High mobility group A1 protein modulates autophagy in cancer cells

Cell Death Differ. 2017 Nov;24(11):1948-1962. doi: 10.1038/cdd.2017.117. Epub 2017 Aug 4.

Abstract

High Mobility Group A1 (HMGA1) is an architectural chromatin protein whose overexpression is a feature of malignant neoplasias with a causal role in cancer initiation and progression. HMGA1 promotes tumor growth by several mechanisms, including increase of cell proliferation and survival, impairment of DNA repair and induction of chromosome instability. Autophagy is a self-degradative process that, by providing energy sources and removing damaged organelles and misfolded proteins, allows cell survival under stress conditions. On the other hand, hyper-activated autophagy can lead to non-apoptotic programmed cell death. Autophagy deregulation is a common feature of cancer cells in which has a complex role, showing either an oncogenic or tumor suppressor activity, depending on cellular context and tumor stage. Here, we report that depletion of HMGA1 perturbs autophagy by different mechanisms. HMGA1-knockdown increases autophagosome formation by constraining the activity of the mTOR pathway, a major regulator of autophagy, and transcriptionally upregulating the autophagy-initiating kinase Unc-51-like kinase 1 (ULK1). Consistently, functional experiments demonstrate that HMGA1 binds ULK1 promoter region and negatively regulates its transcription. On the other hand, the increase in autophagosomes is not associated to a proportionate increase in their maturation. Overall, the effects of HMGA1 depletion on autophagy are associated to a decrease in cell proliferation and ultimately impact on cancer cells viability. Importantly, silencing of ULK1 prevents the effects of HMGA1-knockdown on cellular proliferation, viability and autophagic activity, highlighting how these effects are, at least in part, mediated by ULK1. Interestingly, this phenomenon is not restricted to skin cancer cells, as similar results have been observed also in HeLa cells silenced for HMGA1. Taken together, these results clearly indicate HMGA1 as a key regulator of the autophagic pathway in cancer cells, thus suggesting a novel mechanism through which HMGA1 can contribute to cancer progression.

MeSH terms

  • Animals
  • Autophagy*
  • Autophagy-Related Protein 5 / metabolism
  • Autophagy-Related Protein-1 Homolog / genetics
  • Autophagy-Related Protein-1 Homolog / metabolism
  • Cell Proliferation
  • Cell Survival
  • Gene Knockdown Techniques
  • Gene Silencing
  • Green Fluorescent Proteins / metabolism
  • HMGA1a Protein / metabolism*
  • HeLa Cells
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Mice
  • Microtubule-Associated Proteins / metabolism
  • Neoplasms / metabolism*
  • Neoplasms / pathology*
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Skin Neoplasms / metabolism
  • Skin Neoplasms / pathology
  • Transcription, Genetic

Substances

  • ATG5 protein, human
  • Autophagy-Related Protein 5
  • Intracellular Signaling Peptides and Proteins
  • MAP1LC3A protein, human
  • Microtubule-Associated Proteins
  • HMGA1a Protein
  • Green Fluorescent Proteins
  • Autophagy-Related Protein-1 Homolog
  • Protein Serine-Threonine Kinases
  • ULK1 protein, human
  • Ulk2 protein, human