LIA5 Is Required for Nuclear Reorganization and Programmed DNA Rearrangements Occurring during Tetrahymena Macronuclear Differentiation

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Shieh, Annie Wan Yi ^a   Chalker, Douglas L ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DNA; LIA5 PROTEIN; PDD1P PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS; CONTROLLED STUDY; DNA DAMAGE; FRAGMENTATION REACTION; GENE REARRANGEMENT; GERM LINE; HETEROCHROMATIN; MACRONUCLEUS; NONHUMAN; PROTEIN DEPHOSPHORYLATION; RNA INTERFERENCE; TETRAHYMENA; TRANSPOSON; ULTRAVIOLET RADIATION; WILD TYPE;

AMINO ACID SEQUENCE; CELL NUCLEUS; CHROMOSOME BREAKAGE; CHROMOSOMES; DNA DAMAGE; DNA TRANSPOSABLE ELEMENTS; GENE KNOCKOUT TECHNIQUES; GENE ORDER; GENE REARRANGEMENT; HETEROCHROMATIN; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT; TETRAHYMENA THERMOPHILA; ZINC FINGERS;

EID: 84884222434     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075337     Document Type: Article

References (59)

1. Keeney S, Giroux CN, Kleckner N, (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375-384. doi:10.1016/S0092-8674(00)81876-0. PubMed: 9039264.
2. McBlane JF, van Gent DC, Ramsden DA, Romeo C, Cuomo CA, et al. (1995) Cleavage at a V(D)J recombination signal requires only RAG1 and RAG2 proteins and occurs in two steps. Cell 83: 387-395. doi:10.1016/0092-8674(95)90116-7. PubMed: 8521468.
3. Kanaar R, Wyman C, Rothstein R, (2008) Quality control of DNA break metabolism: in the 'end', it's a good thing. EMBO J 27: 581-588. doi:10.1038/emboj.2008.11. PubMed: 18285819.
4. Bassing CH, Chua KF, Sekiguchi J, Suh H, Whitlow SR, et al. (2002) Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc Natl Acad Sci U S A 99: 8173-8178. doi:10.1073/pnas.122228699. PubMed: 12034884.
5. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, et al. (2002) Genomic instability in mice lacking histone H2AX. Science 296: 922-927. doi:10.1126/science.1069398. PubMed: 11934988.
6. Rogakou EP, Boon C, Redon C, Bonner WM, (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905-916. doi:10.1083/jcb.146.5.905. PubMed: 10477747.
7. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM, (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868. doi:10.1074/jbc.273.10.5858. PubMed: 9488723.
8. 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. doi:10.1038/nrm2651. PubMed: 19277046.
9. Kim JA, Kruhlak M, Dotiwala F, Nussenzweig A, Haber JE, (2007) Heterochromatin is refractory to gamma-H2AX modification in yeast and mammals. J Cell Biol 178: 209-218. doi:10.1083/jcb.200612031. PubMed: 17635934.
10. Ayoub N, Jeyasekharan AD, Venkitaraman AR, (2009) Mobilization and recruitment of HP1: a bimodal response to DNA breakage. Cell Cycle 8: 2945-2950. PubMed: 19657222.
11. Ball AR Jr., Yokomori K, (2009) Revisiting the role of heterochromatin protein 1 in DNA repair. J Cell Biol 185: 573-575. doi:10.1083/jcb.200904033. PubMed: 19451270.
12. Dinant C, Luijsterburg MS, (2009) The emerging role of HP1 in the DNA damage response. Mol Cell Biol 29: 6335-6340. doi:10.1128/MCB.01048-09. PubMed: 19805510.
13. Chalker DL, Yao MC, (2011) DNA elimination in ciliates: transposon domestication and genome surveillance. Annu Rev Genet 45: 227-246. doi:10.1146/annurev-genet-110410-132432. PubMed: 21910632.
14. Kataoka K, Mochizuki K, (2011) Programmed DNA elimination in Tetrahymena: a small RNA-mediated genome surveillance mechanism. Adv Exp Med Biol 722: 156-173. doi:10.1007/978-1-4614-0332-6_10. PubMed: 21915788.
15. Karrer KM, (2000) Tetrahymena genetics: two nuclei are better than one. Methods Cell Biol 62: 127-186. PubMed: 10503190.
16. Orias E, Cervantes MD, Hamilton EP, (2011) Tetrahymena thermophila, a unicellular eukaryote with separate germline and somatic genomes. Res Microbiol 162: 578-586. doi:10.1016/j.resmic.2011.05.001. PubMed: 21624459.
17. Yao MC, Gorovsky MA, (1974) Comparison of the sequences of macro- and micronuclear DNA of Tetrahymena pyriformis. Chromosoma 48: 1-18. PubMed: 4218159.
18. 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: 433-440. doi:10.1016/0092-8674(84)90236-8. PubMed: 6319023.
19. Fass JN, Joshi NA, Couvillion MT, Bowen J, Gorovsky MA, et al. (2011) Genome-Scale Analysis of Programmed DNA Elimination Sites in Tetrahymena thermophila. G3 (Bethesda) 1: 515-522 PubMed: 22384362.
20. Yao MC, Yao CH, Monks B, (1990) The controlling sequence for site-specific chromosome breakage in Tetrahymena. Cell 63: 763-772. doi:10.1016/0092-8674(90)90142-2. PubMed: 2225076.
21. Cassidy-Hanley D, Bisharyan Y, Fridman V, Gerber J, Lin C, et al. (2005) Genome-wide characterization of Tetrahymena thermophila chromosome breakage sites. II. Physical and genetic mapping. Genetics 170: 1623-1631.
22. Hamilton E, Bruns P, Lin C, Merriam V, Orias E, et al. (2005) Genome-wide characterization of Tetrahymena thermophila chromosome breakage sites. I. Cloning and identification of functional sites. Genetics 170: 1611-1621.
23. 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. doi:10.1016/S0092-8674(02)00909-1. PubMed: 12297043.
24. Taverna SD, Coyne RS, Allis CD, (2002) Methylation of histone h3 at lysine 9 targets programmed DNA elimination in tetrahymena. Cell 110: 701-711. doi:10.1016/S0092-8674(02)00941-8. PubMed: 12297044.
25. 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. doi:10.1128/MCB.25.20.9151-9164.2005. PubMed: 16199890.
26. 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. doi:10.1101/gad.1265105. PubMed: 15598983.
27. Liu Y, Taverna SD, Muratore TL, Shabanowitz J, Hunt DF, et al. (2007) RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena. Genes Dev 21: 1530-1545. doi:10.1101/gad.1544207. PubMed: 17575054.
28. Madireddi MT, Coyne RS, Smothers JF, Mickey KM, Yao MC, et al. (1996) Pdd1p, a novel chromodomain-containing protein, links heterochromatin assembly and DNA elimination in Tetrahymena. Cell 87: 75-84. doi:10.1016/S0092-8674(00)81324-0. PubMed: 8858150.
29. 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: 4128-4134. doi:10.1128/MCB.20.11.4128-4134.2000. PubMed: 10805754.
30. Yao MC, Yao CH, Halasz LM, Fuller P, Rexer CH, et al. (2007) Identification of novel chromatin-associated proteins involved in programmed genome rearrangements in Tetrahymena. J Cell Sci 120: 1978-1989. doi:10.1242/jcs.006502. PubMed: 17519286.
31. Baudry C, Malinsky S, Restituito M, Kapusta A, Rosa S, et al. (2009) PiggyMac, a domesticated piggyBac transposase involved in programmed genome rearrangements in the ciliate Paramecium tetraurelia. Genes Dev 23: 2478-2483. doi:10.1101/gad.547309. PubMed: 19884254.
32. 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. doi:10.1091/mbc.E09-12-1079. PubMed: 20357003.
33. Lin IT, Chao JL, Yao MC, (2012) An essential role for the DNA breakage-repair protein Ku80 in programmed DNA rearrangements in Tetrahymena thermophila. Mol Biol Cell 23: 2213-2225. doi:10.1091/mbc.E11-11-0952. PubMed: 22513090.
34. Kapusta A, Matsuda A, Marmignon A, Ku M, Silve A, et al. (2011) Highly precise and developmentally programmed genome assembly in Paramecium requires ligase IV-dependent end joining. PLOS Genet 7: e1002049. PubMed: 21533177.
35. 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. doi:10.1128/EC.00157-07. PubMed: 17586719.
36. De Palmenaer D, Siguier P, Mahillon J, (2008) IS4 family goes genomic. BMC Evol Biol 8: 18. doi:10.1186/1471-2148-8-18. PubMed: 18215304.
37. Shang Y, Song X, Bowen J, Corstanje R, Gao Y, et al. (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 U S A 99: 3734-3739. doi:10.1073/pnas.052016199. PubMed: 11891286.
38. 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. doi:10.1016/S1097-2765(00)80396-2. PubMed: 10619033.
39. Austerberry CF, Yao MC, (1988) Sequence structures of two developmentally regulated, alternative DNA deletion junctions in Tetrahymena thermophila. Mol Cell Biol 8: 3947-3950. PubMed: 3221871.
40. 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. doi:10.1128/EC.00379-09. PubMed: 20495055.
41. Yao MC, Yao CH, (1994) Detection of circular excised DNA deletion elements in Tetrahymena thermophila during development. Nucleic Acids Res 22: 5702-5708. doi:10.1093/nar/22.25.5702. PubMed: 7838725.
42. Smothers JF, Mizzen CA, Tubbert MM, Cook RG, Allis CD, (1997) Pdd1p associates with germline-restricted chromatin and a second novel anlagen-enriched protein in developmentally programmed DNA elimination structures. Development 124: 4537-4545. PubMed: 9409671.
43. Smothers JF, Madireddi MT, Warner FD, Allis CD, (1997) Programmed DNA degradation and nucleolar biogenesis occur in distinct organelles during macronuclear development in Tetrahymena. J Euk Microbiol 44: 79-88. doi:10.1111/j.1550-7408.1997.tb05793.x. PubMed: 9109258.
44. Song X, Gjoneska E, Ren Q, Taverna SD, Allis CD, et al. (2007) Phosphorylation of the SQ H2A.X motif is required for proper meiosis and mitosis in Tetrahymena thermophila. Mol Cell Biol 27: 2648-2660. doi:10.1128/MCB.01910-06. PubMed: 17242195.
45. Chalker DL, (2008) Dynamic nuclear reorganization during genome remodeling of Tetrahymena. Biochim Biophys Acta, 1783: 2130-6. PubMed: 18706458.
46. Chiolo I, Minoda A, Colmenares SU, Polyzos A, Costes SV, et al. (2011) Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144: 732-744. doi:10.1016/j.cell.2011.02.012. PubMed: 21353298.
47. Jakob B, Splinter J, Conrad S, Voss KO, Zink D, et al. (2011) DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin. Nucleic Acids Res 39: 6489-6499. doi:10.1093/nar/gkr230. PubMed: 21511815.
48. Sinzelle L, Izsvák Z, Ivics Z, (2009) Molecular domestication of transposable elements: from detrimental parasites to useful host genes. Cell Mol Life Sci 66: 1073-1093. doi:10.1007/s00018-009-8376-3. PubMed: 19132291.
49. Nekrutenko A, Li WH, (2001) Transposable elements are found in a large number of human protein-coding genes. Trends Genet 17: 619-621. doi:10.1016/S0168-9525(01)02445-3. PubMed: 11672845.
50. Li WH, Gu Z, Wang H, Nekrutenko A, (2001) Evolutionary analyses of the human genome. Nature 409: 847-849. doi:10.1038/35057039. PubMed: 11237007.
51. Chalker DL, (2009) Transposons that clean up after themselves. Genome Biol 10: 224. doi:10.1186/gb-2009-10-6-224. PubMed: 19589181.
52. Nowacki M, Higgins BP, Maquilan GM, Swart EC, Doak TG, et al. (2009) A functional role for transposases in a large eukaryotic genome. Science 324: 935-938. doi:10.1126/science.1170023. PubMed: 19372392.
53. Orias E, Hamilton EP, Orias JD, (2000) Tetrahymena as a laboratory organism: useful strains, cell culture, and cell line maintenance. Methods Cell Biol 62: 189-211. PubMed: 10503191.
54. Motl JA, Chalker DL, (2011) Zygotic expression of the double-stranded RNA binding motif protein Drb2p is required for DNA elimination in the ciliate Tetrahymena thermophila. Eukaryot Cell 10: 1648-1659. doi:10.1128/EC.05216-11. PubMed: 22021239.
55. Fan Q, Sweeney R, Yao MC, (2000) Creation and use of antisense ribosomes in Tetrahymena thermophila. Methods Cell Biol 62: 533-547. PubMed: 10503216.
56. Cassidy-Hanley D, Bowen J, Lee JH, Cole E, VerPlank LA, et al. (1997) Germline and somatic transformation of mating Tetrahymena thermophila by particle bombardment. Genetics 146: 135-147. PubMed: 9136007.
57. Bruns PJ, Cassidy-Hanley D, (2000) Biolistic transformation of macro- and micronuclei. Methods Cell Biol 62: 501-512. PubMed: 10503214.
58. Allen SL, (1967) Cytogenetics of genomic exclusion in Tetrahymena. Genetics 55: 797-822. PubMed: 6036954.
59. 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. doi:10.1093/nar/22.24.5391. PubMed: 7816630.