DNA deletion as a mechanism for developmentally programmed centromere loss

Nucleic Acids Research

Volumn 44, Issue 4, 2015, Pages 1553-1565

  Lhuillier Akakpo, Maoussi ^a,b   Guérin, Frédéric ^a   Frapporti, Andrea ^a   Duharcourt, Sandra ^a  

^a INSTITUT JACQUES MONOD   (France)

^b INSTITUT DE RADIOBIOLOGIE CELLULAIRE ET MOLÉCULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOUBLE STRANDED DNA; GREEN FLUORESCENT PROTEIN; HISTONE H3; HISTONE LYSINE METHYLTRANSFERASE; LYSINE; TRANSPOSASE; AUTOANTIGEN; CENTROMERE PROTEIN A; CHROMATIN; HISTONE; NONHISTONE PROTEIN;

ARTICLE; CELL DIVISION; CELL NUCLEUS; CENTROMERE; CONTROLLED STUDY; DNA SEQUENCE; DNA SYNTHESIS; GENE DELETION; HISTONE METHYLATION; NONHUMAN; PARAMECIUM TETRAURELIA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; CHROMATIN; DOUBLE STRANDED DNA BREAK; GENETICS; PARAMECIUM;

AUTOANTIGENS; CELL DIVISION; CELL NUCLEUS; CENTROMERE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA; DNA BREAKS, DOUBLE-STRANDED; HISTONES; PARAMECIUM; SEQUENCE DELETION; TRANSPOSASES;

EID: 84960478691     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1110     Document Type: Article

References (57)

1. Fukagawa, T. and Earnshaw, W.C. (2014) The centromere: chromatin foundation for the kinetochore machinery. Dev. Cell, 30, 496-508.
2. McClintock, B. (1939) The Behavior in Successive Nuclear Divisions of a Chromosome Broken at Meiosis. Proc. Natl. Acad. Sci. U.S.A., 25, 405-416.
3. McClintock, B. (1941) The Stability of Broken Ends of Chromosomes in Zea Mays. Genetics, 26, 234-282.
4. Stimpson, K.M., Matheny, J.E. and Sullivan, B.A. (2012) Dicentric chromosomes: unique models to study centromere function and inactivation. Chromosome Res., 20, 595-605.
5. Earnshaw, W.C. and Migeon, B.R. (1985) Three related centromere proteins are absent from the inactive centromere of a stable isodicentric chromosome. Chromosoma, 92, 290-296.
6. Sullivan, B.A. and Schwartz, S. (1995) Identification of centromeric antigens in dicentric Robertsonian translocations: CENP-C and CENP-E are necessary components of functional centromeres. Hum. Mol. Genet., 4, 2189-2197.
7. Han, F., Lamb, J.C. and Birchler, J.A. (2006) High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize. Proc. Natl. Acad. Sci. U.S.A., 103, 3238-3243.
8. Hill, A. and Bloom, K. (1989) Acquisition and processing of a conditional dicentric chromosome in Saccharomyces cerevisiae. Mol. Cell. Biol., 9, 1368-1370.
9. Jäger, D. and Philippsen, P. (1989) Stabilization of dicentric chromosomes in Saccharomyces cerevisiae by telomere addition to broken ends or by centromere deletion. EMBO J., 8, 247-254.
10. Sato, H., Masuda, F., Takayama, Y., Takahashi, K. and Saitoh, S. (2012) Epigenetic inactivation and subsequent heterochromatinization of a centromere stabilize dicentric chromosomes. Curr. Biol., 22, 658-667.
11. Stimpson, K.M., Song, I.Y., Jauch, A., Holtgreve-Grez, H., Hayden, K.E., Bridger, J.M. and Sullivan, B.A. (2010) Telomere disruption results in non-random formation of de novo dicentric chromosomes involving acrocentric human chromosomes. PLoS Genet., 6, e1001061.
12. Stevenson, I. and Lloyd, F.P. (1971) Ultrastructure of nuclear division in Paramecium aurelia. I. Mitosis in the micronucleus. Aust. J. Biol. Sci., 24, 963-975.
13. Stevenson, I. and Lloyd, F.P. (1971) Ultrastructure of nuclear division in Paramecium aurelia. II. Amitosis of the macronucleus. Aust. J. Biol. Sci., 24, 977-987.
14. Tucker, J.B., Beisson, J., Roche, D.L. and Cohen, J. (1980) Microtubules and control of macronuclear 'amitosis' in Paramecium. J. Cell. Sci., 44, 135-151.
15. Betermier, M. and Duharcourt, S. (2014) Programmed Rearrangement in Ciliates: Paramecium. Microbiol. Spectr., 2, doi:10.1128/microbiolspec.MDNA3-0035-2014.
16. Aury, J.M., Jaillon, O., Duret, L., Noel, B., Jubin, C., Porcel, B.M., Segurens, B., Daubin, V., Anthouard, V., Aiach, N. et al. (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature, 444, 171-178.
17. Arnaiz, O., Mathy, N., Baudry, C., Malinsky, S., Aury, J.-M., Wilkes, C.D., Garnier, O., Labadie, K., Lauderdale, B.E., Le Moüel, A. et al. (2012) The Paramecium germline genome provides a niche for intragenic parasitic DNA: evolutionary dynamics of internal eliminated sequences. PLoS Genet., 8, e1002984.
18. Baudry, C., Malinsky, S., Restituito, M., Kapusta, A., Rosa, S., Meyer, E. and Betermier, M. (2009) PiggyMac, a domesticated piggyBac transposase involved in programmed genome rearrangements in the ciliate Paramecium tetraurelia. Genes Dev., 23, 2478-2483.
19. Lhuillier-Akakpo, M., Frapporti, A., Denby Wilkes, C., Matelot, M., Vervoort, M., Sperling, L. and Duharcourt, S. (2014) Local effect of enhancer of zeste-like reveals cooperation of epigenetic and cis-acting determinants for zygotic genome rearrangements. PLoS Genet., 10, e1004665.
20. Lepere, G., Nowacki, M., Serrano, V., Gout, J.F., Guglielmi, G., Duharcourt, S. and Meyer, E. (2009) Silencing-associated and meiosis-specific small RNA pathways in Paramecium tetraurelia. Nucleic Acids Res., 37, 903-915.
21. Sandoval, P.Y., Swart, E.C., Arambasic, M. and Nowacki, M. (2014) Functional diversification of dicer-like proteins and small RNAs required for genome sculpting. Dev. Cell, 28, 174-188.
22. Beisson, J., Betermier, M., Bre, M.H., Cohen, J., Duharcourt, S., Duret, L., Kung, C., Malinsky, S., Meyer, E., Preer, J.R. et al. (2010) Maintaining clonal Paramecium tetraurelia cell lines of controlled age through daily reisolation. Cold Spring Harb. Protoc., 2010, pdb.prot5361.
23. Beisson, J., Betermier, M., Bre, M.H., Cohen, J., Duharcourt, S., Duret, L., Kung, C., Malinsky, S., Meyer, E., Preer, J.R. et al. (2010) Mass culture of Paramecium tetraurelia. Cold Spring Harb Protoc, 2010, pdb prot5362.
24. Galvani, A. and Sperling, L. (2002) RNA interference by feeding in Paramecium. Trends Genet., 18, 11-12.
25. Arnaiz, O. and Sperling, L. (2011) ParameciumDB in 2011: new tools and new data for functional and comparative genomics of the model ciliate Paramecium tetraurelia. Nucleic Acids Res., 39, D632-D636.
26. Arnaiz, O., Mathy, N., Baudry, C., Malinsky, S., Aury, J.-M., Wilkes, C.D., Garnier, O., Labadie, K., Lauderdale, B.E., Le Moüel, A. et al. (2012) The Paramecium germline genome provides a niche for intragenic parasitic DNA: evolutionary dynamics of internal eliminated sequences. PLoS Genet.8, e1002984.
27. Malik, H.S. and Henikoff, S. (2003) Phylogenomics of the nucleosome. Nat. Struct. Biol., 10, 882-891.
28. Hake, S.B., Garcia, B.A., Duncan, E.M., Kauer, M., Dellaire, G., Shabanowitz, J., Bazett-Jones, D.P., Allis, C.D. and Hunt, D.F. (2006) Expression patterns and post-translational modifications associated with mammalian histone H3 variants. J. Biol. Chem., 281, 559-568.
29. Bernhard, D. (1999) Several highly divergent histone H3 genes are present in the hypotrichous ciliate Stylonychia lemnae. FEMS Microbiol. Lett., 175, 45-50.
30. Katz, L.A., Bornstein, J.G., Lasek-Nesselquist, E. and Muse, S.V. (2004) Dramatic diversity of ciliate histone H4 genes revealed by comparisons of patterns of substitutions and paralog divergences among eukaryotes. Mol. Biol. Evol., 21, 555-562.
31. Postberg, J., Forcob, S., Chang, W.-J. and Lipps, H.J. (2010) The evolutionary history of histone H3 suggests a deep eukaryotic root of chromatin modifying mechanisms. BMC Evol. Biol., 10, 259.
32. Thatcher, T.H. and Gorovsky, M.A. (1994) Phylogenetic analysis of the core histones H2A, H2B, H3, and H4. Nucleic Acids Res., 22, 174-179.
33. Funabiki, H., Hagan, I., Uzawa, S. and Yanagida, M. (1993) Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J. Cell Biol., 121, 961-976.
34. Padeken, J., Mendiburo, M.J., Chlamydas, S., Schwarz, H.-J., Kremmer, E. and Heun, P. (2013) The nucleoplasmin homolog NLP mediates centromere clustering and anchoring to the nucleolus. Mol. Cell, 50, 236-249.
35. Jones, W. (1956) Nuclear differentiation in Paramecium. Ph.D. Thesis. Wales, Aberystwyth.
36. Sonneborn, T.M. (1947) Recent advances in the genetics of Paramecium and Euplotes. Adv. Genet., 1, 263-358.
37. Buchwitz, B.J., Ahmad, K., Moore, L.L., Roth, M.B. and Henikoff, S. (1999) A histone-H3-like protein in C. elegans. Nature, 401, 547-548.
38. Blower, M.D. and Karpen, G.H. (2001) The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat. Cell. Biol., 3, 730-739.
39. Stoler, S., Keith, K.C., Curnick, K.E. and Fitzgerald-Hayes, M. (1995) A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis. Genes Dev., 9, 573-586.
40. Takahashi, K., Chen, E.S. and Yanagida, M. (2000) Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science, 288, 2215-2219.
41. Betermier, M., Duharcourt, S., Seitz, H. and Meyer, E. (2000) Timing of developmentally programmed excision and circularization of Paramecium internal eliminated sequences. Mol. Cell. Biol., 20, 1553-1561.
42. Preer, L.B., Hamilton, G. and Preer, J.R. (1992) Micronuclear DNA from Paramecium tetraurelia: serotype 51 A gene has internally eliminated sequences. J. Protozool., 39, 678-682.
43. Garnier, O., Serrano, V., Duharcourt, S. and Meyer, E. (2004) RNA-mediated programming of developmental genome rearrangements in Paramecium tetraurelia. Mol. Cell. Biol., 24, 7370-7379.
44. Ingouff, M., Hamamura, Y., Gourgues, M., Higashiyama, T. and Berger, F. (2007) Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr. Biol., 17, 1032-1037.
45. Maehara, K., Takahashi, K. and Saitoh, S. (2010) CENP-A reduction induces a p53-dependent cellular senescence response to protect cells from executing defective mitoses. Mol. Cell. Biol., 30, 2090-2104.
46. Steiner, F.A. and Henikoff, S. (2014) Holocentromeres are dispersed point centromeres localized at transcription factor hotspots. eLife, 3, e02025.
47. Talbert, P.B., Masuelli, R., Tyagi, A.P., Comai, L. and Henikoff, S. (2002) Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell, 14, 1053-1066.
48. Blower, M.D., Sullivan, B.A. and Karpen, G.H. (2002) Conserved organization of centromeric chromatin in flies and humans. Dev. Cell, 2, 319-330.
49. Coyne, R.S., Lhuillier-Akakpo, M. and Duharcourt, S. (2012) RNA-guided DNA rearrangements in ciliates: Is the best genome defence a good offence? Biol. Cell, 104, 1-17.
50. Mérai, Z., Chumak, N., García-Aguilar, M., Hsieh, T.-F., Nishimura, T., Schoft, V.K., Bindics, J., Slusarz, L., Arnoux, S., Opravil, S. et al. (2014) The AAA-ATPase molecular chaperone Cdc48/p97 disassembles sumoylated centromeres, decondenses heterochromatin, and activates ribosomal RNA genes. Proc. Natl. Acad. Sci. U.S.A., 111, 16166-16171.
51. Cui, B. and 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.
52. Cervantes, M.D., Xi, X., Vermaak, D., Yao, M.C. and 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.
53. Drinnenberg, I.A., deYoung, D., Henikoff, S. and Malik, H.S. (2014) Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. eLife, 3, e03676.
54. Akiyoshi, B. and Gull, K. (2014) Discovery of unconventional kinetochores in kinetoplastids. Cell, 156, 1247-1258.
55. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol., 215, 403-410.
56. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797.
57. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J.-F., Guindon, S., Lefort, V., Lescot, M. et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res., 36, W465-W469.