Protein Nucleotidylylation in +ssRNA Viruses

Overview

Journal Viruses

Publisher MDPI

Specialty Microbiology

Date 2021 Aug 28

PMID 34452414

Citations 5

Authors

Alice-Roza Eruera

Alice M McSweeney

Geena M McKenzie-Goldsmith

Vernon K Ward

Affiliations

Soon will be listed here.

Abstract

Nucleotidylylation is a post-transcriptional modification important for replication in the picornavirus supergroup of RNA viruses, including members of the , , and virus families. This modification occurs when the RNA-dependent RNA polymerase (RdRp) attaches one or more nucleotides to a target protein through a nucleotidyl-transferase reaction. The most characterized nucleotidylylation target is VPg (viral protein genome-linked), a protein linked to the 5' end of the genome in , and . The nucleotidylylation of VPg by RdRp is a critical step for the VPg protein to act as a primer for genome replication and, in and for the initiation of translation. In contrast, do not express a VPg protein, but the nucleotidylylation of proteins involved in replication initiation is critical for genome replication. Furthermore, the RdRp proteins of the viruses that perform nucleotidylylation are themselves nucleotidylylated, and in the case of coronavirus, this has been shown to be essential for viral replication. This review focuses on nucleotidylylation within the picornavirus supergroup of viruses, including the proteins that are modified, what is known about the nucleotidylylation process and the roles that these modifications have in the viral life cycle.

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References

Payne D, Vinje J, Szilagyi P, Edwards K, Staat M, Weinberg G . Norovirus and medically attended gastroenteritis in U.S. children. N Engl J Med. 2013; 368(12):1121-30. PMC: 4618551. DOI: 10.1056/NEJMsa1206589. View

Rantalainen K, Uversky V, Permi P, Kalkkinen N, Dunker A, Makinen K . Potato virus A genome-linked protein VPg is an intrinsically disordered molten globule-like protein with a hydrophobic core. Virology. 2008; 377(2):280-8. PMC: 2796300. DOI: 10.1016/j.virol.2008.04.025. View

Murphy J, Rychlik W, Rhoads R, Hunt A, Shaw J . A tyrosine residue in the small nuclear inclusion protein of tobacco vein mottling virus links the VPg to the viral RNA. J Virol. 1991; 65(1):511-3. PMC: 240548. DOI: 10.1128/JVI.65.1.511-513.1991. View

Zhou Z, Qiu Y, Ge X . The taxonomy, host range and pathogenicity of coronaviruses and other viruses in the order. Anim Dis. 2021; 1(1):5. PMC: 8062217. DOI: 10.1186/s44149-021-00005-9. View

Kuhn J, Lauck M, Bailey A, Shchetinin A, Vishnevskaya T, Bao Y . Reorganization and expansion of the nidoviral family Arteriviridae. Arch Virol. 2015; 161(3):755-68. PMC: 5573231. DOI: 10.1007/s00705-015-2672-z. View

Belliot G, Sosnovtsev S, Chang K, McPhie P, Green K . Nucleotidylylation of the VPg protein of a human norovirus by its proteinase-polymerase precursor protein. Virology. 2008; 374(1):33-49. PMC: 2386983. DOI: 10.1016/j.virol.2007.12.028. View

Murray K, Barton D . Poliovirus CRE-dependent VPg uridylylation is required for positive-strand RNA synthesis but not for negative-strand RNA synthesis. J Virol. 2003; 77(8):4739-50. PMC: 152113. DOI: 10.1128/jvi.77.8.4739-4750.2003. View

Fuentes C, Bosch A, Pinto R, Guix S . Identification of human astrovirus genome-linked protein (VPg) essential for virus infectivity. J Virol. 2012; 86(18):10070-8. PMC: 3446559. DOI: 10.1128/JVI.00797-12. View

Hosmillo M, Chaudhry Y, Kim D, Goodfellow I, Cho K . Sapovirus translation requires an interaction between VPg and the cap binding protein eIF4E. J Virol. 2014; 88(21):12213-21. PMC: 4248917. DOI: 10.1128/JVI.01650-14. View

10.

Yang Y, Rijnbrand R, Watowich S, Lemon S . Genetic evidence for an interaction between a picornaviral cis-acting RNA replication element and 3CD protein. J Biol Chem. 2004; 279(13):12659-67. DOI: 10.1074/jbc.M312992200. View

11.

Machin A, Martin Alonso J, Dalton K, Parra F . Functional differences between precursor and mature forms of the RNA-dependent RNA polymerase from rabbit hemorrhagic disease virus. J Gen Virol. 2009; 90(Pt 9):2114-8. DOI: 10.1099/vir.0.011296-0. View

12.

Wylie S, Adams M, Chalam C, Kreuze J, Lopez-Moya J, Ohshima K . ICTV Virus Taxonomy Profile: Potyviridae. J Gen Virol. 2017; 98(3):352-354. PMC: 5797945. DOI: 10.1099/jgv.0.000740. View

13.

Han K, Choi Y, Min B, Jeong H, Cheon D, Kim J . Murine norovirus-1 3Dpol exhibits RNA-dependent RNA polymerase activity and nucleotidylylates on Tyr of the VPg. J Gen Virol. 2010; 91(Pt 7):1713-22. DOI: 10.1099/vir.0.020461-0. View

14.

Lama J, Paul A, Harris K, Wimmer E . Properties of purified recombinant poliovirus protein 3aB as substrate for viral proteinases and as co-factor for RNA polymerase 3Dpol. J Biol Chem. 1994; 269(1):66-70. View

15.

Hemming M, Rasanen S, Huhti L, Paloniemi M, Salminen M, Vesikari T . Major reduction of rotavirus, but not norovirus, gastroenteritis in children seen in hospital after the introduction of RotaTeq vaccine into the National Immunization Programme in Finland. Eur J Pediatr. 2013; 172(6):739-46. PMC: 7086648. DOI: 10.1007/s00431-013-1945-3. View

16.

Kelley L, Mezulis S, Yates C, Wass M, Sternberg M . The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc. 2015; 10(6):845-58. PMC: 5298202. DOI: 10.1038/nprot.2015.053. View

17.

Lobert P, Escriou N, Ruelle J, Michiels T . A coding RNA sequence acts as a replication signal in cardioviruses. Proc Natl Acad Sci U S A. 1999; 96(20):11560-5. PMC: 18073. DOI: 10.1073/pnas.96.20.11560. View

18.

Egloff M, Ferron F, Campanacci V, Longhi S, Rancurel C, Dutartre H . The severe acute respiratory syndrome-coronavirus replicative protein nsp9 is a single-stranded RNA-binding subunit unique in the RNA virus world. Proc Natl Acad Sci U S A. 2004; 101(11):3792-6. PMC: 374323. DOI: 10.1073/pnas.0307877101. View

19.

Sievers F, Wilm A, Dineen D, Gibson T, Karplus K, Li W . Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011; 7:539. PMC: 3261699. DOI: 10.1038/msb.2011.75. View

20.

Leen E, Kwok K, Birtley J, Simpson P, Subba-Reddy C, Chaudhry Y . Structures of the compact helical core domains of feline calicivirus and murine norovirus VPg proteins. J Virol. 2013; 87(10):5318-30. PMC: 3648151. DOI: 10.1128/JVI.03151-12. View