Intracellular cholesterol changes induced by translocator protein (18 kDa) TSPO/PBR ligands

Neuropharmacology

Volumn 53, Issue 2, 2007, Pages 318-329

  Falchi, Angela Maria ^a   Battetta, Barbara ^a   Sanna, Francesca ^a   Piludu, Marco ^a   Sogos, Valeria ^a   Serra, Mariangela ^b   Melis, Marta ^a   Putzolu, Martina ^a   Diaz, Giacomo ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b Center of Excellence Neurobiology of Dependence   (Italy)

Author keywords

Acidic vesicles; Cholesterol; Immunocytochemistry; Lipid droplets; Mitochondria; MTT; PBR; Translocator protein (18 kDa); TSPO

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; 4' CHLORODIAZEPAM; 4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; BENZODIAZEPINE RECEPTOR; CARRIER PROTEIN; CHOLESTEROL; CLONAZEPAM; DIAZEPAM; FAT DROPLET; FORMAZAN; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; PROPRANOLOL;

ACIDIFICATION; ANIMAL CELL; ARTICLE; ASTROCYTE; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE PERMEABILITY; CHOLESTEROL ESTERIFICATION; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; DRUG BINDING; EXOCYTOSIS; FIBROBLAST; IMMUNOCYTOCHEMISTRY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT;

ADENOSINE TRIPHOSPHATASES; ANIMALS; ANTINEOPLASTIC AGENTS; ASTROCYTES; BENZODIAZEPINONES; CARRIER PROTEINS; CELL LINE; CHOLESTEROL; CONVULSANTS; DOSE-RESPONSE RELATIONSHIP, DRUG; EXOCYTOSIS; FIBROBLASTS; INTRACELLULAR FLUID; ISOQUINOLINES; LIGANDS; MEMBRANE PROTEINS; MICE; RECEPTORS, GABA; RHODAMINES; TIME FACTORS;

EID: 34547541523     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2007.05.016     Document Type: Article

References (44)

1. Amchenkova A.A., Bakeeva L.E., Chentsov Y.S., Skulachev V.P., and Zorov D.B. Coupling membranes as energy-transmitting cables. I. Filamentous mitochondria in fibroblasts and mitochondrial clusters in cardiomyocytes. J. Cell Biol. 107 (1988) 481-495
2. Aon M.A., Cortassa S., Marban E., and O'Rourke B. Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J. Biol. Chem. 278 (2003) 44735-44744
3. Basile A.S., Lueddens H.W., and Skolnick P. Regulation of renal peripheral benzodiazepine receptors by anion transport inhibitors. Life Sci. 42 (1988) 715-726
4. Beavis A.D. On the inhibition of the mitochondrial inner membrane anion uniporter by cationic amphiphiles and other drugs. J. Biol. Chem. 264 (1989) 1508-1515
5. Beavis A.D. Properties of the inner membrane anion channel in intact mitochondria. J. Bioenerg. Biomembr. 24 (1992) 77-90
6. Beavis A.D., and Davatol-Hag H. The mitochondrial inner membrane anion channel is inhibited by DIDS. J. Bioenerg. Biomembr. 28 (1996) 207-214
7. Casellas P., Galiegue S., and Basile A.S. Peripheral benzodiazepine receptors and mitochondrial function. Neurochem. Int. 40 (2002) 475-486
8. Chanderbhan R., Noland B.J., Scallen T.J., and Vahouny G.V. Sterol carrier protein2. Delivery of cholesterol from adrenal lipid droplets to mitochondria for pregnenolone synthesis. J. Biol. Chem. 257 (1982) 8928-8934
9. Chelli B., Falleni A., Salvetti F., Gremigni V., Lucacchini A., and Martini C. Peripheral-type benzodiazepine receptor ligands: mitochondrial permeability transition induction in rat cardiac tissue. Biochem. Pharmacol. 61 (2001) 695-705
10. 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. Peripheral benzodiazepine receptor ligands: mitochondrial transmembrane potential depolarization and apoptosis induction in rat C6 glioma cells. Biochem. Pharmacol. 68 (2004) 125-134
11. Clark B.J., Wells J., King S.R., and Stocco D.M. The purification, cloning, and expression of a novel luteinizing hormone-induced mitochondrial protein in MA-10 mouse Leydig tumor cells. Characterization of the steroidogenic acute regulatory protein (StAR). J. Biol. Chem. 269 (1994) 28314-28322
12. Cousin M.A., and Nicholls D.G. Synaptic vesicle recycling in cultured cerebellar granule cells: role of vesicular acidification and refilling. J. Neurochem. 69 (1997) 1927-1935
13. Decaudin D., Castedo M., Nemati F., Beurdeley-Thomas A., De Pinieux G., Caron A., Pouillart P., Wijdenes J., Rouillard D., Kroemer G., and Poupon M.F. Peripheral benzodiazepine receptor ligands reverse apoptosis resistance of cancer cells in vitro and in vivo. Cancer Res. 62 (2002) 1388-1393
14. Fennell D.A., Corbo M., Pallaska A., and Cotter F.E. Bcl-2 resistant mitochondrial toxicity mediated by the isoquinoline carboxamide PK11195 involves de novo generation of reactive oxygen species. Br. J. Cancer 84 (2001) 1397-1404
15. Folch J., Lees M., and Sloane Stanley G.H. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226 (1957) 497-509
16. Frolov A., Petrescu A., Atshaves B.P., So P.T., Gratton E., Serrero G., and Schroeder F. High density lipoprotein-mediated cholesterol uptake and targeting to lipid droplets in intact L-cell fibroblasts. A single- and multiphoton fluorescence approach. J. Biol. Chem. 275 (2000) 12769-12780
17. Gavish M., Bachman I., Shoukrun R., Katz Y., Veenman L., Weisinger G., and Weizman A. Enigma of the peripheral benzodiazepine receptor. Pharmacol. Rev. 51 (1999) 629-650
18. Giatzakis C., and Papadopoulos V. Differential utilization of the promoter of peripheral-type benzodiazepine receptor by steroidogenic versus nonsteroidogenic cell lines and the role of Sp1 and Sp3 in the regulation of basal activity. Endocrinology 145 (2004) 1113-1123
19. Gonzalez-Polo R.A., Carvalho G., Braun T., Decaudin D., Fabre C., Larochette N., Perfettini J.L., Djavaheri-Mergny M., Youlyouz-Marfak I., Codogno P., Raphael M., Feuillard J., and Kroemer G. PK11195 potently sensitizes to apoptosis induction independently from the peripheral benzodiazepine receptor. Oncogene 24 (2005) 7503-7513
20. Hans G., Wislet-Gendebien S., Lallemend F., Robe P., Rogister B., Belachew S., Nguyen L., Malgrange B., Moonen G., and Rigo J.M. Peripheral benzodiazepine receptor (PBR) ligand cytotoxicity unrelated to PBR expression. Biochem. Pharmacol. 69 (2005) 819-830
21. 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. Peripheral-type benzodiazepine receptor-mediated action of steroidogenic acute regulatory protein on cholesterol entry into leydig cell mitochondria. Mol. Endocrinol. 19 (2005) 540-554
22. Jayakumar A.R., Panickar K.S., and Norenberg M.D. Effects on free radical generation by ligands of the peripheral benzodiazepine receptor in cultured neural cells. J. Neurochem. 83 (2002) 1226-1234
23. King S.R., and Stocco D.M. ATP and a mitochondrial electrochemical gradient are required for functional activity of the steroidogenic acute regulatory (StAR) protein in isolated mitochondria. Endocr. Res. 22 (1996) 505-514
24. King S.R., Liu Z., Soh J., Eimerl S., Orly J., and Stocco D.M. Effects of disruption of the mitochondrial electrochemical gradient on steroidogenesis and the Steroidogenic Acute Regulatory (StAR) protein. J. Steroid Biochem. Mol. Biol. 69 (1999) 143-154
25. Kletsas D., Li W., Han Z., and Papadopoulos V. 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 (2004) 1927-1932
26. Kroemer G., Zamzami N., and Susin S.A. Mitochondrial control of apoptosis. Immunol. Today 18 (1997) 44-51
27. Lada A.T., Davis M., Kent C., Chapman J., Tomoda H., Omura S., and Rudel L.L. Identification of ACAT1- and ACAT2-specific inhibitors using a novel, cell-based fluorescence assay: individual ACAT uniqueness. J. Lipid Res. 45 (2004) 378-386
28. Levin E., Premkumar A., Veenman L., Kugler W., Leschiner S., Spanier I., Weisinger G., Lakomek M., Weizman A., Snyder S.H., Pasternak G.W., and Gavish M. The peripheral-type benzodiazepine receptor and tumorigenicity: isoquinoline binding protein (IBP) antisense knockdown in the C6 glioma cell line. Biochemistry 44 (2005) 9924-9935
29. Liu Y., Peterson D.A., Kimura H., and Schubert D. Mechanism of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction. J. Neurochem. 69 (1997) 581-593
30. Liu Y., Peterson D.A., and Schubert D. Amyloid beta peptide alters intracellular vesicle trafficking and cholesterol homeostasis. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 13266-13271
31. McEnery M.W., Snowman A.M., Trifiletti R.R., and Snyder S.H. 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 (1992) 3170-3174
32. McGookey D.J., and Anderson R.G. Morphological characterization of the cholesteryl ester cycle in cultured mouse macrophage foam cells. J. Cell Biol. 97 (1983) 1156-1168
33. Miller W.L. Molecular biology of steroid hormone synthesis. Endocr. Rev. 9 (1988) 295-318
34. Moreno-Sànchez R., Hogue B.A., Bravo C., Newman A.H., Basile A.S., and Chiang P.K. Inhibition of substrate oxidation in mitochondria by the peripheral-type benzodiazepine receptor ligand AHN 086. Biochem. Pharmacol. 41 (1991) 1479-1484
35. Papadopoulos V. In search of the function of the peripheral-type benzodiazepine receptor. Endocr. Res. 30 (2004) 677-684
36. Papadopoulos V., Baraldi M., Guilarte T.R., Knudsen T.B., Lacapère J.-J., Lindemann P., Norenberg M.D., Nutt D., Weizman A., Zhang M.-R., and Gavish M. Translocator protein (18 kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol. Sci. 27 (2006) 402-409
37. Petrescu A.D., Gallegos A.M., Okamura Y., Strauss III J.F., and Schroeder F. Steroidogenic acute regulatory protein binds cholesterol and modulates mitochondrial membrane sterol domain dynamics. J. Biol. Chem. 276 (2001) 36970-36982
38. Prattes S., Horl G., Hammer A., Blaschitz A., Graier W.F., Sattler W., Zechner R., and Steyrer E. Intracellular distribution and mobilization of unesterified cholesterol in adipocytes: triglyceride droplets are surrounded by cholesterol-rich ER-like surface layer structures. J. Cell Sci. 113 Pt 17 (2000) 2977-2989
39. Rukmini R., Rawat S.S., Biswas S.C., and Chattopadhyay A. Cholesterol organization in membranes at low concentrations: effects of curvature stress and membrane thickness. Biophys. J. 81 (2001) 2122-2134
40. Simpson E.R., and Waterman M.R. Regulation by ACTH of steroid hormone biosynthesis in the adrenal cortex. Can. J. Biochem. Cell Biol. 61 (1983) 692-707
41. Soccio R.E., and Breslow J.L. Intracellular cholesterol transport. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 1150-1160
42. Veenman L., and Gavish M. The peripheral-type benzodiazepine receptor and the cardiovascular system. Implications for drug development. Pharmacol. Ther. 110 (2006) 503-524
43. Watari H., Arakane F., Moog-Lutz C., Kallen C.B., Tomasetto C., Gerton G.L., Rio M.C., Baker M.E., and Strauss III J.F. MLN64 contains a domain with homology to the steroidogenic acute regulatory protein (StAR) that stimulates steroidogenesis. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 8462-8467
44. Weisinger G., Kelly-Hershkovitz E., Veenman L., Spanier I., Leschiner S., and Gavish M. Peripheral benzodiazepine receptor antisense knockout increases tumorigenicity of MA-10 Leydig cells in vivo and in vitro. Biochemistry 43 (2004) 12315-12321