Decreased hippocampal translocator protein (18kDa) expression in alcohol dependence: A [11C]PBR28 PET study

Translational Psychiatry

Volumn 7, Issue 1, 2017, Pages

  Kalk, N J ^a   Guo, Q ^a,b   Owen, D ^b   Cherian, R ^c   Erritzoe, D ^b   Gilmour, A ^d   Ribeiro, A S ^b   McGonigle, J ^b   Waldman, A ^b   Matthews, P ^b   Cavanagh, J ^d   McInnes, I ^d   Dar, K ^e   Gunn, R ^f   Rabiner, E A ^f   Lingford Hughes, A R ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c WEST LONDON MENTAL HEALTH NHS TRUST   (United Kingdom)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e CENTRAL AND NORTH WEST LONDON NHS FOUNDATION TRUST   (United Kingdom)

^f Imanova Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

18KDA TRANSLOCATOR PROTEIN; ACEBUTOLOL; ALANINE AMINOTRANSFERASE; ALBUMIN; ALKALINE PHOSPHATASE; ALPHA INTERFERON; BENZODIAZEPINE DERIVATIVE; BILIRUBIN; BRAIN PROTEIN; C REACTIVE PROTEIN; CARRIER PROTEIN; CHLORDIAZEPOXIDE; DIAZEPAM; GAMMA GLUTAMYLTRANSFERASE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; PBR28 C 11; RADIOLIGAND; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; ACETAMIDE DERIVATIVE; CARBON; N-(2-METHOXYBENZYL)-N-(4-PHENOXYPYRIDIN-3-YL)ACETAMIDE; PYRIDINE DERIVATIVE; RADIOPHARMACEUTICAL AGENT; TSPO PROTEIN, HUMAN;

ADULT; ALCOHOLISM; ANTERIOR CINGULATE; ANXIETY; ARTICLE; ASTROCYTE; BRAIN REGION; CELL ACTIVATION; CELL DENSITY; CEREBELLUM; CLINICAL ARTICLE; CONTROLLED STUDY; DEPRESSION; DETOXIFICATION; EVALUATION STUDY; EXECUTIVE FUNCTION; FATIGUE SEVERITY SCALE; GENOTYPE; HIPPOCAMPUS; HUMAN; LEUKOCYTE COUNT; MALE; MESENCEPHALON; MICROGLIA; MIDDLE AGED; NEUROIMAGING; PARTIAL THROMBOPLASTIN TIME; POSITRON EMISSION TOMOGRAPHY; PROTEIN EXPRESSION; PSYCHOPHARMACOTHERAPY; SPATIAL MEMORY; THALAMUS; VERBAL MEMORY; VOLUME OF DISTRIBUTION; VOXEL BASED MORPHOMETRY; YOUNG ADULT; CASE CONTROL STUDY; DIAGNOSTIC IMAGING; DRUG CONTAMINATION; FEMALE; METABOLISM;

ACETAMIDES; ALCOHOLISM; ASTROCYTES; CARBON RADIOISOTOPES; CASE-CONTROL STUDIES; DRUG CONTAMINATION; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MICROGLIA; MIDDLE AGED; POSITRON-EMISSION TOMOGRAPHY; PYRIDINES; RADIOPHARMACEUTICALS; RECEPTORS, GABA;

EID: 85022153714     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2016.264     Document Type: Article

References (75)

1. Davies SJ, Pandit SA, Feeney A, Stevenson BJ, Kerwin RW, Nutt DJ et al. Is there cognitive impairment in clinically 'healthy' abstinent alcohol dependence? Alcohol Alcohol 2005; 40: 498-503.
2. Stavro K, Pelletier J, Potvin S. Widespread and sustained cognitive deficits in alcoholism: A meta-analysis. Addict Biol 2013; 18: 203-213.
3. Bowden SC, Crews FT, Bates ME, Fals-Stewart W, Ambrose ML. Neurotoxicity and neurocognitive impairments with alcohol and drug-use disorders: potential roles in addiction and recovery. Alcohol Clin Exp Res 2001; 25: 317-321.
4. Allsop S, Saunders B, Phillips M. The process of relapse in severely dependent male problem drinkers. Addiction 2000; 95: 95-106.
5. Blume AW, Schmaling KB, Marlatt GA. Memory, executive cognitive function, and readiness to change drinking behavior. Addict Behav 2005; 30: 301-314.
6. Bartels C, Kunert HJ, Stawicki S, Kroner-Herwig B, Ehrenreich H, Krampe H. Recovery of hippocampus-related functions in chronic alcoholics during monitored long-term abstinence. Alcohol Alcohol 2007; 42: 92-102.
7. Zahr NM, Kaufman KL, Harper CG. Clinical and pathological features of alcoholrelated brain damage. Nat Rev Neurol 2011; 7: 284-294.
8. Duka T, Townshend JM, Collier K, Stephens DN. Impairment in cognitive functions after multiple detoxifications in alcoholic inpatients. Alcohol Clin Exp Res 2003; 27: 1563-1572.
9. Duka T, Gentry J, Malcolm R, Ripley TL, Borlikova G, Stephens DN et al. Consequences of multiple withdrawals from alcohol. Alcohol Clin Exp Res 2004; 28: 233-246.
10. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005; 308: 1314-1318.
11. Galea I, Bechmann I, Perry VH. What is immune privilege (not)? Trends Immunol 2007; 28: 153-160.
12. Grabert K, Michoel T, Karavolos MH, Clohisey S, Baillie JK, Stevens MP et al. Microglial brain region-dependent diversity and selective regional sensitivities to aging. Nat Neurosci 2016; 19: 504-516.
13. Chao CC, Hu S, Molitor TW, Shaskan EG, Peterson PK. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J Immunol 1992; 149: 2736-2741.
14. Piani D, Spranger M, Frei K, Schaffner A, Fontana A. Macrophage-induced cytotoxicity of N-methyl-D-aspartate receptor positive neurons involves excitatory amino acids rather than reactive oxygen intermediates and cytokines. Eur J Immunol 1992; 22: 2429-2436.
15. Morgan SC, Taylor DL, Pocock JM. Microglia release activators of neuronal proliferation mediated by activation of mitogen-activated protein kinase, phosphatidylinositol-3-kinase/Akt and delta-Notch signalling cascades. J Neurochem 2004; 90: 89-101.
16. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol 2010; 6: 193-201.
17. Nakajima K, Tohyama Y, Maeda S, Kohsaka S, Kurihara T. Neuronal regulation by which microglia enhance the production of neurotrophic factors for GABAergic, catecholaminergic, and cholinergic neurons. Neurochem Int 2007; 50: 807-820.
18. Wright GA, Sharifi Y, Newman TA, Davies N, Vairappan B, Perry HV et al. Characterisation of temporal microglia and astrocyte immune responses in bile ductligated rat models of cirrhosis. Liver Int 2014; 34: 1184-1191.
19. Obernier JA, White AM, Swartzwelder HS, Crews FT. Cognitive deficits and CNS damage after a 4-day binge ethanol exposure in rats. Pharmacol Biochem Behav 2002; 72: 521-532.
20. Qin L, He J, Hanes RN, Pluzarev O, Hong JS, Crews FT. Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J Neuroinflammation 2008; 5: 10.
21. He J, Overstreet DH, Crews FT. Abstinence from moderate alcohol selfadministration alters progenitor cell proliferation and differentiation in multiple brain regions of male and female P rats. Alcohol Clin Exp Res 2009; 33: 129-138.
22. Achur RN, Freeman WM, Vrana KE. Circulating cytokines as biomarkers of alcohol abuse and alcoholism. J Neuroimmune Pharmacol 2010; 5: 83-91.
23. Umhau JC, Schwandt M, Solomon MG, Yuan P, Nugent A, Zarate CA et al. Cerebrospinal fluid monocyte chemoattractant protein-1 in alcoholics: support for a neuroinflammatory model of chronic alcoholism. Alcohol Clin Exp Res 2014; 38: 1301-1306.
24. Tamborska E, Marangos PJ. Brain benzodiazepine binding sites in ethanol dependent and withdrawal states. Life Sci 1986; 38: 465-472.
25. Nixon K. Alcohol and adult neurogenesis: roles in neurodegeneration and recovery in chronic alcoholism. Hippocampus 2006; 16: 287-295.
26. Marshall SA, McClain JA, Kelso ML, Hopkins DM, Pauly JR, Nixon K. Microglial activation is not equivalent to neuroinflammation in alcohol-induced neurodegeneration: The importance of microglia phenotype. Neurobiol Dis 2013; 54: 239-251.
27. Lavisse S, Guillermier M, Herard AS, Petit F, Delahaye M, Van Camp N et al. Reactive astrocytes overexpress TSPO and are detected by TSPO positron emission tomography imaging. J Neurosci 2012; 32: 10809-10818.
28. Turkheimer FE, Edison P, Pavese N, Roncaroli F, Anderson AN, Hammers A et al. Reference and target region modeling of [11C]-(R)-PK11195 brain studies. J Nucl Med 2007; 48: 158-167.
29. Lockhart A, Davis B, Matthews JC, Rahmoune H, Hong G, Gee A et al. The peripheral benzodiazepine receptor ligand PK11195 binds with high affinity to the acute phase reactant alpha1-acid glycoprotein: implications for the use of the ligand as a CNS inflammatory marker. Nucl Med Biol 2003; 30: 199-206.
30. Cagnin A, Taylor-Robinson SD, Forton DM, Banati RB. In vivo imaging of cerebral "peripheral benzodiazepine binding sites" in patients with hepatic encephalopathy. Gut 2006; 55: 547-553.
31. Riikonen J, Jaatinen P, Rintala J, Porsti I, Karjala K, Hervonen A. Intermittent ethanol exposure increases the number of cerebellar microglia. Alcohol Alcohol 2002; 37: 421-426.
32. Owen DR, Guo Q, Kalk NJ, Colasanti A, Kalogiannopoulou D, Dimber R et al. Determination of [C]PBR28 binding potential in vivo: A first human TSPO blocking study. J Cereb Blood Flow Metab 2014; 19.
33. Kalk NJ, Owen DR, Tyacke RJ, Reynolds R, Rabiner EA, Lingford-Hughes AR et al. Are prescribed benzodiazepines likely to affect the availability of the 18 kDa translocator protein (TSPO) in PET studies?. Synapse 2013; 67: 909-912.
34. Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E et al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 1998; 59 (Suppl 20): 22-33.
35. Owen DR, Yeo AJ, Gunn RN, Song K, Wadsworth G, Lewis A et al. An 18-kDa translocator protein (TSPO) polymorphism explains differences in binding affinity of the PET radioligand PBR28. J Cereb Blood Flow Metab 2012; 32: 1-5.
36. Kreisl WC, Jenko KJ, Hines CS, Lyoo CH, Corona W, Morse CL et al. A genetic polymorphism for translocator protein 18 kDa affects both in vitro and in vivo radioligand binding in human brain to this putative biomarker of neuroinflammation. J Cereb Blood Flow Metab 2013; 33: 53-58.
37. Kreisl WC, Fujita M, Fujimura Y, Kimura N, Jenko KJ, Kannan P et al. Comparison of [(11)C]-(R)-PK 11195 and [(11)C]PBR28, two radioligands for translocator protein (18 kDa) in human and monkey: implications for positron emission tomographic imaging of this inflammation biomarker. Neuroimage 2010; 49: 2924-2932.
38. Sullivan JT, Sykora K, Schneiderman J, Naranjo CA, Sellers EM. Assessment of alcohol withdrawal: The revised clinical institute withdrawal assessment for alcohol scale (CIWA-Ar). Br J Addict 1989; 84: 1353-1357.
39. Skinner HA, Sheu WJ. Reliability of alcohol use indices. The Lifetime Drinking History and the MAST. J Stud Alcohol 1982; 43: 1157-1170.
40. Spielberger B. Manual for the State-Trait Anxiety Inventory. Consulting Psychologists Press: Palo Alto, CA, USA, 1983.
41. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry 1961; 4: 561-571.
42. Krupp LB, LaRocca NG, Muir-Nash J, Steinberg AD. The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol 1989; 46: 1121-1123.
43. Anton RF, Moak DH, Latham PK. The obsessive compulsive drinking scale: A new method of assessing outcome in alcoholism treatment studies. Arch Gen Psychiatry 1996; 53: 225-231.
44. Reitan RM. Validity of the Trail Making test as an indicator of organic brain damage. Percept Mot Skills 1958; 8: 271-276.
45. Osterrieth PA. The test of copying a complex figure: A contribution to the study of perception and memory. Arch Psychol 1944; 30: 286-356.
46. Weschler D. The Weschler Memory Scale -revised San Antonio. Psychological Corporation: San Antonio, TX, USA, 1987.
47. Searle GE. Kinetic analysis of [11C]-IMA107, a novel PET radiotracer for PDE10A. J Nucl Med Meeting Abstracts 2014; 55: 204.
48. Tziortzi AC, Searle GE, Tzimopoulou S, Salinas C, Beaver JD, Jenkinson M et al. Imaging dopamine receptors in humans with [11C]-(+)-PHNO: dissection of D3 signal and anatomy. Neuroimage 2011; 54: 264-277.
49. Fujita M, Imaizumi M, Zoghbi SS, Fujimura Y, Farris AG, Suhara T et al. Kinetic analysis in healthy humans of a novel positron emission tomography radioligand to image the peripheral benzodiazepine receptor, a potential biomarker for inflammation. Neuroimage 2008; 40: 43-52.
50. Coello C, Willoch F, Selnes P, Gjerstad L, Fladby T, Skretting A. Correction of partial volume effect in (18)F-FDG PET brain studies using coregistered MR volumes: voxel based analysis of tracer uptake in the white matter. Neuroimage 2013; 72: 183-192.
51. Ashburner J, Friston KJ. Computing average shaped tissue probability templates. Neuroimage 2009; 45: 333-341.
52. Ashburner J, Friston KJ. Voxel-based morphometry-the methods. Neuroimage 2000; 11(6 Pt 1): 805-821.
53. Guo Q, Owen DR, Rabiner EA, Turkheimer FE, Gunn RN. A graphical method to compare the in vivo binding potential of PET radioligands in the absence of a reference region: application to [C]PBR28 and [F]PBR111 for TSPO imaging. J Cereb Blood Flow Metab 2014; 34: 1162-1168.
54. Kumar A, Muzik O, Shandal V, Chugani D, Chakraborty P, Chugani HT. Evaluation of age-related changes in translocator protein (TSPO) in human brain using (11)C-[R]-PK11195 PET. J Neuroinflammation 2012; 9: 232.
55. Ribiere C, Hininger I, Saffar-Boccara C, Sabourault D, Nordmann R. Mitochondrial respiratory activity and superoxide radical generation in the liver, brain and heart after chronic ethanol intake. Biochem Pharmacol 1994; 47: 1827-1833.
56. Korbo L. Glial cell loss in the hippocampus of alcoholics. Alcohol Clin Exp Res 1999; 23: 164-168.
57. Bartsch AJ, Homola G, Biller A, Smith SM, Weijers HG, Wiesbeck GA et al. Manifestations of early brain recovery associated with abstinence from alcoholism. Brain 2007; 130(Pt 1): 36-47.
58. Mon A, Durazzo TC, Meyerhoff DJ. Glutamate, GABA, and other cortical metabolite concentrations during early abstinence from alcohol and their associations with neurocognitive changes. Drug Alcohol Depend 2012; 125: 27-36.
59. Varga B, Marko K, Hadinger N, Jelitai M, Demeter K, Tihanyi K et al. Translocator protein (TSPO 18kDa) is expressed by neural stem and neuronal precursor cells. Neurosci Lett 2009; 462: 257-262.
60. Sutherland GT, Sheahan PJ, Matthews J, Dennis CV, Sheedy DS, McCrossin T et al. The effects of chronic alcoholism on cell proliferation in the human brain. Exp Neurol 2013; 247: 9-18.
61. Turkheimer FE, Rizzo G, Bloomfield PS, Howes O, Zanotti-Fregonara P, Bertoldo A et al. The methodology of TSPO imaging with positron emission tomography. Biochem Soc Trans 2015; 43: 586-592.
62. Kraszpulski M, Tukaj C, Wrzolkowa T. Hippocampal capillaries in different age groups of chronically ethanol-intoxicated rats. Morphometrical studies. Folia Morphol (Warsz) 2000; 59: 121-129.
63. Zhao YN, Wang F, Fan YX, Ping GF, Yang JY, Wu CF. Activated microglia are implicated in cognitive deficits, neuronal death, and successful recovery following intermittent ethanol exposure. Behav Brain Res 2013; 236: 270-282.
64. Clark KH, Wiley CA, Bradberry CW. Psychostimulant abuse and neuroinflammation: emerging evidence of their interconnection. Neurotox Res 2013; 23: 174-188.
65. Narendran R, Jedema HP, Lopresti BJ, Mason NS, Himes ML, Bradberry CW. Decreased vesicular monoamine transporter type 2 availability in the striatum following chronic cocaine self-administration in nonhuman primates. Biol Psychiatry 2015; 77: 488-492.
66. Fontainhas AM, Wang M, Liang KJ, Chen S, Mettu P, Damani M et al. Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission. PLoS One 2011; 6: e15973.
67. Zhang H, Ma L, Yin YL, Dong LQ, Cheng GG, Ma YQ et al. Over-expression of TSPO in the hippocampal CA1 area alleviates cognitive dysfunction caused by lipopolysaccharide in mice. Brain Res 2016; 1646: 402-409.
68. Salter MW, Beggs S. Sublime microglia: expanding roles for the guardians of the CNS. Cell 2014; 158: 15-24.
69. Ota Y, Zanetti AT, Hallock RM. The role of astrocytes in the regulation of synaptic plasticity and memory formation. Neural Plast 2013; 2013: 185463.
70. Matthews DB, Morrow AL. Effects of acute and chronic ethanol exposure on spatial cognitive processing and hippocampal function in the rat. Hippocampus 2000; 10: 122-130.
71. Fama R, Rosenbloom MJ, Nichols BN, Pfefferbaum A, Sullivan EV. Working and episodic memory in HIV infection, alcoholism, and their comorbidity: baseline and 1-year follow-up examinations. Alcohol Clin Exp Res 2009; 33: 1815-1824.
72. Sullivan EV, Marsh L, Mathalon DH, Lim KO, Pfefferbaum A. Anterior hippocampal volume deficits in nonamnesic, aging chronic alcoholics. Alcohol Clin Exp Res 1995; 19: 110-122.
73. Sullivan EV, Marsh L, Mathalon DH, Lim KO, Pfefferbaum A. Relationship between alcohol withdrawal seizures and temporal lobe white matter volume deficits. Alcohol Clin Exp Res 1996; 20: 348-354.
74. Agartz I, Momenan R, Rawlings RR, Kerich MJ, Hommer DW. Hippocampal volume in patients with alcohol dependence. Arch Gen Psychiatry 1999; 56: 356-363.
75. Laakso MP, Vaurio O, Savolainen L, Repo E, Soininen H, Aronen HJ et al. A volumetric MRI study of the hippocampus in type 1 and 2 alcoholism. Behav Brain Res 2000; 109: 177-186.