Skip to main content
Top
Published in: Journal of Neuroinflammation 1/2017

Open Access 01-12-2017 | Research

Microglial activation in Parkinson’s disease using [18F]-FEPPA

Authors: Christine Ghadery, Yuko Koshimori, Sarah Coakeley, Madeleine Harris, Pablo Rusjan, Jinhee Kim, Sylvain Houle, Antonio P. Strafella

Published in: Journal of Neuroinflammation | Issue 1/2017

Login to get access

Abstract

Background

Neuroinflammatory processes including activated microglia have been reported to play an important role in Parkinson’s disease (PD). Increased expression of translocator protein (TSPO) has been observed after brain injury and inflammation in neurodegenerative diseases. Positron emission tomography (PET) radioligand targeting TSPO allows for the quantification of neuroinflammation in vivo.

Methods

Based on the genotype of the rs6791 polymorphism in the TSPO gene, we included 25 mixed-affinity binders (MABs) (14 PD patients and 11 age-matched healthy controls (HC)) and 27 high-affinity binders (HABs) (16 PD patients and 11 age-matched HC) to assess regional differences in the second-generation radioligand [18F]-FEPPA between PD patients and HC. FEPPA total distribution volume (V T) values in cortical as well as subcortical brain regions were derived from a two-tissue compartment model with arterial plasma as an input function.

Results

Our results revealed a significant main effect of genotype on [18F]-FEPPA V T in every brain region, but no main effect of disease or disease × genotype interaction in any brain region. The overall percentage difference of the mean FEPPA V T between HC-MABs and HC-HABs was 32.6% (SD = 2.09) and for PD-MABs and PD-HABs was 43.1% (SD = 1.21).

Conclusions

Future investigations are needed to determine the significance of [18F]-FEPPA as a biomarker of neuroinflammation as well as the importance of the rs6971 polymorphism and its clinical consequence in PD.
Literature
1.
2.
go back to reference McGeer PL, Itagaki S, Boyes BE, McGeer EG. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology. 1988;38(8):1285–91.CrossRefPubMed McGeer PL, Itagaki S, Boyes BE, McGeer EG. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology. 1988;38(8):1285–91.CrossRefPubMed
3.
go back to reference Imamura K, Hishikawa N, Sawada M, Nagatsu T, Yoshida M, Hashizume Y. Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson's disease brains. Acta Neuropathol. 2003;106(6):518–26.CrossRefPubMed Imamura K, Hishikawa N, Sawada M, Nagatsu T, Yoshida M, Hashizume Y. Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson's disease brains. Acta Neuropathol. 2003;106(6):518–26.CrossRefPubMed
4.
go back to reference Mogi M, Harada M, Kondo T, Riederer P, Inagaki H, Minami M, Nagatsu T. Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neurosci Lett. 1994;180(2):147–50.CrossRefPubMed Mogi M, Harada M, Kondo T, Riederer P, Inagaki H, Minami M, Nagatsu T. Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neurosci Lett. 1994;180(2):147–50.CrossRefPubMed
5.
go back to reference Dobbs RJ, Charlett A, Purkiss AG, Dobbs SM, Weller C, Peterson DW. Association of circulating TNF-alpha and IL-6 with ageing and parkinsonism. Acta Neurol Scand. 1999;100(1):34–41.CrossRefPubMed Dobbs RJ, Charlett A, Purkiss AG, Dobbs SM, Weller C, Peterson DW. Association of circulating TNF-alpha and IL-6 with ageing and parkinsonism. Acta Neurol Scand. 1999;100(1):34–41.CrossRefPubMed
6.
go back to reference Blum-Degen D, Muller T, Kuhn W, Gerlach M, Przuntek H, Riederer P. Interleukin-1 beta and interleukin-6 are elevated in the cerebrospinal fluid of Alzheimer's and de novo Parkinson's disease patients. Neurosci Lett. 1995;202(1–2):17–20.CrossRefPubMed Blum-Degen D, Muller T, Kuhn W, Gerlach M, Przuntek H, Riederer P. Interleukin-1 beta and interleukin-6 are elevated in the cerebrospinal fluid of Alzheimer's and de novo Parkinson's disease patients. Neurosci Lett. 1995;202(1–2):17–20.CrossRefPubMed
7.
go back to reference Venneti S, Lopresti BJ, Wiley CA. Molecular imaging of microglia/macrophages in the brain. Glia. 2013;61(1):10–23.CrossRefPubMed Venneti S, Lopresti BJ, Wiley CA. Molecular imaging of microglia/macrophages in the brain. Glia. 2013;61(1):10–23.CrossRefPubMed
8.
go back to reference Rupprecht R, Papadopoulos V, Rammes G, Baghai TC, Fan J, Akula N, Groyer G, Adams D, Schumacher M. Translocator protein (18 kDa) (TSPO) as a therapeutic target for neurological and psychiatric disorders. Nat Rev Drug Discov. 2010;9(12):971–88.CrossRefPubMed Rupprecht R, Papadopoulos V, Rammes G, Baghai TC, Fan J, Akula N, Groyer G, Adams D, Schumacher M. Translocator protein (18 kDa) (TSPO) as a therapeutic target for neurological and psychiatric disorders. Nat Rev Drug Discov. 2010;9(12):971–88.CrossRefPubMed
10.
go back to reference Ouchi Y, Yoshikawa E, Sekine Y, Futatsubashi M, Kanno T, Ogusu T, Torizuka T. Microglial activation and dopamine terminal loss in early Parkinson's disease. Ann Neurol. 2005;57(2):168–75.CrossRefPubMed Ouchi Y, Yoshikawa E, Sekine Y, Futatsubashi M, Kanno T, Ogusu T, Torizuka T. Microglial activation and dopamine terminal loss in early Parkinson's disease. Ann Neurol. 2005;57(2):168–75.CrossRefPubMed
11.
go back to reference Kobylecki C, Counsell SJ, Cabanel N, Wachter T, Turkheimer FE, Eggert K, Oertel W, Brooks DJ, Gerhard A. Diffusion-weighted imaging and its relationship to microglial activation in parkinsonian syndromes. Parkinsonism Relat Disord. 2013;19(5):527–32.CrossRefPubMed Kobylecki C, Counsell SJ, Cabanel N, Wachter T, Turkheimer FE, Eggert K, Oertel W, Brooks DJ, Gerhard A. Diffusion-weighted imaging and its relationship to microglial activation in parkinsonian syndromes. Parkinsonism Relat Disord. 2013;19(5):527–32.CrossRefPubMed
12.
go back to reference Mizrahi R, Rusjan PM, Kennedy J, Pollock B, Mulsant B, Suridjan I, De Luca V, Wilson AA, Houle S. Translocator protein (18 kDa) polymorphism (rs6971) explains in-vivo brain binding affinity of the PET radioligand [(18)F]-FEPPA. J Cereb Blood Flow Metab. 2012;32(6):968–72.CrossRefPubMedPubMedCentral Mizrahi R, Rusjan PM, Kennedy J, Pollock B, Mulsant B, Suridjan I, De Luca V, Wilson AA, Houle S. Translocator protein (18 kDa) polymorphism (rs6971) explains in-vivo brain binding affinity of the PET radioligand [(18)F]-FEPPA. J Cereb Blood Flow Metab. 2012;32(6):968–72.CrossRefPubMedPubMedCentral
13.
go back to reference Chauveau F, Boutin H, Van Camp N, Dolle F, Tavitian B. Nuclear imaging of neuroinflammation: a comprehensive review of [11C]PK11195 challengers. Eur J Nucl Med Mol Imaging. 2008;35(12):2304–19.CrossRefPubMed Chauveau F, Boutin H, Van Camp N, Dolle F, Tavitian B. Nuclear imaging of neuroinflammation: a comprehensive review of [11C]PK11195 challengers. Eur J Nucl Med Mol Imaging. 2008;35(12):2304–19.CrossRefPubMed
14.
go back to reference Wilson AA, Garcia A, Parkes J, McCormick P, Stephenson KA, Houle S, Vasdev N. Radiosynthesis and initial evaluation of [18F]-FEPPA for PET imaging of peripheral benzodiazepine receptors. Nucl Med Biol. 2008;35(3):305–14.CrossRefPubMed Wilson AA, Garcia A, Parkes J, McCormick P, Stephenson KA, Houle S, Vasdev N. Radiosynthesis and initial evaluation of [18F]-FEPPA for PET imaging of peripheral benzodiazepine receptors. Nucl Med Biol. 2008;35(3):305–14.CrossRefPubMed
15.
go back to reference Rusjan PM, Wilson AA, Bloomfield PM, Vitcu I, Meyer JH, Houle S, Mizrahi R. Quantitation of translocator protein binding in human brain with the novel radioligand [18F]-FEPPA and positron emission tomography. J Cereb Blood Flow Metab. 2011;31(8):1807–16.CrossRefPubMedPubMedCentral Rusjan PM, Wilson AA, Bloomfield PM, Vitcu I, Meyer JH, Houle S, Mizrahi R. Quantitation of translocator protein binding in human brain with the novel radioligand [18F]-FEPPA and positron emission tomography. J Cereb Blood Flow Metab. 2011;31(8):1807–16.CrossRefPubMedPubMedCentral
16.
go back to reference 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. 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):1–5.CrossRefPubMed 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. 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):1–5.CrossRefPubMed
17.
go back to reference Owen DR, Howell OW, Tang SP, Wells LA, Bennacef I, Bergstrom M, Gunn RN, Rabiner EA, Wilkins MR, Reynolds R, Matthews PM, Parker CA. Two binding sites for [3H]PBR28 in human brain: implications for TSPO PET imaging of neuroinflammation. J Cereb Blood Flow Metab. 2010;30(9):1608–18.CrossRefPubMedPubMedCentral Owen DR, Howell OW, Tang SP, Wells LA, Bennacef I, Bergstrom M, Gunn RN, Rabiner EA, Wilkins MR, Reynolds R, Matthews PM, Parker CA. Two binding sites for [3H]PBR28 in human brain: implications for TSPO PET imaging of neuroinflammation. J Cereb Blood Flow Metab. 2010;30(9):1608–18.CrossRefPubMedPubMedCentral
18.
go back to reference Koshimori Y, Ko JH, Mizrahi R, Rusjan P, Mabrouk R, Jacobs MF, Christopher L, Hamani C, Lang AE, Wilson AA, Houle S, Strafella AP. Imaging striatal microglial activation in patients with Parkinson’s disease. PLoS One. 2015;10(9):e0138721.CrossRefPubMedPubMedCentral Koshimori Y, Ko JH, Mizrahi R, Rusjan P, Mabrouk R, Jacobs MF, Christopher L, Hamani C, Lang AE, Wilson AA, Houle S, Strafella AP. Imaging striatal microglial activation in patients with Parkinson’s disease. PLoS One. 2015;10(9):e0138721.CrossRefPubMedPubMedCentral
19.
go back to reference Rusjan P, Mamo D, Ginovart N, Hussey D, Vitcu I, Yasuno F, Tetsuya S, Houle S, Kapur S. An automated method for the extraction of regional data from PET images. Psychiatry Res. 2006;147(1):79–89.CrossRefPubMed Rusjan P, Mamo D, Ginovart N, Hussey D, Vitcu I, Yasuno F, Tetsuya S, Houle S, Kapur S. An automated method for the extraction of regional data from PET images. Psychiatry Res. 2006;147(1):79–89.CrossRefPubMed
20.
go back to reference Rusjan PM, Wilson AA, Miler L, Fan I, Mizrahi R, Houle S, Vasdev N, Meyer JH. Kinetic modeling of the monoamine oxidase B radioligand [(1)(1)C]SL25.1188 in human brain with high-resolution positron emission tomography. J Cereb Blood Flow Metab. 2014;34(5):883–9.CrossRefPubMedPubMedCentral Rusjan PM, Wilson AA, Miler L, Fan I, Mizrahi R, Houle S, Vasdev N, Meyer JH. Kinetic modeling of the monoamine oxidase B radioligand [(1)(1)C]SL25.1188 in human brain with high-resolution positron emission tomography. J Cereb Blood Flow Metab. 2014;34(5):883–9.CrossRefPubMedPubMedCentral
21.
go back to reference Bencherif B, Stumpf MJ, Links JM, Frost JJ. Application of MRI-based partial-volume correction to the analysis of PET images of mu-opioid receptors using statistical parametric mapping. J Nucl Med. 2004;45(3):402–8.PubMed Bencherif B, Stumpf MJ, Links JM, Frost JJ. Application of MRI-based partial-volume correction to the analysis of PET images of mu-opioid receptors using statistical parametric mapping. J Nucl Med. 2004;45(3):402–8.PubMed
22.
go back to reference Kenk M, Selvanathan T, Rao N, Suridjan I, Rusjan P, Remington G, Meyer JH, Wilson AA, Houle S, Mizrahi R. Imaging neuroinflammation in gray and white matter in schizophrenia: an in-vivo PET study with [18F]-FEPPA. Schizophr Bull. 2015;41(1):85–93.CrossRefPubMed Kenk M, Selvanathan T, Rao N, Suridjan I, Rusjan P, Remington G, Meyer JH, Wilson AA, Houle S, Mizrahi R. Imaging neuroinflammation in gray and white matter in schizophrenia: an in-vivo PET study with [18F]-FEPPA. Schizophr Bull. 2015;41(1):85–93.CrossRefPubMed
23.
go back to reference Logan J, Fowler JS, Volkow ND, Wolf AP, Dewey SL, Schlyer DJ, MacGregor RR, Hitzemann R, Bendriem B, Gatley SJ. Graphical analysis of reversible radioligand binding from time-activity measurements applied to [N-11C-methyl]-(−)-cocaine PET studies in human subjects. J Cereb Blood Flow Metab. 1990;10(5):740–7.CrossRefPubMed Logan J, Fowler JS, Volkow ND, Wolf AP, Dewey SL, Schlyer DJ, MacGregor RR, Hitzemann R, Bendriem B, Gatley SJ. Graphical analysis of reversible radioligand binding from time-activity measurements applied to [N-11C-methyl]-(−)-cocaine PET studies in human subjects. J Cereb Blood Flow Metab. 1990;10(5):740–7.CrossRefPubMed
25.
go back to reference Turkheimer FE, Brett M, Aston JA, Leff AP, Sargent PA, Wise RJ, Grasby PM, Cunningham VJ. Statistical modeling of positron emission tomography images in wavelet space. J Cereb Blood Flow Metab. 2000;20(11):1610–8.CrossRefPubMed Turkheimer FE, Brett M, Aston JA, Leff AP, Sargent PA, Wise RJ, Grasby PM, Cunningham VJ. Statistical modeling of positron emission tomography images in wavelet space. J Cereb Blood Flow Metab. 2000;20(11):1610–8.CrossRefPubMed
26.
go back to reference Lahiri DK, Nurnberger Jr JI. A rapid non-enzymatic method for the preparation of HMW DNA from blood for RFLP studies. Nucleic Acids Res. 1991;19(19):5444.CrossRefPubMedPubMedCentral Lahiri DK, Nurnberger Jr JI. A rapid non-enzymatic method for the preparation of HMW DNA from blood for RFLP studies. Nucleic Acids Res. 1991;19(19):5444.CrossRefPubMedPubMedCentral
27.
go back to reference Gerhard A, Banati RB, Goerres GB, Cagnin A, Myers R, Gunn RN, Turkheimer F, Good CD, Mathias CJ, Quinn N, Schwarz J, Brooks DJ. 11C](R)-PK11195 PET imaging of microglial activation in multiple system atrophy. Neurology. 2003;61(5):686–9.CrossRefPubMed Gerhard A, Banati RB, Goerres GB, Cagnin A, Myers R, Gunn RN, Turkheimer F, Good CD, Mathias CJ, Quinn N, Schwarz J, Brooks DJ. 11C](R)-PK11195 PET imaging of microglial activation in multiple system atrophy. Neurology. 2003;61(5):686–9.CrossRefPubMed
28.
go back to reference Gerhard A, Schwarz J, Myers R, Wise R, Banati RB. Evolution of microglial activation in patients after ischemic stroke: a [11C](R)-PK11195 PET study. Neuroimage. 2005;24(2):591–5.CrossRefPubMed Gerhard A, Schwarz J, Myers R, Wise R, Banati RB. Evolution of microglial activation in patients after ischemic stroke: a [11C](R)-PK11195 PET study. Neuroimage. 2005;24(2):591–5.CrossRefPubMed
29.
go back to reference Gerhard A, Pavese N, Hotton G, Turkheimer F, Es M, Hammers A, Eggert K, Oertel W, Banati RB, Brooks DJ. In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson’s disease. Neurobiol Dis. 2006;21(2):404–12.CrossRefPubMed Gerhard A, Pavese N, Hotton G, Turkheimer F, Es M, Hammers A, Eggert K, Oertel W, Banati RB, Brooks DJ. In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson’s disease. Neurobiol Dis. 2006;21(2):404–12.CrossRefPubMed
30.
go back to reference Costa B, Pini S, Gabelloni P, Da Pozzo E, Abelli M, Lari L, Preve M, Lucacchini A, Cassano GB, Martini C. The spontaneous Ala147Thr amino acid substitution within the translocator protein influences pregnenolone production in lymphomonocytes of healthy individuals. Endocrinology. 2009;150(12):5438–45.CrossRefPubMed Costa B, Pini S, Gabelloni P, Da Pozzo E, Abelli M, Lari L, Preve M, Lucacchini A, Cassano GB, Martini C. The spontaneous Ala147Thr amino acid substitution within the translocator protein influences pregnenolone production in lymphomonocytes of healthy individuals. Endocrinology. 2009;150(12):5438–45.CrossRefPubMed
31.
go back to reference Costa B, Pini S, Martini C, Abelli M, Gabelloni P, Landi S, Muti M, Gesi C, Lari L, Cardini A, Galderisi S, Mucci A, Lucacchini A, Cassano GB. Ala147Thr substitution in translocator protein is associated with adult separation anxiety in patients with depression. Psychiatr Genet. 2009;19(2):110–1.CrossRefPubMed Costa B, Pini S, Martini C, Abelli M, Gabelloni P, Landi S, Muti M, Gesi C, Lari L, Cardini A, Galderisi S, Mucci A, Lucacchini A, Cassano GB. Ala147Thr substitution in translocator protein is associated with adult separation anxiety in patients with depression. Psychiatr Genet. 2009;19(2):110–1.CrossRefPubMed
32.
go back to reference Lee DH, Kang SK, Lee RH, Ryu JM, Park HY, Choi HS, Bae YC, Suh KT, Kim YK, Jung JS. Effects of peripheral benzodiazepine receptor ligands on proliferation and differentiation of human mesenchymal stem cells. J Cell Physiol. 2004;198(1):91–9.CrossRefPubMed Lee DH, Kang SK, Lee RH, Ryu JM, Park HY, Choi HS, Bae YC, Suh KT, Kim YK, Jung JS. Effects of peripheral benzodiazepine receptor ligands on proliferation and differentiation of human mesenchymal stem cells. J Cell Physiol. 2004;198(1):91–9.CrossRefPubMed
33.
go back to reference Papadopoulos V, Mukhin AG, Costa E, Krueger KE. The peripheral-type benzodiazepine receptor is functionally linked to Leydig cell steroidogenesis. J Biol Chem. 1990;265(7):3772–9.PubMed Papadopoulos V, Mukhin AG, Costa E, Krueger KE. The peripheral-type benzodiazepine receptor is functionally linked to Leydig cell steroidogenesis. J Biol Chem. 1990;265(7):3772–9.PubMed
34.
go back to reference Casellas P, Galiegue S, Basile AS. Peripheral benzodiazepine receptors and mitochondrial function. Neurochem Int. 2002;40(6):475–86.CrossRefPubMed Casellas P, Galiegue S, Basile AS. Peripheral benzodiazepine receptors and mitochondrial function. Neurochem Int. 2002;40(6):475–86.CrossRefPubMed
35.
go back to reference Streit WJ. Microglial response to brain injury: a brief synopsis. Toxicol Pathol. 2000;28(1):28–30.CrossRefPubMed Streit WJ. Microglial response to brain injury: a brief synopsis. Toxicol Pathol. 2000;28(1):28–30.CrossRefPubMed
36.
go back to reference Owen DR, Gunn RN, Rabiner EA, Bennacef I, Fujita M, Kreisl WC, Innis RB, Pike VW, Reynolds R, Matthews PM, Parker CA. Mixed-affinity binding in humans with 18-kDa translocator protein ligands. J Nucl Med. 2011;52(1):24–32.CrossRefPubMed Owen DR, Gunn RN, Rabiner EA, Bennacef I, Fujita M, Kreisl WC, Innis RB, Pike VW, Reynolds R, Matthews PM, Parker CA. Mixed-affinity binding in humans with 18-kDa translocator protein ligands. J Nucl Med. 2011;52(1):24–32.CrossRefPubMed
37.
go back to reference Varrone A, Oikonen V, Forsberg A, Joutsa J, Takano A, Solin O, Haaparanta-Solin M, Nag S, Nakao R, Al-Tawil N, Wells LA, Rabiner EA, Valencia R, Schultze-Mosgau M, Thiele A, Vollmer S, Dyrks T, Lehmann L, Heinrich T, Hoffmann A, Nordberg A, Halldin C, Rinne JO. "Positron emission tomography imaging of the 18-kDa translocator protein (TSPO) with [18F]FEMPA in Alzheimer's disease patients and control subjects,". Eur J Nucl Med Mol Imaging. 2015;42(3):438–46.CrossRefPubMed Varrone A, Oikonen V, Forsberg A, Joutsa J, Takano A, Solin O, Haaparanta-Solin M, Nag S, Nakao R, Al-Tawil N, Wells LA, Rabiner EA, Valencia R, Schultze-Mosgau M, Thiele A, Vollmer S, Dyrks T, Lehmann L, Heinrich T, Hoffmann A, Nordberg A, Halldin C, Rinne JO. "Positron emission tomography imaging of the 18-kDa translocator protein (TSPO) with [18F]FEMPA in Alzheimer's disease patients and control subjects,". Eur J Nucl Med Mol Imaging. 2015;42(3):438–46.CrossRefPubMed
38.
go back to reference Suridjan I, Rusjan PM, Kenk M, Verhoeff NP, Voineskos AN, Rotenberg D, Wilson AA, Meyer JH, Houle S, Mizrahi R. Quantitative imaging of neuroinflammation in human white matter: a positron emission tomography study with translocator protein 18 kDa radioligand, [18F]-FEPPA. Synapse (New York, NY). 2014;68(11):536–47.CrossRef Suridjan I, Rusjan PM, Kenk M, Verhoeff NP, Voineskos AN, Rotenberg D, Wilson AA, Meyer JH, Houle S, Mizrahi R. Quantitative imaging of neuroinflammation in human white matter: a positron emission tomography study with translocator protein 18 kDa radioligand, [18F]-FEPPA. Synapse (New York, NY). 2014;68(11):536–47.CrossRef
39.
go back to reference Iannaccone S, Cerami C, Alessio M, Garibotto V, Panzacchi A, Olivieri S, Gelsomino G, Moresco RM, Perani D. In vivo microglia activation in very early dementia with Lewy bodies, comparison with Parkinson’s disease. Parkinsonism Relat Disord. 2013;19(1):47–52.CrossRefPubMed Iannaccone S, Cerami C, Alessio M, Garibotto V, Panzacchi A, Olivieri S, Gelsomino G, Moresco RM, Perani D. In vivo microglia activation in very early dementia with Lewy bodies, comparison with Parkinson’s disease. Parkinsonism Relat Disord. 2013;19(1):47–52.CrossRefPubMed
40.
go back to reference Bartels AL, Willemsen AT, Doorduin J, de Vries EF, Dierckx RA, Leenders KL. 11C]-PK11195 PET: quantification of neuroinflammation and a monitor of anti-inflammatory treatment in Parkinson’s disease? Parkinsonism Relat Disord. 2010;16(1):57–9.CrossRefPubMed Bartels AL, Willemsen AT, Doorduin J, de Vries EF, Dierckx RA, Leenders KL. 11C]-PK11195 PET: quantification of neuroinflammation and a monitor of anti-inflammatory treatment in Parkinson’s disease? Parkinsonism Relat Disord. 2010;16(1):57–9.CrossRefPubMed
41.
go back to reference Edison P, Ahmed I, Fan Z, Hinz R, Gelosa G, Ray Chaudhuri K, Walker Z, Turkheimer FE, Brooks DJ. Microglia, amyloid, and glucose metabolism in Parkinson’s disease with and without dementia. Neuropsychopharmacology. 2013;38(6):938–49.CrossRefPubMedPubMedCentral Edison P, Ahmed I, Fan Z, Hinz R, Gelosa G, Ray Chaudhuri K, Walker Z, Turkheimer FE, Brooks DJ. Microglia, amyloid, and glucose metabolism in Parkinson’s disease with and without dementia. Neuropsychopharmacology. 2013;38(6):938–49.CrossRefPubMedPubMedCentral
42.
go back to reference Fan J, Lindemann P, Feuilloley MG, Papadopoulos V. Structural and functional evolution of the translocator protein (18 kDa). Curr Mol Med. 2012;12(4):369–86.PubMed Fan J, Lindemann P, Feuilloley MG, Papadopoulos V. Structural and functional evolution of the translocator protein (18 kDa). Curr Mol Med. 2012;12(4):369–86.PubMed
43.
go back to reference Terada T, Yokokura M, Yoshikawa E, Futatsubashi M, Kono S, Konishi T, Miyajima H, Hashizume T, Ouchi Y. "Extrastriatal spreading of microglial activation in Parkinson's disease: a positron emission tomography study," Annals of Nuclear Medicine 2016;30(8):579–87.CrossRefPubMed Terada T, Yokokura M, Yoshikawa E, Futatsubashi M, Kono S, Konishi T, Miyajima H, Hashizume T, Ouchi Y. "Extrastriatal spreading of microglial activation in Parkinson's disease: a positron emission tomography study," Annals of Nuclear Medicine 2016;30(8):579–87.CrossRefPubMed
44.
go back to reference Setiawan E, Wilson AA, Mizrahi R, Rusjan PM, Miler L, Rajkowska G, Suridjan I, Kennedy JL, Rekkas PV, Houle S, Meyer JH. Role of translocator protein density, a marker of neuroinflammation, in the brain during major depressive episodes. JAMA Psychiat. 2015;72(3):268–75.CrossRef Setiawan E, Wilson AA, Mizrahi R, Rusjan PM, Miler L, Rajkowska G, Suridjan I, Kennedy JL, Rekkas PV, Houle S, Meyer JH. Role of translocator protein density, a marker of neuroinflammation, in the brain during major depressive episodes. JAMA Psychiat. 2015;72(3):268–75.CrossRef
45.
go back to reference Suridjan I, Pollock BG, Verhoeff NP, Voineskos AN, Chow T, Rusjan PM, Lobaugh NJ, Houle S, Mulsant BH, Mizrahi R. In-vivo imaging of grey and white matter neuroinflammation in Alzheimer’s disease: a positron emission tomography study with a novel radioligand, [18F]-FEPPA. Mol Psychiatry. 2015;20(12):1579–87.CrossRefPubMed Suridjan I, Pollock BG, Verhoeff NP, Voineskos AN, Chow T, Rusjan PM, Lobaugh NJ, Houle S, Mulsant BH, Mizrahi R. In-vivo imaging of grey and white matter neuroinflammation in Alzheimer’s disease: a positron emission tomography study with a novel radioligand, [18F]-FEPPA. Mol Psychiatry. 2015;20(12):1579–87.CrossRefPubMed
46.
go back to reference Suridjan I, Rusjan PM, Voineskos AN, Selvanathan T, Setiawan E, Strafella AP, Wilson AA, Meyer JH, Houle S, Mizrahi R. Neuroinflammation in healthy aging: a PET study using a novel Translocator Protein 18 kDa (TSPO) radioligand, [(18)F]-FEPPA. Neuroimage. 2014;84:868–75.CrossRefPubMed Suridjan I, Rusjan PM, Voineskos AN, Selvanathan T, Setiawan E, Strafella AP, Wilson AA, Meyer JH, Houle S, Mizrahi R. Neuroinflammation in healthy aging: a PET study using a novel Translocator Protein 18 kDa (TSPO) radioligand, [(18)F]-FEPPA. Neuroimage. 2014;84:868–75.CrossRefPubMed
Metadata
Title
Microglial activation in Parkinson’s disease using [18F]-FEPPA
Authors
Christine Ghadery
Yuko Koshimori
Sarah Coakeley
Madeleine Harris
Pablo Rusjan
Jinhee Kim
Sylvain Houle
Antonio P. Strafella
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2017
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-016-0778-1

Other articles of this Issue 1/2017

Journal of Neuroinflammation 1/2017 Go to the issue