Quantitative imaging of neuroinflammation in human white matter: A positron emission tomography study with translocator protein 18 kDa radioligand, [18F]-FEPPA

Synapse

Volumn 68, Issue 11, 2014, Pages 536-547

  Suridjan, Ivonne ^a,b   Rusjan, Pablo M ^a   Kenk, Miran ^a   Verhoeff, Nicolaas Paul L G ^b,c,d   Voineskos, Aristotle N ^a,b,c   Rotenberg, David ^a   Wilson, Alan A ^a,b,c   Meyer, Jeffrey H ^a,b,c   Houle, Sylvain ^a   Mizrahi, Romina ^a,b,c  

^a CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d BAYCREST CENTRE FOR GERIATRIC CARE   (Canada)

Author keywords

Neuroinflammation; Positron emission tomography imaging; Translocator protein; White matter; 18F FEPPA

Indexed keywords

FEPPA F 18; MEMBRANE PROTEIN; TRACER; TRANSLOCATOR PROTEIN; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; ANILIDE; N-(2-((N-(4-PHENOXYPYRIDIN-3-YL)ACETAMIDO)METHYL)PHENOXY)ETHYL FLUORIDE; PROTEIN BINDING; PYRIDINE DERIVATIVE; RADIOPHARMACEUTICAL AGENT; TSPO PROTEIN, HUMAN;

ADULT; AGE; AGED; ARTICLE; CAPSULA INTERNA; CINGULUM (BRAIN); CORPUS CALLOSUM; FEMALE; GENETIC POLYMORPHISM; HUMAN; HUMAN EXPERIMENT; MALE; MONTE CARLO METHOD; NERVOUS SYSTEM INFLAMMATION; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PET SCANNER; POSITRON EMISSION TOMOGRAPHY; POSTERIOR LIMB OF INTERNAL CAPSULE; SUPERIOR LONGITUDINAL FASCICULUS; WHITE MATTER; DIAGNOSTIC USE; GENETICS; INFLAMMATION; METABOLISM; MIDDLE AGED; SCINTISCANNING; SINGLE NUCLEOTIDE POLYMORPHISM; TISSUE DISTRIBUTION;

ADULT; AGED; ANILIDES; CORPUS CALLOSUM; FEMALE; HUMANS; INFLAMMATION; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; POSITRON-EMISSION TOMOGRAPHY; PROTEIN BINDING; PYRIDINES; RADIOPHARMACEUTICALS; RECEPTORS, GABA; TISSUE DISTRIBUTION; WHITE MATTER;

EID: 84908510509     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.21765     Document Type: Article

References (56)

1. Akaike H. 1974. A new look at the statistical model identification. IEEE Trans Automat Contr 19:716-723.
2. Ashburner J, Friston KJ. 2005. Unified segmentation. Neuroimage 26:839-851.
3. Banati RB, Newcombe J, Gunn RN, Cagnin A, Turkheimer F, Heppner F, Price G, Wegner F, Giovannoni G, Miller DH, Perkin GD, Smith T, Hewson AK, Bydder G, Kreutzberg GW, Jones T, Cuzner ML, Myers R. 2000. The peripheral benzodiazepine binding site in the brain in multiple sclerosis: quantitative in vivo imaging of microglia as a measure of disease activity. Brain 123 (Pt 11):2321-2337.
4. Cagnin A, Brooks DJ, Kennedy AM, Gunn RN, Myers R, Turkheimer FE, Jones T, Banati RB. 2001. In-vivo measurement of activated microglia in dementia. Lancet 358:461-467.
5. Chen MK, Guilarte TR. 2008. Translocator protein 18 kDa (TSPO): Molecular sensor of brain injury and repair. Pharmacol Ther 118:1-17.
6. Cosenza-Nashat M, Zhao ML, Suh HS, Morgan J, Natividad R, Morgello S, Lee SC. 2009. Expression of the translocator protein of 18 kDa by microglia, macrophages and astrocytes based on immunohistochemical localization in abnormal human brain. Neuropathol Appl Neurobiol 35:306-328.
7. Debruyne JC, Versijpt J, Van Laere KJ, De Vos F, Keppens J, Strijckmans K, Achten E, Slegers G, Dierckx RA, Korf J, De Reuck JL. 2003. PET visualization of microglia in multiple sclerosis patients using [11C]PK11195. Eur J Neurol 10:257-264.
8. Denes A, Vidyasagar R, Feng J, Narvainen J, McColl BW, Kauppinen RA, Allan SM. 2007. Proliferating resident microglia after focal cerebral ischaemia in mice. J Cereb Blood Flow Metab 27:1941-1953.
9. DiPatre PL, Gelman BB. 1997. Microglial cell activation in aging and Alzheimer disease: Partial linkage with neurofibrillary tangle burden in the hippocampus. J Neuropathol Exp Neurol 56:143-149.
10. Endres CJ, Pomper MG, James M, Uzuner O, Hammoud DA, Watkins CC, Reynolds A, Hilton J, Dannals RF, Kassiou M. 2009. Initial evaluation of 11C-DPA-713, a novel TSPO PET ligand, in humans. J Nucl Med 50:1276-1282.
11. Folstein MF, Folstein SE, McHugh PR. 1975. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189-198.
12. Fujimura Y, Ikoma Y, Yasuno F, Suhara T, Ota M, Matsumoto R, Nozaki S, Takano A, Kosaka J, Zhang MR, Nakao R, Suzuki K, Kato N, Ito H. 2006. Quantitative analyses of 18F-FEDAA1106 binding to peripheral benzodiazepine receptors in living human brain. J Nucl Med 47:43-50.
13. Fujita M, Imaizumi M, Zoghbi SS, Fujimura Y, Farris AG, Suhara T, Hong J, Pike VW, Innis RB. 2008. Kinetic analysis in healthy humans of a novel positron emission tomography radioligand to image the peripheral benzodiazepine receptor, a potential biomarker for inflammation. Neuroimage 40:43-52.
14. Guilarte TR, Kuhlmann AC, O'Callaghan JP, Miceli RC. 1995. Enhanced expression of peripheral benzodiazepine receptors in trimethyltin-exposed rat brain: A biomarker of neurotoxicity. Neurotoxicology 16:441-450.
15. Gulyas B, Vas A, Toth M, Takano A, Varrone A, Cselenyi Z, Schain M, Mattsson P, Halldin C. 2011. Age and disease related changes in the translocator protein (TSPO) system in the human brain: Positron emission tomography measurements with [11C]vinpocetine. Neuroimage 56:1111-1121.
16. Guo Q, Colasanti A, Owen DR, Onega M, Kamalakaran A, Bennacef I, Matthews PM, Rabiner EA, Turkheimer FE, Gunn RN. 2013. Quantification of the specific translocator protein signal of 18F-PBR111 in healthy humans: A genetic polymorphism effect on in vivo binding. J Nucl Med 54:1915-1923.
17. Hayes GM, Woodroofe MN, Cuzner ML. 1987. Microglia are the major cell type expressing MHC class II in human white matter. J Neurol Sci 80:25-37.
18. Huang H, Fan X, Weiner M, Martin-Cook K, Xiao G, Davis J, Devous M, Rosenberg R, Diaz-Arrastia R. 2012. Distinctive disruption patterns of white matter tracts in Alzheimer's disease with full diffusion tensor characterization. Neurobiol Aging 33:2029-2045.
19. Innis RB, Cunningham VJ, Delforge J, Fujita M, Gjedde A, Gunn RN, Holden J, Houle S, Huang SC, Ichise M, Iida H, Ito H, Kimura Y, Koeppe RA, Knudsen GM, Knuuti J, Lammertsma AA, Laruelle M, Logan J, Maguire RP, Mintun MA, Morris ED, Parsey R, Price JC, Slifstein M, Sossi V, Suhara T, Votaw JR, Wong DF, Carson RE. 2007. Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J Cereb Blood Flow Metab 27:1533-1539.
20. Kerchner GA, Racine CA, Hale S, Wilheim R, Laluz V, Miller BL, Kramer JH. 2012. Cognitive processing speed in older adults: Relationship with white matter integrity. PLoS One 7:e50425.
21. Kreisl WC, Fujita M, Fujimura Y, Kimura N, Jenko KJ, Kannan P, Hong J, Morse CL, Zoghbi SS, Gladding RL, Jacobson S, Oh U, Pike VW, Innis RB. 2010. 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 49:2924-2932.
22. Kreisl WC, Jenko KJ, Hines CS, Hyoung Lyoo C, Corona W, Morse CL, Zoghbi SS, Hyde T, Kleinman JE, Pike VW, McMahon FJ, Innis RB. 2013. 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 33:53-58.
23. Kumar A, Muzik O, Shandal V, Chugani D, Chakraborty P, Chugani HT. 2012. Evaluation of age-related changes in translocator protein (TSPO) in human brain using (11)C-[R]-PK11195 PET. J Neuroinflammation 9:232.
24. Leenders KL, Perani D, Lammertsma AA, Heather JD, Buckingham P, Healy MJ, Gibbs JM, Wise RJ, Hatazawa J, Herold S, et al. 1990. Cerebral blood flow, blood volume and oxygen utilization. Normal values and effect of age. Brain 113 (Pt 1):27-47.
25. Logan J, Fowler JS, Volkow ND, Ding YS, Wang GJ, Alexoff DL. 2001. A strategy for removing the bias in the graphical analysis method. J Cereb Blood Flow Metab 21:307-320.
26. Lu PH, Lee GJ, Tishler TA, Meghpara M, Thompson PM, Bartzokis G. 2013. Myelin breakdown mediates age-related slowing in cognitive processing speed in healthy elderly men. Brain Cogn 81:131-138.
27. Marazziti D, Pancioli-Guadagnucci ML, Rotondo A, Giannaccini G, Martini C, Lucacchini A, Cassano GB. 1994. Age-related changes in peripheral benzodiazepine receptors of human platelets. J Psychiatry Neurosci 19:136-139.
28. MicroMath. 1995. MicroMath Scientist Handbook Rev 7EEF. MicroMath: Salt Lake City, pp 467
29. Miller KR, Streit WJ. 2007. The effects of aging, injury and disease on microglial function: A case for cellular senescence. Neuron Glia Biol 3:245-253.
30. Mizrahi R, Rusjan PM, Kennedy J, Pollock B, Mulsant B, Suridjan I, De Luca V, Wilson AA, Houle S. 2012. Translocator protein (18 kDa) polymorphism (rs6971) explains in-vivo brain binding affinity of the PET radioligand [(18)F]-FEPPA. J Cereb Blood Flow Metab 32:968-972.
31. Mori S, Oishi K, Jiang H, Jiang L, Li X, Akhter K, Hua K, Faria AV, Mahmood A, Woods R, Toga AW, Pike GB, Neto PR, Evans A, Zhang J, Huang H, Miller MI, van Zijl P, Mazziotta J. 2008. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 40:570-582.
32. Oh U, Fujita M, Ikonomidou VN, Evangelou IE, Matsuura E, Harberts E, Fujimura Y, Richert ND, Ohayon J, Pike VW, Zhang Y, Zoghbi SS, Innis RB, Jacobson S. 2011. Translocator protein PET imaging for glial activation in multiple sclerosis. J Neuroimmune Pharmacol 6:354-361.
33. Ouchi Y, Yoshikawa E, Sekine Y, Futatsubashi M, Kanno T, Ogusu T, Torizuka T. 2005. Microglial activation and dopamine terminal loss in early Parkinson's disease. Ann Neurol 57:168-175.
34. Owen DR, Gunn RN, Rabiner EA, Bennacef I, Fujita M, Kreisl WC, Innis RB, Pike VW, Reynolds R, Matthews PM, Parker CA. 2011. Mixed-affinity binding in humans with 18-kDa translocator protein ligands. J Nucl Med 52:24-32.
35. Owen DR, Howell OW, Tang SP, Wells LA, Bennacef I, Bergstrom M, Gunn RN, Rabiner EA, Wilkins MR, Reynolds R, Matthews PM, Parker CA. 2010. Two binding sites for [3H]PBR28 in human brain: implications for TSPO PET imaging of neuroinflammation. J Cereb Blood Flow Metab 30:1608-1618.
36. Owen DR, Yeo AJ, Gunn RN, Song K, Wadsworth G, Lewis A, Rhodes C, Pulford DJ, Bennacef I, Parker CA, Stjean PL, Cardon LR, Mooser VE, Matthews PM, Rabiner EA, Rubio JP. 2012. An 18-kDa translocator protein (TSPO) polymorphism explains differences in binding affinity of the PET radioligand PBR28. J Cereb Blood Flow Metab 32:1-5.
37. Peters A. 2002. The effects of normal aging on myelin and nerve fibers: A review. J Neurocytol 31:581-593.
38. Rusjan P, Mamo D, Ginovart N, Hussey D, Vitcu I, Yasuno F, Tetsuya S, Houle S, Kapur S. 2006. An automated method for the extraction of regional data from PET images. Psychiatry Res 147:79-89.
39. Rusjan PM, Wilson AA, Bloomfield PM, Vitcu I, Meyer JH, Houle S, Mizrahi R. 2011. Quantitation of translocator protein binding in human brain with the novel radioligand [(18)F]-FEPPA and positron emission tomography. J Cereb Blood Flow Metab 31:1807-1816.
40. Salat DH, Tuch DS, Greve DN, van der Kouwe AJ, Hevelone ND, Zaleta AK, Rosen BR, Fischl B, Corkin S, Rosas HD, Dale AM. 2005. Age-related alterations in white matter microstructure measured by diffusion tensor imaging. Neurobiol Aging 26:1215-1227.
41. Schuitemaker A, van der Doef TF, Boellaard R, van der Flier WM, Yaqub M, Windhorst AD, Barkhof F, Jonker C, Kloet RW, Lammertsma AA, Scheltens P, van Berckel BN. 2010. Microglial activation in healthy aging. Neurobiol Aging 33:1067-1072.
42. Sexton CE, Kalu UG, Filippini N, Mackay CE, Ebmeier KP. 2011. A meta-analysis of diffusion tensor imaging in mild cognitive impairment and Alzheimer's disease. Neurobiol Aging 32:2322.e15-18.
43. Sheng JG, Mrak RE, Griffin WS. 1998. Enlarged and phagocytic, but not primed, interleukin-1 alpha-immunoreactive microglia increase with age in normal human brain. Acta Neuropathol 95:229-234.
44. Simpson JE, Ince PG, Higham CE, Gelsthorpe CH, Fernando MS, Matthews F, Forster G, O'Brien JT, Barber R, Kalaria RN, Brayne C, Shaw PJ, Stoeber K, Williams GH, Lewis CE, Wharton SB. 2007. Microglial activation in white matter lesions and nonlesional white matter of ageing brains. Neuropathol Appl Neurobiol 33:670-683.
45. Sloane JA, Hollander W, Moss MB, Rosene DL, Abraham CR. 1999. Increased microglial activation and protein nitration in white matter of the aging monkey. Neurobiol Aging 20:395-405.
46. Streit WJ, Sammons NW, Kuhns AJ, Sparks DL. 2004. Dystrophic microglia in the aging human brain. Glia 45:208-212.
47. Studholme C, Hill DL, Hawkes DJ. 1997. Automated three-dimensional registration of magnetic resonance and positron emission tomography brain images by multiresolution optimization of voxel similarity measures. Med Phys 24:25-35.
48. Sullivan EV, Adalsteinsson E, Pfefferbaum A. 2006. Selective age-related degradation of anterior callosal fiber bundles quantified in vivo with fiber tracking. Cereb Cortex 16:1030-1039.
49. Sullivan EV, Rohlfing T, Pfefferbaum A. 2010. Quantitative fiber tracking of lateral and interhemispheric white matter systems in normal aging: relations to timed performance. Neurobiol Aging 31:464-481.
50. Suridjan I, Rusjan PM, Voineskos AN, Selvanathan T, Setiawan E, Strafella AP, Wilson AA, Meyer JH, Houle S, Mizrahi R. 2014. Neuroinflammation in healthy aging: A PET study using a novel Translocator Protein 18kDa (TSPO) radioligand, [(18)F]-FEPPA. Neuroimage 84:868-875.
51. Thiel A, Radlinska BA, Paquette C, Sidel M, Soucy JP, Schirrmacher R, Minuk J. 2010. The temporal dynamics of poststroke neuroinflammation: A longitudinal diffusion tensor imaging-guided PET study with 11C-PK11195 in acute subcortical stroke. J Nucl Med 51:1404-1412.
52. Venneti S, Lopresti BJ, Wang G, Hamilton RL, Mathis CA, Klunk WE, Apte UM, Wiley CA. 2009. PK11195 labels activated microglia in Alzheimer's disease and in vivo in a mouse model using PET. Neurobiol Aging 30:1217-1226.
53. Venneti S, Wang G, Nguyen J, Wiley CA. 2008. The positron emission tomography ligand DAA1106 binds with high affinity to activated microglia in human neurological disorders. J Neuropathol Exp Neurol 67:1001-1010.
54. Voineskos AN, Rajji TK, Lobaugh NJ, Miranda D, Shenton ME, Kennedy JL, Pollock BG, Mulsant BH. 2012. Age-related decline in white matter tract integrity and cognitive performance: A DTI tractography and structural equation modeling study. Neurobiol Aging 33:21-34.
55. Wilson AA, Garcia A, Parkes J, McCormick P, Stephenson KA, Houle S, Vasdev N. 2008. Radiosynthesis and initial evaluation of [18F]-FEPPA for PET imaging of peripheral benzodiazepine receptors. Nucl Med Biol 35:305-314.
56. Yasuno F, Ota M, Kosaka J, Ito H, Higuchi M, Doronbekov TK, Nozaki S, Fujimura Y, Koeda M, Asada T, Suhara T. 2008. Increased binding of peripheral benzodiazepine receptor in Alzheimer's disease measured by positron emission tomography with [11C]DAA1106. Biol Psychiatry 64:835-841.