Two GW repeat proteins interact with Tetrahymena thermophila argonaute and promote genome rearrangement

Molecular and Cellular Biology

Volumn 29, Issue 18, 2009, Pages 5020-5030

  Bednenko, Janna ^a   Noto, Tomoko ^b   DeSouza, Leroi V ^c   Siu, K W Michael ^c   Pearlman, Ronald E ^c   Mochizuki, Kazufumi ^b   Gorovsky, Martin A ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

^b ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^c YORK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; DNA; GLYCINE; PROTEIN CNJBP; PROTEIN TWI1P; PROTEIN WAG1P; TRYPTOPHAN; UNCLASSIFIED DRUG; MESSENGER RNA; PROTOZOAL DNA; PROTOZOAL PROTEIN; SMALL INTERFERING RNA; UNTRANSLATED RNA;

ARTICLE; CELL NUCLEUS INCLUSION BODY; CHROMOSOME BREAKAGE; CNJB GENE; CONTROLLED STUDY; DNA STRUCTURE; DOWN REGULATION; GENE; GENE DELETION; GENE EXPRESSION; GENE LOCATION; GENOME; MACRONUCLEUS; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; TETRAHYMENA THERMOPHILA; WAG1 GENE; AMINO ACID SEQUENCE; ANIMAL; CELL NUCLEUS; CHEMISTRY; CYTOLOGY; GENE INACTIVATION; GENE REARRANGEMENT; GENETICS; IMMUNOPRECIPITATION; METABOLISM; PROTEIN BINDING; PROTEIN TRANSPORT;

TETRAHYMENA; TETRAHYMENA THERMOPHILA;

ANIMALS; BASE SEQUENCE; CELL NUCLEUS; DNA, PROTOZOAN; DOWN-REGULATION; GENE KNOCKOUT TECHNIQUES; GENE REARRANGEMENT; GENOME, PROTOZOAN; IMMUNOPRECIPITATION; PHENOTYPE; PROTEIN BINDING; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; REPETITIVE SEQUENCES, AMINO ACID; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA, UNTRANSLATED; TETRAHYMENA THERMOPHILA;

EID: 70249150712     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00076-09     Document Type: Article

References (51)

1. Aronica, L., J. Bednenko, T. Noto, L. V. DeSouza, K. W. Siu, J. Loidl, R. E. Pearlman, M. A. Gorovsky, and K. Mochizuki. 2008. Study of an RNA helicase implicates small RNA-noncoding RNA interactions in programmed DNA elimination in Tetrahymena. Genes Dev. 22:2228-2241.
2. Bies-Etheve, N., D. Pontier, S. Lahmy, C. Picart, D. Vega, R. Cooke, and T. Lagrange. 2009. RNA-directed DNA methylation requires an AGO4-interacting member of the SPT5 elongation factor family. EMBO Rep. 10:649-654.
3. Bühler, M., and D. Moazed. 2007. Transcription and RNAi in heterochromatic gene silencing. Nat. Struct. Mol. Biol. 14:1041-1048. (Pubitemid 350060336)
4. Chalker, D. L. 2008. Dynamic nuclear reorganization during genome remodeling of Tetrahymena. Biochim. Biophys. Acta 1783:2130-2136.
5. Chalker, D. L., P. Fuller, and M. C. Yao. 2005. Communication between parental and developing genomes during Tetrahymena nuclear differentiation is likely mediated by homologous RNAs. Genetics 169:149-160.
6. Chalker, D. L., and M. C. Yao. 1996. Non-Mendelian, heritable blocks to DNA rearrangement are induced by loading the somatic nucleus of Tetrahymena thermophila with germ line-limited DNA. Mol. Cell. Biol. 16:3658-3667. (Pubitemid 26199885)
7. Chalker, D. L., and M. C. Yao. 2001. Nongenic, bidirectional transcription precedes and may promote developmental DNA deletion in Tetrahymena thermophila. Genes Dev. 15:1287-1298.
8. Collins, K., and M. A. Gorovsky. 2005. Tetrahymena thermophila. Curr. Biol. 15:R317-R318.
9. David, E., J. B. McNeil, V. Basile, and R. E. Pearlman. 1997. An unusual fibrillarin gene and protein: structure and functional implications. Mol. Biol. Cell 8:1051-1061. (Pubitemid 27276325)
10. Ding, L., and M. Han. 2007. GW182 family proteins are crucial for micro- RNA-mediated gene silencing. Trends Cell Biol. 17:411-416. (Pubitemid 47375102)
11. Doherty, A. J., L. C. Serpell, and C. P. Ponting. 1996. The helix-hairpin-helix DNA-binding motif: a structural basis for non-sequence-specific recognition of DNA. Nucleic Acids Res. 24:2488-2497.
12. El-Shami, M., D. Pontier, S. Lahmy, L. Braun, C. Picart, D. Vega, M. A. Hakimi, S. E. Jacobsen, R. Cooke, and T. Lagrange. 2007. Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev. 21: 2539-2544. (Pubitemid 47607665)
13. Gorovsky, M. A., M. C. Yao, J. B. Keevert, and G. L. Pleger. 1975. Isolation of micro- and macronuclei of Tetrahymena pyriformis. Methods Cell Biol. 9:311-327.
14. He, X. J., Y. F. Hsu, S. Zhu, A. T. Wierzbicki, O. Pontes, C. S. Pikaard, H. L. Liu, C. S. Wang, H. Jin, and J. K. Zhu. 2009. An effector of RNA-directed DNA methylation in Arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell 137:498-508.
15. Hutvagner, G., and M. J. Simard. 2008. Argonaute proteins: key players in RNA silencing. Nat. Rev. Mol. Cell Biol. 9:22-32.
16. Karrer, K. M. 2000. Tetrahymena genetics: two nuclei are better than one. Methods Cell Biol. 62:127-186.
17. Lee, S. R., and K. Collins. 2007. Physical and functional coupling of RNA-dependent RNA polymerase and Dicer in the biogenesis of endogenous siRNAs. Nat. Struct. Mol. Biol. 14:604-610.
18. Lee, S. R., and K. Collins. 2006. Two classes of endogenous small RNAs in Tetrahymena thermophila. Genes Dev. 20:28-33.
19. Lepère, G., M. Betermier, E. Meyer, and S. Duharcourt. 2008. Maternal noncoding transcripts antagonize the targeting of DNA elimination by scan-RNAs in Paramecium tetraurelia. Genes Dev. 22:1501-1512. (Pubitemid 351793084)
20. Li, C. F., I. R. Henderson, L. Song, N. Fedoroff, T. Lagrange, and S. E. Jacobsen. 2008. Dynamic regulation of ARGONAUTE4 within multiple nuclear bodies in Arabidopsis thaliana. PLoS Genet. 4:e27.
21. Li, C. F., O. Pontes, M. El-Shami, I. R. Henderson, Y. V. Bernatavichute, S. W. Chan, T. Lagrange, C. S. Pikaard, and S. E. Jacobsen. 2006. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126:93-106.
22. Liu, J., M. A. Valencia-Sanchez, G. J. Hannon, and R. Parker. 2005. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7:719-723. (Pubitemid 40975754)
23. Liu, Y., K. Mochizuki, and M. A. Gorovsky. 2004. Histone H3 lysine 9 methylation is required for DNA elimination in developing macronuclei in Tetrahymena. Proc. Natl. Acad. Sci. USA 101:1679-1684. (Pubitemid 38234214)
24. Liu, Y., S. D. Taverna, T. L. Muratore, J. Shabanowitz, D. F. Hunt, and C. D. Allis. 2007. RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena. Genes Dev. 21:1530-1545. (Pubitemid 46955725)
25. Madireddi, M. T., R. S. Coyne, J. F. Smothers, K. M. Mickey, M. C. Yao, and C. D. Allis. 1996. Pdd1p, a novel chromodomain-containing protein, links heterochromatin assembly and DNA elimination in Tetrahymena. Cell 87: 75-84.
26. Madireddi, M. T., M. C. Davis, and C. D. Allis. 1994. Identification of a novel polypeptide involved in the formation of DNA-containing vesicles during macronuclear development in Tetrahymena. Dev. Biol. 165:418-431.
27. Malone, C. D., A. M. Anderson, J. A. Motl, C. H. Rexer, and D. L. Chalker. 2005. Germ line transcripts are processed by a Dicer-like protein that is essential for developmentally programmed genome rearrangements of Tetrahymena thermophila. Mol. Cell. Biol. 25:9151-9164.
28. Martindale, D. W., and P. J. Bruns. 1983. Cloning of abundant mRNA species present during conjugation of Tetrahymena thermophila: identification of mRNA species present exclusively during meiosis. Mol. Cell. Biol. 3:1857-1865.
29. Martindale, D. W., H. M. Martindale, and P. J. Bruns. 1986. Tetrahymena conjugation-induced genes: structure and organization in macro- and micronuclei. Nucleic Acids Res. 14:1341-1354.
30. Matzke, M., T. Kanno, B. Huettel, L. Daxinger, and A. J. Matzke. 2007. Targets of RNA-directed DNA methylation. Curr. Opin. Plant Biol. 10:512-519.
31. McDonald, B. B. 1966. The exchange of RNA and protein during conjugation in Tetrahymena. J. Protozool. 13:277-285.
32. McGrath, K. E., J. F. Smothers, C. A. Dadd, M. T. Madireddi, M. A. Gorovsky, and C. D. Allis. 1997. An abundant nucleolar phosphoprotein is associated with ribosomal DNA in Tetrahymena macronuclei. Mol. Biol. Cell 8:97-108.
33. Meyer, E., and D. L. Chalker. 2006. Epigenetics of ciliates, p. 127-150. In C. D. Allis, T. Jenuwein, D. Reinberg, and M.-L. Caparros (ed.), Epigenetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Mochizuki, K., N. A. Fine, T. Fujisawa, and M. A. Gorovsky. 2002. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell 110:689-699. (Pubitemid 35283959)
35. Mochizuki, K., and M. A. Gorovsky. 2004. Conjugation-specific small RNAs in Tetrahymena have predicted properties of scan (scn) RNAs involved in genome rearrangement. Genes Dev. 18:2068-2073. (Pubitemid 39166624)
36. Mochizuki, K., and M. A. Gorovsky. 2005. A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase. Genes Dev. 19:77-89. (Pubitemid 40095818)
37. Nikiforov, M. A., M. A. Gorovsky, and C. D. Allis. 2000. A novel chromodomain protein, Pdd3p, associates with internal eliminated sequences during macronuclear development in Tetrahymena thermophila. Mol. Cell. Biol. 20:4128-4134.
38. Nowacki, M., W. Zagorski-Ostoja, and E. Meyer. 2005. Nowa1p and Nowa2p: novel putative RNA binding proteins involved in trans-nuclear crosstalk in Paramecium tetraurelia. Curr. Biol. 15:1616-1628. (Pubitemid 41323739)
39. Pall, G. S., C. Codony-Servat, J. Byrne, L. Ritchie, and A. Hamilton. 2007. Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by Northern blot. Nucleic Acids Res. 35:e60.
40. Partridge, J. F., J. L. DeBeauchamp, A. M. Kosinski, D. L. Ulrich, M. J. Hadler, and V. J. Noffsinger. 2007. Functional separation of the requirements for establishment and maintenance of centromeric heterochromatin. Mol. Cell 26:593-602.
41. Ponting, C. P. 2002. Novel domains and orthologues of eukaryotic transcription elongation factors. Nucleic Acids Res. 30:3643-3652.
42. Sen, G. L., and H. M. Blau. 2005. Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat. Cell Biol. 7:633-636.
43. Shang, Y., X. Song, J. Bowen, R. Corstanje, Y. Gao, J. Gaertig, and M. A. Gorovsky. 2002. A robust inducible-repressible promoter greatly facilitates gene knockouts, conditional expression, and overexpression of homologous and heterologous genes in Tetrahymena thermophila. Proc. Natl. Acad. Sci. USA 99:3734-3739. (Pubitemid 34252175)
44. Smothers, J. F., M. T. Madireddi, F. D. Warner, and C. D. Allis. 1997. Programmed DNA degradation and nucleolar biogenesis occur in distinct organelles during macronuclear development in Tetrahymena. J. Eukaryot. Microbiol. 44:79-88.
45. Taverna, S. D., R. S. Coyne, and C. D. Allis. 2002. Methylation of histone H3 at lysine 9 targets programmed DNA elimination in Tetrahymena. Cell 110: 701-711. (Pubitemid 35283960)
46. Taylor, F. M., and D. W. Martindale. 1993. Retroviral-type zinc fingers and glycine-rich repeats in a protein encoded by cnjB, a Tetrahymena gene active during meiosis. Nucleic Acids Res. 21:4610-4614. (Pubitemid 23292729)
47. Till, S., and A. G. Ladurner. 2007. RNA Pol IV plays catch with Argonaute 4. Cell 131:643-645. (Pubitemid 350087208)
48. Till, S., E. Lejeune, R. Thermann, M. Bortfeld, M. Hothorn, D. Enderle, C. Heinrich, M. W. Hentze, and A. G. Ladurner. 2007. A conserved motif in Argonaute-interacting proteins mediates functional interactions through the Argonaute PIWI domain. Nat. Struct. Mol. Biol. 14:897-903. (Pubitemid 47525180)
49. Verdel, A., S. Jia, S. Gerber, T. Sugiyama, S. Gygi, S. I. Grewal, and D. Moazed. 2004. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303:672-676. (Pubitemid 38141633)
50. Wenkert, D., and C. D. Allis. 1984. Timing of the appearance of macronuclear-specific histone variant hv1 and gene expression in developing new macronuclei of Tetrahymena thermophila. J. Cell Biol. 98:2107-2117. (Pubitemid 14121841)
51. Zaratiegui, M., D. V. Irvine, and R. A. Martienssen. 2007. Noncoding RNAs and gene silencing. Cell 128:763-776.