The prion model for progression and diversity of neurodegenerative diseases

The Lancet Neurology

Volumn 16, Issue 4, 2017, Pages 323-332

  Stopschinski, Barbara E ^a   Diamond, Marc I ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; AMYLOID PROTEIN; HUNTINGTIN; TAU PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; BIOSAFETY; DISEASE COURSE; FRONTOTEMPORAL DEMENTIA; HUMAN; MOLECULAR PATHOLOGY; NERVE DEGENERATION; NEUROANATOMY; NEUROPATHOLOGY; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRION DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; VIRUS INFECTIVITY; ANIMAL; BIOLOGICAL MODEL; CLASSIFICATION; DEGENERATIVE DISEASE; DISEASE EXACERBATION; PATHOLOGY;

ANIMALS; DISEASE PROGRESSION; HUMANS; MODELS, BIOLOGICAL; NEURODEGENERATIVE DISEASES; PRION DISEASES;

EID: 85013662802     PISSN: 14744422     EISSN: 14744465     Source Type: Journal    
DOI: 10.1016/S1474-4422(17)30037-6     Document Type: Review

References (103)

1. 1 Walker, LC, Jucker, M, Neurodegenerative diseases: expanding the prion concept. Annu Rev Neurosci 38 (2015), 87–103.
2. 2 Guo, JL, Lee, VM, Cell-to-cell transmission of pathogenic proteins in neurodegenerative diseases. Nat Med 20 (2014), 130–138.
3. 3 Kaufman, SK, Diamond, MI, Prion-like propagation of protein aggregation and related therapeutic strategies. Neurotherapeutics 10 (2013), 371–382.
4. 4 Prusiner, SB, Biology and genetics of prions causing neurodegeneration. Annu Rev Genet 47 (2013), 601–623.
5. 5 Hagiwara, K, Hara, H, Hanada, K, Species-barrier phenomenon in prion transmissibility from a viewpoint of protein science. J Biochem 153 (2013), 139–145.
6. 6 Sanders, DW, Kaufman, SK, DeVos, SL, et al. Distinct tau prion strains propagate in cells and mice and define different tauopathies. Neuron 82 (2014), 1271–1288.
7. 7 Sanders, DW, Kaufman, SK, Holmes, BB, Diamond, MI, Prions and protein assemblies that convey biological information in health and disease. Neuron 89 (2016), 433–448.
8. 8 Baker, HF, Ridley, RM, Duchen, LW, Crow, TJ, Bruton, CJ, Experimental induction of beta-amyloid plaques and cerebral angiopathy in primates. Ann N Y Acad Sci 695 (1993), 228–231.
9. 9 Goudsmit, J, Morrow, CH, Asher, DM, et al. Evidence for and against the transmissibility of Alzheimer disease. Neurology 30 (1980), 945–950.
10. 10 Heilbronner, G, Eisele, YS, Langer, F, et al. Seeded strain-like transmission of β-amyloid morphotypes in APP transgenic mice. EMBO Rep 14 (2013), 1017–1022.
11. 11 Eisele, YS, Bolmont, T, Heikenwalder, M, et al. Induction of cerebral beta-amyloidosis: intracerebral versus systemic Abeta inoculation. Proc Natl Acad Sci USA 106 (2009), 12926–12931.
12. 12 Eisele, YS, Obermuller, U, Heilbronner, G, et al. Peripherally applied Abeta-containing inoculates induce cerebral beta-amyloidosis. Science 330 (2010), 980–982.
13. 13 Irwin, DJ, Abrams, JY, Schonberger, LB, et al. Evaluation of potential infectivity of Alzheimer and Parkinson disease proteins in recipients of cadaver-derived human growth hormone. JAMA Neurol 70 (2013), 462–468.
14. 14 Jaunmuktane, Z, Mead, S, Ellis, M, et al. Evidence for human transmission of amyloid-β pathology and cerebral amyloid angiopathy. Nature 525 (2015), 247–250.
15. 15 Wang, Y, Mandelkow, E, Tau in physiology and pathology. Nat Rev Neurosci 17 (2016), 5–21.
16. 16 Martinez-Murcia, FJ, Gorriz, JM, Ramirez, J, Puntonet, CG, Illan, IA, Alzheimer's Disease Neuroimaging I. Functional activity maps based on significance measures and independent component analysis. Comput Methods Programs Biomed 111 (2013), 255–268.
17. 17 Yanamandra, K, Kfoury, N, Jiang, H, et al. Anti-tau antibodies that block tau aggregate seeding in vitro markedly decrease pathology and improve cognition in vivo. Neuron 80 (2013), 402–414.
18. 18 Yanamandra, K, Jiang, H, Mahan, TE, et al. Anti-tau antibody reduces insoluble tau and decreases brain atrophy. Ann Clin Transl Neurol 2 (2015), 278–288.
19. 19 Wu, JW, Hussaini, SA, Bastille, IM, et al. Neuronal activity enhances tau propagation and tau pathology in vivo. Nat Neurosci 19 (2016), 1085–1092.
20. 20 Clavaguera, F, Akatsu, H, Fraser, G, et al. Brain homogenates from human tauopathies induce tau inclusions in mouse brain. Proc Natl Acad Sci USA 110 (2013), 9535–9540.
21. 21 Iba, M, Guo, JL, McBride, JD, Zhang, B, Trojanowski, JQ, Lee, VM, Synthetic tau fibrils mediate transmission of neurofibrillary tangles in a transgenic mouse model of Alzheimer's-like tauopathy. J Neurosci 33 (2013), 1024–1037.
22. 22 Guo, JL, Narasimhan, S, Changolkar, L, et al. Unique pathological tau conformers from Alzheimer's brains transmit tau pathology in nontransgenic mice. J Exp Med 213 (2016), 2635–2654.
23. 23 Kaufman, SK, Sanders, DW, Thomas, TL, et al. Tau prion strains dictate patterns of cell pathology, progression rate, and regional vulnerability in vivo. Neuron 92 (2016), 796–812.
24. 24 Beach, TG, White, CL 3rd, Hladik, CL, et al. Olfactory bulb alpha-synucleinopathy has high specificity and sensitivity for Lewy body disorders. Acta Neuropathol 117 (2009), 169–174.
25. 25 Ruffmann, C, Parkkinen, L, Gut feelings about α-synuclein in gastrointestinal biopsies: biomarker in the making?. Mov Disord 31 (2016), 193–202.
26. 26 Hilton, D, Stephens, M, Kirk, L, et al. Accumulation of α-synuclein in the bowel of patients in the pre-clinical phase of Parkinson's disease. Acta Neuropathol 127 (2014), 235–241.
27. 27 Sacino, AN, Brooks, M, Thomas, MA, et al. Intramuscular injection of α-synuclein induces CNS α-synuclein pathology and a rapid-onset motor phenotype in transgenic mice. Proc Natl Acad Sci USA 111 (2014), 10732–10737.
28. 28 Kordower, JH, Chu, Y, Hauser, RA, Freeman, TB, Olanow, CW, Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat Med 14 (2008), 504–506.
29. 29 Chu, Y, Kordower, JH, Age-associated increases of alpha-synuclein in monkeys and humans are associated with nigrostriatal dopamine depletion: is this the target for Parkinson's disease?. Neurobiol Dis 25 (2007), 134–149.
30. 30 Li, JY, Englund, E, Holton, JL, et al. Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 14 (2008), 501–503.
31. 31 Hansen, C, Angot, E, Bergstrom, AL, et al. α-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J Clin Invest 121 (2011), 715–725.
32. 32 Freundt, EC, Maynard, N, Clancy, EK, et al. Neuron-to-neuron transmission of α-synuclein fibrils through axonal transport. Ann Neurol 72 (2012), 517–524.
33. 33 Luk, KC, Kehm, VM, Zhang, B, O'Brien, P, Trojanowski, JQ, Lee, VM, Intracerebral inoculation of pathological α-synuclein initiates a rapidly progressive neurodegenerative alpha-synucleinopathy in mice. J Exp Med 209 (2012), 975–986.
34. 34 Luk, KC, Kehm, V, Carroll, J, et al. Pathological α-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science 338 (2012), 949–953.
35. 35 Rey, NL, Steiner, JA, Maroof, N, et al. Widespread transneuronal propagation of α-synucleinopathy triggered in olfactory bulb mimics prodromal Parkinson's disease. J Exp Med 213 (2016), 1759–1778.
36. 36 Watts, JC, Giles, K, Oehler, A, et al. Transmission of multiple system atrophy prions to transgenic mice. Proc Natl Acad Sci USA 110 (2013), 19555–19560.
37. 37 Peelaerts, W, Bousset, L, Van der Perren, A, et al. α-Synuclein strains cause distinct synucleinopathies after local and systemic administration. Nature 522 (2015), 340–344.
38. 38 Woerman, AL, Stohr, J, Aoyagi, A, et al. Propagation of prions causing synucleinopathies in cultured cells. Proc Natl Acad Sci USA 112 (2015), e4949–e4958.
39. 39 Van Langenhove, T, van der Zee, J, Van Broeckhoven, C, The molecular basis of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum. Ann Med 44 (2012), 817–828.
40. 40 Brettschneider, J, Del Tredici, K, Toledo, JB, et al. Stages of pTDP-43 pathology in amyotrophic lateral sclerosis. Ann Neurol 74 (2013), 20–38.
41. 41 Brettschneider, J, Del Tredici, K, Irwin, DJ, et al. Sequential distribution of pTDP-43 pathology in behavioral variant frontotemporal dementia (bvFTD). Acta Neuropathol 127 (2014), 423–439.
42. 42 Maniecka, Z, Polymenidou, M, From nucleation to widespread propagation: a prion-like concept for ALS. Virus Res 207 (2015), 94–105.
43. 43 Ayers, JI, Fromholt, SE, O'Neal, VM, Diamond, JH, Borchelt, DR, Prion-like propagation of mutant SOD1 misfolding and motor neuron disease spread along neuroanatomical pathways. Acta Neuropathol 131 (2016), 103–114.
44. 44 Cleary, JD, Ranum, LP, Repeat associated non-ATG (RAN) translation: new starts in microsatellite expansion disorders. Curr Opin Genet Dev 26 (2014), 6–15.
45. 45 Westergard, T, Jensen, BK, Wen, X, et al. Cell-to-cell transmission of dipeptide repeat proteins linked to C9orf72-ALS/FTD. Cell Rep 17 (2016), 645–652.
46. 46 Saudou, F, Humbert, S, The biology of huntingtin. Neuron 89 (2016), 910–926.
47. 47 Ren, PH, Lauckner, JE, Kachirskaia, I, Heuser, JE, Melki, R, Kopito, RR, Cytoplasmic penetration and persistent infection of mammalian cells by polyglutamine aggregates. Nat Cell Biol 11 (2009), 219–225.
48. 48 Trevino, RS, Lauckner, JE, Sourigues, Y, et al. Fibrillar structure and charge determine the interaction of polyglutamine protein aggregates with the cell surface. J Biol Chem 287 (2012), 29722–29728.
49. 49 Babcock, DT, Ganetzky, B, Transcellular spreading of huntingtin aggregates in the Drosophila brain. Proc Natl Acad Sci USA 112 (2015), E5427–E5433.
50. 50 Pearce, MM, Spartz, EJ, Hong, W, Luo, L, Kopito, RR, Prion-like transmission of neuronal huntingtin aggregates to phagocytic glia in the Drosophila brain. Nat Commun, 6, 2015, 6768.
51. 51 Jeon, I, Cicchetti, F, Cisbani, G, et al. Human-to-mouse prion-like propagation of mutant huntingtin protein. Acta Neuropathol 132 (2016), 577–592.
52. 52 Cicchetti, F, Lacroix, S, Cisbani, G, et al. Mutant huntingtin is present in neuronal grafts in Huntington disease patients. Ann Neurol 76 (2014), 31–42.
53. 53 Kanekiyo, T, Zhang, J, Liu, Q, Liu, CC, Zhang, L, Bu, G, Heparan sulphate proteoglycan and the low-density lipoprotein receptor-related protein 1 constitute major pathways for neuronal amyloid-beta uptake. J Neurosci 31 (2011), 1644–1651.
54. 54 Holmes, BB, DeVos, SL, Kfoury, N, et al. Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc Natl Acad Sci USA 110 (2013), e3138–e3147.
55. 55 Horonchik, L, Tzaban, S, Ben-Zaken, O, et al. Heparan sulfate is a cellular receptor for purified infectious prions. J Biol Chem 280 (2005), 17062–17067.
56. 56 Christianson, HC, Belting, M, Heparan sulfate proteoglycan as a cell-surface endocytosis receptor. Matrix Biol 35 (2014), 51–55.
57. 57 Calafate, S, Flavin, W, Verstreken, P, Moechars, D, Loss of Bin1 promotes the propagation of tau pathology. Cell Rep 17 (2016), 931–940.
58. 58 Mao, X, Ou, MT, Karuppagounder, SS, et al. Pathological α-synuclein transmission initiated by binding lymphocyte-activation gene 3. Science, 2016, 10.1126/science.aah3374 published online Sept 30.
59. 59 Salazar, SV, Strittmatter, SM, Cellular prion protein as a receptor for amyloid-β oligomers in Alzheimers disease. Biochem Biophys Res Commun, 2016, 10.1016/j.bbrc.2016.09.062 published online Sept 14.
60. 60 Freeman, D, Cedillos, R, Choyke, S, et al. Alpha-synuclein induces lysosomal rupture and cathepsin dependent reactive oxygen species following endocytosis. PLoS One, 8, 2013, e62143.
61. 61 Munch, C, O'Brien, J, Bertolotti, A, Prion-like propagation of mutant superoxide dismutase-1 misfolding in neuronal cells. Proc Natl Acad Sci USA 108 (2011), 3548–3553.
62. 62 Cai, X, Xu, H, Chen, ZJ, Prion-like polymerization in immunity and inflammation. Cold Spring Harb Perspect Biol, 2016, 10.1101/cshperspect.a023580 published online Nov 23.
63. 63 Si, K, Kandel, ER, The role of functional prion-like proteins in the persistence of memory. Cold Spring Harb Perspect Biol, 8, 2016, a021774.
64. 64 Pokrishevsky, E, Grad, LI, Cashman, NR, TDP-43 or FUS-induced misfolded human wild-type SOD1 can propagate intercellularly in a prion-like fashion. Sci Rep, 6, 2016, 22155.
65. 65 Ayers, JI, Fromholt, S, Koch, M, et al. Experimental transmissibility of mutant SOD1 motor neuron disease. Acta Neuropathol 128 (2014), 791–803.
66. 66 Magalhaes, AC, Baron, GS, Lee, KS, et al. Uptake and neuritic transport of scrapie prion protein coincident with infection of neuronal cells. J Neurosci 25 (2005), 5207–5216.
67. 67 Kanu, N, Imokawa, Y, Drechsel, DN, et al. Transfer of scrapie prion infectivity by cell contact in culture. Curr Biol 12 (2002), 523–530.
68. 68 Chandler, RL, Encephalopathy in mice produced by inoculation with scrapie brain material. Lancet 1 (1961), 1378–1379.
69. 69 Makarava, N, Kovacs, GG, Bocharova, O, et al. Recombinant prion protein induces a new transmissible prion disease in wild-type animals. Acta Neuropathol 119 (2010), 177–187.
70. 70 Bernoulli, C, Siegfried, J, Baumgartner, G, et al. Danger of accidental person-to-person transmission of Creutzfeldt-Jakob disease by surgery. Lancet 1 (1977), 478–479.
71. 71 Duffy, P, Wolf, J, Collins, G, DeVoe, AG, Streeten, B, Cowen, D, Letter: possible person-to-person transmission of Creutzfeldt-Jakob disease. N Engl J Med 290 (1974), 692–693.
72. 72 Kfoury, N, Holmes, BB, Jiang, H, Holtzman, DM, Diamond, MI, Trans-cellular propagation of Tau aggregation by fibrillar species. J Biol Chem 287 (2012), 19440–19451.
73. 73 Frost, B, Jacks, RL, Diamond, MI, Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 284 (2009), 12845–12852.
74. 74 Guo, JL, Lee, VM, Seeding of normal Tau by pathological Tau conformers drives pathogenesis of Alzheimer-like tangles. J Biol Chem 286 (2011), 15317–15331.
75. 75 Clavaguera, F, Bolmont, T, Crowther, RA, et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11 (2009), 909–913.
76. 76 de Calignon, A, Polydoro, M, Suarez-Calvet, M, et al. Propagation of tau pathology in a model of early Alzheimer's disease. Neuron 73 (2012), 685–697.
77. 77 Bahr, BA, Hoffman, KB, Yang, AJ, Hess, US, Glabe, CG, Lynch, G, Amyloid beta protein is internalized selectively by hippocampal field CA1 and causes neurons to accumulate amyloidogenic carboxyterminal fragments of the amyloid precursor protein. J Comp Neurol 397 (1998), 139–147.
78. 78 Nath, S, Agholme, L, Kurudenkandy, FR, Granseth, B, Marcusson, J, Hallbeck, M, Spreading of neurodegenerative pathology via neuron-to-neuron transmission of β-amyloid. J Neurosci 32 (2012), 8767–8777.
79. 79 Kane, MD, Lipinski, WJ, Callahan, MJ, et al. Evidence for seeding of beta-amyloid by intracerebral infusion of Alzheimer brain extracts in beta-amyloid precursor protein-transgenic mice. J Neurosci 20 (2000), 3606–3611.
80. 80 Meyer-Luehmann, M, Coomaraswamy, J, Bolmont, T, et al. Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science 313 (2006), 1781–1784.
81. 81 Wisniewski, T, Goni, F, Immunotherapeutic approaches for Alzheimer's disease. Neuron 85 (2015), 1162–1176.
82. 82 Orgogozo, JM, Gilman, S, Dartigues, JF, et al. Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization. Neurology 61 (2003), 46–54.
83. 83 Gerald, Z, Ockert, W, Alzheimer's disease market: hope deferred. Nat Rev Drug Discov 12 (2013), 19–20.
84. 84 Sevigny, J, Chiao, P, Bussiere, T, et al. The antibody aducanumab reduces Aβ plaques in Alzheimer's disease. Nature 537 (2016), 50–56.
85. 85 Bergstrom, AL, Kallunki, P, Fog, K, Development of passive immunotherapies for synucleinopathies. Mov Disord 31 (2016), 203–213.
86. 86 Mandler, M, Valera, E, Rockenstein, E, et al. Next-generation active immunization approach for synucleinopathies: implications for Parkinson's disease clinical trials. Acta Neuropathol 127 (2014), 861–879.
87. 87 Polymenidou, M, Stoeck, K, Glatzel, M, Vey, M, Bellon, A, Aguzzi, A, Coexistence of multiple PrPSc types in individuals with Creutzfeldt-Jakob disease. Lancet Neurol 4 (2005), 805–814.
88. 88 Seyhan, AA, RNAi: a potential new class of therapeutic for human genetic disease. Hum Genet 130 (2011), 583–605.
89. 89 DeVos, SL, Miller, TM, Antisense oligonucleotides: treating neurodegeneration at the level of RNA. Neurotherapeutics 10 (2013), 486–497.
90. 90 Pfeifer, A, Eigenbrod, S, Al-Khadra, S, et al. Lentivector-mediated RNAi efficiently suppresses prion protein and prolongs survival of scrapie-infected mice. J Clin Invest 116 (2006), 3204–3210.
91. 91 Smith, RA, Miller, TM, Yamanaka, K, et al. Antisense oligonucleotide therapy for neurodegenerative disease. J Clin Invest 116 (2006), 2290–2296.
92. 92 Miller, TM, Pestronk, A, David, W, et al. An antisense oligonucleotide against SOD1 delivered intrathecally for patients with SOD1 familial amyotrophic lateral sclerosis: a phase 1, randomised, first-in-man study. Lancet Neurol 12 (2013), 435–442.
93. 93 Jiang, J, Zhu, Q, Gendron, TF, et al. Gain of toxicity from ALS/FTD-linked repeat expansions in C9ORF72 is alleviated by antisense oligonucleotides targeting GGGGCC-containing RNAs. Neuron 90 (2016), 535–550.
94. 94 Lagier-Tourenne, C, Baughn, M, Rigo, F, et al. Targeted degradation of sense and antisense C9orf72 RNA foci as therapy for ALS and frontotemporal degeneration. Proc Natl Acad Sci USA 110 (2013), e4530–e4539.
95. 95 DeVos, SL, Miller, RL, Schoch, KM, et al. Tau reduction prevents neuronal loss and reverses pathological tau deposition and seeding in mice with tauopathy. Sci Transl Med, 2017, 10.1126/scitranslmed.aag0481 published online Jan 25.
96. 96 Crowe, A, James, MJ, Lee, VM, et al. Aminothienopyridazines and methylene blue affect Tau fibrillization via cysteine oxidation. J Biol Chem 288 (2013), 11024–11037.
97. 97 Gauthier, S, Feldman, HH, Schneider, LS, et al. Efficacy and safety of tau-aggregation inhibitor therapy in patients with mild or moderate Alzheimer's disease: a randomised, controlled, double-blind, parallel-arm, phase 3 trial. Lancet 388 (2016), 2873–2884.
98. 98 Cebers, G, Alexander, RC, Haeberlein, SB, et al. AZD3293: pharmacokinetic and pharmacodynamic effects in healthy subjects and patients with Alzheimer's Disease. J Alzheimers Dis 55 (2016), 1039–1053.
99. 99 Coelho, T, Maia, LF, Martins da Silva, A, et al. Tafamidis for transthyretin familial amyloid polyneuropathy: a randomized, controlled trial. Neurology 79 (2012), 785–792.
100. 100 Dealler, S, Rainov, NG, Pentosan polysulfate as a prophylactic and therapeutic agent against prion disease. IDrugs 6 (2003), 470–478.
101. 101 Doh-ura, K, Ishikawa, K, Murakami-Kubo, I, et al. Treatment of transmissible spongiform encephalopathy by intraventricular drug infusion in animal models. J Virol 78 (2004), 4999–5006.
102. 102 Tsuboi, Y, Doh-Ura, K, Yamada, T, Continuous intraventricular infusion of pentosan polysulfate: clinical trial against prion diseases. Neuropathology 29 (2009), 632–636.
103. 103 Beekes, M, Thomzig, A, Schulz-Schaeffer, WJ, Burger, R, Is there a risk of prion-like disease transmission by Alzheimer- or Parkinson-associated protein particles?. Acta Neuropathol 128 (2014), 463–476.