The role of Ala231 and Trp227 in the substrate specificities of fungal 17β-hydroxysteroid dehydrogenase and trihydroxynaphthalene reductase: Steroids versus smaller substrates

J Steroid Biochem Mol Biol. 2012 Mar;129(1-2):92-8. doi: 10.1016/j.jsbmb.2011.03.019. Epub 2011 Mar 23.

Abstract

17β-Hydroxysteroid dehydrogenase and trihydroxynaphthalene reductase from the fungus Curvularia lunata (teleomorph: Cochliobolus lunatus; 17β-HSDcl and 3HNR, respectively) are two homologous short-chain dehydrogenase/reductase proteins that are 58% identical and have 86% similar amino acids. The minor differences in their substrate-binding regions are believed to be crucial for their substrate specificities. 3HNR shows high affinity for substrates with two rings, like trihydroxynaphthalene and 2,3-dihydro-2,5-dihydroxy-4H-benzopyran-4-one (DDBO), while 17β-HSDcl can accommodate ligands with four rings, like steroids. In the present study, we examined the role of Ala231 in 17β-HSDcl and Trp227 in 3HNR, as the potential key amino acids in the determination of substrate recognition based on size. We constructed Ala231Trp 17β-HSDcl and Trp227Ala 3HNR mutant proteins and used spectrophotometric analyses to compare their catalytic activities with those of the wild-type enzymes, for oxidation of 4-estrene-17β-ol-3-one and DDBO and for reduction of 4-estrene-3,17-dione and 9,10-phenanthrenequinone (PQ). The Ala231Trp side-chain substitution in 17β-HSDcl abolished and decreased (by 14.6-fold) the initial rates for steroid oxidation and reduction, respectively, while the initial rate for PQ reduction was increased 5.6-fold. The bulky Trp227Ala side-chain substitution in 3HNR enabled oxidation of 4-estrene-17β-ol-3-one, increased the initial rates for reduction of 4-estrene-3,17-dione and PQ by 4.5-fold and 1.5-fold, respectively, while the initial rate for DDBO oxidation was decreased 4.1-fold. Our TLC analysis and docking simulations also support these findings. Our study thus confirms the important roles of Ala231 in 17β-HSDcl and Trp227 in 3HNR, for the selection between larger and smaller substrates. Article from a special issue on steroids and microorganisms.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 17-Hydroxysteroid Dehydrogenases / genetics
  • 17-Hydroxysteroid Dehydrogenases / metabolism*
  • Alanine / chemistry*
  • Amino Acid Sequence
  • Ascomycota / enzymology
  • Benzopyrans / metabolism
  • Catalytic Domain
  • Estrenes / metabolism
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism*
  • Oxidation-Reduction
  • Oxidoreductases Acting on CH-CH Group Donors / genetics
  • Oxidoreductases Acting on CH-CH Group Donors / metabolism*
  • Phenanthrenes / metabolism
  • Steroids / metabolism
  • Substrate Specificity
  • Tryptophan / chemistry*

Substances

  • 2,3-dihydro-2,5-dihydroxy-4H-benzopyran-4-one
  • Benzopyrans
  • Estrenes
  • Fungal Proteins
  • Phenanthrenes
  • Steroids
  • 9,10-phenanthrenequinone
  • Tryptophan
  • 17-Hydroxysteroid Dehydrogenases
  • tetrahydroxynaphthalene reductase
  • 3 (or 17)-beta-hydroxysteroid dehydrogenase
  • Oxidoreductases Acting on CH-CH Group Donors
  • Alanine