Abstract
We described a novel system to study poliovirus replication in Xenopus oocytes. Poliovirus RNA microinjected into Xenopus oocyte initiates a complete cycle of viral replication, yielding a high level of infectious viruses. Two distinct HeLa cell activities are required, one involved in initiation of translation and the other in RNA synthesis. The translation factor is a large cytoplasmic protein or complex, which is specifically used for initiation of poliovirus translation. The replication factor is required at early stages of RNA synthesis. Formation of infectious poliovirus is highly temperature dependent. At temperatures below 27 degrees C, capsid assembly appears to be impaired. The oocyte system described here could be useful in identifying and characterizing viral and cellular factors involved in virus replication.
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- Agol V. I., Drozdov S. G., Ivannikova T. A., Kolesnikova M. S., Korolev M. B., Tolskaya E. A. Restricted growth of attenuated poliovirus strains in cultured cells of a human neuroblastoma. J Virol. 1989 Sep;63(9):4034–4038. doi: 10.1128/jvi.63.9.4034-4038.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Andino R., Rieckhof G. E., Achacoso P. L., Baltimore D. Poliovirus RNA synthesis utilizes an RNP complex formed around the 5'-end of viral RNA. EMBO J. 1993 Sep;12(9):3587–3598. doi: 10.1002/j.1460-2075.1993.tb06032.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Anthony D. D., Merrick W. C. Eukaryotic initiation factor (eIF)-4F. Implications for a role in internal initiation of translation. J Biol Chem. 1991 Jun 5;266(16):10218–10226. [PubMed] [Google Scholar]
- Barton D. J., Black E. P., Flanegan J. B. Complete replication of poliovirus in vitro: preinitiation RNA replication complexes require soluble cellular factors for the synthesis of VPg-linked RNA. J Virol. 1995 Sep;69(9):5516–5527. doi: 10.1128/jvi.69.9.5516-5527.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bernstein H. D., Sarnow P., Baltimore D. Genetic complementation among poliovirus mutants derived from an infectious cDNA clone. J Virol. 1986 Dec;60(3):1040–1049. doi: 10.1128/jvi.60.3.1040-1049.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bienz K., Egger D., Pasamontes L. Association of polioviral proteins of the P2 genomic region with the viral replication complex and virus-induced membrane synthesis as visualized by electron microscopic immunocytochemistry and autoradiography. Virology. 1987 Sep;160(1):220–226. doi: 10.1016/0042-6822(87)90063-8. [DOI] [PubMed] [Google Scholar]
- Borman A., Howell M. T., Patton J. G., Jackson R. J. The involvement of a spliceosome component in internal initiation of human rhinovirus RNA translation. J Gen Virol. 1993 Sep;74(Pt 9):1775–1788. doi: 10.1099/0022-1317-74-9-1775. [DOI] [PubMed] [Google Scholar]
- Brake A. J., Wagenbach M. J., Julius D. New structural motif for ligand-gated ion channels defined by an ionotropic ATP receptor. Nature. 1994 Oct 6;371(6497):519–523. doi: 10.1038/371519a0. [DOI] [PubMed] [Google Scholar]
- Brown B. A., Ehrenfeld E. Translation of poliovirus RNA in vitro: changes in cleavage pattern and initiation sites by ribosomal salt wash. Virology. 1979 Sep;97(2):396–405. doi: 10.1016/0042-6822(79)90350-7. [DOI] [PubMed] [Google Scholar]
- Buller A. L., White M. M. Functional acetylcholine receptors expressed in Xenopus oocytes after injection of Torpedo beta, gamma, and delta subunit RNAs are a consequence of endogenous oocyte gene expression. Mol Pharmacol. 1990 Mar;37(3):423–428. [PubMed] [Google Scholar]
- Burns C. C., Lawson M. A., Semler B. L., Ehrenfeld E. Effects of mutations in poliovirus 3Dpol on RNA polymerase activity and on polyprotein cleavage. J Virol. 1989 Nov;63(11):4866–4874. doi: 10.1128/jvi.63.11.4866-4874.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Caliguiri L. A., Tamm I. The role of cytoplasmic membranes in poliovirus biosynthesis. Virology. 1970 Sep;42(1):100–111. doi: 10.1016/0042-6822(70)90242-4. [DOI] [PubMed] [Google Scholar]
- Chen C. Y., Sarnow P. Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science. 1995 Apr 21;268(5209):415–417. doi: 10.1126/science.7536344. [DOI] [PubMed] [Google Scholar]
- Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dildine S. L., Semler B. L. Conservation of RNA-protein interactions among picornaviruses. J Virol. 1992 Jul;66(7):4364–4376. doi: 10.1128/jvi.66.7.4364-4376.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dubochet J., Ducommun M., Zollinger M., Kellenberger E. A new preparation method for dark-field electron microscopy of biomacromolecules. J Ultrastruct Res. 1971 Apr;35(1):147–167. doi: 10.1016/s0022-5320(71)80148-x. [DOI] [PubMed] [Google Scholar]
- Duke G. M., Palmenberg A. C. Cloning and synthesis of infectious cardiovirus RNAs containing short, discrete poly(C) tracts. J Virol. 1989 Apr;63(4):1822–1826. doi: 10.1128/jvi.63.4.1822-1826.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flanegan J. B., Baltimore D. Poliovirus-specific primer-dependent RNA polymerase able to copy poly(A). Proc Natl Acad Sci U S A. 1977 Sep;74(9):3677–3680. doi: 10.1073/pnas.74.9.3677. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gebhard J. R., Ehrenfeld E. Specific interactions of HeLa cell proteins with proposed translation domains of the poliovirus 5' noncoding region. J Virol. 1992 May;66(5):3101–3109. doi: 10.1128/jvi.66.5.3101-3109.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Giachetti C., Semler B. L. Role of a viral membrane polypeptide in strand-specific initiation of poliovirus RNA synthesis. J Virol. 1991 May;65(5):2647–2654. doi: 10.1128/jvi.65.5.2647-2654.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haller A. A., Semler B. L. Stem-loop structure synergy in binding cellular proteins to the 5' noncoding region of poliovirus RNA. Virology. 1995 Feb 1;206(2):923–934. doi: 10.1006/viro.1995.1015. [DOI] [PubMed] [Google Scholar]
- Hellen C. U., Witherell G. W., Schmid M., Shin S. H., Pestova T. V., Gil A., Wimmer E. A cytoplasmic 57-kDa protein that is required for translation of picornavirus RNA by internal ribosomal entry is identical to the nuclear pyrimidine tract-binding protein. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7642–7646. doi: 10.1073/pnas.90.16.7642. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Helms J. B., Rothman J. E. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature. 1992 Nov 26;360(6402):352–354. doi: 10.1038/360352a0. [DOI] [PubMed] [Google Scholar]
- Irurzun A., Perez L., Carrasco L. Involvement of membrane traffic in the replication of poliovirus genomes: effects of brefeldin A. Virology. 1992 Nov;191(1):166–175. doi: 10.1016/0042-6822(92)90178-r. [DOI] [PubMed] [Google Scholar]
- Jackson R. J., Hunt S. L., Reynolds J. E., Kaminski A. Cap-dependent and cap-independent translation: operational distinctions and mechanistic interpretations. Curr Top Microbiol Immunol. 1995;203:1–29. doi: 10.1007/978-3-642-79663-0_1. [DOI] [PubMed] [Google Scholar]
- Jang S. K., Kräusslich H. G., Nicklin M. J., Duke G. M., Palmenberg A. C., Wimmer E. A segment of the 5' nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J Virol. 1988 Aug;62(8):2636–2643. doi: 10.1128/jvi.62.8.2636-2643.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Julius D., MacDermott A. B., Axel R., Jessell T. M. Molecular characterization of a functional cDNA encoding the serotonin 1c receptor. Science. 1988 Jul 29;241(4865):558–564. doi: 10.1126/science.3399891. [DOI] [PubMed] [Google Scholar]
- Kaminski A., Hunt S. L., Patton J. G., Jackson R. J. Direct evidence that polypyrimidine tract binding protein (PTB) is essential for internal initiation of translation of encephalomyocarditis virus RNA. RNA. 1995 Nov;1(9):924–938. [PMC free article] [PubMed] [Google Scholar]
- Kuhn R. J., Tada H., Ypma-Wong M. F., Semler B. L., Wimmer E. Mutational analysis of the genome-linked protein VPg of poliovirus. J Virol. 1988 Nov;62(11):4207–4215. doi: 10.1128/jvi.62.11.4207-4215.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- La Monica N., Racaniello V. R. Differences in replication of attenuated and neurovirulent polioviruses in human neuroblastoma cell line SH-SY5Y. J Virol. 1989 May;63(5):2357–2360. doi: 10.1128/jvi.63.5.2357-2360.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laskey R. A., Gurdon J. B., Crawford L. V. Translation of encephalomyocarditis viral RNA in oocytes of Xenopus laevis. Proc Natl Acad Sci U S A. 1972 Dec;69(12):3665–3669. doi: 10.1073/pnas.69.12.3665. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li J. P., Baltimore D. Isolation of poliovirus 2C mutants defective in viral RNA synthesis. J Virol. 1988 Nov;62(11):4016–4021. doi: 10.1128/jvi.62.11.4016-4021.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- López-Guerrero J. A., Carrasco L., Martínez-Abarca F., Fresno M., Alonso M. A. Restriction of poliovirus RNA translation in a human monocytic cell line. Eur J Biochem. 1989 Dec 22;186(3):577–582. doi: 10.1111/j.1432-1033.1989.tb15247.x. [DOI] [PubMed] [Google Scholar]
- Marcus-Sekura C. J., Hitchcock M. J. Preparation of oocytes for microinjection of RNA and DNA. Methods Enzymol. 1987;152:284–288. doi: 10.1016/0076-6879(87)52032-8. [DOI] [PubMed] [Google Scholar]
- Masu Y., Nakayama K., Tamaki H., Harada Y., Kuno M., Nakanishi S. cDNA cloning of bovine substance-K receptor through oocyte expression system. 1987 Oct 29-Nov 4Nature. 329(6142):836–838. doi: 10.1038/329836a0. [DOI] [PubMed] [Google Scholar]
- Maynell L. A., Kirkegaard K., Klymkowsky M. W. Inhibition of poliovirus RNA synthesis by brefeldin A. J Virol. 1992 Apr;66(4):1985–1994. doi: 10.1128/jvi.66.4.1985-1994.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meerovitch K., Pelletier J., Sonenberg N. A cellular protein that binds to the 5'-noncoding region of poliovirus RNA: implications for internal translation initiation. Genes Dev. 1989 Jul;3(7):1026–1034. doi: 10.1101/gad.3.7.1026. [DOI] [PubMed] [Google Scholar]
- Meerovitch K., Svitkin Y. V., Lee H. S., Lejbkowicz F., Kenan D. J., Chan E. K., Agol V. I., Keene J. D., Sonenberg N. La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J Virol. 1993 Jul;67(7):3798–3807. doi: 10.1128/jvi.67.7.3798-3807.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meyer K., Petersen A., Niepmann M., Beck E. Interaction of eukaryotic initiation factor eIF-4B with a picornavirus internal translation initiation site. J Virol. 1995 May;69(5):2819–2824. doi: 10.1128/jvi.69.5.2819-2824.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Molla A., Paul A. V., Wimmer E. Cell-free, de novo synthesis of poliovirus. Science. 1991 Dec 13;254(5038):1647–1651. doi: 10.1126/science.1661029. [DOI] [PubMed] [Google Scholar]
- Najita L., Sarnow P. Oxidation-reduction sensitive interaction of a cellular 50-kDa protein with an RNA hairpin in the 5' noncoding region of the poliovirus genome. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5846–5850. doi: 10.1073/pnas.87.15.5846. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pause A., Méthot N., Svitkin Y., Merrick W. C., Sonenberg N. Dominant negative mutants of mammalian translation initiation factor eIF-4A define a critical role for eIF-4F in cap-dependent and cap-independent initiation of translation. EMBO J. 1994 Mar 1;13(5):1205–1215. doi: 10.1002/j.1460-2075.1994.tb06370.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pelletier J., Kaplan G., Racaniello V. R., Sonenberg N. Cap-independent translation of poliovirus mRNA is conferred by sequence elements within the 5' noncoding region. Mol Cell Biol. 1988 Mar;8(3):1103–1112. doi: 10.1128/mcb.8.3.1103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pelletier J., Kaplan G., Racaniello V. R., Sonenberg N. Translational efficiency of poliovirus mRNA: mapping inhibitory cis-acting elements within the 5' noncoding region. J Virol. 1988 Jul;62(7):2219–2227. doi: 10.1128/jvi.62.7.2219-2227.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pelletier J., Sonenberg N. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature. 1988 Jul 28;334(6180):320–325. doi: 10.1038/334320a0. [DOI] [PubMed] [Google Scholar]
- Pestova T. V., Hellen C. U., Wimmer E. Translation of poliovirus RNA: role of an essential cis-acting oligopyrimidine element within the 5' nontranslated region and involvement of a cellular 57-kilodalton protein. J Virol. 1991 Nov;65(11):6194–6204. doi: 10.1128/jvi.65.11.6194-6204.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rombaut B., Vrijsen R., Boeyé A. A pH-dependent dissociation of poliovirus procapsids. Virology. 1987 Mar;157(1):245–247. doi: 10.1016/0042-6822(87)90336-9. [DOI] [PubMed] [Google Scholar]
- Scheper G. C., Voorma H. O., Thomas A. A. Eukaryotic initiation factors-4E and -4F stimulate 5' cap-dependent as well as internal initiation of protein synthesis. J Biol Chem. 1992 Apr 15;267(11):7269–7274. [PubMed] [Google Scholar]
- Svitkin Y. V., Meerovitch K., Lee H. S., Dholakia J. N., Kenan D. J., Agol V. I., Sonenberg N. Internal translation initiation on poliovirus RNA: further characterization of La function in poliovirus translation in vitro. J Virol. 1994 Mar;68(3):1544–1550. doi: 10.1128/jvi.68.3.1544-1550.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takeda N., Kuhn R. J., Yang C. F., Takegami T., Wimmer E. Initiation of poliovirus plus-strand RNA synthesis in a membrane complex of infected HeLa cells. J Virol. 1986 Oct;60(1):43–53. doi: 10.1128/jvi.60.1.43-53.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Trono D., Andino R., Baltimore D. An RNA sequence of hundreds of nucleotides at the 5' end of poliovirus RNA is involved in allowing viral protein synthesis. J Virol. 1988 Jul;62(7):2291–2299. doi: 10.1128/jvi.62.7.2291-2299.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Trono D., Pelletier J., Sonenberg N., Baltimore D. Translation in mammalian cells of a gene linked to the poliovirus 5' noncoding region. Science. 1988 Jul 22;241(4864):445–448. doi: 10.1126/science.2839901. [DOI] [PubMed] [Google Scholar]
- Van Dyke T. A., Flanegan J. B. Identification of poliovirus polypeptide P63 as a soluble RNA-dependent RNA polymerase. J Virol. 1980 Sep;35(3):732–740. doi: 10.1128/jvi.35.3.732-740.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhou S. L., Standring D. N. Production of hepatitis B virus nucleocapsidlike core particles in Xenopus oocytes: assembly occurs mainly in the cytoplasm and does not require the nucleus. J Virol. 1991 Oct;65(10):5457–5464. doi: 10.1128/jvi.65.10.5457-5464.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Wet J. R., Wood K. V., DeLuca M., Helinski D. R., Subramani S. Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol. 1987 Feb;7(2):725–737. doi: 10.1128/mcb.7.2.725. [DOI] [PMC free article] [PubMed] [Google Scholar]