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Reports

Functional gains in energy and cell metabolism after TSPO gene insertion

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Pages 436-447 | Received 03 Oct 2016, Accepted 05 Jan 2017, Published online: 10 Feb 2017

References

  • Eshleman AJ, Murray TF. Differential binding properties of the peripheral-type benzodiazepine ligands [3H]PK 11195 and [3H]Ro 5-4864 in trout and mouse brain membranes. J Neurochem 1989; 53:494-502; PMID:2746235; http://dx.doi.org/10.1111/j.1471-4159.1989.tb07361.x
  • Fan J, Lindemann P, Feuilloley MG, Papadopoulos V. Structural and functional evolution of the translocator protein (18 kDa). Curr Mol Med 2012; 12:369-86; PMID:22364126
  • Snyder MJ, Van Antwerpen R. Evidence for a diazepam-binding inhibitor (DBI) benzodiazepine receptor-like mechanism in ecdysteroidogenesis by the insect prothoracic gland. Cell Tissue Res 1998; 294:161-8; PMID:9724466; http://dx.doi.org/10.1007/s004410051166
  • Papadopoulos V, Baraldi M, Guilarte TR, Knudsen TB, Lacapere JJ, Lindemann P, Norenberg MD, Nutt D, Weizman A, Zhang MR, et al. Translocator protein (18kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 2006; 27:402-9; PMID:16822554; http://dx.doi.org/10.1016/j.tips.2006.06.005
  • Antkiewicz-Michaluk L, Guidotti A, Krueger KE. Molecular characterization and mitochondrial density of a recognition site for peripheral-type benzodiazepine ligands. Mol Pharmacol 1988; 34:272-8. PMID: 2843747
  • Guo Y, Kalathur RC, Liu Q, Kloss B, Bruni R, Ginter C, Kloppmann E, Rost B, Hendrickson WA. Structure and activity of tryptophan-rich TSPO proteins. Science 2015; 347:551-5; PMID:25635100; http://dx.doi.org/10.1126/science.aaa1534
  • Jaremko L, Jaremko M, Giller K, Becker S, Zweckstetter M. Structure of the mitochondrial translocator protein in complex with a diagnostic ligand. Science 2014; 343:1363-6; PMID:24653034; http://dx.doi.org/10.1126/science.1248725
  • Li F, Liu J, Zheng Y, Garavito RM, Ferguson-Miller S. Crystal structures of translocator protein (TSPO) and mutant mimic of a human polymorphism. Science 2015; 347:555-8; PMID:25635101; http://dx.doi.org/10.1126/science.1260590
  • Veenman L, Alten J, Linnemannstons K, Shandalov Y, Zeno S, Lakomek M, Gavish M, Kugler W. 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 2010; 15:753-68; PMID:20107899; http://dx.doi.org/10.1007/s10495-010-0460-5
  • Veenman L, Gavish M. The role of 18 kDa mitochondrial translocator protein (TSPO) in programmed cell death, and effects of steroids on TSPO expression. Curr Mol Med 2012; 12:398-412; PMID:22348610
  • Zeno S, Veenman L, Katz Y, Bode J, Gavish M, Zaaroor M. The 18 kDa mitochondrial translocator protein (TSPO) prevents accumulation of protoporphyrin IX. Involvement of reactive oxygen species (ROS). Curr Mol Med 2012; 12:494-501; PMID:22376065
  • Papadopoulos V, Amri H, Boujrad N, Cascio C, Culty M, Garnier M, Hardwick M, Li H, Vidic B, Brown AS, et al. Peripheral benzodiazepine receptor in cholesterol transport and steroidogenesis. Steroids 1997; 62:21-8; PMID:9029710; http://dx.doi.org/10.1016/S0039-128X(96)00154-7
  • Liu GJ, Middleton RJ, Hatty CR, Kam WW, Chan R, Pham T, Harrison-Brown M, Dodson E, Veale K, Banati RB. The 18 kDa translocator protein, microglia and neuroinflammation. Brain Pathol 2014; 24:631-53; PMID:25345894; http://dx.doi.org/10.1111/bpa.12196
  • Banati RB, Middleton RB, Chan R, Hatty CR, Kam WWY, Quin C, Graeber MB, Parmar A, Zahra D, Callaghan P, et al. Positron emission tomography and functional characterization of a complete PBR/TSPO-knockout. Nat Commun 2014; 5:5452; PMID:25406832; http://dx.doi.org/10.1038/ncomms6452
  • Morohaku K, Pelton SH, Daugherty DJ, Butler WR, Deng W, Selvaraj V. Translocator protein/peripheral benzodiazepine receptor is not required for steroid hormone biosynthesis. Endocrinology 2014; 155:89-97; PMID:24174323; http://dx.doi.org/10.1210/en.2013-1556
  • Sileikyte J, Blachly-Dyson E, Sewell R, Carpi A, Menabo R, Di Lisa F, Ricchelli F, Bernardi P, Forte M. Regulation of the mitochondrial permeability transition pore by the outer membrane does not involve the Peripheral Benzodiazepine Receptor (TSPO). J Biol Chem 2014; 289:13769-81; PMID:24692541; http://dx.doi.org/10.1074/jbc.M114.549634
  • Tu LN, Morohaku K, Manna PR, Pelton SH, Butler WR, Stocco DM, Selvaraj V. Peripheral Benzodiazepine Receptor/Translocator protein global knockout mice are viable with no effects on steroid hormone biosynthesis. J Biol Chem 2014; 289:27444-54; PMID:24936060; http://dx.doi.org/10.1074/jbc.M114.578286
  • Gut P, Zweckstetter M, Banati RB. Lost in translocation: the functions of the 18-kD translocator protein. Trends Endocrinol Metab 2015; 26:349-56; PMID:26026242; http://dx.doi.org/10.1016/j.tem.2015.04.001
  • Middleton RJ, Liu G-J, Banati RB. Guwiyang Wurra–‘Fire Mouse’: a global gene knockout model for TSPO/PBR drug development, loss-of-function and mechanisms of compensation studies. Biochem Soc Trans 2015; 43:553-8; PMID:26551692; http://dx.doi.org/10.1042/BST20150039
  • Middleton RJ, Liu GJ, Banati RB. Epigenetic silencing of the human 18 kDa translocator protein (TSPO) in a T-cell leukemia cell line. DNA Cell Biol 2017; 36:103-8; PMID:28004979; http://dx.doi.org/10.1089/dna.2016.3385
  • Bertomeu T, Zvereff V, Ibrahim A, Zehntner S, Aliaga A, Rosa-Neto P, Bedell B, Falardeau P, Gourdeau H. TLN-4601 peripheral benzodiazepine receptor (PBR/TSPO) binding properties do not mediate apoptosis but confer tumor-specific accumulation. Biochem pharmacol 2010; 80:1572-9; PMID:20655882; http://dx.doi.org/10.1016/j.bcp.2010.07.018
  • Bribes E, Carriere D, Goubet C, Galiegue S, Casellas P, Simony-Lafontaine J. Immunohistochemical assessment of the peripheral benzodiazepine receptor in human tissues. J Histochem Cytochem 2004; 52:19-28; PMID:14688214; http://dx.doi.org/10.1177/002215540405200103
  • Hardwick M, Fertikh D, Culty M, Li H, Vidic B, Papadopoulos V. 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 1999; 59:831-42; PMID:10029072
  • Le Fur G, Vaucher N, Perrier M, Flamier A, Benavides J, Renault C, Dubroeucq M, Gueremy C, Uzan A. Differentiation between two ligands for peripheral benzodiazepine binding sites,[3 H] R05-4864 and [3 H] PK 11195, by thermodynamic studies. Life Sci 1983; 33:449-57; PMID:6308375; http://dx.doi.org/10.1016/0024-3205(83)90794-4
  • Hardwick M, Cavalli LR, Barlow KD, Haddad BR, Papadopoulos V. Peripheral-type benzodiazepine receptor (PBR) gene amplification in MDA-MB-231 aggressive breast cancer cells. Cancer Genet Cytogenet 2002; 139:48-51; PMID:12547158; http://dx.doi.org/10.1016/S0165-4608(02)00604-0
  • Lacapere JJ, Papadopoulos V. Peripheral-type benzodiazepine receptor: structure and function of a cholesterol-binding protein in steroid and bile acid biosynthesis. Steroids 2003; 68:569-85; PMID:12957662; http://dx.doi.org/10.1016/S0039-128X(03)00101-6
  • Brown RC, Degenhardt B, Kotoula M, Papadopoulous V. Location-dependent role of the human glioma cell peripheral-type benzodiazepine receptor in proliferation and steroid biosynthesis. Cancer Lett 2000; 156:125-32; PMID:10880761; http://dx.doi.org/10.1016/S0304-3835(00)00451-1
  • Alvarez-Maubecin V, Garcia-Hernandez F, Williams JT, Van Bockstaele EJ. Functional coupling between neurons and glia. J Neurosci 2000; 20:4091-8; PMID:10818144
  • Gut P, Baeza-Raja B, Andersson O, Hasenkamp L, Hsiao J, Hesselson D, Akassoglou K, Verdin E, Hirschey MD, Stainier DYR. Whole-organism screening for gluconeogenesis identifies activators of fasting metabolism. Nat Chem Biol 2013; 9:97-104; PMID:23201900; http://dx.doi.org/10.1038/nchembio.1136
  • Xiao J, Liang D, Zhang H, Liu Y, Li F, Chen YH. 4′-Chlorodiazepam, a translocator protein (18 kDa) antagonist, improves cardiac functional recovery during postischemia reperfusion in rats. Exp Biol Med (Maywood) 2010; 235:478-86; PMID:20407080; http://dx.doi.org/10.1258/ebm.2009.009291
  • Kugler W, Veenman L, Shandalov Y, Leschiner S, Spanier I, Lakomek M, Gavish M. Ligands of the mitochondrial 18 kDa translocator protein attenuate apoptosis of human glioblastoma cells exposed to erucylphosphohomocholine. Cell Oncol 2008; 30:435-50; PMID:18791274
  • Veenman L, Papadopoulos V, Gavish M. Channel-like functions of the 18-kDa translocator protein (TSPO): regulation of apoptosis and steroidogenesis as part of the host-defense response. Curr Pharm Des 2007; 13:2385-405; PMID:17692008; http://dx.doi.org/10.2174/138161207781368710
  • Zeno S, Zaaroor M, Leschiner S, Veenman L, Gavish M. CoCl(2) induces apoptosis via the 18 kDa translocator protein in U118MG human glioblastoma cells. Biochemistry 2009; 48:4652-61; PMID:19358520; http://dx.doi.org/10.1021/bi900064t
  • Gavish M, Bachman I, Shoukrun R, Katz Y, Veenman L, Weisinger G, Weizman A. Enigma of the peripheral benzodiazepine receptor. Pharmacol Rev 1999; 51:629-50; PMID:10581326
  • Veenman L, Gavish M. The peripheral-type benzodiazepine receptor and the cardiovascular system. Implications for drug development. Pharmacol Ther 2006; 110:503-24; PMID:16337685; http://dx.doi.org/10.1016/j.pharmthera.2005.09.007
  • Carayon P, Portier M, Dussossoy D, Bord A, Petitpretre G, Canat X, Le Fur G, Casellas P. Involvement of peripheral benzodiazepine receptors in the protection of hematopoietic cells against oxygen radical damage. Blood 1996; 87:3170-8; PMID:8605331
  • Banati RB. Visualising microglial activation in vivo. Glia 2002; 40:206-17; PMID:12379908; http://dx.doi.org/10.1002/glia.10144
  • Banati RB. Neuropathological imaging: in vivo detection of glial activation as a measure of disease and adaptive change in the brain. Br Med Bull 2003; 65:121-31; PMID:12697620; http://dx.doi.org/10.1093/bmb/65.1.121
  • Banati RB, Cagnin A, Brooks DJ, Gunn RN, Myers R, Jones T, Birch R, Anand P. Long-term trans-synaptic glial responses in the human thalamus after peripheral nerve injury. Neuroreport 2001; 12:3439-42; PMID:11733686; http://dx.doi.org/10.1097/00001756-200111160-00012
  • Banati RB, Goerres GW, Tjoa C, Aggleton JP, Grasby P. The functional anatomy of visual-tactile integration in man: a study using positron emission tomography. Neuropsychologia 2000; 38:115-24; PMID:10660224; http://dx.doi.org/10.1016/S0028-3932(99)00074-3
  • Cagnin A, Brooks DJ, Kennedy AM, Gunn RN, Myers R, Turkheimer FE, Jones T, Banati RB. In-vivo measurement of activated microglia in dementia. Lancet 2001; 358:461-7; PMID:11513911; http://dx.doi.org/10.1016/S0140-6736(01)05625-2
  • Cagnin A, Myers R, Gunn RN, Lawrence AD, Stevens T, Kreutzberg GW, Jones T, Banati RB. In vivo visualization of activated glia by [11C] (R)-PK11195-PET following herpes encephalitis reveals projected neuronal damage beyond the primary focal lesion. Brain 2001; 124:2014-27; PMID:11571219; http://dx.doi.org/10.1093/brain/124.10.2014
  • Kuhlmann AC, Guilarte TR. Cellular and subcellular localization of peripheral benzodiazepine receptors after trimethyltin neurotoxicity. J Neurochem 2000; 74:1694-704; PMID:10737628; http://dx.doi.org/10.1046/j.1471-4159.2000.0741694.x
  • Pedersen MD, Minuzzi L, Wirenfeldt M, Meldgaard M, Slidsborg C, Cumming P, Finsen B. Up-regulation of PK11195 binding in areas of axonal degeneration coincides with early microglial activation in mouse brain. Eur J Neurosci 2006; 24:991-1000; PMID:16930426; http://dx.doi.org/10.1111/j.1460-9568.2006.04975.x
  • Venneti S, Lopresti BJ, Wiley CA. The peripheral benzodiazepine receptor (Translocator protein 18kDa) in microglia: from pathology to imaging. Prog Neurobiol 2006; 80:308-22; PMID:17156911; http://dx.doi.org/10.1016/j.pneurobio.2006.10.002
  • Wilms H, Claasen J, Rohl C, Sievers J, Deuschl G, Lucius R. Involvement of benzodiazepine receptors in neuroinflammatory and neurodegenerative diseases: evidence from activated microglial cells in vitro. Neurobiol Dis 2003; 14:417-24; PMID:14678758; http://dx.doi.org/10.1016/j.nbd.2003.07.002
  • Tu LN, Zhao AH, Stocco DM, Selvaraj V. PK11195 effect on steroidogenesis is not mediated through the translocator protein (TSPO). Endocrinology 2015; 156:1033-39; PMID:25535830; http://dx.doi.org/10.1210/en.2014-1707
  • Costa B, Salvetti A, Rossi L, Spinetti F, Lena A, Chelli B, Rechichi M, Da Pozzo E, Gremigni V, Martini C. Peripheral Benzodiazepine Receptor: Characterization in Human T-Lymphoma Jurkat Cells. Mol Pharmacol 2006; 69:37-44; PMID:16189298
  • Choi J, Ifuku M, Noda M, Guilarte TR. Translocator protein (18 kDa)/peripheral benzodiazepine receptor specific ligands induce microglia functions consistent with an activated state. Glia 2011; 59:219-30; PMID:21125642; http://dx.doi.org/10.1002/glia.21091
  • Eckert GP, Schiborr C, Hagl S, Abdel-Kader R, Muller WE, Rimbach G, Frank J. Curcumin prevents mitochondrial dysfunction in the brain of the senescence-accelerated mouse-prone 8. Neurochem Int 2013; 62:595-602; PMID:23422877; http://dx.doi.org/10.1016/j.neuint.2013.02.014
  • Krestinina OV, Grachev DE, Odinokova IV, Reiser G, Evtodienko YV, Azarashvili TS. 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. Biochemistry (Mosc) 2009; 74:421-9; PMID:19463096; http://dx.doi.org/10.1134/S0006297909040105
  • Rosenberg N, Rosenberg O, Weizman A, Veenman L, Gavish M. In vitro catabolic effect of protoporphyrin IX in human osteoblast-like cells: possible role of the 18 kDa mitochondrial translocator protein. J Bioenerg Biomembr 2013; 45:333-41; PMID:23475134; http://dx.doi.org/10.1007/s10863-013-9501-4
  • Seneviratne MS, Faccenda D, De Biase V, Campanella M. PK11195 inhibits mitophagy targeting the F1Fo-ATPsynthase in Bcl-2 knock-down cells. Curr Mol Med 2012; 12:476-82; PMID:22348615
  • Veenman L, Gavish M, Kugler W. Apoptosis induction by erucylphosphohomocholine via the 18 kDa mitochondrial translocator protein: implications for cancer treatment. Anticancer Agents Med Chem 2014; 14:559-77; PMID:24628235; http://dx.doi.org/10.2174/1871520614666140309230338
  • Ko YH, Delannoy M, Hullihen J, Chiu W, Pedersen PL. Mitochondrial ATP synthasome. Cristae-enriched membranes and a multiwell detergent screening assay yield dispersed single complexes containing the ATP synthase and carriers for Pi and ADP/ATP. J Biol Chem 2003; 278:12305-9; PMID:12560333; http://dx.doi.org/10.1074/jbc.C200703200
  • McEnery MW, Snowman AM, Trifiletti RR, Snyder SH. 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 1992; 89:3170-4; PMID:1373486; http://dx.doi.org/10.1073/pnas.89.8.3170
  • Ruderman NB, Xu XJ, Nelson L, Cacicedo JM, Saha AK, Lan F, Ido Y. AMPK and SIRT1: a long-standing partnership? Am J Physiol Endocrinol Metab 2010; 298:E751-60; PMID:20103737; http://dx.doi.org/10.1152/ajpendo.00745.2009
  • Casellas P, Galiegue S, Basile AS. Peripheral benzodiazepine receptors and mitochondrial function. Neurochem Int 2002; 40:475-86; PMID:11850104; http://dx.doi.org/10.1016/S0197-0186(01)00118-8
  • Corsi L, Geminiani E, Avallone R, Baraldi M. Nuclear location-dependent role of peripheral benzodiazepine receptor (PBR) in hepatic tumoral cell lines proliferation. Life Sci 2005; 76:2523-33; PMID:15769477; http://dx.doi.org/10.1016/j.lfs.2004.08.040
  • Mendonca-Torres MC, Roberts SS. The translocator protein (TSPO) ligand PK11195 induces apoptosis and cell cycle arrest and sensitizes to chemotherapy treatment in pre- and post-relapse neuroblastoma cell lines. Cancer Biol Ther 2013; 14:319-26; PMID:23358477; http://dx.doi.org/10.4161/cbt.23613
  • Rechichi M, Salvetti A, Chelli B, Costa B, Da Pozzo E, Spinetti F, Lena A, Evangelista M, Rainaldi G, Martini C, et al. TSPO over-expression increases motility, transmigration and proliferation properties of C6 rat glioma cells. Biochim Biophys Acta 2008; 1782:118-25; PMID:18190798; http://dx.doi.org/10.1016/j.bbadis.2007.12.001
  • Wu X, Gallo KA. The 18-kDa translocator protein (TSPO) disrupts mammary epithelial morphogenesis and promotes breast cancer cell migration. PLoS One 2013; 8:e71258; PMID:23967175; http://dx.doi.org/10.1371/journal.pone.0071258
  • Liu GJ, Simpson AM, Swan MA, Tao C, Tuch BE, Crawford RM, Jovanovic A, Martin DK. ATP-sensitive potassium channels induced in liver cells after transfection with insulin cDNA and the GLUT 2 transporter regulate glucose-stimulated insulin secretion. Faseb J 2003; 17:1682-4; PMID:12958175
  • Tamarina NA, Kuznetsov A, Fridlyand LE, Philipson LH. Delayed-rectifier (KV2.1) regulation of pancreatic beta-cell calcium responses to glucose: inhibitor specificity and modeling. Am J Physiol Endocrinol Metab 2005; 289:E578-85; PMID:16014354; http://dx.doi.org/10.1152/ajpendo.00054.2005
  • Liu Y, Sato T, O'Rourke B, Marban E. Mitochondrial ATP-dependent potassium channels: novel effectors of cardioprotection? Circulation 1998; 97:2463-9; PMID:9641699; http://dx.doi.org/10.1161/01.CIR.97.24.2463
  • O'Rourke B. Evidence for mitochondrial K+ channels and their role in cardioprotection. Circ Res 2004; 94:420-32; PMID:15001541; http://dx.doi.org/10.1161/01.RES.0000117583.66950.43
  • Hatty CR, Le Brun AP, Lake V, Clifton LA, Liu GJ, James M, Banati RB. Investigating the interactions of the 18kDa translocator protein and its ligand PK11195 in planar lipid bilayers. Biochim Biophys Acta 2014; 1838:1019-30; PMID:24374318; http://dx.doi.org/10.1016/j.bbamem.2013.12.013
  • Cheng KT, Hou WC, Huang YC, Wang LF. Baicalin induces differential expression of cytochrome C Oxidase in human lung H441 Cell. J Agric Food Chem 2003; 51:7276-9; PMID:14640570; http://dx.doi.org/10.1021/jf0301549
  • Dveksler GS, Basile AA, Dieffenbach CW. Analysis of gene expression: use of oligonucleotide primers for glyceraldehyde-3-phosphate dehydrogenase. PCR Methods Appl 1992; 1:283-5; PMID:1477664; http://dx.doi.org/10.1101/gr.1.4.283
  • Liu GJ, Nagarajah R, Banati RB, Bennett MR. Glutamate induces directed chemotaxis of microglia. Eur J Neurosci 2009; 29:1108-18; PMID:19302147; http://dx.doi.org/10.1111/j.1460-9568.2009.06659.x
  • Milakovic T, Johnson GVW. Mitochondrial respiration and ATP production are significantly impaired in striatal cells expressing mutant Huntingtin. J Biol Chem 2005; 280:30773-82; PMID:15983033; http://dx.doi.org/10.1074/jbc.M504749200