Control of developmental timing in Caenorhabditis elegans

Current Opinion in Genetics and Development

Volumn 10, Issue 4, 2000, Pages 428-433

  Ambros, Victor ^a  

^a Dartmouth College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; LIN 14; LIN 28; PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

CAENORHABDITIS ELEGANS; CELL DIVISION; CELL TYPE; CONTROLLED STUDY; DEVELOPMENT; GENE MUTATION; LARVAL DEVELOPMENT; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

CAENORHABDITIS ELEGANS; DROSOPHILA;

EID: 0033935425     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(00)00108-8     Document Type: Review

References (44)

1. Thummel C.S. From embryogenesis to metamorphosis: the regulation and function of Drosophila nuclear receptor superfamily members. Cell. 83:1995;871-877.
2. Su Y., Damjanovski S., Shi Y., Shi Y.B. Molecular and cellular basis of tissue remodeling during amphibian metamorphosis. Histol Histopathol. 1:1999;175-183.
3. Telfer A., Poethig R.S. HASTY: a gene that regulates the timing of shoot maturation in Arabidopsis thaliana. Development. 125:1998;1889-1898.
4. Lawson E.J., Poethig R.S. Shoot development in plants: time for a change. Trends Genet. 11:1995;263-268.
5. Gellon G., McGinnis W. Shaping animal body plans in development and evolution by modulation of Hox expression patterns. Bioesssays. 20:1998;116-125.
6. Ambros V., Horvitz H.R. Heterochronic mutants of the nematode Caenorhabditis elegans. Science. 226:1984;409-416.
7. Moss E.G., Ambros V. Heterochronic genes and the temporal control of C. elegans development. Trends Genet. 10:1994;123-127.
8. Lee R.C., Feinbaum R., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 75:1993;843-854.
9. Reinhart B.J., Slack F.J., Basson M., Pasquinelli A.E., Bettinger J.C., Rougvie A.E., Horvitz H.R., Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature. 403:2000;901-906. By identifying a second case of a small antisense RNA like lin-4 - different in sequence from lin-4, but likely similar in its mode of action - this paper provides a boost to the notion that this type of RNA regulator could be generally applied. Two such RNA genes in the heterochronic pathway suggest that there may be more at work in C. elegans and in other species as well.
10. Sulston J.E., Horvitz H.R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol. 56:1977;110-156.
11. Slack F., Basson J.M., Liu Z., Ambros V., Horvitz H.R., Ruvkun G. The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the lin-29 transcription factor. Mol Cell. 5:2000;659-669. This paper shows two more cases of post-transcriptional control in the heterochronic gene pathway: LIN-41, a likely RNA binding protein, post-transcriptionally regulates LIN-29 accumulation; lin-41 is itself translationally controlled by the novel small antisense RNA product of the let-7 locus.
12. Jeon M., Gardner H.F., Miller E.A., Deshler J., Rougvie A.E. Similarity of the C. elegans developmental timing protein LIN-42 to circadian rhythm proteins. Science. 286:1999;1141-1146. The authors of this paper describe the startling result that LIN-42 contains an evolutionarily-conserved PAS domain like that found in Drosophila Per and other circadian timing proteins. Further, lin-42 mRNA cycles with the molting cycle, a behavior which parallels the circadian cycling of Per mRNA in flies. These results suggest the intriguing possibility that circadian and developmental timing mechanisms may share common evolutionary origins.
13. Euling S., Ambros V.R. Heterochronic genes control cell cycle progress and developmental competence of C. elegans vulva precursor cells. Cell. 84:1996;667-676.
14. Hallam S.J., Jin Y. lin-14 regulates the timing of synaptic remodeling in Caenorhabditis elegans. Nature. 395:1998;78-82.
15. Liu Z.C., Ambros V. Heterochronic genes control the stage-specific initiation and expression of the dauer larva developmental program in Caenorhabditis elegans. Genes Dev. 3:1989;2039-2049.
16. Liu Z., Kirch S., Ambros V. The Caenorhabditis elegans heterochronic gene pathway controls stage-specific transcription of collagen genes. Development. 121:1995;2471-2478.
17. Euling S., Bettinger J.C., Rougvie A.E. The LIN-29 transcription factor is required for proper morphogenesis of the Caenorhabditis elegans male tail. Dev Biol. 206:1999;142-156.
18. Bettinger J.C., Euling S., Rougvie A.E. The terminal differentiation factor LIN-29 is required for proper vulval morphogenesis and egg laying in Caenorhabditis elegans. Development. 124:1997;4333-4342.
19. 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.
20. Ruvkun G., Guisto J. The Caenorhabditis elegans heterochronic gene lin-14 encodes a nuclear protein that forms a temporal developmental switch. Nature. 337:1989;313.
21. Moss E., Lee R., Ambros V. Control of developmental timing by the cold shock domain protein LIN-28 and its regulation by the lin-4 RNA. Cell. 88:1997;637-646.
22. Ambros V. A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell. 57:1989;49-57.
23. Feinbaum R., Ambros V. The timing of lin-4 RNA accumulation controls the timing of postembryonic developmental events in C. elegans. Dev Biol. 210:1999;87-95. This paper shows that the profile of lin-4 RNA accumulation during the early larval stages corresponds to the timing of LIN-14 protein downregulation. This finding, together with the results of lin-4 mis-expression experiments, indicates that the timing of lin-4 RNA accumulation specifies the timing of postembryonic developmental events.
24. Wightman B., Ha I., Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell. 75:1993;855-862.
25. 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.
26. Arasu P., Wightman B., Ruvkun G. Temporal regulation of lin-14 by the antagonistic action of two other heterochronic genes, lin-4 and lin-28. Genes Dev. 5:1991;1825-1833.
27. Olsen P.H., Ambros V. The lin-4 regulatory RNA controls developmental timing in C. elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol. 216:2000;671-680. This paper explores the mechanism by which lin-4 RNA represses LIN-14 protein synthesis. The rate of synthesis of lin-14 mRNA, its state of polyadenylation, its abundance in the cytoplasmic fraction, and its polysomal sedimentation profile are found to be all unchanged by lin-4 RNA. These results point to the surprising conclusion that lin-4 RNA acts at a step after translational initiation - such as elongation or stabilization of nascent LIN-14 protein.
28. Mathews M.B., Sonenberg N., Hershey J.W.B. Translational Control. 1996;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
29. 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.
30. 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.
31. Ch'ng J.L.C., Shoemaker D.L., Schimmel P., Holmes E.W. Reversal of creatin kinase translational repression by 3′ untranslated sequences. Science. 248:1990;1003-1005.
32. Gavis E.R., Lehmann R. Translational regulation of nanos by RNA localization. Nature. 369:1994;315-318.
33. Antebi A., Yeh W.H., Hedgecock E.N.M., Riddle D.L. daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev. 14:2000;1512-1527. By identifying the product of daf-12, this paper provides evidence for cross-regulation, perhaps involving hormonal signaling, of various aspects of C. elegans life history - including developmental timing, diapause, and aging. Further, the evolutionary conservation of the nuclear receptor protein family suggests a possible evolutionary link between C. elegans heterochronic genes and steroid-based developmental timing mechanisms in other animals.
34. Antebi A., Culotti J.G., Hedgecock E.M. daf-12 regulates developmental age and the dauer alternative in Caenorhabditis elegans. Development. 125:1998;1191-1205.
35. Larsen P.L., Albert P.S., Riddle D.L. Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics. 139:1995;1567-1583.
36. Liu, Z. Genetic control of stage-specific developmental events in C. elegans [PhD Thesis]. Harvard University; 1991.
37. Dunlap J.C. Molecular basis for circadian clocks. Cell. 96:1999;271-290.
38. Rougvie A.E., Ambros V. The heterochronic gene lin-29 encodes a zinc finger protein that controls a terminal differentiation event in Caenorhabditis elegans. Development. 121:1995;491-500.
39. Bettinger J.C., Lee K., Rougvie A.E. Stage-specific accumulation of the terminal differentiation factor LIN-29 during Caenorhabditis elegans development. Development. 122:1996;2517-2527.
40. Hong Y., Lee R.C., Ambros V. Carboxy-terminal domains if LIN-14 mediate its nuclear localization and chromosomal association, and control the timing of postembryonic development. Mol Cell Biol. 20:2000;2285-2295. This paper contributes new perspectives on the functional organization of the LIN-14 protein. Of particular note is the finding that the alternative 5′ exons of LIN-14 are nonessential, and that the carboxy-terminal half of the protein is sufficient for in vivo function.
41. Hong Y., Roy R., Ambros V. Developmental regulation of a cyclin-dependent kinase inhibitor controls postembryonic cell cycle progression in C. elegans. Development. 125:1998;3585-3597.
42. Lane M.E., Sauer K., Wallace K., Jan Y.N., Lehner C.F., Vaessin H. Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during Drosophila development. Cell. 87:1996;1225-1235.
43. de Nooij J.C., Letendre M.A., Hariharan I.K. A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell. 87:1996;1237-1247.
44. Felix M.A., Hill R.J., Schwarz H., Sternberg P.W., Sudhaus W., Sommer R.J. Pristionchus pacificus, a nematode with only three juvenile stages, displays major heterochronic changes relative to Caenorhabditis elegans. Proc R Soc Lond B Biol Sci. 266:1999;1617-1621. This is the first clear demonstration of heterochronic differences in development between two nematode species. The reduced number of larval stages in P. pacificus is particularly intriguing in light of lin-14 and lin-28 mutants of C. elegans, which also undergo only three larval stages. This paper provides a foundation for genetic analysis of developmental timing in P. pacificus, which could illuminate the evolutionary mechanisms for this heterochrony.