Protein tyrosine phosphatase receptor type O serves as a key regulator of insulin resistance-induced α-synuclein aggregation in Parkinson's disease

Cell Mol Life Sci. 2024 Sep 14;81(1):403. doi: 10.1007/s00018-024-05436-4.

Abstract

Insulin resistance (IR) was found to be a critical element in the pathogenesis of Parkinson's disease (PD), facilitating abnormal α-synuclein (α-Syn) aggregation in neurons and thus promoting PD development. However, how IR contributes to abnormal α-Syn aggregation remains ill-defined. Here, we analyzed six PD postmortem brain transcriptome datasets to reveal module genes implicated in IR-mediated α-Syn aggregation. In addition, we induced IR in cultured dopaminergic (DA) neurons overexpressing α-Syn to identify IR-modulated differentially expressed genes (DEGs). Integrated analysis of data from PD patients and cultured neurons revealed 226 genes involved in α-Syn aggregation under IR conditions, of which 53 exhibited differential expression between PD patients and controls. Subsequently, we conducted an integrated analysis of the 53 IR-modulated genes employing transcriptome data from PD patients with different Braak stages and DA neuron subclasses with varying α-Syn aggregation scores. Protein tyrosine phosphatase receptor type O (PTPRO) was identified to be closely associated with PD progression and α-Syn aggregation. Experimental validation in a cultured PD cell model confirmed that both mRNA and protein of PTPRO were reduced under IR conditions, and the downregulation of PTPRO significantly facilitated α-Syn aggregation and cell death. Collectively, our findings identified PTPRO as a key regulator in IR-mediated α-Syn aggregation and uncovered its prospective utility as a therapeutic target in PD patients with IR.

Keywords: Dopaminergic neurons; Insulin resistance; PTPRO; Parkinson’s disease; α-Synuclein aggregation.

MeSH terms

  • Animals
  • Dopaminergic Neurons / metabolism
  • Dopaminergic Neurons / pathology
  • Female
  • Humans
  • Insulin Resistance* / genetics
  • Male
  • Parkinson Disease* / genetics
  • Parkinson Disease* / metabolism
  • Parkinson Disease* / pathology
  • Protein Aggregation, Pathological / genetics
  • Protein Aggregation, Pathological / metabolism
  • Receptor-Like Protein Tyrosine Phosphatases, Class 3 / genetics
  • Receptor-Like Protein Tyrosine Phosphatases, Class 3 / metabolism
  • Transcriptome
  • alpha-Synuclein* / genetics
  • alpha-Synuclein* / metabolism

Substances

  • alpha-Synuclein
  • Receptor-Like Protein Tyrosine Phosphatases, Class 3
  • PTPRO protein, human