Tau deposition patterns are associated with functional connectivity in primary tauopathies.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
15 03 2022
Historique:
received: 30 07 2021
accepted: 14 02 2022
entrez: 16 3 2022
pubmed: 17 3 2022
medline: 6 4 2022
Statut: epublish

Résumé

Tau pathology is the main driver of neuronal dysfunction in 4-repeat tauopathies, including cortico-basal degeneration and progressive supranuclear palsy. Tau is assumed to spread prion-like across connected neurons, but the mechanisms of tau propagation are largely elusive in 4-repeat tauopathies, characterized not only by neuronal but also by astroglial and oligodendroglial tau accumulation. Here, we assess whether connectivity is associated with 4R-tau deposition patterns by combining resting-state fMRI connectomics with both 2

Identifiants

pubmed: 35292638
doi: 10.1038/s41467-022-28896-3
pii: 10.1038/s41467-022-28896-3
pmc: PMC8924216
doi:

Substances chimiques

tau Proteins 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1362

Subventions

Organisme : NIA NIH HHS
ID : P30 AG010124
Pays : United States
Organisme : NIA NIH HHS
ID : P01 AG066597
Pays : United States
Organisme : NINDS NIH HHS
ID : K23 NS120038
Pays : United States
Organisme : NIA NIH HHS
ID : U19 AG062418
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS109260
Pays : United States
Organisme : NCATS NIH HHS
ID : TL1 TR001880
Pays : United States
Organisme : NIA NIH HHS
ID : P30 AG072979
Pays : United States

Informations de copyright

© 2022. The Author(s).

Références

Dickson, D. W. et al. Office of Rare Diseases neuropathologic criteria for corticobasal degeneration. J. Neuropathol. Exp. Neurol. 61, 935–946 (2002).
pubmed: 12430710 doi: 10.1093/jnen/61.11.935
Flament, S., Delacourte, A., Verny, M., Hauw, J. J. & Javoy-Agid, F. Abnormal Tau proteins in progressive supranuclear palsy. Similarities and differences with the neurofibrillary degeneration of the Alzheimer type. Acta Neuropathol. 81, 591–596 (1991).
pubmed: 1831952 doi: 10.1007/BF00296367
Dickson, D. W. Neuropathologic differentiation of progressive supranuclear palsy and corticobasal degeneration. J. Neurol. 246, II6–II15 (1999).
pubmed: 10525997 doi: 10.1007/BF03161076
Rosler, T. W. et al. Four-repeat tauopathies. Prog. Neurobiol. 180, 101644 (2019).
pubmed: 31238088 doi: 10.1016/j.pneurobio.2019.101644
Ling, H. et al. Fulminant corticobasal degeneration: a distinct variant with predominant neuronal tau aggregates. Acta Neuropathol. 139, 717–734 (2020).
pubmed: 31950334 pmcid: 7096362 doi: 10.1007/s00401-019-02119-4
Ling, H. et al. Astrogliopathy predominates the earliest stage of corticobasal degeneration pathology. Brain 139, 3237–3252 (2016).
pubmed: 27797812 doi: 10.1093/brain/aww256
Ling, H. et al. Characteristics of progressive supranuclear palsy presenting with corticobasal syndrome: a cortical variant. Neuropathol. Appl. Neurobiol. 40, 149–163 (2014).
pubmed: 23432126 pmcid: 4260147 doi: 10.1111/nan.12037
Kovacs, G. G. et al. Distribution patterns of tau pathology in progressive supranuclear palsy. Acta Neuropathol. 140, 99–119 (2020).
pubmed: 32383020 pmcid: 7360645 doi: 10.1007/s00401-020-02158-2
Josephs, K. A. et al. Clinicopathological and imaging correlates of progressive aphasia and apraxia of speech. Brain J. Neurol. 129, 1385–1398 (2006).
doi: 10.1093/brain/awl078
Bigio, E. H. et al. Cortical synapse loss in progressive supranuclear palsy. J. Neuropathol. Exp. Neurol. 60, 403–410 (2001).
pubmed: 11379815 doi: 10.1093/jnen/60.5.403
Kouri, N. et al. Neuropathological features of corticobasal degeneration presenting as corticobasal syndrome or Richardson syndrome. Brain J. Neurol. 134, 3264–3275 (2011).
doi: 10.1093/brain/awr234
Armstrong, M. J. et al. Criteria for the diagnosis of corticobasal degeneration. Neurology 80, 496–503 (2013).
pubmed: 23359374 pmcid: 3590050 doi: 10.1212/WNL.0b013e31827f0fd1
Gibbons, G. S., Lee, V. M. Y. & Trojanowski, J. Q. Mechanisms of cell-to-cell transmission of pathological Tau: a review. JAMA Neurol. 76, 101–108 (2019).
pubmed: 30193298 pmcid: 6382549 doi: 10.1001/jamaneurol.2018.2505
Guo, J. L. & Lee, V. M. Seeding of normal Tau by pathological Tau conformers drives pathogenesis of Alzheimer-like tangles. J. Biol. Chem. 286, 15317–15331 (2011).
pubmed: 21372138 pmcid: 3083182 doi: 10.1074/jbc.M110.209296
Narasimhan, S. et al. Pathological Tau strains from human brains recapitulate the diversity of tauopathies in nontransgenic mouse brain. J. Neurosci. 37, 11406–11423 (2017).
pubmed: 29054878 pmcid: 5700423 doi: 10.1523/JNEUROSCI.1230-17.2017
de Calignon, A. et al. Propagation of tau pathology in a model of early Alzheimer’s disease. Neuron 73, 685–697 (2012).
pubmed: 22365544 pmcid: 3292759 doi: 10.1016/j.neuron.2011.11.033
Boluda, S. et al. Differential induction and spread of tau pathology in young PS19 tau transgenic mice following intracerebral injections of pathological tau from Alzheimer’s disease or corticobasal degeneration brains. Acta Neuropathol. 129, 221–237 (2015).
pubmed: 25534024 doi: 10.1007/s00401-014-1373-0
Ahmed, Z. et al. A novel in vivo model of tau propagation with rapid and progressive neurofibrillary tangle pathology: the pattern of spread is determined by connectivity, not proximity. Acta Neuropathol. 127, 667–683 (2014).
pubmed: 24531916 pmcid: 4252866 doi: 10.1007/s00401-014-1254-6
Clavaguera, F. et al. Brain homogenates from human tauopathies induce tau inclusions in mouse brain. Proc. Natl Acad. Sci. USA 110, 9535–9540 (2013).
pubmed: 23690619 pmcid: 3677441 doi: 10.1073/pnas.1301175110
Pooler, A. M., Phillips, E. C., Lau, D. H., Noble, W. & Hanger, D. P. Physiological release of endogenous tau is stimulated by neuronal activity. EMBO Rep. 14, 389–394 (2013).
pubmed: 23412472 pmcid: 3615658 doi: 10.1038/embor.2013.15
Calafate, S. et al. Synaptic contacts enhance cell-to-cell Tau pathology propagation. Cell Rep. 11, 1176–1183 (2015).
pubmed: 25981034 doi: 10.1016/j.celrep.2015.04.043
Wu, J. W. et al. Neuronal activity enhances tau propagation and tau pathology in vivo. Nat. Neurosci. 19, 1085–1092 (2016).
pubmed: 27322420 pmcid: 4961585 doi: 10.1038/nn.4328
Tsuboi, Y. et al. Increased tau burden in the cortices of progressive supranuclear palsy presenting with corticobasal syndrome. Mov. Disord. 20, 982–988 (2005).
pubmed: 15834857 doi: 10.1002/mds.20478
Sakae, N. et al. Clinicopathologic subtype of Alzheimer’s disease presenting as corticobasal syndrome. Alzheimers Dement. 15, 1218–1228 (2019).
pubmed: 31399334 doi: 10.1016/j.jalz.2019.04.011
Robinson, J. L. et al. Neurodegenerative disease concomitant proteinopathies are prevalent, age-related and APOE4-associated. Brain J. Neurol. 141, 2181–2193 (2018).
doi: 10.1093/brain/awy146
Karran, E. & Mercken, M. & De Strooper, B. The amyloid cascade hypothesis for Alzheimer’s disease: an appraisal for the development of therapeutics. Nat. Rev. Drug Discov. 10, 698–712 (2011).
pubmed: 21852788 doi: 10.1038/nrd3505
Brendel, M. et al. Assessment of 18F-PI-2620 as a biomarker in progressive supranuclear palsy. JAMA Neurol. 77, 1408–1419 (2020).
pubmed: 33165511 doi: 10.1001/jamaneurol.2020.2526
Hoglinger, G. U. et al. Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov. Disord. 32, 853–864 (2017).
pubmed: 28467028 pmcid: 5516529 doi: 10.1002/mds.26987
Maass, A. et al. Comparison of multiple tau-PET measures as biomarkers in aging and Alzheimer’s disease. Neuroimage 157, 448–463 (2017).
pubmed: 28587897 doi: 10.1016/j.neuroimage.2017.05.058
Jagust, W. J. et al. The Alzheimer’s Disease Neuroimaging Initiative positron emission tomography core. Alzheimers Dement. 6, 221–229 (2010).
pubmed: 20451870 pmcid: 2920531 doi: 10.1016/j.jalz.2010.03.003
Palleis, C. et al. In vivo assessment of neuroinflammation in 4-repeat tauopathies. Mov. Disord. https://pubmed.ncbi.nlm.nih.gov/33245166/ (2020).
Schaefer, A. et al. Local-global parcellation of the human cerebral cortex from intrinsic functional connectivity MRI. Cereb. Cortex 1–20 https://pubmed.ncbi.nlm.nih.gov/28981612/ (2017).
Tian, Y., Margulies, D. S., Breakspear, M. & Zalesky, A. Topographic organization of the human subcortex unveiled with functional connectivity gradients. Nat. Neurosci. 23, 1421–1432 https://pubmed.ncbi.nlm.nih.gov/33246962/ (2020).
pubmed: 32989295 doi: 10.1038/s41593-020-00711-6
Franzmeier, N. et al. Patient-centered connectivity-based prediction of tau pathology spread in Alzheimer’s disease. Sci. Adv. 6, (2020).
Rolls, E. T., Huang, C. C., Lin, C. P., Feng, J. & Joliot, M. Automated anatomical labelling atlas 3. NeuroImage 206, 116189 (2020).
pubmed: 31521825 doi: 10.1016/j.neuroimage.2019.116189
Brunello, C. A., Merezhko, M., Uronen, R. L. & Huttunen, H. J. Mechanisms of secretion and spreading of pathological tau protein. Cell Mol. Life Sci. 77, 1721–1744 (2020).
pubmed: 31667556 doi: 10.1007/s00018-019-03349-1
Mudher, A. et al. What is the evidence that tau pathology spreads through prion-like propagation? Acta Neuropathol. Commun. 5, 99 (2017).
pubmed: 29258615 pmcid: 5735872 doi: 10.1186/s40478-017-0488-7
Kroth, H. et al. Discovery and preclinical characterization of [(18)F]PI-2620, a next-generation tau PET tracer for the assessment of tau pathology in Alzheimer’s disease and other tauopathies. Eur. J. Nucl. Med. Mol. imaging 46, 2178–2189 (2019).
pubmed: 31264169 pmcid: 6667408 doi: 10.1007/s00259-019-04397-2
Franzmeier, N. et al. Functional brain architecture is associated with the rate of tau accumulation in Alzheimer’s disease. Nat. Commun. 11, 347 (2020).
pubmed: 31953405 pmcid: 6969065 doi: 10.1038/s41467-019-14159-1
Franzmeier, N. et al. Functional connectivity associated with tau levels in ageing, Alzheimer’s, and small vessel disease. Brain J. Neurol. https://pubmed.ncbi.nlm.nih.gov/30770704/ (2019).
Sintini, I. et al. Tau and amyloid relationships with resting-state functional connectivity in atypical Alzheimer’s disease. Cereb. Cortex 31, 1693–1706 (2021).
pubmed: 33152765 doi: 10.1093/cercor/bhaa319
He, Z. et al. Transmission of tauopathy strains is independent of their isoform composition. Nat. Commun. 11, 7 (2020).
pubmed: 31911587 pmcid: 6946697 doi: 10.1038/s41467-019-13787-x
Shi, Y. et al. Structure-based classification of tauopathies. Nature 598, 359–363 (2021).
pubmed: 34588692 doi: 10.1038/s41586-021-03911-7
Arai, T. et al. Identification of amino-terminally cleaved tau fragments that distinguish progressive supranuclear palsy from corticobasal degeneration. Ann. Neurol. 55, 72–79 (2004).
pubmed: 14705114 doi: 10.1002/ana.10793
Taniguchi-Watanabe, S. et al. Biochemical classification of tauopathies by immunoblot, protein sequence and mass spectrometric analyses of sarkosyl-insoluble and trypsin-resistant tau. Acta Neuropathol. 131, 267–280 (2016).
pubmed: 26538150 doi: 10.1007/s00401-015-1503-3
Narasimhan, S. et al. Human tau pathology transmits glial tau aggregates in the absence of neuronal tau. J. Exp. Med. 217, https://pubmed.ncbi.nlm.nih.gov/31826239/ (2020).
Kovacs, G. G. et al. Sequential stages and distribution patterns of aging-related tau astrogliopathy (ARTAG) in the human brain. Acta Neuropathol. Commun. 6, 50 (2018).
pubmed: 29891013 pmcid: 5996526 doi: 10.1186/s40478-018-0552-y
Kovacs, G. G. Astroglia and Tau: new perspectives. Front. Aging Neurosci. 12, 96 (2020).
pubmed: 32327993 pmcid: 7160822 doi: 10.3389/fnagi.2020.00096
Lewis, J. & Dickson, D. W. Propagation of tau pathology: hypotheses, discoveries, and yet unresolved questions from experimental and human brain studies. Acta Neuropathol. 131, 27–48 (2016).
pubmed: 26576562 doi: 10.1007/s00401-015-1507-z
Liu, L. et al. Trans-synaptic spread of tau pathology in vivo. PLoS ONE 7, e31302 (2012).
pubmed: 22312444 pmcid: 3270029 doi: 10.1371/journal.pone.0031302
Vogel, J. W. et al. Spread of pathological tau proteins through communicating neurons in human Alzheimer’s disease. Nat. Commun. 11, 2612 (2020).
pubmed: 32457389 pmcid: 7251068 doi: 10.1038/s41467-020-15701-2
Leal, S. L., Lockhart, S. N., Maass, A., Bell, R. K. & Jagust, W. J. Subthreshold amyloid predicts Tau deposition in aging. J. Neurosci. 38, 4482–4489 (2018).
pubmed: 29686045 pmcid: 5943976 doi: 10.1523/JNEUROSCI.0485-18.2018
Uchihara, T. Neurofibrillary changes undergoing morphological and biochemical changes—how does tau with the profile shift of from four repeat to three repeat spread in Alzheimer brain? Neuropathology 40, 450–459 (2020).
pubmed: 32698244 doi: 10.1111/neup.12669
Zhou, Y., Li, J., Nordberg, A. & Agren, H. Dissecting the binding profile of PET tracers to corticobasal degeneration Tau fibrils. ACS Chem. Neurosci. 12, 3487–3496 (2021).
pubmed: 34464084 doi: 10.1021/acschemneuro.1c00536
Tagai, K. et al. High-contrast in vivo imaging of Tau pathologies in Alzheimer’s and non-Alzheimer’s disease tauopathies. Neuron 109, 42–58 e48 (2021).
pubmed: 33125873 doi: 10.1016/j.neuron.2020.09.042
Bloom, G. S. Amyloid-beta and tau: the trigger and bullet in Alzheimer disease pathogenesis. JAMA Neurol. 71, 505–508 (2014).
pubmed: 24493463 doi: 10.1001/jamaneurol.2013.5847
Iqbal, K., Liu, F., Gong, C. X. & Grundke-Iqbal, I. Tau in Alzheimer disease and related tauopathies. Curr. Alzheimer Res. 7, 656–664 (2010).
pubmed: 20678074 pmcid: 3090074 doi: 10.2174/156720510793611592
Honey, C. J. et al. Predicting human resting-state functional connectivity from structural connectivity. Proc. Natl Acad. Sci. USA 106, 2035–2040 (2009).
pubmed: 19188601 pmcid: 2634800 doi: 10.1073/pnas.0811168106
Abhinav, K. et al. Advanced diffusion MRI fiber tracking in neurosurgical and neurodegenerative disorders and neuroanatomical studies: a review. Biochim. Biophys. Acta 1842, 2286–2297 (2014).
pubmed: 25127851 doi: 10.1016/j.bbadis.2014.08.002
Grandjean, J., Zerbi, V., Balsters, J. H., Wenderoth, N. & Rudin, M. Structural basis of large-scale functional connectivity in the mouse. J. Neurosci. 37, 8092–8101 (2017).
pubmed: 28716961 pmcid: 6596781 doi: 10.1523/JNEUROSCI.0438-17.2017
Lu, H., Jaime, S. & Yang, Y. Origins of the resting-state functional MRI signal: potential limitations of the “Neurocentric” model. Front. Neurosci. 13, 1136 (2019).
pubmed: 31708731 pmcid: 6819315 doi: 10.3389/fnins.2019.01136
Shi, Z. et al. On the relationship between MRI and local field potential measurements of spatial and temporal variations in functional connectivity. Sci. Rep. 9, 8871 (2019).
pubmed: 31222020 pmcid: 6586888 doi: 10.1038/s41598-019-45404-8
Ladefoged, C. N. et al. A multi-centre evaluation of eleven clinically feasible brain PET/MRI attenuation correction techniques using a large cohort of patients. NeuroImage 147, 346–359 (2017).
pubmed: 27988322 doi: 10.1016/j.neuroimage.2016.12.010
Jagust, W. J. et al. The Alzheimer’s disease neuroimaging initiative 2 PET core: 2015. Alzheimers Dement. 11, 757–771 (2015).
pubmed: 26194311 pmcid: 4510459 doi: 10.1016/j.jalz.2015.05.001
Song, M. et al. Feasibility of short imaging protocols for [18F]PI-2620 Tau-PET in progressive supranuclear palsy. Res. Sq. https://pubmed.ncbi.nlm.nih.gov/34021393/ (2020).
Avants, B. B. et al. A reproducible evaluation of ANTs similarity metric performance in brain image registration. NeuroImage 54, 2033–2044 (2011).
pubmed: 20851191 doi: 10.1016/j.neuroimage.2010.09.025
Baker, S. L., Maass, A. & Jagust, W. J. Considerations and code for partial volume correcting [(18)F]-AV-1451 tau PET data. Data Brief. 15, 648–657 (2017).
pubmed: 29124088 pmcid: 5671473 doi: 10.1016/j.dib.2017.10.024
Rousset, O. G., Ma, Y. & Evans, A. C. Correction for partial volume effects in PET: principle and validation. J. Nucl. Med. 39, 904–911 (1998).
pubmed: 9591599
Litvan, I. et al. Natural history of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) and clinical predictors of survival: a clinicopathological study. J. Neurol. Neurosurg. Psychiatry 60, 615–620 (1996).
pubmed: 8648326 pmcid: 1073943 doi: 10.1136/jnnp.60.6.615
Di, X. et al. Do all roads lead to Rome? A comparison of brain networks derived from inter-subject volumetric and metabolic covariance and moment-to-moment hemodynamic correlations in old individuals. Brain Struct. Funct. 222, 3833–3845 (2017).
pubmed: 28474183 doi: 10.1007/s00429-017-1438-7
Pagani, M. et al. Functional pattern of brain FDG-PET in amyotrophic lateral sclerosis. Neurology 83, 1067–1074 (2014).
pubmed: 25122207 doi: 10.1212/WNL.0000000000000792
Landau, S. M. et al. Amyloid deposition, hypometabolism, and longitudinal cognitive decline. Ann. Neurol. 72, 578–586 (2012).
pubmed: 23109153 pmcid: 3786871 doi: 10.1002/ana.23650
Power, J. D. et al. Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 84, 320–341 (2014).
pubmed: 23994314 doi: 10.1016/j.neuroimage.2013.08.048
Franzmeier, N. et al. Left frontal hub connectivity delays cognitive impairment in autosomal-dominant and sporadic Alzheimer’s disease. Brain J. Neurol. https://pubmed.ncbi.nlm.nih.gov/29462334/ (2018).

Auteurs

Nicolai Franzmeier (N)

Institute for Stroke and Dementia Research, University Hospital of Munich, LMU Munich, Munich, Germany. Nicolai.franzmeier@med.uni-muenchen.de.

Matthias Brendel (M)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.
Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.

Leonie Beyer (L)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.

Luna Slemann (L)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.

Gabor G Kovacs (GG)

Center for Neurodegenerative Disease Research (CNDR), Institute On Aging and Department of Pathology & Laboratory Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Tanz Centre for Research in Neurodegenerative Disease (CRND) and Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, Canada.
Laboratory Medicine Program and Krembil Brain Institute, University Health Network, Toronto, ON, Canada.

Thomas Arzberger (T)

Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.
German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Munich, Germany.
Center for Neuropathology and Prion Research, LMU Munich, Munich, Germany.

Carolin Kurz (C)

German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Munich, Germany.

Gesine Respondek (G)

German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Department of Neurology, Klinikum Rechts der Isar, Technical University of Munich, Munich, Germany.
Department of Neurology, Hannover Medical School, Carl-Neuberg-Str. 1, 30625, Hannover, Germany.

Milica J Lukic (MJ)

German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Clinic of Neurology, CCS, University of Belgrade, Belgrade, Republic of Serbia.

Davina Biel (D)

Institute for Stroke and Dementia Research, University Hospital of Munich, LMU Munich, Munich, Germany.

Anna Rubinski (A)

Institute for Stroke and Dementia Research, University Hospital of Munich, LMU Munich, Munich, Germany.

Lukas Frontzkowski (L)

Institute for Stroke and Dementia Research, University Hospital of Munich, LMU Munich, Munich, Germany.

Selina Hummel (S)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.

Andre Müller (A)

Life Molecular Imaging GmbH, Berlin, Germany.

Anika Finze (A)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.

Carla Palleis (C)

Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.
German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Department of Neurology, University Hospital of Munich, LMU Munich, Munich, Germany.

Emanuel Joseph (E)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.

Endy Weidinger (E)

Department of Neurology, University Hospital of Munich, LMU Munich, Munich, Germany.

Sabrina Katzdobler (S)

Department of Neurology, University Hospital of Munich, LMU Munich, Munich, Germany.

Mengmeng Song (M)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.

Gloria Biechele (G)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.

Maike Kern (M)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.

Maximilian Scheifele (M)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.

Boris-Stephan Rauchmann (BS)

Department of Radiology, University Hospital of Munich, LMU Munich, Munich, Germany.

Robert Perneczky (R)

Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.
German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Munich, Germany.
Ageing Epidemiology Research Unit (AGE), School of Public Health, Imperial College, London, UK.

Michael Rullman (M)

Department of Nuclear Medicine, University Hospital Leipzig, Leipzig, Germany.

Marianne Patt (M)

Department of Nuclear Medicine, University Hospital Leipzig, Leipzig, Germany.

Andreas Schildan (A)

Department of Nuclear Medicine, University Hospital Leipzig, Leipzig, Germany.

Henryk Barthel (H)

Department of Nuclear Medicine, University Hospital Leipzig, Leipzig, Germany.

Osama Sabri (O)

Department of Nuclear Medicine, University Hospital Leipzig, Leipzig, Germany.

Jost J Rumpf (JJ)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.
Department of Nuclear Medicine, University Hospital Cologne, Cologne, Germany.

Matthias L Schroeter (ML)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.
Department of Nuclear Medicine, University Hospital Cologne, Cologne, Germany.

Joseph Classen (J)

Department of Neurology, University Hospital Leipzig, Leipzig, Germany.

Victor Villemagne (V)

Department of Molecular Imaging & Therapy, Austin Health, Heidelberg, VIC, Australia.
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA.
Department of Medicine, Austin Health, The University of Melbourne, Melbourne, VIC, Australia.

John Seibyl (J)

InviCRO, LLC, Boston, MA, USA.
Molecular Neuroimaging, A Division of inviCRO, New Haven, CT, USA.

Andrew W Stephens (AW)

Life Molecular Imaging GmbH, Berlin, Germany.

Edward B Lee (EB)

Center for Neurodegenerative Disease Research (CNDR), Institute On Aging and Department of Pathology & Laboratory Medicine, University of Pennsylvania, Philadelphia, PA, USA.

David G Coughlin (DG)

Frontotemporal Degeneration Center, University of Pennsylvania, Philadelphia, PA, USA.
Department of Neurosciences, University of California, La Jolla, San Diego, CA, USA.

Armin Giese (A)

Center for Neuropathology and Prion Research, LMU Munich, Munich, Germany.

Murray Grossman (M)

Frontotemporal Degeneration Center, University of Pennsylvania, Philadelphia, PA, USA.
Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA.

Corey T McMillan (CT)

Frontotemporal Degeneration Center, University of Pennsylvania, Philadelphia, PA, USA.
Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA.

Ellen Gelpi (E)

Neurological Tissue Bank and Neurology Department, Hospital Clínic de Barcelona, Universitat de Barcelona, IDIBAPS, CERCA, Barcelona, Catalonia, Spain.
Institute of Neurology, Medical University of Vienna, Vienna, Austria.

Laura Molina-Porcel (L)

Neurological Tissue Bank and Neurology Department, Hospital Clínic de Barcelona, Universitat de Barcelona, IDIBAPS, CERCA, Barcelona, Catalonia, Spain.
Institute of Neurology, Medical University of Vienna, Vienna, Austria.

Yaroslau Compta (Y)

Parkinson's Disease & Movement Disorders Unit, Hospital Clínic / IDIBAPS / CIBERNED (CB06/05/0018-ISCIII), / European Reference Network for Rare Neurological Diseases (ERN-RND) / Institut de Neurociències (Maria de Maeztu Center), Universitat de Barcelona, Barcelona, Catalonia, Spain.

John C van Swieten (JC)

Department of Neurology, Erasmus Medical Centre, Rotterdam, The Netherlands.

Laura Donker Laat (LD)

Department Clinical Genetics, Erasmus Medical Center, Rotterdam, The Netherlands.

Claire Troakes (C)

London Neurodegenerative Diseases Brain Bank, Institute of Psychiatry, Psychology and Neuroscience, Kings College London, London, UK.

Safa Al-Sarraj (S)

London Neurodegenerative Diseases Brain Bank, Institute of Psychiatry, Psychology and Neuroscience, Kings College London, London, UK.

John L Robinson (JL)

Center for Neurodegenerative Disease Research (CNDR), Institute On Aging and Department of Pathology & Laboratory Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Sharon X Xie (SX)

Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania, Philadelphia, PA, USA.

David J Irwin (DJ)

Department of Neurology, Klinikum Rechts der Isar, Technical University of Munich, Munich, Germany.
Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA.

Sigrun Roeber (S)

Center for Neuropathology and Prion Research, LMU Munich, Munich, Germany.

Jochen Herms (J)

German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.

Mikael Simons (M)

German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.

Peter Bartenstein (P)

Department of Nuclear Medicine, University Hospital of Munich, LMU Munich, Munich, Germany.

Virginia M Lee (VM)

Center for Neurodegenerative Disease Research (CNDR), Institute On Aging and Department of Pathology & Laboratory Medicine, University of Pennsylvania, Philadelphia, PA, USA.

John Q Trojanowski (JQ)

Center for Neurodegenerative Disease Research (CNDR), Institute On Aging and Department of Pathology & Laboratory Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Johannes Levin (J)

Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.
German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Department of Neurology, University Hospital of Munich, LMU Munich, Munich, Germany.

Günter Höglinger (G)

German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Department of Neurology, Hannover Medical School, Hannover, Germany.

Michael Ewers (M)

Institute for Stroke and Dementia Research, University Hospital of Munich, LMU Munich, Munich, Germany.
German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH