Pyrrolidinium fullerene induces apoptosis by activation of procaspase-9 via suppression of Akt in primary effusion lymphoma

Biochem Biophys Res Commun. 2014 Aug 15;451(1):93-100. doi: 10.1016/j.bbrc.2014.07.068. Epub 2014 Jul 22.

Abstract

Primary effusion lymphoma (PEL) is a subtype of non-Hodgkin's B-cell lymphoma and is an aggressive neoplasm caused by Kaposi's sarcoma-associated herpesvirus (KSHV) in immunosuppressed patients. In general, PEL cells are derived from post-germinal center B-cells and are infected with KSHV. To evaluate potential novel anti-tumor compounds against KSHV-associated PEL, seven water-soluble fullerene derivatives were evaluated as potential drug candidates for the treatment of PEL. Herein, we discovered a pyrrolidinium fullerene derivative, 1,1,1',1'-tetramethyl [60]fullerenodipyrrolidinium diiodide, which induced apoptosis of PEL cells via a novel mechanism, the caspase-9 activation by suppressing the caspase-9 phosphorylation, causing caspase-9 inactivation. Pyrrolidinium fullerene treatment reduced significantly the viability of PEL cells compared with KSHV-uninfected lymphoma cells, and induced the apoptosis of PEL cells by activating caspase-9 via procaspase-9 cleavage. Pyrrolidinium fullerene additionally reduced the Ser473 phosphorylation of Akt and Ser196 of procaspase-9. Ser473-phosphorylated Akt (i.e., activated Akt) phosphorylates Ser196 in procaspase-9, causing inactivation of procaspase-9. We also demonstrated that Akt inhibitors suppressed the proliferation of PEL cells compared with KSHV-uninfected cells. Our data therefore suggest that Akt activation is essential for cell survival in PEL and a pyrrolidinium fullerene derivative induced apoptosis by activating caspase-9 via suppression of Akt in PEL cells. In addition, we evaluated whether pyrrolidinium fullerene in combination with the HSP90 inhibitor (geldanamycin; GA) or valproate, potentiated the cytotoxic effects on PEL cells. Compared to treatment with pyrrolidinium fullerene alone, the addition of low-concentration GA or valproate enhanced the cytotoxic activity of pyrrolidinium fullerene. These results indicate that pyrrolidinium fullerene could be used as a novel therapy for the treatment of PEL.

Keywords: Akt; Apoptosis; Caspase-9; Fullerene; KSHV; PEL.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Apoptosis / drug effects
  • Benzoquinones / administration & dosage
  • Benzoquinones / pharmacology
  • Bridged-Ring Compounds / pharmacology*
  • Caspase 9 / metabolism
  • Caspase Inhibitors / pharmacology
  • Cell Line, Tumor
  • Drug Screening Assays, Antitumor / methods
  • Fullerenes / chemistry
  • Fullerenes / pharmacology
  • HSP90 Heat-Shock Proteins / antagonists & inhibitors
  • Herpesvirus 8, Human / pathogenicity
  • Humans
  • Lactams, Macrocyclic / administration & dosage
  • Lactams, Macrocyclic / pharmacology
  • Lymphoma, Primary Effusion / drug therapy*
  • Lymphoma, Primary Effusion / metabolism
  • Lymphoma, Primary Effusion / pathology*
  • Lymphoma, Primary Effusion / virology
  • Phosphorylation / drug effects
  • Proto-Oncogene Proteins c-akt / antagonists & inhibitors*
  • Proto-Oncogene Proteins c-akt / metabolism
  • Pyrrolidines / pharmacology*
  • Serine / metabolism
  • Virion / drug effects

Substances

  • 1,1,1',1'-tetramethyl (60)fullerenodipyrrolidinium
  • Antineoplastic Agents
  • Benzoquinones
  • Bridged-Ring Compounds
  • Caspase Inhibitors
  • Fullerenes
  • HSP90 Heat-Shock Proteins
  • Lactams, Macrocyclic
  • Pyrrolidines
  • Serine
  • Proto-Oncogene Proteins c-akt
  • Caspase 9
  • geldanamycin