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tRNA(His) guanylyltransferase (THG1), a unique 3'-5' nucleotidyl transferase, shares unexpected structural homology with canonical 5'-3' DNA polymerases.

Hyde SJ, Eckenroth BE, Smith BA, Eberley WA, Heintz NH, Jackman JE, Doublié S
Proc Natl Acad Sci U S A 107 20305-10 (2010)
Related entries: 3otc, 3otd, 3ote

Cited: 46 times
EuropePMC logo PMID: 21059936

Abstract

All known DNA and RNA polymerases catalyze the formation of phosphodiester bonds in a 5' to 3' direction, suggesting this property is a fundamental feature of maintaining and dispersing genetic information. The tRNA(His) guanylyltransferase (Thg1) is a member of a unique enzyme family whose members catalyze an unprecedented reaction in biology: 3'-5' addition of nucleotides to nucleic acid substrates. The 2.3-Å crystal structure of human THG1 (hTHG1) reported here shows that, despite the lack of sequence similarity, hTHG1 shares unexpected structural homology with canonical 5'-3' DNA polymerases and adenylyl/guanylyl cyclases, two enzyme families known to use a two-metal-ion mechanism for catalysis. The ability of the same structural architecture to catalyze both 5'-3' and 3'-5' reactions raises important questions concerning selection of the 5'-3' mechanism during the evolution of nucleotide polymerases.

Reviews - 3otb mentioned but not cited (1)

  1. Doing it in reverse: 3'-to-5' polymerization by the Thg1 superfamily. Jackman JE, Gott JM, Gray MW. RNA 18 886-899 (2012)

Articles - 3otb mentioned but not cited (5)

  1. tRNA(His) guanylyltransferase (THG1), a unique 3'-5' nucleotidyl transferase, shares unexpected structural homology with canonical 5'-3' DNA polymerases. Hyde SJ, Eckenroth BE, Smith BA, Eberley WA, Heintz NH, Jackman JE, Doublié S. Proc. Natl. Acad. Sci. U.S.A. 107 20305-20310 (2010)
  2. tRNAHis-guanylyltransferase establishes tRNAHis identity. Heinemann IU, Nakamura A, O'Donoghue P, Eiler D, Söll D. Nucleic Acids Res. 40 333-344 (2012)
  3. Structural studies of a bacterial tRNA(HIS) guanylyltransferase (Thg1)-like protein, with nucleotide in the activation and nucleotidyl transfer sites. Hyde SJ, Rao BS, Eckenroth BE, Jackman JE, Doublié S. PLoS ONE 8 e67465 (2013)
  4. Published Erratum Correction to 'Human Thg1 displays tRNA-inducible GTPase activity'. Nucleic Acids Res 50 11992 (2022)
  5. Human Thg1 displays tRNA-inducible GTPase activity. Antika TR, Nazilah KR, Lee YH, Lo YT, Yeh CS, Yeh FL, Chang TH, Wang TL, Wang CC. Nucleic Acids Res 50 10015-10025 (2022)


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  2. Structural and mechanistic insights into guanylylation of RNA-splicing ligase RtcB joining RNA between 3'-terminal phosphate and 5'-OH. Englert M, Xia S, Okada C, Nakamura A, Tanavde V, Yao M, Eom SH, Konigsberg WH, Söll D, Wang J. Proc. Natl. Acad. Sci. U.S.A. 109 15235-15240 (2012)
  3. Structures of the noncanonical RNA ligase RtcB reveal the mechanism of histidine guanylylation. Desai KK, Bingman CA, Phillips GN, Raines RT. Biochemistry 52 2518-2525 (2013)
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  12. Mitochondrial tRNA 5'-editing in Dictyostelium discoideum and Polysphondylium pallidum. Abad MG, Long Y, Long Y, Kinchen RD, Schindel ET, Gray MW, Jackman JE. J. Biol. Chem. 289 15155-15165 (2014)
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  19. Crystal structure of tRNAHis guanylyltransferase from Saccharomyces cerevisiae. Lee K, Lee EH, Son J, Hwang KY. Biochem. Biophys. Res. Commun. 490 400-405 (2017)
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  22. In vitro substrate specificities of 3'-5' polymerases correlate with biological outcomes of tRNA 5'-editing reactions. Long Y, Long Y, Jackman JE. FEBS Lett. 589 2124-2130 (2015)
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  27. Chemical footprinting and kinetic assays reveal dual functions for highly conserved eukaryotic tRNAHis guanylyltransferase residues. Matlock AO, Smith BA, Jackman JE. J Biol Chem 294 8885-8893 (2019)
  28. Compound heterozygous variants of THG1L result in autosomal recessive cerebellar ataxia. Han R, Chu M, Gao J, Wang J, Wang M, Ma Y, Jia T, Zhang X. J Hum Genet (2023)
  29. Fidelity of base-pair recognition by a 3'-5' polymerase: mechanism of the Saccharomyces cerevisiae tRNAHis guanylyltransferase. Patel KJ, Yourik P, Jackman JE. RNA 27 683-693 (2021)
  30. Recognition of tRNAHis in an RNase P-Free Nanoarchaeum. Ivanesthi IR, Rida GRN, Setiawibawa AA, Tseng YK, Muammar A, Wang CC. Microbiol Spectr e0462122 (2023)


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