Rational incorporation of selenium into temozolomide elicits superior antitumor activity associated with both apoptotic and autophagic cell death

PLoS One. 2012;7(4):e35104. doi: 10.1371/journal.pone.0035104. Epub 2012 Apr 5.

Abstract

Background: The DNA alkylating agent temozolomide (TMZ) is widely used in the treatment of human malignancies such as glioma and melanoma. On the basis of previous structure-activity studies, we recently synthesized a new TMZ selenium analog by rationally introducing an N-ethylselenocyanate extension to the amide functionality in TMZ structure.

Principal findings: This TMZ-Se analog showed a superior cytotoxicity to TMZ in human glioma and melanoma cells and a more potent tumor-inhibiting activity than TMZ in mouse glioma and melanoma xenograft model. TMZ-Se was also effective against a TMZ-resistant glioma cell line. To explore the mechanism underlying the superior antitumor activity of TMZ-Se, we compared the effects of TMZ and TMZ-Se on apoptosis and autophagy. Apoptosis was significantly increased in tumor cells treated with TMZ-Se in comparison to those treated with TMZ. TMZ-Se also triggered greater autophagic response, as compared with TMZ, and suppressing autophagy partly rescued cell death induced by TMZ-Se, indicating that TMZ-Se-triggered autophagy contributed to cell death. Although mRNA level of the key autophagy gene, Beclin 1, was increased, Beclin 1 protein was down-regulated in the cells treated with TMZ-Se. The decrease in Beclin 1 following TMZ-Se treatment were rescued by the calpain inhibitors and the calpain-mediated degradation of Beclin1 had no effect on autophagy but promoted apoptosis in cells treated with TMZ-Se.

Conclusions: Our study indicates that incorporation of Se into TMZ can render greater potency to this chemotherapeutic drug.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antineoplastic Agents, Alkylating / chemistry*
  • Antineoplastic Agents, Alkylating / therapeutic use*
  • Apoptosis / drug effects
  • Apoptosis Regulatory Proteins / biosynthesis
  • Apoptosis Regulatory Proteins / genetics
  • Autophagy / drug effects
  • Beclin-1
  • Brain Neoplasms / drug therapy*
  • Calpain / antagonists & inhibitors
  • Calpain / physiology
  • Cell Line, Tumor
  • Dacarbazine / analogs & derivatives*
  • Dacarbazine / chemistry
  • Dacarbazine / therapeutic use
  • Glioma / drug therapy*
  • Humans
  • Male
  • Melanoma / drug therapy*
  • Membrane Proteins / biosynthesis
  • Membrane Proteins / genetics
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Selenium / chemistry*
  • Skin Neoplasms / drug therapy*
  • Temozolomide
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents, Alkylating
  • Apoptosis Regulatory Proteins
  • BECN1 protein, human
  • Beclin-1
  • Becn1 protein, mouse
  • Membrane Proteins
  • Dacarbazine
  • Calpain
  • Selenium
  • Temozolomide