Identification of a Noroxomaritidine Reductase with Amaryllidaceae Alkaloid Biosynthesis Related Activities

J Biol Chem. 2016 Aug 5;291(32):16740-52. doi: 10.1074/jbc.M116.717827. Epub 2016 Jun 1.

Abstract

Amaryllidaceae alkaloids are a large group of plant natural products with over 300 documented structures and diverse biological activities. Several groups of Amaryllidaceae alkaloids including the hemanthamine- and crinine-type alkaloids show promise as anticancer agents. Two reduction reactions are required for the production of these compounds: the reduction of norcraugsodine to norbelladine and the reduction of noroxomaritidine to normaritidine, with the enantiomer of noroxomaritidine dictating whether the derivatives will be the crinine-type or hemanthamine-type. It is also possible for the carbon-carbon double bond of noroxomaritidine to be reduced, forming the precursor for maritinamine or elwesine depending on the enantiomer reduced to an oxomaritinamine product. In this study, a short chain alcohol dehydrogenase/reductase that co-expresses with the previously discovered norbelladine 4'-O-methyltransferase from Narcissus sp. and Galanthus spp. was cloned and expressed in Escherichia coli Biochemical analyses and x-ray crystallography indicates that this protein functions as a noroxomaritidine reductase that forms oxomaritinamine from noroxomaritidine through a carbon-carbon double bond reduction. The enzyme also reduces norcraugsodine to norbelladine with a 400-fold lower specific activity. These studies identify a missing step in the biosynthesis of this pharmacologically important class of plant natural products.

Keywords: Amaryllidaceae alkaloids; crystal structure; enzyme structure; norbelladine; noroxomaritidine reductase; reductase; secondary metabolism; transcriptomics.

Publication types

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

MeSH terms

  • Amaryllidaceae Alkaloids / chemistry*
  • Amaryllidaceae Alkaloids / metabolism
  • Galanthus / enzymology*
  • Galanthus / genetics
  • Narcissus / enzymology*
  • Narcissus / genetics
  • Oxidation-Reduction
  • Oxidoreductases / chemistry*
  • Oxidoreductases / genetics
  • Oxidoreductases / metabolism
  • Plant Proteins / chemistry*
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism

Substances

  • Amaryllidaceae Alkaloids
  • Plant Proteins
  • Recombinant Proteins
  • Oxidoreductases

Associated data

  • PDB/2AE2
  • PDB/5FEU
  • PDB/5FF9
  • PDB/5FFF