Zinc is the molecular "switch" that controls the catalytic cycle of bacterial leucyl-tRNA synthetase

J Inorg Biochem. 2015 Jan:142:59-67. doi: 10.1016/j.jinorgbio.2014.09.006. Epub 2014 Sep 22.

Abstract

The Escherichia coli (E. coli) leucyl-tRNA synthetase (LeuRS) enzyme is part of the aminoacyl-tRNA synthetase (aaRS) family. LeuRS is an essential enzyme that relies on specialized domains to facilitate the aminoacylation reaction. Herein, we have biochemically characterized a specialized zinc-binding domain 1 (ZN-1). We demonstrate that the ZN-1 domain plays a central role in the catalytic cycle of E. coli LeuRS. The ZN-1 domain, when associated with Zn(2+), assumes a rigid architecture that is stabilized by thiol groups from the residues C159, C176 and C179. When LeuRS is in the aminoacylation complex, these cysteine residues form an equilateral planar triangular configuration with Zn(2+), but when LeuRS transitions to the editing conformation, this geometric configuration breaks down. By generating a homology model of LeuRS while in the editing conformation, we conclude that structural changes within the ZN-1 domain play a central role in LeuRS's catalytic cycle. Additionally, we have biochemically shown that C159, C176 and C179 coordinate Zn(2+) and that this interaction is essential for leucylation to occur, but is not essential for deacylation. Furthermore, calculated Kd values indicate that the wild-type enzyme binds Zn(2+) to a greater extent than any of the mutant LeuRSs. Lastly, we have shown through secondary structural analysis of our LeuRS enzymes that Zn(2+) is an architectural cornerstone of the ZN-1 domain and that without its geometric coordination the domain collapses. We believe that future research on the ZN-1 domain may reveal a possible Zn(2+) dependent translocation mechanism for charged tRNA(Leu).

Keywords: Aminoacylation reaction; Leucyl-tRNA synthetase; ZN-1 domain.

MeSH terms

  • Aminoacyltransferases / chemistry*
  • Aminoacyltransferases / metabolism
  • Catalysis
  • Escherichia coli / enzymology*
  • Escherichia coli Proteins / chemistry*
  • Escherichia coli Proteins / metabolism
  • Protein Domains
  • RNA, Bacterial / chemistry*
  • RNA, Bacterial / metabolism
  • RNA, Transfer, Leu / chemistry*
  • RNA, Transfer, Leu / metabolism
  • Zinc / chemistry*
  • Zinc / metabolism

Substances

  • Escherichia coli Proteins
  • RNA, Bacterial
  • RNA, Transfer, Leu
  • Aminoacyltransferases
  • leucyltransferase
  • Zinc