Structural Elucidation and Synthesis of Eudistidine A: An Unusual Polycyclic Marine Alkaloid that Blocks Interaction of the Protein Binding Domains of p300 and HIF-1α

J Am Chem Soc. 2015 Apr 29;137(16):5569-75. doi: 10.1021/jacs.5b02156. Epub 2015 Apr 20.

Abstract

Low oxygen environments are a hallmark of solid tumors, and transcription of many hypoxia-responsive genes needed for survival under these conditions is regulated by the transcription factor HIF-1 (hypoxia-inducible factor 1). Activation of HIF-1 requires binding of its α-subunit (HIF-1α) to the transcriptional coactivator protein p300. Inhibition of the p300/HIF-1α interaction can suppress HIF-1 activity. A screen for inhibitors of the protein binding domains of p300 (CH1) and HIF-1α (C-TAD) identified an extract of the marine ascidian Eudistoma sp. as active. Novel heterocyclic alkaloids eudistidines A (1) and B (2) were isolated from the extract, and their structures assigned by spectroscopic analyses. They contain an unprecedented tetracyclic core composed of two pyrimidine rings fused with an imidazole ring. Eudistidine A (1) was synthesized in a concise four-step sequence featuring a condensation/cyclization reaction cascade between 4-(2-aminophenyl)pyrimidin-2-amine (3) and 4-methoxy-phenylglyoxal (4), while eudistidine B (2) was synthesized in a similar fashion with glyoxylic acid (5) in place of 4. Naturally occurring eudistidine A (1) effectively inhibited CH1/C-TAD binding with an IC50 of 75 μM, and synthetic 1 had similar activity. The eudistidine A (1) scaffold, which can be synthesized in a concise, scalable manner, may provide potential therapeutic lead compounds or molecular probes to study p300/HIF-1α interactions and the role these proteins play in tumor response to low oxygen conditions. The unique structural scaffolds and functional group arrays often found in natural products make these secondary metabolites a rich source of new compounds that can disrupt critical protein-protein binding events.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • Alkaloids / chemical synthesis
  • Alkaloids / chemistry*
  • Alkaloids / pharmacology*
  • Animals
  • E1A-Associated p300 Protein / chemistry
  • E1A-Associated p300 Protein / metabolism*
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / chemistry
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Neoplasms / drug therapy
  • Neoplasms / metabolism
  • Polycyclic Compounds / chemical synthesis
  • Polycyclic Compounds / chemistry*
  • Polycyclic Compounds / pharmacology*
  • Protein Binding / drug effects
  • Protein Interaction Maps / drug effects*
  • Urochordata / chemistry

Substances

  • Alkaloids
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Polycyclic Compounds
  • E1A-Associated p300 Protein
  • EP300 protein, human