Abstract
The circadian-expressed luciferin-binding protein from the dinoflagellate Gonyaulax polyedra is regulated at the translational level. We detected a protein, apparently a dimer, that binds specifically to the 3' untranslated region of its mRNA. Its binding site was localized within a 22-nt region in the 3' untranslated region containing seven UG repeats. The binding activity of this protein cycles on a daily basis, decreasing at the beginning of the night when synthesis of luciferin-binding protein starts and increasing at the end of the night when synthesis of luciferin-binding protein stops. This suggests that it functions as a clock-controlled repressor, preventing the translation of lbp mRNA during the day.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Abrahams J. P., van den Berg M., van Batenburg E., Pleij C. Prediction of RNA secondary structure, including pseudoknotting, by computer simulation. Nucleic Acids Res. 1990 May 25;18(10):3035–3044. doi: 10.1093/nar/18.10.3035. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dunlap J. C. Genetic analysis of circadian clocks. Annu Rev Physiol. 1993;55:683–728. doi: 10.1146/annurev.ph.55.030193.003343. [DOI] [PubMed] [Google Scholar]
- Fritz L., Morse D., Hastings J. W. The circadian bioluminescence rhythm of Gonyaulax is related to daily variations in the number of light-emitting organelles. J Cell Sci. 1990 Feb;95(Pt 2):321–328. doi: 10.1242/jcs.95.2.321. [DOI] [PubMed] [Google Scholar]
- Giordano T., Sakamoto K., Howard B. H. Detection of protein/RNA interactions in nuclear extracts is facilitated by poly r(G). Nucleic Acids Res. 1990 Aug 11;18(15):4627–4627. doi: 10.1093/nar/18.15.4627. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goodwin E. B., Okkema P. G., Evans T. C., Kimble J. Translational regulation of tra-2 by its 3' untranslated region controls sexual identity in C. elegans. Cell. 1993 Oct 22;75(2):329–339. doi: 10.1016/0092-8674(93)80074-o. [DOI] [PubMed] [Google Scholar]
- Hardin P. E., Hall J. C., Rosbash M. Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature. 1990 Feb 8;343(6258):536–540. doi: 10.1038/343536a0. [DOI] [PubMed] [Google Scholar]
- Hunter T., Karin M. The regulation of transcription by phosphorylation. Cell. 1992 Aug 7;70(3):375–387. doi: 10.1016/0092-8674(92)90162-6. [DOI] [PubMed] [Google Scholar]
- Jackson F. R., Bargiello T. A., Yun S. H., Young M. W. Product of per locus of Drosophila shares homology with proteoglycans. Nature. 1986 Mar 13;320(6058):185–188. doi: 10.1038/320185a0. [DOI] [PubMed] [Google Scholar]
- Jackson R. J. Cytoplasmic regulation of mRNA function: the importance of the 3' untranslated region. Cell. 1993 Jul 16;74(1):9–14. doi: 10.1016/0092-8674(93)90290-7. [DOI] [PubMed] [Google Scholar]
- Jaffrey S. R., Haile D. J., Klausner R. D., Harford J. B. The interaction between the iron-responsive element binding protein and its cognate RNA is highly dependent upon both RNA sequence and structure. Nucleic Acids Res. 1993 Sep 25;21(19):4627–4631. doi: 10.1093/nar/21.19.4627. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson C. H., Roeber J. F., Hastings J. W. Circadian changes in enzyme concentration account for rhythm of enzyme activity in gonyaulax. Science. 1984 Mar 30;223(4643):1428–1430. doi: 10.1126/science.223.4643.1428. [DOI] [PubMed] [Google Scholar]
- Klausner R. D., Rouault T. A., Harford J. B. Regulating the fate of mRNA: the control of cellular iron metabolism. Cell. 1993 Jan 15;72(1):19–28. doi: 10.1016/0092-8674(93)90046-s. [DOI] [PubMed] [Google Scholar]
- Kondo T., Strayer C. A., Kulkarni R. D., Taylor W., Ishiura M., Golden S. S., Johnson C. H. Circadian rhythms in prokaryotes: luciferase as a reporter of circadian gene expression in cyanobacteria. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5672–5676. doi: 10.1073/pnas.90.12.5672. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kwon Y. K., Hecht N. B. Binding of a phosphoprotein to the 3' untranslated region of the mouse protamine 2 mRNA temporally represses its translation. Mol Cell Biol. 1993 Oct;13(10):6547–6557. doi: 10.1128/mcb.13.10.6547. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kwon Y. K., Hecht N. B. Cytoplasmic protein binding to highly conserved sequences in the 3' untranslated region of mouse protamine 2 mRNA, a translationally regulated transcript of male germ cells. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3584–3588. doi: 10.1073/pnas.88.9.3584. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lee D. H., Mittag M., Sczekan S., Morse D., Hastings J. W. Molecular cloning and genomic organization of a gene for luciferin-binding protein from the dinoflagellate Gonyaulax polyedra. J Biol Chem. 1993 Apr 25;268(12):8842–8850. [PubMed] [Google Scholar]
- Mattaj I. W. RNA recognition: a family matter? Cell. 1993 Jun 4;73(5):837–840. doi: 10.1016/0092-8674(93)90265-r. [DOI] [PubMed] [Google Scholar]
- McClung C. R., Fox B. A., Dunlap J. C. The Neurospora clock gene frequency shares a sequence element with the Drosophila clock gene period. Nature. 1989 Jun 15;339(6225):558–562. doi: 10.1038/339558a0. [DOI] [PubMed] [Google Scholar]
- Morse D. S., Fritz L., Hastings J. W. What is the clock? Translational regulation of circadian bioluminescence. Trends Biochem Sci. 1990 Jul;15(7):262–265. doi: 10.1016/0968-0004(90)90050-l. [DOI] [PubMed] [Google Scholar]
- Morse D., Milos P. M., Roux E., Hastings J. W. Circadian regulation of bioluminescence in Gonyaulax involves translational control. Proc Natl Acad Sci U S A. 1989 Jan;86(1):172–176. doi: 10.1073/pnas.86.1.172. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reddy P., Jacquier A. C., Abovich N., Petersen G., Rosbash M. The period clock locus of D. melanogaster codes for a proteoglycan. Cell. 1986 Jul 4;46(1):53–61. doi: 10.1016/0092-8674(86)90859-7. [DOI] [PubMed] [Google Scholar]
- Strub K., Walter P. Assembly of the Alu domain of the signal recognition particle (SRP): dimerization of the two protein components is required for efficient binding to SRP RNA. Mol Cell Biol. 1990 Feb;10(2):777–784. doi: 10.1128/mcb.10.2.777. [DOI] [PMC free article] [PubMed] [Google Scholar]
- You Y., Chen C. Y., Shyu A. B. U-rich sequence-binding proteins (URBPs) interacting with a 20-nucleotide U-rich sequence in the 3' untranslated region of c-fos mRNA may be involved in the first step of c-fos mRNA degradation. Mol Cell Biol. 1992 Jul;12(7):2931–2940. doi: 10.1128/mcb.12.7.2931. [DOI] [PMC free article] [PubMed] [Google Scholar]