Diverging longitudinal changes in astrocytosis and amyloid PET in autosomal dominant Alzheimer's disease

Brain

Volumn 139, Issue 3, 2016, Pages 922-936

  Rodriguez Vieitez, Elena ^a   Saint Aubert, Laure ^a   Carter, Stephen F ^a,e   Almkvist, Ove ^a,b,c   Farid, Karim ^a   Schöll, Michael ^a,f   Chiotis, Konstantinos ^a   Thordardottir, Steinunn ^a,c   Graff, Caroline ^a,c   Wall, Anders ^d   Långström, Bengt ^d   Nordberg, Agneta ^a,c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d UPPSALA UNIVERSITY   (Sweden)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

11C deuterium L deprenyl; 11C Pittsburgh compound B; 18F fluorodeoxyglucose; Astrocytosis; Autosomal dominant Alzheimer's disease

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; AMYLOID PROTEIN; BIOLOGICAL MARKER; DEUTERIUM L DEPRENYL C 11; FLUORODEOXYGLUCOSE F 18; GLUCOSE; PITTSBURGH COMPOUND B; PRESENILIN 1; TRACER; UNCLASSIFIED DRUG;

ADULT; ALZHEIMER DISEASE; AMYLOID PLAQUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; AUTOSOMAL DOMINANT DISORDER; CEREBELLUM; CEREBROSPINAL FLUID; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE COURSE; FAMILY; FEMALE; FOLLOW UP; GENE MUTATION; GLUCOSE METABOLISM; GRAY MATTER; HUMAN; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MILD COGNITIVE IMPAIRMENT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RADIOLOGICAL PARAMETERS; SPORADIC ALZHEIMER DISEASE; STANDARDIZED UPTAKE VALUE; AGED; CROSS-SECTIONAL STUDY; DIAGNOSTIC IMAGING; GENETICS; GLIOSIS; MIDDLE AGED; TRENDS;

ADULT; AGED; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; CROSS-SECTIONAL STUDIES; FEMALE; FOLLOW-UP STUDIES; GLIOSIS; HUMANS; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; PLAQUE, AMYLOID; POSITRON-EMISSION TOMOGRAPHY;

EID: 84960893772     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awv404     Document Type: Article

References (78)

1. Allaman I, Gavillet M, Bélanger M, Laroche T, Viertl D, Lashuel HA, et al. Amyloid-beta aggregates cause alterations of astrocytic metabolic phenotype: impact on neuronal viability. J Neurosci 2010;30:3326-38.
2. Anderson MA, Ao Y, Sofroniew MV. Heterogeneity of reactive astrocytes. Neurosci Lett 2014;565:23-9.
3. Barres BA. The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 2008;60:430-40.
4. Bateman RJ, Aisen PS, De Strooper B, Fox NC, Lemere CA, Ringman JM, et al. Autosomal-dominant Alzheimer's disease: a review and proposal for the prevention of Alzheimer's disease. Alzheimers Res Ther 2011;3:1.
5. Bateman RJ, Xiong C, Benzinger TL, Fagan AM, Goate A, Fox NC, et al. Clinical and biomarker changes in dominantly inherited Alzheimer's disease. N Engl J Med 2012;367:795-804.
6. Benjamini Y, Hochberg Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 1995;57:289-300.
7. Benzinger TL, Blazey T, Jack CR, Jr, Koeppe RA, Su Y, Xiong C, et al. Regional variability of imaging biomarkers in autosomal dominant Alzheimer's disease. Proc Natl Acad Sci USA 2013;110:E4502-9.
8. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991;82:239-59.
9. Carter SF, Schöll M, Almkvist O, Wall A, Engler H, Långström B, et al. Evidence for astrocytosis in prodromal Alzheimer disease provided by 11C-deuterium-L-deprenyl: a multitracer PET paradigm combining 11C-Pittsburgh compound B and 18F-FDG. J Nucl Med 2012;53:37-46.
10. Chételat G. Alzheimer disease: abeta-independent processes-rethinking preclinical AD. Nat Rev Neurol 2013;9:123-4.
11. Choo IH, Carter SF, Schöll ML, Nordberg A. Astrocytosis measured by (11) C-deprenyl PET correlates with decrease in gray matter density in the parahippocampus of prodromal Alzheimer's patients. Eur J Nucl Med Mol Imaging 2014;41:2120-6.
12. Dubois B, Feldman HH, Jacova C, Hampel H, Molinuevo JL, Blennow K, et al. Advancing research diagnostic criteria for Alzheimer's disease: the IWG-2 criteria. Lancet Neurol 2014;13:614-29.
13. Dunn OJ. Multiple comparisons using rank sums. Technometrics 1964;6:241-52.
14. Ekblom J, Jossan SS, Bergström M, Oreland L, Walum E, Aquilonius SM. Monoamine oxidase-B in astrocytes. Glia 1993;8:122-32.
15. Fleisher AS. The value of biomarker comparisons between autosomal dominant and late-onset Alzheimer disease. JAMA Neurol 2014;71:1087-8.
16. Fleisher AS, Chen K, Quiroz YT, Jakimovich LJ, Gomez MG, Langois CM, et al. Florbetapir PET analysis of amyloid-beta deposition in the presenilin 1 E280A autosomal dominant Alzheimer's disease kindred: a cross-sectional study. Lancet Neurol 2012;11:1057-65.
17. Fleisher AS, Chen K, Quiroz YT, Jakimovich LJ, Gutierrez Gomez M, Langois CM, et al. Associations between biomarkers and age in the presenilin 1 E280A autosomal dominant Alzheimer disease kindred: a cross-sectional study. JAMA Neurol 2015;72:316-24.
18. Fortea J, Sala-Llonch R, Bartres-Faz D, Bosch B, Llado A, Bargallo N, et al. Increased cortical thickness and caudate volume precede atrophy in PSEN1 mutation carriers. J Alzheimers Dis 2010;22:909-22.
19. Fowler JS, MacGregor RR, Wolf AP, Arnett CD, Dewey SL, Schlyer D, et al. Mapping human brain monoamine oxidase A and B with 11C-labeled suicide inactivators and PET. Science 1987;235:481-5.
20. Fowler JS, Logan J, Volkow ND, Wang G-J. Translational neuroimaging: positron emission tomography studies of monoamine oxidase. Mol Imaging Biol 2005;7:377-87.
21. Fuller S, Munch G, Steele M. Activated astrocytes: a therapeutic target in Alzheimer's disease?. Expert Rev Neurother 2009;9:1585-94.
22. Furman JL, Sama DM, Gant JC, Beckett TL, Murphy MP, Bachstetter AD, et al. Targeting astrocytes ameliorates neurologic changes in a mouse model of Alzheimer's disease. J Neurosci 2012;32:16129-40.
23. Gulyás B, Pavlova E, Kása P, Gulya K, Bakota L, Várszegi S, et al. Activated MAO-B in the brain of Alzheimer patients, demonstrated by [11C]-L-deprenyl using whole hemisphere autoradiography. Neurochem Int 2011;58:60-8.
24. Hammers A, Allom R, Koepp MJ, Free SL, Myers R, Lemieux L, et al. Three-dimensional maximum probability atlas of the human brain, with particular reference to the temporal lobe. Hum Brain Mapp 2003;19:224-47.
25. Hardy JA, Higgins GA. Alzheimer's disease: the amyloid cascade hypothesis. Science 1992;256:184-5.
26. Heneka MT, Carson MJ, Khoury JE, Landreth GE, Brosseron F, Feinstein DL, et al. Neuroinflammation in Alzheimer's disease. Lancet Neurol 2015a; 14:388-405.
27. Heneka MT, Golenbock DT, Latz E. Innate immunity in Alzheimer's disease. Nat Immunol 2015b; 16:229-36.
28. Holtzman DM, Morris JC, Goate AM. Alzheimer's disease: the challenge of the second century. Sci Transl Med 2011;3:77sr1.
29. Hyman BT. Amyloid-dependent and amyloid-independent stages of Alzheimer disease. Arch Neurol 2011;68:1062-4.
30. Jack CR, Jr, Holtzman DM. Biomarker modeling of Alzheimer's disease. Neuron 2013;80:1347-58.
31. Jacobs AH, Tavitian B, Consortium I. Noninvasive molecular imaging of neuroinflammation. J Cereb Blood Flow Metab 2012;32:1393-415.
32. Johansson A, Engler H, Blomquist G, Scott B, Wall A, Aquilonius SM, et al. Evidence for astrocytosis in ALS demonstrated by [11C] (L) - deprenyl-D2 PET. J Neurol Sci 2007;255:17-22.
33. Kadir A, Marutle A, Gonzalez D, Schöll M, Almkvist O, Mousavi M, et al. Positron emission tomography imaging and clinical progression in relation to molecular pathology in the first Pittsburgh Compound B positron emission tomography patient with Alzheimer's disease. Brain 2011;134(Pt 1):301-17.
34. Keller L, Welander H, Chiang HH, Tjernberg LO, Nennesmo I, Wallin AK, et al. The PSEN1 I143T mutation in a Swedish family with Alzheimer's disease: clinical report and quantification of Abeta in different brain regions. Eur J Hum Genet 2010;18:1202-8.
35. Klunk WE, Price JC, Mathis CA, Tsopelas ND, Lopresti BJ, Ziolko SK, et al. Amyloid deposition begins in the striatum of presenilin-1 mutation carriers from two unrelated pedigrees. J Neurosci 2007;27:6174-84.
36. Koivunen J, Verkkoniemi A, Aalto S, Paetau A, Ahonen JP, Viitanen M, et al. PET amyloid ligand [11C]PIB uptake shows predominantly striatal increase in variant Alzheimer's disease. Brain 2008;131(Pt 7):1845-53.
37. La Joie R, Perrotin A, Barre L, Hommet C, Mezenge F, Ibazizene M, et al. Region-specific hierarchy between atrophy, hypometabolism, and beta-amyloid (Abeta) load in Alzheimer's disease dementia. J Neurosci 2012;32:16265-73.
38. Marutle A, Gillberg PG, Bergfors A, Yu W, Ni R, Nennesmo I, et al. 3H-Deprenyl and 3H-PIB autoradiography show different laminar distributions of astroglia and fibrillar beta-amyloid in Alzheimer brain. J Neuroinflammation 2013;10:90.
39. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of department of health and human services task force on Alzheimer's disease. Neurology 1984;34:939-44.
40. Miller G. Neuroscience. The dark side of glia. Science 2005;308:778-81.
41. Minoshima S, Frey KA, Foster NL, Kuhl DE. Preserved pontine glucose metabolism in Alzheimer disease: a reference region for functional brain image (PET) analysis. J Comput Assist Tomogr 1995;19:541-7.
42. Mulder SD, Veerhuis R, Blankenstein MA, Nielsen HM. The effect of amyloid associated proteins on the expression of genes involved in amyloid-beta clearance by adult human astrocytes. Exp Neurol 2012;233:373-9.
43. Ni R. Multiple amyloid binding sites in Alzheimer brain and their interaction with synaptic and inflammatory mechanisms. Doctoral Thesis. Karolinska Institutet, Sweden; 2015. ISBN: 978-91-7549-873-7.
44. Nordberg A, Carter SF, Rinne J, Drzezga A, Brooks DJ, Vandenberghe R, et al. A European multicentre PET study of fibrillar amyloid in Alzheimer's disease. Eur J Nucl Med Mol Imaging 2013;40:104-14.
45. Oberheim NA, Goldman SA, Nedergaard M. Heterogeneity of astrocytic form and function. Methods Mol Biol 2012;814:23-45.
46. Petersen RC. Mild cognitive impairment as a diagnostic entity. J Intern Med 2004;256:183-94.
47. Potter R, Patterson BW, Elbert DL, Ovod V, Kasten T, Sigurdson W, et al. Increased in vivo amyloid-beta42 production, exchange, and loss in presenilin mutation carriers. Sci Transl Med 2013;5:189ra77.
48. Quiroz YT, Schultz AP, Chen K, Protas HD, Brickhouse M, Fleisher AS, et al. Brain imaging and blood biomarker abnormalities in children with autosomal dominant Alzheimer disease: a cross-sectional study. JAMA Neurol 2015;72:912-9.
49. Ringman JM, Goate A, Masters CL, Cairns NJ, Danek A, Graff-Radford N, et al. Genetic heterogeneity in Alzheimer disease and implications for treatment strategies. Curr Neurol Neurosci Rep 2014;14:499.
50. Rodriguez-Arellano JJ, Parpura V, Zorec R, Verkhratsky A. Astrocytes in physiological aging and Alzheimer's disease. Neuroscience 2015; http://dx.doi.org/10.1016/j.neuroscience.2015.01.007.
51. Rodriguez-Vieitez E, Ni R, Gulyás B, Tóth M, Häggkvist J, Halldin C, et al. Astrocytosis precedes amyloid plaque deposition in Alzheimer APPswe transgenic mouse brain: a correlative positron emission tomography and in vitro imaging study. Eur J Nucl Med Mol Imaging 2015;42:1119-32.
52. Ryan NS, Fox NC. Reply: implications of presymptomatic change in thalamus and caudate in Alzheimer's disease. Brain 2013;136(Pt 11):e259.
53. Ryan NS, Keihaninejad S, Shakespeare TJ, Lehmann M, Crutch SJ, Malone IB, et al. Magnetic resonance imaging evidence for presymptomatic change in thalamus and caudate in familial Alzheimer's disease. Brain 2013;136(Pt 5):1399-414.
54. Ryman DC, Acosta-Baena N, Aisen PS, Bird T, Danek A, Fox NC, et al. Symptom onset in autosomal dominant Alzheimer disease: a systematic review and meta-analysis. Neurology 2014;83:253-60.
55. Sala-Llonch R, Lladó A, Fortea J, Bosch B, Antonell A, Balasa M, et al. Evolving brain structural changes in PSEN1 mutation carriers. Neurobiol Aging 2015;36:1261-70.
56. Santillo AF, Gambini JP, Lannfelt L, Långström B, Ulla-Marja L, Kilander L, et al. In vivo imaging of astrocytosis in Alzheimer's disease: an C-11-L-deuteriodeprenyl and PIB PET study. Eur J Nucl Med Mol Imaging 2011;38:2202-8.
57. Saura J, Luque JM, Cesura AM, Da Prada M, Chan-Palay V, Huber G, et al. Increased monoamine oxidase B activity in plaque-associated astrocytes of Alzheimer brains revealed by quantitative enzyme radioautography. Neuroscience 1994;62:15-30.
58. Schöll M, Almkvist O, Axelman K, Stefanova E, Wall A, Westman E, et al. Glucose metabolism and PIB binding in carriers of a His163Tyr presenilin 1 mutation. Neurobiol Aging 2011a; 32:1388-99.
59. Schöll M, Almkvist O, Bogdanovic N, Wall A, Långström B, Viitanen M, et al. Time course of glucose metabolism in relation to cognitive performance and postmortem neuropathology in Met146Val PSEN1 mutation carriers. J Alzheimers Dis 2011b; 24:495-506.
60. Schöll M, Wall A, Thordardottir S, Ferreira D, Bogdanovic N, Långström B, et al. Low PiB PET retention in presence of pathologic CSF biomarkers in Arctic APP mutation carriers. Neurology 2012;79:229-36.
61. Schöll M, Carter SF, Westman E, Rodriguez-Vieitez E, Almkvist O, Thordardottir S, et al. Early astrocytosis in autosomal dominant Alzheimer's disease measured in vivo by multi-tracer positron emission tomography. Sci Rep 2015;5:16404.
62. Shinohara M, Fujioka S, Murray ME, Wojtas A, Baker M, Rovelet-Lecrux A, et al. Regional distribution of synaptic markers and APP correlate with distinct clinicopathological features in sporadic and familial Alzheimer's disease. Brain 2014;137(Pt 5):1533-49.
63. Smale G, Nichols NR, Brady DR, Finch CE, Horton WE, Jr. Evidence for apoptotic cell death in Alzheimer's disease. Exp Neurol 1995;133:225-30.
64. Song W, Zhou LJ, Zheng SX, Zhu XZ. Amyloid-beta 25-35 peptide induces expression of monoamine oxidase B in cultured rat astrocytes. Acta Pharmacol Sin 2000;21:557-63.
65. Thal DR. The role of astrocytes in amyloid beta-protein toxicity and clearance. Exp Neurol 2012;236:1-5.
66. Thomas JB, Brier MR, Bateman RJ, Snyder AZ, Benzinger TL, Xiong C, et al. Functional connectivity in autosomal dominant and late-onset Alzheimer disease. JAMA Neurol 2014;71:1111-22.
67. Thordardottir S, Ståhlbom AK, Ferreira D, Almkvist O, Westman E, Zetterberg H, et al. Preclinical cerebrospinal fluid and volumetric magnetic resonance imaging biomarkers in Swedish familial Alzheimer's disease. J Alzheimers Dis 2014;43:1393-402.
68. Turkheimer FE, Smith CB, Schmidt K. Estimation of the number of "true" null hypotheses in multivariate analysis of neuroimaging data. Neuroimage 2001;13:920-30.
69. Varley J, Brooks DJ, Edison P. Imaging neuroinflammation in Alzheimer's and other dementias: recent advances and future directions. Alzheimers Dement 2015;11:1110-20.
70. Verkhratsky A, Marutle A, Rodriguez-Arellano JJ, Nordberg A. Glial asthenia and functional paralysis: a new perspective on neurodegeneration and Alzheimer's disease. Neuroscientist 2015;21:552-68.
71. Villemagne VL, Ataka S, Mizuno T, Brooks WS, Wada Y, Kondo M, et al. High striatal amyloid beta-peptide deposition across different autosomal Alzheimer disease mutation types. Arch Neurol 2009;66:1537-44.
72. Villemagne VL, Burnham S, Bourgeat P, Brown B, Ellis KA, Salvado O, et al. Amyloid beta deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer's disease: a prospective cohort study. Lancet Neurol 2013;12:357-67.
73. Yau WW, Tudorascu DL, McDade EM, Ikonomovic S, James JA, Minhas D, et al. Longitudinal assessment of neuroimaging and clinical markers in autosomal dominant Alzheimer's disease: a prospective cohort study. Lancet Neurol 2015;14:804-13.
74. Yoshizawa H, Gazes Y, Stern Y, Miyata Y, Uchiyama S. Characterizing the normative profile of 18F-FDG PET brain imaging: sex difference, aging effect, and cognitive reserve. Psychiatry Res 2014;221:78-85.
75. Yu WF, Guan ZZ, Bogdanovic N, Nordberg A. High selective expression of alpha7 nicotinic receptors on astrocytes in the brains of patients with sporadic Alzheimer's disease and patients carrying Swedish APP 670/671 mutation: a possible association with neuritic plaques. Exp Neurol 2005;192:215-25.
76. Zhang Y, Barres BA. Astrocyte heterogeneity: an underappreciated topic in neurobiology. Curr Opin Neurobiol 2010;20:588-94.
77. Zimmer ER, Leuzy A, Benedet AL, Breitner J, Gauthier S, Rosa-Neto P. Tracking neuroinflammation in Alzheimer's disease: the role of positron emission tomography imaging. J Neuroinflammation 2014;11:120.
78. Zlokovic BV. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat Rev Neurosci 2011;12:723-38.