A Cryptic Plant Terpene Cyclase Producing Unconventional 18- and 14-Membered Macrocyclic C25 and C20 Terpenoids with Immunosuppressive Activity

Angew Chem Int Ed Engl. 2021 Nov 22;60(48):25468-25476. doi: 10.1002/anie.202110842. Epub 2021 Oct 28.

Abstract

A versatile terpene synthase (LcTPS2) producing unconventional macrocyclic terpenoids was characterized from Leucosceptrum canum. Engineered Escherichia coli and Nicotiana benthamiana expressing LcTPS2 produced six 18-/14-membered sesterterpenoids including five new ones and two 14-membered diterpenoids. These products represent the first macrocyclic sesterterpenoids from plants and the largest sesterterpenoid ring system identified to date. Two variants F516A and F516G producing approximately 3.3- and 2.5-fold, respectively, more sesterterpenoids than the wild-type enzyme were engineered. Both 18- and 14-membered ring sesterterpenoids displayed significant inhibitory activity on the IL-2 and IFN-γ production of T cells probably via inhibition of the MAPK pathway. The findings will contribute to the development of efficient biocatalysts to create bioactive macrocyclic sesterterpenoids, and also herald a new potential in the well-trodden territory of plant terpenoid biosynthesis.

Keywords: Leucosceptrum canum; enzyme engineering; immunosuppressive activity; macrocyclic terpenoids; sesterterpene synthase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkyl and Aryl Transferases / metabolism*
  • Humans
  • Immunosuppressive Agents / chemistry
  • Immunosuppressive Agents / metabolism
  • Immunosuppressive Agents / pharmacology*
  • Interferon-gamma / antagonists & inhibitors*
  • Interferon-gamma / biosynthesis
  • Interleukin-2 / antagonists & inhibitors*
  • Interleukin-2 / biosynthesis
  • Lamiaceae / chemistry
  • Lamiaceae / metabolism
  • Macrocyclic Compounds / chemistry
  • Macrocyclic Compounds / metabolism
  • Macrocyclic Compounds / pharmacology*
  • Molecular Structure
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / metabolism
  • Terpenes / chemistry
  • Terpenes / metabolism
  • Terpenes / pharmacology*

Substances

  • Immunosuppressive Agents
  • Interleukin-2
  • Macrocyclic Compounds
  • Terpenes
  • Interferon-gamma
  • Alkyl and Aryl Transferases
  • terpene synthase