Rescue of the temperature-sensitive, autosomal-recessive mutation R298S in the sodium-bicarbonate cotransporter NBCe1-A characterized by a weakened dimer and abnormal aggregation

Biochim Biophys Acta. 2015 Jun;1850(6):1286-96. doi: 10.1016/j.bbagen.2015.02.014. Epub 2015 Mar 3.

Abstract

Background: Band keratopathy, an ocular disease that is characterized by hypercalcemia and opaque bands across the cornea, has been associated with kidney disease. Type-II renal tubular acidosis (RTA), a condition in which the kidneys fail to recover bicarbonate (HCO3-) in the proximal tubule of the nephron, results in HCO3- wastage in the urine and low blood pH. The development of these diseases is associated with autosomal-recessive mutations in the Na+-coupled HCO3- cotransporter NBCe1-A located at the basolateral membranes of either cell type.

Methods: We provide insight into the devastating R298S mutation found in type-II RTA-afflicted individuals using confocal-microscopy imaging of fluorescently-tagged NBCe1-A and NBCe1-A-R298S molecules expressed in human corneal endothelial and proximal tubule cells and from in-depth biophysical studies of their cytoplasmic N-terminal domains (Nt and Nt-R298S), including Nt crystal structure, melting-temperature, and homodimer dissociation constant (KD) analyses.

Results: We illuminate and rescue trafficking defects of the R298S mutation of NBCe1-A. The KD for Nt monomer-dimer equilibrium is established. The KD for Nt-R298S is significantly higher, but immeasurable due to environmental factors (pH, temperature, concentration) that result in dimer instability leading to precipitation. The crystal structure of Nt-dimer shows that R298 is part of a putative substrate conduit and resides near the dimer interface held together by hydrogen-bond networks.

Conclusions: The R298S is a temperature-sensitive mutation in Nt that results in instability of the colloidal system leading to abnormal aggregation.

General significance: Our findings provide new perspectives to the aberrant mechanism of certain ocular pathologies and type-II RTA associated with the R298S mutation.

Keywords: Composition-gradient light scattering; Confocal microscopy; Protein aggregation; X-ray crystallography.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Cell Line
  • Colloids
  • Computer Simulation
  • Endothelium, Corneal / metabolism*
  • Genotype
  • Humans
  • Hydrogen Bonding
  • Kidney Tubules, Proximal / metabolism*
  • Kinetics
  • Models, Chemical
  • Models, Molecular
  • Mutation*
  • Phenotype
  • Protein Aggregates
  • Protein Conformation
  • Protein Denaturation
  • Protein Multimerization
  • Protein Stability
  • Protein Transport
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Sodium-Bicarbonate Symporters / chemistry
  • Sodium-Bicarbonate Symporters / genetics*
  • Sodium-Bicarbonate Symporters / metabolism*
  • Transfection
  • Transition Temperature*

Substances

  • Colloids
  • Protein Aggregates
  • Recombinant Fusion Proteins
  • SLC4A4 protein, human
  • Sodium-Bicarbonate Symporters