Discovery of a Novel and Potent Dual-Targeting Inhibitor of ATM and HDAC2 Through Structure-Based Virtual Screening for the Treatment of Testicular Cancer

Drug Des Devel Ther. 2024 Nov 20:18:5283-5297. doi: 10.2147/DDDT.S479113. eCollection 2024.

Abstract

Purpose: Dual inhibition of ataxia telangiectasia mutated (ATM) and histone deacetylase 2 (HDAC2) may be a potential strategy to improve antitumor efficacy in testicular cancer.

Methods: A combined virtual screening protocol including pharmacophore modeling and molecular docking was used for screening potent dual-target ATM/HDAC2 inhibitors. In order to obtain the optimal lead compound, the dual ATM/HDAC2 inhibitory activity of the screened compounds was further evaluated using enzyme inhibition methods. The binding stability of the optimal compound to the dual targets was verified by molecular dynamics (MD) simulation. MTT assay and in vivo antitumor experiment were performed to validate antitumor efficacy of the optimal compound in testicular cancer.

Results: Here, we successfully discovered six potent dual-target ATM/HDAC2 inhibitors (AMHs 1-6), which exhibited good inhibitory activity against both ATM and HDAC2. Among them, AMH-4 showed strong inhibitory activity against both ATM (IC50 = 1.12 ± 0.03 nM) and HDAC2 (IC50 = 3.04 ± 0.08 nM). MD simulation indicated that AMH-4 binds to ATM and HDAC2 with satisfactory stability. Importantly, AMH-4 had significant antiproliferative activity on human testicular tumor cells, especially NTERA-2 cL.D1 cells, and no inhibitory effect on normal human testicular cells. In vivo experiments exhibited that AMH-4 was more effective than lartesertib and vorinostat in inhibiting the growth of NTERA-2 cL.D1 xenograft tumors with low toxicity.

Conclusion: Overall, these results suggest that AMH-4 is an effective and low toxicity candidate for the treatment of testicular germ cell tumors.

Keywords: ataxia telangiectasia mutated; dual-targeting inhibitors; histone deacetylase 2; structure-based virtual screening; testicular germ cell tumors.

MeSH terms

  • Animals
  • Antineoplastic Agents* / chemical synthesis
  • Antineoplastic Agents* / chemistry
  • Antineoplastic Agents* / pharmacology
  • Ataxia Telangiectasia Mutated Proteins* / antagonists & inhibitors
  • Ataxia Telangiectasia Mutated Proteins* / metabolism
  • Cell Line, Tumor
  • Cell Proliferation* / drug effects
  • Dose-Response Relationship, Drug
  • Drug Discovery
  • Drug Screening Assays, Antitumor*
  • Histone Deacetylase 2* / antagonists & inhibitors
  • Histone Deacetylase 2* / metabolism
  • Histone Deacetylase Inhibitors* / chemical synthesis
  • Histone Deacetylase Inhibitors* / chemistry
  • Histone Deacetylase Inhibitors* / pharmacology
  • Humans
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Molecular Docking Simulation
  • Molecular Dynamics Simulation
  • Molecular Structure
  • Neoplasms, Experimental / drug therapy
  • Neoplasms, Experimental / metabolism
  • Neoplasms, Experimental / pathology
  • Structure-Activity Relationship
  • Testicular Neoplasms* / drug therapy
  • Testicular Neoplasms* / metabolism
  • Testicular Neoplasms* / pathology

Substances

  • Histone Deacetylase 2
  • Ataxia Telangiectasia Mutated Proteins
  • HDAC2 protein, human
  • Antineoplastic Agents
  • Histone Deacetylase Inhibitors
  • ATM protein, human