Methionine sulfoxide reductase A (MsrA) restores alpha-crystallin chaperone activity lost upon methionine oxidation

Biochim Biophys Acta. 2009 Dec;1790(12):1665-72. doi: 10.1016/j.bbagen.2009.08.011. Epub 2009 Sep 3.

Abstract

Background: Lens cataract is associated with protein oxidation and aggregation. Two proteins that cause cataract when deleted from the lens are methionine sulfoxide reductase A (MsrA) that repairs protein methionine sulfoxide (PMSO) oxidized proteins and alpha-crystallin which is a two-subunit (alphaA and alphaB) chaperone. Here, we tested whether PMSO formation damages alpha-crystallin chaperone function and whether MsrA could repair PMSO-alpha-crystallin.

Methods: Total alpha-crystallin was oxidized to PMSO and evaluated by CNBr-cleavage and mass spectrometry. Chaperone activity was measured by light scattering using lysozyme as target. PMSO-alpha-crystallin was treated with MsrA, and repair was assessed by CNBr cleavage, mass spectrometry and recovery of chaperone function. The levels of alpha-crystallin-PMSO in the lenses of MsrA-knockout relative to wild-type mice were determined.

Results: PMSO oxidation of total alpha-crystallin (met 138 of alphaA and met 68 of alphaB) resulted in loss of alpha-crystallin chaperone activity. MsrA treatment of PMSO-alpha-crystallin repaired its chaperone activity through reduction of PMSO. Deletion of MsrA in mice resulted in increased levels of PMSO-alpha-crystallin.

Conclusions: Methionine oxidation damages alpha-crystallin chaperone function and MsrA can repair PMSO-alpha-crystallin restoring its chaperone function. MsrA is required for maintaining the reduced state of alpha-crystallin methionines in the lens.

Significance: Methionine oxidation of alpha-crystallin in combination with loss of MsrA repair causes loss of alpha-crystallin chaperone function. Since increased PMSO levels and loss of alpha-crystallin function are hallmarks of cataract, these results provide insight into the mechanisms of cataract development and likely those of other age-related diseases.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cells, Cultured
  • Humans
  • Lens, Crystalline / metabolism
  • Methionine / chemistry
  • Methionine / metabolism*
  • Methionine Sulfoxide Reductases
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Models, Biological
  • Molecular Chaperones / metabolism
  • Molecular Chaperones / physiology*
  • Oxidation-Reduction
  • Oxidoreductases / genetics
  • Oxidoreductases / metabolism
  • Oxidoreductases / physiology*
  • Protein Binding
  • Spectrometry, Mass, Electrospray Ionization
  • alpha-Crystallins / chemistry
  • alpha-Crystallins / metabolism
  • alpha-Crystallins / physiology*

Substances

  • Molecular Chaperones
  • alpha-Crystallins
  • Methionine
  • Oxidoreductases
  • Methionine Sulfoxide Reductases
  • methionine sulfoxide reductase