Developmentally programmed, RNA-directed genome rearrangement in Tetrahymena

Development Growth and Differentiation

Volumn 54, Issue 1, 2012, Pages 108-119

  Mochizuki, Kazufumi ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

Chromatin diminution; DNA elimination; Heterochromatin; RNAi; Tetrahymena

Indexed keywords

DICER; PIWI INTERACTING RNA; SMALL INTERFERING RNA; DNA; HETEROCHROMATIN; RNA; TRANSPOSASE;

ASCARIS SUUM; DNA SEQUENCE; EPIGENETICS; EUKARYOTE; GENE REARRANGEMENT; GENETIC REGULATION; HETEROCHROMATIN; MACRONUCLEUS; NONHUMAN; REVIEW; TETRAHYMENA; ACTIVE TRANSPORT; ANIMAL; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GENOME; GERMLINE MICRONUCLEUS; METABOLISM; RNA INTERFERENCE;

ASCARIS SUUM; EUKARYOTA; MYXOZOA; PROTISTA; TETRAHYMENA; VERTEBRATA;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ASCARIS SUUM; DNA; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REARRANGEMENT; GENOME; GENOME, PROTOZOAN; HETEROCHROMATIN; MACRONUCLEUS; MICRONUCLEUS, GERMLINE; RNA; RNA INTERFERENCE; SEQUENCE ANALYSIS, DNA; TETRAHYMENA; TRANSPOSASES;

EID: 84855954076     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/j.1440-169X.2011.01305.x     Document Type: Review

References (76)

1. Akematsu, T., Pearlman, R. E. & Endoh, H. 2010. Gigantic macroautophagy in programmed nuclear death of Tetrahymena thermophila. Autophagy 6, 901-911.
2. Aronica, L., Bednenko, J., Noto, T., Desouza, L. V., Siu, K. W., Loidl, J., Pearlman, R. E., Gorovsky, M. A. & Mochizuki, K. 2008. Study of an RNA helicase implicates small RNA-noncoding RNA interactions in programmed DNA elimination in Tetrahymena. Genes Dev. 22, 2228-2241.
3. Austerberry, C. F., Snyder, R. O. & Yao, M. C. 1989. Sequence microheterogeneity is generated at junctions of programmed DNA deletions in Tetrahymena thermophila. Nucleic Acids Res. 17, 7263-7272.
4. Austerberry, C. F. & Yao, M. C. 1988. Sequence structures of two developmentally regulated, alternative DNA deletion junctions in Tetrahymena thermophila. Mol. Cell. Biol. 8, 3947-3950.
5. Baldauf, S. L., Roger, A. J., Wenk-Siefert, I. & Doolittle, W. F. 2000. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290, 972-977.
6. Baudry, C., Malinsky, S., Restituito, M., Kapusta, A., Rosa, S., Meyer, E. & Betermier, M. 2009. PiggyMac, a domesticated piggyBac transposase involved in programmed genome rearrangements in the ciliate Paramecium tetraurelia. Genes Dev. 23, 2478-2483.
7. Bednenko, J., Noto, T., Desouza, L. V., Siu, K. W., Pearlman, R. E., Mochizuki, K. & Gorovsky, M.A. 2009. Two GW repeat proteins interact with the tetrahymena argonaute and promote genome rearrangement. Mol. Cell. Biol. 29, 5020-5030.
8. Beermann, S. 1977. The diminution of heterochromatic chromosomal segments in Cyclops (Crustacea, Copepoda). Chromosoma 60, 297-344.
9. Biemont, C. & Vieira, C. 2006. Genetics: junk DNA as an evolutionary force. Nature 443, 521-524.
10. Bouhouche, K., Gout, J. F., Kapusta, A., Betermier, M. & Meyer, E. 2011. Functional specialization of Piwi proteins in Paramecium tetraurelia from post-transcriptional gene silencing to genome remodelling. Nucleic Acids Res. 39, 4249-4264.
11. Cervantes, M. D., Xi, X., Vermaak, D., Yao, M. C. & Malik, H. S. 2006. The CNA1 histone of the ciliate Tetrahymena thermophila is essential for chromosome segregation in the germline micronucleus. Mol. Biol. Cell 17, 485-497.
12. Chalker, D. L., Fuller, P. & Yao, M. C. 2005. Communication between parental and developing genomes during tetrahymena nuclear differentiation is likely mediated by homologous RNAs. Genetics 169, 149-160.
13. Chalker, D. L. & Yao, M. C. 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.
14. Chalker, D. L. & Yao, M. C. 2001. Nongenic, bidirectional transcription precedes and may promote developmental DNA deletion in Tetrahymena thermophila. Genes Dev. 15, 1287-1298.
15. Cheng, C. Y., Vogt, A., Mochizuki, K. & Yao, M. C. 2010. A domesticated piggyBac transposase plays key roles in heterochromatin dynamics and DNA cleavage during programmed DNA deletion in Tetrahymena thermophila. Mol. Biol. Cell 21, 1753-1762.
16. Claycomb, J. M., Batista, P. J., Pang, K. M., Gu, W., Vasale, J. J., van Wolfswinkel, J. C., Chaves, D. A., Shirayama, M., Mitani, S., Ketting, R. F., Conte, D. & Mello, C. C. 2009. The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 139, 123-134.
17. Couvillion, M. T., Lee, S. R., Hogstad, B., Malone, C. D., Tonkin, L. A., Sachidanandam, R., Hannon, G. J. & Collins, K. 2009. Sequence, biogenesis, and function of diverse small RNA classes bound to the Piwi family proteins of Tetrahymena thermophila. Genes Dev. 23, 2016-2032.
18. Coyne, R. S., Nikiforov, M. A., Smothers, J. F., Allis, C. D. & Yao, M. C. 1999. Parental expression of the chromodomain protein Pdd1p is required for completion of programmed DNA elimination and nuclear differentiation. Mol. Cell 4, 865-872.
19. Coyne, R. S., Thiagarajan, M., Jones, K. M., Wortman, J. R., Tallon, L. J., Haas, B. J., Cassidy-Hanley, D. M., Wiley, E. A., Smith, J. J., Collins, K., Lee, S. R., Couvillion, M. T., Liu, Y., Garg, J., Pearlman, R. E., Hamilton, E. P., Orias, E., Eisen, J. A. & Methe, B. A. 2008. Refined annotation and assembly of the Tetrahymena thermophila genome sequence through EST analysis, comparative genomic hybridization, and targeted gap closure. BMC Genomics 9, 562.
20. Cui, B. & Gorovsky, M. A. 2006. Centromeric histone H3 is essential for vegetative cell division and for DNA elimination during conjugation in Tetrahymena thermophila. Mol. Cell. Biol. 26, 4499-4510.
21. Duharcourt, S., Butler, A. & Meyer, E. 1995. Epigenetic self-regulation of developmental excision of an internal eliminated sequence on Paramecium tetraurelia. Genes Dev. 9, 2065-2077.
22. Eisen, J. A., Coyne, R. S., Wu, M., Wu, D., Thiagarajan, M., Wortman, J. R., Badger, J. H., Ren, Q., Amedeo, P., Jones, K. M., Tallon, L. J., Delcher, A. L., Salzberg, S. L., Silva, J. C., Haas, B. J., Majoros, W. H., Farzad, M., Carlton, J. M., Smith. Jr, R. K., Garg, J., Pearlman, R. E., Karrer, K. M., Sun, L., Manning, G., Elde, N. C., Turkewitz, A. P., Asai, D. J., Wilkes, D. E., Wang, Y., Cai, H., Collins, K., Stewart, B. A., Lee, S. R., Wilamowska, K., Weinberg, Z., Ruzzo, W. L., Wloga, D., Gaertig, J., Frankel, J., Tsao, C. C., Gorovsky, M. A., Keeling, P. J., Waller, R. F., Patron, N. J., Cherry, J. M., Stover, N. A., Krieger, C. J., del Toro, C., Ryder, H. F., Williamson, S. C., Barbeau, R. A., Hamilton, E. P. & Orias, E. 2006. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol. 4, e286.
23. Ender, C. & Meister, G. 2010. Argonaute proteins at a glance. J. Cell Sci. 123, 1819-1823.
24. Epstein, L. M. & Forney, J. D. 1984. Mendelian and non-mendelian mutations affecting surface antigen expression in Paramecium tetraurelia. Mol. Cell. Biol. 4, 1583-1590.
25. Fillingham, J. S., Thing, T. A., Vythilingum, N., Keuroghlian, A., Bruno, D., Golding, G. B. & Pearlman, R. E. 2004. A non-long terminal repeat retrotransposon family is restricted to the germ line micronucleus of the ciliated protozoan Tetrahymena thermophila. Eukaryot. Cell 3, 157-169.
26. Gilbert, S. F. 2010. Developmental Biology. Sinauer Associates Inc., Sunderland, MA.
27. Girard, A. & Hannon, G. J. 2008. Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol. 18, 136-148.
28. Goday, C. & Esteban, M. R. 2001. Chromosome elimination in sciarid flies. Bioessays 23, 242-250.
29. Goday, C., Gonzalez-Garcia, J. M., Esteban, M. R., Giovinazzo, G. & Pimpinelli, S. 1992. Kinetochores and chromatin diminution in early embryos of Parascaris univalens. J. Cell Biol. 118, 23-32.
30. Godiska, R., James, C. & Yao, M. C. 1993. A distant 10-bp sequence specifies the boundaries of a programmed DNA deletion in Tetrahymena. Genes Dev. 7, 2357-2365.
31. Grewal, S. I. 2010. RNAi-dependent formation of heterochromatin and its diverse functions. Curr. Opin. Genet. Dev. 20, 134-141.
32. Hamilton, E. P., Williamson, S., Dunn, S., Merriam, V., Lin, C., Vong, L., Russell-Colantonio, J. & Orias, E. 2006. The highly conserved family of Tetrahymena thermophila chromosome breakage elements contains an invariant 10-base-pair core. Eukaryot. Cell 5, 771-780.
33. Heinonen, T. Y. & Pearlman, R. E. 1994. A germ line-specific sequence element in an intron in Tetrahymena thermophila. J. Biol. Chem. 269, 17428-17433.
34. Horwich, M. D., Li, C., Matranga, C., Vagin, V., Farley, G., Wang, P. & Zamore, P. D. 2007. The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr. Biol. 17, 1265-1272.
35. Howard-Till, R. A. & Yao, M. C. 2007. Tudor nuclease genes and programmed DNA rearrangements in Tetrahymena thermophila. Eukaryot. Cell 6, 1795-1804.
36. Karamysheva, Z., Wang, L., Shrode, T., Bednenko, J., Hurley, L. A. & Shippen, D. E. 2003. Developmentally programmed gene elimination in Euplotes crassus facilitates a switch in the telomerase catalytic subunit. Cell 113, 565-576.
37. Karrer, K. M. 2000. Tetrahymena genetics: two nuclei are better than one. Methods Cell Biol. 62, 127-186.
38. Kirino, Y. & Mourelatos, Z. 2007. The mouse homolog of HEN1 is a potential methylase for Piwi-interacting RNAs. RNA 13, 1397-1401.
39. Kohno, S., Nakai, Y., Satoh, S., Yoshida, M. & Kobayashi, H. 1986. Chromosome elimination in the Japanese hagfish, Eptatretus burgeri (Agnatha, Cyclostomata). Cytogenet. Cell Genet. 41, 209-214.
40. Kowalczyk, C. A., Anderson, A. M., Arce-Larreta, M. & Chalker, D. L. 2006. The germ line limited M element of Tetrahymena is targeted for elimination from the somatic genome by a homology-dependent mechanism. Nucleic Acids Res. 34, 5778-5789.
41. Kurth, H. M. & Mochizuki, K. 2009. 2'-O-methylation stabilizes Piwi-associated small RNAs and ensures DNA elimination in Tetrahymena. RNA 15, 675-685.
42. Lee, S. R. & Collins, K. 2006. Two classes of endogenous small RNAs in Tetrahymena thermophila. Genes Dev. 20, 28-33.
43. Lee, S. R. & Collins, K. 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.
44. Lepere, G., Betermier, M., Meyer, E. & Duharcourt, S. 2008. Maternal noncoding transcripts antagonize the targeting of DNA elimination by scanRNAs in Paramecium tetraurelia. Genes Dev. 22, 1501-1512.
45. Liu, Y., Mochizuki, K. & Gorovsky, M. A. 2004. Histone H3 lysine 9 methylation is required for DNA elimination in developing macronuclei in Tetrahymena. Proc. Natl Acad. Sci. USA 101, 1679-1684.
46. Liu, Y., Song, X., Gorovsky, M. A. & Karrer, K. M. 2005. Elimination of foreign DNA during somatic differentiation in Tetrahymena thermophila shows position effect and is dosage dependent. Eukaryot. Cell 4, 421-431.
47. Liu, Y., Taverna, S. D., Muratore, T. L., Shabanowitz, J., Hunt, D. F. & Allis, C. D. 2007. RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena. Genes Dev. 21, 1530-1545.
48. rd Edition. Springer.
49. Madireddi, M. T., Coyne, R. S., Smothers, J. F., Mickey, K. M., Yao, M. C. & Allis, C. D. 1996. Pdd1p, a novel chromodomain-containing protein, links heterochromatin assembly and DNA elimination in Tetrahymena. Cell 87, 75-84.
50. Majewski, J. & Ott, J. 2000. GT repeats are associated with recombination on human chromosome 22. Genome Res. 10, 1108-1114.
51. Malone, C. D., Anderson, A. M., Motl, J. A., Rexer, C. H. & Chalker, D. L. 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.
52. Martindale, D. W., Allis, C. D. & Bruns, P. J. 1985. RNA and protein synthesis during meiotic prophase in Tetrahymena thermophila. J. Protozool. 32, 644-649.
53. Meyer, E. & Duharcourt, S. 1996. Epigenetic regulation of programmed genomic rearrangements in Paramecium aurelia. J. Eukaryot. Microbiol. 43, 453-461.
54. Mochizuki, K., Fine, N. A., Fujisawa, T. & Gorovsky, M. A. 2002. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in tetrahymena. Cell 110, 689-699.
55. Mochizuki, K. & Gorovsky, M. A. 2004a. Conjugation-specific small RNAs in Tetrahymena have predicted properties of scan (scn) RNAs involved in genome rearrangement. Genes Dev. 18, 2068-2073.
56. Mochizuki, K. & Gorovsky, M. A. 2004b. RNA polymerase II localizes in Tetrahymena thermophila meiotic micronuclei when micronuclear transcription associated with genome rearrangement occurs. Eukaryot. Cell 3, 1233-1240.
57. Mochizuki, K. & Gorovsky, M. A. 2005. A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase. Genes Dev. 19, 77-89.
58. Muller, F. & Tobler, H. 2000. Chromatin diminution in the parasitic nematodes ascaris suum and parascaris univalens. Int. J. Parasitol. 30, 391-399.
59. Nikiforov, M. A., Smothers, J. F., Gorovsky, M. A. & Allis, C. D. 1999. Excision of micronuclear-specific DNA requires parental expression of pdd2p and occurs independently from DNA replication in Tetrahymena thermophila. Genes Dev. 13, 2852-2862.
60. Noto, T., Kurth, H. M., Kataoka, K., Aronica, L., Desouza, L. V., Siu, K. W., Pearlman, R. E., Gorovsky, M. A. & Mochizuki, K. 2010. The tetrahymena argonaute-binding protein Giw1p directs a mature argonaute-siRNA complex to the nucleus. Cell 140, 692-703.
61. Nowacki, M., Zagorski-Ostoja, W. & Meyer, E. 2005. Nowa1p and Nowa2p: novel putative RNA binding proteins involved in trans-nuclear crosstalk in Paramecium tetraurelia. Curr. Biol. 15, 1616-1628.
62. Saito, K., Sakaguchi, Y., Suzuki, T., Suzuki, T., Siomi, H. & Siomi, M. C. 2007. Pimet, the Drosophila homolog of HEN1, mediates 2'-O-methylation of Piwi- interacting RNAs at their 3' ends. Genes Dev. 21, 1603-1608.
63. Satzinger, H. 2008. Theodor and Marcella Boveri: chromosomes and cytoplasm in heredity and development. Nat. Rev. 9, 231-238.
64. Saveliev, S. V. & Cox, M. M. 1996. Developmentally programmed DNA deletion in Tetrahymena thermophila by a transposition-like reaction pathway. EMBO J. 15, 2858-2869.
65. Seto, A. G., Kingston, R. E. & Lau, N. C. 2007. The coming of age for Piwi proteins. Mol. Cell 26, 603-609.
66. Sugai, T. & Hiwatashi, K. 1974. Cytologic and autoradiographic studies of the micronucleus at meiotic prophase in Tetrahymena pyriformis. J. Protozool. 21, 542-548.
67. Taverna, S. D., Coyne, R. S. & Allis, C. D. 2002. Methylation of histone h3 at lysine 9 targets programmed DNA elimination in tetrahymena. Cell 110, 701-711.
68. Van De Lagemaat, L. N., Landry, J. R., Mager, D. L. & Medstrand, P. 2003. Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet. 19, 530-536.
69. Wang, H. G. & Fraser, M. J. 1993. TTAA serves as the target site for TFP3 lepidopteran transposon insertions in both nuclear polyhedrosis virus and Trichoplusia ni genomes. Insect Mol. Biol. 1, 109-116.
70. Wang, J., Czech, B., Crunk, A., Wallace, A., Mitreva, M., Hannon, G.J. & Davis, R.E. 2011. Deep small RNA sequencing from the nematode Ascaris reveals conservation, functional diversification, and novel developmental profiles. Genome Res. 21, 1462-1477.
71. Wuitschick, J. D., Gershan, J. A., Lochowicz, A. J., Li, S. & Karrer, K. M. 2002. A novel family of mobile genetic elements is limited to the germline genome in Tetrahymena thermophila. Nucleic Acids Res. 30, 2524-2537.
72. Yao, M. C., Choi, J., Yokoyama, S., Austerberry, C. F. & Yao, C. H. 1984. DNA elimination in Tetrahymena: a developmental process involving extensive breakage and rejoining of DNA at defined sites. Cell 36, 433-440.
73. Yao, M. C., Fuller, P. & Xi, X. 2003. Programmed DNA deletion as an RNA-guided system of genome defense. Science 300, 1581-1584.
74. You, Y., Scott, J. & Forney, J. 1994. The role of macronuclear DNA sequences in the permanent rescue of a non-mendelian mutation in Paramecium tetraurelia. Genetics 136, 1319-1324.
75. Yu, B., Yang, Z., Li, J., Minakhina, S., Yang, M., Padgett, R. W., Steward, R. & Chen, X. 2005. Methylation as a crucial step in plant microRNA biogenesis. Science 307, 932-935.
76. Zou, S., Ke, N., Kim, J. M. & Voytas, D. F. 1996. The Saccharomyces retrotransposon Ty5 integrates preferentially into regions of silent chromatin at the telomeres and mating loci. Genes Dev. 10, 634-645.