Generation of complexity in fungal terpene biosynthesis: discovery of a multifunctional cytochrome P450 in the fumagillin pathway

J Am Chem Soc. 2014 Mar 19;136(11):4426-36. doi: 10.1021/ja500881e. Epub 2014 Mar 11.

Abstract

Fumagillin (1), a meroterpenoid from Aspergillus fumigatus, is known for its antiangiogenic activity due to binding to human methionine aminopeptidase 2. 1 has a highly oxygenated structure containing a penta-substituted cyclohexane that is generated by oxidative cleavage of the bicyclic sesquiterpene β-trans-bergamotene. The chemical nature, order, and biochemical mechanism of all the oxygenative tailoring reactions has remained enigmatic despite the identification of the biosynthetic gene cluster and the use of targeted-gene deletion experiments. Here, we report the identification and characterization of three oxygenases from the fumagillin biosynthetic pathway, including a multifunctional cytochrome P450 monooxygenase, a hydroxylating nonheme-iron-dependent dioxygenase, and an ABM family monooxygenase for oxidative cleavage of the polyketide moiety. Most significantly, the P450 monooxygenase is shown to catalyze successive hydroxylation, bicyclic ring-opening, and two epoxidations that generate the sesquiterpenoid core skeleton of 1. We also characterized a truncated polyketide synthase with a ketoreductase function that controls the configuration at C-5 of hydroxylated intermediates.

Publication types

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

MeSH terms

  • Aspergillus fumigatus / chemistry*
  • Aspergillus fumigatus / metabolism
  • Cyclohexanes / chemistry
  • Cyclohexanes / metabolism*
  • Cytochrome P-450 Enzyme System / metabolism*
  • Fatty Acids, Unsaturated / chemistry
  • Fatty Acids, Unsaturated / metabolism*
  • Molecular Structure
  • Sesquiterpenes / chemistry
  • Sesquiterpenes / metabolism
  • Terpenes / chemistry
  • Terpenes / metabolism*

Substances

  • Cyclohexanes
  • Fatty Acids, Unsaturated
  • Sesquiterpenes
  • Terpenes
  • fumagillin
  • Cytochrome P-450 Enzyme System