The drosophila histone variant H2A.V works in concert with HP1 to promote kinetochore-driven microtubule formation

Cell Cycle

Volumn 14, Issue 4, 2015, Pages 577-588

  Vernì, Fiammetta ^a   Cenci, Giovanni ^a,b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b Temple University   (United States)

Author keywords

Chromosome segregation; Drosophila; H2A.V; HP1; Mitosis

Indexed keywords

BRAIN EXTRACT; HETEROCHROMATIN PROTEIN 1; HISTONE H2A; HISTONE H2AV; UNCLASSIFIED DRUG; CHROMATIN; DROSOPHILA PROTEIN; HETEROCHROMATIN PROTEIN 1, DROSOPHILA; HISTONE; NONHISTONE PROTEIN;

ANAPHASE; ARTICLE; CELL CYCLE PROGRESSION; CELL MUTANT; CENTROMERE; CENTROSOME; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME; CHROMOSOME SEGREGATION; COLD EXPOSURE; CONTROLLED STUDY; DNA DAMAGE; DROSOPHILA; GENE MUTATION; GENE OVEREXPRESSION; GENETIC VARIABILITY; HETEROCHROMATIN; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; METAPHASE; METAPHASE CHROMOSOME; MICROTUBULE; MITOSIS; MITOSIS INDEX; MITOSIS SPINDLE; NEUROBLAST; NONHUMAN; PHENOTYPE; POLYTENE CHROMOSOME; PROMETAPHASE; PROTEIN DEPLETION; SISTER CHROMATID; TRANSGENE; ANIMAL; DROSOPHILA MELANOGASTER; GENETICS; LARVA; METABOLISM; PHYSIOLOGY; WESTERN BLOTTING;

DROSOPHILA MELANOGASTER;

ANIMALS; BLOTTING, WESTERN; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HISTONES; KINETOCHORES; LARVA; MICROTUBULES; MITOSIS;

EID: 84923605889     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/15384101.2014.991176     Document Type: Article

References (60)

1. Kornberg RD, Thomas JO. Chromatin structure; oligomers of the histones. Science 1974; 184:865-8; PMID:4825888; http://dx.doi.org/10.1126/science. 184.4139.865
2. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997; 389:251-60; PMID:9305837; http://dx.doi.org/10.1038/38444
3. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res 2011; 21:381-95; PMID:21321607; http://dx.doi.org/10.1038/cr.2011.22
4. Kouzarides T. Chromatin modifications and their function. Cell 2007; 128:693-705; PMID:17320507; http://dx.doi.org/10.1016/j.cell.2007.02.005
5. Ruthenburg AJ, Li H, Patel DJ, Allis CD. Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 2007; 8:983-94; PMID:18037899; http://dx.doi.org/10.1038/nrm2298
6. Henikoff S, Ahmad K. Assembly of variant histones into chromatin. Ann Rev Cell Dev Biol 2005; 21:133-53; PMID:16212490; http://dx.doi.org/10.1146/ annurev.cellbio.21.012704.133518
7. Malik HS, Henikoff S. Phylogenomics of the nucleosome. Nat Struct Biol 2003; 10:882-91; PMID:14583738; http://dx.doi.org/10.1038/nsb996
8. Liu X, Li B, GorovskyMa. Essential and nonessential histone H2A variants in Tetrahymena thermophila. Mol Cell Biol 1996; 16:4305-11; PMID:8754831
9. Clarkson MJ, Wells JR, Gibson F, Saint R, Tremethick DJ. Regions of variant histone His2AvD required for Drosophila development. Nature 1999; 399:694-7; PMID:10385122; http://dx.doi.org/10.1038/21436
10. Ridgway P, Brown KD, Rangasamy D, Svensson U, Tremethick DJ. Unique residues on the H2A.Z containing nucleosome surface are important for Xenopus laevis development. J Biol Chem 2004; 279:43815-20; PMID:15299007; http://dx.doi.org/10.1074/jbc. M408409200
11. Faast R, Thonglairoam V, Schulz TC, Beall J,Wells JR, Taylor H, Matthaei K, Rathjen PD, Tremethick DJ, Lyons I. Histone variant H2A.Z is required for early mammalian development. Curr Biol 2001; 11:1183-7; PMID:11516949; http://dx.doi.org/10.1016/S0960-9822(01)00329-3
12. Ahmed S, Dul B, Qiu X, Walworth NC. Msc1 acts through histone H2A.Z to promote chromosome stability in Schizosaccharomyces pombe. Genetics 2007; 177:1487-97; PMID:17947424; http://dx.doi.org/ 10.1534/genetics.107.078691
13. Rangasamy D, Greaves I, Tremethick DJ. RNA interference demonstrates a novel role forH2A.Z in chromosome segregation. Nat Struct Mol Biol 2004; 11:650-5; PMID:15195148; http://dx.doi.org/10.1038/nsmb786
14. Hou H, Wang Y, Kallgren SP, Thompson J, Yates JR, 3rd, Jia S. Histone variant H2A.Z regulates centromere silencing and chromosome segregation in fission yeast. J Biol Chem 2010; 285:1909-18; PMID:19910462; http://dx.doi.org/10.1074/jbc.M109.058487
15. Draker R, Cheung P. Transcriptional and epigenetic functions of histone variant H2A.Z. Biochem Cell Biol 2009; 87:19-25; PMID:19234520; http://dx.doi.org/ 10.1139/O08-117
16. Guillemette B, Gaudreau L. Reuniting the contrasting functions of H2A.Z. Biochem Cell Biol 2006; 84:528-35; PMID:16936825; http://dx.doi.org/10.1139/o06-077
17. Greaves IK, Rangasamy D, Devoy M, Marshall Graves JA, Tremethick DJ. The X and Y chromosomes assemble into H2A.Z-containing [corrected] facultative heterochromatin [corrected] following meiosis. Mol Cell Biol 2006; 26:5394-405
18. Meneghini MD, Wu M, Madhani HD. Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 2003; 112:725-36; PMID:12628191; http://dx.doi.org/ 10.1016/S0092-8674(03)00123-5
19. Sarcinella E, Zuzarte PC, Lau PN, Draker R, Cheung P. Monoubiquitylation of H2A.Z distinguishes its association with euchromatin or facultative heterochromatin. Mol Cell Biol 2007; 27:6457-68; PMID:17636032; http://dx.doi.org/10.1128/MCB.00241-07
20. Baldi S, Becker PB. The variant histone H2A.V of Drosophila-three roles, two guises. Chromosoma 2013; 122:245-58; PMID:23553272; http://dx.doi.org/ 10.1007/s00412-013-0409-x
21. Joyce EF, Pedersen M, Tiong S, White-Brown SK, Paul A, Campbell SD, McKim KS. Drosophila ATM and ATR have distinct activities in the regulation of meiotic DNA damage and repair. J Cell Biol 2011; 195:359-67; PMID:22024169; http://dx.doi.org/10.1083/ jcb.201104121
22. Madigan JP, Chotkowski HL, Glaser RL. DNA dou-ble-strand break-induced phosphorylation of Drosophila histone variant H2Av helps prevent radiationinduced apoptosis. Nucleic Acids Res 2002; 30:3698-705; PMID:12202754; http://dx.doi.org/10.1093/nar/ gkf496
23. van Daal A, Elgin SC. A histone variant, H2AvD, is essential in Drosophila melanogaster. Mol Biol Cell 1992; 3:593-602; PMID:1498368; http://dx.doi.org/ 10.1091/mbc.3.6.593
24. Hardy S, Jacques PE, Gevry N, Forest A, Fortin ME, Laflamme L, Gaudreau L, Robert F. The euchromatic and heterochromatic landscapes are shaped by antagonizing effects of transcription on H2A.Z deposition. PLoS Genet 2009; 5:e1000687; PMID:19834540; http://dx.doi.org/10.1371/journal.pgen.1000687
25. Leach TJ, Mazzeo M, Chotkowski HL, Madigan JP, Wotring MG, Glaser RL. Histone H2A.Z is widely but nonrandomly distributed in chromosomes of Drosophila melanogaster. J Biol Chem 2000; 275:23267-72; PMID:10801889; http://dx.doi.org/10.1074/jbc. M910206199
26. Swaminathan J, Baxter EM, Corces VG. The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev 2005; 19:65-76; PMID:15630020; http://dx. doi.org/10.1101/gad.1259105
27. Messina G, Damia E, Fanti L, Atterrato MT, Celauro E, Mariotti FR, Accardo MC, Walther M, Verni F, Picchioni D, et al. Yeti, an essential Drosophila melanogaster gene, encodes a protein required for chromatin organization. J Cell Sci 2014; 127:2577-88; PMID:24652835; http://dx.doi.org/10.1242/ jcs.150243
28. Giansanti MG, Bucciarelli E, Bonaccorsi S, Gatti M. Drosophila SPD-2 is an essential centriole component required for PCM recruitment and astral-microtubule nucleation. Curr Biol 2008; 18:303-9; PMID:18291647; http://dx. doi.org/10.1016/j.cub.2008.01.058
29. Bucciarelli E, Pellacani C, Naim V, Palena A, Gatti M, Somma MP. Drosophila Dgt6 interacts with Ndc80, Msps/XMAP215, and gamma-tubulin to promote kinetochore-driven MT formation. Curr Biol 2009; 19:1839-45; PMID:19836241; http://dx.doi.org/ 10.1016/j.cub.2009.09.043
30. Somma MP, Fasulo B, Cenci G, Cundari E, Gatti M. Molecular dissection of cytokinesis by RNA interference in Drosophila cultured cells. Mol Biol Cell 2002; 13:2448-60; PMID:12134082; http://dx.doi.org/ 10.1091/mbc.01-12-0589
31. Karess R. Rod-Zw10-Zwilch: a key player in the spindle checkpoint. Trends Cell Biol 2005; 15:386-92; PMID:15922598; http://dx.doi.org/10.1016/j.tcb. 2005.05.003
32. Williams BC, Karr TL, Montgomery JM, Goldberg ML. The Drosophila l(1)zw10 gene product, required for accurate mitotic chromosome segregation, is redistributed at anaphase onset. J Cell Biol 1992; 118:759-73; PMID:1339459; http://dx.doi.org/10.1083/jcb.118.4.759
33. Goshima G,Mayer M, Zhang N, Stuurman N, Vale RD. Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J Cell Biol 2008; 181:421-9; PMID:18443220; http://dx.doi. org/10.1083/jcb.200711053
34. Mottier-Pavie V, Cenci G, Verni F, Gatti M, Bonaccorsi S. Phenotypic analysis of misato function reveals roles of noncentrosomal microtubules in Drosophila spindle formation. J Cell Sci 2011; 124:706-17; PMID:21285248; http://dx.doi.org/10.1242/jcs. 072348
35. Fanti L, Pimpinelli S. HP1: a functionally multifaceted protein. Curr Opin Genet Dev 2008; 18:169-74; PMID:18329871; http://dx.doi.org/10.1016/j.gde. 2008.01.009
36. Fanti L, Giovinazzo G, Berloco M, Pimpinelli S. The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol Cell 1998; 2:527-38; PMID:9844626; http://dx.doi.org/10.1016/S1097-2765(00)80152-5
37. Musaro M, Ciapponi L, Fasulo B, Gatti M, Cenci G. Unprotected Drosophila melanogaster telomeres activate the spindle assembly checkpoint. Nat Genet 2008; 40:362-6; PMID:18246067; http://dx.doi.org/ 10.1038/ng.2007.64
38. Meireles AM, Fisher KH, Colombie N, Wakefield JG, Ohkura H. Wac: a new Augmin subunit required for chromosome alignment but not for acentrosomal microtubule assembly in female meiosis. J Cell Biol 2009; 184:777-84; PMID:19289792; http://dx.doi. org/10.1083/jcb.200811102
39. Carr AM, Dorrington SM, Hindley J, Phear GA, Aves SJ, Nurse P. Analysis of a histone H2A variant from fission yeast: evidence for a role in chromosome stability. Mol Gen Genet 1994; 245:628-35; PMID:NOT-FOUND; http://dx.doi.org/10.1007/BF00282226
40. Kim HS, Vanoosthuyse V, Fillingham J, Roguev A, Watt S, Kislinger T, Treyer A, Carpenter LR, Bennett CS, Emili A, et al. An acetylated form of histone H2A. Z regulates chromosome architecture in Schizosaccharomyces pombe. Nat Struct Mol Biol 2009; 16:1286-93; PMID:19915592; http://dx.doi.org/10.1038/ nsmb.1688
41. Rangasamy D, Berven L, Ridgway P, Tremethick DJ. Pericentric heterochromatin becomes enriched with H2A.Z during early mammalian development. EMBO J 2003; 22:1599-607; PMID:12660166; http://dx.doi. org/10.1093/emboj/cdg160
42. Sharma U, Stefanova D, Holmes SG. Histone variant H2A.Z functions in sister chromatid cohesion in Saccharomyces cerevisiae. Mol Cell Biol 2013; 33:3473-81; PMID:23816883; http://dx.doi.org/10.1128/ MCB.00162-12
43. Jacobs SA, Taverna SD, Zhang Y, Briggs SD, Li J, Eissenberg JC, Allis CD, Khorasanizadeh S. Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. EMBO J 2001; 20:5232-41; PMID:11566886; http://dx.doi.org/10.1093/emboj/ 20.18.5232
44. Fan JY, Rangasamy D, Luger K, Tremethick DJ. H2A. Z alters the nucleosome surface to promote HP1alphamediated chromatin fiber folding. Mol Cell 2004; 16:655-61; PMID:15546624; http://dx.doi.org/ 10.1016/j.molcel.2004.10.023
45. Yamagishi Y, Sakuno T, Shimura M, Watanabe Y. Heterochromatin links to centromeric protection by recruiting shugoshin. Nature 2008; 455:251-5; PMID:18716626; http://dx.doi.org/10.1038/nature07217
46. Kang J, Chaudhary J, Dong H, Kim S, Brautigam CA, Yu HT. Mitotic centromeric targeting of HP1 and its binding to Sgo1 are dispensable for sister-chromatid cohesion in human cells. Mol Biol Cell 2011; 22:1181-90; PMID:21346195; http://dx.doi.org/10.1091/mbc. E11-01-0009
47. Ainsztein AM, Kandels-Lewis SE, Mackay AM, Earnshaw WC. INCENP centromere and spindle targeting:Identification of essential conserved motifs and involvement of heterochromatin protein HP1. J Cell Biol 1998; 143:1763-74; PMID:9864353; http://dx.doi. org/10.1083/jcb.143.7.1763
48. Nozawa RS, Nagao K, Masuda HT, Iwasaki O, Hirota T, Nozaki N, Kimura H, Obuse C. Human POGZ modulates dissociation of HP1 alpha from mitotic chromosome arms through Aurora B activation. Nat Cell Biol 2010; 12:719-U212; PMID:20562864; http://dx.doi.org/10.1038/ncb2075
49. Canzio D, Larson A, Narlikar GJ. Mechanisms of functional promiscuity by HP1 proteins. Trends Cell Biol 2014; 24:377-86; PMID:24618358; http://dx.doi.org/ 10.1016/j.tcb.2014.01.002
50. Eissenberg JC, Elgin SC. HP1a: a structural chromosomal protein regulating transcription. Trends Genet 2014; 30:103-10; PMID:24555990; http://dx.doi.org/ 10.1016/j.tig.2014.01.002
51. Obuse C, Iwasaki O, Kiyomitsu T, Goshima G, Toyoda Y, Yanagida M. A conserved Mis12 centromere complex is linked to heterochromatic HP1 and outer kinetochore protein Zwint-1. Nat Cell Biol 2004; 6:1135-U37; PMID:15502821; http://dx.doi.org/10.1038/ncb1187
52. Auth T, Kunkel E, Grummt F. Interaction between HP1alpha and replication proteins in mammalian cells. Exp Cell Res 2006; 312:3349-59; PMID:16950245; http://dx.doi.org/10.1016/j.yexcr.2006.07.014
53. Guenatri M, Bailly D, Maison C, Almouzni G. Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 2004; 166:493-505; PMID:15302854; http://dx.doi.org/10.1083/ jcb.200403109
54. Koch B, Kueng S, Ruckenbauer C, Wendt KS, Peters JM. The Suv39h-HP1 histone methylation pathway is dispensable for enrichment and protection of cohesin at centromeres in mammalian cells. Chromosoma 2008; 117:199-210; PMID:18075750; http://dx.doi.org/ 10.1007/s00412-007-0139-z
55. Giansanti MG, Bonaccorsi S, Kurek R, Farkas RM, Dimitri P, Fuller MT, Gatti M. The class I PITP giotto is required for Drosophila cytokinesis. Curr Biol 2006; 16:195-201; PMID:16431372; http://dx.doi.org/ 10.1016/j.cub.2005.12.011
56. Cenci G, Rawson RB, Belloni G, Castrillon DH, Tudor M, Petrucci R, Goldberg ML, Wasserman SA, Gatti M. UbcD1, a Drosophila ubiquitin-conjugating enzyme required for proper telomere behavior. Genes Dev 1997; 11:863-75; PMID:9106658; http://dx.doi. org/10.1101/gad.11.7.863
57. Ciapponi L, Cenci G, Gatti M. The Drosophila Nbs protein functions in multiple pathways for the maintenance of genome stability. Genetics 2006; 173:1447-54; PMID:16648644; http://dx.doi.org/10.1534/ genetics.106.058081
58. Bonaccorsi S, Giansanti MG, Gatti M. Spindle assembly in Drosophila neuroblasts and ganglion mother cells. Nat Cell Biol 2000; 2:54-6; PMID:10620808; http://dx.doi.org/10.1038/71378
59. Blower MD, Karpen GH. The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. N Cell Biol 2001; 3:730-9; PMID:11483958; http://dx.doi.org/10.1038/ 35087045
60. Raffa GD, Siriaco G, Cugusi S, Ciapponi L, Cenci G, Wojcik E, Gatti M. The Drosophila modigliani (moi) gene encodes a HOAP-interacting protein required for telomere protection. Proc Natl Acad Sci U S A 2009; 106:2271-6; PMID:19181850; http://dx.doi.org/ 10.1073/pnas.0812702106