KSHV dysregulates bulk macroautophagy, mitophagy and UPR to promote endothelial to mesenchymal transition and CCL2 release, key events in viral-driven sarcomagenesis

Int J Cancer. 2020 Dec 15;147(12):3500-3510. doi: 10.1002/ijc.33163. Epub 2020 Jul 23.

Abstract

Kaposi's sarcoma-associated herpesvirus (KSHV) is the causative agent of KS, an aggressive neoplasm that mainly occurs in immune-compromised patients. Spindle cells represent the main feature of this aggressive malignancy and arise from KSHV-infected endothelial cells undergoing endothelial to mesenchymal transition (EndMT), which changes their cytoskeletal composition and organization. As in epithelial to mesenchymal transition (EMT), EndMT is driven by transcription factors such as SNAI1 and ZEB1 and implies a cellular reprogramming mechanism regulated by several molecular pathways, particularly PI3K/AKT/MTOR. Here we found that KSHV activated MTOR and its targets 4EBP1 and ULK1 and reduced bulk macroautophagy and mitophagy to promote EndMT, activate ER stress/unfolded protein response (UPR), and increase the release of the pro-angiogenic and pro-inflammatory chemokine CCL2 by HUVEC cells. Our study suggests that the manipulation of macroautophagy, mitophagy and UPR and the interplay between the three could be a promising strategy to counteract EndMT, angiogenesis and inflammation, the key events of KSHV-driven sarcomagenesis.

Keywords: CCCP; EndMT; HUVEC; KSHV; PERK; RAB7; SNAI1; macroautophagy; metformin; mitophagy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism
  • Autophagy-Related Protein-1 Homolog / metabolism
  • Cell Cycle Proteins / metabolism
  • Chemokine CCL2 / metabolism*
  • Endothelial Cells / cytology*
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Endothelial Cells / virology
  • Epithelial-Mesenchymal Transition
  • Herpesvirus 8, Human / pathogenicity*
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Macroautophagy
  • Mitochondria / metabolism*
  • Mitophagy
  • Models, Biological
  • Primary Cell Culture
  • Reactive Oxygen Species / metabolism
  • Sarcoma, Kaposi / metabolism
  • Sarcoma, Kaposi / virology*
  • Signal Transduction
  • TOR Serine-Threonine Kinases / metabolism
  • Unfolded Protein Response

Substances

  • Adaptor Proteins, Signal Transducing
  • CCL2 protein, human
  • Cell Cycle Proteins
  • Chemokine CCL2
  • EIF4EBP1 protein, human
  • Intracellular Signaling Peptides and Proteins
  • Reactive Oxygen Species
  • MTOR protein, human
  • Autophagy-Related Protein-1 Homolog
  • TOR Serine-Threonine Kinases
  • ULK1 protein, human