Skip to main content
NCBI home page
Elsevier - PMC COVID-19 Collection logoLink to Elsevier - PMC COVID-19 Collection
. 2004 Feb 10;186(2):543–550. doi: 10.1016/0042-6822(92)90020-P

RNA editing in the phosphoprotein gene of the human parainfluenza virus type 3

Mark S Galinski 1, Roberta M Troy 1, Amiya K Banerjee 1
PMCID: PMC7130814  PMID: 1310183

Abstract

RNA editing of the human parainfluenza virus type 3 (HPIV3) phosphoprotein (P) gene was found to occur for the accession of an alternate discontinuous cistron. Editing occurred within a purine-rich sequence (AAUUAAAAAAGGGGG) found at the mRNA nucleotides 791–805. This sequence resembles an HPIV3 consensus transcription termination sequence and is located at the 5′-end of the putative D protein coding sequences. Editing at an alternate site (AAUUGGAAAGGAAAGG), mRNA nucleotides 1121–1136, for accession of a conserved V cistron, which is present in a number of paramyxovirus P genes, was not found to occur in HPIV3. In contrast with many other paramyxoviruses, editing was indiscriminate with the insertion of 1–12 additional G residues not present in the gene template. RNA editing was found to occur in both in vivo (HPIV3 infected cells) and in vitro (purified nucleocapsid complexes) synthesized mRNAs. Further, the in vitro prepared mRNA was edited regardless of whether the nucleocapsid complexes were transcribed in the presence or absence of uninfected human lung carcinoma (HLC) cell lysates. These results support the notion that RNA editing appears to be exclusively a function of viral proteins.

References

  1. Bellini W.J., Englund G., Rozenblatt S., Arnheiter H., Richardson C.D. Measles virus P gene codes for two proteins. J. Virol. 1985;53:908–919. doi: 10.1128/jvi.53.3.908-919.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bonner W.M., Laskey R.A. A film detection method for tritium-labeled proteins and nucleic acids in polyacrylamide gels. Eur. J. Biochem. 1974;46:83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  3. Brierley I., Digard P., Inglis S.C. Characterization of an efficient coronavirus ribosomal frameshifting signal: Requirement for an RNA pseudoknot. Cell. 1989;57:537–547. doi: 10.1016/0092-8674(89)90124-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cattaneo R., Kaelin K., Baczko K., Billeter M.A. Measles virus editing provides an additional cysteine-rich protein. Cell. 1989;56:759–764. doi: 10.1016/0092-8674(89)90679-x. [DOI] [PubMed] [Google Scholar]
  5. Chinchar V.G., Portner A. Functions of Sendai virus nucleocapsid polypeptides: Enzymatic activities in nucleocapsids following cleavage of polypeptide P by Staphylococcus aureus protease V8. Virology. 1981;109:59–71. doi: 10.1016/0042-6822(81)90471-2. [DOI] [PubMed] [Google Scholar]
  6. Craigen W.J., Caskey C.T. Translational frameshifting: Where will it stop? Cell. 1987;50:1–2. doi: 10.1016/0092-8674(87)90652-0. [DOI] [PubMed] [Google Scholar]
  7. De B.P., Galinski M.S., Banerjee A.K. Characterization of an in vitro system for the synthesis of mRNA from human parainfluenza virus type 3. J. Virol. 1990;64:1135–1142. doi: 10.1128/jvi.64.3.1135-1142.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. De B.P., Lesoon A., Banerjee A.K. Human parainfluenza virus type 3 transcription in vitro: role of cellular actin in mRNA synthesis. J. Virol. 1991;65:3268–3275. doi: 10.1128/jvi.65.6.3268-3275.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Deshpande K.L., Portner A. Monoclonal antibodies to the P protein of Sendai virus define its structure and role in transcription. Virology. 1985;140:125–134. doi: 10.1016/0042-6822(85)90451-9. [DOI] [PubMed] [Google Scholar]
  10. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic-Acids Res. 1984;12:387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Elliott G.D., Yeo R.P., Afzal M.A., Simpson E.I.B., Curran J.A., Rima B.K. Strain variable editing during transcription of the P gene of mumps virus may lead to the generation of non-structural proteins NS1 (V) and NS2. J. Gen. Virol. 1990;71:1555–1560. doi: 10.1099/0022-1317-71-7-1555. [DOI] [PubMed] [Google Scholar]
  12. Galinski M.S. Paramyxoviridae: Transcription and replication. In: Maramorosch K., Murphy F.A., Shatkin A.J., editors. Vol. 39. Academic Press; San Diego: 1991. pp. 129–162. (Advances in Virus Research). [DOI] [PubMed] [Google Scholar]
  13. Galinski M.S., Mink M.A., Lambert D.M., Wechsler S.W., Pons M.W. Molecular cloning and sequence analysis of the human parainfluenza 3 virus RNA encoding the nucleocapsid protein. Virology. 1986;149:139–151. doi: 10.1016/0042-6822(86)90116-9. [DOI] [PubMed] [Google Scholar]
  14. Galinski M.S., Mink M.A., Lambert D.M., Wechsler S.L., Pons M.W. Molecular cloning and sequence analysis of the human parainfluenza 3 virus mRNA encoding the P and C proteins. Virology. 1986;154:46–60. doi: 10.1016/0042-6822(86)90167-4. [DOI] [PubMed] [Google Scholar]
  15. Galinski M.S., Wechsler S.L. The molecular biology of the Paramyxovirus genus. In: Kingsbury D.W., editor. The Paramyxoviruses. Plenum Press; New York: 1991. pp. 41–82. [Google Scholar]
  16. Galinski M.S., Stanik V.H., Rohrmann G.F., Beaudreau G.S. Comparison of sequence diversity in several cytoplasmic polyhedrosis viruses. Virology. 1983;130:372–380. doi: 10.1016/0042-6822(83)90091-0. [DOI] [PubMed] [Google Scholar]
  17. Giorgi C., Blumberg B.M., Kolakofsky D. Sendai virus contains overlapping genes expressed from a single mRNA. Cell. 1983;35:829–836. doi: 10.1016/0092-8674(83)90115-0. [DOI] [PubMed] [Google Scholar]
  18. 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;128:105–117. doi: 10.1016/0042-6822(83)90322-7. [DOI] [PubMed] [Google Scholar]
  19. Kingsbury D.W. Paramyxoviridae and their replication. In: Fields B.N., Knipe D.M., editors. Virology. 2nd ed. Raven Press; New York: 1990. pp. 945–962. [Google Scholar]
  20. Kingsbury D.W. Plenum Press; New York: 1991. The Paramyxoviruses. [Google Scholar]
  21. Konarska M.M., Padgett R.A., Sharp P.A. Recognition of cap structure in splicing in vitro of mRNA. Cell. 1984;38:731–736. doi: 10.1016/0092-8674(84)90268-x. [DOI] [PubMed] [Google Scholar]
  22. Kondo K., Bando H., Tsurudome M., Kawano M., Nishio M., Ito Y. Sequence analysis of the phosphoprotein (P) genes of human parainfluenza type 4A and 4B viruses and RNA editing at transcript of the P genes: The number of G residues added is imprecise. Virology. 1990;178:321–326. doi: 10.1016/0042-6822(90)90413-l. [DOI] [PubMed] [Google Scholar]
  23. Luk D., Sanchez A., Banerjee A.K. Messenger RNA encoding the phosphoprotein (P) of human parainfluenza virus 3 is bicistronic. Virology. 1986;153:318–325. doi: 10.1016/0042-6822(86)90036-x. [DOI] [PubMed] [Google Scholar]
  24. Maizel J.V., Jr . Polyacrylamide gel electrophoresis of viral proteins. In: Maramorosch K., Koprowski H., editors. Methods in Virology. Academic Press; New York: 1971. pp. 179–246. [Google Scholar]
  25. Matsuoka Y., Curran J., Pelet T., Kolakofsky D., Ray R., Compans R.W. The P gene of human parainfluenza virus type 1 encodes P and C proteins but not a cysteine-rich V protein. J. Virol. 1991;65:3406–3410. doi: 10.1128/jvi.65.6.3406-3410.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ohgimoto S., Bando H., Kawano M., Okamoto K., Kondo K., Tsurudome M., Nishio M., Ito Y. Sequence analysis of P gene of human parainfluenza type 2 virus: P and cysteine-rich proteins are translated by two mRNAs that differ by two nontemplated G residues. Virology. 1990;177:116–123. doi: 10.1016/0042-6822(90)90465-4. [DOI] [PubMed] [Google Scholar]
  27. Paterson R.G., Lamb R.A. RNA editing by G-nucleotide insertion in mumps virus P-gene mRNA transcripts. J. Virol. 1990;64:4137–4145. doi: 10.1128/jvi.64.9.4137-4145.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Pelet T., Curran J., Kolakofsky D. The P gene of bovine parainfluenza virus 3 expresses all three reading frames from a single mRNA editing site. EMBO J. 1991;10:443–448. doi: 10.1002/j.1460-2075.1991.tb07966.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Queen C., Korn L.J. A comprehensive sequence analysis program for the IBM personal computer. Nucleic Acids Res. 1984;12:581–599. doi: 10.1093/nar/12.1part2.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ryan K.W., Kingsbury D.W. Carboxyl-terminal region of Sendai virus P protein is required for binding to viral nucleocapsids. Virology. 1988;167:106–112. doi: 10.1016/0042-6822(88)90059-1. [DOI] [PubMed] [Google Scholar]
  31. Ryan K.W., Murti K.G., Portner A. Localization of P protein binding sites on the Sendai virus nucleocapsid. J. Gen. Virol. 1990;71:997–1000. doi: 10.1099/0022-1317-71-4-997. [DOI] [PubMed] [Google Scholar]
  32. Ryan K.W., Portner A. Separate domains of Sendai virus P protein are required for binding to viral nucleocapsids. Virology. 1990;174:515–521. doi: 10.1016/0042-6822(90)90105-z. [DOI] [PubMed] [Google Scholar]
  33. Sakai Y., Suzu S., Shioda T., Shibuta H. Nucleotide sequence of the bovine parainfluenza 3 virus genome: its 3′ end and the genes of NP, P, C and M proteins. Nucleic Acids Res. 1987;15:2927–2945. doi: 10.1093/nar/15.7.2927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shioda T., Hidaka Y., Kanda T., Shibuta H., Nomoto A., Iwasaki K. Sequence of 3,687 nucleotides from the Tend of Sendai virus genome RNA and the predicted amino acid sequences of viral NP, P, and C proteins. Nucleic Acids Res. 1983;11:7317–7330. doi: 10.1093/nar/11.21.7317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Southern J.A., Precious B., Randall R.E. Two nontemplated nucleotide additions are required to generate the P mRNA of parainfluenza virus type 2 since the RNA genome encodes protein V. Virology. 1990;177:388–390. doi: 10.1016/0042-6822(90)90497-f. [DOI] [PubMed] [Google Scholar]
  36. Spriggs M.K., Collins P.L. Human parainfluenza virus type 3: messenger RNAs, polypeptide coding assignments, intergenic sequences, and genetic map. J. Virol. 1986;59:646–654. doi: 10.1128/jvi.59.3.646-654.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Spriggs M.K., Collins P.L. Sequence analysis of the P and C protein genes of human parainfluenza virus type 3: Patterns of amino acid sequence homology among paramyxovirus proteins. J. Gen. Virol. 1986;67:2705–2719. doi: 10.1099/0022-1317-67-12-2705. [DOI] [PubMed] [Google Scholar]
  38. Thomas S.M., Lamb R.A., Paterson R.G. Two mRNAs that differ by two nontemplated nucleotides encode the amino coterminal proteins P and V of the paramyxovirus SV5. Cell. 1988;54:891–902. doi: 10.1016/S0092-8674(88)91285-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Udem S.A., Cook K.A. Isolation and characterization of measles virus intracellular nucleocapsid RNA. J. Virol. 1984;49:57–65. doi: 10.1128/jvi.49.1.57-65.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Vidal S., Curran J., Kolakofsky D. Editing of the Sendai virus P/C mRNA by G insertion occurs during mRNA synthesis via a virus-encoded activity. J. Virol. 1990;64:239–246. doi: 10.1128/jvi.64.1.239-246.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wechsler S.L., Lambert D.M., Galinski M.S., Heineke B.E., Pons M.W. Human parainfluenza virus 3: Purification and characterization of subviral components, viral proteins and viral RNA. Virus Res. 1985;3:339–351. doi: 10.1016/0168-1702(85)90434-4. [DOI] [PubMed] [Google Scholar]

Articles from Virology are provided here courtesy of Elsevier

RESOURCES