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PLOS Genetics  2007 

The Essential Role of Drosophila HIRA for De Novo Assembly of Paternal Chromatin at Fertilization

DOI: 10.1371/journal.pgen.0030182

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Abstract:

In many animal species, the sperm DNA is packaged with male germ line–specific chromosomal proteins, including protamines. At fertilization, these non-histone proteins are removed from the decondensing sperm nucleus and replaced with maternally provided histones to form the DNA replication competent male pronucleus. By studying a point mutant allele of the Drosophila Hira gene, we previously showed that HIRA, a conserved replication-independent chromatin assembly factor, was essential for the assembly of paternal chromatin at fertilization. HIRA permits the specific assembly of nucleosomes containing the histone H3.3 variant on the decondensing male pronucleus. We report here the analysis of a new mutant allele of Drosophila Hira that was generated by homologous recombination. Surprisingly, phenotypic analysis of this loss of function allele revealed that the only essential function of HIRA is the assembly of paternal chromatin during male pronucleus formation. This HIRA-dependent assembly of H3.3 nucleosomes on paternal DNA does not require the histone chaperone ASF1. Moreover, analysis of this mutant established that protamines are correctly removed at fertilization in the absence of HIRA, thus demonstrating that protamine removal and histone deposition are two functionally distinct processes. Finally, we showed that H3.3 deposition is apparently not affected in Hira mutant embryos and adults, suggesting that different chromatin assembly machineries could deposit this histone variant.

References

[1]  Polo SE, Almouzni G (2006) Chromatin assembly: a basic recipe with various flavours. Curr Opin Genet Dev 16(2): 104–111.
[2]  Akey CW, Luger K (2003) Histone chaperones and nucleosome assembly. Curr Opin Struct Biol 13(1): 6–14.
[3]  Poccia D, Collas P (1996) Transforming sperm nuclei into male pronuclei in vivo and in vitro. Curr Top Dev Biol 34: 25–88.
[4]  McLay DW, Clarke HJ (2003) Remodelling the paternal chromatin at fertilization in mammals. Reproduction 125(5): 625–633.
[5]  Wright SJ (1999) Sperm nuclear activation during fertilization. Curr Top Dev Biol 46: 133–178.
[6]  Carrell DT, De Jonge C, Lamb DJ (2006) The genetics of male infertility: a field of study whose time is now. Arch Androl 52(4): 269–274.
[7]  Caron C, Govin J, Rousseaux S, Khochbin S (2005) How to pack the genome for a safe trip. Prog Mol Subcell Biol 38: 65–89.
[8]  Rousseaux S, Caron C, Govin J, Lestrat C, Faure AK, et al. (2005) Establishment of male-specific epigenetic information. Gene 345(2): 139–153.
[9]  Kawasaki K, Philpott A, Avilion AA, Berrios M, Fisher PA (1994) Chromatin decondensation in Drosophila embryo extracts. J Biol Chem 269(13): 10169–10176.
[10]  Crevel G, Cotterill S (1995) DF 31, a sperm decondensation factor from Drosophila melanogaster: purification and characterization. EMBO J 14(8): 1711–1717.
[11]  Ito T, Tyler JK, Bulger M, Kobayashi R, Kadonaga JT (1996) ATP-facilitated chromatin assembly with a nucleoplasmin-like protein from Drosophila melanogaster. J Biol Chem 271(40): 25041–25048.
[12]  Crevel G, Huikeshoven H, Cotterill S, Simon M, Wall J, et al. (1997) Molecular and cellular characterization of CRP1, a Drosophila chromatin decondensation protein. J Struct Biol 118(1): 9–22.
[13]  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 sésame in the removal of these proteins from the male pronucleus. Mol Cell Biol 25(14): 6165–6177. Erratum in: Mol Cell Biol 26(9):3682 (2006).
[14]  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(9): 1689–1700.
[15]  Loppin B, Docquier M, Bonneton F, Couble P (2000) The maternal effect mutation sésame affects the formation of the male pronucleus in Drosophila melanogaster. Dev Biol 222(2): 392–404.
[16]  Loppin B, Berger F, Couble P (2001) The Drosophila maternal gene sésame is required for sperm chromatin remodeling at fertilization. Chromosoma 110(6): 430–440.
[17]  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(7063): 1386–1390.
[18]  Ray-Gallet D, Quivy JP, Scamps C, Martini EM, Lipinski M, et al. (2002) HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol Cell 9(5): 1091–1100.
[19]  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(1): 51–61.
[20]  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 Dev 21(5): 552–561.
[21]  Smith TF, Gaitatzes C, Saxena K, Neer EJ (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24(5): 181–185.
[22]  Gong WJ, Golic KG (2003) Ends-out, or replacement, gene targeting in Drosophila. Proc Natl Acad Sci U S A 100(5): 2556–2561.
[23]  Gong WJ, Golic KG (2004) Genomic deletions of the Drosophila melanogaster Hsp70 genes. Genetics 168(3): 1467–1476.
[24]  Fuller MT (1993) Spermatogenesis. In: Bate M, Martinez-Arias A, editors. The development of Drosophila melanogaster. Cold Spring Harbor Press. pp. pp–71.
[25]  Fitch KR, Wakimoto BT (1998) The paternal effect gene ms(3)sneaky is required for sperm activation and the initiation of embryogenesis in Drosophila melanogaster. Dev Biol 197(2): 270–282.
[26]  Foe VE, Odell GM, Edgar BA (1993) Mitosis and morphogenesis in the Drosophila embryo. In: Bate M, Martinez-Arias A, editors. The development of Drosophila melanogaster. Cold Spring Harbor Press. pp. pp–149.
[27]  Horner VL, Czank A, Jang JK, Singh N, Williams BC, et al. (2006) The Drosophila calcipressin Sarah is required for several aspects of egg activation. Curr Biol 16(14): 1441–1446.
[28]  Ner SS, Travers AA (1994) HMG-D, the Drosophila melanogaster homologue of HMG 1 protein, is associated with early embryonic chromatin in the absence of histone H1. EMBO J 13(8): 1817–1822.
[29]  Mousson F, Ochsenbein F, Mann C (2007) The histone chaperone Asf1 at the crossroads of chromatin and DNA checkpoint pathways. Chromosoma 116(2): 79–93.
[30]  English CM, Adkins MW, Carson JJ, Churchill ME, Tyler JK (2006) Structural basis for the histone chaperone activity of Asf1. Cell 127(3): 495–508.
[31]  Antczak AJ, Tsubota T, Kaufman PD, Berger JM (2006) Structure of the yeast histone H3-ASF1 interaction: implications for chaperone mechanism, species-specific interactions, and epigenetics. BMC Struct Biol 6: 26.
[32]  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(22): 2044–2049.
[33]  Tang Y, Poustovoitov MV, Zhao K, Garfinkel M, Canutescu A, et al. (2006) Structure of a human ASF1a-HIRA complex and insights into specificity of histone chaperone complex assembly. Nat Struct Mol Biol 13(10): 921–929.
[34]  Moshkin YM, Armstrong JA, Maeda RK, Tamkun JW, Verrijzer P, et al. (2002) Histone chaperone ASF1 cooperates with the Brahma chromatin-remodelling machinery. Genes Dev 2002 16(20): 2621–2626.
[35]  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. doi:10.1007/s00412–007-0112-x.
[36]  Schwartz BE, Ahmad K (2005) Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19(7): 804–814.
[37]  Van Doren M, Williamson AL, Lehmann R (1998) Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr Biol 8(4): 243–246.
[38]  Schaner CE, Deshpande G, Schedl PD, Kelly WG (2003) A conserved chromatin architecture marks and maintains the restricted germ cell lineage in worms and flies. Dev Cell 5(5): 747–757.
[39]  Fuyama Y (1984) Gynogenesis in Drosophila melanogaster. Japan J Genet 59: 91–96.
[40]  Loppin B, Berger F, Couble P (2001) Paternal chromosome incorporation into the zygote nucleus is controlled by maternal haploid in Drosophila. Dev Biol 231(2): 383–396.
[41]  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(6): 335–347.
[42]  Philpott A, Leno GH, Laskey RA (1991) Sperm decondensation in Xenopus egg cytoplasm is mediated by nucleoplasmin. Cell 65(4): 569–578.
[43]  Philpott A, Leno GH (1992) Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts. Cell 69(5): 759–767.
[44]  Prado A, Ramos I, Frehlick LJ, Muga A, Ausio J (2004) Nucleoplasmin: a nuclear chaperone. Biochem Cell Biol 82(4): 437–445.
[45]  Frehlick LJ, Eirin-Lopez JM, Ausio J (2007) New insights into the nucleophosmin/nucleoplasmin family of nuclear chaperones. Bioessays 29(1): 49–59.
[46]  Frehlick LJ, Eirin-Lopez JM, Jeffery ED, Hunt DF, Ausio J (2006) The characterization of amphibian nucleoplasmins yields new insight into their role in sperm chromatin remodeling. BMC Genomics 7: 99.
[47]  Balhorn R, Gledhill BL, Wyrobek AJ (1977) Mouse sperm chromatin proteins: quantitative isolation and partial characterization. Biochemistry 16(18): 4074–4080.
[48]  Burns KH, Viveiros MM, Ren Y, Wang P, DeMayo FJ, et al. (2003) Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science 300(5619): 633–636.
[49]  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(9): 1008–1022.
[50]  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(5): 455–461.
[51]  Ohsumi K, Katagiri C (1991) Characterization of the ooplasmic factor inducing decondensation of and protamine removal from toad sperm nuclei: involvement of nucleoplasmin. Dev Biol 148(1): 295–305.
[52]  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(7): 2318–2328.
[53]  Kirov N, Shtilbans A, Rushlow C (1998) Isolation and characterization of a new gene encoding a member of the HIRA family of proteins from Drosophila melanogaster. Gene 212(2): 323–332.
[54]  Llevadot R, Marques G, Pritchard M, Estivill X, Ferrus A, et al. (1998) Cloning, chromosome mapping and expression analysis of the HIRA gene from Drosophila melanogaster. Biochem Biophys Res Commun 249(2): 486–491.
[55]  Ahmad K, Henikoff S (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9(6): 1191–1200.
[56]  Meshorer E, Yellajoshula D, George E, Scambler PJ, Brown DT, et al. (2006) Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 10(1): 105–116.
[57]  Schwartz BE, Ahmad K (2006) 2. Chromatin assembly with H3 histones: full throttle down multiple pathways. Curr Top Dev Biol 74: 31–55.
[58]  Adkins MW, Tyler JK (2006) Transcriptional activators are dispensable for transcription in the absence of Spt6-mediated chromatin reassembly of promoter regions. Mol Cell 21(3): 405–16. Erratum in: Mol Cell 22(1): 147–148.
[59]  Adkins MW, Howar SR, Tyler JK (2004) Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes. Mol Cell 14(5): 657–666.
[60]  Schermer UJ, Korber P, Horz W (2005) Histones are incorporated in trans during reassembly of the yeast PHO5 promoter. Mol Cell 19(2): 279–285.
[61]  Kaplan CD, Morris JR, Wu C, Winston F (2000) Spt5 and spt6 are associated with active transcription and have characteristics of general elongation factors in D. melanogaster. Genes Dev 14(20): 2623–2634.
[62]  Andrulis ED, Guzman E, Doring P, Werner J, Lis JT (2000) High-resolution localization of Drosophila Spt5 and Spt6 at heat shock genes in vivo: roles in promoter proximal pausing and transcription elongation. Genes Dev 14(20): 2635–2649.
[63]  Mito Y, Henikoff JG, Henikoff S (2007) Histone replacement marks the boundaries of cis-regulatory domains. Science 315(5817): 1408–1411.
[64]  Malik HS, Henikoff S (2003) Phylogenomics of the nucleosome. Nat Struct Biol 10(11): 882–891.
[65]  Cui B, Liu Y, Gorovsky MA (2006) Deposition and function of histone H3 variants in Tetrahymena thermophila. Mol Cell Biol 26(20): 7719–7730.
[66]  Ooi SL, Priess JR, Henikoff S (2006) Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans. PLoS Genet 2(6): 97.
[67]  Ingouff M, Hamamura Y, Gourgues M, Higashiyama T, Berger F (2007) Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr Biol 17(12): 1032–1037.
[68]  Zhang R, Liu ST, Chen W, Bonner M, Pehrson J, Yen TJ, Adams PD (2007) HP1 proteins are essential for a dynamic nuclear response that rescues the function of perturbed heterochromatin in primary human cells. Mol Cell Biol 27(3): 949–962.
[69]  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(2): 251–258.
[70]  Zhang R, Chen W, Adams PD (2007) Molecular dissection of formation of senescence-associated heterochromatin foci. Mol Cell Biol 27(6): 2343–2358.
[71]  Nagamori I, Yomogida K, Adams PD, Sassone-Corsi P, Nojima H (2006) Transcription factors, cAMP-responsive element modulator (CREM) and Tisp40, act in concert in postmeiotic transcriptional regulation. J Biol Chem 281(22): 15073–15081.
[72]  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(5841): 1087–1090.

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