The STAR/Maxi-KH domain protein GLD-1 mediates a developmental switch in the translational control of C. elegans PAL-1

Development

Volumn 131, Issue 14, 2004, Pages 3263-3272

  Mootz, Darcy ^a,b   Hunter, Craig P ^a  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

C. elegans; GLD 1; PAL 1; Post initiation repression; STAR Maxi KH domain; Translational control

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; MESSENGER RNA; PROTEIN GLD 1; PROTEIN PAL 1; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; GLD 1 PROTEIN, C ELEGANS; GLD-1 PROTEIN, C ELEGANS; GREEN FLUORESCENT PROTEIN; HELMINTH PROTEIN; HELMINTH RNA; HOMEODOMAIN PROTEIN; MEX 3 PROTEIN, C ELEGANS; MEX-3 PROTEIN, C ELEGANS; PAL 1 PROTEIN, C ELEGANS; PAL-1 PROTEIN, C ELEGANS; PHOTOPROTEIN; RIBONUCLEASE; TRANSACTIVATOR PROTEIN;

3' UNTRANSLATED REGION; ARTICLE; BLASTOMERE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; EMBRYO PATTERN FORMATION; GENE CONTROL; GENE EXPRESSION; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; RNA TRANSLATION; ANIMAL; BIOLOGICAL MODEL; CELL FRACTIONATION; CHEMISTRY; GENE; GENE EXPRESSION REGULATION; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN SYNTHESIS; PROTEIN TERTIARY STRUCTURE; REPORTER GENE; RIBOSOME;

CAENORHABDITIS; CAENORHABDITIS ELEGANS; INVERTEBRATA; NEMATODA;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HELMINTH; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HELMINTH PROTEINS; HOMEODOMAIN PROTEINS; LUMINESCENT PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEASES; RIBOSOMES; RNA INTERFERENCE; RNA, HELMINTH; RNA, MESSENGER; RNA-BINDING PROTEINS; SUBCELLULAR FRACTIONS; TRANS-ACTIVATORS;

EID: 4243066443     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01196     Document Type: Article

References (50)

1. Arning, S., Gruter, P., Bilbe, G. and Kramer, A. (1996). Mammalian splicing factor SF1 is encoded by variant cDNAs and binds to RNA. RNA 2, 794-810.
2. Beanan, M. J. and Strome, S. (1992). Characterization of a germ-line proliferation mutation in C. elegans. Development 116, 755-766.
3. Berleth, T., Burri, M., Thoma, G., Bopp, D., Richstein, S., Frigerio, G., Noll, M. and Nusslein-Volhard, C. (1988). The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J. 7, 1749-1756.
4. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
5. Caudy, A. A., Myers, M., Hannon, G. J. and Hammond, S. M. (2002). Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev. 16, 2491-2496.
6. Clark, I. E., Wyckoff, D. and Gavis, E. R. (2000). Synthesis of the posterior determinant Nanos is spatially restricted by a novel cotranslational regulatory mechanism. Curr. Biol. 10, 1311-1314.
7. Clifford, R., Lee, M. H., Nayak, S., Ohmachi, M., Giorgini, F. and Schedl, T. (2000). FOG-2, a novel F-box containing protein, associates with the GLD-1 RNA binding protein and directs male sex determination in the C. elegans hermaphrodite germline. Development 127, 5265-5276.
8. Dahanukar, A., Walker, J. A. and Wharton, R. P. (1999). Smaug, a novel RNA-binding protein that operates a translational switch in Drosophila. Mol. Cell 4, 209-218.
9. Draper, B. W., Mello, C. C., Bowerman, B., Hardin, J. and Priess, J. R. (1996). MEX-3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos. Cell 87, 205-216.
10. Driever, W. and Nusslein-Volhard, C. (1988). A gradient of bicoid protein in Drosophila embryos. Cell 54, 83-93.
11. Dubnau, J. and Struhl, G. (1996). RNA recognition and translational regulation by a homeodomain protein. Nature 379, 694-699.
12. Edgar, L. G., Carr, S., Wang, H. and Wood, W. B. (2001). Zygotic expression of the caudal homolog pal-1 is required for posterior patterning in Caenorhabditis elegans embryogenesis. Dev. Biol. 229, 71-88.
13. Evans, T. C., Crittenden, S. L., Kodoyianni, V. and Kimble, J. (1994). Translational control of maternal glp-1 mRNA establishes an asymmetry in the C. elegans embryo. Cell 77, 183-194.
14. Fire, A., Harrison, S. W. and Dixon, D. (1990). A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene 93, 189-198.
15. Francis, R., Barton, M. K., Kimble, J. and Schedl, T. (1995a). gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics 139, 579-606.
16. Francis, R., Maine, E. and Schedl, T. (1995b). Analysis of the multiple roles of gld-1 in germline development: interactions with the sex determination cascade and the glp-1 signaling pathway. Genetics 139, 607-630.
17. Gomes, J. E., Encalada, S. E., Swan, K. A., Shelton, C. A., Carter, J. C. and Bowerman, B. (2001). The maternal gene spn-4 encodes a predicted RRM protein required for mitotic spindle orientation and cell fate patterning in early C. elegans embryos. Development. 128, 4301-4314.
18. Goodwin, E. B., Okkema, P. G., Evans, T. C. and Kimble, J. (1993). Translational regulation of tra-2 by its 3′ untranslated region controls sexual identity in C. elegans. Cell 75, 329-339.
19. Gray, N. K. and Hentze, M. W. (1994). Iron regulatory protein prevents binding of the 43S translation pre-initiation complex to ferritin and eALAS mRNAs. EMBO J 13, 3882-3891.
20. Huang, N. N., Mootz, D. E., Walhout, A. J., Vidal, M. and Hunter, C. P. (2002). MEX-3 interacting proteins link cell polarity to asymmetric gene expression in Caenorhabditis elegans. Development 129, 747-759.
21. Hunter, C. P. and Kenyon, C. (1996). Spatial and temporal controls target pal-1 blastomere-specification activity to a single blastomere lineage in C. elegans embryos. Cell 87, 217-226.
22. Ishizuka, A., Siomi, M. C. and Siomi, H. (2002). A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 16, 2497-2508.
23. Jan, E., Motzny, C. K., Graves, L. E. and Goodwin, E. B. (1999). The STAR protein, GLD-1, is a translational regulator of sexual identity in Caenorhabditis elegans. EMBO J. 18, 258-269.
24. Jones, A. R. and Schedl, T. (1995). Mutations in gld-1, a female germ cell-specific tumor suppressor gene in Caenorhabditis elegans, affect a conserved domain also found in Src-associated protein Sam68. Genes Dev. 9, 1491-1504.
25. Jones, A. R., Francis, R. and Schedl, T. (1996). GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev. Biol. 180, 165-183.
26. Kelly, W. G., Xu, S., Montgomery, M. K. and Fire, A, (1997). Distinct requirements for somatic and germline expression of a generally expressed Caenorhabditis elegans gene. Genetics 146, 227-238.
27. Kramer, G., Ramachandiran, V. and Hardesty, B. (2001). Cotranslational folding - omnia mea mecum porto? Int. J. Biochem. Cell. Biol. 33, 541-553.
28. Kuwabara, P. E. and Perry, M. D. (2001). It ain't over till it's ova: germline sex determination in C. elegans. BioEssays 23, 596-604.
29. Larocque, D., Pilotte, J., Chen, T., Cloutier, F., Massie, B., Pedraza, L., Couture, R., Lasko, P., Almazan, G. and Richard, S. (2002). Nuclear retention of MBP mRNAs in the quaking viable mice. Neuron 36, 815-829.
30. Lee, M. H. and Schedl, T. (2001). Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development. Genes Dev. 15, 2408-2420.
31. Marin, V. A. and Evans, T. C. (2003). Translational repression of a C. elegans Notch mRNA by the STAR/KH domain protein GLD-1. Development 130, 26323-26332.
32. Mendez, R. and Richter, J. D. (2001). Translational control by CPEB: a means to the end. Nat. Rev. Mol. Cell. Biol. 7, 521-529.
33. Mitchell, P. and Tollervey, D. (2000). mRNA stability in eukaryotes. Curr. Opin. Genet. Dev. 10, 193-198.
34. Mlodzik, M. and Gehring, W. J. (1987). Expression of the caudal gene in the germ line of Drosophila: formation of an RNA and protein gradient during early embryogenesis. Cell 48, 465-478.
35. Muckenthaler, M., Gray, N. K. and Hentze, M. W. (1998). IRP-1 binding to ferritin mRNA prevents the recruitment of the small ribosomal subunit by the cap-binding complex eIF4F. Mol. Cell 2, 383-388.
36. Niessing, D., Blanke, S. and Jackie, H. (2002). Bicoid associates with the 5′-cap-bound complex of caudal mRNA and represses translation. Genes Dev. 16, 2576-2582.
37. Olsen, P. H. and Ambros, V. (1999). The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216, 671-680.
38. Praitis, V., Casey, E., Collar, D. and Austin, J. (2001). Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157, 1217-1226.
39. Rivera-Pomar, R., Niessing, D., Schmidt-Ott, U., Gehring, W. J. and Jackie, H. (1996). RNA binding and translational suppression by bicoid. Nature 379, 746-749.
40. Saccomanno, L., Loushin, C., Jan, E., Punkay, E., Artzt, K. and Goodwin, E. B. (1999). The STAR protein QKI-6 is a translational repressor. Proc. Natl. Acad. Sci. USA 96, 12605-12610.
41. Schubert, C. M., Lin, R., de Vries, C. J., Plasterk, R. H. and Priess, J. R. (2000). MEX-5 and MEX-6 function to establish soma/germline asymmetry in early C. elegans embryos. Mol. Cell 5, 671-682.
42. Seggerson, K., Tang, L. and Moss, E. G. (2002). Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev. Biol. 243, 215-225.
43. Seydoux, G. and Fire, A. (1995). Whole-mount in situ hybridization for the detection of RNA in Caenorhabditis elegans embryos. Methods Cell Biol. 48, 323-337.
44. Simbert, C. A., Wilson, J. E., Kerr, K. and Macdonald, P. M. (1996). smaug protein represses translation of unlocalized nanos mRNA in the Drosophila embryo. Genes Dev. 10, 2600-2609.
45. Stebbins-Boaz, B., Cao, Q., de Moor, C. H., Mendez, R. and Richter, J. D. (1999). Maskin is a CPEB-associated factor that transiently interacts with e1F-4E. Mol. Cell 4, 1017-1027.
46. Vernet, C. and Artzt, K. (1997). STAR, a gene family involved in signal transduction and activation of RNA. Trends Genet. 13, 479-484.
47. Wickens, M., Kimble, J. and Strickland, S. (1996). Translational control of developmental decisions. In Translational Control (ed. J. W. B. Hershey, M. B. Mathew and N. Sonenberg), pp. 411-50. Plainview, New York: Cold Spring Harbor Laboratory Press.
48. Winston, W. M., Molodowitch, C. and Hunter, C. P. (2002). Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295, 2456-2459.
49. Xu, L., Paulsen, J., Yoo, Y., Goodwin, E. B. and Strome, S. (2001). Caenorhabditis elegans MES-3 is a target of GLD-1 and functions epigenetically in germline development. Genetics 159, 1007-1017.
50. Zalfa, F., Giorgi, M., Primerano, B., Moro, A., Di Penta, A., Reis, S., Oostra, B. and Bagni, C. (2003). The Fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell 112, 317-327.