Distribution patterns of leucocyte subpopulations expressing different cell markers in the cumulus–oocyte complexes of pregnant and pseudopregnant mice
Gökhan Akkoyunlu A B , Emin Türkay Korgun A , Çiler Çelik-Özenci A , Yasemin Seval A , Ramazan Demir A and İsmail Üstünel AA Department of Histology and Embryology, Faculty of Medicine, Akdeniz University, 07070 Antalya, Turkey.
B To whom correspondence should be addressed. email: akkoyunlu@akdeniz.edu.tr
Reproduction, Fertility and Development 15(7) 389-395 https://doi.org/10.1071/RD03037
Submitted: 11 June 2003 Accepted: 3 December 2003 Published: 3 December 2003
Abstract
The nature of leucocyte subpopulations expressing different cell markers around the cumulus–oocyte complex (COC) of pregnant and pseudopregnant mice was investigated in the present study. Immunolabelling for CD4, CD8, CD14, CD45 and CD163 and transmission electron microscopy were used to determine whether leucocytes differ between pregnant and pseudopregnant mice. Sexually mature female BALB/c mice (n = 36; 18 pregnant, 18 pseudopregnant) were stimulated to superovulate with pregnant mare’s serum gonadotropin and human chorionic gonadotrophin, then mated with either fertile or vasectomised males. Postovulatory oocytes were collected after mating. The cumulus cell masses of the pregnant group contained spermatozoa between cells and were more variable than COCs of the pseudopregnant group. Streptavidin–biotin–peroxidase immunohistochemical labelling of the cell markers CD4, CD8, CD14, CD45 and CD163 showed that there were fewer leucocytes in the COCs of the pseudopregnant group compared with the pregnant group. Transmission electron microscopy revealed that often there were macrophage-like cells containing spermiophagic bodies between the cumulus cells. These observations suggest that, together with other cumulus cells and oviducal cells, these macrophage-like cells may be involved in removing unsuitable or excess spermatozoa and, therefore, in maintaining a suitable microenvironment for normal fertilisation.
Extra keywords: CD4
Acknowledgments
This work is in partial fulfillment of a PhD degree by Gokhan Akkoyunlu at the Institute of Health Sciences, Akdeniz University, Antalya. The study was supported by the Akdeniz University Research Fund, grant no. AKD-20.01.0103.15. The authors would like to thank Dr Charles W. Archer of Cardiff University, UK for his critical reading of this manuscript. Thanks also to Sibel Özden Özer, as well as Arife Demirtop and Hakan Er (TEMGA Unit), for their technical assistance.
Adams, E. C. , and Hertig, A. T. (1969). Studies on the human corpus luteum. I. Observations on the ultrastructure of development and regression of the luteal cells during the menstrual cycle. J. Cell Biol. 41, 696–715.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Aviles, M. , Jaber, L. , Castells, M. T. , Ballesta, J. , and Kan, F. W. (1997). Modifications of carbohydrate residues and ZP2 and ZP3 glycoproteins in the mouse zona pellucida after fertilization. Biol. Reprod. 57, 1155–1163.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Aviles, M. , Castells, M. T. , Abascal, I. , Martinez-Menarguez, J. A. , Draber, P. , Kan, F. W. , and Ballesta, J. (1999). Cytochemical localization of GalNAc and GalNAcbeta1,4Galbeta1,4 disaccharide in mouse zona pellucida. Cell Tissue Res. 295, 269–277.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Barak, V. , Yanai, P. , Treves, A. J. , Roisman, I. , Simon, A. , and Laufer, N. (1992). Interleukin-1: local production and modulation of human granulosa luteal cells steroidogenesis. Fertil. Steril. 58, 719–725.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Brannstrom, M. , and Norman, R. J. (1993). Involvement of leukocytes and cytokines in the ovulatory process and corpus luteum function. Hum. Reprod. 8, 1762–1775.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Channing, C. P. , Bae, I. H. , Stone, S. L. , Anderson, L. D. , Edelson, S. , and Fowler, S. C. (1981). Porcine granulosa and cumulus cell properties. LH/hCG receptors, ability to secrete progesterone and ability to respond to LH. Mol. Cell. Endocrinol. 22, 359–370.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Crisp, T. M. , Dessouky, D. A. , and Denys, F. R. (1970). The fine structure of the human corpus luteum of early pregnancy and during the progestational phase of the mestrual cycle. Am. J. Anat. 127, 37–69.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Familiari, G. , Verlengia, C. , Nottola, S. A. , Renda, T. , Micara, G. , Aragona, C. , Zardi, L. , and Motta, P. M. (1996). Heterogeneous distribution of fibronectin, tenascin-C, and laminin immunoreactive material in the cumulus–corona cells surrounding mature human oocytes from IVF-ET protocols: evidence that they are composed of different subpopulations. An immunohistochemical study using scanning confocal laser and fluorescence microscopy. Mol. Reprod. Dev. 43, 392–402.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Gulyas, B. J. (1984). Fine structure of the luteal tissue. In
Harper, M. J. K. (1988). Gamete and zygote transport. In
Huszar, G. , Ozenci, C. C. , Cayli, S. , Zavaczki, Z. , Hansch, E. , and Vigue, L. (2003). Hyaluronic acid binding by human sperm indicates cellular maturity, viability, and unreacted acrosomal status. Fertil. Steril. 79, 1616–1624.Suppl. 3
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Larsen, W. J., Wert, S. E., Chen, L., Russell, P. and Hendrix, E. M. (1991). Expansion of the cumulus–oocyte complex during the preovulatory period: possible roles in oocyte maturation, ovulation and fertilization. In
Motta, P. , Takeva, Z. , and Palermo, D. (1971). On the presence of cilia in different cells of the mammalian ovary. Acta Anat. 78, 591–603.
![](../../media/share/OpenURL_Image.gif)
Motta, P. M., Nottola, S. A., Familiari, G., Macchiarelli, G. and Vizza, E. (1992). Follicular structures, an ultrastructural study by scanning and transmission electron microscopy and correlated techniques. In
Motta, P. M. , Makabe, S. , Naguro, T. , and Correr, S. (1994). Oocyte follicle cells association during development of human ovarian follicle. A study by high resolution scanning and transmission electron microscopy. Arch. Histol. Cytol. 57, 369–394.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Motta, P. M. , Nottola, S. A. , Pereda, J. , Croxatto, H. B. , and Familiari, G. (1995). Ultrastructure of human cumulus oophorus: a transmission electron microscopic study on oviductal oocytes and fertilized eggs. Hum. Reprod. 10, 2361–2367.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Nottola, S. A. , Familiari, G. , Micara, G. , Aragona, C. , and Motta, P. M. (1991). The ultrastructure of human cumulus–corona cells at the time of fertilization and early embryogenesis. A scanning and transmission electron microscopic study in an in vitro fertilization program. Arch. Histol. Cytol. 54, 145–161.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Nottola, S. A. , Macchiarelli, G. , Familiari, G. , Stallone, T. , Sathananthan, A. H. , and Motta, P. M. (1998). Egg–sperm interactions in humans: ultrastructural aspects. Ital. J. Anat. Embryol. 103, 85–101.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Pereda, J. , and Coppo, M. (1984). Ultrastructure of the cumulus cell mass surrounding a human egg in the pronuclear stage. Anat. Embryol.) 170, 107–112.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Pereda, J. , and Coppo, M. (1985). An electron microscopic study of sperm penetration into the human egg investments. Anat. Embryol. 173, 247–252.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Pijnenborg, R. , Gordts, S. , Ongkowidjojo, R. , and Brosens, I. (1985). Sperm phagocytosis by corona cells in a human in vitro fertilization system. Ann. N.Y. Acad. Sci. 442, 310–317.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Simon, C. , Frances, A. , Piquette, G. , and Polan, M. L. (1994). Immunohistochemical localization of the interleukin-1 system in the mouse ovary during follicular growth, ovulation, and luteinization. Biol. Reprod. 50, 449–457.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Terranova, P. F. , and Rice, V. M. (1997). Review: cytokine involvement in ovarian processes. Am. J. Reprod. Immunol. 37, 50–63.
| PubMed |
![](../../media/share/OpenURL_Image.gif)