The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation

Developmental Biology

Volumn 216, Issue 2, 1999, Pages 671-680

  Olsen, Philip H ^a   Ambros, Victor ^a  

^a Lamont Doherty Earth Observatory   (United States)

Author keywords

C. elegans; Heterochronic genes; Lin 4 RNA; Polyribosomes; Translation

Indexed keywords

MESSENGER RNA; POLYADENYLATED RNA; RNA;

ARTICLE; CAENORHABDITIS ELEGANS; GENE EXPRESSION; GENE REPRESSION; LARVAL DEVELOPMENT; NONHUMAN; POLYADENYLATION; POLYSOME; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; TRANSLATION INITIATION;

CAENORHABDITIS ELEGANS; INVERTEBRATA;

EID: 0033572284     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9523     Document Type: Article

References (39)

1. Ahringer J., Rosenquist T. A., Lawson D. N., Kimble J. The Caenorhabditis elegans sex determining gene fem-3 is regulated post-transcriptionally. EMBO J. 11:1992;2303-2310.
2. Ambros V. A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell. 57:1989;49-57.
3. Ambros V., Horvitz H. R. The lin-14 locus of Caenorhabditis elegans controls the time of expression of specific postembryonic developmental events. Genes Dev. 1:1987;398-414.
4. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. Current Protocols in Molecular Biology. 1989;Wiley, New York.
5. Aziz N., Munro H. N. Iron regulates ferritin mRNA translation through a segment of its 5′ untranslated region. Proc. Natl. Acad. Sci. USA. 84:1987;8478-8482.
6. Berry J. O., Carr J. P., Klessig D. F. mRNAs encoding ribulose-1,5- bisphosphate carboxylase remain bound to polysomes but are not translated in amaranth seedlings transferred to darkness. Proc. Natl. Acad. Sci. USA. 85:1988;4190-4194.
7. Candido E. P., Jones D., Dixon D. K., Graham R. W., Russnak R. H., Kay R. J. Structure, organization, and expression of the 16-kd heat shock gene family of Caenorhabditis elegans. Genome. 31:1989;690-697.
8. Ch'ng J. L. C., Shoemaker D. L., Schimmel P., Holmes E. W. Reversal of creatine kinase translational repression by 3′ untranslated sequences. Science. 248:1990;1003-1005.
9. Davies E. Methods for the isolation and analysis of polyribosomes. Methods in Cell Biology. 1995;Academic Press, San Diego. p. 209-222.
10. Dissous C., Lempereur C., Verwaerde C., Krembel J. The use of metrizamide as a density-gradient medium in studies of rat-liver polysomes. Eur. J. Biochem. 64:1976;361-367.
11. Feinbaum R., Ambros V. The timing of lin-4 RNA accumulation controls the timing of postembryonic developmental events in Caenorhabditis elegans. Dev. Biol. 210:1999;87-95.
12. Gavis E. R., Lehmann R. Translational regulation of nanos by RNA localization. Nature. 369:1994;315-318.
13. 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. 75:1993;329-339.
14. Gunkel N., Yano T., Markussen F.-H., Olsen L. C., Ephrussi A. Localization-dependent translation requires a functional interaction between the 5′ and 3′ ends of oskar mRNA. Genes Dev. 12:1998;1652-1664.
15. Henshaw E. C. Messenger RNA in rat liver polyribosomes: Evidence that it exists as ribonucleoprotein particles. J. Mol. Biol. 36:1968;401-411.
16. Jacobson A. Poly(A) metabolism and translation: The closed-loop model. Hershey J. W. B., Matthews M. B., Sonenberg N. Translational Control. 1996;451-480 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
17. Kaspar R. L., Gherke L. Peripheral blood mononuclear cells stimulated with C5a or lipopolysaccharide to synthesize equivalent levels of IL-1b mRNA show unequal IL-1b protein accumulation but similar polyribosome profiles. J. Immunol. 153:1994;277-286.
18. Krause M., Wild M., Rosenzweig B., Hirsh D. Wild-type and mutant actin genes in Caenorhabditis elegans. J. Mol. Biol. 208:1989;381-392.
19. Labarca C., Paigen K. A simple, rapid and sensitive DNA assay procedure. Anal. Biochem. 102:1980;344-352.
20. Lee R. C., Feinbaum R., Ambros V. The heterochronic gene lin-4 of C. elegans encodes two small RNA's with antisense complementarity to lin-14. Cell. 75:1993;843-854.
21. Lie Y. S., Macdonald P. M. Apontic binds the translational repressor Bruno and is implicated in regulation of oskar mRNA translation. Development. 126:1999;1129-11138.
22. Lieberfarb M. E., Chu T., Wreden C., Theurkauf W., Gergen J. P., Strickland S. Mutations that perturb poly(A)-dependent maternal mRNA activation block the initiation of development. Development. 122:1996;579-588.
23. Mathews M. B., Sonenberg N., Hershey J. W. B. Origins and targets of translational control. Hershey J. W. B., Mathews M. B., Sonenberg N. Translational Control. 1996;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
24. Moss E. G., Ambros V. Heterochronic genes and the temporal control of C. elegans development. Trends Genet. 10:1997;123-127.
25. Moss E. G., Lee R. C., Ambros V. The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell. 88:1997;637-646.
26. Roussell D. L., Bennett K. L. Caenorhabditis cDNA encodes an eIF-4A-like protein. Nucleic Acids Res. 20:1992;3783.
27. Ruvkun G., Giusto J. The Caenorhabditis elegans heterochronic gene lin-14 encodes a nuclear protein that forms a temporal developmental switch. Nature. 338:1989;313-319.
28. Salles F. J., Lieberfarb M. E., Wreden C., Gergen J. P., Strickland S. Coordinate initiation of Drosophila development by regulated polyadenylation of maternal messenger RNAs. Science. 266:1994;1996-1999.
29. Salles F. J., Strickland S. Rapid and sensitive analysis of mRNA polyadenylation states by PCR. PCR Methods Appl. 4:1995;317-321.
30. Schauer I. E., Wood W. B. Early C. elegans embryos are transcriptionally active. Development. 110:1990;1303-1317.
31. Tarun S. Z., Sachs A. B. A common function for mRNA 5′ and 3′ ends in translation initiation in yeast. Genes Dev. 9:1995;2997-3007.
32. Tarun S. Z. Jr., Sachs A. B. Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J. 15.24:1996;7168-7177.
33. Wharton R. P., Sonoda J., Lee T., Patterson M., Murata Y. The Pumilio RNA-binding domain is also a translational regulator. Mol. Cell. 1:1998;863-872.
34. Wickens M. Forward, backward, how much, when: Mechanisms of poly(A) addition and removal and their role in early development. Semin. Dev. Biol. 3:1992;399-412.
35. Wickens M., Kimble J., Strickland S. Translational control of developmental decisions. Hershey J. W. B., Mathews M. B., Sonenberg N. Translational Control. 1996;411-450 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
36. Wightman B., Burglin T. R., Gatto J., Arasu P., Ruvkun G. Negative regulatory sequences in the lin-14 3′-untranslated region are necessary to generate a temporal switch during Caenorhabditis elegans development. Genes Dev. 5:1991;1813-1824.
37. Wightman B., Ha I., Ruvkun G. Post-transcriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell. 75:1993;855-862.
38. Wood W. B. The Nematode Caenorhabditis elegans. 1988;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
39. Zhang B., Gallegos M., Puoti A., Durkin E., Fields S., Kimble J., Wickens M. P. A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature. 390:1997;477-484.