Abstract
Chromatin constitution in the male germ line of Drosophila is discussed with respect to the substitution of somatic histones by protamines or other basic proteins. The specific properties of germ line chromatin include the initiation and completion of the spermatogenic pathway and the reprogramming of the genome for embryonic development. During meiotic prophase cell cycle-regulated H3 histones appear to a large extent to be substituted by the histone H3.3 replacement variant protein, which is generally found associated with transcriptionally active chromatin. Condensation of the chromosomes during meiosis and the subsequent compaction for packaging in the sperm head require suitable proteins, but the cell cycle-regulated histones are not available as their expression is limited to S-phase. It is, therefore, proposed that any basic protein with a limited range of sequence requirements may take over this packaging function. Suitable proteins may have evolved by divergence from histone variants not restricted in their expression to S-phase, similar to the testes-predominant histone H3.3A of Drosophila.
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References
Ahmad K, Henikoff S (2002a) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9:1191–1200
Ahmad K, Henikoff S (2002b) Histone H3 variants specify modes of chromatin assembly. Proc Natl Acad Sci U S A 99 Suppl 4:16477–16484
Allen MJ, Lee C, Lee JD (1993) Atomic force microscopy of mammalian sperm chromatin. Chromosoma 102:623–630
Ausió J (1999) Histone H1 and evolution of sperm nuclear basic proteins. J Biol Chem 274:31115–31118
Akhmanova AS, Bindels PC, Xu J, Miedema K, Kremer H, Hennig W (1995) Structure and expression of histone H3.3 genes in Drosophila melanogaster and Drosophila hydei. Genome 38:586–600
Akhmanova A, Miedema K, Wang Y, van Bruggen M, Berden JH, Moudrianakis EN, Hennig W (1997a) 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
Akhmanova A, Kremer H, Miedema K, Hennig W (1997b) Naturally occurring testis-specific histone H3 antisense transcripts in Drosophila. Mol Reprod Dev 48:413–420
Bassing CH, Chua KF, Sekiguchi J, Suh H, Whitlow SR, Fleming JC, Monroe BC, Ciccone DN, Yan C, Vlasakova K, Livingston DM, Ferguson DO, Scully R, Alt FW (2002) Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc Natl Acad Sci U S A 99:8173–8178
Bedford JM, Calvin HL (1974) The occurrence and possible functional significance of -S-S-crosslinks in sperm heads, with particular reference to eutherian mammals. J Exp Zool 188:137–155
Blümer N, Schreiter K, Hempel L, Santel A, Hollmann M, Schäfer MA, Renkawitz-Pohl R (2002) A new translational repression element and unusual transcriptional control regulate expression of don juan during Drosophila spermatogenesis. Mech Dev 110:97–112
Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, Sedelnikova OA, Reina-San-Martin B, Coppola V, Meffre E, Difilippantonio MJ, Redon C, Pilch DR, Olaru A, Eckhaus M, Camerini-Otero RD, Tessarollo L, Livak F, Manova K, Bonner WM, Nussenzweig MC, Nussenzweig A (2002) Genomic instability in mice lacking histone H2AX. Science 296:922–927
Eddy EM (2002) Male germ cell gene expression. Recent Prog Horn Res 57:103–128
Engel W, Keime S, Kremling H, Hameister H, Schlüter G (1992) The genes for protamine 1 and 2 (PRM1 and PRM2) and transition protein 2 (TNP2) are closely linked in the mammalian genome. Cytogenet Cell Genet 61:158–159
Goday C, Ruiz MF (2002) Differential acetylation of histones H3 and H4 in paternal and maternal germline chromosomes during development of sciarid flies. J Cell Sci 115:4765–4775
Hecht NB (1998) Molecular mechanisms of male germ cell differentiation. Bioassays 20:555–561
Hennig W (1967) Untersuchungen zur Struktur und Funktion des Lampenbürsten-Y-Chromosoms in der Spermatogenese von Drosophila. Chromosoma 22:294–357
Hennig W (2001) DNA packaging in sperm. In: Encyclopaedia of Life Sciences. Nature Publishing Group, London
Hill CS, Rimmer JM, Green BN, Finch JT, Thomas JO (1991) Histone-DNA interactions and their modulation by phosphorylation of -Ser-Pro-Lys/Arg-motifs. EMBO J 10:1939–1948
Huijser P, Kirchhoff C, Lankenau DH, Hennig W (1988) Retrotransposon-like sequences are expressed in Y chromosomal lampbrush loops of Drosophila hydei. J Mol Biol 203:689–697
Jamieson BGM (1987) The ultrastructure and phylogeny of insect spermatozoa. Cambridge University Press, Cambridge, UK
Jutglar L, Borerell JI, Ausió J (1991) Primary, secondary, and tertiary structure of the core of a histone H1-like protein from sperm of Mytilus. J Biol Chem 266:8184–8191
Kashiwabara S, Noguchi J, Zhuang T, Ohmura K, Honda A, Sugiura S, Miyamoto K, Takahashi S, Inoue K, Ogura A, Baba T (2002) Regulation of spermatogenesis by testis-specific, cytoplasmic poly(A) polymerase TPAP. Science 298:1999–2002
Kettaneh NP, Hartl DL (1976) Histone transition during spermiogenesis is absent in segregation distorter males of Drosophila melanogaster. Sciencel 93:1020–1201
Kimura Y, Yanagimachi R (1995) Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development 121:2397–2405
Kremer H, Hennig W, Dijkhof R (1986) Chromatin organization in the male germ line of Drosophila hydei. Chromosoma 94:147–161
Lankenau S, Corces VG, Lankenau DH (1994) The Drosophila micropia retrotransposon encodes a testis-specific antisense RNA complementary to reverse transcriptase. Mol Cell Biol 14:1764–1775
Li E (2002) Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 3:662–673
Maleszewski M, Kuretake S, Evenson D, Yanagimachi H, Bjordahl J, Yanagimachi R (1998) Behavior of transgenic mouse spermatozoa with galline protamine. Biol Reprod 58:8–14
McPherson S, Longo FJ (1993) Chromatin structure-function alterations during mammalian spermatogenesis: DNA nicking and repair in elongating spermatids. Eur J Histochem 37:109–128
Meistrich M (1989) Histone and basic nuclear protein transition in mammalian spermatogenesis. In: Hnilica LS, Stein GS, Stein JL (eds) Histones and other basic nuclear proteins. CRC Press, Orlando, pp 165–182
Nasmyth K (2002) Segregating sister genomes: the molecular biology of chromosome separation. Science 297:559–565
Oliva R, Dixon GH (1991) Vertebrate protamine genes and the histone-to-protamine replacement reaction. Prog Nucleic Acid Res Mol Biol 40:25–94
Pienta KJ, Coffey DS (1984) Structural analysis of the role of nuclear matrix and DNA loops in the organization of the nucleus and chromosome. J Cell Sci Suppl 1:123–135
Poccia DL, Green GR (1992) Packaging and unpackaging the sea urchin sperm genome. Trends Biochem Sci 17:223–227
Rocchini C, Zhang F, Ausió J (1995) Two highly specialized histone H1 proteins are the major chromosomal proteins of the sperm of the sea anemone Urticina (Tealia) crassicornis. Biochemistry 34:15704–15712
Roth SY, Allis CD (1992) Chromatin condensation: does histone H1 dephosphorylation play a role? Trend Biochem Sci 17:93–98
Santi S, Rubbini S, Cinti C, et al (1994) Nuclear matrix involved in sperm head structural organization. Biol Cell 81:47–57
van der Schans GP, Haring R, van Dijk-Knijnenburg HC, Bruijnzeel PL, den Daas NH (2000) An immunochemical assay to detect DNA damage in bovine sperm. J Androl 21:250–257
Waterborg JH (1993) Histone synthesis and turnover in alfalfa. Fast loss of highly acetylated replacement histone variant H3.2. J Biol Chem 268:4912–4917
Wouters-Tyrou D, Martinage A, Chevaillier P, Sautiere P (1998) Nuclear basic proteins in spermatogenesis. Biochimie 80:117–128
Yelick PC, Kwon YH, Flynn JF, Borzorgzadeh A, Kleene KC, Hecht NB (1989) Mouse transition protein 1 is translationally regulated during the postmeiotic stages of spermatogenesis. Mol Reprod Dev 1:193–200
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This paper is dedicated to Guenther F. Meyer in memory of the many years of our cooperation
Published online: 28 March 2003
Guest Editor. J. Ausió
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Hennig, W. Chromosomal proteins in the spermatogenesis of Drosophila . Chromosoma 111, 489–494 (2003). https://doi.org/10.1007/s00412-003-0236-6
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DOI: https://doi.org/10.1007/s00412-003-0236-6