Misregulation of human sortilin splicing leads to the generation of a nonfunctional progranulin receptor

Proc Natl Acad Sci U S A. 2012 Dec 26;109(52):21510-5. doi: 10.1073/pnas.1211577110. Epub 2012 Dec 10.

Abstract

Sortilin 1 regulates the levels of brain progranulin (PGRN), a neurotrophic growth factor that, when deficient, is linked to cases of frontotemporal lobar degeneration with TAR DNA-binding protein-43 (TDP-43)-positive inclusions (FTLD-TDP). We identified a specific splicing enhancer element that regulates the inclusion of a sortilin exon cassette (termed Ex17b) not normally present in the mature sortilin mRNA. This enhancer element is consistently present in sortilin RNA of mice and other species but absent in primates, which carry a premature stop codon within the Ex17b sequence. In the absence of TDP-43, which acts as a regulatory inhibitor, Ex17b is included in the sortilin mRNA. In humans, in contrast to mice, the inclusion of Ex17b in sortilin mRNA generates a truncated, nonfunctional, extracellularly released protein that binds to but does not internalize PGRN, essentially acting as a decoy receptor. Based on these results, we propose a potential mechanism linking misregulation of sortilin splicing with altered PGRN metabolism.

Publication types

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

MeSH terms

  • Adaptor Proteins, Vesicular Transport / genetics*
  • Adaptor Proteins, Vesicular Transport / metabolism
  • Amino Acid Motifs
  • Animals
  • Base Sequence
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / metabolism
  • Down-Regulation
  • Endocytosis
  • Enhancer Elements, Genetic / genetics
  • Exons / genetics
  • Glycine / metabolism
  • Humans
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Mice
  • Models, Biological
  • Molecular Sequence Data
  • Progranulins
  • Protein Binding
  • Protein Biosynthesis
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • Protein Structure, Tertiary
  • RNA Splicing / genetics*
  • Structure-Activity Relationship

Substances

  • Adaptor Proteins, Vesicular Transport
  • DNA-Binding Proteins
  • GRN protein, human
  • Intercellular Signaling Peptides and Proteins
  • Progranulins
  • Protein Isoforms
  • Glycine
  • sortilin