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. 1992 Mar;66(3):1765–1768. doi: 10.1128/jvi.66.3.1765-1768.1992

The parainfluenza virus type 1 P/C gene uses a very efficient GUG codon to start its C' protein.

R Boeck 1, J Curran 1, Y Matsuoka 1, R Compans 1, D Kolakofsky 1
PMCID: PMC240931  PMID: 1310778

Abstract

Parainfluenza virus type 1 (PIV1) and Sendai virus (SEN) are very closely related, but the PIV1 P/C gene does not contain the ACG codon which initiates the SEN C' protein. Nevertheless, a protein corresponding to the PIV1 C' protein was observed both in vivo and in vitro. The initiation site of this protein maps upstream of the PIV1 C protein AUG in a region that does not contain an AUG codon. We have used site-directed mutagenesis to demonstrate that the PIV1 C' protein initiates from a GUG codon, four codons upstream of where the ACG is found in SEN. Remarkably, this GUG appears to initiate in vivo almost as frequently as AUG in the same context. However, whereas GUG permits downstream expression of the P and C proteins, AUG in this context does not. The conservation of an upstream non-AUG initiation codon for C' among PIV1 and SEN suggests that it is important for virus replication, even though some paramyxoviruses express only the C protein and others have no C open reading frame at all.

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Selected References

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  1. Acland P., Dixon M., Peters G., Dickson C. Subcellular fate of the int-2 oncoprotein is determined by choice of initiation codon. Nature. 1990 Feb 15;343(6259):662–665. doi: 10.1038/343662a0. [DOI] [PubMed] [Google Scholar]
  2. Becerra S. P., Rose J. A., Hardy M., Baroudy B. M., Anderson C. W. Direct mapping of adeno-associated virus capsid proteins B and C: a possible ACG initiation codon. Proc Natl Acad Sci U S A. 1985 Dec;82(23):7919–7923. doi: 10.1073/pnas.82.23.7919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bernards A., de la Monte S. M. The ltk receptor tyrosine kinase is expressed in pre-B lymphocytes and cerebral neurons and uses a non-AUG translational initiator. EMBO J. 1990 Jul;9(7):2279–2287. doi: 10.1002/j.1460-2075.1990.tb07399.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Curran J., Boeck R., Kolakofsky D. The Sendai virus P gene expresses both an essential protein and an inhibitor of RNA synthesis by shuffling modules via mRNA editing. EMBO J. 1991 Oct;10(10):3079–3085. doi: 10.1002/j.1460-2075.1991.tb07860.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Curran J., Kolakofsky D. Ribosomal initiation from an ACG codon in the Sendai virus P/C mRNA. EMBO J. 1988 Jan;7(1):245–251. doi: 10.1002/j.1460-2075.1988.tb02806.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Curran J., Kolakofsky D. Scanning independent ribosomal initiation of the Sendai virus Y proteins in vitro and in vivo. EMBO J. 1989 Feb;8(2):521–526. doi: 10.1002/j.1460-2075.1989.tb03406.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Etkind P. R., Cross R. K., Lamb R. A., Merz D. C., Choppin P. W. In vitro synthesis of structural and nonstructural proteins of Sendai and SV5 viruses. Virology. 1980 Jan 15;100(1):22–33. doi: 10.1016/0042-6822(80)90548-6. [DOI] [PubMed] [Google Scholar]
  8. Florkiewicz R. Z., Sommer A. Human basic fibroblast growth factor gene encodes four polypeptides: three initiate translation from non-AUG codons. Proc Natl Acad Sci U S A. 1989 Jun;86(11):3978–3981. doi: 10.1073/pnas.86.11.3978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fuerst T. R., Niles E. G., Studier F. W., Moss B. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8122–8126. doi: 10.1073/pnas.83.21.8122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gorman W. L., Gill D. S., Scroggs R. A., Portner A. The hemagglutinin-neuraminidase glycoproteins of human parainfluenza virus type 1 and Sendai virus have high structure-function similarity with limited antigenic cross-reactivity. Virology. 1990 Mar;175(1):211–221. doi: 10.1016/0042-6822(90)90201-2. [DOI] [PubMed] [Google Scholar]
  11. Gupta K. C., Patwardhan S. ACG, the initiator codon for a Sendai virus protein. J Biol Chem. 1988 Jun 25;263(18):8553–8556. [PubMed] [Google Scholar]
  12. Hann S. R., King M. W., Bentley D. L., Anderson C. W., Eisenman R. N. A non-AUG translational initiation in c-myc exon 1 generates an N-terminally distinct protein whose synthesis is disrupted in Burkitt's lymphomas. Cell. 1988 Jan 29;52(2):185–195. doi: 10.1016/0092-8674(88)90507-7. [DOI] [PubMed] [Google Scholar]
  13. Huber M., Cattaneo R., Spielhofer P., Orvell C., Norrby E., Messerli M., Perriard J. C., Billeter M. A. Measles virus phosphoprotein retains the nucleocapsid protein in the cytoplasm. Virology. 1991 Nov;185(1):299–308. doi: 10.1016/0042-6822(91)90777-9. [DOI] [PubMed] [Google Scholar]
  14. KUROYA M., ISHIDA N. Newborn virus pneumonitis (type Sendai). II. The isolation of a new virus possessing hemagglutinin activity. Yokohama Med Bull. 1953 Aug;4(4):217–233. [PubMed] [Google Scholar]
  15. Kadowaki H., Kadowaki T., Wondisford F. E., Taylor S. I. Use of polymerase chain reaction catalyzed by Taq DNA polymerase for site-specific mutagenesis. Gene. 1989 Mar 15;76(1):161–166. doi: 10.1016/0378-1119(89)90018-8. [DOI] [PubMed] [Google Scholar]
  16. Kozak M. Context effects and inefficient initiation at non-AUG codons in eucaryotic cell-free translation systems. Mol Cell Biol. 1989 Nov;9(11):5073–5080. doi: 10.1128/mcb.9.11.5073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kozak M. Downstream secondary structure facilitates recognition of initiator codons by eukaryotic ribosomes. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8301–8305. doi: 10.1073/pnas.87.21.8301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lyn D., Gill D. S., Scroggs R. A., Portner A. The nucleoproteins of human parainfluenza virus type 1 and Sendai virus share amino acid sequences and antigenic and structural determinants. J Gen Virol. 1991 Apr;72(Pt 4):983–987. doi: 10.1099/0022-1317-72-4-983. [DOI] [PubMed] [Google Scholar]
  19. 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 Jun;65(6):3406–3410. doi: 10.1128/jvi.65.6.3406-3410.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Matsuoka Y., Ray R., Compans R. W. Sequence of the hemagglutinin-neuraminidase gene of human parainfluenza virus type 1. Virus Res. 1990 Apr;16(1):107–113. doi: 10.1016/0168-1702(90)90047-f. [DOI] [PubMed] [Google Scholar]
  21. Matsuoka Y., Ray R. Sequence analysis and expression of the human parainfluenza type 1 virus nucleoprotein gene. Virology. 1991 Mar;181(1):403–407. doi: 10.1016/0042-6822(91)90514-c. [DOI] [PubMed] [Google Scholar]
  22. Mehdi H., Ono E., Gupta K. C. Initiation of translation at CUG, GUG, and ACG codons in mammalian cells. Gene. 1990 Jul 16;91(2):173–178. doi: 10.1016/0378-1119(90)90085-6. [DOI] [PubMed] [Google Scholar]
  23. Merson J. R., Hull R. A., Estes M. K., Kasel J. A. Molecular cloning and sequence determination of the fusion protein gene of human parainfluenza virus type 1. Virology. 1988 Nov;167(1):97–105. doi: 10.1016/0042-6822(88)90058-x. [DOI] [PubMed] [Google Scholar]
  24. Prats A. C., De Billy G., Wang P., Darlix J. L. CUG initiation codon used for the synthesis of a cell surface antigen coded by the murine leukemia virus. J Mol Biol. 1989 Jan 20;205(2):363–372. doi: 10.1016/0022-2836(89)90347-1. [DOI] [PubMed] [Google Scholar]
  25. Prats H., Kaghad M., Prats A. C., Klagsbrun M., Lélias J. M., Liauzun P., Chalon P., Tauber J. P., Amalric F., Smith J. A. High molecular mass forms of basic fibroblast growth factor are initiated by alternative CUG codons. Proc Natl Acad Sci U S A. 1989 Mar;86(6):1836–1840. doi: 10.1073/pnas.86.6.1836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Saris C. J., Domen J., Berns A. The pim-1 oncogene encodes two related protein-serine/threonine kinases by alternative initiation at AUG and CUG. EMBO J. 1991 Mar;10(3):655–664. doi: 10.1002/j.1460-2075.1991.tb07994.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sugihara H., Andrisani V., Salvaterra P. M. Drosophila choline acetyltransferase uses a non-AUG initiation codon and full length RNA is inefficiently translated. J Biol Chem. 1990 Dec 15;265(35):21714–21719. [PubMed] [Google Scholar]
  28. Taira M., Iizasa T., Shimada H., Kudoh J., Shimizu N., Tatibana M. A human testis-specific mRNA for phosphoribosylpyrophosphate synthetase that initiates from a non-AUG codon. J Biol Chem. 1990 Sep 25;265(27):16491–16497. [PubMed] [Google Scholar]
  29. 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 Jan;64(1):239–246. doi: 10.1128/jvi.64.1.239-246.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]

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