Pathogenic PTPN11 variants involving the poly-glutamine Gln255 -Gln256 -Gln257 stretch highlight the relevance of helix B in SHP2's functional regulation

Hum Mutat. 2020 Jun;41(6):1171-1182. doi: 10.1002/humu.24007. Epub 2020 Mar 11.

Abstract

Germline PTPN11 mutations cause Noonan syndrome (NS), the most common disorder among RASopathies. PTPN11 encodes SHP2, a protein tyrosine-phosphatase controlling signaling through the RAS-MAPK and PI3K-AKT pathways. Generally, NS-causing PTPN11 mutations are missense changes destabilizing the inactive conformation of the protein or enhancing its binding to signaling partners. Here, we report on two PTPN11 variants resulting in the deletion or duplication of one of three adjacent glutamine residues (Gln255 -to-Gln257 ). While p.(Gln257dup) caused a typical NS phenotype in carriers of a first family, p.(Gln257del) had incomplete penetrance in a second family. Missense mutations involving Gln256 had previously been reported in NS. This poly-glutamine stretch is located on helix B of the PTP domain, a region involved in stabilizing SHP2 in its autoinhibited state. Molecular dynamics simulations predicted that changes affecting this motif perturb the SHP2's catalytically inactive conformation and/or substrate recognition. Biochemical data showed that duplication and deletion of Gln257 variably enhance SHP2's catalytic activity, while missense changes involving Gln256 affect substrate specificity. Expression of mutants in HEK293T cells documented their activating role on MAPK signaling, uncoupling catalytic activity and modulation of intracellular signaling. These findings further document the relevance of helix B in the regulation of SHP2's function.

Keywords: ERK phosphorylation studies; Noonan syndrome; PTPN11; SHP2; in vitro phosphatase assay; molecular dynamics simulations.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Child
  • Child, Preschool
  • Female
  • Glutamine / genetics
  • HEK293 Cells
  • Humans
  • Infant
  • Male
  • Middle Aged
  • Noonan Syndrome / genetics*
  • Peptides / genetics*
  • Protein Domains
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / genetics*
  • Signal Transduction

Substances

  • Peptides
  • Glutamine
  • polyglutamine
  • PTPN11 protein, human
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11