Structural basis of selective beta-carotene binding by a soluble protein

Structure. 2024 Nov 7;32(11):2123-2133.e3. doi: 10.1016/j.str.2024.09.014. Epub 2024 Oct 8.

Abstract

β-carotene (BCR) is the most abundant carotenoid, a colorant, antioxidant, and provitamin A. The extreme hydrophobicity of this hydrocarbon requires special mechanisms for distribution in aqueous media, including water-soluble carotenoproteins. However, all known carotenoproteins prefer oxygenated carotenoids and bind BCR inefficiently. Here, we present the crystal structure of the BCR-binding protein (BBP) from gregarious male locusts, which is responsible for their vivid yellow body coloration, in complex with its natural ligand, BCR. BBP forms an antiparallel tubular homodimer with α/β-wrap folded monomers, each forming a hydrophobic 47 Å long, coaxial tunnel that opens outward and is occupied by one s-cisC6-C7, all-trans BCR molecule. In the BCR absence, BBP accepts a range of xanthophylls, with reduced efficiency depending on the position and number of oxygen atoms, but rejects lycopene. The structure captures a pigment complex with a Takeout 1 protein and inspires potential applications of BBP as a BCR solubilizer.

Keywords: Takeout 1 domain; X-ray structure; body coloration; carotenoprotein; gregarious locusts; homodimer; hypsochromic shift; ligand specificity; tubular lipid-binding proteins; yellow protein.

MeSH terms

  • Animals
  • Binding Sites
  • Carotenoids / chemistry
  • Carotenoids / metabolism
  • Crystallography, X-Ray
  • Hydrophobic and Hydrophilic Interactions
  • Lycopene / chemistry
  • Lycopene / metabolism
  • Male
  • Models, Molecular*
  • Protein Binding*
  • Protein Multimerization
  • Solubility
  • Xanthophylls / chemistry
  • Xanthophylls / metabolism
  • beta Carotene* / chemistry
  • beta Carotene* / metabolism

Substances

  • beta Carotene
  • Carotenoids
  • Lycopene
  • Xanthophylls