Structural and functional evolution of the translocator protein (18 kDa)

Current Molecular Medicine

Volumn 12, Issue 4, 2012, Pages 369-386

  Fan, J ^a   Lindemann, P ^b   Feuilloley, M G J ^c   Papadopoulos, V ^a,d  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c UNIVERSITÉ DE ROUEN   (France)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

Cholesterol transport binding; Evolutionary origin; Gene family; Oxygen sensor; Peripheral benzodiazepine receptor; Steroidogenesis; Translocator protein (18 kDa)

Indexed keywords

PROTEIN; TRANSLOCATOR PROTEIN; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; APOPTOSIS; ARCHAEON; BACTERIUM; EUKARYOTE; GENE DUPLICATION; HUMAN; MITOCHONDRION; MOLECULAR EVOLUTION; NONHUMAN; PARALOGY; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; STEROIDOGENESIS;

AVES; EUKARYOTA; MAMMALIA;

EID: 84860313330     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/1566524011207040369     Document Type: Review

References (135)

1. Braestrup C, Squires RF. Specific benzodiazepine receptors in rat brain characterized by high-affinity (3H)diazepam binding. Proc Natl Acad Sci USA 1977; 74: 3805-9.
2. Batarseh A, Papadopoulos V. Regulation of translocator protein 18 kDa (TSPO) expression in health and disease states. Mol Cell Endocrinol 2010; 327: 1-12.
3. 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.
4. Hardwick M, Rone J, Han Z, Haddad B, Papadopoulos V. Peripheral-type benzodiazepine receptor levels correlate with the ability of human breast cancer MDA-MB-231 cell line to grow in SCID mice. Int J Cancer 2001; 94: 322-7.
5. 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.
6. Papadopoulos V, Kapsis A, Li H, et al. Drug-induced inhibition of the peripheral-type benzodiazepine receptor expression and cell proliferation in human breast cancer cells. Anticancer Res 2000; 20: 2835-47.
7. Papadopoulos V, Baraldi M, Guilarte TR, 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.
8. Fan J, Rone MB, Papadopoulos V. Translocator protein 2 is involved in cholesterol redistribution during erythropoiesis. J Biol Chem 2009; 284: 30484-97.
9. Simos G, Maison C, Georgatos SD. Characterization of p18, a component of the lamin B receptor complex and a new integral membrane protein of the avian erythrocyte nuclear envelope. J Biol Chem 1996; 271: 12617-25.
10. Nakazawa F, Alev C, Shin M, Nakaya Y, Jakt LM, Sheng G. PBRL, a putative peripheral benzodiazepine receptor, in primitive erythropoiesis. Gene Expr Patterns 2009; 9: 114-21.
11. Rampon C, Bouzaffour M, Ostuni MA, et al. Translocator protein (18 kDa) is involved in primitive erythropoiesis in zebrafish. FASEB J 2009; 23: 4181-92.
12. Chapalain A, Chevalier S, Orange N, Murillo L, Papadopoulos V, Herman C. Bacterial Ortholog of Mammalian Translocator Protein (TSPO) with Virulence. PLoS ONE 2009; 4: e6096.
13. Frank W, Baar KM, Qudeimat E, et al. A mitochondrial protein homologous to the mammalian peripheral-type benzodiazepine receptor is essential for stress adaptation in plants. Plant J 2007; 51: 1004-18.
14. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 1990; 87: 4576-9.
15. Riond J, Leplatois P, Laurent P, et al. Expression and pharmacological characterization of the human peripheraltype benzodiazepine receptor in yeast. Eur J Pharmacol 1991; 208: 307-12.
16. Yeliseev AA, Krueger KE, Kaplan S. A mammalian mitochondrial drug receptor functions as a bacterial "oxygen" sensor. Proc Natl Acad Sci USA 1997; 94: 5101-6.
17. Armstrong GA, Alberti M, Leach F, Hearst JE. Nucleotide sequence, organization, and nature of the protein products of the carotenoid biosynthesis gene cluster of Rhodobacter capsulatus. Mol Gen Genet 1989; 216: 254-68.
18. Phadwal K. Carotenoid biosynthetic pathway: molecular phylogenies and evolutionary behavior of crt genes in eubacteria. Gene 2005; 345: 35-43.
19. Yeliseev AA, Kaplan S. A sensory transducer homologous to the mammalian peripheral-type benzodiazepine receptor regulates photosynthetic membrane complex formation in Rhodobacter sphaeroides 2.4.1. J Biol Chem 1995; 270: 21167-75.
20. Yeliseev AA, Kaplan S. TspO of rhodobacter sphaeroides. A structural and functional model for the mammalian peripheral benzodiazepine receptor. J Biol Chem 2000; 275: 5657-67.
21. Zeng X, Kaplan S. TspO as a modulator of the repressor/antirepressor (PpsR/AppA) regulatory system in Rhodobacter sphaeroides 2.4. 1. J Bacteriol 2001; 183: 6355-64.
22. Davey ME, de Bruijn FJ. A homologue of the tryptophan-rich sensory protein TspO and FixL regulate a novel nutrient deprivation-induced Sinorhizobium meliloti locus. Appl Environ Microbiol 2000; 66: 5353-9.
23. Tong Y, Guo M. Bacterial heme-transport proteins and their heme-coordination modes. Arch Biochem Biophys 2009; 481: 1-15.
24. Baysse C, Matthijs S, Schobert M, Layer G, Jahn D, Cornelis P. Co-ordination of iron acquisition, iron porphyrin chelation and iron-protoporphyrin export via the cytochrome c biogenesis protein CcmC in Pseudomonas fluorescens. Microbiology 2003; 149: 3543-52.
25. Cornelis P, Matthijs S. Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ Microbiol 2002; 4: 787-98.
26. Korkhov VM, Sachse C, Short JM, Tate CG. Threedimensional structure of TspO by electron cryomicroscopy of helical crystals. Structure 2010; 18: 677-87.
27. Lindemann P, Koch A, Degenhardt B, Hause G, Grimm B, Papadopoulos V. A novel Arabidopsis thaliana protein is a functional peripheral-type benzodiazepine receptor. Plant Cell Physiol 2004; 45: 723-33.
28. Wendler G, Lindemann P, Lacapere JJ, Papadopoulos V. Protoporphyrin IX binding and transport by recombinant mouse PBR. Biochem Biophys Res Commun 2003; 311: 847-52.
29. Donohue TJ. Eubacterial signal transduction by ligands of the mammalian peripheral benzodiazepine receptor complex. Proc Natl Acad Sci USA 1997; 94: 4821-2.
30. Li H, Papadopoulos V. Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern. Endocrinology 1998; 139: 4991-7.
31. Steen BR, Lian T, Zuyderduyn S, et al. Temperatureregulated transcription in the pathogenic fungus Cryptococcus neoformans. Genome Res 2002; 12: 1386-400.
32. Kellis M, Birren BW, Lander ES. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 2004; 428: 617-24.
33. Chen D, Toone WM, Mata J, et al. Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 2003; 14: 214-29.
34. Dujon B, Sherman D, Fischer G, et al. Genome evolution in yeasts. Nature 2004; 430: 35-44.
35. Luckner M. Secondary metabolism in microorganisms, plants and animals. Springer: Berlin 1990.
36. Yurdaydin C, Walsh TJ, Engler HD, et al. Gut bacteria provide precursors of benzodiazepine receptor ligands in a rat model of hepatic encephalopathy. Brain Res 1995; 679: 42-8.
37. Weinstein JD, Beale SI. Separate physiological roles and subcellular compartments for two tetrapyrrole biosynthetic pathways in Euglena gracilis. J Biol Chem 1983; 258: 6799-807.
38. Corsi L, Avallone R, Geminiani E, Cosenza F, Venturini I, Baraldi M. Peripheral benzodiazepine receptors in potatoes (Solanum tuberosum). Biochem Biophys Res Commun 2004; 313: 62-6.
39. Schmid M, Davison TS, Henz SR, et al. A gene expression map of Arabidopsis thaliana development. Nat Genet 2005; 37: 501-6.
40. Guillaumot D, Guillon S, Morsomme P, Batoko H. ABA, porphyrins and plant TSPO-related protein. Plant Signal Behav 2009; 4: 1087-90.
41. Sun M, Li L, Xie H, Ma R, He Y. Differentially expressed genes under cold acclimation in Physcomitrella patens. J Biochem Mol Biol 2007; 40: 986-1001.
42. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 2002; 130: 2129-41.
43. Flinn B, Rothwell C, Griffiths R, et al. Potato expressed sequence tag generation and analysis using standard and unique cDNA libraries. Plant Mol Biol 2005; 59: 407-33.
44. Guillaumot D, Guillon S, Dëplanque T, et al. The Arabidopsis TSPO-related protein is a stress and abscisic acid-regulated, endoplasmic reticulum-Golgi-localized membrane protein. Plant J 2009; 60: 242-56.
45. Hermans C, Vuylsteke M, Coppens F, Craciun A, Inzé D, Verbruggen N. Early transcriptomic changes induced by magnesium deficiency in Arabidopsis thaliana reveal the alteration of circadian clock gene expression in roots and the triggering of abscisic acid-responsive genes. New Phytol 2010; 187: 119-31.
46. Mizoguchi M, Umezawa T, Nakashima K, et al. Two closely related subclass II SnRK2 protein kinases cooperatively regulate drought-inducible gene expression. Plant Cell Physiol 2010; 51: 842-7.
47. Medina JH, Pena C, Levi SM, Wolfman C, Paladini AC. Benzodiazepine-like molecules, as well as other ligands for the brain benzodiazepine receptors, are relatively common constituents of plants. Biochem Biophys Res Commun 1989; 165: 547-53.
48. Avallone R, Zanoli P, Corsi L, Cannazza G, Baraldi M. Benzodiazepine-like compounds and GABA in flower heads of Matricaria chamomilla. Phytother Res 1996; 10: S177-S179.
49. Wildmann J. Increase of natural benzodiazepines in wheat and potato during germination. Biochem Biophys Res Commun 1988; 157: 1436-43.
50. Tanaka R, Tanaka A. Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 2007; 58: 321-46.
51. Jung S, Lee HJ, Lee Y, et al. Toxic tetrapyrrole accumulation in protoporphyrinogen IX oxidase-overexpressing transgenic rice plants. Plant Mol Biol 2008; 67: 535-46.
52. Masuda T, Suzuki T, Shimada H, Ohta H, Takamiya K. Subcellular localization of two types of ferrochelatase in cucumber. Planta 2003; 217: 602-9.
53. Janeczko A, Skoczowski A. Mammalian sex hormones in plants. Fol Histoch Cytochem 2005; 43: 71-9.
54. Iino M, Nomura T, Tamaki Y, et al. Progesterone: its occurrence in plants and involvement in plant growth. Phytochemistry 2007; 68: 1664-73.
55. Simersky R, Novák O, Morris DA, Pouzar V, Strnad M. Identification and quantification of several mammalian steroid hormones in plants by UPLC-MS/MS. J Plant Growth Regul 2009; 28: 125-36.
56. Janeczko A, Budziszewska B, Skoczowski A, Dybala M. Specific binding sites for progesterone and 17 -estradiol in cells of Triticum aestivum L. Acta Biochim Pol 2008; 55: 707-11.
57. Janeczko A, Filek W, Biesaga-Kocielniak J, Marciska I, Janeczko Z. The influence of animal sex hormones on the induction of flowering in Arabidopsis thaliana: comparison with the effect of 24-epibrassinolide. Plant Cell, Tissue Organ Cult 2003; 72: 147-51.
58. Bennett RD, Heftmann E, Winter BJ. A function of sitosterol. Phytochemistry 1969; 8: 2325-8.
59. Lindemann P, Luckner M. Biosynthesis of pregnane derivatives in somatic embryos of Digitalis lanata. Phytochemistry 1997; 46: 507-13.
60. Palazon J, Bonfill M, Cusido RM, Pinol MT, Morales C. Effects of auxin and phenobarbital on morphogenesis and production of digitoxin in Digitalis callus. Plant Cell Physiol 1995; 36: 247-52.
61. Grinberg AV, Hannemann F, Schiffler B, Müller J, Heinemann U, Bernhardt R. Adrenodoxin: structure, stability, and electron transfer properties. Proteins: Structure, Function, and Bioinformatics 2000; 40: 590-612.
62. Ohta D, Mizutani M. Redundancy or flexibility: molecular diversity of the electron transfer components for P450 monooxygenases in higher plants. Front Biosci 2004; 9: 1587-97.
63. Millar AH, Heazlewood JL, Kristensen BK, Braun HP, Moller IM. The plant mitochondrial proteome. Trends Plant Sci 2005; 10: 36-43.
64. Luzikov VN, Novikova LA, Spiridonova VA, et al. Design of heterologous mitochondria: import of cattle cytochrome P-450SCC precursors in plant mitochondria. Biokhimiia (Moscow, Russia) 1994; 59: 1098-101.
65. Spivak SG, Berdichevets IN, Yarmolinsky DG, Maneshina TV, Shpakovski GV, Kartel NA. Construction and characteristics of transgenic tobacco Nicotiana tabacum L. plants expressing CYP11A1 cDNA encoding cytochrome P450 SCC. Russ J Genet 2009; 45: 1067-73.
66. Spivak SG, Berdichevets IN, Litvinovskaya RP, Drach SV, Kartel NA, Shpakovski GV. Some peculiarities of steroid metabolism in transgenic Nicotiana tabacum plants bearing the CYP11A1 cDNA of cytochrome P450 SCC from the bovine adrenal cortex. Russ J Org Chem 2010; 36: 224-32.
67. Pilgrim H. 'Cholesterol side-chain cleaving enzyme' aktivitat in keimlingen und in vitro kultivierten geweben von Digitalis purpurea. Phytochemistry 1972; 11: 1725-8.
68. Ghedin E, Wang S, Spiro D, et al. Draft genome of the filarial nematode parasite Brugia malayi. Science 2007; 317: 1756-60.
69. Snyder MJ, Van Antwerpen R. Evidence for a diazepambinding inhibitor (DBI) benzodiazepine receptor-like mechanism in ecdysteroidogenesis by the insect prothoracic gland. Cell Tissue Res 1998; 294: 161-8.
70. Roth GE, Gierl MS, Vollborn L, Meise M, Lintermann R, Korge G. The Drosophila gene Start1: a putative cholesterol transporter and key regulator of ecdysteroid synthesis. Proc Natl Acad Sci USA 2004; 101: 1601-6.
71. Warren JT, Petryk A, Marqués G, et al. Molecular and biochemical characterization of two P450 enzymes in the ecdysteroidogenic pathway of Drosophila melanogaster. Proc Natl Acad Sci USA 2002; 99: 11043-8.
72. Guzov VM, Unnithan GC, Chernogolov AA, Feyereisen R. CYP12A1, a mitochondrial cytochrome P450 from the house fly. Arch Biochem Biophys 1998; 359: 231-40.
73. Markov GV, Tavares R, Dauphin-Villemant C, Demeneix BA, Baker ME, Laudet V. Independent elaboration of steroid hormone signaling pathways in metazoans. Proc Natl Acad Sci USA 2009; 106: 11913-8.
74. Ranson H, Claudianos C, Ortelli F, et al. Evolution of supergene families associated with insecticide resistance. Science 2002; 298: 179-81.
75. Feyereisen R. Evolution of insect P450. Biochem Soc T 2006; 34: 1252-5.
76. Giot L, Bader JS, Brouwer C, et al. A protein interaction map of Drosophila melanogaster. Science 2003; 302: 1727-36.
77. Tonoki A, Kuranaga E, Tomioka T, et al. Genetic evidence linking age-dependent attenuation of the 26S proteasome with the aging process. Mol Cell Biol 2009; 29: 1095-106.
78. Curtis C, Landis G, Folk D, et al. Transcriptional profiling of MnSOD-mediated lifespan extension in Drosophila reveals a species-general network of aging and metabolic genes. Genome Biol 2007; 8: R262.
79. Santos TM, Johnston DA, Azevedo V, et al. Analysis of the gene expression profile of Schistosoma mansoni cercariae using the expressed sequence tag approach. Mol Biochem Parasitol 1999; 103: 79-98.
80. Noel F, Mendonca-Silva DL, Thibaut JP, Lopes DV. Characterization of two classes of benzodiazepine binding sites in Schistosoma mansoni. Parasitology 2007; 134: 1003-12.
81. Pica-Mattoccia L, Ruppel A, Xia CM, Cioli D. Praziquantel and the benzodiazepine Ro11-3128 do not compete for the same binding sites in schistosomes. Parasitology 2007; 135: 47-54.
82. Betti L, Giannaccini G, Nigro M, Dianda S, Gremigni V, Lucacchini A. Studies of peripheral benzodiazepine receptors in mussels: comparison between a polluted and a nonpolluted site. Ecotox Environ Safe 2003; 54: 36-42.
83. 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.
84. Hsu HJ, Hsiao P, Kuo MW, Chung B. Expression of zebrafish cyp11a1 as a maternal transcript and in yolk syncytial layer. Gene Expr Patterns 2002; 2: 219-22.
85. Hsu HJ, Lin G, Chung B. Parallel early development of zebrafish interrenal glands and pronephros: differential control by wt1 and ff1b. Development 2003; 130: 2107-16.
86. Lesouhaitier O, Feuilloley M, Lihrmann I, et al. Localization of diazepam-binding inhibitor-related peptides and peripheral type benzodiazepine receptors in the frog adrenal gland. Cell Tissue Res 1996; 283: 403-12.
87. Ziyadeh FN, Kelepouris E, Agus ZS. Benzodiazepines stimulate sodium ion transport in frog skin epithelium. BBABiomembranes 1988; 940: 93-8.
88. Papadopoulos V. Peripheral-type benzodiazepine/diazepam binding inhibitor receptor: biological role in steroidogenic cell function. Endocr Rev 1993; 14: 222-40.
89. Rone MB, Fan J, Papadopoulos V. Cholesterol transport in steroid biosynthesis: Role of proteinûprotein interactions and implications in disease states. BBA-Mol Cell Biol L 2009; 1791: 646-58.
90. Papadopoulos V. In search of the function of the peripheraltype benzodiazepine receptor. Endocr Res 2004; 30: 677-84.
91. Lacapere JJ, Delavoie F, Li H, et al. Structural and functional study of reconstituted peripheral benzodiazepine receptor. Biochem Biophys Res Commun 2001; 284: 536-41.
92. Beurdeley-Thomas A, Miccoli L, Oudard S, Dutrillaux B, Poupon MF. The peripheral benzodiazepine receptors: a review. J Neuro-Oncol 2000; 46: 45-56.
93. Culty M, Li H, Boujrad N, et al. In vitro studies on the role of the peripheral-type benzodiazepine receptor in steroidogenesis. J Steroid Biochem Mol Biol 1999; 69: 123-30.
94. Gavish M, Bachman I, Shoukrun R, et al. Enigma of the Peripheral Benzodiazepine Receptor. Pharmacol Rev 1999; 51: 629-50.
95. Farges R, Joseph-Liauzun E, Shire D, et al. Molecular basis for the different binding properties of benzodiazepines to human and bovine peripheral-type benzodiazepine receptors. FEBS Lett 1993; 335: 305-8.
96. Farges R, Joseph-Liauzun E, Shire D, Caput D, Le Fur G, Ferrara P. Site-directed mutagenesis of the peripheral benzodiazepine receptor: identification of amino acids implicated in the binding site of Ro5-4864. Mol Pharmacol 1994; 46: 1160-7.
97. Joseph-Liauzun E, Farges R, Delmas P, Ferrara P, Loison G. The Mr 18,000 subunit of the peripheral-type benzodiazepine receptor exhibits both benzodiazepine and isoquinoline carboxamide binding sites in the absence of the voltage-dependent anion channel or of the adenine nucleotide carrier. J Biol Chem 1997; 272: 28102-6.
98. 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 USA 1992; 89: 3170-4.
99. Garnier M, Dimchev AB, Boujrad N, Price JM, Musto NA, Papadopoulos V. In vitro reconstitution of a functional peripheral-type benzodiazepine receptor from mouse Leydig tumor cells. Mol Pharmacol 1994; 45: 201-11.
100. Sigel E, Buhr A. The benzodiazepine binding site of GABAA receptors. Trends Pharmacol Sci 1997; 18: 425-9.
101. Slocinska M, Szewczyk A, Hryniewiecka L, Kmita H. Benzodiazepine binding to mitochondrial membranes of the amoeba Acanthamoeba castellanii and the yeast Saccharomyces cerevisiae. Acta Biochim Pol 2004; 51: 953-62.
102. Avallone R, Cosenza F, Farina F, Baraldi C, Baraldi M. Extraction and purification from Ceratonia siliqua of compounds acting on central and peripheral benzodiazepine receptors. Fitoterapia 2002; 73: 390-6.
103. Anzini M, Cappelli A, Vomero S, et al. Mapping and fitting the peripheral benzodiazepine receptor binding site by carboxamide derivatives. Comparison of different approaches to quantitative ligand-receptor interaction modeling. J Med Chem 2001; 44: 1134-50.
104. Ourisson G, Rohmer M, Poralla K. Prokaryotic hopanoids and other polyterpenoid sterol surrogates. Annu Rev Microbiol 1987; 41: 301-33.
105. Welander PV, Hunter RC, Zhang L, Sessions AL, Summons RE, Newman DK. Hopanoids play a role in membrane integrity and pH homeostasis in Rhodopseudomonas palustris TIE-1. J Bacteriol 2009; 191: 6145-56.
106. Kurzchalia TV, Ward S. Why do worms need cholesterol? Nat Cell Biol 2003; 5: 684-8.
107. Kamath RS, Fraser AG, Dong Y, et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003; 421: 231-7.
108. Lafont R. Understanding insect endocrine systems: molecular approaches. Entomol Exp Appl 2000; 97: 123-36.
109. Gilbert LI, Rybczynski R, Warren JT. Control and biochemical nature of the ecdysteroidogenic pathway. Annu Rev Entomol 2002; 47: 883-916.
110. 1 mutation. Insect Biochem Mol Biol 1996; 26: 931-43.
111. Granot Z, Kobiler O, Melamed-Book N, et al. Turnover of mitochondrial steroidogenic acute regulatory (StAR) protein by Lon protease: the unexpected effect of proteasome inhibitors. Mol Endocrinol 2007; 21: 2164-77.
112. Nakagawa T, Shirane M, Iemura S, Natsume T, Nakayama KI. Anchoring of the 26S proteasome to the organellar membrane by FKBP38. Genes Cells 2007; 12: 709-19.
113. Soccio RE, Breslow JL. StAR-related lipid transfer (START) proteins: mediators of intracellular lipid metabolism. J Biol Chem 2003; 278: 22183-6.
114. Ohno S. Evolution by gene duplication. New York: Springer-Verlag 1970.
115. Jamin N, Neumann JM, Ostuni MA, et al. Characterization of the cholesterol recognition amino acid consensus sequence of the peripheral-type benzodiazepine receptor. Mol Endocrinol 2005; 19: 588-94.
116. Gu X, Vander VK. DIVERGE: phylogeny-based analysis for functional-structural divergence of a protein family. Bioinformatics 2002; 18: 500-1.
117. Rone MB, Liu J, Blonder J, et al. Targeting and insertion of the cholesterol-binding translocator protein into the outer mitochondrial membrane. Biochemistry 2009; 48: 6909-20.
118. Parola AL, Yamamura HI, rd HE. Peripheral-type benzodiazepine receptors. Life Sci 1993; 52: 1329-42.
119. Bernassau JM, Reversat JL, Ferrara P, Caput D, Lefur G. A 3D model of the peripheral benzodiazepine receptor and its implication in intra mitochondrial cholesterol transport. J Mol Graphics 1993; 11: 236-44.
120. 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.
121. Carayon P, Portier M, Dussossoy D, et al. Involvement of peripheral benzodiazepine receptors in the protection of hematopoietic cells against oxygen radical damage. Blood 1996; 87: 3170-8.
122. O'Hara MF, Nibbio BJ, Craig RC, Nemeth KR, Charlap JH, Knudsen TB. Mitochondrial benzodiazepine receptors regulate oxygen homeostasis in the early mouse embryo. Reprod Toxicol 2003; 17: 365-75.
123. Knudsen TB, Green ML. Response characteristics of the mitochondrial DNA genome in developmental health and disease. Birth Defects Res C Embryo Today 2004; 72: 313-29.
124. Delavoie F, Li H, Hardwick M, et al. In vivo and in vitro peripheral-type benzodiazepine receptor polymerization: functional significance in drug ligand and cholesterol binding. Biochemistry 2003; 42: 4506-19.
125. Hanukoglu I. Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metab Rev 2006; 38: 171-96.
126. Summons RE, Bradley AS, Jahnke LL, Waldbauer JR. Steroids, triterpenoids and molecular oxygen. Philos T Roy Soc B 2006; 361: 951-68.
127. Fan J, Traore K, Li W, et al. Molecular mechanisms mediating the effect of mono-(2-ethylhexyl) phthalate (MEHP) on hormone-stimulated steroidogenesis in MA-10 mouse tumor Leydig cells. Endocrinology 2010; 151: 3348-62.
128. Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol 1982; 157: 105-32.
129. Hofmann K, Stoffel W. TMbase: a database of membrane spanning proteins segments. Biol Chem Hoppe-Seyler 1993; 347: 166-70.
130. Rice P, Longden I, Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Genet 2000; 16: 276-7.
131. Kumar S, Tamura K, Nei M. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 2004; 5: 150-63.
132. Higgins DG, Bleasby AJ, Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci 1992; 8: 189-91.
133. Konvicka K, Campagne F, Weinstein H. Interactive construction of residue-based diagrams of proteins: the RbDe web service. Protein Eng 2000; 13: 395-6.
134. Rupprecht R, Papadopoulos V, Rammes G, et al. Translocator protein (18 kDa)(TSPO) as a therapeutic target for neurological and psychiatric disorders. Nat Rev Drug Discov 2010; 9: 971-88.
135. Fan J, Papadopoulos V. Translocator protein 2 (TSPO2), a new family of proteins involved in cholesterol redistribution in erythropoiesis. FASEB J 2009; 23 (1_MeetingAbstracts) 521.1.