Novel pyrrolone-fused benzosuberene MK2 inhibitors: synthesis, pharmacophore modelling, molecular docking, and anti-cancer efficacy evaluation in HNSCC cells

J Biomol Struct Dyn. 2024;42(21):11954-11975. doi: 10.1080/07391102.2023.2265993. Epub 2023 Oct 11.

Abstract

Head and neck Squamous Cell Carcinoma (HNSCC) is a growing concern worldwide and MAPKAPK2/MK2 (Mitogen-Activated Protein Kinase Activated Protein Kinase 2) is crucially involved in HNSCC progression. Increased disease burden and lacuna of targeted therapies require novel and safe pharmacological inhibitors to suppress the well-explored molecular targets in HNSCC. Here, we used dibromo-substituted benzosuberene synthesized from the mixture of α, β, γ-himachalenes and utilized as a precursor for the synthesis of Pyrrolone-fused benzosuberenes (PfBS) as MK2 inhibitors through aminocarbonylation approach in a single-pot reaction. The devised protocol provides a broad substrate scope, facile recovery, recyclability of Polystyrene-supported palladium (Pd@PS) nanoparticle catalyst, and fewer synthesis steps. In-silico molecular docking, pharmacophore modeling, and ADMET revealed MK2-inhibitory potential and drug-likeliness of PfBS analogues. Surface plasmon resonance (SPR) analysis revealed effective high binding affinity (KD) and kinetics of PfBS analogues with MK2. Additionally, the SPR-mediated in-solution inhibition assay established the MK2-inhibition properties of PfBS analogues through abrogation of MK2-Hsp27 interaction. Further, in-vitro studies validate the findings in HNSCC cells. PfBS analogues exhibited significant anti-proliferative effects on CAL 27 tongue squamous carcinoma cells and were found safe on IEC-6 intestinal epithelial cells. Moreover, immunofluorescence analysis and western-blot assays potentiated, that selected analogues inhibited the inflammatory cytokine TNF-α induced activation of MK2 on cellular and molecular levels in HNSCC cells. In conclusion, this study presents novel MK2-inhibitors and opens the avenue for further pre-clinical and clinical efficacy evaluation of developed PfBS analogues in the treatment of HNSCC.Communicated by Ramaswamy H. Sarma.

Keywords: HNSCC; MAPKAPK2; MK2 inhibitors; Pyrrolone-fused benzosuberenes (PfBS); SPR; molecular docking.

MeSH terms

  • Antineoplastic Agents* / chemical synthesis
  • Antineoplastic Agents* / chemistry
  • Antineoplastic Agents* / pharmacology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Head and Neck Neoplasms / drug therapy
  • Head and Neck Neoplasms / metabolism
  • Head and Neck Neoplasms / pathology
  • Humans
  • Intracellular Signaling Peptides and Proteins / antagonists & inhibitors
  • Intracellular Signaling Peptides and Proteins / chemistry
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Molecular Docking Simulation*
  • Molecular Dynamics Simulation
  • Pharmacophore
  • Protein Binding
  • Protein Kinase Inhibitors* / chemical synthesis
  • Protein Kinase Inhibitors* / chemistry
  • Protein Kinase Inhibitors* / pharmacology
  • Protein Serine-Threonine Kinases* / antagonists & inhibitors
  • Protein Serine-Threonine Kinases* / chemistry
  • Protein Serine-Threonine Kinases* / metabolism
  • Pyrroles* / chemical synthesis
  • Pyrroles* / chemistry
  • Pyrroles* / pharmacology
  • Squamous Cell Carcinoma of Head and Neck* / drug therapy
  • Squamous Cell Carcinoma of Head and Neck* / metabolism
  • Squamous Cell Carcinoma of Head and Neck* / pathology
  • Structure-Activity Relationship

Substances

  • MAP-kinase-activated kinase 2
  • Protein Serine-Threonine Kinases
  • Antineoplastic Agents
  • Pyrroles
  • Protein Kinase Inhibitors
  • Intracellular Signaling Peptides and Proteins