An essential role for the DNA breakage-repair protein Ku80 in programmed DNA rearrangements in Tetrahymena thermophila

Molecular Biology of the Cell

Volumn 23, Issue 11, 2012, Pages 2213-2225

  Lin, I Ting ^a,b   Chao, Ju Lan ^a   Yao, Meng Chao ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA NUCLEOTIDYLEXOTRANSFERASE; PROTEIN; PROTEIN KU80; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN STRUCTURE; CHROMOSOME BREAKAGE; CONTROLLED STUDY; DNA CLEAVAGE; DNA DETERMINATION; DNA REPAIR; DNA STRAND BREAKAGE; HETEROCHROMATIN; MACRONUCLEUS; NONHUMAN; PRIORITY JOURNAL; TELOMERE; TETRAHYMENA THERMOPHILA;

ANTIGENS, NUCLEAR; BASE SEQUENCE; CHROMOSOME BREAKAGE; CONJUGATION, GENETIC; DNA BREAKS; DNA REPAIR; DNA, PROTOZOAN; DNA-BINDING PROTEINS; GENE REARRANGEMENT; GREEN FLUORESCENT PROTEINS; HISTONES; MACRONUCLEUS; METHYLATION; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; TETRAHYMENA THERMOPHILA;

MYXOZOA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

EID: 84861707950     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-11-0952     Document Type: Article

References (68)

1. Agrawal A, Eastman QM, Schatz DG (1998). Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394, 744-751. (Pubitemid 28391631)
2. Aronica L, Bednenko J, Noto T, DeSouza LV, Siu KW, Loidl J, Pearlman RE, Gorovsky MA, Mochizuki K (2008). Study of an RNA helicase implicates small RNA-noncoding RNA interactions in programmed DNA eliminationin Tetrahymena. Genes Dev 22, 2228-2241.
3. Austerberry CF, Allis CD, Yao MC (1984). Specific DNA rearrangements in synchronously developing nuclei of Tetrahymena. Proc Natl Acad Sci USA 81, 7383-7387. (Pubitemid 15196187)
4. Austerberry CF, Snyder RO, Yao MC (1989). Sequence microheterogeneity is generated at junctions of programmed DNA deletions in Tetrahymena thermophila. Nucleic Acids Res 17, 7263-7272.
5. Austerberry CF, Yao MC (1987). Nucleotide sequence structure and consistency of a developmentally regulated DNA deletion in Tetrahymena thermophila. Mol Cell Biol 7, 435-443. (Pubitemid 17230428)
6. Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan MB, Bartek J, Lukas J (2006). Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J Cell Biol 173, 195-206.
7. Borst P, Greaves DR (1987). Programmed gene rearrangements altering gene expression. Science 235, 658-667. (Pubitemid 17011105)
8. Bruns PJ, Cassidy-Hanley D (2000). Biolistic transformation of macro- and micronuclei. Methods Cell Biol 62, 501-512.
9. 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, 661-678.
10. Chalker DL (2008). Dynamic nuclear reorganization during genome remodeling of Tetrahymena. Biochim Biophys Acta 1783, 2130-2136.
11. Chalker DL, Yao MC (2001). Nongenic, bidirectional transcription precedes and may promote developmental DNA deletion in Tetrahymena thermophila. Genes Dev 15, 1287-1298.
12. Chalker DL, Yao MC (2011). DNA elimination in ciliates: transposon domestication and genome surveillance. Annu Rev Genet 45, 227-246.
13. Challoner PB, Blackburn EH (1986). Conservation of sequences adjacent to the telomeric C4A2 repeats of ciliate macronuclear ribosomal RNA gene molecules. Nucleic Acids Res 14, 6299-6311.
14. Cheng CY, Vogt A, Mochizuki K, Yao MC (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.
15. 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, 865-872.
16. 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, 942-946.
17. Downs JA, Jackson SP (2004). A means to a DNA end: the many roles of Ku. Nat Rev Mol Cell Biol 5, 367-378. (Pubitemid 38579474)
18. Ferguson DO, Alt FW (2001). DNA double strand break repair and chromosomal translocation: lessons from animal models. Oncogene 20, 5572-5579. (Pubitemid 32928098)
19. Gaertig J, Gu L, Hai B, Gorovsky MA (1994). High frequency vector-mediated transformation and gene replacement in Tetrahymena. Nucleic Acids Res 22, 5391-5398.
20. Gellert M (2002). V(D)J recombination: RAG proteins, repair factors, and regulation. Annu Rev Biochem 71, 101-132.
21. Gilley D, Preer JR Jr, Aufderheide KJ, Polisky B (1988). Autonomous replication and addition of telomerelike sequences to DNA microinjected into Paramecium tetraurelia macronuclei. Mol Cell Biol 8, 4765-4772.
22. Jeggo PA, Taccioli GE, Jackson SP (1995). Menage a trois: double strand break repair, V(D)J recombination and DNA-PK. Bioessays 17, 949-957.
23. Kapitonov VV, Jurka J (2005). RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 3, e181.
24. Kapusta A, Matsuda A, Marmignon A, Ku M, Silve A, Meyer E, Forney JD, Malinsky S, Betermier M (2011). Highly precise and developmentally programmed genome assembly in Paramecium requires ligase IV-dependent end joining. PLoS Genet 7, e1002049.
25. Klobutcher LA, Herrick G (1997). Developmental genome reorganization in ciliated protozoa: the transposon link. Prog Nucleic Acid Res Mol Biol 56, 1-62.
26. Le Mouel A, Butler A, Caron F, Meyer E (2003). Developmentally regulated chromosome fragmentation linked to imprecise elimination of repeated sequences in paramecia. Eukaryot Cell 2, 1076-1090. (Pubitemid 37298722)
27. Li J, Pearlman RE (1996). Programmed DNA rearrangement from an intron during nuclear development in Tetrahymena thermophila: molecular analysis and identification of potential cis-acting sequences. Nucleic Acids Res 24, 1943-1949. (Pubitemid 26156073)
28. Lieber MR (2010). The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 79, 181-211.
29. Lisby M, Barlow JH, Burgess RC, Rothstein R (2004). Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118, 699-713. (Pubitemid 39221730)
30. Liu Y, Taverna SD, Muratore TL, Shabanowitz J, Hunt DF, Allis CD (2007). RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena. Genes Dev 21, 1530-1545. (Pubitemid 46955725)
31. Lukas C, Bartek J, Lukas J (2005). Imaging of protein movement induced by chromosomal breakage: tiny "local" lesions pose great 'global' challenges. Chromosoma 114, 146-154. (Pubitemid 41349173)
32. 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. (Pubitemid 26337392)
33. Madireddi MT, Davis MC, Allis CD (1994). Identification of a novel polypeptide involved in the formation of DNA-containing vesicles during macronuclear development in Tetrahymena. Dev Biol 165, 418-431. (Pubitemid 24359807)
34. Malone CD, Anderson AM, Motl JA, Rexer CH, Chalker DL (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. (Pubitemid 41429102)
35. Matsuda A, Shieh AW, Chalker DL, Forney JD (2010). The conjugation-specific Die5 protein is required for development of the somatic nucleus in both Paramecium and Tetrahymena. Eukaryot Cell 9, 1087-1099.
36. Miao W, Xiong J, Bowen J, Wang W, Liu Y, Braguinets O, Grigull J, Pearlman RE, Orias E, Gorovsky MA (2009). Microarray analyses of gene expression during the Tetrahymena thermophila life cycle. PLoS One 4, e4429.
37. Misteli T, Soutoglou E (2009). The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat Rev Mol Cell Biol 10, 243-254.
38. Mochizuki K (2004). Conjugation-specific small RNAs in Tetrahymena have predicted properties of scan (scn) RNAs involved in genome rearrangement. Gene Dev 18, 2068-2073.
39. Mochizuki K, Fine NA, Fujisawa T, Gorovsky MA (2002). Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell 110, 689-699. (Pubitemid 35283959)
40. 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. (Pubitemid 40095818)
41. Mpoke S, Wolfe J (1996). DNA digestion and chromatin condensation during nuclear death in Tetrahymena. Exp Cell Res 225, 357-365. (Pubitemid 26183953)
42. Nikiforov MA, Smothers JF, Gorovsky MA, Allis CD (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.
43. Nowacki M, Higgins BP, Maquilan GM, Swart EC, Doak TG, Landweber LF (2009). A functional role for transposases in a large eukaryotic genome. Science 324, 935-938.
44. Orias E, Hamilton EP, Orias JD (2000). Tetrahymena as a laboratory organism: useful strains, cell culture, and cell line maintenance. Method Cell Biol 62, 189-211.
45. Pan WC, Blackburn EH (1981). Single extrachromosomal ribosomal RNA gene copies are synthesized during amplification of the rDNA in Tetrahymena. Cell 23, 459-466. (Pubitemid 11096339)
46. 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, 518-522. (Pubitemid 27398781)
47. Pergola F, Zdzienicka MZ, Lieber MR (1993). V(D)J recombination in mammalian cell mutants defective in DNA double-strand break repair. Mol Cell Biol 13, 3464-3471. (Pubitemid 23157283)
48. Rexer CH, Chalker DL (2007). Lia1p, a novel protein required during nuclear differentiation for genome-wide DNA rearrangements in Tetrahymena thermophila. Eukaryot Cell 6, 1320-1329. (Pubitemid 47257701)
49. Riha K, Heacock ML, Shippen DE (2006). The role of the nonhomologous end-joining DNA double-strand break repair pathway in telomere biology. Annu Rev Genet 40, 237-277. (Pubitemid 44956786)
50. Rio DC (2002). P transposable elements in Drosophila melanogaster. In: Mobile DNA II, eds. NL Craig, R Craigie, M Gellert, AM Lambowitz, Washington, DC: ASM Press, 484-518.
51. Saveliev SV, Cox MM (1994). The fate of deleted DNA produced during programmed genomic deletion events in Tetrahymena thermophila. Nucleic Acids Res 22, 5695-5701.
52. Saveliev SV, Cox MM (1995). Transient DNA breaks associated with programmed genomic deletion events in conjugating cells of Tetrahymena thermophila. Genes Dev 9, 248-255.
53. Saveliev SV, Cox MM (1996). Developmentally programmed DNA deletion in Tetrahymena thermophila by a transposition-like reaction pathway. EMBO J 15, 2858-2869. (Pubitemid 26176264)
54. Saveliev SV, Cox MM (2001). Product analysis illuminates the final steps of IES deletion in Tetrahymena thermophila. EMBO J 20, 3251-3261. (Pubitemid 32612012)
55. Smith JJ, Antonacci F, Eichler EE, Amemiya CT (2009). Programmed loss of millions of base pairs from a vertebrate genome. Proc Natl Acad Sci USA 106, 11212-11217.
56. Stover NA, Krieger CJ, Binkley G, Dong Q, Fisk DG, Nash R, Sethuraman A, Weng S, Cherry JM (2006). Tetrahymena Genome Database (TGD): a new genomic resource for Tetrahymena thermophila research. Nucleic Acids Res 34, D500-D503.
57. Taccioli GE, Rathbun G, Oltz E, Stamato T, Jeggo PA, Alt FW (1993). Impairment of V(D)J recombination in double-strand break repair mutants. Science 260, 207-210. (Pubitemid 23140884)
58. Tamura K, Dudley J, Nei M, Kumar S (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24, 1596-1599. (Pubitemid 47236692)
59. Taverna SD, Coyne RS, Allis CD (2002). Methylation of histone h3 at lysine 9 targets programmed DNA elimination in Tetrahymena. Cell 110, 701-711. (Pubitemid 35283960)
60. Wuitschick JD, Gershan JA, Lochowicz AJ, Li S, Karrer KM (2002). A novel family of mobile genetic elements is limited to the germline genome in Tetrahymena thermophila. Nucleic Acids Res 30, 2524-2537. (Pubitemid 34619006)
61. Yao MC (1989). Site-specific chromosome breakage and DNA deletion in ciliates. In: Mobile DNA, eds. DE Berg, MM Howe, Washington, DC: American Society for Microbiology, 715-734.
62. Yao MC, Chao JL (2005). RNA-guided DNA deletion in Tetrahymena: an RNAi-based mechanism for programmed genome rearrangements. Annu Rev Genet 39, 537-559.
63. Yao MC, Duharcourt S, Chalker DL (2002). Genome-wide rearrangements of DNA in ciliates. In: Mobile DNA II, eds. NL Craig, R Craigie, M Gellert, AM Lambowitz, Washington, DC: American Society for Microbiology, 730-758.
64. Yao MC, Fuller P, Xi X (2003). Programmed DNA deletion as an RNA-guided system of genome defense. Science 300, 1581-1584. (Pubitemid 36682891)
65. Yao MC, Gorovsky MA (1974). Comparison of the sequences of macro- and micronuclear DNA of Tetrahymena pyriformis. Chromosoma 48, 1-18.
66. Yao MC, Yao CH (1994). Detection of circular excised DNA deletion elements in Tetrahymena thermophila during development. Nucleic Acids Res 22, 5702-5708.
67. Yao MC, Yao CH, Halasz LM, Fuller P, Rexer CH, Wang SH, Jain R, Coyne RS, Chalker DL (2007). Identification of novel chromatin-associated proteins involved in programmed genome rearrangements in Tetrahymena. J Cell Sci 120, 1978-1989. (Pubitemid 47009994)
68. Zhu C, Bogue MA, Lim DS, Hasty P, Roth DB (1996). Ku86-deficient mice exhibit severe combined immunodeficiency and defective processing of V(D)J recombination intermediates. Cell 86, 379-389. (Pubitemid 26272078)