Direct evidence of Parkinson pathology spread from the gastrointestinal tract to the brain in rats

Acta Neuropathologica

Volumn 128, Issue 6, 2014, Pages 805-820

  Holmqvist, Staffan ^a,b   Chutna, Oldriska ^a   Bousset, Luc ^c   Aldrin Kirk, Patrick ^a   Li, Wen ^a   Björklund, Tomas ^a   Wang, Zhan You ^d   Roybon, Laurent ^b   Melki, Ronald ^c   Li, Jia Yi ^a,d  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c CNRS   (France)

^d NORTHEASTERN UNIVERSITY   (China)

Author keywords

Alpha synuclein; Lewy body; Parkinson s disease; Protein aggregation; Protein propagation

Indexed keywords

ALPHA SYNUCLEIN; RECOMBINANT PROTEIN; SNCA PROTEIN, HUMAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CELL DIFFERENTIATION; CELL LYSATE; CONTROLLED STUDY; GASTROINTESTINAL TRACT; HUMAN; HUMAN CELL; IN VIVO STUDY; INTESTINE WALL; LEWY BODY; MEDULLA OBLONGATA; MOLECULAR WEIGHT; MOTONEURON NUCLEUS; NERVE FIBER TRANSPORT; NEUROBLASTOMA CELL LINE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RAT; VAGUS NERVE; ANIMAL; BRAIN; DISEASE COURSE; DISEASE MODEL; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT; TUMOR CELL LINE;

ALPHA-SYNUCLEIN; ANIMALS; AXONAL TRANSPORT; BRAIN; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GASTROINTESTINAL TRACT; HUMANS; PARKINSON DISEASE; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; VAGUS NERVE;

EID: 84922092995     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-014-1343-6     Document Type: Article

References (50)

1. Aguzzi A, Rajendran L (2009) The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64:783–790
2. Ahmad FJ, Echeverri CJ, Vallee RB, Baas PW (1998) Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. J Cell Biol 140:391–401
3. Axelrod D, Koppel DE, Schlessinger J, Elson E, Webb WW (1976) Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys J 16:1055–1069. doi:10.1016/S0006-3495(76)85755-4
4. Black MM, Lasek RJ (1979) Axonal transport of actin: slow component b is the principal source of actin for the axon. Brain Res 171:401–413
5. Braak H, de Vos RA, Bohl J, Del Tredici K (2006) Gastric alpha-synuclein immunoreactive inclusions in Meissner’s and Auerbach’s plexuses in cases staged for Parkinson’s disease-related brain pathology. Neurosci Lett 396:67–72
6. Braak H, Del Tredici K (2009) Neuroanatomy and pathology of sporadic Parkinson’s disease. Adv Anat Embryol Cell Biol 201:1–119
7. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211
8. Braak H, Ghebremedhin E, Rub U, Bratzke H, Del Tredici K (2004) Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res 318:121–134
9. Braak H, Rub U, Gai WP, Del Tredici K (2003) Idiopathic Parkinson’s disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J Neural Transm 110:517–536
10. Danzer KM, Haasen D, Karow AR, Moussaud S, Habeck M, Giese A, Kretzschmar H, Hengerer B, Kostka M (2007) Different species of alpha-synuclein oligomers induce calcium influx and seeding. J Neurosci 27:9220–9232
11. Desplats P, Lee HJ, Bae EJ, Patrick C, Rockenstein E, Crews L, Spencer B, Masliah E, Lee SJ (2009) Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha-synuclein. Proc Natl Acad Sci 106:13010–13015
12. Ellenberg J, Siggia ED, Moreira JE, Smith CL, Presley JF, Worman HJ, Lippincott-Schwartz J (1997) Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J Cell Biol 138:1193–1206
13. Freundt EC, Maynard N, Clancy EK, Roy S, Bousset L, Sourigues Y, Covert M, Melki R, Kirkegaard K, Brahic M (2012) Neuron-to-neuron transmission of alpha-synuclein fibrils through axonal transport. Ann Neurol 72:517–524. doi:10.1002/ana.23747
14. Ghee M, Melki R, Michot N, Mallet J (2005) PA700, the regulatory complex of the 26S proteasome, interferes with alpha-synuclein assembly. FEBS J 272:4023–4033
15. Hansen C, Angot E, Bergstrom AL, Steiner JA, Pieri L, Paul G, Outeiro TF, Melki R, Kallunki P, Fog K et al (2011) alpha-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J Clin Invest 121:715–725. doi:10.1172/JCI43366
16. Hardy J (2005) Expression of normal sequence pathogenic proteins for neurodegenerative disease contributes to disease risk: ‘permissive templating’ as a general mechanism underlying neurodegeneration. Biochem Soc Trans 33:578–581
17. Hawkes CH, Del Tredici K, Braak H (2009) Parkinson’s disease: the dual hit theory revisited. Ann N Y Acad Sci 1170:615–622
18. Jellinger KA (2008) A critical reappraisal of current staging of Lewy-related pathology in human brain. Acta Neuropathol 116:1–16
19. Jensen PH, Li JY, Dahlstrom A, Dotti CG (1999) Axonal transport of synucleins is mediated by all rate components. Eur J Neurosci 11:3369–3376
20. Jordan MA, Wilson L (2004) Microtubules as a target for anticancer drugs. Nat Rev Cancer 4:253–265. doi:10.1038/nrc1317
21. Kordower JH, Chu Y, Hauser RA, Freeman TB, Olanow CW (2008) Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson’s disease. Nat Med 14:504–506
22. Kordower JH, Chu Y, Hauser RA, Olanow CW, Freeman TB (2008) Transplanted dopaminergic neurons develop PD pathologic changes: a second case report. Mov Disord 23:2303–2306
23. Kurowska Z, Englund E, Widner H, Lindvall O, Li J-Y, Brundin P (2011) Signs of degeneration in 12–22 year old grafts of mesencephalic dopamine neurons in patients with Parkinson’s disease. J Parkinsons Dis 1:83–92. doi:10.3233/jpd-2011-11004
24. Lasek RJ, Garner JA, Brady ST (1984) Axonal transport of the cytoplasmic matrix. J Cell Biol 99:212–221
25. Lebouvier T, Chaumette T, Paillusson S, Duyckaerts C, Bruley des Varannes S, Neunlist M, Derkinderen P (2009) The second brain and Parkinson’s disease. Eur J Neurosci 30:735–741
26. Lee HJ, Suk JE, Lee KW, Park SH, Blumbergs PC, Gai WP, Lee SJ (2011) Transmission of synucleinopathies in the enteric nervous system of A53T alpha-synuclein transgenic mice. Exp Neurobiol 20:181–188. doi:10.5607/en.2011.20.4.181
27. Lee HJ, Suk JE, Patrick C, Bae EJ, Cho JH, Rho S, Hwang D, Masliah E, Lee SJ (2010) Direct transfer of alpha-synuclein from neuron to astroglia causes inflammatory responses in synucleinopathies. J Biol Chem 285:9262–9272
28. Lerner A, Bagic A (2008) Olfactory pathogenesis of idiopathic Parkinson disease revisited. Mov Disord 23:1076–1084
29. Li JY, Englund E, Holton JL, Soulet D, Hagell P, Lees AJ, Lashley T, Quinn NP, Rehncrona S, Bjorklund A et al (2008) Lewy bodies in grafted neurons in subjects with Parkinson’s disease suggest host-to-graft disease propagation. Nat Med 14:501–503. doi:10.1038/nm1746
30. Li JY, Englund E, Widner H, Rehncrona S, Bjorklund A, Lindvall O, Brundin P (2010) Characterization of Lewy body pathology in 12- and 16-year-old intrastriatal mesencephalic grafts surviving in a patient with Parkinson’s disease. Mov Disord 25:1091–1096. doi:10.1002/mds.23012
31. Luk KC, Kehm V, Carroll J, Zhang B, O’Brien P, Trojanowski JQ, Lee VM (2012) Pathological alpha-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science 338:949–953. doi:10.1126/science.1227157
32. Luk KC, Kehm VM, Zhang B, O’Brien P, Trojanowski JQ, Lee VM (2012) Intracerebral inoculation of pathological alpha-synuclein initiates a rapidly progressive neurodegenerative alpha-synucleinopathy in mice. J Exp Med 209:975–986. doi:10.1084/jem.20112457
33. Luk KC, Song C, O’Brien P, Stieber A, Branch JR, Brunden KR, Trojanowski JQ, Lee VM (2009) Exogenous {alpha}-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc Natl Acad Sci 106:20051–20056
34. Nonaka T, Watanabe ST, Iwatsubo T, Hasegawa M (2010) Seeded aggregation and toxicity of {alpha}-synuclein and tau: cellular models of neurodegenerative diseases. J Biol Chem 285:34885–34898. doi:10.1074/jbc.M110.148460
35. Outeiro TF, Putcha P, Tetzlaff JE, Spoelgen R, Koker M, Carvalho F, Hyman BT, McLean PJ (2008) Formation of toxic oligomeric alpha-synuclein species in living cells. PLoS One 3:e1867
36. Pan-Montojo F, Schwarz M, Winkler C, Arnhold M, O’Sullivan GA, Pal A, Said J, Marsico G, Verbavatz JM, Rodrigo-Angulo M et al (2012) Environmental toxins trigger PD-like progression via increased alpha-synuclein release from enteric neurons in mice. Sci Rep 2:898. doi:10.1038/srep00898
37. Parkkinen L, Kauppinen T, Pirttila T, Autere JM, Alafuzoff I (2005) Alpha-synuclein pathology does not predict extrapyramidal symptoms or dementia. Ann Neurol 57:82–91
38. Parkkinen L, Pirttila T, Alafuzoff I (2008) Applicability of current staging/categorization of alpha-synuclein pathology and their clinical relevance. Acta Neuropathol 115(4):399–407
39. Phair RD, Gorski SA, Misteli T (2004) Measurement of dynamic protein binding to chromatin in vivo, using photobleaching microscopy. Methods Enzymol 375:393–414
40. Phillips RJ, Walter GC, Wilder SL, Baronowsky EA, Powley TL (2008) Alpha-synuclein-immunopositive myenteric neurons and vagal preganglionic terminals: autonomic pathway implicated in Parkinson’s disease? Neuroscience 153:733–750
41. Prots I, Veber V, Brey S, Campioni S, Buder K, Riek R, Bohm KJ, Winner B (2013) alpha-Synuclein oligomers impair neuronal microtubule-kinesin interplay. J Biol Chem 288:21742–21754. doi:10.1074/jbc.M113.451815
42. Recasens A, Dehay B, Bove J, Carballo-Carbajal I, Dovero S, Perez-Villalba A, Fernagut PO, Blesa J, Parent A, Perier C et al (2014) Lewy body extracts from Parkinson disease brains trigger alpha-synuclein pathology and neurodegeneration in mice and monkeys. Ann Neurol 75:351–362. doi:10.1002/ana.24066
43. Rey NL, Petit GH, Bousset L, Melki R, Brundin P (2013) Transfer of human alpha-synuclein from the olfactory bulb to interconnected brain regions in mice. Acta Neuropathol 126:555–573. doi:10.1007/s00401-013-1160-3
44. Roy S, Winton MJ, Black MM, Trojanowski JQ, Lee VM (2008) Cytoskeletal requirements in axonal transport of slow component-b. J Neurosci 28:5248–5256
45. Roy S, Winton MJ, Black MM, Trojanowski JQ, Lee VM (2007) Rapid and intermittent cotransport of slow component-b proteins. J Neurosci 27:3131–3138
46. Scott DA, Das U, Tang Y, Roy S (2011) Mechanistic logic underlying the axonal transport of cytosolic proteins. Neuron 70:441–454. doi:10.1016/j.neuron.2011.03.022
47. Shea TB, Flanagan LA (2001) Kinesin, dynein and neurofilament transport. Trends Neurosci 24:644–648
48. Snapp EL, Altan N, Lippincott-Schwartz J (2003) Measuring protein mobility by photobleaching GFP chimeras in living cells. Curr Protoc Cell Biol. doi: 10.1002/0471143030.cb2101s19
49. Ulusoy A, Rusconi R, Perez-Revuelta BI, Musgrove RE, Helwig M, Winzen-Reichert B, Di Monte DA (2013) Caudo-rostral brain spreading of alpha-synuclein through vagal connections. EMBO Mol Med 5:1051–1059. doi:10.1002/emmm.201302475
50. Winner B, Jappelli R, Maji SK, Desplats PA, Boyer L, Aigner S, Hetzer C, Loher T, Vilar M, Campioni S et al (2011) In vivo demonstration that alpha-synuclein oligomers are toxic. Proc Natl Acad Sci 108:4194–4199. doi:10.1073/pnas.1100976108