Unique properties of PTEN-L contribute to neuroprotection in response to ischemic-like stress

Sci Rep. 2019 Feb 28;9(1):3183. doi: 10.1038/s41598-019-39438-1.

Abstract

Phosphatase and tensin homolog (PTEN) signalling might influence neuronal survival after brain ischemia. However, the influence of the less studied longer variant termed PTEN-L (or PTENα) has not been studied to date. Therefore, we examined the translational variant PTEN-L in the context of neuronal survival. We identified PTEN-L by proteomics in murine neuronal cultures and brain lysates and established a novel model to analyse PTEN or PTEN-L variants independently in vitro while avoiding overexpression. We found that PTEN-L, unlike PTEN, localises predominantly in the cytosol and translocates to the nucleus 10-20 minutes after glutamate stress. Genomic ablation of PTEN and PTEN-L increased neuronal susceptibility to oxygen-glucose deprivation. This effect was rescued by expression of either PTEN-L indicating that both PTEN isoforms might contribute to a neuroprotective response. However, in direct comparison, PTEN-L replaced neurons were protected against ischemic-like stress compared to neurons expressing PTEN. Neurons expressing strictly nuclear PTEN-L NLS showed increased vulnerability, indicating that nuclear PTEN-L alone is not sufficient in protecting against stress. We identified mutually exclusive binding partners of PTEN-L or PTEN in cytosolic or nuclear fractions, which were regulated after ischemic-like stress. GRB2-associated-binding protein 2, which is known to interact with phosphoinositol-3-kinase, was enriched specifically with PTEN-L in the cytosol in proximity to the plasma membrane and their interaction was lost after glutamate exposure. The present study revealed that PTEN and PTEN-L have distinct functions in response to stress and might be involved in different mechanisms of neuroprotection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics*
  • Animals
  • Brain / metabolism*
  • Brain / pathology
  • Brain Ischemia / genetics*
  • Brain Ischemia / pathology
  • Cell Nucleus / genetics
  • Disease Models, Animal
  • GRB2 Adaptor Protein / genetics
  • Gene Expression Regulation / genetics
  • Glucose / metabolism
  • Humans
  • Mice
  • Neurons / metabolism
  • Neurons / pathology
  • Neuroprotection / genetics
  • Oxygen / metabolism
  • PTEN Phosphohydrolase / genetics*
  • Protein Isoforms / genetics
  • Proteomics / methods
  • Signal Transduction / genetics
  • Stroke / genetics*
  • Stroke / metabolism
  • Stroke / pathology

Substances

  • Adaptor Proteins, Signal Transducing
  • GRB2 Adaptor Protein
  • Gab2 protein, mouse
  • Grb2 protein, mouse
  • Protein Isoforms
  • PTEN Phosphohydrolase
  • Pten protein, mouse
  • Glucose
  • Oxygen

Associated data

  • figshare/10.6084/m9.figshare.c.4339814