Different biochemical properties explain why two equivalent Gα subunit mutants cause unrelated diseases

J Biol Chem. 2014 Aug 8;289(32):21818-27. doi: 10.1074/jbc.M114.549790. Epub 2014 Jun 30.

Abstract

There is an increasing number of disease-associated Gα mutations identified from genome-wide sequencing campaigns or targeted efforts. Albright's Hereditary Osteodystrophy (AHO) was the first inherited disease associated with loss-of-function mutations in a G protein (Gαs) and other studies revealed gain-of-function Gα mutations in cancer. Here we attempted to solve the apparent quandary posed by the fact that the same mutation in two different G proteins appeared associated with both AHO and cancer. We first confirmed the presence of an inherited Gαs-R265H mutation from a previously described clinical case report of AHO. This mutation is structurally analogous to Gαo-R243H, an oncogenic mutant with increased activity in vitro and in cells due to rapid nucleotide exchange. We found that, contrary to Gαo-R243H, Gαs-R265H activity is compromised due to greatly impaired nucleotide binding in vitro and in cells. We obtained equivalent results when comparing another AHO mutation in Gαs (D173N) with a counterpart cancer mutation in Gαo (D151N). Gαo-R243H binds nucleotides efficiently under steady-state conditions but releases GDP much faster than the WT protein, suggesting diminished affinity for the nucleotide. These results indicate that the same disease-linked mutation in two different G proteins affects a common biochemical feature (nucleotide affinity) but to a different grade depending on the G protein (mild decrease for Gαo and severe for Gαs). We conclude that Gαs-R265H has dramatically impaired nucleotide affinity leading to the loss-of-function in AHO whereas Gαo-R243H has a mild decrease in nucleotide affinity that causes rapid nucleotide turnover and subsequent hyperactivity in cancer.

Keywords: Albright's Hereditary Osteodystrophy; Cancer; Enzyme Kinetics; G Protein-coupled receptor (GPCR); Heterotrimeric G Protein; Oncogene; Pseudohypoparathyroidism Ia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Amino Acid Substitution
  • Chromogranins
  • Female
  • GTP-Binding Protein alpha Subunits, Gi-Go / chemistry*
  • GTP-Binding Protein alpha Subunits, Gi-Go / genetics
  • GTP-Binding Protein alpha Subunits, Gi-Go / metabolism*
  • GTP-Binding Protein alpha Subunits, Gs / chemistry*
  • GTP-Binding Protein alpha Subunits, Gs / genetics
  • GTP-Binding Protein alpha Subunits, Gs / metabolism*
  • Guanosine Triphosphate / metabolism
  • HEK293 Cells
  • Humans
  • Male
  • Models, Molecular
  • Molecular Sequence Data
  • Mutant Proteins / chemistry*
  • Mutant Proteins / genetics
  • Mutant Proteins / metabolism*
  • Mutation*
  • Neoplasms / genetics*
  • Neoplasms / metabolism*
  • Pedigree
  • Protein Subunits
  • Pseudohypoparathyroidism / genetics*
  • Pseudohypoparathyroidism / metabolism*
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Sequence Homology, Amino Acid
  • Structural Homology, Protein

Substances

  • Chromogranins
  • GNAO1 protein, human
  • Mutant Proteins
  • Protein Subunits
  • Recombinant Proteins
  • Guanosine Triphosphate
  • GNAS protein, human
  • GTP-Binding Protein alpha Subunits, Gi-Go
  • GTP-Binding Protein alpha Subunits, Gs