Localizing the chaperone activity of erythroid spectrin

Cytoskeleton (Hoboken). 2019 Jun;76(6):383-397. doi: 10.1002/cm.21556. Epub 2019 Aug 19.

Abstract

Spectrin, the major protein of the erythrocyte membrane skeleton has canonically been thought to only serve a structural function. We have previously described a novel chaperone-like property of spectrin and also hypothesized that the chaperone activity and binding of a hydrophobic ligand, Prodan are localized in the self-association domain. Here we probe the location and molecular origin of the chaperone activity of multi-domain spectrin using a selection of individual recombinant spectrin domains, which we have characterized using intrinsic tryptophan fluorescence and CD spectroscopy to show their identity to native spectrin. Aggregation assays using insulin, ADH, α- and β-globin as well as enzyme refolding assays using alkaline phosphatase and α-glucosidase show that the chaperone activity is not only localized in the self-association domain but is a generalized property of spectrin domains. This is to our understanding, a unique feature in the case of modular multi-repeat proteins, possibly implicating that the large family of "spectrin-repeat" domain containing proteins may also have chaperone like property. Substrate selectivity of chaperone activity as evidenced by the preferential protection of α- over β-globin chains is seen; which has implications in hemoglobin diseases. Moreover, enzyme-refolding assays also indicate alternate modes of chaperone action. We propose that the molecular origin of chaperone activity resides in the surface exposed hydrophobic patches of the spectrin domains as shown by ANS (1-anilinonaphthalene-8-sulfonic acid) and Prodan (6-propionyl-2[dimethylamino]-naphthalene) binding. We also show that Prodan does indeed have a unique binding site on spectrin located at the self-association domain.

Keywords: ANS; Prodan; chaperone; chaperone-substrate; spectrin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkaline Phosphatase / metabolism
  • Anisotropy
  • Erythrocytes / metabolism*
  • Fluorescent Dyes / metabolism
  • Humans
  • Ligands
  • Molecular Chaperones / metabolism*
  • Protein Binding
  • Protein Domains
  • Spectrin / chemistry
  • Spectrin / metabolism*
  • Spectrometry, Fluorescence
  • alpha-Glucosidases / metabolism

Substances

  • Fluorescent Dyes
  • Ligands
  • Molecular Chaperones
  • Spectrin
  • Alkaline Phosphatase
  • alpha-Glucosidases