Preferential translation mediated by Hsp81-3 5′-UTR during heat shock involves ribosome entry at the 5′-end rather than an internal site in Arabidopsis suspension cells

Journal of Bioscience and Bioengineering

Volumn 105, Issue 1, 2008, Pages 39-47

  Matsuura, Hideyuki ^a   Shinmyo, Atsuhiko ^a   Kato, Ko ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

5 untranslated region; Arabidopsis Hsp90gene; heat shock; protoplast transient expression assay; translational regulation

Indexed keywords

ARABIDOPSIS HSP90GENE; PROTOPLAST TRANSIENT EXPRESSION ASSAYS; RIBOSOME; TRANSLATIONAL REGULATION;

BIOASSAY; GENES; PLANTS (BOTANY); RNA;

PROTEINS;

HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 81; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARABIDOPSIS; ARTICLE; CELL SUSPENSION; HEAT SHOCK; HOUSEKEEPING GENE; POLYSOME; PROTEIN FAMILY; PROTOPLAST; RIBOSOME; RNA CAPPING; RNA TRANSLATION; TEMPERATURE; TRANSLATION INITIATION; TRANSLATION REGULATION;

5' UNTRANSLATED REGIONS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; HEAT-SHOCK RESPONSE; HSP90 HEAT-SHOCK PROTEINS; MOLECULAR SEQUENCE DATA; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; RIBOSOMES;

ARABIDOPSIS;

EID: 39449089219     PISSN: 13891723     EISSN: None     Source Type: Journal    
DOI: 10.1263/jbb.105.39     Document Type: Article

References (44)

1. Schneider R.J. Translational control during heat shock. In: Sonenberg N., Hershey J.W.B., and Mathews M.B. (Eds). Translational control of gene expression (2000), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 581-593
2. Panniers R. Translational control during heat shock. Biochimie 76 (1994) 737-747
3. Duncan R.F. Translational control during heat shock. In: Hershey J.W.B., Mathews M.B., and Sonenberg N. (Eds). Translational control (1996), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 271-294
4. Kozak M. Pushing the limits of the scanning mechanism for initiation of translation. Gene 299 (2002) 1-34
5. Raught B., Gingras A.-C., and Sonenberg N. Regulation of ribosome recruitment in eukaryotes. In: Sonenberg N., Hershey J.W.B., and Mathews M.B. (Eds). Translational control of gene expression (2000), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 245-293
6. Joshi-Barve S., De Benedetti A., and Rhoads R.E. Preferential translation of heat shock mRNAs in HeLa cells deficient in protein syntheses initiation factors eIF-4E and eIF-4 gamma. J. Biol. Chem. 267 (1992) 21038-21043
7. Elroy-Stein O., and Merrick W.C. Translation initiation via cellular internal ribosome entry sites. In: Mathews M.B., Sonenberg N., and Herwhey J.W. (Eds). Translational control in biology and medicine (2007), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 155-172
8. Holcik M., and Sonenberg N. Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol. 6 (2005) 318-327
9. Neumann D., Nover L., Parthier B., Rieger R., Scharf K.D., Wollgiehn R., and zur Nieden U. Heat shock and other stress response systems of plants. Results Probl. Cell Differ. 16 (1989) 1-155
10. Gallie D.R., Caldwell C., and Pitto L. Heat shock disrupts cap and poly(A) tail function during translation and increases mRNA stability of introduced reporter mRNA. Plant Physiol. 108 (1995) 1703-1713
11. Pitto L., Gallie D.R., and Walbot V. Role of the leader sequence during thermal repression of translation in maize, tobacco, and carrot protoplasts. Plant Physiol. 100 (1992) 1827-1833
12. Dinkova T.D., Zepeda H., Martinez-Salas E., Martinez L.M., Nieto-Sotelo J., and de Jimenez E.S. Cap-independent translation of maize Hsp101. Plant J. 41 (2005) 722-731
13. Kawaguchi R., and Bailey-Serres J. Regulation of translational initiation in plants. Curr. Opin. Plant Biol. 5 (2002) 460-465
14. Yabe N., Takahashi T., and Komeda Y. Analysis of tissue-specific expression of Arabidopsis thaliana HSP90-family gene HSP81. Plant Cell Physiol. 35 (1994) 1207-1219
15. Axelos M., Curie C., Mazzolini L., Bardet C., and Lescure B. A protocol for transient gene expression in Arabidopsis thaliana protoplasts isolated from cell suspension cultures. Plant Physiol. Biochem. 30 (1992) 123-128
16. Kodama Y., Nagaya S., Shinmyo A., and Kato K. Mapping and characterization of DNase I hypersensitive sites in Arabidopsis chromatin. Plant Cell Physiol. 48 (2007) 459-470
17. Davies E., and Abe S. Methods for isolation and analysis of polyribosomes. Methods Cell Biol. 50 (1995) 209-222
18. Matsuo N., Gilmartin P.M., and Hiratsuka K. Characterization of the EMCV-IRES mediated bicistronic translation in plant cells. Plant Biotechnol. 21 (2004) 119-126
19. Van Lijsebettens M., Vanderhaeghen R., De Block M., Bauw G., Villarroel R., and Van Montagu M. An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J. 13 (1994) 3378-3388
20. Satoh J., Kato K., and Shinmyo A. The 5′-untranslated region of the tobacco alcohol dehydrogenase gene functions as an effective translational enhancer in plant. J. Biosci. Bioeng. 98 (2004) 1-8
21. Kovtun Y., Chiu W.L., Tena G., and Sheen J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97 (2000) 2940-2945
22. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
23. Key J.L., Lin C.Y., and Chen Y.M. Heat shock proteins of higher plants. Proc. Natl. Acad. Sci. USA 78 (1981) 3526-3530
24. Stuger R., Ranostaj S., Materna T., and Forreiter C. Messenger RNA-binding properties of nonpolysomal ribonucleoproteins from heat-stressed tomato cells. Plant Physiol. 120 (1999) 23-32
25. Apuya N.R., and Zimmerman J.L. Heat shock gene expression is controlled primarily at the translational level in carrot cells and somatic embryos. Plant Cell 4 (1992) 657-665
26. Nover L., Scharf K.D., and Neumann D. Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs. Mol. Cell. Biol. 9 (1989) 1298-1308
27. Calzone F.J., Angerer R.C., and Gorovsky M.A. Regulation of protein syntheses in Tetrahymena: isolation and characterization of polysomes by gel filtration and precipitation at pH 5.3. Nucleic Acids Res. 10 (1982) 2145-2161
28. Kozak M. Effects of intercistronic length on the efficiency of reinitiation by eucaryotic ribosomes. Mol. Cell. Biol. 7 (1987) 3438-3445
29. Wang L., and Wessler S.R. Inefficient reinitiation is responsible for upstream open reading frame-mediated translational repression of the maize R gene. Plant Cell 10 (1998) 1733-1746
30. Hultmark D., Klemenz R., and Gehring W.J. Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22. Cell 44 (1986) 429-438
31. Klemenz R., Hultmark D., and Gehring W.J. Selective translation of heat shock mRNA in Drosophila melanogaster depends on sequence information in the leader. EMBO J. 4 (1985) 2053-2060
32. McGarry T.J., and Lindquist S. The preferential translation of Drosophila hsp70 mRNA requires sequences in the untranslated leader. Cell 42 (1985) 903-911
33. Coldwell M.J., deSchoolmeester M.L., Fraser G.A., Pickering B.M., Packham G., and Willis A.E. The p36 isoform of BAG-1 is translated by internal ribosome entry following heat shock. Oncogene 20 (2001) 4095-4100
34. Macejak D.G., and Sarnow P. Internal initiation of translation mediated by the 5′ leader of a cellular mRNA. Nature 353 (1991) 90-94
35. Hess M.A., and Duncan R.F. Sequence and structure determinants of Drosophila Hsp70 mRNA translation: 5′UTR secondary structure specifically inhibits heat shock protein mRNA translation. Nucleic Acids Res. 24 (1996) 2441-2449
36. Yueh A., and Schneider R.J. Translation by ribosome shunting on adenovirus and hsp70 mRNAs facilitated by complementarity to 18S rRNA. Genes Dev. 14 (2000) 414-421
37. Ahmed R., and Duncan R.F. Translational regulation of Hsp90 mRNA. AUG-proximal 5′-untranslated region elements essential for preferential heat shock translation. J. Biol. Chem. 279 (2004) 49919-49930
38. De Gregorio E., Preiss T., and Hentze M.W. Translational activation of uncapped mRNAs by the central part of human eIF4G is 5′ end-dependent. RNA 4 (1998) 828-836
39. Gunnery S., Maivali U., and Mathews M.B. Translation of an uncapped mRNA involves scanning. J. Biol. Chem. 272 (1997) 21642-21646
40. Borman A.M., Kirchweger R., Ziegler E., Rhoads R.E., Skern T., and Kean K.M. elF4G and its proteolytic cleavage products: effect on initiation of protein syntheses from capped, uncapped, and IRES-containing mRNAs. RNA 3 (1997) 186-196
41. Ohlmann T., Rau M., Pain V.M., and Morley S.J. The C-terminal domain of eukaryotic protein syntheses initiation factor (eIF) 4G is sufficient to support cap-independent translation in the absence of eIF4E. EMBO J. 15 (1996) 1371-1382
42. Ali I.K., McKendrick L., Morley S.J., and Jackson R.J. Truncated initiation factor eIF4G lacking an eIF4E binding site can support capped mRNA translation. EMBO J. 20 (2001) 4233-4242
43. Bert A.G., Grepin R., Vadas M.A., and Goodall G.J. Assessing IRES activity in the HIF-1alpha and other cellular 5′ UTRs. RNA 12 (2006) 1074-1083
44. Kozak M. A second look at cellular mRNA sequences said to function as internal ribosome entry sites. Nucleic Acids Res. 33 (2005) 6593-6602