Macromolecular crowding in the Escherichia coli periplasm maintains alpha-synuclein disorder

J Mol Biol. 2006 Feb 3;355(5):893-7. doi: 10.1016/j.jmb.2005.11.033. Epub 2005 Dec 1.

Abstract

The natively disordered protein alpha-synuclein is the primary component of Lewy bodies, the cellular hallmark of Parkinson's disease. Most studies of this protein are performed in dilute solution, but its biologically relevant role is performed in the crowded environment inside cells. We addressed the effects of macromolecular crowding on alpha-synuclein by combining NMR data acquired in living Escherichia coli with in vitro NMR data. The crowded environment in the E.coli periplasm prevents a conformational change that is detected at 35 degrees C in dilute solution. This change is associated with an increase in hydrodynamic radius and the formation of secondary structure in the N-terminal 100 amino acid residues. By preventing this temperature-induced conformational change, crowding in the E.coli periplasm stabilizes the disordered monomer. We obtain the same stabilization in vitro upon crowding alpha-synuclein with 300 g/l of bovine serum albumin, indicating that crowding alone is sufficient to stabilize the disordered, monomeric protein. Two disease-associated variants (A30P and A53T) behave in the same way in both dilute solution and in the E.coli periplasm. These data reveal the importance of approaching the effects of macromolecular crowding on a case-by-case basis. Additionally, our work shows that discrete structured protein conformations may not be achieved by alpha-synuclein inside cells, implicating the commonly overlooked aspect of macromolecular crowding as a possible factor in the etiology of Parkinson's disease.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Aged
  • Animals
  • Cattle
  • Escherichia coli Proteins / chemistry*
  • Escherichia coli Proteins / metabolism
  • Escherichia coli* / chemistry
  • Escherichia coli* / cytology
  • Humans
  • Nuclear Magnetic Resonance, Biomolecular
  • Periplasm / chemistry*
  • Protein Conformation*
  • alpha-Synuclein / chemistry*
  • alpha-Synuclein / metabolism

Substances

  • Escherichia coli Proteins
  • alpha-Synuclein