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Dissecting the unique nucleotide specificity of mimivirus nucleoside diphosphate kinase.

Jeudy S, Lartigue A, Claverie JM, Abergel C
J Virol 83 7142-50 (2009)
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Cited: 12 times
EuropePMC logo PMID: 19439473

Abstract

The analysis of the Acanthamoeba polyphaga mimivirus genome revealed the first virus-encoded nucleoside diphosphate kinase (NDK), an enzyme that is central to the synthesis of RNA and DNA, ubiquitous in cellular organisms, and well conserved among the three domains of life. In contrast with the broad specificity of cellular NDKs for all types of ribo- and deoxyribonucleotides, the mimivirus enzyme exhibits a strongly preferential affinity for deoxypyrimidines. In order to elucidate the molecular basis of this unique substrate specificity, we determined the three-dimensional (3D) structure of the Acanthamoeba polyphaga mimivirus NDK alone and in complex with various nucleotides. As predicted from a sequence comparison with cellular NDKs, the 3D structure of the mimivirus enzyme exhibits a shorter Kpn loop, previously recognized as a main feature of the NDK active site. The structure of the viral enzyme in complex with various nucleotides also pinpointed two residue changes, both located near the active site and specific to the viral NDK, which could explain its stronger affinity for deoxynucleotides and pyrimidine nucleotides. The role of these residues was explored by building a set of viral NDK variants, assaying their enzymatic activities, and determining their 3D structures in complex with various nucleotides. A total of 26 crystallographic structures were determined at resolutions ranging from 2.8 A to 1.5 A. Our results suggest that the mimivirus enzyme progressively evolved from an ancestral NDK under the constraints of optimizing its efficiency for the replication of an AT-rich (73%) viral genome in a thymidine-limited host environment.

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  2. Dissecting the unique nucleotide specificity of mimivirus nucleoside diphosphate kinase. Jeudy S, Lartigue A, Claverie JM, Abergel C. J Virol 83 7142-7150 (2009)
  3. Hyper-cryptic marine meiofauna: species complexes in Nemertodermatida. Meyer-Wachsmuth I, Curini Galletti M, Jondelius U. PLoS One 9 e107688 (2014)


Reviews citing this publication (5)

  1. The rapidly expanding universe of giant viruses: Mimivirus, Pandoravirus, Pithovirus and Mollivirus. Abergel C, Legendre M, Claverie JM. FEMS Microbiol Rev 39 779-796 (2015)
  2. Mimivirus and its virophage. Claverie JM, Abergel C. Annu Rev Genet 43 49-66 (2009)
  3. Host Range and Coding Potential of Eukaryotic Giant Viruses. Sun TW, Yang CL, Kao TT, Wang TH, Lai MW, Ku C. Viruses 12 E1337 (2020)
  4. Horizontal gene transfers with or without cell fusions in all categories of the living matter. Sinkovics JG. Adv Exp Med Biol 714 5-89 (2011)
  5. Structure, Folding and Stability of Nucleoside Diphosphate Kinases. Georgescauld F, Song Y, Dautant A. Int J Mol Sci 21 E6779 (2020)

Articles citing this publication (4)

  1. Signaling transcript profile of the asexual intraerythrocytic development cycle of Plasmodium falciparum induced by melatonin and cAMP. Lima WR, Tessarin-Almeida G, Rozanski A, Parreira KS, Moraes MS, Martins DC, Hashimoto RF, Galante PAF, Garcia CRS. Genes Cancer 7 323-339 (2016)
  2. Substrate specificity and nucleotides binding properties of NM23H2/nucleoside diphosphate kinase homolog from Plasmodium falciparum. Kandeel M, Kitade Y. J Bioenerg Biomembr 42 361-369 (2010)
  3. Nucleoside diphosphate kinase and the activation of antiviral phosphonate analogs of nucleotides: binding mode and phosphorylation of tenofovir derivatives. Koch K, Chen Y, Feng JY, Borroto-Esoda K, Deville-Bonne D, Gallois-Montbrun S, Janin J, Moréra S. Nucleosides Nucleotides Nucleic Acids 28 776-792 (2009)
  4. Comparative genomic and biochemical analyses identify a collagen galactosylhydroxylysyl glucosyltransferase from Acanthamoeba polyphaga mimivirus. Wu W, Kim JS, Bailey AO, Russell WK, Richards SJ, Chen T, Chen T, Chen Z, Liang B, Yamauchi M, Guo H. Sci Rep 12 16806 (2022)


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