Augmented expression of TSPO after intracerebral hemorrhage: A role in inflammation?

Journal of Neuroinflammation

Volumn 13, Issue 1, 2016, Pages

  Bonsack, Frederick ^a   Alleyne, Cargill H ^a   Sukumari Ramesh, Sangeetha ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

ICH; Microglial activation; TSPO

Indexed keywords

MEMBRANE PROTEIN; PROTEIN TSPO; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; BZRP PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY DETECTION; ARTICLE; BRAIN HEMORRHAGE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; MACROPHAGE; MALE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEQUENCE HOMOLOGY; ANIMAL; BIOSYNTHESIS; BRAIN; CELL LINE; GENE EXPRESSION; GENE SILENCING; GENETICS; INFLAMMATION; METABOLISM; PATHOLOGY; PROCEDURES;

ANIMALS; BRAIN; CELL LINE; CEREBRAL HEMORRHAGE; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; INFLAMMATION; MALE; MICE; RECEPTORS, GABA;

EID: 84975261037     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-016-0619-2     Document Type: Article

References (83)

1. Qureshi AI, Ling GS, Khan J, Suri MF, Miskolczi L, et al. Quantitative analysis of injured, necrotic, and apoptotic cells in a new experimental model of intracerebral hemorrhage. Crit Care Med. 2001;29:152-7.
2. van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, et al. Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol. 2010;9:167-76.
3. Nilsson OG, Lindgren A, Brandt L, Saveland H. Prediction of death in patients with primary intracerebral hemorrhage: a prospective study of a defined population. J Neurosurg. 2002;97:531-6.
4. Broderick JP, Adams Jr HP, Barsan W, Feinberg W, Feldmann E, et al. Guidelines for the management of spontaneous intracerebral hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke. 1999;30:905-15.
5. Broderick J, Connolly S, Feldmann E, Hanley D, Kase C, et al. Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Association Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisciplinary Working Group. Stroke. 2007;38:2001-23.
6. Casellas P, Galiegue S, Basile AS. Peripheral benzodiazepine receptors and mitochondrial function. Neurochem Int. 2002;40:475-86.
7. Braestrup C, Albrechtsen R, Squires RF. High densities of benzodiazepine receptors in human cortical areas. Nature. 1977;269:702-4.
8. Papadopoulos V, Baraldi M, Guilarte TR, Knudsen TB, Lacapere JJ, et al. Translocator protein (18 kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci. 2006;27:402-9.
9. Sprengel R, Werner P, Seeburg PH, Mukhin AG, Santi MR, et al. Molecular cloning and expression of cDNA encoding a peripheral-type benzodiazepine receptor. J Biol Chem. 1989;264:20415-21.
10. Parola AL, Stump DG, Pepperl DJ, Krueger KE, Regan JW, et al. Cloning and expression of a pharmacologically unique bovine peripheral-type benzodiazepine receptor isoquinoline binding protein. J Biol Chem. 1991;266:14082-7.
11. Riond J, Mattei MG, Kaghad M, Dumont X, Guillemot JC, et al. Molecular cloning and chromosomal localization of a human peripheral-type benzodiazepine receptor. Eur J Biochem. 1991;195:305-11.
12. Chang YJ, McCabe RT, Rennert H, Budarf ML, Sayegh R, et al. The human "peripheral-type" benzodiazepine receptor: regional mapping of the gene and characterization of the receptor expressed from cDNA. DNA Cell Biol. 1992;11:471-80.
13. Garnier M, Dimchev AB, Boujrad N, Price JM, Musto NA, et al. In vitro reconstitution of a functional peripheral-type benzodiazepine receptor from mouse Leydig tumor cells. Mol Pharmacol. 1994;45:201-11.
14. Anholt RR, Pedersen PL, De Souza EB, Snyder SH. The peripheral-type benzodiazepine receptor. Localization to the mitochondrial outer membrane. J Biol Chem. 1986;261:576-83.
15. Mukhin AG, Papadopoulos V, Costa E, Krueger KE. Mitochondrial benzodiazepine receptors regulate steroid biosynthesis. Proc Natl Acad Sci U S A. 1989;86:9813-6.
16. Krueger KE, Papadopoulos V. Peripheral-type benzodiazepine receptors mediate translocation of cholesterol from outer to inner mitochondrial membranes in adrenocortical cells. J Biol Chem. 1990;265:15015-22.
17. Rupprecht R, Papadopoulos V, Rammes G, Baghai TC, Fan J, et al. Translocator protein (18 kDa) (TSPO) as a therapeutic target for neurological and psychiatric disorders. Nat Rev Drug Discov. 2010;9:971-88.
18. Costa E, Auta J, Guidotti A, Korneyev A, Romeo E. The pharmacology of neurosteroidogenesis. J Steroid Biochem Mol Biol. 1994;49:385-9.
19. 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.
20. Romeo E, Cavallaro S, Korneyev A, Kozikowski AP, Ma D, et al. Stimulation of brain steroidogenesis by 2-aryl-indole-3-acetamide derivatives acting at the mitochondrial diazepam-binding inhibitor receptor complex. J Pharmacol Exp Ther. 1993;267:462-71.
21. Morohaku K, Pelton SH, Daugherty DJ, Butler WR, Deng W, et al. Translocator protein/peripheral benzodiazepine receptor is not required for steroid hormone biosynthesis. Endocrinology. 2014;155:89-97.
22. Banati RB, Middleton RJ, Chan R, Hatty CR, Kam WW, et al. Positron emission tomography and functional characterization of a complete PBR/TSPO knockout. Nat Commun. 2014;5:5452.
23. Tu LN, Morohaku K, Manna PR, Pelton SH, Butler WR, et al. Peripheral benzodiazepine receptor/translocator protein global knock-out mice are viable with no effects on steroid hormone biosynthesis. J Biol Chem. 2014;289:27444-54.
24. Chen MK, Guilarte TR. Translocator protein 18 kDa (TSPO): molecular sensor of brain injury and repair. Pharmacol Ther. 2008;118:1-17.
25. Cosenza-Nashat M, Zhao ML, Suh HS, Morgan J, Natividad R, et al. Expression of the translocator protein of 18 kDa by microglia, macrophages and astrocytes based on immunohistochemical localization in abnormal human brain. Neuropathol Appl Neurobiol. 2009;35:306-28.
26. 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.
27. Liu J, Rone MB, Papadopoulos V. Protein-protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis. J Biol Chem. 2006;281:38879-93.
28. Maeda J, Higuchi M, Inaji M, Ji B, Haneda E, et al. Phase-dependent roles of reactive microglia and astrocytes in nervous system injury as delineated by imaging of peripheral benzodiazepine receptor. Brain Res. 2007;1157:100-11.
29. Zurcher NR, Loggia ML, Lawson R, Chonde DB, Izquierdo-Garcia D, et al. Increased in vivo glial activation in patients with amyotrophic lateral sclerosis: assessed with [(11)C]-PBR28. Neuroimage Clin. 2015;7:409-14.
30. Karlstetter M, Nothdurfter C, Aslanidis A, Moeller K, Horn F, et al. Translocator protein (18 kDa) (TSPO) is expressed in reactive retinal microglia and modulates microglial inflammation and phagocytosis. J Neuroinflammation. 2014;11:3.
31. Liu GJ, Middleton RJ, Hatty CR, Kam WW, Chan R, et al. The 18 kDa translocator protein, microglia and neuroinflammation. Brain Pathol. 2014;24:631-53.
32. Politis M, Su P, Piccini P. Imaging of microglia in patients with neurodegenerative disorders. Front Pharmacol. 2012;3:96.
33. Venneti S, Lopresti BJ, Wiley CA. Molecular imaging of microglia/macrophages in the brain. Glia. 2013;61:10-23.
34. Nothdurfter C, Baghai TC, Schule C, Rupprecht R. Translocator protein (18 kDa) (TSPO) as a therapeutic target for anxiety and neurologic disorders. Eur Arch Psychiatry Clin Neurosci. 2012;262 Suppl 2:S107-12.
35. Sukumari-Ramesh S, Alleyne Jr CH, Dhandapani KM. Astrocyte-specific expression of survivin after intracerebral hemorrhage in mice: a possible role in reactive gliosis? J Neurotrauma. 2012;29:2798-804.
36. Sukumari-Ramesh S, Alleyne Jr CH, Dhandapani KM. Astrogliosis: a target for intervention in intracerebral hemorrhage? Transl Stroke Res. 2012;3:80-7.
37. Laird MD, Sukumari-Ramesh S, Swift AE, Meiler SE, Vender JR, et al. Curcumin attenuates cerebral edema following traumatic brain injury in mice: a possible role for aquaporin-4? J Neurochem. 2010;113:637-48.
38. Emsley HC, Tyrrell PJ. Inflammation and infection in clinical stroke. J Cereb Blood Flow Metab. 2002;22:1399-419.
39. Qureshi AI, Tuhrim S, Broderick JP, Batjer HH, Hondo H, et al. Spontaneous intracerebral hemorrhage. N Engl J Med. 2001;344:1450-60.
40. Sukumari-Ramesh S, Alleyne Jr CH, Dhandapani KM. The histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) confers acute neuroprotection after intracerebral hemorrhage in mice. Transl Stroke Res. 2016;7:141-8.
41. Sukumari-Ramesh S, Alleyne Jr CH. Post-injury administration of tert-butylhydroquinone attenuates acute neurological injury after intracerebral hemorrhage in mice. J Mol Neurosci. 2016;58:525-31.
42. Lin S, Yin Q, Zhong Q, Lv FL, Zhou Y, et al. Heme activates TLR4-mediated inflammatory injury via MyD88/TRIF signaling pathway in intracerebral hemorrhage. J Neuroinflammation. 2012;9:46.
43. O'Donnell MJ, Xavier D, Liu L, Zhang H, Chin SL, et al. Risk factors for ischaemic and intracerebral haemorrhagic stroke in 22 countries (the INTERSTROKE study): a case-control study. Lancet. 2010;376:112-23.
44. Aguilar MI, Freeman WD. Spontaneous intracerebral hemorrhage. Semin Neurol. 2010;30:555-64.
45. Broderick J, Connolly S, Feldmann E, Hanley D, Kase C, et al. Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Association Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisciplinary Working Group. Circulation. 2007;116:e391-413.
46. Ribo M, Grotta JC. Latest advances in intracerebral hemorrhage. Curr Neurol Neurosci Rep. 2006;6:17-22.
47. Wang J. Preclinical and clinical research on inflammation after intracerebral hemorrhage. Prog Neurobiol. 2010;92:463-77.
48. Xi G, Keep RF, Hoff JT. Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol. 2006;5:53-63.
49. Diringer MN. Intracerebral hemorrhage: pathophysiology and management. Crit Care Med. 1993;21:1591-603.
50. Greve MW, Zink BJ. Pathophysiology of traumatic brain injury. Mt Sinai J Med. 2009;76:97-104.
51. Dirnagl U, Iadecola C, Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 1999;22:391-7.
52. Wang J, Dore S. Inflammation after intracerebral hemorrhage. J Cereb Blood Flow Metab. 2007;27:894-908.
53. Carmichael ST, Vespa PM, Saver JL, Coppola G, Geschwind DH, et al. Genomic profiles of damage and protection in human intracerebral hemorrhage. J Cereb Blood Flow Metab. 2008;28:1860-75.
54. Aronowski J, Hall CE. New horizons for primary intracerebral hemorrhage treatment: experience from preclinical studies. Neurol Res. 2005;27:268-79.
55. Zhang D, Hu X, Qian L, Wilson B, Lee C, et al. Prostaglandin E2 released from activated microglia enhances astrocyte proliferation in vitro. Toxicol Appl Pharmacol. 2009;238:64-70.
56. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science. 2005;308:1314-8.
57. Liao B, Zhao W, Beers DR, Henkel JS, Appel SH. Transformation from a neuroprotective to a neurotoxic microglial phenotype in a mouse model of ALS. Exp Neurol. 2012;237:147-52.
58. Kobayashi K, Imagama S, Ohgomori T, Hirano K, Uchimura K, et al. Minocycline selectively inhibits M1 polarization of microglia. Cell Death Dis. 2013;4, e525.
59. Ponomarev ED, Maresz K, Tan Y, Dittel BN. CNS-derived interleukin-4 is essential for the regulation of autoimmune inflammation and induces a state of alternative activation in microglial cells. J Neurosci. 2007;27:10714-21.
60. Wang J, Rogove AD, Tsirka AE, Tsirka SE. Protective role of tuftsin fragment 1-3 in an animal model of intracerebral hemorrhage. Ann Neurol. 2003;54:655-64.
61. Moller T, Hanisch UK, Ransom BR. Thrombin-induced activation of cultured rodent microglia. J Neurochem. 2000;75:1539-47.
62. van Rossum D, Hanisch UK. Microglia. Metab Brain Dis. 2004;19:393-411.
63. Aronowski J, Zhao X. Molecular pathophysiology of cerebral hemorrhage: secondary brain injury. Stroke. 2011;42:1781-6.
64. Babu R, Bagley JH, Di C, Friedman AH, Adamson C. Thrombin and hemin as central factors in the mechanisms of intracerebral hemorrhage-induced secondary brain injury and as potential targets for intervention. Neurosurg Focus. 2012;32, E8.
65. Letarte PB, Lieberman K, Nagatani K, Haworth RA, Odell GB, et al. Hemin: levels in experimental subarachnoid hematoma and effects on dissociated vascular smooth-muscle cells. J Neurosurg. 1993;79:252-5.
66. Wang M, Wang X, Zhao L, Ma W, Rodriguez IR, et al. Macroglia-microglia interactions via TSPO signaling regulates microglial activation in the mouse retina. J Neurosci. 2014;34:3793-806.
67. Kuhlmann AC, Guilarte TR. Cellular and subcellular localization of peripheral benzodiazepine receptors after trimethyltin neurotoxicity. J Neurochem. 2000;74:1694-704.
68. Gomez-Nicola D, Fransen NL, Suzzi S, Perry VH. Regulation of microglial proliferation during chronic neurodegeneration. J Neurosci. 2013;33:2481-93.
69. Ganter S, Northoff H, Mannel D, Gebicke-Harter PJ. Growth control of cultured microglia. J Neurosci Res. 1992;33:218-30.
70. Kloss CU, Kreutzberg GW, Raivich G. Proliferation of ramified microglia on an astrocyte monolayer: characterization of stimulatory and inhibitory cytokines. J Neurosci Res. 1997;49:248-54.
71. Mander PK, Jekabsone A, Brown GC. Microglia proliferation is regulated by hydrogen peroxide from NADPH oxidase. J Immunol. 2006;176:1046-52.
72. Veiga S, Carrero P, Pernia O, Azcoitia I, Garcia-Segura LM. Translocator protein 18 kDa is involved in the regulation of reactive gliosis. Glia. 2007;55:1426-36.
73. Ma L, Zhang H, Liu N, Wang PQ, Guo WZ, et al. TSPO ligand PK11195 alleviates neuroinflammation and beta-amyloid generation induced by systemic LPS administration. Brain Res Bull. 2016;121:192-200.
74. Zhao YY, Yu JZ, Li QY, Ma CG, Lu CZ, et al. TSPO-specific ligand vinpocetine exerts a neuroprotective effect by suppressing microglial inflammation. Neuron Glia Biol. 2011;7:187-97.
75. Ferzaz B, Brault E, Bourliaud G, Robert JP, Poughon G, et al. SSR180575 (7-chloro-N, N,5-trimethyl-4-oxo-3-phenyl-3,5-dihydro-4H-pyridazino[4,5-b]indole-1 -acetamide), a peripheral benzodiazepine receptor ligand, promotes neuronal survival and repair. J Pharmacol Exp Ther. 2002;301:1067-78.
76. Ryu JK, Choi HB, McLarnon JG. Peripheral benzodiazepine receptor ligand PK11195 reduces microglial activation and neuronal death in quinolinic acid-injected rat striatum. Neurobiol Dis. 2005;20:550-61.
77. Veenman L, Leschiner S, Spanier I, Weisinger G, Weizman A, et al. PK 11195 attenuates kainic acid-induced seizures and alterations in peripheral-type benzodiazepine receptor (PBR) protein components in the rat brain. J Neurochem. 2002;80:917-27.
78. Veiga S, Azcoitia I, Garcia-Segura LM. Ro5-4864, a peripheral benzodiazepine receptor ligand, reduces reactive gliosis and protects hippocampal hilar neurons from kainic acid excitotoxicity. J Neurosci Res. 2005;80:129-37.
79. Scholz R, Sobotka M, Caramoy A, Stempfl T, Moehle C, et al. Minocycline counter-regulates pro-inflammatory microglia responses in the retina and protects from degeneration. J Neuroinflammation. 2015;12:209.
80. Ferrero P, Santi MR, Conti-Tronconi B, Costa E, Guidotti A. Study of an octadecaneuropeptide derived from diazepam binding inhibitor (DBI): biological activity and presence in rat brain. Proc Natl Acad Sci U S A. 1986;83:827-31.
81. Yanase H, Shimizu H, Yamada K, Iwanaga T. Cellular localization of the diazepam binding inhibitor in glial cells with special reference to its coexistence with brain-type fatty acid binding protein. Arch Histol Cytol. 2002;65:27-36.
82. Hong SH, Choi HB, Kim SU, McLarnon JG. Mitochondrial ligand inhibits store-operated calcium influx and COX-2 production in human microglia. J Neurosci Res. 2006;83:1293-8.
83. Hirsch T, Decaudin D, Susin SA, Marchetti P, Larochette N, et al. PK11195, a ligand of the mitochondrial benzodiazepine receptor, facilitates the induction of apoptosis and reverses Bcl-2-mediated cytoprotection. Exp Cell Res. 1998;241:426-34.