The cystic fibrosis transmembrane conductance regulator. Overexpression, purification, and characterization of wild type and delta F508 mutant forms of the first nucleotide binding fold in fusion with the maltose-binding protein

J Biol Chem. 1993 Nov 15;268(32):24330-8.

Abstract

The first nucleotide binding fold (NBF1) of the cystic fibrosis transmembrane conductance regulator (CFTR) and its disease-causing mutant form (delta F508,NBF1) were overexpressed in high yield in Escherichia coli in fusion with the maltose-binding protein (MBP). The rationale for producing the chimerae was to aid in domain purification, solubilization, and crystallization and to examine the effect of protein-protein interactions on the properties of the mutant NBF1. Both the purified wild type and delta F508 mutant fusion proteins fold into functional nucleotide binding domains as determined by using the fluorescent nucleotide analog TNP-ATP (2'-(3')-O-(2,4,6-trinitrophenyl)adenosine-5'-triphosphate). Moreover, the prominent secondary structural features of the two proteins as assessed by ultraviolet circular dichroism spectropolarimetry are very similar, as is the higher order structure evident in three separate protease digestion patterns. Finally, the stability of the nucleotide binding function of the two proteins is similar as assessed by sensitivity to urea. Gel filtration chromatography and electron and confocal microscopy reveal that both fusion proteins, but not MBP alone, form organized fibers, suggesting that NBF1 self-associates, thus raising the possibility that CFTR may be oligomeric in the plasma membrane. Significantly, in the presence of high salt, these fusion proteins also have a propensity to form microcrystals. Finally, the two separate domains (NBF1 and MBP) constituting the fusion proteins appear to interact quite strongly as both proteins remain associated even after cleavage of their fusion junction. The possible relevance of these novel findings to those approaches that might be taken to elucidate the three-dimensional structural differences between the wild type and delta F508 mutant forms of CFTR, as well as to ameliorate the severity of cystic fibrosis, is discussed.

Publication types

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

MeSH terms

  • ATP-Binding Cassette Transporters*
  • Adenosine Triphosphate / analogs & derivatives
  • Base Sequence
  • Binding Sites
  • Carrier Proteins / metabolism*
  • Chromatography, Gel
  • Cloning, Molecular
  • Crystallization
  • Cystic Fibrosis / genetics*
  • Cystic Fibrosis Transmembrane Conductance Regulator
  • DNA Primers
  • Electrophoresis, Polyacrylamide Gel
  • Escherichia coli / genetics
  • Escherichia coli Proteins*
  • Hydrolysis
  • Maltose-Binding Proteins
  • Membrane Proteins / genetics*
  • Membrane Proteins / isolation & purification
  • Membrane Proteins / metabolism
  • Microscopy, Electron
  • Molecular Sequence Data
  • Monosaccharide Transport Proteins*
  • Mutation*
  • Nucleotides / metabolism*
  • Protein Denaturation
  • Recombinant Fusion Proteins / metabolism
  • Recombinant Fusion Proteins / ultrastructure

Substances

  • ATP-Binding Cassette Transporters
  • Carrier Proteins
  • DNA Primers
  • Escherichia coli Proteins
  • Maltose-Binding Proteins
  • Membrane Proteins
  • Monosaccharide Transport Proteins
  • Nucleotides
  • Recombinant Fusion Proteins
  • maltose transport system, E coli
  • Cystic Fibrosis Transmembrane Conductance Regulator
  • 2',3'-O-(2,4,6-trinitro-cyclohexadienylidine)adenosine 5'-triphosphate
  • Adenosine Triphosphate