Two conserved regulatory cytoplasmic poly(A) polymerases, GLD-4 and GLD-2, regulate meiotic progression in C. elegans

Genes and Development

Volumn 23, Issue 7, 2009, Pages 824-836

  Schmid, Mark ^a   Küchler, Beate ^a,b   Eckmann, Christian R ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Deadenylase; Germ stem cell fate; Meiotic progression; Poly(A) polymerases; PUF proteins; Translational control

Indexed keywords

MESSENGER RNA; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; RNA BINDING PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; GLD 1 PROTEIN, C ELEGANS; GLD 2 PROTEIN, C ELEGANS; GLD-1 PROTEIN, C ELEGANS; GLD-2 PROTEIN, C ELEGANS;

ARTICLE; CAENORHABDITIS ELEGANS; ENZYME ACTIVITY; GAMETE; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CYTOPLASM; GENE EXPRESSION REGULATION; GENE ORDER; GENETICS; GERM CELL; HERMAPHRODITISM; METABOLISM; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PROTEIN BINDING; RNA STABILITY; SEQUENCE ALIGNMENT;

CAENORHABDITIS ELEGANS; SACCHAROMYCETALES;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CONSERVED SEQUENCE; CYTOPLASM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE ORDER; GERM CELLS; HERMAPHRODITISM; MEIOSIS; PHYLOGENY; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; PROTEIN BINDING; RNA STABILITY; SEQUENCE ALIGNMENT;

EID: 64349118428     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.494009     Document Type: Article

References (50)

1. Belfiore, M., Pugnale, P., Saudan, Z., and Puoti, A. 2004. Roles of the C. elegans cyclophilin-like protein MOG-6 in MEP-1 binding and germline fates. Development 131: 2935-2945.
2. Benoit, P., Papin, C., Kwak, J.E., Wickens, M., and Simonelig, M. 2008. PAP- and GLD-2-type poly(A) polymerases are required sequentially in cytoplasmic polyadenylation and oogenesis in Drosophila. Development 135: 1969-1979.
3. Crittenden, S.L. and Kimble, J. 1999. Confocal methods for Caenorhabditis elegans. Methods Mol. Biol. 122: 141-151.
4. Crittenden, S.L., Bernstein, D.S., Bachorik, J.L., Thompson, B.E., Gallegos, M., Petcherski, A.G., Moulder, G., Barstead, R., Wickens, M., and Kimble, J. 2002. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417: 660-663.
5. Dernburg, A.F., McDonald, K., Moulder, G., Barstead, R., Dresser, M., and Villeneuve, A.M. 1998. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387-398.
6. Dreyfuss, G., Kim, V.N., and Kataoka, N. 2002. Messenger- RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol. 3: 195-205.
7. Eckmann, C.R., Kraemer, B., Wickens, M., and Kimble, J. 2002. GLD-3, a bicaudal-C homolog that inhibits FBF to control germline sex determination in C. elegans. Dev. Cell 3: 697- 710.
8. Eckmann, C.R., Crittenden, S.L., Suh, N., and Kimble, J. 2004. GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans. Genetics 168: 147- 160.
9. Egecioglu, D.E., Henras, A.K., and Chanfreau, G.F. 2006. Contributions of Trf4p- and Trf5p-dependent polyadenylation to the processing and degradative functions of the yeast nuclear exosome. RNA 12: 26-32.
10. Francis, R., Barton, M.K., Kimble, J., and Schedl, T. 1995. gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics 139: 579-606.
11. Goldstrohm, A.C., Hook, B.A., Seay, D.J., and Wickens, M. 2006. PUF proteins bind Pop2p to regulate messenger RNAs. Nat. Struct. Mol. Biol. 13: 533-539.
12. Goldstrohm, A.C., Seay, D.J., Hook, B.A., and Wickens, M. 2007. PUF protein-mediated deadenylation is catalyzed by Ccr4p. J. Biol. Chem. 282: 109-114.
13. Hansen, D., Wilson-Berry, L., Dang, T., and Schedl, T. 2004. Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 131: 93-104.
14. Haracska, L., Johnson, R.E., Prakash, L., and Prakash, S. 2005. Trf4 and Trf5 proteins of Saccharomyces cerevisiae exhibit poly(A) RNA polymerase activity but no DNA polymerase activity. Mol. Cell. Biol. 25: 10183-10189.
15. Holm, L. and Sander, C. 1995. DNA polymerase β belongs to an ancient nucleotidyltransferase superfamily. Trends Biochem. Sci. 20: 345-347.
16. Hook, B.A., Goldstrohm, A.C., Seay, D.J., and Wickens, M. 2007. Two yeast PUF proteins negatively regulate a single mRNA. J. Biol. Chem. 282: 15430-15438.
17. Houseley, J. and Tollervey, D. 2006. Yeast Trf5p is a nuclear poly(A) polymerase. EMBO Rep. 7: 205-211.
18. Jacobson, A. and Peltz, S.W. 1996. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem. 65: 693-739.
19. Jones, A.R., Francis, R., and Schedl, T. 1996. GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stageand sex-specific expression during Caenorhabditis elegans germline development. Dev. Biol. 180: 165-183.
20. Kadyk, L.C. and Kimble, J. 1998. Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 125: 1803- 1813.
21. Kadyrova, L.Y., Habara, Y., Lee, T.H., and Wharton, R.P. 2007. Translational control of maternal Cyclin B mRNA by Nanos in the Drosophila germline. Development 134: 1519-1527.
22. Kawasaki, I., Shim, Y.H., Kirchner, J., Kaminker, J., Wood, W.B., and Strome, S. 1998. PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell 94: 635-645.
23. Keene, J.D. 2007. RNA regulons: Coordination of post-transcriptional events. Nat. Rev. Genet. 8: 533-543.
24. Kim, J.H. and Richter, J.D. 2006. Opposing polymerase-deadenylase activities regulate cytoplasmic polyadenylation. Mol. Cell 24: 173-183.
25. Kimble, J. and Crittenden, S.L. 2007. Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in C. elegans. Annu. Rev. Cell Dev. Biol. 23: 405-433.
26. Kindler, S., Wang, H., Richter, D., and Tiedge, H. 2005. RNA transport and local control of translation. Annu. Rev. Cell Dev. Biol. 21: 223-245.
27. Kraemer, B., Crittenden, S., Gallegos, M., Moulder, G., Barstead, R., Kimble, J., and Wickens, M. 1999. NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans. Curr. Biol. 9: 1009-1018.
28. Kuersten, S. and Goodwin, E.B. 2003. The power of the 3' UTR: Translational control and development. Nat. Rev. Genet. 4: 626-637.
29. Kwak, J.E. and Wickens, M. 2007. A family of poly(U) polymerases. RNA 13: 860-867.
30. Kwak, J.E., Wang, L., Ballantyne, S., Kimble, J., and Wickens, M. 2004. Mammalian GLD-2 homologs are poly(A) polymerases. Proc. Natl. Acad. Sci. 101: 4407-4412.
31. LaCava, J., Houseley, J., Saveanu, C., Petfalski, E., Thompson, E., Jacquier, A., and Tollervey, D. 2005. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121: 713-724.
32. Lamont, L.B., Crittenden, S.L., Bernstein, D., Wickens, M., and Kimble, J. 2004. FBF-1 and FBF-2 regulate the size of the mitotic region in the C. elegans germline. Dev. Cell 7: 697- 707.
33. Maciejowski, J., Ahn, J.H., Cipriani, P.G., Killian, D.J., Chaudhary, A.L., Lee, J.I., Voutev, R., Johnsen, R.C., Baillie, D.L., Gunsalus, K.C., et al. 2005. Autosomal genes of autosomal/X-linked duplicated gene pairs and germ-line proliferation in Caenorhabditis elegans. Genetics 169: 1997-2011.
34. Martin, G. and Keller, W. 2007. RNA-specific ribonucleotidyl transferases. RNA 13: 1834-1849.
35. Martin, G., Keller, W., and Doublie, S. 2000. Crystal structure of mammalian poly(A) polymerase in complex with an analog of ATP. EMBO J. 19: 4193-4203.
36. Motamedi, M.R., Verdel, A., Colmenares, S.U., Gerber, S.A., Gygi, S.P., and Moazed, D. 2004. Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119: 789-802.
37. Nakanishi, T., Kumagai, S., Kimura, M., Watanabe, H., Sakurai, T., Kashiwabara, S., and Baba, T. 2007. Disruption of mouse poly(A) polymerase mGLD-2 does not alter polyadenylation status in oocytes and somatic cells. Biochem. Biophys. Res. Commun. 364: 14-19.
38. Parker, R. and Sheth, U. 2007. P bodies and the control of mRNA translation and degradation. Mol. Cell 25: 635-646.
39. Richter, J.D. 2007. CPEB: A life in translation. Trends Biochem. Sci. 32: 279-285.
40. Semotok, J.L., Cooperstock, R.L., Pinder, B.D., Vari, H.K., Lipshitz, H.D., and Smibert, C.A. 2005. Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo. Curr. Biol. 15: 284-294.
41. Song, M.G. and Kiledjian, M. 2007. 39 Terminal oligo U-tractmediated stimulation of decapping. RNA 13: 2356-2365.
42. Stevenson, A.L. and Norbury, C.J. 2006. The Cid1 family of noncanonical poly(A) polymerases. Yeast 23: 991-1000.
43. Strome, S. 2005. Specification of the germ line. WormBook (ed. The C. elegans Research Community). WormBook. doi: 10.1895/wormbook.1.9.1, http://www.wormbook.org.
44. Suh, N., Jedamzik, B., Eckmann, C.R., Wickens, M., and Kimble, J. 2006. The GLD-2 poly(A) polymerase activates gld-1 mRNA in the Caenorhabditis elegans germ line. Proc. Natl. Acad. Sci. 103: 15108-15112.
45. Vanacova, S., Wolf, J., Martin, G., Blank, D., Dettwiler, S., Friedlein, A., Langen, H., Keith, G., and Keller, W. 2005. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 3: e189. doi: 10.1371/journal. pbio.0030189.
46. Wang, L., Eckmann, C.R., Kadyk, L.C., Wickens, M., and Kimble, J. 2002. A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans. Nature 419: 312-316.
47. Wang, S.W., Stevenson, A.L., Kearsey, S.E., Watt, S., and Bahler, J. 2008. Global role for polyadenylation-assisted nuclear RNA degradation in posttranscriptional gene silencing. Mol. Cell. Biol. 28: 656-665.
48. Win, T.Z., Stevenson, A.L., and Wang, S.W. 2006. Fission yeast Cid12 has dual functions in chromosome segregation and checkpoint control. Mol. Cell. Biol. 26: 4435-4447.
49. Wyers, F., Rougemaille, M., Badis, G., Rousselle, J.C., Dufour, M.E., Boulay, J., Regnault, B., Devaux, F., Namane, A., Seraphin, B., et al. 2005. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725-737.
50. Zetka, M.C., Kawasaki, I., Strome, S., and Muller, F. 1999. Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes & Dev. 13: 2258-2270.