Elisidepsin Interacts Directly with Glycosylceramides in the Plasma Membrane of Tumor Cells to Induce Necrotic Cell Death

PLoS One. 2015 Oct 16;10(10):e0140782. doi: 10.1371/journal.pone.0140782. eCollection 2015.

Abstract

Plasma membrane integrity is essential for cell life. Any major break on it immediately induces the death of the affected cell. Different molecules were described as disrupting this cell structure and thus showing antitumor activity. We have previously defined that elisidepsin (Irvalec®, PM02734) inserts and self-organizes in the plasma membrane of tumor cells, inducing a rapid loss of membrane integrity, cell permeabilization and necrotic death. Here we show that, in sensitive HCT-116 colorectal cells, all these effects are consequence of the interaction of elisidepsin with glycosylceramides in the cell membrane. Of note, an elisidepsin-resistant subline (HCT-116-Irv) presented reduced levels of glycosylceramides and no accumulation of elisidepsin in the plasma membrane. Consequently, drug treatment did not induce the characteristic necrotic cell death. Furthermore, GM95, a mutant derivative from B16 mouse melanoma cells lacking ceramide glucosyltransferase (UGCG) activity and thus the synthesis of glycosylceramides, was also resistant to elisidepsin. Over-expression of UGCG gene in these deficient cells restored glycosylceramides synthesis, rendering them sensitive to elisidepsin, at a similar level than parental B16 cells. These results indicate that glycosylceramides act as membrane targets of elisidepsin, facilitating its insertion in the plasma membrane and the subsequent membrane permeabilization that leads to drug-induced cell death. They also indicate that cell membrane lipids are a plausible target for antineoplastic therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Membrane / metabolism*
  • Cell Membrane / pathology
  • Colorectal Neoplasms / drug therapy
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / metabolism*
  • Colorectal Neoplasms / pathology
  • Depsipeptides / pharmacology*
  • Glucosylceramides / genetics
  • Glucosylceramides / metabolism*
  • Humans
  • Melanoma / drug therapy
  • Melanoma / genetics
  • Melanoma / metabolism*
  • Melanoma / pathology
  • Mice
  • Necrosis

Substances

  • Depsipeptides
  • Glucosylceramides
  • elisidepsin

Grants and funding

The work of CV, AM and CM was partially supported by Ministerio de Economía y Competitividad (www.mineco.gob.es) [grant numbers SAF2010-14916 and SAF2013-45800-R], and Instituto de Salud Carlos III (www.isciii.es) [grant numbers FIS-RECAVA RD06/0014/0025 and FIS-RIC RD12/0042/0019]. The work of MPL and CG was partially supported by Ministerio de Economía y Competitividad [grant number CTQ 2010-1645]. CM and AM hold FPI and JAE-Predoc (www.csic.es) fellowships, respectively. These funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. In addition, the work of CV and MPL was supported in part by a grant from PharmaMar S.A. JMMG, LFGF, JFML, RF, VM and CMG are employees and shareholders of PharmaMar S.A. and played a role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.