Drosophila Yemanuclein and HIRA Cooperate for De Novo Assembly of H3.3-Containing Nucleosomes in the Male Pronucleus

PLoS Genetics

Volumn 9, Issue 2, 2013, Pages

  Orsi, Guillermo A ^a,d   Algazeery, Ahmed ^b   Meyer, Régis E ^b,e   Capri, Michèle ^b   Sapey Triomphe, Laure M ^a   Horard, Béatrice ^a   Gruffat, Henri ^c   Couble, Pierre ^a   Aït Ahmed, Ounissa ^b   Loppin, Benjamin ^a  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^b INSTITUTE OF HUMAN GENETICS   (France)

^c UNIVERSITÉ DE LYON   (France)

^d HARVARD MEDICAL SCHOOL   (United States)

^e OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; HIRA PROTEIN; HISTONE H3; HISTONE H3.3; PROTEIN YEMANUCLEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DROSOPHILA; EGG; FEMALE; FERTILIZATION; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; MALE; MUTANT; NONHUMAN; NUCLEOSOME; PRONUCLEUS; PROTEIN ANALYSIS; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; ZYGOTE;

ANIMALS; CELL CYCLE PROTEINS; CELL NUCLEUS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA REPLICATION; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FERTILIZATION; HISTONE CHAPERONES; HISTONES; MALE; NUCLEAR PROTEINS; NUCLEOSOMES; SPERMATOZOA; TRANSCRIPTION FACTORS; ZYGOTE;

EID: 84874787476     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003285     Document Type: Article

References (76)

1. Polo SE, Almouzni G, (2006) Chromatin assembly: a basic recipe with various flavours. Curr Opin Genet Dev 16: 104-111.
2. Ahmad K, Henikoff S, (2002) Histone H3 variants specify modes of chromatin assembly. Proc Natl Acad Sci U S A 99 Suppl 4: 16477-16484.
3. Talbert PB, Ahmad K, Almouzni G, Ausio J, Berger F, et al. (2012) A unified phylogeny-based nomenclature for histone variants. Epigenetics Chromatin 5: 7.
4. Corpet A, Almouzni G, (2009) Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information. Trends Cell Biol 19: 29-41.
5. Elsaesser SJ, Goldberg AD, Allis CD, (2010) New functions for an old variant: no substitute for histone H3.3. Curr Opin Genet Dev 20: 110-117.
6. Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, et al. (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140: 678-691.
7. Szenker E, Ray-Gallet D, Almouzni G, (2011) The double face of the histone variant H3.3. Cell Res 21: 421-434.
8. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y, (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116: 51-61.
9. Ahmad K, Henikoff S, (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9: 1191-1200.
10. Mito Y, Henikoff JG, Henikoff S, (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37: 1090-1097.
11. Schwartz BE, Ahmad K, (2005) Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19: 804-814.
12. Wirbelauer C, Bell O, Schubeler D, (2005) Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Genes Dev 19: 1761-1766.
13. Chow CM, Georgiou A, Szutorisz H, Maia e Silva A, Pombo A, et al. (2005) Variant histone H3.3 marks promoters of transcriptionally active genes during mammalian cell division. EMBO Rep 6: 354-360.
14. Deal RB, Henikoff JG, Henikoff S, (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328: 1161-1164.
15. Mito Y, Henikoff JG, Henikoff S, (2007) Histone replacement marks the boundaries of cis-regulatory domains. Science 315: 1408-1411.
16. Schneiderman JI, Sakai A, Goldstein S, Ahmad K, (2009) The XNP remodeler targets dynamic chromatin in Drosophila. Proc Natl Acad Sci U S A 106: 14472-14477.
17. Wong LH, Ren H, Williams E, McGhie J, Ahn S, et al. (2009) Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res 19: 404-414.
18. Nakayama T, Nishioka K, Dong YX, Shimojima T, Hirose S, (2007) Drosophila GAGA factor directs histone H3.3 replacement that prevents the heterochromatin spreading. Genes & development 21: 552-561.
19. Talbert PB, Henikoff S, (2010) Histone variants-ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11: 264-275.
20. Ooi SL, Henikoff S, (2007) Germline histone dynamics and epigenetics. Curr Opin Cell Biol 19: 257-265.
21. Orsi GA, Couble P, Loppin B, (2009) Epigenetic and replacement roles of histone variant H3.3 in reproduction and development. Int J Dev Biol 53: 231-243.
22. Banaszynski LA, Allis CD, Lewis PW, (2010) Histone variants in metazoan development. Dev Cell 19: 662-674.
23. van der Heijden GW, Derijck AA, Posfai E, Giele M, Pelczar P, et al. (2007) Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation. Nat Genet 39: 251-258.
24. Couldrey C, Carlton MB, Nolan PM, Colledge WH, Evans MJ, (1999) A retroviral gene trap insertion into the histone 3.3A gene causes partial neonatal lethality, stunted growth, neuromuscular deficits and male sub-fertility in transgenic mice. Hum Mol Genet 8: 2489-2495.
25. Santenard A, Ziegler-Birling C, Koch M, Tora L, Bannister AJ, et al. (2010) Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat Cell Biol 12: 853-862.
26. Szenker E, Lacoste N, Almouzni G, (2012) A Developmental Requirement for HIRA-Dependent H3.3 Deposition Revealed at Gastrulation in Xenopus. Cell Rep 1: 730-740.
27. Hodl M, Basler K, (2009) Transcription in the absence of histone H3.3. Curr Biol 19: 1221-1226.
28. Sakai A, Schwartz BE, Goldstein S, Ahmad K, (2009) Transcriptional and developmental functions of the H3.3 histone variant in Drosophila. Curr Biol 19: 1816-1820.
29. Akhmanova A, Miedema K, Wang Y, van Bruggen M, Berden JH, et al. (1997) The localization of histone H3.3 in germ line chromatin of Drosophila males as established with a histone H3.3-specific antiserum. Chromosoma 106: 335-347.
30. Carrell DT, (2012) Epigenetics of the male gamete. Fertil Steril 97: 267-274.
31. Eirin-Lopez JM, Ausio J, (2009) Origin and evolution of chromosomal sperm proteins. Bioessays 31: 1062-1070.
32. Miller D, Brinkworth M, Iles D, (2010) Paternal DNA packaging in spermatozoa: more than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction 139: 287-301.
33. Ashburner M, Misra S, Roote J, Lewis SE, Blazej R, et al. (1999) An exploration of the sequence of a 2.9-Mb region of the genome of Drosophila melanogaster: the Adh region. Genetics 153: 179-219.
34. Jayaramaiah Raja S, Renkawitz-Pohl R, (2005) Replacement by Drosophila melanogaster protamines and Mst77F of histones during chromatin condensation in late spermatids and role of sesame in the removal of these proteins from the male pronucleus. Mol Cell Biol 25: 6165-6177.
35. Rathke C, Baarends WM, Jayaramaiah-Raja S, Bartkuhn M, Renkawitz R, et al. (2007) Transition from a nucleosome-based to a protamine-based chromatin configuration during spermiogenesis in Drosophila. J Cell Sci 120: 1689-1700.
36. Bonnefoy E, Orsi GA, Couble P, Loppin B, (2007) The essential role of Drosophila HIRA for de novo assembly of paternal chromatin at fertilization. PLoS Genet 3: e182 doi:10.1371/journal.pgen.0030182.
37. Loppin B, Bonnefoy E, Anselme C, Laurencon A, Karr TL, et al. (2005) The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437: 1386-1390.
38. van der Heijden GW, Dieker JW, Derijck AA, Muller S, Berden JH, et al. (2005) Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech Dev 122: 1008-1022.
39. Torres-Padilla ME, Bannister AJ, Hurd PJ, Kouzarides T, Zernicka-Goetz M, (2006) Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int J Dev Biol 50: 455-461.
40. Zhao ZK, Li W, Wang MY, Zhou L, Wang JL, et al. (2011) The role of HIRA and maternal histones in sperm nucleus decondensation in the gibel carp and color crucian carp. Mol Reprod Dev 78: 139-147.
41. Green EM, Antczak AJ, Bailey AO, Franco AA, Wu KJ, et al. (2005) Replication-independent histone deposition by the HIR complex and Asf1. Curr Biol 15: 2044-2049.
42. Prochasson P, Florens L, Swanson SK, Washburn MP, Workman JL, (2005) The HIR corepressor complex binds to nucleosomes generating a distinct protein/DNA complex resistant to remodeling by SWI/SNF. Genes Dev 19: 2534-2539.
43. Amin AD, Vishnoi N, Prochasson P, (2011) A global requirement for the HIR complex in the assembly of chromatin. Biochim Biophys Acta 1819: 264-276.
44. Balaji S, Iyer LM, Aravind L, (2009) HPC2 and ubinuclein define a novel family of histone chaperones conserved throughout eukaryotes. Mol Biosyst 5: 269-275.
45. Rai TS, Puri A, McBryan T, Hoffman J, Tang Y, et al. (2011) Human CABIN1 is a functional member of the human HIRA/UBN1/ASF1a histone H3.3 chaperone complex. Mol Cell Biol 31: 4107-4118.
46. Anderson HE, Kagansky A, Wardle J, Rappsilber J, Allshire RC, et al. (2010) Silencing mediated by the Schizosaccharomyces pombe HIRA complex is dependent upon the Hpc2-like protein, Hip4. PLoS ONE 5: e13488 doi:10.1371/journal.pone.0013488.
47. Aho S, Buisson M, Pajunen T, Ryoo YW, Giot JF, et al. (2000) Ubinuclein, a novel nuclear protein interacting with cellular and viral transcription factors. J Cell Biol 148: 1165-1176.
48. Banumathy G, Somaiah N, Zhang R, Tang Y, Hoffmann J, et al. (2009) Human UBN1 is an ortholog of yeast Hpc2p and has an essential role in the HIRA/ASF1a chromatin-remodeling pathway in senescent cells. Mol Cell Biol 29: 758-770.
49. Tang Y, Puri A, Ricketts MD, Rai TS, Hoffmann J, et al. (2012) Identification of an ubinuclein 1 region required for stability and function of the human HIRA/UBN1/CABIN1/ASF1a histone H3.3 chaperone complex. Biochemistry 51: 2366-2377.
50. Ait-Ahmed O, Thomas-Cavallin M, Rosset R, (1987) Isolation and characterization of a region of the Drosophila genome which contains a cluster of differentially expressed maternal genes (yema gene region). Dev Biol 122: 153-162.
51. Ait-Ahmed O, Bellon B, Capri M, Joblet C, Thomas-Delaage M, (1992) The yemanuclein-alpha: a new Drosophila DNA binding protein specific for the oocyte nucleus. Mech Dev 37: 69-80.
52. Meyer RE, Delaage M, Rosset R, Capri M, Ait-Ahmed O, (2010) A single mutation results in diploid gamete formation and parthenogenesis in a Drosophila yemanuclein-alpha meiosis I defective mutant. BMC Genet 11: 104.
53. Moshkin YM, Kan TW, Goodfellow H, Bezstarosti K, Maeda RK, et al. (2009) Histone chaperones ASF1 and NAP1 differentially modulate removal of active histone marks by LID-RPD3 complexes during NOTCH silencing. Mol Cell 35: 782-793.
54. Konev AY, Tribus M, Park SY, Podhraski V, Lim CY, et al. (2007) CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science 317: 1087-1090.
55. Fuller M (1993) Spermatogenesis. In: Bate M, Martinez Arias A, editors. The development of Drosophila melanogaster. 1 ed. Cold Spring Harbor, NY. Cold Spring Harbor Laboratory Press: 71-148.
56. Loppin B, Docquier M, Bonneton F, Couble P, (2000) The maternal effect mutation sesame affects the formation of the male pronucleus in Drosophila melanogaster. Dev Biol 222: 392-404.
57. Loppin B, Berger F, Couble P, (2001) The Drosophila maternal gene sesame is required for sperm chromatin remodeling at fertilization. Chromosoma 110: 430-440.
58. Drane P, Ouararhni K, Depaux A, Shuaib M, Hamiche A, (2010) The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev 24: 1253-1265.
59. Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD, (2010) Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc Natl Acad Sci U S A 107: 14075-14080.
60. Wong LH, McGhie JD, Sim M, Anderson MA, Ahn S, et al. (2010) ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res 20: 351-360.
61. Bassett AR, Cooper SE, Ragab A, Travers AA, (2008) The chromatin remodelling factor dATRX is involved in heterochromatin formation. PLoS ONE 3: e2099 doi:10.1371/journal.pone.0002099.
62. Roberts C, Sutherland HF, Farmer H, Kimber W, Halford S, et al. (2002) Targeted mutagenesis of the Hira gene results in gastrulation defects and patterning abnormalities of mesoendodermal derivatives prior to early embryonic lethality. Mol Cell Biol 22: 2318-2328.
63. Ray-Gallet D, Woolfe A, Vassias I, Pellentz C, Lacoste N, et al. (2011) Dynamics of histone H3 deposition in vivo reveal a nucleosome gap-filling mechanism for H3.3 to maintain chromatin integrity. Mol Cell 44: 928-941.
64. Kennedy AL, McBryan T, Enders GH, Johnson FB, Zhang R, et al. (2010) Senescent mouse cells fail to overtly regulate the HIRA histone chaperone and do not form robust Senescence Associated Heterochromatin Foci. Cell Div 5: 16.
65. Mousson F, Ochsenbein F, Mann C, (2007) The histone chaperone Asf1 at the crossroads of chromatin and DNA checkpoint pathways. Chromosoma 116: 79-93.
66. Ray-Gallet D, Quivy JP, Sillje HW, Nigg EA, Almouzni G, (2007) The histone chaperone Asf1 is dispensable for direct de novo histone deposition in Xenopus egg extracts. Chromosoma 116: 487-496.
67. Ye X, Zerlanko B, Zhang R, Somaiah N, Lipinski M, et al. (2007) Definition of pRB- and p53-dependent and-independent steps in HIRA/ASF1a-mediated formation of senescence-associated heterochromatin foci. Mol Cell Biol 27: 2452-2465.
68. Singer AB, Gall JG, (2011) An inducible nuclear body in the Drosophila germinal vesicle. Nucleus 2: 403-409.
69. Dubruille R, Orsi GA, Delabaere L, Cortier E, Couble P, et al. (2010) Specialization of a Drosophila capping protein essential for the protection of sperm telomeres. Curr Biol 20: 2090-2099.
70. Schuh M, Lehner CF, Heidmann S, (2007) Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr Biol 17: 237-243.
71. Thummel CS, Boulet AM, Lipshitz HD, (1988) Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene 74: 445-456.
72. Bischof J, Maeda RK, Hediger M, Karch F, Basler K, (2007) An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci U S A 104: 3312-3317.
73. Groth AC, Fish M, Nusse R, Calos MP, (2004) Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166: 1775-1782.
74. Capri M, Santoni MJ, Thomas-Delaage M, Ait-Ahmed O, (1997) Implication of a 5′ coding sequence in targeting maternal mRNA to the Drosophila oocyte. Mech Dev 68: 91-100.
75. Aho S, Lupo J, Coly PA, Sabine A, Castellazzi M, et al. (2009) Characterization of the ubinuclein protein as a new member of the nuclear and adhesion complex components (NACos). Biol Cell 101: 319-334.
76. Jager H, Herzig A, Lehner CF, Heidmann S, (2001) Drosophila separase is required for sister chromatid separation and binds to PIM and THR. Genes Dev 15: 2572-2584.