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Sperm Chromatin: An Overview

Chapter

Abstract

The dramatic changes in the structure and function of sperm chromatin that occur during spermatogenesis have continued to intrigue researchers for more than a century. In addition to wanting to understand how these changes in chromatin organization affect genome function, many of the studies conducted in placental mammals have been driven by a desire to understand the relationship between sperm chromatin organization and sperm function (fertility) or dysfunction (subfertility or infertility). While we have learned a great deal, many important questions still remain unanswered. Major technological advances in imaging techniques, transgenic animal production, gene function disruption, molecular and compositional analysis at the single cell and subcellular level as well as the development of many new molecular probes now make it possible to design and carry out studies that examine structure and function at the level of the individual cell in ways that have not been previously possible.

Keywords

Sperm chromatin Spermatogenesis Chromatin remodeling DNA–protamine complex Chromatin reorganization 

References

  1. 1.
    Mendel G. Experiment in plant hybribization. Paper presented at: Brunn Natural History Society; March, 1865, 1865; Brunn, Czechoslovakia.Google Scholar
  2. 2.
    Haeckel E. Generelle Morphologie der Organismen. Berlin: Reimer; 1866.Google Scholar
  3. 3.
    Miescher F. Letter I to Wilhelm His; Tubingen, February 26th, 1869. In: His W, ed. Die Histochemischen und Physiologischen Arbeiten von Friedrich Miescher – Aus dem sissenschaft – lichen Briefwechsel von F. Miescher. Vol 1. Liepzig: F. C. W. Vogel; 1869:pp. 33–8.Google Scholar
  4. 4.
    Miescher F. Uber die chemische Zusammensetzung der Eiter – zellen. Med Chem Unters. 1871;4:441–60.Google Scholar
  5. 5.
    Flemming W. Uber das Verhalten des Kern bei der Zellltheilung und uber dei Bedeutung mekrkerniger Zellen. Arch Pathol Anat Physiol. 1879;77:1–29.Google Scholar
  6. 6.
    Miescher F. Das Protamin – Eine neue organishe Basis aus den Samenssden des Rheinlachses. Ber Dtesch Chem Ges. 1874;7:376.Google Scholar
  7. 7.
    Kossel A. Ueber die Constitution der einfachsten Eiweissstoffe. Z Pysiologische Chemie. 1898;25:165–89.Google Scholar
  8. 8.
    Kossel A, Dakin HD. Uber Salmin und Clupein. Z Pysiologische Chemie. 1904;41:407–15.Google Scholar
  9. 9.
    Kossel A, Dakin HD. Weitere Beitrage zum System der einfachsten Eiweisskorper. Z Pysiologische Chemie. 1905;44:342–6.Google Scholar
  10. 10.
    Kossel A, Edlbacher F. Uber einige Spaltungsprodukte des Thynnins und Pereins. Z Pysiologische Chemie. 1913;88:186–9.Google Scholar
  11. 11.
    Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet. 2001;2(1):21–32.PubMedGoogle Scholar
  12. 12.
    Solter D. Differential imprinting and expression of maternal and paternal genomes. Annu Rev Genet. 1988;22:127–46.PubMedGoogle Scholar
  13. 13.
    Gartler SM, Goldman MA. X-chromosome inactivation, Encyclopedia of life. New York: Wiley Interscience; 2005. p. 1–6.Google Scholar
  14. 14.
    Heard E, Clerc P, Avner P. X-chromosome inactivation in mammals. Annu Rev Genet. 1997;31:571–610.PubMedGoogle Scholar
  15. 15.
    Ney PA. Gene expression during terminal erythroid differentiation. Curr Opin Hematol. 2006;13(4):203–8.PubMedGoogle Scholar
  16. 16.
    Berlowitz L. Chromosomal inactivation and reactivation in mealy bugs. Genetics. 1974;78(1):311–22.PubMedGoogle Scholar
  17. 17.
    Bloch D. Handbook of Genetics, vol. 5. New York: Plenum Press; 1976.Google Scholar
  18. 18.
    Palau J, Ruiz-Carrillo A, Subirana JA. Histones from sperm of the sea urchin Arbacia lixula. Eur J Biochem. 1969;7(2):209–13.PubMedGoogle Scholar
  19. 19.
    Eirin-Lopez JM, Ausio J. Origin and evolution of chromosomal sperm proteins. Bioessays. 2009;31(10):1062–70.PubMedGoogle Scholar
  20. 20.
    Kasinsky HE, Huang SY, Mann M, Roca J, Subirana JA. On the diversity of sperm histones in the ­vertebrates: IV. Cytochemical and amino acid ­analysis in Anura. J Exp Zool. 1985;234(1):33–46.PubMedGoogle Scholar
  21. 21.
    Mann M, Risley MS, Eckhardt RA, Kasinsky HE. Characterization of spermatid/sperm basic chromosomal proteins in the genus Xenopus (Anura, Pipidae). J Exp Zool. 1982;222(2):173–86.PubMedGoogle Scholar
  22. 22.
    Takamune K, Nishida H, Takai M, Katagiri C. Primary structure of toad sperm protamines and nucleotide sequence of their cDNAs. Eur J Biochem. 1991;196(2):401–6.PubMedGoogle Scholar
  23. 23.
    Su H. Characterization of nuclear basic proteins in sperm and erythrocytes of vertebrates. Vancouver: Department of Zoology, University of British Columbia; 2004.Google Scholar
  24. 24.
    Kadura SN, Khrapunov SN, Chabanny VN, Berdyshev GD. Changes in chromatin basic proteins during male gametogenesis of grass carp. Comp Biochem Physiol B. 1983;74(2):343–50.PubMedGoogle Scholar
  25. 25.
    Saperas N, Lloris D, Chiva M. Sporadic appearance of histones, histone-like proteins, and protamines in sperm chromatin of bony fish. J Exp Zool. 2005;265(5):575–86.Google Scholar
  26. 26.
    Kurtz K, Saperas N, Ausio J, Chiva M. Spermiogenic nuclear protein transitions and chromatin condensation. Proposal for an ancestral model of nuclear ­spermiogenesis. J Exp Zool B Mol Dev Evol. 2009;312B(3):149–63.PubMedGoogle Scholar
  27. 27.
    Ausio J. Histone H1 and evolution of sperm nuclear basic proteins. J Biol Chem. 1999;274(44):31115–8.PubMedGoogle Scholar
  28. 28.
    Kasinsky HE, Gutovich L, Kulak D, et al. Protamine-like sperm nuclear basic proteins in the primitive frog Ascaphus truei and histone reversions among more advanced frogs. J Exp Zool. 1999;284(7):717–28.PubMedGoogle Scholar
  29. 29.
    Saperas N, Chiva M, Pfeiffer DC, Kasinsky HE, Ausio J. Sperm nuclear basic proteins (SNBPs) of agnathans and chondrichthyans: variability and evolution of sperm proteins in fish. J Mol Evol. 1997;44(4):422–31.PubMedGoogle Scholar
  30. 30.
    Churikov D, Zalenskaya IA, Zalensky AO. Male germline-specific histones in mouse and man. Cytogenet Genome Res. 2004;105(2–4):203–14.PubMedGoogle Scholar
  31. 31.
    Oko RJ, Jando V, Wagner CL, Kistler WS, Hermo LS. Chromatin reorganization in rat spermatids ­during the disappearance of testis-specific histone, H1t, and the appearance of transition proteins TP1 and TP2. Biol Reprod. 1996;54(5):1141–57.PubMedGoogle Scholar
  32. 32.
    Kistler WS, Henriksen K, Mali P, Parvinen M. Sequential expression of nucleoproteins during rat spermiogenesis. Exp Cell Res. 1996;225(2):374–81.PubMedGoogle Scholar
  33. 33.
    Steger K, Klonisch T, Gavenis K, Drabent B, Doenecke D, Bergmann M. Expression of mRNA and protein of nucleoproteins during human spermiogenesis. Mol Hum Reprod. 1998;4(10):939–45.PubMedGoogle Scholar
  34. 34.
    Alfonso P, Kistler WS. Immunohistochemical localization of spermatid nuclear transition protein 2 in the testes of rats and mice. Biol Reprod. 1993;48(3):522–9.PubMedGoogle Scholar
  35. 35.
    Pradeepa MM, Rao MR. Chromatin remodeling ­during mammalian spermatogenesis: role of testis specific histone variants and transition proteins. Soc Reprod Fertil Suppl. 2007;63:1–10.PubMedGoogle Scholar
  36. 36.
    Caron N, Veilleux S, Boissonneault G. Stimulation of DNA repair by the spermatidal TP1 protein. Mol Reprod Dev. 2001;58(4):437–43.PubMedGoogle Scholar
  37. 37.
    Unni E, Zhang Y, Meistrich ML, Balhorn R. Rat spermatid basic nuclear protein Tp3 is the precursor of protamine 2. Exp Cell Res. 1994;210(1):39–45.PubMedGoogle Scholar
  38. 38.
    Queralt R, Adroer R, Oliva R, Winkfein RJ, Retief JD, Dixon GH. Evolution of protamine P1 genes in mammals. J Mol Evol. 1995;40(6):601–7.PubMedGoogle Scholar
  39. 39.
    Retief JD, Dixon GH. Evolution of pro-protamine P2 genes in primates. Eur J Biochem. 1993;214(2):609–15.PubMedGoogle Scholar
  40. 40.
    Retief JD, Krajewski C, Westerman M, Dixon GH. The evolution of protamine P1 genes in dasyurid marsupials. J Mol Evol. 1995;41(5):549–55.PubMedGoogle Scholar
  41. 41.
    Retief JD, Krajewski C, Westerman M, Winkfein RJ, Dixon GH. Molecular phylogeny and evolution of marsupial protamine P1 genes. Proc Biol Sci. 1995;259(1354):7–14.PubMedGoogle Scholar
  42. 42.
    Cree LH, Balhorn R, Brewer LR. Single molecule studies of DNA-protamine interactions. Protein Pept Lett. 2011;18(8):802–­10.Google Scholar
  43. 43.
    Bench GS, Friz AM, Corzett MH, Morse DH, Balhorn R. DNA and total protamine masses in individual sperm from fertile mammalian subjects. Cytometry. 1996;23(4):263–71.PubMedGoogle Scholar
  44. 44.
    Gatewood JM, Cook GR, Balhorn R, Schmid CW, Bradbury EM. Isolation of four core histones from human sperm chromatin representing a minor subset of somatic histones. J Biol Chem. 1990;265(33):20662–6.PubMedGoogle Scholar
  45. 45.
    Gusse M, Sautière P, Bélaiche D, et al. Purification and characterization of nuclear basic proteins of human sperm. Biochim Biophys Acta. 1986;884(1):124–34.PubMedGoogle Scholar
  46. 46.
    Tanphaichitr N, Sobhon P, Taluppeth N, Chalermisarachai P. Basic nuclear proteins in testicular cells and ejaculated spermatozoa in man. Exp Cell Res. 1978;117(2):347–56.PubMedGoogle Scholar
  47. 47.
    Wykes SM, Krawetz SA. The structural organization of sperm chromatin. J Biol Chem. 2003;278(32):29471–7.PubMedGoogle Scholar
  48. 48.
    Zalenskaya IA, Zalensky AO. Non-random positioning of chromosomes in human sperm nuclei. Chromosome Res. 2004;12(2):163–73.PubMedGoogle Scholar
  49. 49.
    Gardiner-Garden M, Ballesteros M, Gordon M, Tam PP. Histone- and protamine-DNA association: conservation of different patterns within the beta-globin domain in human sperm. Mol Cell Biol. 1998;18(6):3350–6.PubMedGoogle Scholar
  50. 50.
    Banerjee S, Smallwood A. Chromatin modification of imprinted H19 gene in mammalian spermatozoa. Mol Reprod Dev. 1998;50(4):474–84.PubMedGoogle Scholar
  51. 51.
    Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. Distinctive chromatin in human sperm packages genes for embryo development. Nature. 2009;460(7254):473–8.PubMedGoogle Scholar
  52. 52.
    Lin M, Jones RC. Spermiogenesis and spermiation in a monotreme mammal, the platypus, Ornitho­rhynchus anatinus. J Anat. 2000;196(Pt 2):217–32.PubMedGoogle Scholar
  53. 53.
    Soon LL, Bottema C, Breed WG. Atomic force microscopy and cytochemistry of chromatin from marsupial spermatozoa with special reference to Sminthopsis crassicaudata. Mol Reprod Dev. 1997;48(3):367–74.PubMedGoogle Scholar
  54. 54.
    Horowitz RA, Agard DA, Sedat JW, Woodcock CL. The three-dimensional architecture of chromatin in situ: electron tomography reveals fibers composed of a continuously variable zig-zag nucleosomal ribbon. J Cell Biol. 1994;125(1):1–10.PubMedGoogle Scholar
  55. 55.
    Allen MJ, Lee C, Lee JDt, et al. Atomic force microscopy of mammalian sperm chromatin. Chromosoma. 1993;102(9):623–30.PubMedGoogle Scholar
  56. 56.
    Balhorn R, Cosman M, Thornton K, et al. Protamine mediated condensation of DNA in mammalian sperm. In: Gagnon C, editor. The male gamete: from basic knowledge to clinical applications: Proceedings of the 8th International Symposium of Spermatology. Vienna, IL: Cache River; 1999.Google Scholar
  57. 57.
    Evenson DP, Witkin SS, de Harven E, Bendich A. Ultrastructure of partially decondensed human ­spermatozoal chromatin. J Ultrastruct Res. 1978;63(2):178–87.PubMedGoogle Scholar
  58. 58.
    Koehler JK. Fine structure observations in frozen-etched bovine spermatozoa. J Ultrastruct Res. 1966;16(3):359–75.PubMedGoogle Scholar
  59. 59.
    Koehler JK. A freeze-etching study of rabbit ­spermatozoa with particular reference to head structures. J Ultrastruct Res. 1970;33(5):598–614.PubMedGoogle Scholar
  60. 60.
    Koehler JK, Wurschmidt U, Larsen MP. Nuclear and chromatin structure in rat spermatozoa. Gamate Res. 1983;8:357–77.Google Scholar
  61. 61.
    Sobhon P, Chutatape C, Chalermisarachai P, Vongpayabal P, Tanphaichitr N. Transmission and scanning electron microscopic studies of the human sperm chromatin decondensed by micrococcal nuclease and salt. J Exp Zool. 1982;221(1):61–79.PubMedGoogle Scholar
  62. 62.
    Wagner TE, Yun JS. Fine structure of human sperm chromatin. Arch Androl. 1979;2(4):291–4.PubMedGoogle Scholar
  63. 63.
    Allen MJ, Bradbury EM, Balhorn R. AFM analysis of DNA-protamine complexes bound to mica. Nucleic Acids Res. 1997;25(11):2221–6.PubMedGoogle Scholar
  64. 64.
    Bloomfield VA. Condensation of DNA by multivalent cations: considerations on mechanism. Biopolymers. 1991;31(13):1471–81.PubMedGoogle Scholar
  65. 65.
    Marquet R, Wyart A, Houssier C. Influence of DNA length on spermine-induced condensation. Importance of the bending and stiffening of DNA. Biochim Biophys Acta. 1987;909(3):165–72.PubMedGoogle Scholar
  66. 66.
    Brewer LR, Corzett M, Balhorn R. Protamine-induced condensation and decondensation of the same DNA molecule. Science. 1999;286(5437):120–3.PubMedGoogle Scholar
  67. 67.
    Koehler JK. Human sperm head ultrastructure: a freeze-etching study. J Ultrastruct Res. 1972;39(5):520–39.PubMedGoogle Scholar
  68. 68.
    Finch JT, Lutter LC, Rhodes D, et al. Structure of nucleosome core particles of chromatin. Nature. 1977;269(5623):29–36.PubMedGoogle Scholar
  69. 69.
    Corzett M, Mazrimas J, Balhorn R. Protamine 1: protamine 2 stoichiometry in the sperm of eutherian mammals. Mol Reprod Dev. 2002;61(4):519–27.PubMedGoogle Scholar
  70. 70.
    Balhorn R. The protamine family of sperm nuclear proteins. Genome Biol. 2007;8(9):227.PubMedGoogle Scholar
  71. 71.
    Retief JD, Winkfein RJ, Dixon GH. Evolution of the monotremes. The sequences of the protamine P1 genes of platypus and echidna. Eur J Biochem. 1993;218(2):457–61.PubMedGoogle Scholar
  72. 72.
    Retief JD, Rees JS, Westerman M, Dixon GH. Convergent evolution of cysteine residues in sperm protamines of one genus of marsupials, the Planigales. Mol Biol Evol. 1995;12(4):708–12.PubMedGoogle Scholar
  73. 73.
    Hud NV, Milanovich FP, Balhorn R. Evidence of novel secondary structure in DNA-bound protamine is revealed by raman spectroscopy. Biochemistry. 1994;33(24):7528–35.PubMedGoogle Scholar
  74. 74.
    Balhorn R. Mammalian protamines: structure and molecular interactions. In: Adolph KW, editor. Molecular biology of chromosome function. New York: Springer; 1989. p. 366–95.Google Scholar
  75. 75.
    Yelick PC, Balhorn R, Johnson PA, et al. Mouse protamine 2 is synthesized as a precursor whereas mouse protamine 1 is not. Mol Cell Biol. 1987;7(6):2173–9.PubMedGoogle Scholar
  76. 76.
    Carré-Eusèbe D, Lederer F, Lê KH, Elsevier SM. Processing of the precursor of protamine P2 in mouse. Peptide mapping and N-terminal sequence analysis of intermediates. Biochem J. 1991;277(Pt 1):39–45.PubMedGoogle Scholar
  77. 77.
    Chauviere M, Martinage A, Debarle M, Sautiere P, Chevaillier P. Molecular characterization of six intermediate proteins in the processing of mouse protamine P2 precursor. Eur J Biochem. 1992;204(2):759–65.PubMedGoogle Scholar
  78. 78.
    Elsevier SM, Noiran J, Carre-Eusebe D. Processing of the precursor of protamine P2 in mouse. Identification of intermediates by their insolubility in the presence of sodium dodecyl sulfate. Eur J Biochem. 1991;196(1):167–75.PubMedGoogle Scholar
  79. 79.
    Schellman JA, Parthasarathy N. X-ray diffraction studies on cation-collapsed DNA. J Mol Biol. 1984;175(3):313–29.PubMedGoogle Scholar
  80. 80.
    Hud NV, Vilfan ID. Toroidal DNA condensates: unraveling the fine structure and the role of nucleation in determining size. Annu Rev Biophys Biomol Struct. 2005;34:295–318.PubMedGoogle Scholar
  81. 81.
    Livolant F. Cholesteric organization of DNA in the stallion sperm head. Tissue Cell. 1984;16(4):535–55.PubMedGoogle Scholar
  82. 82.
    Bianchi F, Rousseaux-Prevost R, Bailly C, Rousseaux J. Interaction of human P1 and P2 protamines with DNA. Biochem Biophys Res Commun. 1994;201(3):1197–204.PubMedGoogle Scholar
  83. 83.
    Feughelman M, Langridge R, Seeds WE, et al. Molecular structure of deoxyriboncleic acid and nucleoprotein. Nature. 1955;175:834–8.PubMedGoogle Scholar
  84. 84.
    Prieto MC, Maki AH, Balhorn R. Analysis of ­DNA-protamine interactions by optical detection of magnetic resonance. Biochemistry. 1997;36(39):11944–51.PubMedGoogle Scholar
  85. 85.
    Wilkins MFH. Physical studies of the molecular structure of deoxyribonucleic acid and nucleoprotein. Cold Spring Harb Symp Quant Biol. 1956;21:75–90.PubMedGoogle Scholar
  86. 86.
    Cremer T, Cremer C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet. 2001;2(4):292–301.PubMedGoogle Scholar
  87. 87.
    Lichter P, Cremer T, Borden J, Manuelidis L, Ward DC. Delineation of individual human chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombinant DNA libraries. Hum Genet. 1988;80(3):224–34.PubMedGoogle Scholar
  88. 88.
    Savage JR. Interchange and intra-nuclear architecture. Environ Mol Mutagen. 1993;22(4):234–44.PubMedGoogle Scholar
  89. 89.
    Schardin M, Cremer T, Hager HD, Lang M. Specific staining of human chromosomes in Chinese hamster × man hybrid cell lines demonstrates interphase chromosome territories. Hum Genet. 1985;71(4):281–7.PubMedGoogle Scholar
  90. 90.
    Weierich C, Brero A, Stein S, et al. Three-dimensional arrangements of centromeres and telomeres in nuclei of human and murine lymphocytes. Chromosome Res. 2003;11(5):485–502.PubMedGoogle Scholar
  91. 91.
    Manuelidis L. Individual interphase chromosome domains revealed by in situ hybridization. Hum Genet. 1985;71(4):288–93.PubMedGoogle Scholar
  92. 92.
    Manvelyan M, Hunstig F, Bhatt S, et al. Chromosome distribution in human sperm – a 3D multicolor ­banding-study. Mol Cytogenet. 2008;1:25.PubMedGoogle Scholar
  93. 93.
    Mudrak O, Tomilin N, Zalensky A. Chromosome architecture in the decondensing human sperm nucleus. J Cell Sci. 2005;118(Pt 19):4541–50.PubMedGoogle Scholar
  94. 94.
    Zalensky A, Zalenskaya I. Organization of chromosomes in spermatozoa: an additional layer of ­epigenetic information? Biochem Soc Trans. 2007;35(Pt 3):609–11.PubMedGoogle Scholar
  95. 95.
    Chen JL, Guo SH, Gao FH. Nuclear matrix in ­developing rat spermatogenic cells. Mol Reprod Dev. 2001;59(3):314–21.PubMedGoogle Scholar
  96. 96.
    Santi S, Rubbini S, Cinti C, et al. Ultrastructural organization of the sperm nuclear matrix. Ital J Anat Embryol. 1995;100 Suppl 1:39–46.PubMedGoogle Scholar
  97. 97.
    Ward WS, Coffey DS. DNA packaging and ­organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod. 1991;44(4):569–74.PubMedGoogle Scholar
  98. 98.
    Yaron Y, Kramer JA, Gyi K, et al. Centromere sequences localize to the nuclear halo of human spermatozoa. Int J Androl. 1998;21(1):13–8.PubMedGoogle Scholar
  99. 99.
    Heng HH, Goetze S, Ye CJ, et al. Chromatin loops are selectively anchored using scaffold/matrix-attachment regions. J Cell Sci. 2004;117(Pt 7):999–1008.PubMedGoogle Scholar
  100. 100.
    Heng HH, Krawetz SA, Lu W, Bremer S, Liu G, Ye CJ. Re-defining the chromatin loop domain. Cytogenet Cell Genet. 2001;93(3–4):155–61.PubMedGoogle Scholar
  101. 101.
    Shaman JA, Yamauchi Y, Ward WS. Function of the sperm nuclear matrix. Arch Androl. 2007;53(3):135–40.PubMedGoogle Scholar
  102. 102.
    Shaman JA, Yamauchi Y, Ward WS. The sperm nuclear matrix is required for paternal DNA replication. J Cell Biochem. 2007;102(3):680–8.PubMedGoogle Scholar
  103. 103.
    Frehlick LJ, Eirin-Lopez JM, Jeffery ED, Hunt DF, Ausio J. The characterization of amphibian ­nucleoplasmins yields new insight into their role in sperm chromatin remodeling. BMC Genomics. 2006;7:99.PubMedGoogle Scholar
  104. 104.
    McLay DW, Clarke HJ. Remodelling the paternal chromatin at fertilization in mammals. Reproduction. 2003;125(5):625–33.PubMedGoogle Scholar
  105. 105.
    Philpott A, Leno GH. Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts. Cell. 1992;69(5):759–67.PubMedGoogle Scholar
  106. 106.
    Katagiri C, Ohsumi K. Remodeling of sperm chromatin induced in egg extracts of amphibians. Int J Dev Biol. 1994;38(2):209–16.PubMedGoogle Scholar
  107. 107.
    Derijck A, van der Heijden G, Giele M, Philippens M, de Boer P. DNA double-strand break repair in parental chromatin of mouse zygotes, the first cell cycle as an origin of de novo mutation. Hum Mol Genet. 2008;17(13):1922–37.PubMedGoogle Scholar
  108. 108.
    Generoso WM, Cain KT, Krishna M, Huff SW. Genetic lesions induced by chemicals in spermatozoa and spermatids of mice are repaired in the egg. Proc Natl Acad Sci USA. 1979;76(1):435–7.PubMedGoogle Scholar
  109. 109.
    Matsuda Y, Seki N, Utsugi-Takeuchi T, Tobari I. Changes in X-ray sensitivity of mouse eggs from fertilization to the early pronuclear stage, and their repair capacity. Int J Radiat Biol. 1989;55(2):233–56.PubMedGoogle Scholar
  110. 110.
    Matsuda Y, Yamada T, Tobari I. Studies on chromosome aberrations in the eggs of mice fertilized in vitro after irradiation. I. Chromosome aberrations induced in sperm after X-irradiation. Mutat Res. 1985;148(1–2):113–7.PubMedGoogle Scholar
  111. 111.
    Blanchard Y, Lescoat D, Le Lannou D. Anomalous distribution of nuclear basic proteins in round-headed human spermatozoa. Andrologia. 1990;22(6):549–55.PubMedGoogle Scholar
  112. 112.
    de Yebra L, Ballesca JL, Vanrell JA, Bassas L, Oliva R. Complete selective absence of protamine-P2 in humans. J Biol Chem. 1993;268(14):10553–7.PubMedGoogle Scholar
  113. 113.
    Foresta C, Zorzi M, Rossato M, Varotto A. Sperm nuclear instability and staining with aniline blue: abnormal persistence of histones in spermatozoa in infertile men. Int J Androl. 1992;15(4):330–7.PubMedGoogle Scholar
  114. 114.
    Hofmann N, Hilscher B. Use of aniline blue to assess chromatin condensation in morphologically normal spermatozoa in normal and infertile men. Hum Reprod. 1991;6(7):979–82.PubMedGoogle Scholar
  115. 115.
    Terquem A, Dadoune J. Aniline bule staining of human spermatozoa chromatin: evaluation of nuclear maturation. The Hague: Martinus Nijhoff; 1983.Google Scholar
  116. 116.
    van Roijen HJ, Ooms MP, Spaargaren MC, et al. Immunoexpression of testis-specific histone 2B in human spermatozoa and testis tissue. Hum Reprod. 1998;13(6):1559–66.PubMedGoogle Scholar
  117. 117.
    Zhang X, SanGabriel M, Zini A. Sperm nuclear histone to protamine ratio in fertile and infertile men: evidence of heterogeneous subpopulations of spermatozoa in the ejaculate. J Androl. 2006;27(3):414–20.PubMedGoogle Scholar
  118. 118.
    Aoki VW, Liu L, Carrell DT. Identification and evaluation of a novel sperm protamine abnormality in a population of infertile males. Hum Reprod. 2005;20(5):1298–306.PubMedGoogle Scholar
  119. 119.
    Balhorn R, Reed S, Tanphaichitr N. Aberrant protamine 1/protamine 2 ratios in sperm of infertile human males. Experientia. 1988;44(1):52–5.PubMedGoogle Scholar
  120. 120.
    Belokopytova IA, Kostyleva EI, Tomilin AN, Vorobev VI. Human male infertility may be due to a decrease of the protamine-P2 content in sperm chromatin. Mol Reprod Dev. 1993;34(1):53–7.PubMedGoogle Scholar
  121. 121.
    Carrell DT, Emery BR, Hammoud S. Altered protamine expression and diminished spermatogenesis: what is the link? Hum Reprod Update. 2007;13(3):313–27.PubMedGoogle Scholar
  122. 122.
    Carrell DT, Liu L. Altered protamine 2 expression is uncommon in donors of known fertility, but common among men with poor fertilizing capacity, and may reflect other abnormalities of spermiogenesis. J Androl. 2001;22(4):604–10.PubMedGoogle Scholar
  123. 123.
    Chevaillier P, Mauro N, Feneux D, Jouannet P, David G. Anomalous protein complement of sperm nuclei in some infertile men. Lancet. 1987;2(8562):806–7.PubMedGoogle Scholar
  124. 124.
    Oliva R. Protamines and male infertility. Hum Reprod Update. 2006;12(4):417–35.PubMedGoogle Scholar
  125. 125.
    Aoki VW, Christensen GL, Atkins JF, Carrell DT. Identification of novel polymorphisms in the nuclear protein genes and their relationship with human sperm protamine deficiency and severe male infertility. Fertil Steril. 2006;86(5):1416–22.PubMedGoogle Scholar
  126. 126.
    Aoki VW, Emery BR, Liu L, Carrell DT. Protamine levels vary between individual sperm cells of infertile human males and correlate with viability and DNA integrity. J Androl. 2006;27(6):890–8.PubMedGoogle Scholar
  127. 127.
    Aoki VW, Liu L, Jones KP, et al. Sperm protamine 1/protamine 2 ratios are related to in vitro fertilization pregnancy rates and predictive of fertilization ability. Fertil Steril. 2006;86(5):1408–15.PubMedGoogle Scholar
  128. 128.
    Cho C, Jung-Ha H, Willis WD, et al. Protamine 2 deficiency leads to sperm DNA damage and embryo death in mice. Biol Reprod. 2003;69(1):211–7.PubMedGoogle Scholar
  129. 129.
    Depa-Martynow M, Kempisty B, Lianeri M, Jagodzinski PP, Jedrzejczak P. Association between fertilin beta, protamines 1 and 2 and spermatid-­specific linker histone H1-like protein mRNA levels, fertilization ability of human spermatozoa, and quality of preimplantation embryos. Folia Histochem Cytobiol. 2007;45 Suppl 1:S79–85.PubMedGoogle Scholar
  130. 130.
    Mengual L, Ballesca JL, Ascaso C, Oliva R. Marked differences in protamine content and P1/P2 ratios in sperm cells from percoll fractions between patients and controls. J Androl. 2003;24(3):438–47.PubMedGoogle Scholar
  131. 131.
    Bedford JM, Calvin HI. The occurrence and possible functional significance of -S-S- crosslinks in sperm heads, with particular reference to eutherian mammals. J Exp Zool. 1974;188(2):137–55.PubMedGoogle Scholar
  132. 132.
    Calvin HI, Bedford JM. Formation of disulphide bonds in the nucleus and accessory structures of mammalian spermatozoa during maturation in the epididymis. J Reprod Fertil Suppl. 1971;13 Suppl 13:65–75.PubMedGoogle Scholar
  133. 133.
    Calvin HI, Yu CC, Bedford JM. Effects of epididymal maturation, zinc (II) and copper (II) on the reactive sulfhydryl content of structural elements in rat spermatozoa. Exp Cell Res. 1973;81(2):333–41.PubMedGoogle Scholar
  134. 134.
    Saowaros W, Panyim S. The formation of disulfide bonds in human protamines during sperm maturation. Experientia. 1979;35(2):191–2.PubMedGoogle Scholar
  135. 135.
    Sega GA, Generoso EE. Measurement of DNA breakage in spermiogenic germ-cell stages of mice exposed to ethylene oxide, using an alkaline elution procedure. Mutat Res. 1988;197(1):93–9.PubMedGoogle Scholar
  136. 136.
    Sega GA, Owens JG. Methylation of DNA and protamine by methyl methanesulfonate in the germ cells of male mice. Mutat Res. 1983;111(2):227–44.PubMedGoogle Scholar
  137. 137.
    Sega GA, Owens JG. Binding of ethylene oxide in spermiogenic germ cell stages of the mouse after low-level inhalation exposure. Environ Mol Mutagen. 1987;10(2):119–27.PubMedGoogle Scholar
  138. 138.
    Bjorndahl L, Kvist U. Human sperm chromatin ­stabilization: a proposed model including zinc bridges. Mol Hum Reprod. 2010;16(1):23–9.PubMedGoogle Scholar
  139. 139.
    Bench G, Corzett MH, Kramer CE, Grant PG, Balhorn R. Zinc is sufficiently abundant within mammalian sperm nuclei to bind stoichiometrically with protamine 2. Mol Reprod Dev. 2000;56(4):512–9.PubMedGoogle Scholar
  140. 140.
    Bianchi F, Rousseaux-Prevost R, Sautiere P, Rousseaux J. P2 protamines from human sperm are zinc -finger proteins with one CYS2/HIS2 motif. Biochem Biophys Res Commun. 1992;182(2):540–7.PubMedGoogle Scholar
  141. 141.
    Gatewood JM, Schroth GP, Schmid CW, Bradbury EM. Zinc-induced secondary structure transitions in human sperm protamines. J Biol Chem. 1990;265(33):20667–72.PubMedGoogle Scholar
  142. 142.
    Hernandez-Ochoa I, Sanchez-Gutierrez M, Solis-Heredia MJ, Quintanilla-Vega B. Spermatozoa nucleus takes up lead during the epididymal maturation altering chromatin condensation. Reprod Toxicol. 2006;21(2):171–8.PubMedGoogle Scholar
  143. 143.
    Johansson L, Pellicciari CE. Lead-induced changes in the stabilization of the mouse sperm chromatin. Toxicology. 1988;51(1):11–24.PubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of Applied ScienceUniversity of CaliforniaDavisUSA

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