Editing of the Sendai Virus P/C MRNA by G Insertion Occurs During MRNA Synthesis Via a Virus-encoded Activity

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 1990 Jan 1

PMID 1688384

Citations 79

Authors

S Vidal

J Curran

D Kolakofsky

Affiliations

Soon will be listed here.

Abstract

Two forms of the Sendai virus P/C mRNA have been predicted: one an exact copy of the viral genome, and the other with a single G insertion within a run of three G's. We directly cloned the mRNA or portions of it containing the insertion site and screened the resulting colonies with oligonucleotides that could distinguish the presence of three or four G's at this position. We found that 31% of the mRNAs did in fact contain the predicted insertion, whereas the viral genomes contained no heterogeneity at this position. A smaller fraction (7%) of the mRNA contained two to eight G's inserted at this position. The insertions also took place during RNA synthesis in vitro with purified virions but were not detected when the mRNA was expressed in vivo via a vaccinia virus recombinant. When the Sendai virus- and vaccinia virus-derived P/C mRNAs were coexpressed in the same cells under conditions in which each could be distinguished, those from the Sendai genome were altered as before, but those from the vaccinia virus genome remained unaltered. The activity that alters the mRNA is therefore likely to be coded for by the virus and cannot function in trans.

Citing Articles

Recent Advances of Nipah Virus Disease: Pathobiology to Treatment and Vaccine Advancement.

Saha S, Bhattacharya M, Lee S, Chakraborty C J Microbiol. 2024; 62(10):811-828.

PMID: 39292378 DOI: 10.1007/s12275-024-00168-3.

Phylogenetic analysis of the promoter element 2 of paramyxo- and filoviruses.

Ashida S, Kojima S, Okura T, Kato F, Furuyama W, Urata S Microbiol Spectr. 2024; 12(5):e0041724.

PMID: 38606982 PMC: 11064532. DOI: 10.1128/spectrum.00417-24.

C Proteins Have a Common Origin and a Common Structural Organization.

Roy A, Chan Mine E, Gaifas L, Leyrat C, Volchkova V, Baudin F Biomolecules. 2023; 13(3).

PMID: 36979390 PMC: 10046310. DOI: 10.3390/biom13030455.

Nipah Virus Disease: Epidemiological, Clinical, Diagnostic and Legislative Aspects of This Unpredictable Emerging Zoonosis.

Bruno L, Nappo M, Ferrari L, Di Lecce R, Guarnieri C, Cantoni A Animals (Basel). 2023; 13(1).

PMID: 36611767 PMC: 9817766. DOI: 10.3390/ani13010159.

Ribosomal control in RNA virus-infected cells.

Wang X, Zhu J, Zhang D, Liu G Front Microbiol. 2022; 13:1026887.

PMID: 36419416 PMC: 9677555. DOI: 10.3389/fmicb.2022.1026887.

References

Benne R, van den Burg J, Brakenhoff J, Sloof P, VAN Boom J, Tromp M . Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell. 1986; 46(6):819-26. DOI: 10.1016/0092-8674(86)90063-2. View

Curran J, Kolakofsky D . Scanning independent ribosomal initiation of the Sendai virus Y proteins in vitro and in vivo. EMBO J. 1989; 8(2):521-6. PMC: 400836. DOI: 10.1002/j.1460-2075.1989.tb03406.x. View

Thomas S, Lamb R, PATERSON R . Two mRNAs that differ by two nontemplated nucleotides encode the amino coterminal proteins P and V of the paramyxovirus SV5. Cell. 1988; 54(6):891-902. PMC: 7133244. DOI: 10.1016/s0092-8674(88)91285-8. View

Feagin J, Abraham J, Stuart K . Extensive editing of the cytochrome c oxidase III transcript in Trypanosoma brucei. Cell. 1988; 53(3):413-22. DOI: 10.1016/0092-8674(88)90161-4. View

Shaw J, Feagin J, Stuart K, Simpson L . Editing of kinetoplastid mitochondrial mRNAs by uridine addition and deletion generates conserved amino acid sequences and AUG initiation codons. Cell. 1988; 53(3):401-11. DOI: 10.1016/0092-8674(88)90160-2. View

McGinnes L, McQuain C, Morrison T . The P protein and the nonstructural 38K and 29K proteins of Newcastle disease virus are derived from the same open reading frame. Virology. 1988; 164(1):256-64. DOI: 10.1016/0042-6822(88)90643-5. View

PATERSON R, Harris T, Lamb R . Analysis and gene assignment of mRNAs of a paramyxovirus, simian virus 5. Virology. 1984; 138(2):310-23. DOI: 10.1016/0042-6822(84)90354-4. View

Chen S, Habib G, Yang C, Gu Z, Lee B, Weng S . Apolipoprotein B-48 is the product of a messenger RNA with an organ-specific in-frame stop codon. Science. 1987; 238(4825):363-6. DOI: 10.1126/science.3659919. View

Powell L, Wallis S, Pease R, Edwards Y, Knott T, Scott J . A novel form of tissue-specific RNA processing produces apolipoprotein-B48 in intestine. Cell. 1987; 50(6):831-40. DOI: 10.1016/0092-8674(87)90510-1. View

10.

Sato H, Ishida N, Imamura Y, Hattori S, Kawakita M . Molecular cloning and nucleotide sequence of P, M and F genes of Newcastle disease virus avirulent strain D26. Virus Res. 1987; 7(3):241-55. DOI: 10.1016/0168-1702(87)90031-1. View

11.

Feagin J, Jasmer D, Stuart K . Developmentally regulated addition of nucleotides within apocytochrome b transcripts in Trypanosoma brucei. Cell. 1987; 49(3):337-45. DOI: 10.1016/0092-8674(87)90286-8. View

12.

Bellini W, Englund G, Rozenblatt S, Arnheiter H, Richardson C . Measles virus P gene codes for two proteins. J Virol. 1985; 53(3):908-19. PMC: 254726. DOI: 10.1128/JVI.53.3.908-919.1985. View

13.

Hamaguchi M, Yoshida T, Nishikawa K, Naruse H, Nagai Y . Transcriptive complex of Newcastle disease virus. I. Both L and P proteins are required to constitute an active complex. Virology. 1983; 128(1):105-17. DOI: 10.1016/0042-6822(83)90322-7. View

14.

Giorgi C, Blumberg B, Kolakofsky D . Sendai virus contains overlapping genes expressed from a single mRNA. Cell. 1983; 35(3 Pt 2):829-36. DOI: 10.1016/0092-8674(83)90115-0. View

15.

Shioda T, Hidaka Y, Kanda T, Shibuta H, Nomoto A, Iwasaki K . Sequence of 3,687 nucleotides from the 3' end of Sendai virus genome RNA and the predicted amino acid sequences of viral NP, P and C proteins. Nucleic Acids Res. 1983; 11(21):7317-30. PMC: 326485. DOI: 10.1093/nar/11.21.7317. View

16.

Collins P, Wertz G, Ball L, Hightower L . Coding assignments of the five smaller mRNAs of Newcastle disease virus. J Virol. 1982; 43(3):1024-31. PMC: 256213. DOI: 10.1128/JVI.43.3.1024-1031.1982. View

17.

Roux L, Holland J . Role of defective interfering particles of Sendai virus in persistent infections. Virology. 1979; 93(1):91-103. DOI: 10.1016/0042-6822(79)90278-2. View

18.

Kolakofsky D, Altman S . Endoribonuclease activity associated with animal RNA viruses. J Virol. 1978; 25(1):274-84. PMC: 353924. DOI: 10.1128/JVI.25.1.274-284.1978. View

19.

Peluso R, Lamb R, Choppin P . Polypeptide synthesis in simian virus 5-infected cells. J Virol. 1977; 23(1):177-87. PMC: 515813. DOI: 10.1128/JVI.23.1.177-187.1977. View

20.

Curran J, Kolakofsky D . Scanning independent ribosomal initiation of the Sendai virus X protein. EMBO J. 1988; 7(9):2869-74. PMC: 457080. DOI: 10.1002/j.1460-2075.1988.tb03143.x. View