Global deletion of TSPO does not affect the viability and gene expression profile

PLoS ONE

Volumn 11, Issue 12, 2016, Pages

  Wang, Huaishan ^a   Zhai, Kangle ^a   Xue, Yingchao ^a   Yang, Jia ^a   Yang, Qi ^a   Fu, Yi ^a   Hu, Yu ^a   Liu, Fang ^b   Wang, Weiqing ^c   Cui, Lianxian ^a   Chen, Hui ^a   Zhang, Jianmin ^a   He, Wei ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b Beijing Thorgene Medical Laboratory   (China)

^c PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

OUTER MEMBRANE PROTEIN; TRANSLOCATOR PROTEIN; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; BZRP PROTEIN, MOUSE; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIRTH RATE; BRONCHOALVEOLAR LAVAGE FLUID; CELL VIABILITY; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION PROFILING; HETEROZYGOTE; HOMEOSTASIS; LUNG ALVEOLUS EPITHELIUM CELL; LUNG ALVEOLUS MACROPHAGE; LUNG PARENCHYMA; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RNA SEQUENCE; SEQUENCE ANALYSIS; TSPO GENE; ANIMAL; ANTIBODY SPECIFICITY; CLUSTER ANALYSIS; FEMALE; GENE TARGETING; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHENOTYPE;

ANIMALS; CLUSTER ANALYSIS; FEMALE; GENE DELETION; GENE EXPRESSION PROFILING; GENE TARGETING; MACROPHAGES, ALVEOLAR; MALE; MICE; MICE, KNOCKOUT; ORGAN SPECIFICITY; PHENOTYPE; RECEPTORS, GABA; TRANSCRIPTOME;

EID: 84999861890     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0167307     Document Type: Article

References (52)

1. Anholt RR, Pedersen PL, De Souza EB, Snyder SH (1986) The peripheral-type benzodiazepine receptor. Localization to the mitochondrial outer membrane. J Biol Chem 261: 576-583. PMID: 3001071
2. Murail S, Robert JC, Coic YM, Neumann JM, Ostuni MA, Yao ZX, et al. (2008) Secondary and tertiary structures of the transmembrane domains of the translocator protein TSPO determined by NMR. Stabilization of the TSPO tertiary fold upon ligand binding. Biochim Biophys Acta 1778: 1375-1381. doi: 10. 1016/j.bbamem.2008.03.012 PMID: 18420025
3. Gavish M, Bachman I, Shoukrun R, Katz Y, Veenman L, Weisinger G, et al. (1999) Enigma of the peripheral benzodiazepine receptor. Pharmacol Rev 51: 629-650. PMID: 10581326
4. Banati RB, Middleton RJ, Chan R, Hatty CR, Wai-Ying Kam W, Quin C, et al. (2014) Positron emission tomography and functional characterization of a complete PBR/TSPO knockout. Nat Commun 5: 5452. doi: 10.1038/ncomms6452 PMID: 25406832
5. Stocco DM (2014) The Role of PBR/TSPO in Steroid Biosynthesis Challenged. Endocrinology 155: 6-9. doi: 10.1210/en.2013-2041 PMID: 24364584
6. Karlstetter M, Nothdurfter C, Aslanidis A, Moeller K, Horn F, Scholz R, et al. (2014) Translocator protein (18 kDa) (TSPO) is expressed in reactive retinal microglia and modulates microglial inflammation and phagocytosis. J Neuroimmunol 11: 3.
7. Hatori A, Yui J, Yamasaki T, Xie L, Kumata K, Fujinaga M, et al. (2012) PET imaging of lung inflammation with [18F]FEDAC, a radioligand for translocator protein (18 kDa). PLoS One 7: e45065. doi: 10.1371/journal.pone.0045065 PMID: 22984611
8. Rupprecht R, Papadopoulos V, Rammes G, Baghai TC, Fan J, Akula N, et al. (2010) Translocator protein (18 kDa)(TSPO) as a therapeutic target for neurological and psychiatric disorders. Nat Rev Drug Discov 9: 971-988. doi: 10.1038/nrd3295 PMID: 21119734
9. Liu GJ, Middleton RJ, Hatty CR, Kam WW, Chan R, Pham T, et al. (2014) The 18 kDa Translocator Protein, Microglia and Neuroinflammation. Brain Pathol 24: 631-653. doi: 10.1111/bpa.12196 PMID: 25345894
10. Mirzaei N, Tang SP, Ashworth S, Coello C, Plisson C, Passchier J, et al. (2016) In vivo imaging of microglial activation by positron emission tomography with [11C] PBR28 in the 5XFAD model of Alzheimer's disease. Glia 64: 993-1006. doi: 10.1002/glia.22978 PMID: 26959396
11. Papadopoulos V, Amri H, Boujrad N, Cascio C, Culty M, Garnier M, et al. (1997) Peripheral benzodiazepine receptor in cholesterol transport and steroidogenesis. Steroids 62: 21-28. PMID: 9029710
12. Morohaku K, Pelton SH, Daugherty DJ, Butler WR, Deng W, Selvaraj V (2014) Translocator Protein/Peripheral Benzodiazepine Receptor Is Not Required for Steroid Hormone Biosynthesis. Endocrinology 155: 89-97. doi: 10.1210/en.2013-1556 PMID: 24174323
13. S J., Blachly-Dyson E, Sewell R, Carpi A, Menabò R, Di-Lisa F, et al. (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. doi: 10.1074/jbc. M114.549634 PMID: 24692541
14. Selvaraj V, Tu LN, Stocco DM (2016) Crucial role reported for TSPO in viability and steroidogenesis is a misconception. A commentary on: Conditional steroidogenic cell-targeted deletion of TSPO unveils a crucial role in viability and hormone-dependent steroid formation by Fan, J., Campioli, E., Midzak, A., Culty, M., and Papadopoulos, V.(2015). Proc. Natl. Acad. Sci. USA. 112, 7261-7266. Front Endocrinol 7: 91.
15. O'Gorman S, Dagenais NA, Qian M, Marchuk Y (1997) Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc Natl Acad Sci U S A 94: 14602-14607. PMID: 9405659
16. Seidler B, Schmidt A, Mayr U, Nakhai H, Schmid RM, Schneider G, et al. (2008) A Cre-loxP-based mouse model for conditional somatic gene expression and knockdown in vivo by using avian retroviral vectors. Proc Natl Acad Sci U S A 105: 10137-10142. doi: 10.1073/pnas.0800487105 PMID: 18621715
17. Tu LN, Morohaku K, Manna PR, Pelton SH, Butler WR, Stocco DM, et al. (2014) Peripheral Benzodiazepine Receptor/Translocator Protein Global Knockout Mice are Viable with no Effects on Steroid Hormone Biosynthesis. J Biol Chem 289: 27444-27454. doi: 10.1074/jbc.M114.578286 PMID: 24936060
18. https://www.jax.org/jax-mice-and-services/customer-support/technical-support/genotyping-resources/dna-isolation-protocols#. The Jackson Laboratory.
19. Yin S, Zhang J, Mao Y, Hu Y, Cui L, Kang N, et al. (2013) Vav1-phospholipase C-γ1 (Vav1-PLC-γ1) Pathway Initiated by T Cell Antigen Receptor (TCRγδ) Activation Is Required to Overcome Inhibition by Ubiquitin Ligase Cbl-b during γδT Cell Cytotoxicity. J Biol Chem 288: 26448-26462. doi: 10.1074/jbc. M113.484600 PMID: 23897818
20. Anders S, HuberW(2012) Differential expression of RNA-Seq data at the gene level-The DESeq package. Heidelberg, Germany: European Molecular Biology Laboratory (EMBL).
21. Anders S (2010) Analysing RNA-Seq data with the DESeq package. Mol Biol 43: 1-17.
22. Wang W, Gao Z, Wang H, Li T, He W, Lv W, et al. (2016) Transcriptome Analysis Reveals Distinct Gene Expression Profiles in Eosinophilic and Noneosinophilic Chronic Rhinosinusitis with Nasal Polyps. Sci Rep 6: 26604. doi: 10.1038/srep26604 PMID: 27216292
23. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29. PMID: 10802651
24. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30. PMID: 10592173
25. Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57. doi: 10.1038/nprot.2008.211 PMID: 19131956
26. Huang DW, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13. doi: 10.1093/nar/gkn923 PMID: 19033363
27. Thorvaldsdottir H, Robinson JT, Mesirov JP (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14: 178-192. doi: 10.1093/bib/bbs017 PMID: 22517427
28. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, et al. (2011) Integrative genomics viewer. Nat Biotechnol 29: 24-26. doi: 10.1038/nbt.1754 PMID: 21221095
29. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868. PMID: 9843981
30. Yin S, Mao Y, Li X, Yue C, Zhou C, Huang L, et al. (2015) Hyperactivation and in situ recruitment of inflammatory Vδ2 T cells contributes to disease pathogenesis in systemic lupus erythematosus. Sci Rep 5: 14432. doi: 10.1038/srep14432 PMID: 26395317
31. Huttlin EL, Ting L, Bruckner RJ, Gebreab F, Gygi MP, Szpyt J, et al. (2015) The BioPlex Network: A Systematic Exploration of the Human Interactome. Cell 162: 425-440. doi: 10.1016/j.cell.2015.06.043 PMID: 26186194
32. Liu J, Rone MB, Papadopoulos V (2006) Protein-protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis. J Biol Chem 281: 38879-38893. doi: 10.1074/jbc.M608820200 PMID: 17050526
33. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, et al. (2015) STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43: D447-452. doi: 10.1093/nar/gku1003 PMID: 25352553
34. Hussell T, Bell TJ (2014) Alveolar macrophages: plasticity in a tissue-specific context. Nat Rev Immunol 14: 81-93. doi: 10.1038/nri3600 PMID: 24445666
35. Papadopoulos V, Baraldi M, Guilarte TR, Knudsen TB, Lacapère JJ, Lindemann P, et al. (2006) Translocator protein (18kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 27: 402-409. doi: 10.1016/j.tips.2006.06. 005 PMID: 16822554
36. Korkhov VM, Sachse C, Short JM, Tate CG (2010) Three-dimensional structure of TspO by electron cryomicroscopy of helical crystals. Structure 18: 677-687. doi: 10.1016/j.str.2010.03.001 PMID: 20541505
37. Li F, Liu J, Zheng Y, Garavito RM, Ferguson-Miller S (2015) Protein structure. Crystal structures of translocator protein (TSPO) and mutant mimic of a human polymorphism. Science 347: 555-558. PMID: 25635101
38. Guo Y, Kalathur RC, Liu Q, Kloss B, Bruni R, Ginter C, et al. (2015) Protein structure. Structure and activity of tryptophan-rich TSPO proteins. Science 347: 551-555. PMID: 25635100
39. Tu LN, Zhao AH, Stocco DM, Selvaraj V (2015) PK11195 effect on steroidogenesis is not mediated through the translocator protein (TSPO). Endocrinology 156: 1033-1039. doi: 10.1210/en.2014-1707 PMID: 25535830
40. Zhao AH, Tu LN, Mukai C, Sirivelu MP, Pillai VV, Morohaku K, et al. (2016) Mitochondrial Translocator Protein (TSPO) Function Is Not Essential for Heme Biosynthesis. J Biol Chem 291: 1591-1603. doi: 10.1074/jbc.M115.686360 PMID: 26627829
41. Tu LN, Zhao AH, Hussein M, Stocco DM, Selvaraj V (2016) Translocator Protein (TSPO) Affects Mitochondrial Fatty Acid Oxidation in Steroidogenic Cells. Endocrinology 157: 1110-1121. doi: 10.1210/en. 2015-1795 PMID: 26741196
42. Daugherty DJ, Chechneva O, Mayrhofer F, DengW(2016) The hGFAP-driven conditional TSPO knockout is protective in a mouse model of multiple sclerosis. Sci Rep 6: 22556. doi: 10.1038/srep22556 PMID: 26925573
43. Barron AM, Garcia-Segura LM, Caruso D, Jayaraman A, Lee JW, Melcangi RC, et al. (2013) Ligand for translocator protein reverses pathology in a mouse model of Alzheimer's disease. J Neurosci 33: 8891-8897. doi: 10.1523/JNEUROSCI.1350-13.2013 PMID: 23678130
44. Rupprecht R, Rammes G, Eser D, Baghai TC, Schule C, Nothdurfter C, et al. (2009) Translocator Protein (18 kD) as Target for Anxiolytics Without Benzodiazepine-Like Side Effects. Science 325: 490-493. doi: 10.1126/science.1175055 PMID: 19541954
45. Daugherty DJ, Selvaraj V, Chechneva OV, Liu XB, Pleasure DE, Deng WB (2013) A TSPO ligand is protective in a mouse model of multiple sclerosis. EMBO Mol Med 5: 891-903. doi: 10.1002/emmm. 201202124 PMID: 23681668
46. Fan J, Campioli E, Midzak A, Culty M, Papadopoulos V (2015) Conditional steroidogenic cell-targeted deletion of TSPO unveils a crucial role in viability and hormone-dependent steroid formation. Proc Natl Acad Sci U S A 112: 7261-7266. doi: 10.1073/pnas.1502670112 PMID: 26039990
47. Selvaraj V, Stocco DM, Tu LN (2015) Minireview: Translocator Protein (TSPO) and Steroidogenesis: A Reappraisal. Mol Endocrinol 29: 490-501. doi: 10.1210/me.2015-1033 PMID: 25730708
48. Hatty CR, Banati RB (2015) Protein-ligand and membrane-ligand interactions in pharmacology: The case of the translocator protein (TSPO). Pharmacol Res 100: 58-63. doi: 10.1016/j.phrs.2015.07.029 PMID: 26238176
49. Guilarte TR, Loth MK, Guariglia SR (2016) TSPO Finds NOX2 in Microglia for Redox Homeostasis. Trends Pharmacol Sci 37: 334-343.
50. Selvaraj V, Tu LN (2016) Current status and future perspectives: TSPO in steroid neuroendocrinology. J Endocrinol 231: R1-R30. doi: 10.1530/JOE-16-0241 PMID: 27422254
51. Middleton RJ, Liu GJ, Banati RB (2015) 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 43: 553-558. doi: 10.1042/BST20150039 PMID: 26551692
52. Selvaraj V, Stocco DM (2015) The changing landscape in translocator protein (TSPO) function. Trends Endocrinol Metab 26: 341-348. doi: 10.1016/j.tem.2015.02.007 PMID: 25801473