Paternal DNA packaging in spermatozoa: More than the sum of its parts? DNA, histones, protamines and epigenetics

Reproduction

Volumn 139, Issue 2, 2010, Pages 287-301

  Miller, David ^a   Brinkworth, Martin ^b   Iles, David ^c  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF BRADFORD   (United Kingdom)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE; PROTAMINE;

CHROMATIN; CLINICAL RESEARCH; DNA PACKAGING; EMBRYO DEVELOPMENT; EPIGENETICS; HUMAN; MAMMAL; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; REVIEW; SPERM; SPERMATOGENESIS; SPERMATOZOON;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC CODE; GENOMIC IMPRINTING; HISTONES; HUMANS; MALE; NUCLEOSOMES; PATERNITY; PROTAMINES; SPERM-OVUM INTERACTIONS; SPERMATOGENESIS; SPERMATOZOA;

EUTHERIA; MAMMALIA;

EID: 75149161556     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-09-0281     Document Type: Review

References (143)

1. Aitken RJ & De Iuliis GN 2007 Origins and consequences of DNA damage in male germ cells. Reproductive Biomedicine Online 14 727-733.
2. Albrethsen J, Knol JC & Jimenez CR 2009 Unravelling the nuclear matrix proteome. Journal of Proteomics 72 71-81.
3. Allen MJ, Bradbury EM & Balhorn R 1996 The chromatin structure of wellspread demembranated human sperm nuclei revealed by atomic force microscopy. Scanning Microscopy 10 989-994 (discussion 986-994).
4. Aoki F, Worrad DM & Schultz RM 1997 Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Developmental Biology 181 296-307.
5. Aoki VW, Moskovtsev SI, Willis J, Liu L, Mullen JB & Carrell DT 2005 DNA integrity is compromised in protamine-deficient human sperm. Journal of Andrology 26 741-748.
6. Aoki VW, Emery BR, Liu L & Carrell DT 2006a Protamine levels vary between individual sperm cells of infertile human males and correlate with viability and DNA integrity. Journal of Andrology 27 890-898.
7. Aoki VW, Liu L, Jones KP, Hatasaka HH, Gibson M, Peterson CM & Carrell DT 2006b Sperm protamine 1/protamine 2 ratios are related to in vitro fertilization pregnancy rates and predictive of fertilization ability. Fertility and Sterility 86 1408-1415.
8. Arpanahi A, Brinkworth M, Iles D, Krawetz SA, Paradowska A, Platts AE, Saida M, Steger K, Tedder P & Miller D 2009 Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Research 19 1338-1349.
9. Ausio J, Eirin-Lopez JM & Frehlick LJ 2007 Evolution of vertebrate chromosomal sperm proteins: implications for fertility and sperm competition. Society of Reproduction and Fertility Supplement 65 63-79.
10. Balen AH 2008 Infertility - epidemiology, diagnosis, counseling. In Infertility in Practice, 3 edn, pp 1-122. Eds AH Balen & HS Jacobs. London: Informa Healthcare.
11. Balhorn R 2007 The protamine family of sperm nuclear proteins. Genome Biology 8 227.
12. Balhorn R, Gledhill BL & Wyrobek AJ 1977 Mouse sperm chromatin proteins: quantitative isolation and partial characterization. Biochemistry 16 4074-4080.
13. Banerjee S & Smallwood A 1995 A chromatin model of IGF2/H19 imprinting. Nature Genetics 11 237-238.
14. Barboro P, D'Arrigo C, Mormino M, Coradeghini R, Parodi S, Patrone E & Balbi C 2003 An intranuclear frame for chromatin compartmentalization and higher-order folding. Journal of Cellular Biochemistry 88 113-120.
15. Barreau C, Benson E, Gudmannsdottir E, Newton F & White-Cooper H 2008 Post-meiotic transcription in Drosophila testes. Development 135 1897-1902.
16. Belokopytova IA, Kostyleva EI, Tomilin AN & Vorob'ev VI 1993 Human male infertility may be due to a decrease of the protamine P2 content in sperm chromatin. Molecular Reproduction and Development 34 53-57.
17. Bench GS, Friz AM, Corzett MH, Morse DH & Balhorn R 1996 DNA and total protamine masses in individual sperm from fertile mammalian subjects. Cytometry 23 263-271.
18. Benchaib M, Braun V, Ressnikof D, Lornage J, Durand P, Niveleau A & Guerin JF 2005 Influence of global sperm DNA methylation on IVF results. Human Reproduction 20 768-773.
19. de Boer P, Redi CA, Garagna S & Winking H 1990 Protamine amount and cross linking in mouse teratospermatozoa and aneuploid spermatozoa. Molecular Reproduction and Development 25 297-301.
20. Braun RE 2001 Packaging paternal chromosomes with protamine. Nature Genetics 28 10-12.
21. Brewer LR, Corzett M & Balhorn R 1999 Protamine-induced condensation and decondensation of the same DNA molecule. Science 286 120-123.
22. Brewer L, Corzett M, Lau EY & Balhorn R 2003 Dynamics of protamine 1 binding to single DNA molecules. Journal of Biological Chemistry 278 42403-42408.
23. Bryan PN, Wright EB & Olins DE 1979 Core nucleosomes by digestion of reconstructed histone - DNA complexes. Nucleic Acids Research 6 1449-1465.
24. Chambeyron S & Bickmore WA 2004 Does looping and clustering in the nucleus regulate gene expression? Current Opinion in Cell Biology 16 256-262.
25. Cho C, Willis WD, Goulding EH, Jung-Ha H, Choi YC, Hecht NB & Eddy EM 2001 Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nature Genetics 28 82-86.
26. Chong S & Whitelaw E 2004 Epigenetic germline inheritance. Current Opinion in Genetics & Development 14 692-696.
27. Churikov D, Zalenskaya IA & Zalensky AO 2004a Male germline-specific histones in mouse and man. Cytogenetic and Genome Research 105 203-214.
28. Churikov D, Siino J, Svetlova M, Zhang K, Gineitis A, Morton Bradbury E & Zalensky A 2004b Novel human testis-specific histone H2B encoded by the interrupted gene on the X chromosome. Genomics 84 745-756.
29. Davie JR & Saunders CA 1981 Chemical composition of nucleosomes among domains of calf thymus chromatin differing in micrococcal nuclease accessibility and solubility properties. Journal of Biological Chemistry 256 12574-12580.
30. Delaval K, Govin J, Cerqueira F, Rousseaux S, Khochbin S & Feil R 2007 Differential histone modifications mark mouse imprinting control regions during spermatogenesis. EMBO Journal 26 720-729.
31. Dixon GH 1972 The basic proteins of trout testis chromatin: aspects of their synthesis, post-synthetic modifications and binding to DNA. Acta Endocrinologica Supplementum (Copenhagen) 168 130-154.
32. Dorus S, Busby SA, Gerike U, Shabanowitz J, Hunt DF & Karr TL 2006 Genomic and functional evolution of the Drosophila melanogaster sperm proteome. Nature Genetics 38 1440-1445.
33. Dym M & Fawcett DW 1971 Further observations on the numbers of spermatogonia, spermatocytes, and spermatids connected by intercellular bridges in the mammalian testis. Biology of Reproduction 4 195-215.
34. Farthing CR, Ficz G, Ng RK, Chan CF, Andrews S, Dean W, Hemberger M & Reik W 2008 Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLoS Genetics 4 e1000116.
35. Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, Bonner WM, Manova K, Burgoyne P & Nussenzweig A 2003 H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Developmental Cell 4 497-508.
36. Gardiner-Garden M, Ballesteros M, Gordon M & Tam PP 1998 Histoneand protamine-DNA association: conservation of different patterns within the b-globin domain in human sperm. Molecular and Cellular Biology 18 3350-3356.
37. Gatewood JM, Cook GR, Balhorn R, Bradbury EM & Schmid CW 1987 Sequence-specific packaging of DNA in human sperm chromatin. Science 236 962-964.
38. Gatewood JM, Cook GR, Balhorn R, Schmid CW & Bradbury EM 1990 Isolation of 4 core histones from human sperm chromatin representing a minor subset of somatic histones. Journal of Biological Chemistry 265 20662-20666.
39. Gillies EA, Cannon RM, Green RB & Pacey AA 2009 Hydrodynamic propulsion of human sperm. Journal of Fluid Mechanics 625 445-474.
40. Golan R, Cooper TG, Oschry Y, Oberpenning F, Schulze H, Shochat L & Lewin LM 1996 Changes in chromatin condensation of human spermatozoa during epididymal transit as determined by flow cytometry. Human Reproduction 11 1457-1462.
41. Govin J, Escoffier E, Rousseaux S, Kuhn L, Ferro M, Thevenon J, Catena R, Davidson I, Garin J, Khochbin S et al. 2007 Pericentric heterochromatin reprogramming by new histone variants during mouse spermiogenesis. Journal of Cell Biology 176 283-294.
42. Grimes SR Jr & Henderson N 1983 Acetylation of histones during spermatogenesis in the rat. Archives of Biochemistry and Biophysics 221 108-116.
43. Gusse M & Chevaillier P 1980a Electron microscope evidence for the presence of globular structures in different sperm chromatins. Journal of Cell Biology 87 280-284.
44. Gusse M & Chevaillier P 1980b Molecular structure of chromatin during sperm differentiation of the dogfish Scyliorhinus caniculus (L). Chromosoma 77 57-68.
45. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT & Cairns BR 2009 Distinctive chromatin in human sperm packages genes for embryo development. Nature 460 473-478.
46. Hancock R 2000 A new look at the nuclear matrix. Chromosoma 109 219-225.
47. Haraguchi CM, Mabuchi T, Hirata S, Shoda T, Hoshi K, Akasaki K & Yokota S 2005 Chromatoid bodies: aggresome-like characteristics and degradation sites for organelles of spermiogenic cells. Journal of Histochemistry and Cytochemistry 53 455-465.
48. Hazzouri M, Rousseaux S, Mongelard F, Usson Y, Pelletier R, Faure AK, Vourc'h C & Sele B 2000 Genome organization in the human sperm nucleus studied by FISH and confocal microscopy. Molecular Reproduction and Development 55 307-315.
49. Heard E & Bickmore W 2007 The ins and outs of gene regulation and chromosome territory organisation. Current Opinion in Cell Biology 19 311-316.
50. van der Heijden GW, Derijck AA, Ramos L, Giele M, van der Vlag J & de Boer P 2006 Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin. Developmental Biology 298 458-469.
51. van der Heijden GW, Ramos L, Baart EB, van den Berg IM, Derijck AA, van der Vlag J, Martini E & de Boer P 2008 Sperm-derived histones contribute to zygotic chromatin in humans. BMC Developmental Biology 8 34.
52. Houshdaran S, Cortessis VK, Siegmund K, Yang A, Laird PW & Sokol RZ 2007 Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm. PLoS ONE 2 e1289.
53. Huang HF & Nieschlag E 1984 Alteration of free sulphydryl content of rat sperm heads by suppression of intratesticular testosterone. Journal of Reproduction and Fertility 70 31-38.
54. Hud NV, Allen MJ, Downing KH, Lee J & Balhorn R 1993 Identification of the elemental packing unit of DNA in mammalian sperm cells by atomic force microscopy. Biochemical and Biophysical Research Communications 193 1347-1354.
55. Huebert DJ, Kamal M, O'Donovan A & Bernstein BE 2006 Genomewide analysis of histone modifications by ChIP-on-chip. Methods 40 365-369.
56. Iarovaia OV, Bystritskiy A, Ravcheev D, Hancock R & Razin SV 2004 Visualization of individual DNA loops and a map of loop domains in the human dystrophin gene. Nucleic Acids Research 32 2079-2086.
57. Joshi NV, Medina H, Colasante C & Osuna A 2000 Ultrastructural investigation of human sperm using atomic force microscopy. Archives of Andrology 44 51-57.
58. Kerjean A, Dupont JM, Vasseur C, Le Tessier D, Cuisset L, Paldi A, Jouannet P & Jeanpierre M 2000 Establishment of the paternal methylation imprint of the human H19 and MEST/PEG1 genes during spermatogenesis. Human Molecular Genetics 9 2183-2187.
59. Khor B, Bredemeyer AL, Huang CY, Turnbull IR, Evans R, Maggi LB Jr, White JM, Walker LM, Carnes K, Hess RA et al. 2006 Proteasome activator PA200 is required for normal spermatogenesis. Molecular and Cellular Biology 26 2999-3007.
60. Kim TH, Abdullaev ZK, Smith AD, Ching KA, Loukinov DI, Green RD, Zhang MQ, Lobanenkov VV & Ren B 2007 Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 128 1231-1245.
61. Kornberg RD 1974 Chromatin structure: a repeating unit of histones and DNA. Science 184 868-871.
62. Kotaja N, Bhattacharyya SN, Jaskiewicz L, Kimmins S, Parvinen M, Filipowicz W & Sassone-Corsi P 2006 The chromatoid body of male germ cells: similarity with processing bodies and presence of Dicer and microRNA pathway components. PNAS 103 2647-2652.
63. Kurtz K, Martinez-Soler F, Ausio J & Chiva M 2007 Acetylation of histone H4 in complex structural transitions of spermiogenic chromatin. Journal of Cellular Biochemistry 102 1432-1441.
64. Lee K, Haugen HS, Clegg CH & Braun RE 1995 Premature translation of protamine 1 mRNA causes precocious nuclear condensation and arrests spermatid differentiation in mice. PNAS 92 12451-12455.
65. Li T, Vu TH, Ulaner GA, Littman E, Ling JQ, Chen HL, Hu JF, Behr B, Giudice L & Hoffman AR 2005 IVF results in de novo DNA methylation and histone methylation at an Igf2-H19 imprinting epigenetic switch. Molecular Human Reproduction 11 631-640.
66. Li Z, Yang J & Huang H 2006 Oxidative stress induces H2AX phosphorylation in human spermatozoa. FEBS Letters 580 6161-6168.
67. Li Y, Lalancette C, Miller D & Krawetz SA 2008 Characterization of nucleohistone and nucleoprotamine components in the mature human sperm nucleus. Asian Journal of Andrology 10 535-541.
68. Lilley DM & Pardon JF 1979 Structure and function of chromatin. Annual Review of Genetics 13 197-233.
69. Loppin B, Bonnefoy E, Anselme C, Laurencon A, Karr TL & Couble P 2005 The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437 1386-1390.
70. Lucifero D, Mertineit C, Clarke HJ, Bestor TH & Trasler JM 2002 Methylation dynamics of imprinted genes in mouse germ cells. Genomics 79 530-538.
71. Ma H, Siegel AJ & Berezney R 1999 Association of chromosome territories with the nuclear matrix. Disruption of human chromosome territories correlates with the release of a subset of nuclear matrix proteins. Journal of Cell Biology 146 531-542.
72. Maier WM, Nussbaum G, Domenjoud L, Klemm U & Engel W 1990 The lack of protamine 2 (P2) in boar and bull spermatozoa is due to mutations within the P2 gene. Nucleic Acids Research 18 1249-1254.
73. Malo AF, Gomendio M, Garde J, Lang-Lenton B, Soler AJ & Roldan ER 2006 Sperm design and sperm function. Biology Letters 2 246-249.
74. Marchal R, Chicheportiche A, Dutrillaux B & Bernardino-Sgherri J 2004 DNA methylation in mouse gametogenesis. Cytogenetic and Genome Research 105 316-324.
75. Marques CJ, Costa P, Vaz B, Carvalho F, Fernandes S, Barros A & Sousa M 2008 Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Molecular Human Reproduction 14 67-74.
76. Martelli AM, Cocco L, Riederer BM & Neri LM 1996 The nuclear matrix: a critical appraisal. Histology and Histopathology 11 1035-1048.
77. Marushige K & Dixon GH 1971 Transformation of trout testis chromatin. Journal of Biological Chemistry 246 5799-5805.
78. McLay DW & Clarke HJ 2003 Remodelling the paternal chromatin at fertilization in mammals. Reproduction 125 625-633.
79. McKay DJ, Renaux BS & Dixon GH 1986 Rainbow trout protamines. Amino acid sequences of six distinct proteins from a single testis. European Journal of Biochemistry 158 361-366.
80. Meistrich ML, Bucci LR, Trostle-Weige PK & Brock WA 1985 Histone variants in rat spermatogonia and primary spermatocytes. Developmental Biology 112 230-240.
81. Miller D 2007 Ensuring continuity of the paternal genome: potential roles for spermatozoal RNA in mammalian embryogenesis. Society of Reproduction and Fertility Supplement 65 373-389.
82. Miller D & Ostermeier GC 2006 Towards a better understanding of RNA carriage by ejaculate spermatozoa. Human Reproduction 12 757-767.
83. Mohar I, Szczygiel MA, Yanagimachi R & Ward WS 2002 Sperm nuclear halos can transform into normal chromosomes after injection into oocytes. Molecular Reproduction and Development 62 416-420.
84. Moreno Diaz de la Espina S, Alverca E, Cuadrado A & Franca S 2005 Organization of the genome and gene expression in a nuclear environment lacking histones and nucleosomes: the amazing dinoflagellates. European Journal of Cell Biology 84 137-149.
85. Moulson CL, Fong LG, Gardner JM, Farber EA, Go G, Passariello A, Grange DK, Young SG & Miner JH 2007 Increased progerin expression associated with unusual LMNA mutations causes severe progeroid syndromes. Human Mutation 28 882-889.
86. Munshi A, Shafi G, Aliya N & Jyothy A 2009 Histone modifications dictate specific biological readouts. Journal of Genetics and Genomics 36 75-88.
87. Nadel B, de Lara J, Finkernagel SW & Ward WS 1995 Cell-specific organization of the 5S ribosomal RNA gene cluster DNA loop domains in spermatozoa and somatic cells. Biology of Reproduction 53 1222-1228.
88. Nazarov IB, Shlyakhtenko LS, Lyubchenko YL, Zalenskaya IA & Zalensky AO 2008 Sperm chromatin released by nucleases. Systems Biology in Reproductive Medicine 54 37-46.
89. Nickel BE, Roth SY, Cook RG, Allis CD & Davie JR 1987 Changes in the histone H2A variant H2A.Z and polyubiquitinated histone species in developing trout testis. Biochemistry 26 4417-4421.
90. Ohlsson R, Renkawitz R & Lobanenkov V 2001 CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends in Genetics 17 520-527.
91. Olins AL & Olins DE 1974 Spheroid chromatin units (v bodies). Science 183 330-332.
92. Oliva R 2006 Protamines and male infertility. Human Reproduction Update 12 417-435.
93. Olivares C, Lila Vera M & Ruiz-Lara S 1993 Coexistence of two chromatin structures in sperm nuclei of the bivalve mollusc Protothaca thaca. Molecular and Cellular Biochemistry 125 87-95.
94. Ooi SL & Henikoff S 2007 Germline histone dynamics and epigenetics. Current Opinion in Cell Biology 19 257-265.
95. Ostermeier GC, Sargeant GA, Yandell BS, Evenson DP & Parrish JJ 2001 Relationship of bull fertility to sperm nuclear shape. Journal of Andrology 22 595-603.
96. Palmer DK, O'Day K & Margolis RL 1990 The centromere specific histone CENP-A is selectively retained in discrete foci in mammalian sperm nuclei. Chromosoma 100 32-36.
97. Paterson L, DeSousa P, Ritchie W, King T & Wilmut I 2003 Application of reproductive biotechnology in animals: implications and potentials. Applications of reproductive cloning. Animal Reproduction Science 79 137-143.
98. Philippe M & Chevaillier P 1978 Extraction and biochemical characterization of a nuclear deoxyribonucleic acid polymerase activity in bull spermatozoa. Biochemical Journal 175 585-594.
99. Pittoggi C, Renzi L, Zaccagnini G, Cimini D, Degrassi F, Giordano R, Magnano AR, Lorenzini R, Lavia P & Spadafora C 1999 A fraction of mouse sperm chromatin is organized in nucleosomal hypersensitive domains enriched in retroposon DNA. Journal of Cell Science 112 3537-3548.
100. Pivot-Pajot C, Caron C, Govin J, Vion A, Rousseaux S & Khochbin S 2003 Acetylation-dependent chromatin reorganization by BRDT, a testisspecific bromodomain-containing protein. Molecular and Cellular Biology 23 5354-5365.
101. Poccia DL, Simpson MV & Green GR 1987 Transitions in histone variants during sea urchin spermatogenesis. Developmental Biology 121 445-453.
102. Puwaravutipanich T & Panyim S 1975 The nuclear basic proteins of human testes and ejaculated spermatozoa. Experimental Cell Research 90 153-158.
103. Queralt R, Adroer R, Oliva R, Winkfein RJ, Retief JD & Dixon GH 1995 Evolution of protamine P1 genes in mammals. Journal of Molecular Evolution 40 601-607.
104. Ramos L, van der Heijden GW, Derijck A, Berden JH, Kremer JA, van der Vlag J & de Boer P 2008 Incomplete nuclear transformation of human spermatozoa in oligo-astheno-teratospermia: characterization by indirect immunofluorescence of chromatin and thiol status. Human Reproduction 23 259-270.
105. Rathke C, Baarends WM, Jayaramaiah-Raja S, Bartkuhn M, Renkawitz R & Renkawitz-Pohl R 2007 Transition from a nucleosome-based to a protamine-based chromatin configuration during spermiogenesis in Drosophila. Journal of Cell Science 120 1689-1700.
106. Razin SV, Iarovaia OV, Sjakste N, Sjakste T, Bagdoniene L, Rynditch AV, Eivazova ER, Lipinski M & Vassetzky YS 2007 Chromatin domains and regulation of transcription. Journal of Molecular Biology 369 597-607.
107. Roest HP, van Klaveren J, de Wit J, van Gurp CG, Koken MH, Vermey M, van Roijen JH, Hoogerbrugge JW, Vreeburg JT, Baarends WM et al. 1996 Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification. Cell 86 799-810.
108. Rousseaux S, Reynoird N, Escoffier E, Thevenon J, Caron C & Khochbin S 2008 Epigenetic reprogramming of the male genome during gametogenesis and in the zygote. Reproductive Biomedicine Online 16 492-503.
109. Rousseaux-Prevost R, Engelhardt RP, Rousseaux J, Wouters-Tyrou D & Sautiere P 1988 Nuclear protein transitions in cuttle-fish spermiogenesis: immunocytochemical localization of a protein specific for the spermatid stage. Gamete Research 19 277-290.
110. Sanders MM 1978 Fractionation of nucleosomes by salt elution from micrococcal nuclease-digested nuclei. Journal of Cell Biology 79 97-109.
111. Santos F, Peters AH, Otte AP, Reik W & Dean W 2005 Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Developmental Biology 280 225-236.
112. Schaefer CB, Ooi SK, Bestor TH & Bourc'his D 2007 Epigenetic decisions in mammalian germ cells. Science 316 398-399.
113. Sherwood PW, Tsang SV & Osley MA 1993 Characterization of HIR1 and HIR2, two genes required for regulation of histone gene transcription in Saccharomyces cerevisiae. Molecular and Cellular Biology 13 28-38.
114. Shirley CR, Hayashi S, Mounsey S, Yanagimachi R & Meistrich ML 2004 Abnormalities and reduced reproductive potential of spermfromTnp1- and Tnp2-null double mutant mice. Biology of Reproduction 71 1220-1229.
115. Sims RJ III & Reinberg D 2008 Is there a code embedded in proteins that is based on post-translational modifications? Nature Reviews. Molecular Cell Biology 9 815-820.
116. Sobhon P, Chutatape C, Chalermisarachai P, Vongpayabal P & Tanphaichitr N 1982 Transmission and scanning electron microscopic studies of the human sperm chromatin decondensed by micrococcal nuclease and salt. Journal of Experimental Zoology 221 61-79.
117. Solov'eva L, Svetlova M, Bodinski D & Zalensky AO 2004 Nature of telomere dimers and chromosome looping in human spermatozoa. Chromosome Research 12 817-823.
118. Soon LL, Ausio J, Breed WG, Power JH & Muller S 1997 Isolation of histones and related chromatin structures from spermatozoa nuclei of a dasyurid marsupial, Sminthopsis crassicaudata. Journal of Experimental Zoology 278 322-332.
119. Steger K 1999 Transcriptional and translational regulation of gene expression in haploid spermatids. Anatomy and Embryology 199 471-487.
120. Steger K, Fink L, Failing K, Bohle RM, Kliesch S,Weidner W & Bergmann M 2003 Decreased protamine-1 transcript levels in testes from infertile men. Molecular Human Reproduction 9 331-336.
121. Surani MA & Barton SC 1983 Development of gynogenetic eggs in the mouse: implications for parthenogenetic embryos. Science 222 1034-1036.
122. Sutovsky P, McCauley TC, Sutovsky M & Day BN 2003 Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG132. Biology of Reproduction 68 1793-1800.
123. Tanphaichitr N, Sobhon P, Taluppeth N & Chalermisarachai P 1978 Basic nuclear proteins in testicular cells and ejaculated spermatozoa in man. Experimental Cell Research 117 347-356.
124. Tomsu M, Sharma V & Miller D 2002 Embryo quality and IVF treatment outcomes may correlate with different sperm comet assay parameters. Human Reproduction 17 1856-1862.
125. Tovich PR & Oko RJ 2003 Somatic histones are components of the perinuclear theca in bovine spermatozoa. Journal of Biological Chemistry 278 32431-32438.
126. Trasler JM 1998 Origin and roles of genomic methylation patterns in male germ cells. Seminars in Cell and Developmental Biology 9 467-474.
127. Trostle-Weige PK, Meistrich ML, Brock WA & Nishioka K 1984 Isolation and characterization of TH3, a germ cell-specific variant of histone 3 in rat testis. Journal of Biological Chemistry 259 8769-8776.
128. Wan LB, Pan H, Hannenhalli S, Cheng Y, Ma J, Fedoriw A, Lobanenkov V, Latham KE, Schultz RM & Bartolomei MS 2008 Maternal depletion of CTCF reveals multiple functions during oocyte and preimplantation embryo development. Development 135 2729-2738.
129. Ward WS, Kimura Y & Yanagimachi R 1999 An intact sperm nuclear matrix may be necessary for the mouse paternal genome to participate in embryonic development. Biology of Reproduction 60 702-706.
130. Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, Rebhan M & Schubeler D 2007 Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nature Genetics 39 457-466.
131. Wilming LG, Snoeren CA, van Rijswijk A, Grosveld F & Meijers C 1997 The murine homologue of HIRA, a DiGeorge syndrome candidate gene, is expressed in embryonic structures affected in human CATCH22 patients. Human Molecular Genetics 6 247-258.
132. Wu Q, Kumagai T, Kawahara M, Ogawa H, Hiura H, Obata Y, Takano R & Kono T 2006 Regulated expression of two sets of paternally imprinted genes is necessary for mouse parthenogenetic development to term. Reproduction 131 481-488.
133. Wu F, Caron C, De Robertis C, Khochbin S & Rousseaux S 2008 Testisspecific histone variants H2AL1/2 rapidly disappear from paternal heterochromatin after fertilization. Journal of Reproduction and Development 54 413-417.
134. Wykes SM & Krawetz SA 2003 The structural organization of sperm chromatin. Journal of Biological Chemistry 278 29471-29477.
135. Yu YE, Zhang Y, Unni E, Shirley CR, Deng JM, Russell LD, Weil MM, Behringer RR & Meistrich ML 2000 Abnormal spermatogenesis and reduced fertility in transition nuclear protein 1-deficient mice. PNAS 97 4683-4688.
136. Zakeri ZF, Ponzetto C &Wolgemuth DJ 1988 Translational regulation of the novel haploid-specific transcripts for the C-Abl-proto-oncogene and a member of the 70 kDa heat-shock protein gene family in the male germ line. Developmental Biology 125 417-422.
137. Zalenskaya IA, Pospelov VA, Zalensky AO & Vorob'ev VI 1981 Nucleosomal structure of sea urchin and starfish sperm chromatin. Histone H2B is possibly involved in determining the length of linker DNA. Nucleic Acids Research 9 473-487.
138. Zalenskaya IA, Bradbury EM & Zalensky AO 2000 Chromatin structure of telomere domain in human sperm. Biochemical and Biophysical Research Communications 279 213-218.
139. Zalensky AO, Allen MJ, Kobayashi A, Zalenskaya IA, Balhorn R & Bradbury EM 1995 Well-defined genome architecture in the human sperm nucleus. Chromosoma 103 577-590.
140. Zalensky AO, Siino JS, Gineitis AA, Zalenskaya IA, Tomilin NV, Yau P & Bradbury EM 2002 Human testis/sperm-specific histone H2B (hTSH2B). Molecular cloning and characterization. Journal of Biological Chemistry 277 43474-43480.
141. Zentgraf H & Franke WW 1984 Differences of supranucleosomal organization in different kinds of chromatin: cell type-specific globular subunits containing different numbers of nucleosomes. Journal of Cell Biology 99 272-286.
142. Zhao M, Shirley CR, Yu YE, Mohapatra B, Zhang Y, Unni E, Deng JM, Arango NA, Terry NH, Weil MM et al. 2001 Targeted disruption of the transition protein 2 gene affects sperm chromatin structure and reduces fertility in mice. Molecular and Cellular Biology 21 7243-7255.
143. Zhao M, Shirley CR, Hayashi S, Marcon L, Mohapatra B, Suganuma R, Behringer RR, Boissonneault G, Yanagimachi R & Meistrich ML 2004 Transition nuclear proteins are required for normal chromatin condensation and functional sperm development. Genesis 38 200-213.