The Amaryllidaceae Alkaloid Haemanthamine Binds the Eukaryotic Ribosome to Repress Cancer Cell Growth

Structure. 2018 Mar 6;26(3):416-425.e4. doi: 10.1016/j.str.2018.01.009. Epub 2018 Feb 8.

Abstract

Alkaloids isolated from the Amaryllidaceae plants have potential as therapeutics for treating human diseases. Haemanthamine has been studied as a novel anticancer agent due to its ability to overcome cancer cell resistance to apoptosis. Biochemical experiments have suggested that hemanthamine targets the ribosome. However, a structural characterization of its mechanism has been missing. Here we present the 3.1 Å resolution X-ray structure of haemanthamine bound to the Saccharomyces cerevisiae 80S ribosome. This structure reveals that haemanthamine targets the A-site cleft on the large ribosomal subunit rearranging rRNA to halt the elongation phase of translation. Furthermore, we provide evidence that haemanthamine and other Amaryllidaceae alkaloids also inhibit specifically ribosome biogenesis, triggering nucleolar stress response and leading to p53 stabilization in cancer cells. Together with a computer-aided interpretation of existing structure-activity relationships of Amaryllidaceae alkaloids congeners, we provide a rationale for designing molecules with enhanced potencies and reduced toxicities.

Keywords: Amaryllidaceae alkaloids; X-ray crystallography; cancer; haemanthamine; nucleolar stress response; p53; peptidyl transferase center; ribosome; ribosome biogenesis; translation elongation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amaryllidaceae Alkaloids / chemistry
  • Amaryllidaceae Alkaloids / pharmacology*
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology*
  • Binding Sites
  • Cell Proliferation / drug effects
  • Colonic Neoplasms / drug therapy
  • Colonic Neoplasms / metabolism*
  • Crystallography, X-Ray
  • HCT116 Cells
  • Humans
  • Models, Molecular
  • Molecular Conformation
  • Phenanthridines / chemistry
  • Phenanthridines / pharmacology*
  • RNA, Ribosomal / chemistry
  • RNA, Ribosomal / metabolism
  • Ribosomes / chemistry
  • Ribosomes / metabolism*
  • Saccharomyces cerevisiae / metabolism*
  • Saccharomyces cerevisiae Proteins / metabolism
  • Structure-Activity Relationship
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Amaryllidaceae Alkaloids
  • Antineoplastic Agents
  • Phenanthridines
  • RNA, Ribosomal
  • Saccharomyces cerevisiae Proteins
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • hemanthamine