Ribosome shunting in the cauliflower mosaic virus 35S RNA leader is a special case of reinitiation of translation functioning in plant and animal systems

Genes and Development

Volumn 14, Issue 7, 2000, Pages 817-829

  Ryabova, Lyubov A ^a   Hohn, Thomas ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

AdoMetDC; Rabbit reticulocyte lysate; Scanning; sORF; Translational control; Wheat germ extract

Indexed keywords

ARTICLE; CAULIFLOWER MOSAIC VIRUS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; RNA SEQUENCE; RNA TRANSLATION; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CAULIMOVIRUS; CELL-FREE SYSTEM; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; OPEN READING FRAMES; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PLASMIDS; PROTEIN BIOSYNTHESIS; RABBITS; RETICULOCYTES; RIBOSOMES; RNA, SPLICED LEADER; RNA, VIRAL; SEEDS; TRANSCRIPTION, GENETIC; TRITICUM;

ANIMALIA; BRASSICA OLERACEA VAR. BOTRYTIS; CAULIFLOWER MOSAIC VIRUS; MAMMALIA; ORYCTOLAGUS CUNICULUS; TRITICUM AESTIVUM;

EID: 0034175559     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (55)

1. Anthony, D.D. and W.C. Merrick. 1992. Analysis of 40 S and 80 S complexes with mRNA as measured by sucrose density gradients and primer extension inhibition. J. Biol. Chem. 267: 1554-1562.
2. Bonneville, J.-M., H. Sanfacon, J. Fütterer, and T. Hohn. 1989. Posttranscriptional transactivation in cauliflower mosaic virus. Cell 59: 1135-1143.
3. Cao, J. and A.P. Geballe. 1996a. Coding sequence-dependent ribosomal arrest at termination of translation. Mol. Cell. Biol. 16: 603-608.
4. _. 1996b. Inhibition of nascent-peptide release at translation termination. Mol. Cell. Biol. 16: 7109-7114.
5. _. 1998. Ribosomal release without peptidyl tRNA hydrolysis at translation termination in a eukaryotic system. RNA 4: 181-188.
6. Curran, J. and D. Kolakofsky. 1988. Scanning independent ribosomal initiation of the sendai virus X protein. EMBO J. 7: 2869-2874.
7. Delbecq, P., M. Werner, A. Feller, R.K. Filipkowski, F. Messenguy, and A. Piérard. 1994. A segment of mRNA encoding the leader peptide of the CPA1 gene confers repression by arginine on a heterologous yeast gene transcript. Mol. Cell. Biol. 14: 2378-2390.
8. Dever, T.E., L. Feng, R.C. Wek, A.M. Cigan, T.F. Donahue, and A.G. Hinnebusch. 1992. Phosphorylation of initiation factor 2 alpha by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68: 585-596.
9. Dominguez, D.I., L.A. Ryabova, M.M. Pooggin, W. Schmidt-Puchta, J. Fütterer, and T. Hohn. 1998. Ribosome shunting in cauliflower mosaic virus. Identification of an essential and sufficient structural element. J. Biol. Chem. 273: 3669-3678.
10. Franck, A., H. Guilley, G. Jonard, K.E. Richards, and L. Hirth. 1980. Nucleotide sequence of cauliflower mosaic virus DNA. Cell 21: 285-294.
11. Fütterer, J. and T. Hohn. 1991. Translation of a polycistronic mRNA in presence of the cauliflower mosaic virus transactivator protein. EMBO J. 10: 3887-3896.
12. _. 1992. Role of an upstream open reading frame in the translation of polycistronic mRNA in plant cells. Nucleic Acids Res. 20: 3851-3857.
13. _. 1996. Translation in plants - rules and exceptions. Plant Mol. Biol. 32: 159-189.
14. Fütterer, J., K. Gordon, P. Pfeiffer, H. Sanfaçon, B. Pisan, J. Bonneville, and T. Hohn. 1989. Differential inhibition of downstream gene expression by the cauliflower mosaic virus 35S RNA leader. Virus Genes 3: 45-55.
15. Fütterer, J., K. Gordon, H. Sanfaçon, J.M. Bonneville, and T. Hohn. 1990. Positive and negative control of translation by the leader of cauliflower mosaic virus pregenomic 35S RNA. EMBO J. 9: 1697-1707.
16. Fütterer, J., Z. Kiss-László, and T. Hohn. 1993. Nonlinear ribosome migration on cauliflower mosaic virus 35S RNA. Cell 73: 789-802.
17. Fütterer, J., I. Potrykus, Y. Bao, L. Li, T.M. Burns, R. Hull, and T. Hohn. 1996. Position-dependent ATT initiation during plant pararetrovirus Rice Tungro Bacilliform Virus translation. J. Virol. 70: 2999-3010.
18. Geballe, A.P. and D.R. Morris. 1994. Initiation codons within 5′-leaders of mRNAs as regulators of translation. Trends Biochem. Sci. 19: 159-164.
19. Gowda, S., F.C. Wu, H.B. Schlthof, and R.J. Shepherd. 1989. Gene VI of figwort mosaic virus (caulimovirus group) functions in posttranscriptional expression of genes on the full-length RNA transcript. Proc. Natl. Acad. Sci. 86: 9203-9207.
20. Gurevich, V.V. 1996. Use of bacteriophage RNA polymerase in RNA synthesis. Methods Enzymol. 275: 382-397.
21. Hemmings-Mieszczak, M. and T. Hohn. 1999. A stable hairpin preceded by a short ORF promotes nonlinear ribosome migration on a synthetic mRNA leader. RNA 5: 1149-1157.
22. Hemmings-Mieszczak, M., G. Steger, and T. Hohn. 1997. Alternative structures of the cauliflower mosaic virus 35 S RNA leader: Implications for viral expression and replication. J. Mol. Biol. 267: 1075-1088.
23. _. 1998. Regulation of CaMV 35 S RNA translation is mediated by a stable hairpin in the leader. RNA 4: 101-111.
24. Herbst, K.L., L.M. Nichols, R.F. Gesteland, and R.B. Weiss. 1994. A mutation in ribosomal protein L9 affects ribosomal hopping during translation of gene 60 from bacteriophage T4. Proc. Natl. Acad. Sci. 91: 12525-12529.
25. Hill, J.R. and D.R. Morris. 1992. Cell-specific translation of S-adenosylmethionine decarboxylase mRNA. J. Biol. Chem. 267: 21886-21893.
26. _. 1993. Cell-specific translational regulation of S-adenosylmethionine decarboxylase mRNA. J. Biol. Chem. 268: 726-731.
27. Hinnebusch, A.G. 1997. Translational regulation of yeast GCN4. A window on factors that control initiator-tRNA binding to the ribosome. J. Biol. Chem. 272: 21661-21664.
28. Hohn, T., D.I. Dominguez, N. Schärer-Hernandez, M.M. Pooggin, W. Schmidt-Puchta, M. Hemmings-Mieszczak, and J. Fütterer. 1998. Ribosome shunting in eukaryotes: What the viruses tell me. In A look beyond transcription: Mechanisms determining mRNA stability and translation in plants (ed. J. Bailey-Serres and D.R. Gallie) pp. 84-95. American Society of Plant Physiologists, Rockville, MD.
29. Jackson, R.J. 1996. A comparative view of initiation site selection mechanisms. In Translational control (ed. J.W.B. Hershey, M.B. Mathews, and N. Sonenberg), pp. 71-112. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
30. Jaramillo, M., T.E. Dever, W.C. Merrick, and N. Sonenberg. 1991. RNA unwinding in translation: assembly of helicase complex intermediates comprising eukaryotic initiation factors eIF-4F and eIF-4B. Mol. Cell. Biol. 11: 5992-5997.
31. Kozak, M. 1987. Effects of intercistronic length on the efficiency of reinitiation by eukaryotic ribosomes. Mol. Cell. Biol. 7: 3438-3445.
32. _. 1989. Context effects and inefficient initiation at non-AUG codons in eukaryotic cell-free translation systems. Mol. Cell. Biol. 9: 5073-5080.
33. _. 1990. Downstream secondary structure facilitates recognition of initiator codons by eukaryotic ribosomes. Proc. Natl. Acad. Sci. 87: 8301-8305.
34. _. 1999. Initiation of translation in prokaryotes and eukaryotes. Gene 234: 187-208.
35. Latorre, P., D. Kolakofsky, and J. Curran. 1998. Sendai virus Y proteins are initiated by a ribosomal shunt. Mol. Cell. Biol. 18: 5021-5031.
36. Luukkonen, B.C., W. Tan, and S. Schwartz. 1995. Efficiency of reinitiation of translation on human immunodeficiency virus type 1 mRNAs is determined by the length of the upstream open reading frame and by intercistronic distance. J. Virol. 69: 4086-4094.
37. Miller, P.F. and A.G. Hinnebusch. 1989. Sequences that surround the stop codons of upstream open reading frames in GCN4 mRNA determine their distinct functions in translational control. Genes & Dev. 3: 1217-1225.
38. Mize, G.J., H. Ruan, J.J. Low, and D.R. Morris. 1998. The inhibitory upstream open reading frame from mammalian S-adenosylmethionine decarhoxylase mRNA has a strict sequence specificity in critical positions. J. Biol. Chem. 273: 32500-32505.
39. Paraskeva, E., N.K. Gray, B. Schlager, K. Wehr, and M.W. Hentze. 1999. Ribosomal pausing and scanning arrest as mechanisms of translation regulation from cap-distal iron-responsive elements. Mol. Cell Biol. 19: 807-816.
40. Pestova, T.V., S.I. Borukhov, and C.U. Hellen. 1998. Eukaryotic ribosomes require initiation factors 1 and 1A to locate initiation codons. Nature 394: 854-859.
41. Pooggin, M.M., T. Hohn, and J. Fütterer. 1998. Forced evolution reveals the importance of short open reading frame A and secondary structure in the cauliflower mosaic virus 35S RNA leader. J. Virol. 72: 4157-4169.
42. Pooggin, M.M., J. Fütterer, K.G. Skryabin, and T. Hohn. 1999. A short open reading frame terminating in front of a stable hairpin is the conserved feature in pregenomic RNA leaders of plant pararetroviruses. J. Gen. Virol. 80: 2217-2228.
43. Pooggin, M.M., T. Hohn, and J. Fütterer. 2000. Role of a short ORF in ribosome shunt on the CaMV RNA leader. J. Biol. Chem. (in press).
44. Remm, M., A. Remm, and M. Ustav. 1999. Human papillomavirus type 18 E1 protein is translated from polycistronic mRNA by a discontinuous scanning mechanism. J. Virol. 73: 3062-3070.
45. Reynolds, J.E., A. Kaminski, H.J. Kettinen, K. Grace, B.E. Clarke, A.R. Carroll, D.J. Rowlands, and R.J. Jackson. 1995. Unique features of internal initiation of hepatitis C virus RNA translation. EMBO J. 14: 6010-6020.
46. Roberts, B.E. and B.M. Paterson. 1973. Efficient translation of tobacco mosaic virus RNA and rabbit globin 9S RNA in a cell-free system from commercial wheat germ. Proc. Natl. Acad. Sci. 70: 2330-2334.
47. Schagger, H. and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166: 368-379.
48. Schleiss, M.R., C.R. Degnin, and A.P. Geballe. 1991. Translational control of human cytomegalovirus gp48 expression. J. Virol. 65: 6782-6789.
49. Schmidt-Puchta, W., D. Dominguez, D. Lewetag, and T. Hohn. 1997. Plant ribosome shunting in vitro. Nucleic Acids Res. 25: 2854-2860.
50. Wang, Z. and M.S. Sachs. 1997a. Arginine-specific regulation mediated by the Neurospora crassa arg-2 upstream open reading frame in a homologous, cell-free in vitro translation system. J. Biol. Chem. 272: 255-261.
51. _. 1997b. Ribosomal stalling is responsible for arginine-specific translation attenuation in Neurospora crassa. J. Biol. Chem. 272: 255-261.
52. Werner, M., A. Feller, F. Messcnguy, and A. Piérard. 1987. The leader peptide of yeast gene CPA1 is essential for the translational repression of its expression. Cell 49: 805-813.
53. Yueh, A. and R.J. Schneider. 1996. Selective translation initiation by ribosome jumping in adenovirus-infected and heat shocked cells. Genes & Dev. 10: 1557-1567.
54. _. 2000. Translation by ribosome shunting on adenovirus and hsp70 mRNAs facilitated by complementarity to 18S rRNA. Genes & Dev. 14: 414-421.
55. Zuker, M. 1989. Computer prediction of RNA structure. Methods Enzymol. 180: 262-288.