Cataract-causing G18V eliminates the antagonization by ATP against the crowding-induced destabilization of human γS-crystallin

Biochem Biophys Res Commun. 2020 Sep 24;530(3):554-560. doi: 10.1016/j.bbrc.2020.07.070. Epub 2020 Aug 1.

Abstract

In lens, ∼90% of ocular proteins are αβγ-crystallins with concentrations ≥400 mg/ml, which need to remain soluble for the whole life-span and their aggregation leads to cataract. The G18V mutation of human γS-crystallin causes hereditary childhood-onset cortical cataract. Mysteriously, despite being a metabolically-quiescent organ, lens maintains ATP concentrations of 3-7 mM. Very recently, we found that ATP has no significant binding to γS-crystallin as well as no alternation of its conformation. Nevertheless, ATP antagonizes the crowding-induced destabilization of γS-crystallin even at 1:1, most likely by interacting with the hydration shell. Here by DSF and NMR, we characterized the effect of ATP on binding, conformation, stability of G18V γS-crystallin and its interactions with α-crystallin. The results reveal: 1) G18V significantly accelerates the crowding-induced destabilization with Tm of 67 °C reduced to 50.5 °C at 1 mM. 2) Most unexpectedly, G18V almost completely eliminates the antagonizing effect of ATP against the crowding-induced destabilization. 3) ATP shows no significant effect on the interactions of α-crystallin with both WT and G18V γS-crystallin. Results together decode for the first time that G18V causes cataract not only by accelerating the crowding-induced destabilization, but also by eliminating the antagonizing effect of ATP against the crowding-induced destabilization.

Keywords: Adenosine triphosphate (ATP); Cataract-causing G18V mutant; Human eye lens; Molecular crowding; NMR spectroscopy; γS-crystallin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Cataract / genetics*
  • Cataract / metabolism
  • Humans
  • Models, Molecular
  • Point Mutation*
  • Protein Binding
  • Protein Conformation
  • Protein Interaction Maps
  • Protein Stability
  • Thermodynamics
  • alpha-Crystallins / metabolism
  • gamma-Crystallins / chemistry
  • gamma-Crystallins / genetics
  • gamma-Crystallins / metabolism*

Substances

  • alpha-Crystallins
  • gamma-Crystallins
  • CRYGS protein, human
  • Adenosine Triphosphate