Fertility and Sterility
Volume 93, Issue 4 , Pages 1134-1141 , 1 March 2010

Expression of human oocyte-specific linker histone protein and its incorporation into sperm chromatin during fertilization

  • Yuri Mizusawa, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, Keio University School of Medicine, Tokyo, Japan
  • ,
  • Naoaki Kuji, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, Keio University School of Medicine, Tokyo, Japan
    • Corresponding Author InformationReprint requests: Naoaki Kuji, M.D., Department of Obstetrics and Gynecology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan (FAX: 81-3-3226-1667).
  • ,
  • Yudai Tanaka, M.D.

      Affiliations

    • Yazaki Hospital, Kanagawa, Japan
  • ,
  • Mamoru Tanaka, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, Keio University School of Medicine, Tokyo, Japan
  • ,
  • Eiji Ikeda, M.D.

      Affiliations

    • Department of Pathology, Keio University School of Medicine, Tokyo, Japan
  • ,
  • Setsuko Komatsu, Ph.D.

      Affiliations

    • National Institute of Crop Science, Tsukuba, Japan
  • ,
  • Shingo Kato, Ph.D.

      Affiliations

    • Department of Microbiology and Immunology, Keio University School of Medicine, Tokyo, Japan
  • ,
  • Yasunori Yoshimura, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, Keio University School of Medicine, Tokyo, Japan

Received 20 August 2008 ,Revised 11 November 2008 ,Accepted 24 November 2008.

References 

  1. Parseghian MH, Hamkalo BA. A compendium of the histone H1 family of somatic subtypes: an elusive cast of characters and their characteristics. Biochem Cell Biol. 2001;79:289–304
  2. Marzluff WF, Gongidi P, Woods KR, Jin J, Maltais LJ. The human and mouse replication-dependent histone genes. Genomics. 2002;80:487–498
  3. Alami R, Fan Y, Pack S, Sonbuchner TM, Besse A, Lin Q, et al. Mammalian linker-histone subtypes differentially affect gene expression in vivo. Proc Natl Acad Sci USA. 2003;100:5920–5925
  4. Rupp RA, Becker PB. Gene regulation by histone H1: new links to DNA methylation. Cell. 2005;123:1178–1179
  5. Ausió J. Histone variants—the structure behind the function. Brief Funct Genomic Proteomic. 2006;5:228–243
  6. Tanaka M, Hennebold JD, Macfarlane J, Adashi EY. A mammalian oocyte–specific linker histone gene H1oo: homology with the genes for the oocyte-specific cleavage stage histone (cs-H1) of sea urchin and the B4/H1M histone of the frog. Development. 2001;128:655–664
  7. Gao S, Chung YG, Parseghian MH, King GJ, Adashi EY, Latham KE. Rapid H1 linker histone transitions following fertilization or somatic cell nuclear transfer: evidence for a uniform developmental program in mice. Dev Biol. 2004;266:62–75
  8. Dimitrov S, Dasso MC, Wolffe AP. Remodeling sperm chromatin in Xenopus laevis egg extracts: the role of core histone phosphorylation and linker histone B4 in chromatin assembly. J Cell Biol. 1994;126:591–601
  9. Bouvet P, Dimitrov S, Wolffe AP. Specific regulation of Xenopus chromosomal 5S rRNA gene transcription in vivo by histone H1. Genes Dev. 1994;8:1147–1159
  10. Kandolf H. The H1A histone variant is an in vivo repressor of oocyte type 5S gene transcription in Xenopus laevis embryos. Proc Natl Acad Sci USA. 1994;91:7257–7261
  11. Teranishi T, Tanaka M, Kimoto S, Ono Y, Miyakoshi K, Kono T, et al. Rapid replacement of somatic linker histones with the oocyte-specific linker histone H1foo in nuclear transfer. Dev Biol. 2004;266:76–86
  12. Tanaka Y, Kato S, Tanaka M, Kuji N, Yoshimura Y. Structure and expression of the human oocyte–specific histone H1 gene elucidated by direct RT-nested PCR of a single oocyte. Biochem Biophys Res Commun. 2003;304:351–357
  13. Sutcliffe AG, Taylor B, Saunders K, Thornton S, Lieberman BA, Grudzinskas JG. Outcome in the second year of life after in-vitro fertilisation by intracytoplasmic sperm injection: a UK case-control study. Lancet. 2001;357:2080–2084
  14. Palermo G, Joris H, Derde MP, Camus M, Devroey P, Van SA. Sperm characteristics and outcome of human assisted fertilization by subzonal insemination and intracytoplasmic sperm injection. Fertil Steril. 1993;59:826–835
  15. Flaherty SP, Payne D, Swann NJ, Matthews CD. Aetiology of failed and abnormal fertilization after intracytoplasmic sperm injection. Hum Reprod. 1995;10:2623–2629
  16. Payne D, Flaherty SP, Jeffrey R, Warnes GM, Matthews CD. Successful treatment of severe male factor infertility in 100 consecutive cycles using intracytoplasmic sperm injection. Hum Reprod. 1994;9:2051–2057
  17. Montgomery JC, Guarnieri MH, Tartaglia KE, Flaherty LA. Assessment of fertilization failure and abnormal fertilization after intracytoplasmic sperm injection (ICSI). Reprod Fertil Dev. 1995;7:197–210
  18. McLay DW, Clarke HJ. Remodelling the paternal chromatin at fertilization in mammals. Reproduction. 2003;125:625–633
  19. Nonchev S, Tsanev R. Protamine-histone replacement and DNA replication in the male mouse pronucleus. Mol Reprod Dev. 1996;25:72–76
  20. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1974;227:680–685
  21. Sutovsky P, Schatten G. Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol Reprod. 1997;56:1503–1512
  22. Tanaka M, Kihara M, Hennebold JD, Eppig JJ, Viveiros MM, Emery BR, et al. H1FOO is coupled to the initiation of oocytic growth. Biol Reprod. 2005;72:135–142
  23. Clarke HJ, Bustin M, Oblin C. Chromatin modifications during oogenesis in the mouse: removal of somatic subtypes of histone H1 from oocyte chromatin occurs post-natally through a post-transcriptional mechanism. J Cell Sci. 1997;110:477–487
  24. McGraw S, Vigneault C, Tremblay K, Sirard MA. Characterization of linker histone H1FOO during bovine in vitro embryo development. Mol Reprod Dev. 2006;73:692–699
  25. Nakazawa Y, Shimada A, Noguchi J, Domeki I, Kaneko H, Kikuchi K. Replacement of nuclear protein by histone in pig sperm nuclei during in vitro fertilization. Reproduction. 2002;124:565–572
  26. Shimada A, Kikuchi K, Noguchi J, Akama K, Nakano M, Kaneko H. Protamine dissociation before decondensation of sperm nuclei during in vitro fertilization of pig oocytes. J Reprod Fertil. 2000;120:247–256
  27. Rosenbusch BE. Frequency and patterns of premature sperm chromosome condensation in oocytes failing to fertilize after intracytoplasmic sperm injection. J Assist Reprod Genet. 2000;17:253–259
  28. Sakkas D, Urner F, Bianchi PG. Sperm chromatin anomalies can influence decondensation after intracytoplasmic sperm injection. Hum Reprod. 1996;11:837–843
  29. Adenot PG, Szöllösi MS, Geze M, Renard JP, Debey P. Dynamics of paternal chromatin changes in live one-cell mouse embryo after natural fertilization. Mol Reprod Dev. 1991;28:23–34
  30. Nakai M, Kashiwazaki N, Takizawa A, Maedomari N, Ozawa M, Noguchi J, et al. Morphologic changes in boar sperm nuclei with reduced disulfide bonds in electro stimulated porcine oocytes. Reproduction. 2006;131:603–611
  31. Usui N, Yanagimachi R. Behavior of hamster sperm nuclei incorporated into eggs at various stages of maturation, fertilization, and early development. The appearance and disappearance of factors involved in sperm chromatin decondensation in egg cytoplasm. J Ultrastruct Res. 1976;57:276–288
  32. Komar A. Fertilization of parthenogenetically activate mouse eggs. I. Behaviour of sperm nuclei in the cytoplasm of parthenogenetically activated eggs. Exp Cell Res. 1982;139:361–367
  33. Maleszewski M. Behavior of sperm nuclei incorporated into parthenogenetic mouse eggs prior to the first cleavage division. Mol Reprod Dev. 1992;33:215–221
  34. Dozortsev D, De Sutter P. Behaviour of spermatozoa in human oocytes displaying no or one pronucleus after intracytoplasmic sperm injection. Hum Reprod. 1994;9:2139–2144

 Y.M. has nothing to disclose. N.K. has nothing to disclose. Y.T. has nothing to disclose. M.T. has nothing to disclose. E.I. has nothing to disclose. S.K. has nothing to disclose. S.K. has nothing to disclose. Y.Y. has nothing to disclose.

 Supported in part by a Grant-in-Aid for Scientific Research from the Ministry of Education, Science, and Culture of Japan (No. 17591757 and No. 19591910), and Grant-in-Aid from the National Research Institute for Child Health and Development (No. 18-1).

PII: S0015-0282(08)04655-4

doi: 10.1016/j.fertnstert.2008.11.028

Fertility and Sterility
Volume 93, Issue 4 , Pages 1134-1141 , 1 March 2010