Holocentromeres are dispersed point centromeres localized at transcription factor hotspots

eLife

Volumn 2014, Issue 3, 2014, Pages

  Steiner, Florian A ^a   Henikoff, Steven ^a  

^a USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; CENTROMERE ANTIBODY; MICROCOCCAL NUCLEASE; NUCLEOSOME ANTIBODY; RNA POLYMERASE II; NUCLEOSOME; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CENTROMERE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CROSS LINKING; EMBRYO DEVELOPMENT; EPIGENETICS; GENE MAPPING; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; HOLOCENTROMERE; IMMUNOFLUORESCENCE MICROSCOPY; KINETOCHORE MICROTUBULE; NONHUMAN; NUCLEOSOME; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; SACCHAROMYCES CEREVISIAE; X CHROMOSOME; ANIMAL; CAENORHABDITIS ELEGANS; CELL CYCLE; CYTOLOGY; GENETICS; METABOLISM;

ANIMALS; CAENORHABDITIS ELEGANS; CELL CYCLE; CENTROMERE; NUCLEOSOMES; TRANSCRIPTION FACTORS;

EID: 84898464557     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.02025     Document Type: Article

References (66)

1. Ahmad K, Henikoff S. 2002. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Molecular Cell 9:1191-1200. doi: 10.1016/S1097-2765(02)00542-7.
2. Albertson DG, Thomson JN. 1982. The kinetochores of Caenorhabditis elegans. Chromosoma 86:409-428. doi: 10.1007/BF00292267.
3. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Research 37:W202-W208. doi: 10.1093/nar/gkp335.
4. Buchwitz BJ, Ahmad K, Moore LL, Roth MB, Henikoff S. 1999. A histone-H3-like protein in C. elegans. Nature 401:547-548. doi: 10.1038/44062.
5. Conde e Silva N, Black BE, Sivolob A, Filipski J, Cleveland DW, Prunell A. 2007. CENP-A-containing nucleosomes: easier disassembly versus exclusive centromeric localization. Journal of Molecular Biology 370:555-573.
6. Camahort R, Shivaraju M, Mattingly M, Li B, Nakanishi S, Zhu D, Shilatifard A, Workman JL, Gerton JL. 2009. Cse4 is part of an octameric nucleosome in budding yeast. Molecular Cell 35:794-805. doi: 10.1016/j.molcel.2009.07.022.
7. Carroll CW, Milks KJ, Straight AF. 2010. Dual recognition of CENP-A nucleosomes is required for centromere assembly. The Journal of Cell Biology 189:1143-1155. doi: 10.1083/jcb.201001013.
8. Cheeseman IM, Niessen S, Anderson S, Hyndman F, Yates JR III, Oegema K, Desai A. 2004. A conserved protein network controls assembly of the outer kinetochore and its ability to sustain tension. Genes & Development 18:2255-2268. doi: 10.1101/gad.1234104.
9. Chen RA, Down TA, Stempor P, Chen QB, Egelhofer TA, Hillier LW, Jeffers TE, Ahringer J. 2013. The landscape of RNA polymerase II transcription initiation in C. elegans reveals promoter and enhancer architectures. Genome Research 23:1339-1347. doi: 10.1101/gr.153668.112.
10. Clarke L, Carbon J. 1980. Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature 287:504-509. doi: 10.1038/287504a0.
11. Dalal Y, Wang H, Lindsay S, Henikoff S. 2007. Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLOS Biology 5:e218. doi: 10.1371/journal.pbio.0050218.
12. Deal RB, Henikoff JG, Henikoff S. 2010. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328:1161-1164. doi: 10.1126/science.1186777.
13. Densmore L, Payne WE, Fitzgerald-Hayes M. 1991. In vivo genomic footprint of a yeast centromere. Molecular and Cellular Biology 11:154-165.
14. Folco HD, Pidoux AL, Urano T, Allshire RC. 2008. Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science 319:94-97. doi: 10.1126/science.1150944.
15. Furuyama S, Biggins S. 2007. Centromere identity is specified by a single centromeric nucleosome in budding yeast. Proceedings of the National Academy of Sciences of the United States of America 104:14706-14711. doi: 10.1073/pnas.0706985104.
16. Gascoigne KE, Takeuchi K, Suzuki A, Hori T, Fukagawa T, Cheeseman IM. 2011. Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell 145:410-422. doi: 10.1016/j. cell.2011.03.031.
17. Gassmann R, Rechtsteiner A, Yuen KW, Muroyama A, Egelhofer T, Gaydos L, Barron F, Maddox P, Essex A, Monen J, Ercan S, Lieb JD, Oegema K, Strome S, Desai A. 2012. An inverse relationship to germline transcription defines centromeric chromatin in C. elegans. Nature 484:534-537. doi: 10.1038/nature10973.
18. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, Liu T, Yip KY, Robilotto R, Rechtsteiner A, Ikegami K, Alves P, Chateigner A, Perry M, Morris M, Auerbach RK, Feng X, Leng J, Vielle A, Niu W, Rhrissorrakrai K, Agarwal A, Alexander RP, Barber G, Brdlik CM, Brennan J, Brouillet JJ, Carr A, Cheung MS, Clawson H, Contrino S, Dannenberg LO, Dernburg AF, Desai A, Dick L, Dosé AC, Du J, Egelhofer T, Ercan S, Euskirchen G, Ewing B, Feingold EA, Gassmann R, Good PJ, Green P, Gullier F, Gutwein M, Guyer MS, Habegger L, Han T, Henikoff JG, Henz SR, Hinrichs A, Holster H, Hyman T, Iniguez AL, Janette J, Jensen M, Kato M, Kent WJ, Kephart E, Khivansara V, Khurana E, Kim JK, Kolasinska-Zwierz P, Lai EC, Latorre I, Leahey A, Lewis S, Lloyd P, Lochovsky L, Lowdon RF, Lubling Y, Lyne R, MacCoss M, Mackowiak SD, Mangone M, McKay S, Mecenas D, Merrihew G, Miller DM 3rd, Muroyama A, Murray JI, Ooi SL, Pham H, Phippen T, Preston EA, Rajewsky N, Rätsch G, Rosenbaum H, Rozowsky J, Rutherford K, Ruzanov P, Sarov M, Sasidharan R, Sboner A, Scheid P, Segal E, Shin H, Shou C, Slack FJ, Slightam C, Smith R, Spencer WC, Stinson EO, Taing S, Takasaki T, Vafeados D, Voronina K, Wang G, Washington NL, Whittle CM, Wu B, Yan KK, Zeller G, Zha Z, Zhong M, Zhou X, modENCODE Consortium, Ahringer J, Strome S, Gunsalus KC, Micklem G, Liu XS, Reinke V, Kim SK, Hillier LW, Henikoff S, Piano F, Snyder M, Stein L, Lieb JD, Waterston RH. 2010. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330:1775-1787. doi: 10.1126/science.1196914.
19. Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S, Dewell S, Law M, Guo X, Li X, Wen D, Chapgier A, DeKelver RC, Miller JC, Lee YL, Boydston EA, Holmes MC, Gregory PD, Greally JM, Rafii S, Yang C, Scambler PJ, Garrick D, Gibbons RJ, Higgs DR, Cristea IM, Urnov FD, Zheng D, Allis CD. 2010. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140:678-691. doi: 10.1016/j. cell.2010.01.003.
20. Gu SG, Fire A. 2010. Partitioning the C. elegans genome by nucleosome modification, occupancy, and positioning. Chromosoma 119:73-87. doi: 10.1007/s00412-009-0235-3.
21. Hasson D, Panchenko T, Salimian KJ, Salman MU, Sekulic N, Alonso A, Warburton PE, Black BE. 2013. The octamer is the major form of CENP-A nucleosomes at human centromeres. Nature Structural & Molecular Biology 20:687-695. doi: 10.1038/nsmb.2562.
22. Henikoff JG, Belsky JA, Krassovsky K, MacAlpine DM, Henikoff S. 2011. Epigenome characterization at single base-pair resolution. Proceedings of the National Academy of Sciences of the United States of America 108:18318-18323. doi: 10.1073/pnas.1110731108.
23. Henikoff S, Furuyama T. 2012. The unconventional structure of centromeric nucleosomes. Chromosoma 121:341-352. doi: 10.1007/s00412-012-0372-y.
24. Henikoff S, Henikoff JG. 2012. Point" centromeres of Saccharomyces harbor single centromere-specific nucleosomes. Genetics 190:1575-1577. doi: 10.1534/genetics.111.137711.
25. Hori T, Shang WH, Takeuchi K, Fukagawa T. 2013. The CCAN recruits CENP-A to the centromere and forms the structural core for kinetochore assembly. The Journal of Cell Biology 200:45-60. doi: 10.1083/jcb.201210106.
26. Jin C, Felsenfeld G. 2007. Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Development 21:1519-1529. doi: 10.1101/gad.1547707.
27. Jullien J, Astrand C, Szenker E, Garrett N, Almouzni G, Gurdon JB. 2012. HIRA dependent H3.3 deposition is required for transcriptional reprogramming following nuclear transfer to Xenopus oocytes. Epigenetics & Chromatin 5:17. doi: 10.1186/1756-8935-5-17.
28. Kagansky A, Folco HD, Almeida R, Pidoux AL, Boukaba A, Simmer F, Urano T, Hamilton GL, Allshire RC. 2009. Synthetic heterochromatin bypasses RNAi and centromeric repeats to establish functional centromeres. Science 324:1716-1719. doi: 10.1126/science.1172026.
29. Kato H, Jiang J, Zhou BR, Rozendaal M, Feng H, Ghirlando R, Xiao TS, Straight AF, Bai Y. 2013. A conserved mechanism for centromeric nucleosome recognition by centromere protein CENP-C. Science 340:1110-1113. doi: 10.1126/science.1235532.
30. Kent NA, Adams S, Moorhouse A, Paszkiewicz K. 2011. Chromatin particle spectrum analysis: a method for comparative chromatin structure analysis using paired-end mode next-generation DNA sequencing. Nucleic Acids Research 39:e26. doi: 10.1093/nar/gkq1183.
31. Krassovsky K, Henikoff JG, Henikoff S. 2012. Tripartite organization of centromeric chromatin in budding yeast. Proceedings of the National Academy of Sciences of the United States of America 109:243-248. doi: 10.1073/ pnas.1118898109.
32. Krause M. 1995. MyoD and myogenesis in C. elegans. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 17:219-228. doi: 10.1002/bies.950170308.
33. Kvon EZ, Stampfel G, Yanez-Cuna JO, Dickson BJ, Stark A. 2012. HOT regions function as patterned developmental enhancers and have a distinct cis-regulatory signature. Genes & Development 26:908-913. doi: 10.1101/ gad.188052.112.
34. Lacoste N, Woolfe A, Tachiwana H, Garea AV, Barth T, Cantaloube S, Kurumizaka H, Imhof A, Almouzni G. 2014. Mislocalization of the centromeric histone variant CenH3/CENP-a in human cells depends on the Chaperone DAXX. Molecular Cell 53:631-644. doi: 10.1016/j.molcel.2014.01.018.
35. Lefrancois P, Auerbach RK, Yellman CM, Roeder GS, Snyder M. 2013. Centromere-like regions in the budding yeast genome. PLOS Genetics 9:e1003209.
36. Lefrancois P, Euskirchen GM, Auerbach RK, Rozowsky J, Gibson T, Yellman CM, Gerstein M, Snyder M. 2009. Efficient yeast ChIP-Seq using multiplex short-read DNA sequencing. BMC Genomics 10:37.
37. Liu T, Rechtsteiner A, Egelhofer TA, Vielle A, Latorre I, Cheung MS, Ercan S, Ikegami K, Jensen M, Kolasinska- Zwierz P, Rosenbaum H, Shin H, Taing S, Takasaki T, Iniguez AL, Desai A, Dernburg AF, Kimura H, Lieb JD, Ahringer J, Strome S, Liu XS. 2011. Broad chromosomal domains of histone modification patterns in C. elegans. Genome Research 21:227-236. doi: 10.1101/gr.115519.110.
38. Lopes da Rosa J, Holik J, Green EM, Rando OJ, Kaufman PD. 2011. Overlapping regulation of CenH3 localization and histone H3 turnover by CAF-1 and HIR proteins in Saccharomyces cerevisiae. Genetics 187:9-19. doi: 10.1534/ genetics.110.123117.
39. Maddox PS, Hyndman F, Monen J, Oegema K, Desai A. 2007. Functional genomics identifies a Myb domain-containing protein family required for assembly of CENP-A chromatin. The Journal of Cell Biology 176:757-763. doi: 10.1083/jcb.200701065.
40. Malik HS, Henikoff S. 2009. Major evolutionary transitions in centromere complexity. Cell 138:1067-1082. doi: 10.1016/j.cell.2009.08.036.
41. Marshall OJ, Chueh AC, Wong LH, Choo KH. 2008. Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. American Journal of Human Genetics 82:261-282. doi: 10.1016/j. ajhg.2007.11.009.
42. Mello CC, Kramer JM, Stinchcomb D, Ambros V. 1991. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. The EMBO Journal 10:3959-3970.
43. Melters DP, Paliulis LV, Korf IF, Chan SW. 2012. Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Research: an International Journal on the Molecular, Supramolecular and Evolutionary Aspects of Chromosome Biology 20:579-593. doi: 10.1007/ s10577-012-9292-1.
44. Mito Y, Henikoff JG, Henikoff S. 2005. Genome-scale profiling of histone H3.3 replacement patterns. Nature Genetics 37:1090-1097. doi: 10.1038/ng1637.
45. Moore LL, Roth MB. 2001. HCP-4, a CENP-C-like protein in Caenorhabditis elegans, is required for resolution of sister centromeres. The Journal of Cell Biology 153:1199-1208. doi: 10.1083/jcb.153.6.1199.
46. Moorman C, Sun LV, Wang J, de Wit E, Talhout W, Ward LD, Greil F, Lu XJ, White KP, Bussemaker HJ, van Steensel B. 2006. Hotspots of transcription factor colocalization in the genome of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America 103:12027-12032. doi: 10.1073/pnas.0605003103.
47. Niu W, Lu ZJ, Zhong M, Sarov M, Murray JI, Brdlik CM, Janette J, Chen C, Alves P, Preston E, Slightham C, Jiang L, Hyman AA, Kim SK, Waterston RH, Gerstein M, Snyder M, Reinke V. 2011. Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans. Genome Research 21:245-254. doi: 10.1101/ gr.114587.110.
48. Oegema K, Desai A, Rybina S, Kirkham M, Hyman AA. 2001. Functional analysis of kinetochore assembly in Caenorhabditis elegans. The Journal of Cell Biology 153:1209-1226. doi: 10.1083/jcb.153.6.1209.
49. Ooi SL, Henikoff JG, Henikoff S. 2010. A native chromatin purification system for epigenomic profiling in Caenorhabditis elegans. Nucleic Acids Research 38:e26. doi: 10.1093/nar/gkp1090.
50. Ooi SL, Priess JR, Henikoff S. 2006. Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans. PLOS Genetics 2:e97. doi: 10.1371/journal.pgen.0020097.
51. O'Toole ET, McDonald KL, Mantler J, McIntosh JR, Hyman AA, Muller-Reichert T. 2003. Morphologically distinct microtubule ends in the mitotic centrosome of Caenorhabditis elegans. The Journal of Cell Biology 163:451-456. doi: 10.1083/jcb.200304035.
52. Polizzi C, Clarke L. 1991. The chromatin structure of centromeres from fission yeast: differentiation of the central core that correlates with function. The Journal of Cell Biology 112:191-201. doi: 10.1083/jcb.112.2.191.
53. Przewloka MR, Venkei Z, Bolanos-Garcia VM, Debski J, Dadlez M, Glover DM. 2011. CENP-C is a structural platform for kinetochore assembly. Current Biology: CB 21:399-405. doi: 10.1016/j.cub.2011.02.005.
54. Reece-Hoyes JS, Deplancke B, Shingles J, Grove CA, Hope IA, Walhout AJ. 2005. A compendium of Caenorhabditis elegans regulatory transcription factors: a resource for mapping transcription regulatory networks. Genome Biology 6:R110. doi: 10.1186/gb-2005-6-13-r110.
55. Schrader F. 1935. Notes on the mitotic behavior of long chromosomes. Cytologia 6:422-430. doi: 10.1508/ cytologia.6.422.
56. Schrader F. 1947. The role of the kinetochore in the chromosomal evolution of the heteroptera and homoptera. Evolution 1:134-142. doi: 10.2307/2405489.
57. Shang WH, Hori T, Martins NM, Toyoda A, Misu S, Monma N, Hiratani I, Maeshima K, Ikeo K, Fujiyama A, Kimura H, Earnshaw WC, Fukagawa T. 2013. Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Developmental Cell 24:635-648. doi: 10.1016/j.devcel.2013.02.009.
58. Sheth U, Pitt J, Dennis S, Priess JR. 2010. Perinuclear P granules are the principal sites of mRNA export in adult C. elegans germ cells. Development 137:1305-1314. doi: 10.1242/dev.044255.
59. Steiner FA, Talbert PB, Kasinathan S, Deal RB, Henikoff S. 2012. Cell-type-specific nuclei purification from whole animals for genome-wide expression and chromatin profiling. Genome Research 22:766-777. doi: 10.1101/ gr.131748.111.
60. Stinchcomb DT, Shaw JE, Carr SH, Hirsh D. 1985. Extrachromosomal DNA transformation of Caenorhabditis elegans. Molecular and Cellular Biology 5:3484-3496.
61. Takahashi K, Murakami S, Chikashige Y, Funabiki H, Niwa O, Yanagida M. 1992. A low copy number central sequence with strict symmetry and unusual chromatin structure in fission yeast centromere. Molecular Biology of the Cell 3:819-835. doi: 10.1091/mbc.3.7.819.
62. Teves SS, Henikoff S. 2011. Heat shock reduces stalled RNA polymerase II and nucleosome turnover genome-wide. Genes & Development 25:2387-2397. doi: 10.1101/gad.177675.111.
63. The C. elegans Sequencing Consortium. 1998. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012-2018.
64. van Steensel B, Delrow J, Bussemaker HJ. 2003. Genomewide analysis of Drosophila GAGA factor target genes reveals context-dependent DNA binding. Proceedings of the National Academy of Sciences of the United States of America 100:2580-2585. doi: 10.1073/pnas.0438000100.
65. Yuen KW, Nabeshima K, Oegema K, Desai A. 2011. Rapid de novo centromere formation occurs independently of heterochromatin protein 1 in C. elegans embryos. Current Biology: CB 21:1800-1807. doi: 10.1016/j. cub.2011.09.016.
66. Zhang T, Talbert PB, Zhang W, Wu Y, Yang Z, Henikoff JG, Henikoff S, Jiang J. 2013. The CentO satellite confers translational and rotational phasing on cenH3 nucleosomes in rice centromeres. Proceedings of the National Academy of Sciences of the United States of America 110:E4875-E4883. doi: 10.1073/pnas.1319548110.