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생화학분자생물학회 (Korean Society for Biochemistry and Molecular Biology)
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Epigenetic aspects of telomeric chromatin in Arabidopsis thaliana

  • 투고 : 2019.01.10
  • 발행 : 2019.03.31
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초록

Telomeres are nucleoprotein complexes at the physical ends of linear eukaryotic chromosomes. They protect the chromosome ends from various external attacks to avoid the loss of genetic information. Telomeres are maintained by cellular activities associated with telomerase and telomere-binding proteins. In addition, epigenetic regulators have pivotal roles in controlling the chromatin state at telomeres and subtelomeric regions, contributing to the maintenance of chromosomal homeostasis in yeast, animals, and plants. Here, we review the recent findings on chromatin modifications possibly associated with the dynamic states of telomeres in Arabidopsis thaliana.

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참고문헌

  1. O'Sullivan RJ and Karlseder J (2010) Telomeres: protecting chromosomes against genome instability. Nat Rev Mol Cell Biol 11, 171-181 https://doi.org/10.1038/nrm2848
  2. Blackburn EH (2010) Telomeres and telomerase: the means to the end (Nobel lecture). Angew Chem Int Ed Engl 49, 7405-7421 https://doi.org/10.1002/anie.201002387
  3. Louis EJ and Vershinin AV (2005) Chromosome ends: different sequences may provide conserved functions. Bioessays 27, 685-697 https://doi.org/10.1002/bies.20259
  4. Gallardo F and Chartrand P (2008) Telomerase biogenesis. RNA Biol 5, 212-215 https://doi.org/10.4161/rna.7115
  5. de Lange T (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19, 2100-2110 https://doi.org/10.1101/gad.1346005
  6. Webb CJ, Wu Y and Zakian VA (2013) DNA repair at telomeres: keeping the ends intact. Cold Spring Harb Perspect Biol 5, a012666 https://doi.org/10.1101/cshperspect.a012666
  7. Brock GJ, Charlton J and Bird A (1999) Densely methylated sequences that are preferentially localized at telomere-proximal regions of human chromosomes. Gene 240, 269-277 https://doi.org/10.1016/S0378-1119(99)00442-4
  8. Ottaviani A, Gilson E and Magdinier F (2008) Telomeric position effect: From the yeast paradigm to human pathologies? Biochimie 90, 93-107 https://doi.org/10.1016/j.biochi.2007.07.022
  9. Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E and Lingner J (2007) Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318, 798-801 https://doi.org/10.1126/science.1147182
  10. Balk B, Maicher A, Dees M et al (2013) Telomeric RNA-DNA hybrids affect telomere-length dynamics and senescence. Nat Struct Mol Biol 20, 1199-1205 https://doi.org/10.1038/nsmb.2662
  11. Zellinger B and Riha K (2007) Composition of plant telomeres. Biochim Biophys Acta 1769, 399-409 https://doi.org/10.1016/j.bbaexp.2007.02.001
  12. Kupiec M (2014) Biology of telomeres: lessons from budding yeast. FEMS Microbiol Rev 38, 144-171 https://doi.org/10.1111/1574-6976.12054
  13. Lamb JC, Yu W, Han F and Birchler JA (2007) Plant chromosomes from end to end: telomeres, heterochromatin and centromeres. Curr Opin Plant Biol 10, 116-122 https://doi.org/10.1016/j.pbi.2007.01.008
  14. Blasco MA (2007) The epigenetic regulation of mammalian telomeres. Nat Rev Genet 8, 299-309 https://doi.org/10.1038/nrg2047
  15. Galati A, Micheli E and Cacchione S (2013) Chromatin structure in telomere dynamics. Front Oncol 3, 46 https://doi.org/10.3389/fonc.2013.00046
  16. Jing H and Lin H (2015) Sirtuins in epigenetic regulation. Chem Rev 115, 2350-2375 https://doi.org/10.1021/cr500457h
  17. Tennen RI, Bua DJ, Wright WE and Chua KF (2011) SIRT6 is required for maintenance of telomere position effect in human cells. Nat Commun 2, 433 https://doi.org/10.1038/ncomms1443
  18. Michishita E, McCord RA, Berber E et al (2008) SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 452, 492-496 https://doi.org/10.1038/nature06736
  19. Baur JA, Zou Y, Shay JW and Wright WE (2001) Telomere position effect in human cells. Science 292, 2075-2077 https://doi.org/10.1126/science.1062329
  20. Koering CE, Pollice A, Zibella MP et al (2002) Human telomeric position effect is determined by chromosomal context and telomeric chromatin integrity. EMBO Rep 3, 1055-1061 https://doi.org/10.1093/embo-reports/kvf215
  21. Garcia-Cao M, O'Sullivan R, Peters AH, Jenuwein T and Blasco MA (2004) Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat Genet 36, 94-99 https://doi.org/10.1038/ng1278
  22. Benetti R, Gonzalo S, Jaco I et al (2007) Suv4-20h deficiency results in telomere elongation and derepression of telomere recombination. J Cell Biol 178, 925-936 https://doi.org/10.1083/jcb.200703081
  23. Gonzalo S, Jaco I, Fraga MF et al (2006) DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nat Cell Biol 8, 416-424 https://doi.org/10.1038/ncb1386
  24. Yehezkel S, Segev Y, Viegas-Pequignot E, Skorecki K and Selig S (2008) Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions. Hum Mol Genet 17, 2776-2789 https://doi.org/10.1093/hmg/ddn177
  25. Jenuwein T and Allis CD (2001) Translating the histone code. Science 293, 1074-1080 https://doi.org/10.1126/science.1063127
  26. Gong F and Miller KM (2013) Mammalian DNA repair: HATs and HDACs make their mark through histone acetylation. Mutat Res 750, 23-30 https://doi.org/10.1016/j.mrfmmm.2013.07.002
  27. Ma X, Lv S, Zhang C and Yang C (2013) Histone deacetylases and their functions in plants. Plant Cell Rep 32, 465-478 https://doi.org/10.1007/s00299-013-1393-6
  28. Bowen AJ, Gonzalez D, Mullins JG, Bhatt AM, Martinez A and Conlan RS (2010) PAH-Domain-Specific Interactions of the Arabidopsis Transcription Coregulator SIN3-LIKE1 (SNL1) with Telomere-Binding Protein 1 and ALWAYS EARLY2 Myb-DNA Binding Factors. J Mol Biol 395, 937-949 https://doi.org/10.1016/j.jmb.2009.11.065
  29. Lee WK and Cho MH (2016) Telomere-binding protein regulates the chromosome ends through the interaction with histone deacetylases in Arabidopsis thaliana. Nucleic Acids Res 44, 4610-4624 https://doi.org/10.1093/nar/gkw067
  30. Aufsatz W, Stoiber T, Rakic B and Naumann K (2007) Arabidopsis histone deacetylase 6: a green link to RNA silencing. Oncogene 26, 5477-5488 https://doi.org/10.1038/sj.onc.1210615
  31. Luo M, Cheng K, Xu Y, Yang S and Wu K (2017) Plant Responses to Abiotic Stress Regulated by Histone Deacetylases. Front Plant Sci 8, 2147 https://doi.org/10.3389/fpls.2017.02147
  32. Ehrentraut S, Weber JM, Dybowski JN, Hoffmann D and Ehrenhofer-Murray AE (2010) Rpd3-dependent boundary formation at telomeres by removal of Sir2 substrate. Proc Natl Acad Sci U S A 107, 5522-5527 https://doi.org/10.1073/pnas.0909169107
  33. Zhou J, Zhou BO, Lenzmeier BA and Zhou JQ (2009) Histone deacetylase Rpd3 antagonizes Sir2-dependent silent chromatin propagation. Nucleic Acids Res 37, 3699-3713 https://doi.org/10.1093/nar/gkp233
  34. Thurtle-Schmidt DM, Dodson AE and Rine J (2016) Histone Deacetylases with Antagonistic Roles in Saccharomyces cerevisiae Heterochromatin Formation. Genetics 204, 177-190 https://doi.org/10.1534/genetics.116.190835
  35. Suka N, Luo K and Grunstein M (2002) Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin. Nat Genet 32, 378-383 https://doi.org/10.1038/ng1017
  36. Kimura A, Umehara T and Horikoshi M (2002) Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nat Genet 32, 370-377 https://doi.org/10.1038/ng993
  37. Grafi G, Ben-Meir H, Avivi Y, Moshe M, Dahan Y and Zemach A (2007) Histone methylation controls telomerase-independent telomere lengthening in cells undergoing dedifferentiation. Dev Biol 306, 838-846 https://doi.org/10.1016/j.ydbio.2007.03.023
  38. Vaquero-Sedas MI, Gamez-Arjona FM and Vega-Palas MA (2011) Arabidopsis thaliana telomeres exhibit euchromatic features. Nucleic Acids Res 39, 2007-2017 https://doi.org/10.1093/nar/gkq1119
  39. Zhou Y, Wang Y, Krause K et al (2018) Telobox motifs recruit CLF/SWN-PRC2 for H3K27me3 deposition via TRB factors in Arabidopsis. Nat Genet 50, 638-644 https://doi.org/10.1038/s41588-018-0109-9
  40. Colot V and Rossignol JL (1999) Eukaryotic DNA methylation as an evolutionary device. Bioessays 21, 402-411 https://doi.org/10.1002/(SICI)1521-1878(199905)21:5<402::AID-BIES7>3.0.CO;2-B
  41. Chan SW, Henderson IR and Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6, 351-360 https://doi.org/10.1038/nrg1601
  42. Cedar H and Bergman Y (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 10, 295-304 https://doi.org/10.1038/nrg2540
  43. Lindroth AM, Shultis D, Jasencakova Z et al (2004) Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J 23, 4146-4155 https://doi.org/10.1038/sj.emboj.7600430
  44. Liu X, Yu CW, Duan J et al (2012) HDA6 Directly Interacts with DNA Methyltransferase MET1 and Maintains Transposable Element Silencing in Arabidopsis. Plant Physiol 158, 119-129 https://doi.org/10.1104/pp.111.184275
  45. To TK, Kim JM, Matsui A et al (2011) Arabidopsis HDA6 Regulates Locus-Directed Heterochromatin Silencing in Cooperation with MET1. PLoS Genet 7, e1002055 https://doi.org/10.1371/journal.pgen.1002055
  46. Vrbsky J, Akimcheva S and Watson JM (2010) siRNA-Mediated Methylation of Arabidopsis Telomeres. PLoS Genet 6, e1000986 https://doi.org/10.1371/journal.pgen.1000986
  47. Mathieu O, Probst AV and Paszkowski J (2005) Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis. EMBO J 24, 2783-2791 https://doi.org/10.1038/sj.emboj.7600743
  48. Jacob Y, Feng S, LeBlanc CA et al (2009) ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing. Nat Struct Mol Biol 16, 763-768 https://doi.org/10.1038/nsmb.1611
  49. Jacob Y, Stroud H, Leblanc C et al (2010) Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases. Nature 466, 987-991 https://doi.org/10.1038/nature09290
  50. Raynaud C, Sozzani R, Glab N et al (2006) Two cell-cycle regulated SET-domain proteins interact with proliferating cell nuclear antigen (PCNA) in Arabidopsis. Plant J 47, 395-407 https://doi.org/10.1111/j.1365-313X.2006.02799.x
  51. Brzeski J and Jerzmanowski A (2003) Deficient in DNA methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors. J Biol Chem 278, 823-828 https://doi.org/10.1074/jbc.M209260200
  52. Zemach A, Kim MY, Hsieh PH et al (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153, 193-205 https://doi.org/10.1016/j.cell.2013.02.033
  53. Xie X and Shippen DE (2018) DDM1 guards against telomere truncation in Arabidopsis. Plant Cell Rep 37, 501-513 https://doi.org/10.1007/s00299-017-2245-6
  54. Richards EJ and Elgin SC (2002) Epigenetic codes for heterochromatin formation and silencing: Rounding up the usual suspects. Cell 108, 489-500 https://doi.org/10.1016/S0092-8674(02)00644-X
  55. Fuchs J, Demidov D, Houben A and Schubert I (2006) Chromosomal histone modification patterns - from conservation to diversity. Trends Plant Sci 11, 199-208 https://doi.org/10.1016/j.tplants.2006.02.008
  56. Benetti R, Schoeftner S, Munoz P and Blasco MA (2008) Role of TRF2 in the assembly of telomeric chromatin. Cell Cycle 7, 3461-3468 https://doi.org/10.4161/cc.7.21.7013
  57. Benetti R, Garcia-Cao M and Blasco MA (2007) Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat Genet 39, 243-250 https://doi.org/10.1038/ng1952
  58. Cubiles MD, Barroso S, Vaquero-Sedas MI, Enguix A, Aguilera A and Vega-Palas MA (2018) Epigenetic features of human telomeres. Nucleic Acids Res 46, 2347-2355 https://doi.org/10.1093/nar/gky006
  59. Conomos D, Stutz MD, Hills M et al (2012) Variant repeats are interspersed throughout the telomeres and recruit nuclear receptors in ALT cells. J Cell Biol 199, 893-906 https://doi.org/10.1083/jcb.201207189
  60. O'Sullivan RJ and Almouzni G (2014) Assembly of telomeric chromatin to create ALTernative endings. Trends Cell Biol 24, 675-685 https://doi.org/10.1016/j.tcb.2014.07.007
  61. Vaquero-Sedas MI, Luo C and Vega-Palas MA (2012) Analysis of the epigenetic status of telomeres by using ChIP-seq data. Nucleic Acids Res 40, e163 https://doi.org/10.1093/nar/gks730
  62. Vaquero-Sedas MI and Vega-Palas MA (2013) Differential association of Arabidopsis telomeres and centromeres with histone H3 variants. Sci Rep 3, 1202 https://doi.org/10.1038/srep01202
  63. Vega-Vaquero A, Bonora G, Morselli M et al (2016) Novel features of telomere biology revealed by the absence of telomeric DNA methylation. Genome Res 26, 1047-1056 https://doi.org/10.1101/gr.202465.115
  64. Galati A, Magdinier F, Colasanti V et al (2012) TRF2 controls telomeric nucleosome organization in a cell cycle phase-dependent manner. PLoS One 7, e34386 https://doi.org/10.1371/journal.pone.0034386
  65. Deng Z, Norseen J, Wiedmer A, Riethman H and Lieberman PM (2009) TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol Cell 35, 403-413 https://doi.org/10.1016/j.molcel.2009.06.025
  66. Lee WK, Yun JH, Lee W and Cho MH (2012) DNA-Binding Domain of AtTRB2 Reveals Unique Features of a Single Myb Histone Protein Family that Binds to Both Arabidopsis- and Human-Type Telomeric DNA Sequences. Mol Plant 5, 1406-1408 https://doi.org/10.1093/mp/sss063