MGMT-inhibitor in combination with TGF-βRI inhibitor or CDK 4/6 inhibitor increases temozolomide sensitivity in temozolomide-resistant glioblastoma cells

Clin Transl Oncol. 2021 Mar;23(3):612-619. doi: 10.1007/s12094-020-02456-x. Epub 2020 Jul 25.

Abstract

Background: Glioblastoma (GB) remains an incurable and deadly brain malignancy that often proves resistant to upfront treatment with temozolomide. Nevertheless, temozolomide remains the most commonly prescribed FDA-approved chemotherapy for GB. The DNA repair protein methylguanine-DNA methyl transferase (MGMT) confers resistance to temozolomide. Unsurprisingly temozolomide-resistant tumors tend to possess elevated MGMT protein levels or lack inhibitory MGMT promotor methylation. In this study, cultured human temozolomide resistance GB (43RG) cells were introduced to the MGMT inhibitor O6-benzylguanine combined with temozolomide and either LY2835219 (CDK 4/6 inhibitor) or LY2157299 (TGF-βRI inhibitor) seeking to overcome GB treatment resistance.

Methods: Treatment effects were assessed using MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) assay, western blot, cell viability, and cell cycle progression.

Results: Our in vitro study demonstrated that sequential treatment of O6-Benzylguanine with either LY2385219 or LY2157299-enhanced temozolomide enhanced sensitivity in MGMT+ 43RG cells. Importantly, normal human neurons and astrocytes remained impervious to the drug therapies under these conditions. Furthermore, LY2835219 has additional anti-proliferative effects on cell cycling, including induction of an RB-associated G (1) arrest via suppression of cyclin D-CDK4/6-Rb pathway. LY2157299 enhances anti-tumor effect by disrupting TGF-β-dependent HIF-1α signaling and by activating both Smad and PI3K-AKT pathways towards transcription of S/G2 checkpoints.

Conclusion: This study establishes the groundwork for the development of a combinatorial pharmacologic approach by using either LY2385219 or LY2157299 inhibitor plus O6-Benzylguanine to augment temozolomide response in temozolomide-resistant GB cells.

Keywords: CDK 4/6 inhibitor; Glioblastoma; MGMT; Signaling pathway; TGF-βRI inhibitor; Temozolomide resistance.

MeSH terms

  • Aminopyridines / pharmacology
  • Antineoplastic Agents, Alkylating / pharmacology*
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Astrocytes / drug effects
  • Benzimidazoles / pharmacology
  • Brain Neoplasms / drug therapy*
  • Brain Neoplasms / enzymology
  • Cell Cycle / drug effects
  • Cell Survival / drug effects
  • Cells, Cultured
  • Cyclin D / antagonists & inhibitors
  • Cyclin-Dependent Kinase 4 / antagonists & inhibitors*
  • Cyclin-Dependent Kinase 6 / antagonists & inhibitors*
  • DNA Modification Methylases / antagonists & inhibitors*
  • DNA Repair Enzymes / antagonists & inhibitors*
  • Drug Resistance, Neoplasm / drug effects
  • G1 Phase Cell Cycle Checkpoints
  • Glioblastoma / drug therapy*
  • Glioblastoma / enzymology
  • Guanine / analogs & derivatives
  • Guanine / pharmacology
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / drug effects
  • Neurons / drug effects
  • Phosphatidylinositol 3-Kinases / drug effects
  • Pyrazoles / pharmacology
  • Quinolines / pharmacology
  • Receptor, Transforming Growth Factor-beta Type I / antagonists & inhibitors*
  • Smad Proteins / drug effects
  • Temozolomide / pharmacology*
  • Tumor Suppressor Proteins / antagonists & inhibitors*

Substances

  • Aminopyridines
  • Antineoplastic Agents, Alkylating
  • Benzimidazoles
  • Cyclin D
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Pyrazoles
  • Quinolines
  • Smad Proteins
  • Tumor Suppressor Proteins
  • O(6)-benzylguanine
  • Guanine
  • abemaciclib
  • LY-2157299
  • DNA Modification Methylases
  • MGMT protein, human
  • CDK4 protein, human
  • CDK6 protein, human
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase 6
  • Receptor, Transforming Growth Factor-beta Type I
  • DNA Repair Enzymes
  • Temozolomide