Targeted isolation of diketopiperazines from a deep-sea derived fungus with anti-neuroinflammatory effects

Bioorg Chem. 2024 Dec 24:154:108099. doi: 10.1016/j.bioorg.2024.108099. Online ahead of print.

Abstract

Prenylated indole diketopiperazines represent a diverse array of alkaloids with complex chemical scaffolds and with a wide range of biological activities. Aiming to discover bioactive metabolites with structural novelty, genomic annotation in association with the MS/MS-based molecular networking demonstrated a deep-sea derived fungus Aspergillus puulaauensis F77 containing a profile of diketopiperazines. Targeted separation of the cultured fungus led to the isolation of 19 undescribed austamide-type diketopiperazines namely versicoines A-S. Their structures were elucidated by the 2D NMR data, in association with Snatzke'method, ECD calculations, and single-crystal X-ray diffraction data for configurational assignments. Versicoine N-S represent a unique class of austamide-type alkaloids with a spirocenter at C-3. Bioassay results demonstrated versicoine N and relevant analogs possessing inhibitory effects against NO production in LPS-stimulated BV-2 cells. Further mechanistic investigation demonstrated the significant inhibition of versicoine N against p65 expression and its nuclear translocation, along with the inhibition toward phosphorylation of IKK/IκB in NF-κB signaling pathway. In addition, versicoine N also inhibited NLRP3 inflammasome activation and its related proteins, including caspase 1, pro-caspase1, IL-1β and pro-IL-1β. This study largely extends the chemical diversity of austamide-type alkaloids, and provides promising lead compounds for anti-neuroinflammation.

Keywords: Anti-neuroinflammation; Aspergillus puulaauensis F77; Diketopiperazines; Marine fungus; Structure elucidation.