Formation and development of Lewy pathology: a critical update

J Neurol. 2009 Aug:256 Suppl 3:270-9. doi: 10.1007/s00415-009-5243-y.

Abstract

Filamentous protein inclusions in neurons (Lewy bodies, LB) and dystrophic neurites containing pathologic alpha-synuclein (alpha Syn) are the morphologic hallmarks of sporadic Parkinson disease (PD) and dementia with Lewy bodies (DLB), but are also found in aged subjects and in a variety of neurogenerative disorders. They occur in the central, peripheral, and autonomic nervous system as an essential or coincident feature. Their formation runs through several phases from initial dust-like particles cross-linked with alpha Syn to aggregation of ubiquitinated dense filaments, formation of LBs, finally degradation and death of the afflicted neurons. Pathologic accumulation of alpha Syn/LBs proposed by Braak et al. (Neurobiol Aging 24:197-211, 2003), following a predictable sequence of lesions in six stages with ascending progression from medullary and olfactory nuclei to the cortex, has been considered to be linked to clinical dysfunctions. The consensus pathologic guidelines of DLB (Neurology 65:1863-1872, 2005), by semiquantitative scoring to alpha Syn pathology (LB density and distribution) in specific brain regions, distinguish three phenotypes (brainstem, transitional/limbic, and diffuse neocortical), and also consider concomitant Alzheimer-related pathology. alpha Syn pathology in the amygdala is often associated with Alzheimer disease. Although some retrospective clinico-pathologic studies have largely confirmed the Braak LB staging system, it shows neither correlation to the clinical severity and duration of parkinsonism nor to nigral alpha Syn burden and cell loss which significantly correlates with resulting striatal loss of dopamine, dopamine transporter and tyrosine hydroxylase, duration and severity of motor dysfunction. Between 6.3 and 43% of clinically manifested PD cases did not follow this pattern, and in 7-8.3% of those with alpha Syn-positive inclusions in midbrain and cortex the medullary nuclei were spared. On the other hand, 30-55% of elderly subjects with widespread Lewy pathology revealed no neuropsychiatric symptoms or were not classifiable. Therefore, detection and staging of Lewy pathology without assessment of neuronal loss in specific areas may not have clinical impact and its predictive validity is questionable. For demented patients, modified criteria for categorization of Lewy pathology were proposed. If robust correlations between clinical course and Lewy/alpha Syn pathology are to be confirmed by future studies, the currently used morphologic staging/classification systems should be revised accordingly.

Publication types

  • Review

MeSH terms

  • Biomarkers / analysis
  • Biomarkers / metabolism
  • Brain / metabolism
  • Brain / pathology*
  • Brain / physiopathology
  • Disease Progression
  • Humans
  • Lewy Bodies / metabolism
  • Lewy Bodies / pathology
  • Lewy Body Disease / metabolism
  • Lewy Body Disease / pathology*
  • Lewy Body Disease / physiopathology
  • Neurons / metabolism
  • Neurons / pathology
  • Parkinson Disease / metabolism
  • Parkinson Disease / pathology*
  • Parkinson Disease / physiopathology
  • alpha-Synuclein / analysis
  • alpha-Synuclein / metabolism

Substances

  • Biomarkers
  • alpha-Synuclein