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01-04-2008 | Editorial

A not entirely benign procedure: progression of Parkinson’s disease

Authors: Kelly Del Tredici, Heiko Braak

Published in: Acta Neuropathologica | Issue 4/2008

Excerpt

During the last 5 years, the definition and understanding of the synucleinopathy Parkinson’s disease (PD) have been very much in flux, not the least owing to novel findings and new hypotheses in the field of neuropathology and contributions from other disciplines. Although it is generally accepted that the clinical phenotype in idiopathic Parkinson’s disease is primarily a motor one (parkinsonism), a consensus regarding the pathogenesis and pathological process(es) that underlie(s) the syndrome is only just beginning to emerge [1]. All of the articles in this April issue of Acta Neuropathologica reflect this status nascendi in research with a focus on one or more aspects of the pathology (α-synuclein inclusions, Lewy neurites/bodies) or pathologies (e.g., Alzheimer’s disease-related lesions, cerebral amyloid angiopathy) in Lewy body disease. …

Litvan I, Halliday G, Hallet M, Goetz CG, Rocca W, Duyckaerts Ch, Ben-Shlomo Y, Dickson DW, Lang AE, Chesselet M-F, Langston WJ, DiMonte DA, Gasser T, Hagg T, Hardy J, Jenner P, Melamed E, Myers RH, Parker D, Price DL (2007) The etiopathogenesis of Parkinson disease and suggestions for future research. Part I. J Neuropathol Exp Neurol 66:251–257PubMed

Jellinger K, Attems J (2008) Prevalence and impact of vascular and Alzheimer pathologies in Lewy body disease. Acta Neuropathol. doi:10.1007/s00401-008-0347-5

Lashley T, Holton JL, Gray E, Kirkham K, O’Sullivan SS, Hilbig A, Wood NW, Lees AJ, Revesz T (2008) Cortical α-synuclein load is associated with amyloid-βplaque burden in a subset of Parkinson’s disease patients. Acta Neuropathol. doi:10.1007/s00401-007-0336-0

Braak H, Del Tredici K, Rüb U, de Vos RAI, Jansen Steur ENH, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211PubMedCrossRef

McKeith IG, Dickson DW, Lowe J, Emre E, O’Brien JT, Feldman H, Cummings J, Duda JE, Lippa C, Perry EK, Aarsland D, Arai H, Ballard CG, Boeve B, Burn DJ, Costa D, Del Ser T, Dubois B, Galasko D, Gauthier S, Goetz CG, Gómez-Tortosa E, Halliday G, Hansen LA, Hardy J, Iwatsubo T, Kalaria RN, Kaufer D, Korczyn A, Kosaka K, Lee VM-Y, Lees A, Litvan I, Londos E, Lopez OL, Minoshima S, Mizuno Y, Molina JA, Mukaetova-Ladinska EB, Pasquier F, Perry RH, Schulz JB, Trojanowski JQ, Yamada M (2005) Diagnosis and management of dementia with Lewy bodies: Third report of the DLB consortium. Neurology 65:1863–1872PubMedCrossRef

Halliday G, Hely M, Reid W, Morris J (2008) The progression of pathology in longitudinally followed patients with Parkinson’s disease. Acta Neuropathol. doi:10.1007/s00401-008-0344-8

Mori F, Tanji K, Zhang H, Kakita A, Takahashi H, Wakabayashi K (2008) α-Synuclein pathology in the neostriatum in Parkinson’s disease. Acta Neuropathol. doi:10.1007/s00401-007-0316-4

Forno L (1969) Concentric hyalin intraneuronal inclusions of Lewy type in the brains of elderly persons (50 incidental cases): relationship to parkinsonism. J Am Geriatr Soc 17:557–575PubMed

Wakabayashi K, Takahashi H, Ohama E, Takeda S, Ikuta F (1991) Lewy bodies in the visceral autonomic nervous system in Parkinson’s disease. Adv Neurol 60:609–612

10.

Bloch A, Probst A, Bissig H, Adams H, Tolnay M (2006) Synuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects. Neuropathol Appl Neurol 12:284–295CrossRef

11.

Dickson DW, Fujishiro H, DelleDonne A, Menke J, Zeshan A, Klos KJ, Josephs KA, Frigerio R, Burnett M, Parisi JE, Ahlskog JE (2008) Evidence that incidental Lewy body disease is presymptomatic Parkinson’s disease. Acta Neuropathol. doi:10.1007/s00401-008-0345-7

12.

Uchihara T, Paulus W (2008) Research into neurodegenerative disease: an entangled web of mice and men. Acta Neuropathol 115:1–4PubMedCrossRef

13.

Beach TG, Adler CH, Sue LI, Peirce JB, Bachalakuri J, Dalsing-Hernandez JE, Lue LF, Caviness JN, Connor DJ, Sabbagh MN, Walker DG (2008) Reduced striatal tyrosine hydroxylase in incidental Lewy body disease. Acta Neuropathol. doi:10.1007/s00401-007-0313-7

14.

Parkkinen L, Pirttilä T, Alafuzoff I (2008) Applicability of current staging systems of α-synuclein pathology and their clinical relevance. Acta Neuropathol (in press)

15.

Halliday GM, McCann H (2008) Human-based studies on a-synuclein deposition and relationship to Parkinson’s disease symptoms. Exp Neurol 209:12–21PubMedCrossRef

16.

Braak H, Müller CM, Rüb U, Ackermann H, Bratzke H, de Vos RAI, Del Tredici K (2006) Pathology associated with sporadic Parkinson’s disease – where does it end? J Neural Trans Suppl 70:89–97CrossRef

17.

Duda JE, Noorigian JV, Petrovitch H, White LR, Ross GW (2007) Pattern of Lewy pathology progression suggested by Braak staging system is supported by analysis of a population-based cohort of patients. The Movement Disorders Society’s 11th international congress late breaking abstracts, A3

18.

Pandey N, Strider J, Nolan WC, Yan SX, Galvin JE (2008) Curcumin inhibits aggregation of a-synuclein. Acta Neuropathol. doi:10.1007/s00401-007-0332-4

19.

Van Den Eeden SK, Tanner CM, Berstein AL, Fross RD, Leimpeter A, Bloch DA, Nelson LM (2003) Incidence of Parkinson’s disease: variation by age, gender, and race/ethnicity. Am J Epidemiol 157:1015–1022CrossRef

20.

Minguez-Castellanos A, Chamorro CE, Escamilla-Sevilla F, Ortega-Moreno A, Rebollo AC, Gomez-Rio M, Concha A, Munoz DG (2007). Do α-synuclein aggregates in autonomic plexuses predate Lewy body disorders? A cohort study. Neurology 68:2012–2018PubMedCrossRef

21.

McNaught KS, Perl DP, Brownell AL, Olanow CW (2004) Systemic exposure to proteasome inhibitors causes a progressive model of Parkinson’s disease. Ann Neurol 56:149–162PubMedCrossRef

22.

Beal F, Lang A (2006). The proteasomal inhibition model of Parkinson’s disease: “boon or bust”? Ann Neurol 60:158–161PubMedCrossRef

23.

Tofaris GK, Reitböck PG, Humby T, Lambourne SL, O’Connell M, Ghetti B, Gossage H, Emson PC, Wilkinson LS, Goedert M, Spillantini MG (2006) Pathological changes in dopaminergic nerve cells of the substantia nigra and olfactory bulb in mice transgenic for truncated human α-synuclein (1–120): implications for Lewy body disorders. J Neurosci 26:3942–3950PubMedCrossRef

24.

Fleming SM, Fernagut P-O, Chesselet M-F (2005) Genetic mouse models of parkinsonism: strengths and limitations. NeuroRx 2:495–503PubMedCrossRef

25.

Ulusoy A, Bjorklund T, Hermening S, Kirik D (2008) In vivo gene delivery for development of mammalian models for Parkinson’s disease. Exp Neurol 209:89–100PubMedCrossRef

26.

Meredith G, Sonsalla P, Chesselet M-F (2008) Animal models of Parkinson’s disease progression. Acta Neuropathol. doi:10.1007/s00401-008-0350-x

27.

Phillips RJ, Powley TL (2007) Innervation of the gastrointestinal tract: patterns in aging. Auton Neurosci 136:1–19PubMedCrossRef

28.

Miwa H, Kubo T, Suzuki A, Kondo T (2006) Intragastric proteasome inhibition induces alpha-synuclein-immunopositive aggregations in neurons in the dorsal motor nucleus of the vagus in rats. Neurosci Lett 401:46–149CrossRef

29.

Phillips RJ, Powley T (2008) Alpha-synuclein-immunopositive myenteric neurons and vagal preganglionic terminals: Autonomic pathway implicated in Parkinson’s disease? Neuroscience (in press)

30.

Moran LB, Hickey L, Michael GJ, Derkacs M, Christian LM, Kalaitzakis ME, Pearce RKB, Graeber M (2008) Neuronal pentraxin II is highly upregulated in Parkinson’s disease and a novel component of Lewy bodies. Acta Neuropathol. doi:10.2007/s00401-007-0309-3

31.

Thannickal TC, Lai Y-Y, Siegel JM (2007) Hypocretin (orexin) cell loss in Parkinson’s disease. Brain 130:1586–1595PubMedCrossRef

32.

Wakabayashi K, Tanji K, Mori F, Takahashi H (2007) The Lewy body in Parkinson’s disease: molecules implicated in the formation and degradation of alpha-synuclein aggregates. Neuropathol 27:494–506CrossRef

33.

Wakabayashi K, Takahashi H, Obata K, Ikuta F (1992) Immunocytochemical localization of synaptic vesicle-specific protein in Lewy body-containing neurons in Parkinson’s disease. Neurosci Lett 138:237–240PubMedCrossRef

34.

Orimo S, Amino T, Itoh Y, Takahashi A, Kojo T, Uchihara T, Tsuchiya K, Mori F, Wakabayashi K, Takahashi H (2005) Cardiac sympathetic denervation precedes neuronal loss in the sympathetic ganglia in Lewy body disease. Acta Neuropathol 109:583–588PubMedCrossRef

35.

Braak H, Sandmann-Keil D, Gai W, Braak E (1999) Extensive axonal Lewy neurites in Parkinson’s disease: a novel pathological feature revealed by alpha-synuclein immunocytochemistry. Neurosci Lett 265:67–69PubMedCrossRef

36.

Duda JE, Giasson BI, Mahon ME, Lee VM, Trojanowski JQ (2002) Novel antibodies to synuclein show abundant striatal pathology in Lewy body diseases. Ann Neurol 52:205–210PubMedCrossRef

37.

Duda JE (2004) Pathology and neurostransmitter abnormalities of dementia with Lewy bodies. Dement Geriatr Cogn Disord 17(Suppl 1):3–14PubMedCrossRef

38.

Saha AR, Hill J, Utton MA, Asuni AA, Ackerley S, Grierson AJ, Miller CC, Davies AL, Buchman VL, Anderton BH, Hanger DP (2003) Parkinson’s disease α-synuclein mutations exhibit defective axonal transport in cultured neurons. J Cell Sci 117:1017–1024CrossRef

39.

Braak H, Bohl JR, Müller CM, Rüb U, de Vos RAI, Del Tredici K (2006). Stanley Fahn Lecture 2005: the staging procedure for the inclusion body pathology associated with sporadic Parkinson’s disease reconsidered. Mov Disord 21: 2042–2051PubMedCrossRef

Title: A not entirely benign procedure: progression of Parkinson’s disease
Authors: Kelly Del Tredici
Heiko Braak
Publication date: 01-04-2008
Publisher: Springer-Verlag
Published in: Acta Neuropathologica / Issue 4/2008
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI: https://doi.org/10.1007/s00401-008-0355-5

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A not entirely benign procedure: progression of Parkinson’s disease

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Other articles of this Issue 4/2008

Applicability of current staging/categorization of α-synuclein pathology and their clinical relevance

Neuronal pentraxin II is highly upregulated in Parkinson’s disease and a novel component of Lewy bodies

Prevalence and impact of vascular and Alzheimer pathologies in Lewy body disease

The progression of pathology in longitudinally followed patients with Parkinson’s disease

Animal models of Parkinson’s disease progression

Evidence that incidental Lewy body disease is pre-symptomatic Parkinson’s disease