, C. (1983) Peripheral benzodiazepine binding sites: effect of PK 11195, 1-(2-chlorophenyl)-N-methyl-N-(1-methylpropyl)-3-isoquinolinecarboxamide. I. In vitro studies. Life Sci. 32, 1839-1847 CrossRef PubMed
34. Caballero, B., Veenman, L., Bode, J., Leschiner, S. and Gavish, M. (2014) Concentration-dependent bimodal effect of specific 18 kDa translocator protein (TSPO) ligands on cell death processes induced by ammonium chloride: potential implications for neuropathological effects due to hyperammonemia. CNS Neurol. Disord. Drug Targets 13, 574-592 CrossRef PubMed
35. Hatty, C.R., Le Brun, A.P., Lake, V., Clifton, L.A., Liu, G.J., James, M. and Banati, R.B. (2014) Investigating the interactions of the 18kDa translocator protein and its ligand PK11195 in planar lipid bilayers. Biochim. Biophys. Acta 1838, 1019-1030 CrossRef PubMed
36. Yeliseev, A.A., Krueger, K.E. and Kaplan, S. (1997) A mammalian mitochondrial drug receptor functions as a bacterial "oxygen" sensor. Proc. Natl. Acad. Sci. U.S.A. 94, 5101-5106 CrossRef PubMed
37. 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 PubMed
38. Larcher, J.C., Vayssiere, J.L., Le Marquer, F.J., Cordeau, L.R., Keane, P.E., Bachy, A., Gros, F. and Croizat, B.P. (1989) Effects of peripheral benzodiazepines upon the O2 consumption of neuroblastoma cells. Eur. J. Pharmacol. 161, 197-202 CrossRef PubMed
39. 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 PubMed
40. Lin, R., Angelin, A., Da Settimo, F., Martini, C., Taliani, S., Zhu, S. and Wallace, D.C. (2014) Genetic analysis of dTSPO, an outer mitochondrial membrane protein, reveals its functions in apoptosis, longevity, and Ab42-induced neurodegeneration. Aging Cell 13, 507-518 CrossRef PubMed
41. Lin, M.T. and Beal, M.F. (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787-795 CrossRef PubMed
42. Bournat, J.C. and Brown, C.W. (2010) Mitochondrial dysfunction in obesity. Curr. Opin. Endocrinol. Diabetes Obes. 17, 446-452 CrossRef PubMed
43. Scaglia, F. (2010) The role of mitochondrial dysfunction in psychiatric disease. Dev. Disabil. Res. Rev. 16, 136-143 CrossRef PubMed
44. Boland, M.L., Chourasia, A.H. and Macleod, K.F. (2013) Mitochondrial dysfunction in cancer. Front. Oncol. 3, 292 CrossRef PubMed
45. Lopez-Armada, M.J., Riveiro-Naveira, R.R., Vaamonde-Garcia, C. and Valcarcel-Ares, M.N. (2013) Mitochondrial dysfunction and the inflammatory response. Mitochondrion 13, 106-118 CrossRef PubMed
46. Gatliff, J., East, D., Crosby, J., Abeti, R., Harvey, R., Craigen, W., Parker, P. and Campanella, M. (2014) TSPO interacts with VDAC1 and triggers a ROS-mediated inhibition of mitochondrial quality control. Autophagy 10, 2279-2296 CrossRef PubMed