Suppression of G6PD induces the expression and bisecting GlcNAc-branched N-glycosylation of E-Cadherin to block epithelial-mesenchymal transition and lymphatic metastasis

Br J Cancer. 2020 Oct;123(8):1315-1325. doi: 10.1038/s41416-020-1007-3. Epub 2020 Jul 28.

Abstract

Background: As the rate-limit enzyme of the pentose phosphate pathway, glucose-6-phosphate dehydrogenase (G6PD) plays important roles in tumour progression, but the exact mechanism through which G6PD controls cancer metastasis remains unclear.

Methods: G6PD expression in resected oral squamous cell carcinoma (OSCC) samples was analysed by immunohistochemistry. The effects and mechanism of G6PD suppression on OSCC cell lines were measured by transwell assay, wound healing assay, western and lectin blot, mass spectrometer analysis, ChIP-PCR, and luciferase reporter assay. BALB/c-nude mice were used to establish orthotopic xenograft model.

Results: G6PD expression in the tumours of 105 OSCC patients was associated with lymphatic metastasis and prognosis. In vitro cellular study suggested that G6PD suppression impaired cell migration, invasion, and epithelial-mesenchymal transition. Furtherly, G6PD knockdown activated the JNK pathway, which then blocked the AKT/GSK-3β/Snail axis to induce E-Cadherin expression and transcriptionally regulated MGAT3 expression to promote bisecting GlcNAc-branched N-glycosylation of E-Cadherin. An orthotopic xenograft model further confirmed that dehydroepiandrosterone reduced lymphatic metastatic rate of OSCC, which was partially reversed by JNK inhibition.

Conclusions: Suppression of G6PD promoted the expression and bisecting GlcNAc-branched N-glycosylation of E-Cadherin via activating the JNK pathway, which thus acted on OSCC metastasis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylglucosamine / metabolism*
  • Animals
  • Cadherins / metabolism*
  • Cell Line, Tumor
  • Epithelial-Mesenchymal Transition / physiology*
  • Female
  • Glucosephosphate Dehydrogenase / antagonists & inhibitors
  • Glucosephosphate Dehydrogenase / physiology*
  • Glycogen Synthase Kinase 3 beta / physiology
  • Glycosylation
  • Humans
  • JNK Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • JNK Mitogen-Activated Protein Kinases / physiology
  • Lymphatic Metastasis
  • Mice
  • Mice, Inbred BALB C
  • Mouth Neoplasms / metabolism
  • Mouth Neoplasms / mortality
  • Mouth Neoplasms / pathology*
  • Proto-Oncogene Proteins c-akt / physiology
  • Squamous Cell Carcinoma of Head and Neck / metabolism
  • Squamous Cell Carcinoma of Head and Neck / mortality
  • Squamous Cell Carcinoma of Head and Neck / pathology*

Substances

  • Cadherins
  • Glucosephosphate Dehydrogenase
  • Glycogen Synthase Kinase 3 beta
  • Proto-Oncogene Proteins c-akt
  • JNK Mitogen-Activated Protein Kinases
  • Acetylglucosamine