RNA-guided DNA deletion in tetrahymena: An RNAi-based mechanism for programmed genome rearrangements

Annual Review of Genetics

Volumn 39, Issue , 2005, Pages 537-559

  Yao, Meng Chao ^a,b   Chao, Ju Lan ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Chromatin diminution; Gene silencing; Genome surveillance; Heterochromatin; sRNA

Indexed keywords

CHROMATIN STRUCTURE; DNA FLANKING REGION; GENE REARRANGEMENT; GENE SILENCING; HETEROCHROMATIN; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; TETRAHYMENA;

ANIMALS; CHROMATIN; GENE REARRANGEMENT; LIFE CYCLE STAGES; RNA INTERFERENCE; TETRAHYMENA;

CILIOPHORA; MYXOZOA; NEMATODA; PROTISTA; TETRAHYMENA;

EID: 27244436895     PISSN: 00664197     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.genet.39.073003.095906     Document Type: Review

References (100)

1. Altschuler MI, Yao MC. 1985. Macronuclear DNA of Tetrahymena thermophila exists as defined subchromosomal-sized molecules. Nucleic Acids Res. 13:5817-31
2. Austerberry CF, Allis CD, Yao MC. 1984. Specific DNA rearrangements in synchronously developing nuclei of Tetrahymena. Proc. Natl. Acad. Sci. USA 81:7383-87
3. Austerberry CF, Snyder RO, Yao MC. 1989. Sequence microheterogeneity is generated at junctions of programmed DNA deletions in Tetrahymena thermophila. Nucleic Acids Res. 17:7263-72
4. Austerberry CF, Yao MC. 1987. Nucleotide sequence structure and consistency of a developmentally regulated DNA deletion in Tetrahymena thermophila. Mol. Cell. Biol. 7:435-43
5. Austerberry CF, Yao MC. 1988. Sequence structures of two developmentally regulated, alternative DNA deletion junctions in Tetrahymena thermophila. Mol. Cell. Biol. 8:3947-50
6. Baird SE, Fino GM, Tausta SL, Klobutcher LA. 1989. Micronuclear genome organization in Euplotes crassus: a transposonlike element is removed during macronuclear development. Mol. Cell. Biol. 9:3793-807
7. Beerman S. 1977. The diminution of heterochromatic chromosomal segments in Cyclops (Crustacea, Copepoda). Chromosoma 60:297-344
8. Beerman S. 1984. Circular and linear structures in chromatin diminution of Cyclops. Chromosoma 89:321-28
9. Betermier M, Duharcourt S, Seitz H, Meyer E. 2000. Timing of developmentally programmed excision and circularization of Paramecium internal eliminated sequences. Mol. Cell. Biol. 20:1553-61
10. Borst P, Greaves PR. 1987. Programmed gene rearragements altering gene expression. Science 235:658-67
11. Boveri T. 1887. Über Differenzierung der Zellkerne während der Furchung des Eies von Ascaris megalocepbala. Anat. Anz. 2:688-93
12. Callahan RC, Shalke G, Gorovsky MA. 1984. Developmental rearrangements associated with a single type of expressed alpha-tubulin gene in Tetrahymena. Cell 36:441-45
13. Caron F. 1992. A high degree of macronuclear chromosome polymorphism is generated by variable DNA rearrangements in Paramecium primaurelia during macronuclear differentiation. J. Mol. Biol. 225:661-78
14. Chalker DL, Fuller P, Yao MC. 2005. Communication between parental and developing genomes during tetrahymena nuclear differentiation is likely mediated by homologous RNAs. Genetics 169:149-60
15. Chalker DL, La Terza A, Wilson A, Kroenke CD, Yao MC. 1999. Flanking regulatory sequences of the Tetrahymena R deletion element determine the boundaries of DNA rearrangement. Mol. Cell. Biol. 19:5631-41
16. Chalker DL, Yao MC. 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. 16:3658-67
17. Chalker DL, Yao MC. 2001. Nongenic, bidirectional transcription precedes and may promote developmental DNA deletion in Tetrahymena thermophila. Genes Dev. 15:1287-98
18. Cherry JM, Blackburn EH. 1985. The internally located telomeric sequences in the germline chromosomes of Tetrahymena are at the conserved ends of transposon-like elements. Cell 43:747-58
19. Conover RK, Brunk CF. 1986. Macronuclear DNA molecules of Tetrahymena thermophila. Mol. Cell. Biol. 6:900-5
20. Coyne RS, Chalker DL, Yao MC. 1996. Genome downsizing during ciliate development: nuclear division of labor through chromosome restructuring. Annu. Rev. Genet. 30:557-78
21. Coyne RS, Nikiforov MA, Smothers JF, Allis CD, Yao MC. 1999. Parental expression of the chromodomain protein Pdd1p is required for completion of programmed DNA elimination and nuclear differentiation. Mol. Cell 4:865-72
22. Coyne RS, Yao MC. 1996. Evolutionary conservation of sequences directing chromosome breakage and rDNA palindrome formation in tetrahymenine ciliates. Genetics 144:1479-87
23. Doak TG, Doerder FP, Jahn CL, Herrick G. 1994. A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common D35E motif. Proc. Natl. Acad. Sci. USA 91:942-46
24. Duharcourt S, Butler A, Meyer E. 1995. Epigenetic self-regulation of developmental excision of an internal eliminated sequence on Paramecium tetraurelia. Genes Dev. 9:2065-77
25. Duharcourt S, Yao MC. 2002. Role of histone deacetylation in developmentally programmed DNA rearrangements in Tetrahymena thermophila. Eukaryot. Cell 1:293-303
26. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-98
27. Epstein LM, Forney JD. 1984. Mendelian and non-Mendelian mutations affecting surface antigen expression in Paramecium tetraurelia. Mol. Cell. Biol. 4:1583-90
28. Fan Q, Yao M-C. 2000. Along stringent sequence for programmed chromosome breakage in Tetrahymena thermophila. Nucleic Acids Res. 28:895-900
29. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-11
30. Forney JD, Blackburn EH. 1988. Developmentally controlled telomere addition in wild-type and mutant Paramecia. Mol. Cell. Biol. 8:251-58
31. Freitag M, Lee DW, Kothe GO, Pratt RJ, Aramayo R, Selker EU. 2004. DNA methylation is independent of RNA interference in Neurospora. Science 304:1939
32. Gershan JA, Karrer KM. 2000. A family of developmentally excised DNA elements in Tetrahymena is under selective pressure to maintain an open reading frame encoding an integrase-like protein. Nucleic Acids Res. 28:4105-12
33. Godiska R, James C, Yao MC. 1993. A distant 10-bp sequence specifies the boundaries of a programmed DNA deletion in Tetrahymena. Genes Dev. 7:2357-65
34. Godiska R, Yao MC. 1990. A programmed site-specific DNA rearrangement in Tetrahymena thermophila requires flanking polypurine tracts. Cell 61:1237-46
35. Greslin AF, Prescott DM, Oka Y, Loukin SH, Chappell JC. 1989. Reordering of nine exons is necessary to form a functional actin gene in Oxytricha nova. Proc. Natl. Acad. Sci. USA 86:6264-68
36. Grewal SI, Moazed D. 2003. Heterochromatin and epigenetic control of gene expression. Science 301:798-802
37. Grishok A, Sinskey JL, Sharp PA. 2005. Transcriptional silencing of a transgene by RNAi in the soma of C. elegans. Genes Dev. 19:683-96
38. Heinonen TY, Pearlman RE. 1994. A germ line-specific sequence element in an intron in Tetrahymena thermophila. J. Biol. Chem. 269:17428-33
39. Herrick G, Cartinhour S, Dawson D, Ang D, Sheets R, et al. 1985. Mobile elements bounded by C4A4 telomeric repeats in Oxytricha fallax. Cell 43:759-68
40. Jahn CL, Krikau MF, Shyman S. 1989. Developmentally coordinated en masse excision of a highly repetitive element in Euplotes crassus. Cell 59:1009-18
41. Jahn CL, Nilles LA, Krikau MF. 1988. Organization of the Euplotes crassus micronuclear genome. J. Protozoal. 35:590-601
42. Katoh M, Hirono M, Takemasa T, Kimura M, Watanabe Y. 1993. A micronucleus-specific sequence exists in the 5′-upstream region of calmodulin gene in Tetrahymena thermophila. Nucleic Acids Res. 21:2409-14
43. King BO, Yao MC. 1982. Tandemly repeated hexanucleotide at Tetrahymena rDNA free end is generated from a single copy during development. Cell 31:177-82
44. Klobutcher LA, Herrick G. 1997. Developmental genome reorganization in ciliated protozoa: the transposon link. Prog. Nucleic Acid Res. Mol. Biol. 56:1-62
45. Kubota S, Kuro-o M, Mizuno S, Kohno S-I. 1993. Germ line-restricted, highly repeated DNA sequences and their chromosomal localization in a Japanese hagfish (Eptatretus okinoseanus). Chromosoma 102:163-73
46. Kuhn EJ, Geyer PK. 2003. Genomic insulators: connecting properties to mechanism. Curr. Opin. Cell Biol. 15:259-65
47. Landweber LF, Kuo T-C, Curtis EA. 2000. Evolution and assembly of an extremely scrambled gene. Proc. Natl. Acad. Sci. USA 97:3298-303
48. Lawn RM, Heumann JM, Herrick G, Prescott DM. 1978. The gene-size DNA molecules in Oxytricha. Cold Spring Harbor Symp. Quant. Biol. 43:483-92
49. Liu Y, Mochizuki K, Gorovsky MA. 2004. Histone H3 lysine 9 methylation is required for DNA elimination in developing macronuclei in Tetrahymena. Proc. Natl. Acad. Sci. USA 101:1679-84
50. Liu Y, Song X, Gorovsky MA, Karrer KM. 2005. Elimination of foreign DNA during somatic differentiation in Tetrahymena thermophila shows position effect and is dosage dependent. Eukaryot. Cell 4:421-31
51. Madireddi MT, Coyne RS, Smothers JF, Mickey KM, Yao MC, Allis CD. 1996. Pdd1p, a novel chromodomain-containing protein, links heterochromatin assembly and DNA elimination in Tetrahymena. Cell 87:75-84
52. Marczynski GT, Jaehning JA. 1985. A transcription map of a yeast centromere plasmid: unexpected transcripts and altered gene expression. Nucleic Acids Res. 13:8487-506
53. Matzke MA, Birchler JA. 2005. RNAi-mediated pathways in the nucleus. Nat. Rev. Genet. 6:24-35
54. Meister G, Tuschl T. 2004. Mechanisms of gene silencing by double-stranded RNA. Nature 431:343-49
55. Mello CC, Conte D Jr. 2004. Revealing the world of RNA interference. Nature 431:338-42
56. Meyer E, Duharcourt S. 1996. Epigenetic programming of developmental genome rearrangements in ciliates. Cell 87:9-12
57. Mochizuki K, Fine N, Fujisawa T, Gorovsky M. 2002. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell 110:689-99
58. Mochizuki K, Gorovsky MA. 2004. Conjugation-specific small RNAs in Tetrahymena have predicted properties of scan (scn) RNAs involved in genome rearrangement. Genes Dev. 18:2068-73
59. Mochizuki K, Gorovsky MA. 2004. Small RNAs in genome rearrangement in Tetrahymena. Curr. Opin. Genet. Dev. 14:181-87
60. Mochizuki K, Gorovsky MA. 2005. A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase. Genes Dev. 19:77-89
61. Muller F, Chantal W, Spicher A, Tobler H. 1991. New telomere formation after developmentally regulated chromosomal breakage during the process of chromatin dimunition in Ascaris lumbricoides. Cell 67:815-22
62. Nakai Y, Kubota S, Kohno S. 1991. Chromatin diminution and chromosome elimination in four Japanese hagfish species. Cytogenet. Cell Genet. 65:196-98
63. Nikiforov MA, Gorovsky MA, Allis CD. 2000. A novel chromodomain protein pdd3p, associates with internal eliminated sequences during macronuclear development in Tetrahymena thermophila. Mol. Cell. Biol. 20:4128-34
64. Orias E. 1986. Ciliate conjugation. In The Molecular Biology of Ciliated Protozoa, ed. JG Gall, pp. 45-84. Orlando, FL: Academic
65. Patil NS, Hempen PM, Udani RA, Karrer KM. 1997. Alternate junctions and microheterogeneity of Tlr1, a developmentally regulated DNA rearrangement in Tetrahymena thermophila. J. Eukaryot. Microbiol. 44:518-22
66. Preer JR, Freer LB. 1979. The size of macronuclear DNA and its relationships to models for maintaining genic balance. J. Protozool. 26:14-18
67. Prescott DM. 1994. The DNA of ciliated protozoa. Microbiol. Rev. 58:233-67
68. Prescott DM, Murti KG, Bostock CJ. 1973. Genetic apparatus of Stylonychia sp. Nature 242:597-600
69. Saveliev SV, Cox MM. 1994. The fate of deleted DNA produced during programmed genomic deletion events in Tetrahymena thermophila. Nucleic Acids Res. 22:5695-701
70. Saveliev SV, Cox MM. 1995. Transient DNA breaks associated with programmed genomic deletion events in conjugating cells of Tetrahymena thermophila. Genes Dev. 9:248-55
71. Saveliev SV, Cox MM. 1996. Developmentally programmed DNA deletion in Tetrahymena thermophila by a transposition-like reaction pathway. EMBO J. 15:2858-69
72. Selker EU. 1999. Gene silencing: repeats that count. Cell 97:157-60
73. Selker EU, Cambareri EB, Jensen BC, Haack KR. 1987. Rearrangement of duplicated DNA in specialized cells of Neurospora. Cell 51:741-52
74. Sharp PA, Zamore PD. 2000. Molecular biology. RNA interference. Science 287:2431-33
75. Sijen T, Plasterk RH. 2003. Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature 426:310-14
76. Sonneborn TM. 1977. Genetics of cellular differentiation: stable nuclear differentiation in eukaryotic unicells. Annu. Rev. Genet. 11:349-67
77. Swanton MT, Heumann JM, Prescott DM. 1980. Gene-sized DNA molecules of the macronuclei in three species of hypotrichs: size distributions and absence of nicks. DNA of ciliated protozoa. VIII. Chromosoma 77:217-27
78. Tausta SL, Klobutcher LA. 1989. Detection of circular forms of eliminated DNA during macronuclear development in E. crassus. Cell 59:1019-26
79. Taverna S, Coyne R, Allis C. 2002. Methylation of histone H3 at lysine 9 targets programmed DNA elimination in Tetrahymena. Cell 110:701
80. Tobler H. 1986. The differentiation of germinal and somatic cell lines in nematodes. In Germ Line-Soma Differentiation, ed. W Hennig, pp. 1-70. New York: Springer-Verlag Press
81. Tobler H, Eiter A, Muller F. 1992. Chromatin dimunition in nematode development. Trends Genet. 8:427-32
82. Verona RI, Mann MR, Bartolomei MS. 2003. Genomic imprinting: intricacies of epigenetic regulation in clusters. Annu. Rev. Cell Dev. Biol. 19:237-59
83. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA. 2002. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833-37
84. Wells JM, Ellingson JL, Catt DM, Berger PJ, Karrer KM. 1994. A small family of elements with long inverted repeats is located near sites of developmentally regulated DNA rearrangement in Tetrahymena thermophila. Mol. Cell. Biol. 14:5939-49
85. Williams K, Doak TG, Herrick G. 1993. Developmental precise excision of Oxytricha trifallax telomere-bearing elements and formation of circles closed by a copy of the flanking target duplication. EMBO J. 12:4593-601
86. Wuitschick JD, Karrer KM. 2003. Diverse sequences within Tlr elements target programmed DNA elimination in Tetrahymena thermophila. Eukaryot. Cell 2:678-89
87. Yao M, Duharcourt S, Chalker D. 2002. Genome-wide rearrangements of DNA in ciliates. In Mobile DNA II, ed. N Craig, R Craigie, M Gellert, A Lambowitz, pp. 730-58. Washington, DC: ASM Press
88. Deleted in proof
89. Yao MC. 1986. Amplification of ribosomal RNA genes. In The Molecular Biology of Ciliated Protozoa, ed. JG Gall, pp. 179-201. Orlando, FL: Academic
90. Yao MC, Yao C-H, Monks B. 1990. The controlling sequence for site-specific chromosome breakage in Tetrahymena. Cell 63:763-72
91. Yao MC, Zheng K, Yao C-H. 1987. A conserved nucleotide sequence at the sites of developmentally regulated chromosomal breakage in Tetrahymena. Cell 48:779-88
92. Yao MC. 1981. Ribosomal RNA gene amplification in Tetrahymena may be associated with chromosome breakage and DNA elimination. Cell 24:765-74
93. Yao MC. 1982. Elimination of specific DNA sequences from the somatic nucleus of the ciliate Tetrahymena. J. Cell Biol. 92:783-89
94. Yao MC, Choi J, Yokoyama S, Austerberry CF, Yao CH. 1984. DNA elimination in Tetrahymena: a developmental process involving extensive breakage and rejoining of DNA at defined sites. Cell 36:433-40
95. Yao MC, Fuller P, Xi X. 2003. Programmed DNA deletion as an RNA-guided system of genome defense. Science 300:1581-84
96. Yao MC, Gorovsky MA. 1974. Comparison of the sequences of macro- and micronuclear DNA of Tetrahymena pyriformis. Chromosoma 48:1-18
97. Yao MC, Kimmel AR, Gorovsky MA. 1974. A small number of cistrons for ribosomal RNA in the germinal nucleus of a eukaryote, Tetrahymena pyriformis. Proc. Natl. Acad. Sci. USA 71:3082-86
98. Yao MC, Yao CH. 1989. Accurate processing and amplification of cloned germ line copies of ribosomal DNA injected into developing nuclei of Tetrahymena thermophila. Mol. Cell. Biol. 9:1092-99
99. Yao MC, Yao CH. 1994. Detection of circular excised DNA deletion elements in Tetrahymena thermophila during development. Nucleic Acids Res. 22:5702-8
100. Yao MC, Zhu SG, Yao CH. 1985. Gene amplification in Tetrahymena thermophila: formation of extrachromosomal palindromic genes coding for rRNA. Mol. Cell. Biol. 5:1260-67