Brain region-specific susceptibility of Lewy body pathology in synucleinopathies is governed by α-synuclein conformations

Acta Neuropathol. 2022 Apr;143(4):453-469. doi: 10.1007/s00401-022-02406-7. Epub 2022 Feb 9.

Abstract

The protein α-synuclein, a key player in Parkinson's disease (PD) and other synucleinopathies, exists in different physiological conformations: cytosolic unfolded aggregation-prone monomers and helical aggregation-resistant multimers. It has been shown that familial PD-associated missense mutations within the α-synuclein gene destabilize the conformer equilibrium of physiologic α-synuclein in favor of unfolded monomers. Here, we characterized the relative levels of unfolded and helical forms of cytosolic α-synuclein in post-mortem human brain tissue and showed that the equilibrium of α-synuclein conformations is destabilized in sporadic PD and DLB patients. This disturbed equilibrium is decreased in a brain region-specific manner in patient samples pointing toward a possible "prion-like" propagation of the underlying pathology and forms distinct disease-specific patterns in the two different synucleinopathies. We are also able to show that a destabilization of multimers mechanistically leads to increased levels of insoluble, pathological α-synuclein, while pharmacological stabilization of multimers leads to a "prion-like" aggregation resistance. Together, our findings suggest that these disease-specific patterns of α-synuclein multimer destabilization in sporadic PD and DLB are caused by both regional neuronal vulnerability and "prion-like" aggregation transmission enabled by the destabilization of local endogenous α-synuclein protein.

Keywords: Aggregation; Aggregation transmission; DLB; Multimers; PD; α-Synuclein.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Brain / pathology
  • Humans
  • Lewy Bodies / pathology
  • Lewy Body Disease* / pathology
  • Parkinson Disease* / pathology
  • Prions* / metabolism
  • Synucleinopathies*
  • alpha-Synuclein / metabolism

Substances

  • Prions
  • SNCA protein, human
  • alpha-Synuclein