A Xenopus laevis homologue of the La autoantigen binds the pyrimidine tract of the 5' UTR of ribosomal protein mRNAs in vitro: Implication of a protein factor in complex formation

Journal of Molecular Biology

Volumn 259, Issue 5, 1996, Pages 904-915

  Pellizzoni, Livio ^a   Cardinali, Beatrice ^a   Lin Marq, Nathalie ^b   Mercanti, Delio ^a   Pierandrei Amaldi, Paola ^a  

^a CNR   (Italy)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

La protein; Ribosomal protein mRNA; RNA protein interaction; Translational control; Xenopus

Indexed keywords

AUTOANTIGEN; BINDING PROTEIN; DNA DIRECTED RNA POLYMERASE III; MESSENGER RNA; PYRIMIDINE; RIBOSOME PROTEIN;

ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; IMMUNOPRECIPITATION; NONHUMAN; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN RNA BINDING; TRANSCRIPTION TERMINATION; TRANSLATION INITIATION; TRANSLATION REGULATION; XENOPUS LAEVIS;

EID: 0030604692     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0368     Document Type: Article

References (48)

1. Agrawal, M. G. & Bowman, L. H. (1987). Transcriptional and translational regulation of ribosomal protein formation during mouse myoblast differentiation. J. Biol. Chem. 262, 4868-4875.
2. Avni, D., Shama, S., Loreni, F. & Meyuhas, O. (1994). Vertebrate mRNAs with a 5′-terminal pyrimidine tract are candidates for translational repression in quiescent cells. Characterization of the translational cis-regulatory element (TLRE). Mol. Cell. Biol. 14, 3822-3833.
3. Buchmann, M., Pfeifer, K., Schroeder, H. C. & Muller, W. E. G. (1989). La antigen shuttles between the nucleus and the cytoplasm in CV-1 cells. Mol. Cell. Biochem. 85, 103-114.
4. Bachman, M., Pfeifer, K., Schroeder H. C. & Muller, W. E. G. (1990). Characterization of the autoantigen La as a nucleic acid-dependent ATPase/dATPase with melting properties. Cell, 60, 85-93.
5. Cardinali, B., Di Cristina, M. & Pierandrei-Amaldi, P. (1993). Interaction of proteins with the mRNA for ribosomal protein L1 in Xenopus: structural characterization of in vivo complexes and identification of proteins that bind in vitro to its 5′ UTR. Nucl. Acids Res. 21, 2301-2308.
6. Chambers, J. C., Kurilla, M. G. & Keene, J. D. (1983). Association between the 7S RNA and the lupus La protein varies among cell types. J. Biol. Chem. 258, 11438-11441.
7. Chang, Y. N., Kenan, D. J., Keene, J. D., Gatignol, A. & Jeang K.-T. (1994). Direct interactions between autoantigen La and human immunodeficiency virus leader RNA. J. Virol. 68, 7008-7020.
8. Cleveland, D. W., Fischer, S. G., Kirschner, M. W. & Laemli, U. K. (1977). Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J. Biol. Chem. 252, 1102-1106.
9. Dignam, J. D., Lebovitz, R. M. & Roeder, R. G. (1983). Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucl. Acids Res. 11, 1475-1489.
10. Garcia-Blanco, M. A., Jamison, S. G. & Sharp, P. A. (1989). Identification and purification of a 62,000-dalton protein that binds specifically to the polypyrimidine tract of introns. Genes Dev. 3, 1874-1886.
11. Geyer, P. K., Meyuhas, O., Perry, R. P. & Johnson, L. F. (1982). Regulation of ribosomal protein mRNA content and translation in growth-stimulated mouse fibroblasts. Mol. Cell. Biol. 2, 685-693.
12. Gottlieb, E. & Steitz, J. A. (1989). The RNA binding protein La influences both the accuracy and the efficiency of RNA polymerase III transcription in vitro. EMBO J. 8, 841-850.
13. Habets, W. J., den Brok, J. H., Boerbooms, M. T., van de Putte, L. B. A. & van Venrooij, W. J. (1983). Characterization of the SS-B (La) antigen in adenovirus-infected and uninfected HeLa cells. EMBO J. 2, 1625-1631.
14. Hammond, M. L., Merrick, W. & Bowman, L. H. (1991). Sequences mediating the translation of mouse S16 ribosomal protein mRNA during myoblast differentiation and in vitro and possible control points for the in vitro translation. Genes Dev. 5, 1723-1736.
15. Hendrick, J. P., Wolin, S. L., Rinke, J., Lerner, M. R. & Steitz, J. A. (1991). Ro small cytoplasmic ribonucleoproteins are a subclass of La ribonucleoproteins: further characterization of the Ro and La small ribonucleoproteins from infected mammalian cells. Mol. Cell. Biol. 1, 1138-1149.
16. Jackson, R. J. & Kaminski, A. (1995). Internal initiation of translation in eukaryotes: The picornavirus paradigm and beyond. RNA, 1, 985-1000.
17. Jefferies, H. B. J., Reinhard, C., Kozma, S. C. & Thomas, G. (1994). Rapamycin selectively represses translation of the "polypyrimidine tract" mRNA family. Proc. Natl Acad. Sci. USA, 91, 4441-4445.
18. Kaspar, R. L., Tomohito, K., Cranston, H., Morris, D. R. & White, M. W. (1992). A regulatory cis element and a specific binding factor involved in the mitogenetic control of murine ribosomal protein L32 translation. J. Biol. Chem. 267, 508-514.
19. Kurilla, M. G. & Keene, J. D. (1983). The leader RNA of vesicular stomatitis virus is bound by a cellular protein reactive with anti-La lupus antibodies. Cell 34, 837-845.
20. Lerner, M. R. & Steitz, J. A. (1979). Antibodies to small nuclear RNA complexed with proteins are produced by patients with systemic lupus erythematosus. Proc. Natl Acad. Sci. USA, 76, 5495-5499.
21. Levy, S., Avni, D., Hariharan, N., Perry, R. P. & Meyuhas, O. (1991). Oligopyrimidine tract at the 5′ end of mammalian ribosomal protein mRNAs is required for their translational control. Proc. Natl Acad. Sci. USA, 88, 3319-3323.
22. Loreni, F. & Amaldi, F. (1992). Translational regulation of ribosomal protein synthesis in Xenopus cultured cells: mRNA relocation between polysomes and RNP during nutrition shift. Eur. J. Biochem. 205, 1027-1032.
23. Loreni, F., Francesconi, A. & Amaldi, F. (1993). Coordinate translational regulation in the synthesis of elongation factor la and ribosomal protein in Xenopus laevis. Nucl. Acids Res. 21, 4721-4725.
24. Madore, S. J., Wieben, E. D. & Pederson, T. (1984). Eukaryotic small ribonucleoproteins. Anti-La human autoantibodies react with U1 RNA-protein complexes. J. Biol. Chem. 259, 1929-1933.
25. Mariottini, P. & Amaldi, F. (1989). The 5′ untranslated region of mRNA for ribosomal protein S19 is involved in its translational regulation during Xenopus development. Mol. Cell. Biol. 10, 816-822.
26. Mathews, M. B. & Francoeur, A. M. (1984). La antigen recognizes and binds to the 3′-oligouridylate tail of a small RNA. Mol. Cell. Biol. 4, 1134-1140.
27. 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 reticolocyte lysate. J. Virol. 67, 3798-3807.
28. Meyuhas, O., Avni, D. & Shama, S. (1996). Translational control of ribosomal protein mRNAs in eukaryotes. In Translational Control (Hershey, J. W. B., Mathews, M. & Sonenberg, N., eds), pp. 363-388, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
29. Milligan, J. F., Groebe, D. R., Witherell, G. W. & Uhlenbeck O. C. (1987). Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucl. Acids Res. 15, 8783-8798.
30. Murray, M. T., Krohne, G. & Franke, W. W. (1991). Different forms of soluble cytoplasmic mRNA binding proteins and particles in Xenopus laevis oocytes and embryos. J. Cell Biol. 112, 1-11.
31. Neupert, B., Thompson, N. A., Meyer, C. & Kuhn, L. C. (1990). A high yield affinity purification method for specific RNA-binding proteins: isolation of the iron regulatory factor from human placenta. Nucl. Acids Res. 18, 51-55.
32. O'Brien, C. A., Margelot, K. & Wolin, S. L. (1993). Xenopus Ro ribonucleoproteins: Members of an evolutionary conserved class of cytoplasmic ribonucleoproteins. Proc. Natl Acad. Sci. USA, 90, 7250-7254.
33. Patton, J. G., Mayer, S. A., Tempst, P. & Nadal-Ginard, B. (1991). Characterization and molecular cloning of polypyrimidine tract-binding protein: a component of a complex is necessary for pre-mRNA splicing. Genes Dev. 5, 1237-1251.
34. Peek, R., Pruijn, G. J. M., van der Kemp A. J. W. & van Venrooij, W. J. (1993). Subcellular distribution of Ro ribonucleoprotein complexes and their constituents. J. Cell Sci. 106, 929-935.
35. Pierandrei-Amaldi, P. & Amaldi, F. (1994). Aspects of regulation of ribosomal protein synthesis in Xenopus laevis. Genetica, 94, 181-193.
36. Pierandrei-Amaldi, P. & Beccari, E. (1980). Messenger RNA for ribosomal proteins in Xenopus laevis oocytes. Eur. J. Biochem. 106, 603-611.
37. Pierandrei-Amaldi P., Campioni, N., Beccari E., Bozzoni, I. & Amaldi, F. (1982). Expression of ribosomal protein genes in Xenopus laevis. Cell, 30, 163-171.
38. Pierandrei-Amaldi, P., Beccari, E., Bozzoni, I. & Amaldi, F. (1985). Ribosomal protein production in normal and anucleolate Xenopus embryos: regulation at the post-transcriptional and translational levels. Cell, 42, 317-323.
39. Pruijn, G. J. M., Slobbe, R. L. & van Venrooij, W. J. (1990). Structure and function of La and Ro RNPs. Mol. Biol. Rep. 14, 43-48.
40. Scherly, D., Stutz, F., Lin-Marq, N. & Clarkson, S. G. (1993). La proteins from Xenopus laevis cDNA cloning and developmental expression. J. Mol. Biol. 231, 196-204.
41. L32 is a RNA/DNA-binding protein which interacts with conserved elements of the murine L32 ribosomal protein mRNA. Eur. J. Biochem. 229, 426-432.
42. Simons, F. H. M., Pruijn, G. J. M. & van Venrooij, W. J. (1994). Analysis of the intracellular localization and assembly of Ro ribonucleoprotein particles by microinjection into Xenopus laevis oocytes. J. Cell Biol. 125, 981-988.
43. Stefano, J. E. (1984). Purified lupus antigen La recognizes an oligouridylate stretch common to the 3′ termini of RNA polymerase III transcripts. Cell, 36, 145-154.
44. Sonenberg, N. & Meerovitch, K. (1990). Translation of poliovirus mRNA. Enzyme, 44, 93-105.
45. 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. J. Virol. 68, 1544-1550.
46. Svitkin, Y. V., Pause, A. & Sonenberg, N. (1994). La autoantigen alleviates translational repression by the 5′ leader sequence of the human immunodeficiency virus type 1 mRNA. J. Virol. 68, 7001-7007.
47. Terada, N., Patel, H. R., Takase, K., Kohno, K., Nairn, A. C. & Gelfand E. W. (1994). Rapamycin selectively inhibits translation of mRNA encoding elongation factors and ribosomal proteins. Proc. Natl Acad. Sci. USA, 91, 11477-11481.
48. Wool, I. G., Endo, Y., Chan, Y. L. & Gluck, A. (1990). Structure, function and evolution of mammalian ribosomes. In The Ribosome: Structure, Function and Evolution (Hiel, W. E., Dahlberg, A., Garret, R. A., Moore, P. B., Schlessinger, D. & Warner, J. R., eds), pp. 203-214, Am. Soc. Microbiol. Press, Washington, DC.