Tau, amyloid, and cascading network failure across the Alzheimer's disease spectrum

Cortex

Volumn 97, Issue , 2017, Pages 143-159

  Jones, David T ^a   Graff Radford, Jonathan ^a   Lowe, Val J ^a   Wiste, Heather J ^a   Gunter, Jeffrey L ^a   Senjem, Matthew L ^a   Botha, Hugo ^a   Kantarci, Kejal ^a   Boeve, Bradley F ^a   Knopman, David S ^a   Petersen, Ronald C ^a   Jack, Clifford R ^a  

^a MAYO CLINIC   (United States)

Author keywords

Alzheimer's disease; AV 1451; Braak staging; Cascading network failure; Complex systems

Indexed keywords

AMYLOID BETA PROTEIN; TAU PROTEIN;

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; COHORT ANALYSIS; CROSS-SECTIONAL STUDY; DEFAULT MODE NETWORK; ECHO PLANAR IMAGING; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MOLECULAR IMAGING; NEUROPATHOLOGY; NEUROPHYSIOLOGY; PATHOPHYSIOLOGY; STEREOTYPY; ADULT; BRAIN; COGNITION; DIAGNOSTIC IMAGING; DISEASE EXACERBATION; METABOLISM; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHYSIOLOGY; POSITRON EMISSION TOMOGRAPHY; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; BRAIN; COGNITION; DISEASE PROGRESSION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; POSITRON-EMISSION TOMOGRAPHY; TAU PROTEINS;

EID: 85033447801     PISSN: 00109452     EISSN: 19738102     Source Type: Journal    
DOI: 10.1016/j.cortex.2017.09.018     Document Type: Article

References (66)

1. Alafuzoff, I., Arzberger, T., Al-Sarraj, S., Bodi, I., Bogdanovic, N., Braak, H., et al. Staging of neurofibrillary pathology in Alzheimer's disease: A study of the BrainNet Europe Consortium. Brain Pathology 18:4 (2008 Oct.), 484–496.
2. Albert, M.S., DeKosky, S.T., Dickson, D., Dubois, B., Feldman, H.H., Fox, N.C., et al. The diagnosis of mild cognitive impairment due to Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers & Dementia 7:3 (2011 May), 270–279.
3. Alladi, S., Xuereb, J., Bak, T., Nestor, P., Knibb, J., Patterson, K., et al. Focal cortical presentations of Alzheimer's disease. Brain 130 (2007 Oct.), 2636–2645.
4. Baddeley, A.D., Hitch, G.J., Working memory. Bower, G.A., (eds.) The psychology of learning and motivation, 1974, Academic Press, New York, 47–89.
5. Bateman, R.J., Xiong, C., Benzinger, T.L., Fagan, A.M., Goate, A., Fox, N.C., et al. Clinical and biomarker changes in dominantly inherited Alzheimer's disease. The New England Journal of Medicine 367:9 (2012 Aug. 30), 795–804.
6. Bates, D., Machler, M., Bolker, B.M., Walker, S.C., Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1 (2015 Oct.), 1–48.
7. Bennett, D.A., Schneider, J.A., Wilson, R.S., Bienias, J.L., Arnold, S.E., Neurofibrillary tangles mediate the association of amyloid load with clinical Alzheimer disease and level of cognitive function. Archives of Neurology 61:3 (2004 Mar.), 378–384.
8. Bero, A.W., Yan, P., Roh, J.H., Cirrito, J.R., Stewart, F.R., Raichle, M.E., et al. Neuronal activity regulates the regional vulnerability to amyloid-beta deposition. Nature Neuroscience, 14(6), 2011 Jun. 750–U353.
9. Braak, H., Alafuzoff, I., Arzberger, T., Kretzschmar, H., Del Tredici, K., Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathologica 112:4 (2006 Oct.), 389–404.
10. Braak, H., Braak, E., Neuropathological stageing of Alzheimer-related changes. Acta neuropathologica 82:4 (1991), 239–259.
11. Braak, H., Braak, E., Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiology of Aging 18:4 (1997 Jul-Aug), 351–357.
12. Braak, H., Braak, E., Bohl, J., Reintjes, R., Age, neurofibrillary changes, A beta-amyloid and the onset of Alzheimer's disease. Neuroscience Letters 210:2 (1996 May 31), 87–90.
13. Braak, H., Thal, D.R., Ghebremedhin, E., Del Tredici, K., Stages of the pathologic process in Alzheimer disease: Age categories from 1 to 100 years. Journal of Neuropathology and Experimental Neurology 70:11 (2011 Nov.), 960–969.
14. Brier, M.R., Gordon, B., Friedrichsen, K., McCarthy, J., Stern, A., Christensen, J., et al. Tau and Abeta imaging, CSF measures, and cognition in Alzheimer's disease. Science Translational Medicine, 8(338), 2016 May 11 338ra66.
15. Buckner, R.L., Sepulcre, J., Talukdar, T., Krienen, F.M., Liu, H., Hedden, T., et al. Cortical hubs revealed by intrinsic functional connectivity: Mapping, assessment of stability, and relation to Alzheimer's disease. The Journal of Neuroscience: the official journal of the Society for Neuroscience 29:6 (2009 Feb. 11), 1860–1873.
16. Calhoun, V.D., Adali, T., Pearlson, G.D., Pekar, J.J., A method for making group inferences from functional MRI data using independent component analysis. Human Brain Mapping 14:3 (2001 Nov.), 140–151.
17. Cho, H., Choi, J.Y., Hwang, M.S., Kim, Y.J., Lee, H.M., Lee, H.S., et al. In vivo cortical spreading pattern of tau and amyloid in the Alzheimer's disease spectrum. Annals of Neurology, 2016 Jun. 20.
18. Cirrito, J.R., Yamada, K.A., Finn, M.B., Sloviter, R.S., Bales, K.R., May, P.C., et al. Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo. Neuron 48:6 (2005 Dec. 22), 913–922.
19. Crary, J.F., Trojanowski, J.Q., Schneider, J.A., Abisambra, J.F., Abner, E.L., Alafuzoff, I., et al. Primary age-related tauopathy (PART): A common pathology associated with human aging. Acta Neuropathologica 128:6 (2014 Dec.), 755–766.
20. Dickson, D.W., Crystal, H.A., Mattiace, L.A., Masur, D.M., Blau, A.D., Davies, P., et al. Identification of normal and pathological aging in prospectively studied nondemented elderly humans. Neurobiology of Aging 13:1 (1992 Jan-Feb), 179–189.
21. Duyckaerts, C., Bennecib, M., Grignon, Y., Uchihara, T., He, Y., Piette, F., et al. Modeling the relation between neurofibrillary tangles and intellectual status. Neurobiology of Aging 18:3 (1997 May-Jun), 267–273.
22. Greicius, M.D., Kimmel, D.L., Neuroimaging insights into network-based neurodegeneration. Current Opinion in Neurology 25:6 (2012 Dec.), 727–734.
23. Gunter, J.L., Bernstein, M.A., Borowski, B.J., Ward, C.P., Britson, P.J., Felmlee, J.P., et al. Measurement of MRI scanner performance with the ADNI phantom. Medical Physics 36:6 (2009 Jun.), 2193–2205.
24. Haberman, R.P., Koh, M.T., Gallagher, M., Heightened cortical excitability in aged rodents with memory impairment. Neurobiology of Aging, 2017 Jan. 03.
25. Jack, C.R. Jr., Bernstein, M.A., Fox, N.C., Thompson, P., Alexander, G., Harvey, D., et al. The Alzheimer's disease neuroimaging Initiative (ADNI): MRI methods. Journal of Magnetic Resonance Imaging: JMRI 27:4 (2008 Apr.), 685–691.
26. Jack, C.R. Jr., Knopman, D.S., Jagust, W.J., Petersen, R.C., Weiner, M.W., Aisen, P.S., et al. Tracking pathophysiological processes in Alzheimer's disease: An updated hypothetical model of dynamic biomarkers. Lancet Neurology 12:2 (2013 Feb.), 207–216.
27. Jack, C.R. Jr., Knopman, D.S., Weigand, S.D., Wiste, H.J., Vemuri, P., Lowe, V., et al. An operational approach to National Institute on Aging-Alzheimer's Association criteria for preclinical Alzheimer disease. Annals of Neurology 71:6 (2012 Jun.), 765–775.
28. Jack, C.R. Jr., Wiste, H.J., Lesnick, T.G., Weigand, S.D., Knopman, D.S., Vemuri, P., et al. Brain beta-amyloid load approaches a plateau. Neurology 80:10 (2013 Mar. 5), 890–896.
29. Jack, C.R. Jr., Wiste, H.J., Weigand, S.D., Therneau, T.M., Lowe, V.J., Knopman, D.S., et al. Defining imaging biomarker cut points for brain aging and Alzheimer's disease. Alzheimer's & Dementia: the Journal of the Alzheimer's Association 13:3 (2017 Mar.), 205–216.
30. Johnson, K.A., Schultz, A., Betensky, R.A., Becker, J.A., Sepulcre, J., Rentz, D., et al. Tau positron emission tomographic imaging in aging and early Alzheimer disease. Annals of Neurology 79:1 (2016 Jan.), 110–119.
31. Jones, D.T., Knopman, D.S., Gunter, J.L., Graff-Radford, J., Vemuri, P., Boeve, B.F., et al. Cascading network failure across the Alzheimer's disease spectrum. Brain: A Journal of Neurology 139:Pt 2 (2016 Feb.), 547–562.
32. Jones, D.T., Vemuri, P., Murphy, M.C., Gunter, J.L., Senjem, M.L., Machulda, M.M., et al. Non-stationarity in the “resting brain's” modular architecture. Plos One, 7(6), 2012, e39731.
33. Klunk, W.E., Engler, H., Nordberg, A., Wang, Y., Blomqvist, G., Holt, D.P., et al. Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Annals of Neurology 55:3 (2004), 306–319.
34. Lowe, V.J., Curran, G., Fang, P., Liesinger, A.M., Josephs, K.A., Parisi, J.E., et al. An autoradiographic evaluation of AV-1451 Tau PET in dementia. Acta Neuropathologica Communications, 4(1), 2016, 58.
35. Maass, A., Landau, S., Baker, S.L., Horng, A., Lockhart, S.N., La Joie, R., et al. Comparison of multiple tau-PET measures as biomarkers in aging and Alzheimer's disease. NeuroImage 8/15/:157 (2017), 448–463.
36. McKhann, G.M., Knopman, D.S., Chertkow, H., Hyman, B.T., Jack, C.R., Kawas, C.H., et al. The diagnosis of dementia due to Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers & Dementia 7:3 (2011 May), 263–269.
37. Mesulam, N.M., Neuroplasticity failure in Alzheimer's disease: Bridging the gap between plaques and tangles. Neuron 24:3 (1999 Nov.), 521–529.
38. Mesulam, M.M., Weintraub, S., Rogalski, E.J., Wieneke, C., Geula, C., Bigio, E.H., Asymmetry and heterogeneity of Alzheimer's and frontotemporal pathology in primary progressive aphasia. Brain 137 (2014 Apr.), 1176–1192.
39. Mishra, S., Gordon, B.A., Su, Y., Christensen, J., Friedrichsen, K., Jackson, K., et al. AV-1451 PET imaging of tau pathology in preclinical Alzheimer disease: Defining a summary measure. NeuroImage, 2017 2017/07/26/.
40. Murray, M.E., Graff-Radford, N.R., Ross, O.A., Petersen, R.C., Duara, R., Dickson, D.W., Neuropathologically defined subtypes of Alzheimer's disease with distinct clinical characteristics: A retrospective study. Lancet Neurology 10:9 (2011 Sep.), 785–796.
41. Ossenkoppele, R., Schonhaut, D.R., Scholl, M., Lockhart, S.N., Ayakta, N., Baker, S.L., et al. Tau PET patterns mirror clinical and neuroanatomical variability in Alzheimer's disease. Brain, 2016 Mar. 8.
42. Palop, J.J., Mucke, L., Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: From synapses toward neural networks. Nature Neuroscience 13:7 (2010 Jul.), 812–818.
43. Petersen, R.C., (eds.) Mild cognitive impairment: Aging to Alzheimer's disease, 2003, Oxford University Press, New York, NY, US.
44. Petersen, R.C., Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine 256:3 (2004 Sep.), 183–194.
45. Petersen, R.C., Graff-Radford, J., Bradley's neurology in clinical practice/[edited by] Robert B. Daroff. [et al.]., 7th ed. Daroff, R.B., Jankovic, J., Mazziotta, J.C., Pomeroy, S.L., (eds.) Bradley's neurology in clinical practice, 2016, Elsevier/Saunders, Philadelphia, PA, 1380–1421.
46. Raj, A., Kuceyeski, A., Weiner, M., A network diffusion model of disease progression in dementia. Neuron 73:6 (2012 Mar. 22), 1204–1215.
47. Roberts, R.O., Geda, Y.E., Knopman, D.S., Cha, R.H., Pankratz, V.S., Boeve, B.F., et al. The Mayo clinic study of aging: Design and sampling, participation, baseline measures and sample characteristics. Neuroepidemiology 30:1 (2008), 58–69.
48. Saper, C.B., Wainer, B.H., German, D.C., Axonal and transneuronal transport in the transmission of neurological disease: Potential role in system degenerations, including Alzheimer's disease. Neuroscience 23:2 (1987 Nov.), 389–398.
49. Scholl, M., Lockhart, S.N., Schonhaut, D.R., O'Neil, J.P., Janabi, M., Ossenkoppele, R., et al. PET imaging of tau deposition in the aging human brain. Neuron 89:5 (2016 Mar. 2), 971–982.
50. Schwarz, A.J., Yu, P., Miller, B.B., Shcherbinin, S., Dickson, J., Navitsky, M., et al. Regional profiles of the candidate tau PET ligand 18F-AV-1451 recapitulate key features of Braak histopathological stages. Brain, 2016 Mar. 2.
51. Seeley, W.W., Crawford, R.K., Zhou, J., Miller, B.L., Greicius, M.D., Neurodegenerative diseases target large-scale human brain networks. Neuron 62:1 (2009 Apr. 16), 42–52.
52. Senjem, M.L., Gunter, J.L., Shiung, M.M., Petersen, R.C., Jack, C.R. Jr., Comparison of different methodological implementations of voxel-based morphometry in neurodegenerative disease. NeuroImage 26:2 (2005 Jun.), 600–608.
53. Sepulcre, J., Schultz, A.P., Sabuncu, M., Gomez-Isla, T., Chhatwal, J., Becker, A., et al. In vivo tau, amyloid, and gray matter profiles in the aging brain. The Journal of Neuroscience 36:28 (2016 Jul. 13), 7364–7374.
54. Spires-Jones, T.L., Hyman, B.T., The Intersection of amyloid beta and tau at synapses in Alzheimer's disease. Neuron 82:4 (2014 May 21), 756–771.
55. Stam, C.J., Modern network science of neurological disorders. Nature Reviews. Neuroscience 15:10 (2014 Oct.), 683–695.
56. Tingley, D., Yamamoto, T., Hirose, K., Keele, L., Imai, K., Mediation: R package for causal mediation analysis. Journal of Statistical Software, 59(5), 2014 Aug.
57. Vemuri, P., Senjem, M.L., Gunter, J.L., Lundt, E.S., Tosakulwong, N., Weigand, S.D., et al. Alzheimer's Disease Neuroimaging I. Accelerated vs. unaccelerated serial MRI based TBM-SyN measurements for clinical trials in Alzheimer's disease. NeuroImage 113 (2015 Jun.), 61–69.
58. Villemagne, V.L., Burnham, S., Bourgeat, P., Brown, B., Ellis, K.A., Salvado, O., et al. Amyloid beta deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer's disease: A prospective cohort study. The Lancet Neurology 12:4 (2013 Apr.), 357–367.
59. Walsh, D.M., Selkoe, D.J., A critical appraisal of the pathogenic protein spread hypothesis of neurodegeneration. Nature Reviews. Neuroscience 17:4 (2016 Mar. 18), 251–260.
60. Warren, J.D., Fletcher, P.D., Golden, H.L., The paradox of syndromic diversity in Alzheimer disease. Nature Reviews. Neurology 8:8 (2012 Aug.), 451–464.
61. Warren, J.D., Rohrer, J.D., Schott, J.M., Fox, N.C., Hardy, J., Rossor, M.N., Molecular nexopathies: A new paradigm of neurodegenerative disease. Trends in Neurosciences 36:10 (2013 Oct.), 561–569.
62. Whitwell, J.L., Jones, D.T., Duffy, J.R., Strand, E.A., Machulda, M.M., Przybelski, S.A., et al. Working memory and language network dysfunctions in logopenic aphasia: A task-free fMRI comparison with Alzheimer's dementia. Neurobiology of Aging 36:3 (2015), 1245–1252.
63. Wiepert, D., Lowe, V., Knopman, D., Boeve, B., Graff-Radford, J., Petersen, R., et al. A robust biomarker of large-scale network failure in Alzheimer's disease. Alzheimer's and dementia: Diagnosis. Assessment & Disease Monitoring 6 (2017), 152–161.
64. Wood, S.N., Generalized additive models: An introduction with R. 2006, Chapman & Hall/CRC, Boca Raton.
65. Xia, C.F., Arteaga, J., Chen, G., Gangadharmath, U., Gomez, L.F., Kasi, D., et al. [(18)F]T807, a novel tau positron emission tomography imaging agent for Alzheimer's disease. Alzheimer's & Dementia: the Journal of the Alzheimer's Association 9:6 (2013 Nov.), 666–676.
66. Zhou, J., Gennatas, E.D., Kramer, J.H., Miller, B.L., Seeley, W.W., Predicting regional neurodegeneration from the healthy brain functional connectome. Neuron 73:6 (2012 Mar. 22), 1216–1227.