The crystal structure of phenylalanyl-tRNA synthetase from Thermus thermophilus complexed with cognate tRNA(Phe)

Yehuda Goldgur, Lidia Mosyak, Ludmila Reshetnikova, Valentina Ankilova, Olga Lavrik, Svetlana Khodyreva, Mark Safro

Research output: Contribution to journalArticlepeer-review

187 Scopus citations

Abstract

Background: In the translation of the genetic code each aminoacyl-tRNA synthetase (aaRS) must recognize its own (cognate) tRNA and attach the corresponding amino acid to the acceptor end of tRNA, discriminating all the others. The (αβ)2 phenylalanyl-tRNA synthetase (PheRS) is one of the most complex enzymes in the aaRS family and is characterized by anomalous charging properties. Structurally, the enzyme belongs to class II aaRSs, as its catalytic domain is built around an antiparallel β sheet, but functionally it resembles class I as it aminoacylates the 2'OH of the terminal ribose of tRNA (class II aaRSs aminoacylate the 3'OH). With the availability of the three-dimensional structure of the complex between multisubunit PheRS and tRNA(Phe), a fuller picture of the specific tRNA-aaRS interactions is beginning to emerge. Results: The crystal structure of Thermus thermophilus PheRS complexed with cognate tRNA has been solved at 3.28 Å resolution. It reveals that one tRNA(Phe) molecule binds across all four PheRS subunits. The interactions of PheRS with tRNA stabilize the flexible N-terminal part of the α subunit, which appeared to form the enzyme's 11th domain, comprising a coiled-coil structure (helical arm) built up of two long antiparallel α helices. The helical arms are similar to those observed in SerRS and are in the same relative orientation with respect to the catalytic domain. Anticodon recognition upon tRNA binding is performed by the B8 domain, the structure of which is similar to that of the RNA-binding domain (RBD) of the small spliceosomal protein U1A. The Th. thermophilus PheRS approaches the anticodon loop from the minor groove side. Conclusions: The mode of interaction with tRNA explains the absolute necessity for the (αβ)2 architecture of PheRS. The interactions of tRNA(Phe) with PheRS and particularly with the coiled-coil domain of the α subunit result in conformational changes in TΨC and D loops seen by comparison with uncomplexed yeast tRNA(Phe). The tRNA(Phe) is a newly recognized type of RNA molecule specifically interacting with the RBD fold. In addition, a new type of anticodon-binding domain emerges in the aaRS family. The uniqueness of PheRS in charging 2'OH of tRNA is dictated by the size of its adenine-binding pocket and by the local conformation of the tRNA's CCA end.

Original languageEnglish
Pages (from-to)59-68
Number of pages10
JournalStructure
Volume5
Issue number1
DOIs
StatePublished - 15 Jan 1997
Externally publishedYes

Keywords

  • X-ray crystallography
  • complex
  • phenylalanyl-tRNA synthetase
  • recognition
  • tRNA(Phe)

ASJC Scopus subject areas

  • Structural Biology
  • Molecular Biology

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