Structure-function relationships in the four repeats of human interphotoreceptor retinoid-binding protein (IRBP)

Mol Vis. 1998 Dec 31:4:33.

Abstract

Purpose: Interphotoreceptor retinoid-binding protein (IRBP) binds hydrophobic ligands in the interphotoreceptor space. Human IRBP consists of 1230 amino acids in four 300 amino acid long repeats. We asked: 1. Whether each of the four repeats can bind retinoids or fatty acids, 2. Whether each repeat can prevent retinol degradation in aqueous solutions, 3. Whether a ligand can stabilize the protein from thermal denaturation, 4. Whether the four repeats can be further classified into two groups. Our rationale was to make each repeat from the human cDNA and then examine structural and functional characteristics.

Methods: Individual repeats were produced in E. coli and the whole protein was expressed in baculovirus. Binding properties with all-trans-retinol were characterized by ligand fluorescence enhancement. The quenching of protein fluorescence by retinol, 9-cis-retinal, all-trans-retinoic acid, beta-ionine, alpha-ionine, trans-parinaric acid, and DHA was also examined. Binding curves were analyzed by nonlinear regression. Prevention of retinol decomposition was measured by absorption spectroscopy. Circular dichroism was examined in the far UV range to study protein secondary structure and the near UV range to study ligand binding effects on the tryptophan environment.

Results: Temperature dependent denaturation suggests that EcR1 is the most stable of the four repeats. Each repeat possesses the capability of binding 9-cis-retinal, all-trans-retinol, all-trans retinoic acid, docosahexaenoic acid, alpha- and beta-ionine, and trans-parinaric acid. Protein fluorescence quenching by retinol and retinol fluorescence enhancement assays yielded similar binding parameters for each repeat. Each expressed repeat prevents the degradation of retinol in aqueous solutions.

Conclusions: The data contrast with the idea that two or more repeats are needed to bind one molecule of ligand. Each repeat binds both retinoids and analogs, suggesting that each has multiple ligand binding sites or one binding site with affinity for different ligands. Together, the results suggest that each repeat retains all functions of the whole protein. However, there are distinguishing characteristics among the repeats in their ligand binding properties, though the four repeats cannot be classified into just two distinctive groups. Last, these data fit well with the current model of multiple binding sites in IRBP derived from quadruplication of an ancestral monomeric binding protein.

Publication types

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

MeSH terms

  • Circular Dichroism
  • Eye Proteins*
  • Fatty Acids / metabolism*
  • Hot Temperature
  • Humans
  • Protein Binding
  • Protein Denaturation
  • Retinoids / metabolism*
  • Retinol-Binding Proteins / chemistry*
  • Retinol-Binding Proteins / metabolism*
  • Spectrometry, Fluorescence
  • Structure-Activity Relationship
  • Tryptophan / chemistry
  • Vitamin A / pharmacology

Substances

  • Eye Proteins
  • Fatty Acids
  • Retinoids
  • Retinol-Binding Proteins
  • interstitial retinol-binding protein
  • Vitamin A
  • Tryptophan