1887

Abstract

Translation initiation of poliovirus and hepatitis C virus (HCV) RNA occurs by entry of ribosomes to the internal RNA sequence, called the internal ribosomal entry site (IRES). Both IRES bind to the La protein and are thought to require the protein for their translation initiation activity, although they are greatly different in both the primary and predicted secondary structures. To compare the La protein requirement for these IRES, we took advantage of I-RNA from the yeast , which has been reported to bind to La protein and block poliovirus IRES-mediated translation initiation. In a cell-free translation system prepared from HeLa cells, yeast I-RNA inhibited translation initiation on poliovirus RNA as expected, but did not significantly inhibit translation initiation on HCV RNA. However, the translation initiation directed by either IRES was apparently inhibited by I-RNA in rabbit reticulocyte lysates, in which La protein is limiting. I-RNA-mediated inhibition of HCV IRES-dependent translation in rabbit reticulocyte lysates was reversed by exogenous addition of purified recombinant La protein of smaller amounts than necessary to reverse poliovirus IRES-dependent translation. These results suggest that HCV IRES requires lower concentrations of La protein for its function than does poliovirus IRES. Immunofluorescence studies showed that HCV infection appeared not to affect the subcellular localization of La protein, which exists mainly in the nucleus, although La protein redistributed to the cytoplasm after poliovirus infection. The data are compatible with the low requirement of La protein for HCV IRES activity.

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1999-09-01
2019-11-15
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References

  1. Ali, N. & Siddiqui, A. ( 1997; ). The La antigen binds 5′ noncoding region of the hepatitis C virus RNA in the context of the initiator AUG codon and stimulates internal ribosome entry site-mediated translation. Proceedings of the National Academy of Sciences, USA 94, 2249-2254.[CrossRef]
    [Google Scholar]
  2. Bachmann, M., Falke, D., Schröder, H.-C. & Müller, W. E. G. ( 1989a; ). Intracellular distribution of the La antigen in CV-1 cells after herpes simplex virus type 1 infection compared with the localization of U small nuclear ribonucleoprotein particles. Journal of General Virology 70, 881-891.[CrossRef]
    [Google Scholar]
  3. Bachmann, M., Pfeifer, K., Schröder, H. C. & Müller, W. E. G. ( 1989b; ). The La antigen shuttles between the nucleus and the cytoplasm in CV-1 cells. Molecular and Cellular Biochemistry 85, 103-114.[CrossRef]
    [Google Scholar]
  4. Berlioz, C. & Darlix, J.-L. ( 1995; ). An internal ribosomal entry mechanism promotes translation of murine leukemia virus gag polyprotein precursors. Journal of Virology 69, 2214-2222.
    [Google Scholar]
  5. Blyn, L. B., Towner, J. S., Semler, B. L. & Ehrenfeld, E. ( 1997; ). Requirement of poly(rC) binding protein 2 for translation of poliovirus RNA. Journal of Virology 71, 6243-6246.
    [Google Scholar]
  6. Borman, A., Howell, M. T., Patton, J. G. & Jackson, R. J. ( 1993; ). The involvement of a spliceosome component in internal initiation of human rhinovirus RNA translation. Journal of General Virology 74, 1775-1788.[CrossRef]
    [Google Scholar]
  7. Brown, B. A. & Ehrenfeld, E. ( 1979; ). Translation of polivirus RNA in vitro: changes in cleavage pattern and initiation sites by ribosomal salt wash. Virology 97, 396-405.[CrossRef]
    [Google Scholar]
  8. Brown, E. A., Zhang, H., Ping, L.-H. & Lemon, S. M. ( 1992; ). Secondary structure of the 5′ nontranslated regions of hepatitis C virus and pestivirus genomic RNAs. Nucleic Acids Research 20, 5041-5045.[CrossRef]
    [Google Scholar]
  9. Chan, E. K., Sullivan, K. F., Fox, R. I. & Tan, E. M. ( 1989; ). Sjögren’s syndrome nuclear antigen B (La): cDNA cloning, structural domains, and autoepitopes. Journal of Autoimmunity 2, 321-327.[CrossRef]
    [Google Scholar]
  10. Choo, Q.-L., Kuo, G., Weiner, A. J., Overby, L. R., Bradley, D. W. & Houghton, M. ( 1989; ). Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244, 359-362.[CrossRef]
    [Google Scholar]
  11. Coward, P. & Dasgupta, A. ( 1992; ). Yeast cells are incapable of translating RNAs containing the poliovirus 5′ untranslated region: evidence for a translational inhibitor. Journal of Virology 66, 286-295.
    [Google Scholar]
  12. Craig, A. W. B., Svitkin, Y. V., Lee, H. S., Belsham, G. J. & Sonenberg, N. ( 1997; ). The La autoantigen contains a dimerization domain that is essential for enhancing translation. Molecular & Cellular Biology 17, 163-169.
    [Google Scholar]
  13. Das, S., Coward, P. & Dasgupta, A. ( 1994; ). A small yeast RNA selectively inhibits internal initiation of translation programmed by poliovirus RNA: specific interaction with cellular proteins that bind to the viral 5′-untranslated region. Journal of Virology 68, 7200-7211.
    [Google Scholar]
  14. Das, S., Kenan, D. J., Bocskai, D., Keene, J. D. & Dasgupta, A. ( 1996; ). Sequences within a small yeast RNA required for inhibition of internal initiation of translation: interaction with La and other cellular proteins influences its inhibitory activity. Journal of Virology 70, 1624-1632.
    [Google Scholar]
  15. Dorner, A. J., Semler, B. L., Jackson, R. J., Hanecak, R., Duprey, E. & Wimmer, E. ( 1984; ). In vitro translation of poliovirus RNA: utilization of internal initiation sites in reticulocyte lysate. Journal of Virology 50, 507-514.
    [Google Scholar]
  16. Evans, D. M. A., Dunn, G., Minor, P. D., Schild, G. C., Cann, A. J., Stanway, G., Almond, J. W., Currey, K. & Maizel, J. V.Jr ( 1984; ). Increased neurovirulence associated with a single nucleotide change in a noncoding region of the Sabin type 3 poliovirus genome. Nature 314, 548-550.
    [Google Scholar]
  17. Gottlieb, E. & Steitz, J. A. ( 1989a; ). Function of the mammalian La protein: evidence for its action in transcription termination by RNA polymerase III. EMBO Journal 8, 851-861.
    [Google Scholar]
  18. Gottlieb, E. & Steitz, J. A. ( 1989b; ). The RNA binding protein La influences both the accuracy and the efficiency of RNA polymerase III transcription in vitro. EMBO Journal 8, 841-850.
    [Google Scholar]
  19. Hellen, C. U. T., Witherell, G. W., Schmid, M., Shin, S. H., Pestova, T. V., Gil, A. & Wimmer, E. ( 1993; ). 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. Proceedings of the National Academy of Sciences, USA 90, 7642-7646.[CrossRef]
    [Google Scholar]
  20. Honda, M., Brown, E. A. & Lemon, S. M. ( 1996; ). Stability of a stem–loop involving the initiator AUG controls the efficiency of internal initiation of translation on hepatitis C virus RNA. RNA 2, 955-968.
    [Google Scholar]
  21. Horie, H., Koike, S., Kurata, T., Sato-Yoshida, Y., Ise, I., Ota, Y., Abe, S., Hioki, K., Kato, H., Taya, C., Nomura, T., Hashizume, S., Yonekawa, H. & Nomoto, A. ( 1994; ). Transgenic mice carrying the human poliovirus receptor: new animal model for study of poliovirus neurovirulence. Journal of Virology 68, 681-688.
    [Google Scholar]
  22. Iizuka, N., Yonekawa, H. & Nomoto, A. ( 1991; ). Nucleotide sequences important for translation initiation of enterovirus RNA. Journal of Virology 65, 4867-4873.
    [Google Scholar]
  23. Iizuka, N., Najita, L., Franzusoff, A. & Sarnow, P. ( 1994; ). Cap-dependent and cap-independent translation by internal initiation of mRNAs in cell extracts prepared from Saccharomyces cerevisiae. Molecular and Cellular Biology 14, 7322-7330.
    [Google Scholar]
  24. Ito, T., Mukaigawa, J., Zuo, J., Mitamura, K. & Yasui, K. (1996). Propagation of hepatitis C virus in a hybrid cell line derived from a human hepatocyte and a hepatoblastoma cell line. XI Triennial International Symposium on Viral Hepatitis and Liver Disease, April 21–25 1996, Rome. Abstract, p. 151.
  25. Ivanov, P. A., Karpova, O. V., Skulachev, M. V., Tomashevskaya, O. L., Rodionova, N. P., Dorokhov, Y. L. & Atabekov, J. G. ( 1997; ). A tobamovirus genome that contains an internal ribosome entry site functional in vitro. Virology 232, 32-43.[CrossRef]
    [Google Scholar]
  26. Jang, S. K., Kräusslich, H. G., Nicklin, M. J. H., Duke, G. M., Palmenberg, A. C. & Wimmer, E. ( 1988; ). A segment of the 5′ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. Journal of Virology 62, 2636-2643.
    [Google Scholar]
  27. Kaminski, A., Howell, M. T. & Jackson, R. J. ( 1990; ). Initiation of encephalomyocarditis virus RNA translation: the authentic initiation site is not selected by a scanning mechanism. EMBO Journal 9, 3753-3759.
    [Google Scholar]
  28. Kamoshita, N., Tsukiyama-Kohara, K., Kohara, M. & Nomoto, A. ( 1997; ). Genetic analysis of internal ribosomal entry site on hepatitis C virus RNA: implication for involvement of the highly ordered structure and cell type-specific transacting factors. Virology 233, 9-18.[CrossRef]
    [Google Scholar]
  29. Kato, N., Hijikata, M., Ootsuyama, Y., Nakagawa, M., Ohkoshi, S., Sugimura, T. & Shimotohno, K. ( 1990; ). Molecular cloning of the human hepatitis C virus genome from Japanese patient with nonA, nonB hepatitis. Proceedings of the National Academy of Sciences, USA 87, 9524-9528.[CrossRef]
    [Google Scholar]
  30. Kawamura, N., Kohara, M., Abe, S., Komatsu, T., Tago, K., Arita, M. & Nomoto, A. ( 1989; ). Determinants in the 5′ noncoding region of poliovirus Sabin 1 RNA that influence the attenuation phenotype. Journal of Virology 63, 1302-1309.
    [Google Scholar]
  31. Kohara, M., Kaito, M., Wakita, T., Kohara, K. T., Higashi, K., Ohmori, H., Inoue, K., Matsuura, Y., Yasui, K. & Watanabe, S. (1998). Maturation process of virion-like structure in transfected IMY cells with entire HCV genome. 5th International Meeting on Hepatitis C Virus & Related Viruses, Session B. June 24–28 1998, Venezia. Abstract.
  32. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.[CrossRef]
    [Google Scholar]
  33. Le, S.-Y., Sonenberg, N. & Maizel, J. V.Jr ( 1995; ). Unusual folding regions and ribosome landing pad within hepatitis C virus and pestivirus RNAs. Gene 154, 137-143.[CrossRef]
    [Google Scholar]
  34. Lu, H.-H. & Wimmer, E. ( 1996; ). Poliovirus chimeras replicating under the translational control of genetic elements of hepatitis C virus reveal unusual properties of the internal ribosomal entry site of hepatitis C virus. Proceedings of the National Academy of Sciences, USA 93, 1412-1417.[CrossRef]
    [Google Scholar]
  35. Macadam, A. J., Pollard, S. R., Ferguson, G., Dunn, G., Skuce, R., Almond, J. W. & Minor, P. D. ( 1991; ). The 5′ noncoding region of the type 2 poliovirus vaccine strain contains determinants of attenuation and temperature sensitivity. Virology 181, 451-458.[CrossRef]
    [Google Scholar]
  36. Macejak, D. G. & Sarnow, P. ( 1991; ). Internal initiation of translation mediated by the 5′ leader of a cellular mRNA. Nature 353, 90-94.
    [Google Scholar]
  37. Maraia, R. J. ( 1996; ). Transcription termination factor La is also an initiation factor for RNA polymerase III. Proceedings of the National Academy of Sciences, USA 93, 3383-3387.[CrossRef]
    [Google Scholar]
  38. Maraia, R. J., Kenan, D. J. & Keene, J. D. ( 1994; ). Eukaryotic transcription termination factor La mediates transcript release and facilitates reinitiation by RNA polymerase III. Molecular and Cellular Biology 14, 2147-2158.
    [Google Scholar]
  39. Meerovitch, K., Pelletier, J. & Sonenberg, N. ( 1989; ). A cellular protein that binds to the 5′-noncoding region of poliovirus RNA: implications for internal translation initiation. Genes and Development 3, 1026-1034.[CrossRef]
    [Google Scholar]
  40. Meerovitch, K., Svitkin, Y. V., Lee, H. S., Lejbkowicz, F., Kenan, D. J., Chan, E. K. L., Agol, V. I., Keene, J. D. & Sonenberg, N. ( 1993; ). La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. Journal of Virology 67, 3798-3807.
    [Google Scholar]
  41. Oh, S.-K., Scott, M. P. & Sarnow, P. ( 1992; ). Homeotic gene Antennapedia mRNA contains 5′-noncoding sequences that confer translational initiation by internal ribosome binding. Genes & Development 6, 1643-1653.[CrossRef]
    [Google Scholar]
  42. Pelletier, J. & Sonenberg, N. ( 1988; ). Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334, 320-325.[CrossRef]
    [Google Scholar]
  43. Pestova, T. V., Shatsky, I. N., Fletcher, S. P., Jackson, R. J. & Hellen, C. U. T. ( 1998; ). A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes & Development 12, 67-83.[CrossRef]
    [Google Scholar]
  44. Poole, T. L., Wang, C., Popp, R. A., Potgieter, L. N. D., Siddiqui, A. & Collet, M. S. ( 1995; ). Pestivirus translation initiation occurs by internal ribosome entry. Virology 206, 750-754.[CrossRef]
    [Google Scholar]
  45. Reynolds, J. E., Kaminski, A., Kettinen, H. J., Grace, K., Clarke, B. E., Carroll, A. R., Rowlands, D. J. & Jackson, R. J. ( 1995; ). Unique features of internal initiation of hepatitis C virus RNA translation. EMBO Journal 14, 6010-6020.
    [Google Scholar]
  46. Scheper, G. C., Voorma, H. O. & Thomas, A. A. M. ( 1992; ). Eukaryotic initiation factors-4E and -4F stimulate 5′cap-dependent as well as internal initiation of protein synthesis. Journal of Biological Chemistry 267, 7269-7274.
    [Google Scholar]
  47. Shiroki, K., Ishii, T., Aoki, T., Ota, Y., Yang, W.-X., Komatsu, T., Ami, Y., Arita, M., Abe, S., Hashizume, S. & Nomoto, A. ( 1997; ). Host range phenotype induced by mutations in the internal ribosomal entry site of poliovirus RNA. Journal of Virology 71, 1-8.
    [Google Scholar]
  48. Shiroki, K., Isoyama, T., Kuge, S., Ishii, T., Ohmi, S., Hata, S., Suzuki, K., Takasaki, Y. & Nomoto, A. ( 1999; ). Intracellular redistribution of truncated La protein produced by poliovirus 3Cpro-mediated cleavage. Journal of Virology 73, 2193-2200.
    [Google Scholar]
  49. Sizova, D. V., Kolupaeva, V. G., Pestova, T. V., Shatsky, I. N. & Hellen, C. U. T. ( 1998; ). Specific interaction of eukaryotic translation initiation factor 3 with the 5′ nontranslated regions of hepatitis C virus and classical swine fever virus RNAs. Journal of Virology 72, 4775-4782.
    [Google Scholar]
  50. Svitkin, Y. V., Meerovitch, K., Lee, H. S., Dholakia, J. N., Kenan, D. J., Agol, V. I. & Sonenberg, N. ( 1994; ). Internal translation initiation on poliovirus RNA: further characterization of La function in poliovirus translation in vitro. Journal of Virology 68, 1544-1550.
    [Google Scholar]
  51. Takamizawa, A., Mori, C., Fuke, I., Manabe, S., Murakami, S., Fujita, J., Onishi, E., Andoh, T., Yoshida, I. & Okayama, H. ( 1991; ). Structure and organization of the hepatitis C virus genome isolated from human carriers. Journal of Virology 65, 1105-1113.
    [Google Scholar]
  52. Tan, E. M. ( 1989; ). Antinuclear antibodies: diagnostic markers for autoimmune diseases and probes for cell biology. Advances in Immunology 44, 93-151.
    [Google Scholar]
  53. Thiel, V. & Siddell, S. G. ( 1994; ). Internal ribosome entry in the coding region of murine hepatitis virus mRNA 5. Journal of General Virology 75, 3041-3046.[CrossRef]
    [Google Scholar]
  54. Toyoda, H., Koide, N., Kamiyama, M., Tobita, K., Mizumoto, K. & Imura, N. ( 1994; ). Host factors required for internal initiation of translation on poliovirus RNA. Archives of Virology 138, 1-15.[CrossRef]
    [Google Scholar]
  55. Tsukiyama-Kohara, K., Iizuka, N., Kohara, M. & Nomoto, A. ( 1992; ). Internal ribosome entry site within hepatitis C virus RNA. Journal of Virology 66, 1476-1483.
    [Google Scholar]
  56. Wang, C., Sarnow, P. & Siddiqui, A. ( 1993; ). Translation of human hepatitis C virus RNA in cultured cells is mediated by an internal ribosome-binding mechanism. Journal of Virology 67, 3338-3344.
    [Google Scholar]
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