Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Characterisation of a human sperm cell subpopulation marked by the presence of the TSH2B histone

Stephanie Singleton* A , Olga Mudrak* A B , Mahmood Morshedi A , Sergio Oehninger A , Irina Zalenskaya A and Andrei Zalensky A C
+ Author Affiliations
- Author Affiliations

A The Jones Institute for Reproductive Medicine, Eastern Virginia Medical School, 601 Colley Avenue, Norfolk, VA 23507, USA.

B Institute of Cytology, Russian Academy of Sciences, St Petersburg 194064, Russia.

C Corresponding author. Email: zalensao@evms.edu

Reproduction, Fertility and Development 19(2) 392-397 https://doi.org/10.1071/RD06099
Submitted: 30 August 2006  Accepted: 6 November 2006   Published: 29 January 2007

Abstract

During the process of mammalian spermiogenesis, a significant reorganisation of the chromatin structure occurs involving the sequential substitution of somatic histones with protamines. In the human sperm nucleus, ~15% of the basic nuclear protein complement is maintained as histones. Human testis/sperm-specific histone H2B (hTSH2B) is a variant of the histone H2B expressed exclusively in spermatogenic germline cells and present in some mature sperm cells. Thus, this protein marks a subpopulation of sperm cells in the ejaculate. Using indirect immunofluorescence, we examined the influence of hTSH2B on zona pellucida binding and sperm head decondensation in amphibian egg cell-free extract. As suggested by previous studies, we found that hTSH2B can be localised in only ~30% of sperm cells within a given ejaculate. We established that the presence of hTSH2B does not influence sperm zona pellucida binding capacity. Finally, we found that decondensation occurred more rapidly and to a greater extent in those cells containing hTSH2B. We propose that the presence or absence of hTSH2B within spermatozoa influences pronuclei formation and the activation of paternal genes following fertilisation and during early embryonic development.


Acknowledgements

We would like to thank Dr E.W. Godfrey for providing the Xenopus facility. This work has been supported by The Endocrine Fellows Foundation Grant to S. S. and NIH grant HD-042748 to A. O. Z.


References

Berkovitz, A. , Eltes, F. , Lederman, H. , Peer, S. , Ellenbogen, A. , Feldberg, B. , and Bartoov, B. (2006). How to improve IVF-ICSI outcome by sperm selection. Reprod. Biomed. Online 12, 634–638.
PubMed | Menut S., Lemaitre J. M., Hair A., and Méchali M. (1999). DNA replication and chromatin assembly using Xenopus egg extracts. In ‘Advances in Molecular Biology: A Comparative Methods Approach to the Study of Oocytes and Embryos’. (Ed. J. D. Richter.) pp. 198–226. (Oxford University Press: Oxford.)

Mudrak, O. , Tomilin, N. , and Zalensky, A. (2005). Chromosome architecture in the decondensing human sperm nucleus. J. Cell Sci. 118, 4541–4550.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Neuber, E. , Havari, E. , Aquiles Sanchez, J. , Powers, R. D. , and Wangh, L. J. (1999). Efficient human sperm pronucleus formation and replication in Xenopus egg extracts. Biol. Reprod. 61, 912–920.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Oehninger, S. , Toner, J. , Muasher, S. , Coddington, C. , Acosta, A. , and Hodgen, G. D. (1992). Prediction of fertilization in vitro with human gametes: is there a litmus test? Am. J. Obstet. Gynecol. 167, 1760–1767.
PubMed |

Oehninger, S. , Mahoney, M. , Ozgur, K. , Kolm, P. , Kruger, T. , and Franken, D. (1997). Clinical significance of human sperm–zona pellucida binding. Fertil. Steril. 67, 1121–1127.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sassone-Corsi, P. (2002). Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 296, 2176–2178.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Schultz, R. , and Worrad, D. (1995). Role of chromatin structure in zygotic gene activation in the mammalian embryo. Semin. Cell Biol. 6, 201–208.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Simerly, C. , Zoran, S. S. , Payne, C. , Dominko, T. , Sutovsky, P. , Navara, C. S. , Salisbury, J. L. , and Schatten, G. (1999). Biparental inheritance of gamma-tubulin during human fertilization: molecular reconstitution of functional zygotic centrosomes in inseminated human oocytes and in cell-free extracts nucleated by human sperm. Mol. Biol. Cell 10, 2955–2969.
PubMed |

Singleton, S. , Zalensky, A. , Doncel, G. F. , Morshedi, M. , and Zalenskaya, I. A. (2006). Testis/sperm-specific histone 2B in the sperm of donors and subfertile patients: variability and relation to chromatin packaging. Hum. Reprod. ,in press.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tarlatzis, B. C. , and Bili, H. (1998). Survey on intracytoplasmic sperm injection: report from the ESHRE ICSI Task Force. European Society of Human Reproduction and Embryology. Hum. Reprod. 13((Suppl. 1)), 165–177.
PubMed |

Tesarik, J. , Greco, E. , and Mendoza, C. (2004). Late, but not early, paternal effect on human embryo development is related to sperm DNA fragmentation. Hum. Reprod. 19, 611–615.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Unni, E. , Zhang, Y. , Kangasniemi, M. , Saperstein, W. , Moss, S. B. , and Meistrich, M. L. (1995). Stage-specific distribution of the spermatid-specific histone 2B in the rat testis. Biol. Reprod. 53, 820–826.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Van Dyk, Q. , Lanzendorf, S. , Kolm, P. , Hodgen, G. D. , and Mahony, M. C. (2000). Incidence of aneuploidy spermatozoa from subfertile men: selected with motility versus hemizona-bound. Hum. Reprod. 15, 1529–1536.
Crossref | GoogleScholarGoogle Scholar | PubMed |

van Roijen, J. H. , Ooms, M. P. , Spaargaren, M. C. , Baarends, W. M. , Weber, R. F. A. , Grootegoed, J. A. , and Vreeburg, J. T. (1998). Immunoexpression of testis-specific histone 2B in human spermatozoa and testis tissue. Hum. Reprod. 13, 1559–1566.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ventela, S. , Toppari, J. , and Parvinen, M. (2003). Intracellular organelle traffic through cytoplasmic bridges in early spermatids of the rat: mechanisms of haploid gene product sharing. Mol. Biol. Cell 14, 2768–2780.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wyrobek, A. J. , Alhborn, T. , Balhorn, R. , Stanker, L. , and Pinkel, D. (1990). Fluorescence in situ hybridization to Y chromosomes in decondensed human sperm nuclei. Mol. Reprod. Dev. 27, 200–208.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Zalenskaya, I. A. , and Zalensky, A. O. (2004). Non-random positioning of chromosomes in human sperm nuclei. Chromosome Res. 12, 163–173.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Zalensky, A. O. , Siino, J. S. , Gineitis, A. A. , Zalenskaya, I. A. , Tomilin, N. V. , Yau, P. , and Bradbury, E. M. (2002). Human testis/sperm specific histone H2B (hTSH2B): Molecular cloning and characterization. J. Biol. Chem. 277, 43 474–43 480.
Crossref | GoogleScholarGoogle Scholar | PubMed |




* Stephanie Singleton and Olga Mudrak contributed equally to this paper.