Elimination of foreign DNA during somatic differentiation in Tetrahymena thermophila shows position effect and is dosage dependent

Eukaryotic Cell

Volumn 4, Issue 2, 2005, Pages 421-431

  Liu, Yifan ^a,c   Song, Xiaoyuan ^a   Gorovsky, Martin A ^a   Karrer, Kathleen M ^a,b  

^a UNIVERSITY OF ROCHESTER   (United States)

^b Marquette University   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTOZOAL DNA;

ANIMAL; ARTICLE; CELL DIFFERENTIATION; CYTOLOGY; GENE SILENCING; GENETICS; GERMLINE MICRONUCLEUS; NUCLEOTIDE REPEAT; PHYSIOLOGY; TETRAHYMENA THERMOPHILA;

ANIMALS; CELL DIFFERENTIATION; DNA, PROTOZOAN; GENE SILENCING; MICRONUCLEUS, GERMLINE; REPETITIVE SEQUENCES, NUCLEIC ACID; TETRAHYMENA THERMOPHILA;

BACTERIA (MICROORGANISMS); CILIOPHORA; TETRAHYMENA THERMOPHILA;

EID: 13844306887     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.4.2.421-431.2005     Document Type: Article

References (87)

1. Ahlquist, P. 2002. RNA-dependent RNA polymerases, viruses, and RNA silencing. Science 296:1270-1273.
2. Austerberry, C. F., and M. C. Yao. 1987. Nucleotide sequence structure and consistency of a developmentally regulated DNA deletion in Tetrahymena thermophila. Mol. Cell. Biol. 7:435-443.
3. Austerberry, C. F., and M. C. Yao. 1988. Sequence structures of two developmentally regulated, alternative DNA deletion junctions in Tetrahymena thermophila. Mol. Cell. Biol. 8:3947-3950.
4. Bannister, A. J., P. Zegerman, J. F. Partridge, E. A. Miska, J. O. Thomas, R. C. Allshire, and T. Kouzarides. 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120-124.
5. Birchler, J. A., M. P. Bhadra, and U. Bhadra. 2000. Making noise about silence: repression of repeated genes in animals. Curr. Opin. Genet Dev. 10:211-216.
6. Bird, A. P., and A. P. Wolffe. 1999. Methylation-induced repression-belts, braces, and chromatin. Cell 99:451-454.
7. Brown, J. M., C. Marsala, R. Kosoy, and J. Gaertig. 1999. Kinesin-II is preferentially targeted to assembling cilia and is required for ciliogenesis and normal cytokinesis in Tetrahymena. Mol. Biol. Cell 10:3081-3096.
8. Burgess-Beusse, B., C. Farrell, M. Gaszner, M. Litt, V. Mutskov, F. Recillas-Targa, M. Simpson, A. West, and G. Felsenfeld. 2002. The insulation of genes from external enhancers and silencing chromatin. Proc. Natl. Acad. Sci. USA 99(Suppl. 4):16433-16437.
9. Carmell, M. A., Z. Xuan, M. Q. Zhang, and G. J. Hannon. 2002. The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16:2733-2742.
10. Cassidy-Hanley, D., J. Bowen, J. Lee, E. S. Cole, L. A. VerPlank, J. Gaertig, M. A. Gorovsky, and P. J. Bruns. 1997. Germline and somatic transformation of mating Tetrahymena thermophila by particle bombardment. Genetics 146:135-147.
11. Chaboissier, M. C., A. Bucheton, and D. J. Finnegan. 1998. Copy number control of a transposable element, the I factor, a LINE-like element in Drosophila. Proc. Natl. Acad. Sci. USA 95:11781-11785.
12. Chalker, D. L., A. La Terza, A. Wilson, C. D. Kroenke, and M. C. Yao. 1999. Flanking regulatory sequences of the Tetrahymena R deletion element determine the boundaries of DNA rearrangement. Mol. Cell. Biol. 19:5631-5641.
13. 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. Gill. Biol. 16:3658-3667.
14. Chalker, D. L., and M. C. Yao. 2001. Nongenic, bidirectional transcription precedes and may promote developmental DNA deletion in Tetmhymena thermophila. Genes Dev. 15:1287-1298.
15. Chau, M. F., and E. Orias. 1996. Developmentally programmed DNA rearrangement in Tetrohymena thermophila: Isolation and sequence characterization of three new alternative deletion systems. Biol. Cell 86:111-120.
16. Cherry, J. M., and E. H. Blackburn. 1985. The internally located telomeric sequences in the germ-line chromosomes of Tetrahymena are at the ends of transposon-like elements. Cell 43:747-758.
17. Coyne, R. S., D. L. Chalker, and M. C. Yao. 1996. Genome downsizing during ciliate development: nuclear division of labor through chromosome restructuring. Annu. Rev. Genet. 30:557-578.
18. Coyne, R. S., M. A. Nikiforov, J. F. Smothers, C. D. Allis, and M. C. Yao. 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. Czermin, B., R. Melfi, D. McCabe, V. Seitz, A. Imhof, and V. Pirrotta. 2002. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111:185-196.
20. Dernburg, A. F., and G. H. Karpen. 2002. A chromosome RNAissance. Cell 111:159-162.
21. Fillingham, J. S., D. Bruno, and R. E. Pearlman. 2001. Cis-acting requirements in flanking DNA for the programmed elimination of mse2.9: a common mechanism for deletion of internal eliminated sequences from the developing macronucleus of Tetrahymena thermophila. Nucleic Acids Res. 29:488-498.
22. Forrest, E. C., C. Cogoni, and G. Macino. 2004. The RNA-dependent RNA polymerase, QDE-1, is a rate-limiting factor in post-transcriptional gene silencing in Neurospora crassa. Nucleic Acids Res. 32:2123-2128.
23. Gaertig, J., L. Gu, B. Hai, and M. A. Gorovsky. 1994. High frequency vector-mediated transformation and gene replacement in Tetrahymena. Nucleic Acids Res. 22:5391-5398.
24. Godiska, R., C. James, and M. C. Yao. 1993. A distant 10-bp sequence specifies the boundaries of a programmed DNA deletion in Tetrahymena. Genes Dev. 7:2357-2365.
25. Godiska, R., and M. C. Yao. 1990. A programmed site-specific DNA rearrangement in Tetrahymena thermophila requires flanking polypurine tracts. Cell 61:1237-1246.
26. Gorovsky, M. A. 1970. Studies on nuclear structure and function in Tetrahymena pyriformis. II. Isolation of macro- and micronuclei. J. Cell Biol. 47:619-630.
27. Gorovsky, M. A., and J. Woodard. 1967. Histone content of chromosomal loci active and inactive in RNA synthesis. J. Cell Biol. 33:723-728.
28. Gorovsky, M. A., M.-C. Yao, J. B. Keevert, and G. L. Pieger. 1975. Isolation of micro- and macronuclei of Tetrahymena pyriformis. Methods Cell Biol. IX: 311-327.
29. Hai, B., and M. A. Gorovsky. 1997. Germ-line knockout heterokaryons of an essential a-tubulin gene enable high-frequency gene replacement and a test of gene transfer from somatic to germ-line in Tetrahymena thermophila. Proc. Natl. Acad. Sci. USA 94:1310-1315.
30. Hall, I. M., G. D. Shankaranarayana, K. Noma, N. Ayoub, A. Cohen, and S. I. Grewal. 2002. Establishment and maintenance of a heterochromatin domain. Science 297:2232-2237.
31. Howard, E. A., and E. H. Blackburn. 1985. Reproducible and variable genomic rearrangements occur in the developing somatic: nucleus of the ciliate Tetrahymena thermophila. Mol. Cell. Biol. 5:2039-2050.
32. Huvos, P. E., M. Wu, and M. A. Gorovsky. 1998. A developmentally eliminated sequence in the flanking region of the histone H1 gene in Tetrahymena thermophila contains short repeats. J. Eukaryot. Microbiol. 45:189-197.
33. Jackson, J. P., A. M. Lindroth, X. Cao, and S. E. Jacobsen. 2002. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556-560.
34. Jahn, C. L., and L. A. Klobutcher. 2002. Genome remodeling in ciliated protozoa. Annu. Rev. Microbiol. 56:489-520.
35. Jensen, S., M. P. Gassama, and T. Heidmann. 1999. Taming of transposable elements by homology-dependent gene silencing. Nat. Genot. 21:209-212.
36. Jenuwein, T. 2002. Molecular biology. An RNA-guided pathway for the epigenome. Science 297:2215-2218.
37. Kahn, R. W., B. H. Andersen, and C. F. Brunk. 1993. Transformation of Tetrahymena thermophila by microinjection of a foreign gene. Proc. Natl. Acad. Sci. USA 90:9295-9299.
38. Karrer, K. M. 1983. Germ line-specific DNA sequences are present on all five micronuclear chromosomes in Tetrahymena thermophila. Mol. Cell. Biol. 3:1909-1919.
39. Karrer, K. M. 2000. Tetrahymena genetics: two nuclei are better than one. Methods Cell Biol. 62:127-186.
40. Kelly, W. G., and A. Fire. 1998. Chromatin silencing and the maintenance of a functional germline in Caenorhabditis elegans. Development 125:2451-2456.
41. Retting, R. F., T. H. Haverkamp, H. G. van Luenen, and R. H. Plasterk. 1999. Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell 99:133-141.
42. Lachner, M., D. O'Carroll, S. Rea, K. Mechtler, and T. Jenuwein. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116-120.
43. Lingel, A., B. Simon, E. Izaurralde, and M. Sattler. 2003. Structure and nucleic-acid binding of the Drosophila Argonaute 2 PAZ domain. Nature 426:465-469.
44. 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.
45. 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.
46. Maison, C., D. Bailly, A. H. Peters, J. P. Quivy, D. Roche, A. Taddei, M. Lachner, T. Jenuwein, and G. Almouzni. 2002. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat. Genet. 30:329-334.
47. Martindale, D. W., C. D. Allis, and P. J. Bruns. 1985. RNA and protein synthesis during meiotic prophase in Tetrahymena thermophila. J. Protozool. 32:644-649.
48. 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.
49. Meyer, E., and S. Duharcourt. 1996. Epigenetic programming of developmental genome rearrangements in ciliates. Cell 87:9-12.
50. 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.
51. Mochizuki, K., and M. A. Gorovsky. 2004. Conjugation-specific small RNAs in Tetrahymena have predicted properties of scan (sen) RNAs involved in genome rearrangement. Genes Dev. 18:2068-2073.
52. Mochizuki, K., and M. A. Gorovsky. 2004. Small RNAs in genome rearrangement in Tetrahymena. Curr. Opin. Genet. Dev. 14:1-7.
53. Muchardt, C., M. Guilleme, J. S. Seeler, D. Trouche, A. Dejean, and M. Yaniv. 2002. Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1alpha. EMBO Rep. 3:975-981.
54. Muller, J., C. M. Hart, N. J. Francis, M. L. Vargas, A. Sengupta, B. Wild, E. L. Miller, M. B. O'Connor, R. E. Kingston, and J. A. Simon. 2002. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111:197-208.
55. Nakayama, J., J. C. Rice, B. D. Strahl, C. D. Allis, and S. I. Grewal. 2001. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292:110-113.
56. Napoli, C., C. Lemieux, and R. Jorgensen. 1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279-289.
57. Orias, E., and M. Flacks. 1975. Macronuclear genetics of Tetrahymena. I. Random distribution of macronuclear genecopies in T. pyriformis, syngen 1. Genetics 79:187-206.
58. Pal-Bhadra, M., U. Bhadra, and J. A. Birchler. 2002. RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila. Mol. Cell 9:315-327.
59. Pal-Bhadra, M., B. A. Leibovitch, S. G. Gandhi, M. Rao, U. Bhadra, J. A. Birchler, and S. C. Elgin. 2004. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303:669-672.
60. Patil, N. S., P. M. Hempen, R. A. Udani, and K. M. Karrer. 1997. Alternate junctions and microheterogeneity of Tlr1, a developmentally regulated DNA rearrangement in Tetrahymena thermophila. J. Eukaryot. Microbiol. 44:518-522.
61. Plasterk, R. H. 2002. RNA silencing: the genome's immune system. Science 296:1263-1265.
62. Que, Q., and R. A. Jorgensen. 1998. Homology-based control of gene expression patterns in transgenic petunia flowers. Dev. Genet. 22:100-109.
63. Reinhart, B. J., and D. P. Bartel. 2002. Small RNAs correspond to centromere heterochromatic repeats. Science 297:1831.
64. Rogers, M. B., and K. M. Karrer. 1985. Adolescence in Tetrahymena thermophila. Proc. Natl. Acad. Sci. USA 82:436-439.
65. Romano, N., and G. Macino. 1992. Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol. Microbiol. 6:3343-3353.
66. Selker, E. U. 1997. Epigenetic phenomena in filamentous fungi: useful paradigms or repeat-induced confusion? Trends Genet. 13:296-301.
67. 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.
68. Shen, X., L. Yu, J. W. Weir, and M. A. Gorovsky. 1995. Linker histones are not essential and affect chromatin condensation in vivo. Cell 82:47-56.
69. Sijen, T., J. Fleenor, F. Simmer, K. L. Thijssen, S. Parrish, L. Timmons, R. H. Plasterk, and A. Fire. 2001. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107:465-476.
70. Song, J. J., J. Liu, N. H. Tolia, J. Schneiderman, S. K. Smith, R. A. Martienssen, G. J. Hannon, and L. Joshua-Tor. 2003. The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat. Struct. Biol. 10:1026-1032.
71. Sugai, T., and K. Hiwatashi. 1974. Cytologic and autoradiographic studies of the micronucleus at meiotic prophase in Tetrahymena pyriformis. J. Protozool. 21:542-548.
72. Tabara, H., M. Sarkissian, W. G. Kelly, J. Fleenor, A. Grishok, L. Timmons, A. Fire, and C. C. Mello. 1999. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell. 99:123-132.
73. 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.
74. Tie, F., T. Furuyama, and P. J. Harte. 1998. The Drosophila Polycomb group proteins ESC and E(Z) bind directly to each other and co-localize at multiple chromosomal sites. Development 125:3483-3496.
75. Tijsterman, M., R. F. Retting, and R. H. Plasterk. 2002. The genetics of RNA silencing. Annu. Rev. Genet. 36:489-519.
76. van der Krol, A. R., L. A. Mur, M. Beld, J. N. Mol, and A. R. Stuitje. 1990. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2:291-299.
77. 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.
78. Volpe, T. A., C. Kidner, I. M. Hall, G. Teng, S. I. Grewal, and R. A. Martienssen. 2002. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833-1837.
79. Wolffe, A. P., and M. A. Matzke. 1999. Epigenetics: Regulation through repression. Science 286:481-486.
80. Wuitschick, J. D., J. A. Gershan, A. J. Lochowicz, S. Li, and K. M. Karrer. 2002. A novel family of mobile genetic elements is limited to the germline genome in Tetrahymena thermophila. Nucleic Acids Res. 30:2524-2537.
81. Wuitschick, J. D., and K. M. Karrer. 2003. Diverse sequences within TIr elements target programmed DNA elimination in Tetrahymena thermophila. Eukaryot. Cell 2:678-689.
82. Yan, K. S., S. Yan, A. Farooq, A. Han, L. Zeng, and M. M. Zhou. 2003. Structure and conserved RNA binding of the PAZ domain. Nature 426:468-474.
83. Yao, M. C. 1996. Programmed DNA deletions in Tetrahymena: mechanisms and implications. Trends Genet. 12:26-30.
84. Yao, M. C., P. Fuller, and X. Xi. 2003. Programmed DNA deletion as an RNA-guided system of genome defense. Science 300:1581-1584.
85. Yao, M. C., and M. A. Gorovsky. 1974. Comparison of the sequences of macro- and micronuclear DNA of Telrahymena pyriformis. Chromosoma 48:1-18.
86. Yu, L., and M. A. Gorovsky. 1997. Constitutive expression, not a particular primary sequence, is the important feature of the H3 replacement variant hv2 in Tetrahymena thermophila. Mol. Cell. Biol. 17:6303-6310.
87. Zilberman, D., X. Cao, and S. E. Jacobsen. 2003. ARGONAUTE4 control of locus-specific small interfering RNA accumulation and DNA and histone methylation. Science 299:716-719.