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. 2004 Sep 30;54(6):891–902. doi: 10.1016/S0092-8674(88)91285-8

Two mRNAs that differ by two nontemplated nucleotides encode the amino coterminal proteins P and V of the paramyxovirus SV5

Sheila M Thomas 1, Robert A Lamb 1, Reay G Paterson 1
PMCID: PMC7133244  PMID: 3044614

Summary

The “P≓ gene of the paramyxovirus SV5 encodes two known proteins, P (Mr ≈ 44,000) and V (Mr ≈ 24,000). The complete nucleotide sequence of the “P≓ gene has been obtained and is found to contain two open reading frames, neither of which is large enough to encode the P protein. We have shown that the P and V proteins are translated from two mRNAs that differ by the presence of two nontemplated G residues in the P mRNA. These two additional nucleotides convert the two open reading frames to one of 392 amino acids. The P and V proteins are amino coterminal and have 164 amino acids in common. The unique C terminus of V consists of a cysteine-rich region that resembles a cysteine-rich metal binding domain. An open reading frame that contains this cysteine-rich region exists in all other paramyxovirus “P≓ gene sequences examined, which suggests that it may have important biological significance.

References

  1. Air G.M. Nucleotide sequence coding for the “signal peptide≓ and N terminus of the hemagglutinin from an Asian (H2N2) strain of influenza virus. Virology. 1979;97:468–472. doi: 10.1016/0042-6822(79)90358-1. [DOI] [PubMed] [Google Scholar]
  2. Atkins J.F., Steitz J.A., Anderson C.W., Model P. Binding of mammalian ribosomes to MS2 phage RNA reveals an overlapping gene encoding a lysis function. Cell. 1979;18:247–256. doi: 10.1016/0092-8674(79)90044-8. [DOI] [PubMed] [Google Scholar]
  3. Barrett T., Shrimpton S.B., Russell S.E.H. Nucleotide sequence of the entire protein coding region of canine distemper virus polymerase-associated (P) protein mRNA. Virus Res. 1985;3:367–372. doi: 10.1016/0168-1702(85)90436-8. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Beene R., Van Den Burg J., Brackenhoff J.P.J., Sloof P., Van Boom J.H., Tromp M.C. Major transcript of the frameshift coxll gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell. 1986;46:819–826. doi: 10.1016/0092-8674(86)90063-2. [DOI] [PubMed] [Google Scholar]
  6. Bertholet C., Van Meir E., ten Heggeler-Bordier B., Wittek R. Vaccinia virus produces late mRNAs by discontinuous synthesis. Cell. 1987;50:153–162. doi: 10.1016/0092-8674(87)90211-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bos J.L., Polder L.J., Bernards R., Schrier P.I., van den Elsen P.J., van der Eb A.J., van Ormondt H. The 2.2 kb E1b mRNA of human Ad12 and Ad5 codes for two tumor antigens starting at different AUG triplets. Cell. 1981;27:121–131. doi: 10.1016/0092-8674(81)90366-4. [DOI] [PubMed] [Google Scholar]
  8. Boursnell M.E.G., Brown T.D.K., Foulds I.J., Green P.F., Tomley F.M., Binns M.M. Completion of the sequence of the genome of the coronavirus avian infectious bronchitis virus. J. Gen. Virol. 1987;68:57–77. doi: 10.1099/0022-1317-68-1-57. [DOI] [PubMed] [Google Scholar]
  9. Breitbart R.E., Andreadis A., Nadal-Ginard B. Alternative splicing: a ubiquitous mechanism for the generation of multiple protein isoforms from single genes. Annu. Rev. Biochem. 1987;56:467–495. doi: 10.1146/annurev.bi.56.070187.002343. [DOI] [PubMed] [Google Scholar]
  10. Briedis D.J., Lamb R.A. Influenza B virus genome: sequences and structural organization of RNA segment 8 and the mRNAs coding for the NS1 and NS2 proteins. J. Virol. 1982;42:186–193. doi: 10.1128/jvi.42.1.186-193.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brierley I., Boursnell M.E.G., Binns M.M., Bilimoria B., Blok V.C., Brown T.D.K., Inglis S.G. An efficient ribosome frameshifting signal in the polymerase-encoding region of the corona-virus IBV. EMBO J. 1987;6:3779–3785. doi: 10.1002/j.1460-2075.1987.tb02713.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Buetti E., Choppin P.W. The transcriptase complex of the paramyxovirus SV5. Virology. 1977;82:493–508. doi: 10.1016/0042-6822(77)90021-6. [DOI] [PubMed] [Google Scholar]
  13. Chen S.-H., Habib G., Yang C.-Y., Gu Z.-W., Lee B.R., Weng S.A., Silberman S.R., Cai S.-J., Desylpere J.P., Rosseneu M., Gotto A.M., Jr., Li W.-H., Chan L. Apolipoprotein B-48 is the product of a messenger RNA with an organ-specific in-frame stop codon. Science. 1987;238:363–366. doi: 10.1126/science.3659919. [DOI] [PubMed] [Google Scholar]
  14. Choppin P.W. Multiplication of a myxovirus (SV5) with minimal cytopathic effects and without interference. Virology. 1964;23:224–233. doi: 10.1016/0042-6822(64)90286-7. [DOI] [PubMed] [Google Scholar]
  15. Collins P.L., Wertz G.W., Ball L.A., Hightower L.E. Coding assignments of the five smaller mRNAs of Newcastle disease virus. J. Virol. 1982;43:1024–1031. doi: 10.1128/jvi.43.3.1024-1031.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Curran J.A., Richardson C.D., Kolakofsky D. Ribosomal initiation at alternate AUGs on the Sendai virus P/C mRNA. J. Virol. 1986;57:684–687. doi: 10.1128/jvi.57.2.684-687.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Erickson A.H., Blobel G. Early events in the biosynthesis of the lysosomal enzyme cathepsin. J. Biol. Chem. 1979;254:11771–11774. [PubMed] [Google Scholar]
  18. Evans R.A. The steroid and thyroid hormone receptor superfamily. Science. 1988;240:889–895. doi: 10.1126/science.3283939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Feagin J.E., Abraham J.M., Stuart K. Extensive editing of the cytochrome c oxidase III transcript in Trypanosoma brucei. Cell. 1988;53:413–422. doi: 10.1016/0092-8674(88)90161-4. [DOI] [PubMed] [Google Scholar]
  20. Feagin J.E., Jasmer D.P., Stuart K. Developmentally regulated addition of nucleotides within the apocytochrome b transcripts in Trypanosoma brucei. Cell. 1987;49:337–345. doi: 10.1016/0092-8674(87)90286-8. [DOI] [PubMed] [Google Scholar]
  21. Frankel A.D., Bredt D.S., Pabo C.O. Tat protein from human immunodeficiency virus forms a metal-linked dimer. Science. 1988;240:70–73. doi: 10.1126/science.2832944. [DOI] [PubMed] [Google Scholar]
  22. 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;155:46–60. doi: 10.1016/0042-6822(86)90167-4. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Gupta K.C., Kingsbury D.W. Translational modulation in vitro of a eukaryotic viral mRNA encoding overlapping genes: ribosome scanning and potential roles of conformational changes in the P/C mRNA of Sendai virus. Biochem. Biophys. Res. Commu. 1985;131:91–97. doi: 10.1016/0006-291x(85)91774-7. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Hansen U., Tenen D.G., Livingstone D.M., Sharp P.A. T antigen repression of SV40 early transcription from two promoters. Cell. 1981;27:603–612. doi: 10.1016/0092-8674(81)90402-5. [DOI] [PubMed] [Google Scholar]
  27. Herrler G., Compans R.W. Synthesis of mumps virus polypeptides in infected vero cells. Virology. 1982;100:433–449. doi: 10.1016/0042-6822(82)90102-7. [DOI] [PubMed] [Google Scholar]
  28. Hiebert S.W., Paterson R.G., Lamb R.A. Hemagglutinin-neuraminidase protein of the paramyxovirus simian virus 5 nucleotide sequence of the mRNA predicts an N-terminal membrane anchor. J. Virol. 1985;54:1–6. doi: 10.1128/jvi.54.1.1-6.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hull J.D., Gilmore R., Lamb R.A. Integration of a small integral membrane protein, M2, of influenza virus into the endoplasmic reticulum: analysis of the internal signal-anchor domain of a protein with an ectoplasmic NH2 terminus. J. Cell. Biol. 1988;106:1489–1498. doi: 10.1083/jcb.106.5.1489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Jacks T., Varmus H.E. Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting. Science. 1985;230:1237–1242. doi: 10.1126/science.2416054. [DOI] [PubMed] [Google Scholar]
  31. Jacks T., Townsley K., Varmus H.E., Majors J. Vol. 84. 1987. Two efficient ribosomal frameshifting events are required for synthesis of mouse mammary tumour virus gag-related polyproteins; pp. 4298–4302. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Johnston M., Dover J. Vol. 84. 1987. Mutations that inactivate a yeast transcriptional regulatory protein cluster in an evolutionary conserved DNA binding domain; pp. 2401–2405. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Koller B., Frommn H., Galun E., Edelman M. Evidence for in vivo trans splicing of pre-mRNAs in tobacco chloroplasts. Cell. 1987;48:111–119. doi: 10.1016/0092-8674(87)90361-8. [DOI] [PubMed] [Google Scholar]
  34. Konarska M.M., Padgett R.A., Sharp P.A. Trans splicing of mRNA precursors in vitro. Cell. 1985;42:165–171. doi: 10.1016/s0092-8674(85)80112-4. [DOI] [PubMed] [Google Scholar]
  35. Krause M., Hirsh D. A trans-spliced leader sequence on actin mRNA in C. elegans. Cell. 1987;49:753–761. doi: 10.1016/0092-8674(87)90613-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Lamb R.A., Lai C.-J. Sequence of interrupted and uninterrupted mRNAs and cloned DNA coding for the two overlapping nonstructural proteins of influenza virus. Cell. 1980;21:475–485. doi: 10.1016/0092-8674(80)90484-5. [DOI] [PubMed] [Google Scholar]
  37. Lamb R.A., Lai C.-J. Spliced and unspliced messenger RNAs synthesized from cloned influenza virus M DNA in an SV40 vector: expression of the influenza virus membrane protein (M1) Virology. 1982;123:237–256. doi: 10.1016/0042-6822(82)90258-6. [DOI] [PubMed] [Google Scholar]
  38. Lamb R.A., Etkind P.R., Choppin P.W. Evidence for a ninth influenza viral polypeptide. Virology. 1978;91:60–78. doi: 10.1016/0042-6822(78)90355-0. [DOI] [PubMed] [Google Scholar]
  39. Lamb R.A., Lai C.-J., Choppin P.W. Vol. 78. 1981. Sequences of mRNAs derived from genome RNA segment 7 of influenza virus colinear and interrupted mRNAs code for overlapping proteins; pp. 4170–4174. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Luk D., Sanchez A., Banerjee A.K. Messenger RNA encoding the phosphoprotein (P) gene of human parainfluenza virus 3 is bicistronic. Virology. 1986;153:318–325. doi: 10.1016/0042-6822(86)90036-x. [DOI] [PubMed] [Google Scholar]
  41. Maxam A.M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Meth. Enzymol. 1980;65:499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  42. McGinnes L., McQuain C., Morrison T. The P protein and the non-structural 38K and 29K proteins of Newcastle disease virus are derived from the same open reading frame. Virology. 1988;164:256–264. doi: 10.1016/0042-6822(88)90643-5. [DOI] [PubMed] [Google Scholar]
  43. Moran E., Mathews M.B. Multiple functional domains in the adenovirus E1A gene. Cell. 1987;48:177–178. doi: 10.1016/0092-8674(87)90418-1. [DOI] [PubMed] [Google Scholar]
  44. Murphy W.J., Watkins K.P., Agabian N. Identification of a novel Y branch structure as an intermediate in trypanosome mRNA processing: evidence for trans splicing. Cell. 1986;47:517–525. doi: 10.1016/0092-8674(86)90616-1. [DOI] [PubMed] [Google Scholar]
  45. Padgett R.A., Grabowski P.J., Konarska M.N., Seiter S., Sharp P.A. Splicing of messenger RNA precursors. Annu. Rev. Biochem. 1986;55:1119–1150. doi: 10.1146/annurev.bi.55.070186.005351. [DOI] [PubMed] [Google Scholar]
  46. Paterson R.G., Lamb R.A. Ability of the hydrophobic fusion-related external domain of a paramyxovirus F protein to act as a membrane anchor. Cell. 1987;48:441–452. doi: 10.1016/0092-8674(87)90195-4. [DOI] [PubMed] [Google Scholar]
  47. Paterson R.G., Harris T.J.R., Lamb R.A. Analysis and gene assignment of mRNAs of a paramyxovirus, simian virus 5. Virology. 1984;138:310–323. doi: 10.1016/0042-6822(84)90354-4. [DOI] [PubMed] [Google Scholar]
  48. Peluso R.W., Lamb R.A., Choppin P.W. Polypeptide synthesis in simian virus 5 infected cells. J. Virol. 1977;23:177–187. doi: 10.1128/jvi.23.1.177-187.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Powell L.M., Wallis S.C., Pease R.J., Edwards Y.H., Knott T.J., Scott J. A novel form of tissue-specific RNA processing produces apolipoprotein-B48 in intestine. Cell. 1987;50:831–840. doi: 10.1016/0092-8674(87)90510-1. [DOI] [PubMed] [Google Scholar]
  50. Randall R.E., Young D.F., Goswami K.K.A., Russell W.C. Isolation and characterization of monoclonal antibodies to simian virus 5 and their use in revealing antigenic differences between human, canine and simian isolates. J. Gen. Virol. 1987;68:2769–2780. doi: 10.1099/0022-1317-68-11-2769. [DOI] [PubMed] [Google Scholar]
  51. Sanger F., Nicklen S., Coulson A.R. Vol. 74. 1977. DNA sequencing with chain-terminating inhibitors; pp. 5463–5467. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Sato H., Oh-Hira M., 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 Research. 1987;7:241–255. doi: 10.1016/0168-1702(87)90031-1. [DOI] [PubMed] [Google Scholar]
  53. Schwer B., Stunnenberg H.G. Vaccinia virus late transcripts generated in vitro have a poly(A) head. EMBO J. 1988;7:1183–1190. doi: 10.1002/j.1460-2075.1988.tb02929.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Schwer B., Visca P., Vos J.C., Stunnenberg H.G. Discontinuous transcription or RNA processing of vaccinia virus late messengers results in a 5′ poly(A) leader. Cell. 1987;50:163–169. doi: 10.1016/0092-8674(87)90212-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Shaw M.W., Choppin P.W., Lamb R.A. Vol. 80. 1983. A previously unrecognized influenza B virus glycoprotein from a bicistronic mRNA that also encodes the viral neuraminidase; pp. 4879–4883. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Shaw J.M., Feagin J.E., 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;53:401–411. doi: 10.1016/0092-8674(88)90160-2. [DOI] [PubMed] [Google Scholar]
  57. 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 protein. Nucl. Acids Res. 1983;11:7317–7330. doi: 10.1093/nar/11.21.7317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Solnick D. Trans splicing of mRNA precursors. Cell. 1985;42:157–164. doi: 10.1016/s0092-8674(85)80111-2. [DOI] [PubMed] [Google Scholar]
  59. 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]
  60. Strauss E.G., Rice C.M., Strauss J.H. Vol. 80. 1983. Sequence coding for the alphavirus nonstructural proteins is interrupted by an opal termination codon; pp. 5271–5275. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sutton R.E., Bothroyd J.C. Evidence for trans splicing in trypanosomes. Cell. 1986;47:527–535. doi: 10.1016/0092-8674(86)90617-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Tabor S. United States Biochemical Corporation; New York: 1987. Sequence™: step-by-step protocols for DNA sequencing with Sequenase™. [Google Scholar]
  63. Takeuchi K., Hishiyama M., Yamada A., Sugiwa A. Molecular cloning and sequence analysis of mumps virus gene encoding the P protein: mumps virus P gene is monocistronic. J. Gen. Virol. 1988 doi: 10.1099/0022-1317-69-8-2043. in press. [DOI] [PubMed] [Google Scholar]
  64. Varmus H. Retroviruses. Science. 1988;240:1427–1435. doi: 10.1126/science.3287617. [DOI] [PubMed] [Google Scholar]
  65. Yoshinaka Y., Katoh I., Copeland T.D., Oroszlan S. Vol. 82. 1985. Murine leukemia virus protease is encoded by the gag-pol gene and is synthesized through suppression of an amber termination codon; pp. 1618–1622. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Zoller M.J., Smith M. Oligonucleotide-directed mutagenesis using M13-derived vectors: an efficient and general procedure for the production of point mutations in any fragment. Nucl. Acids Res. 1982;10:6487–6500. doi: 10.1093/nar/10.20.6487. [DOI] [PMC free article] [PubMed] [Google Scholar]

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