Increased prostaglandin E2–EP2 signalling in cumulus cells of female mice sired by males with the Y-chromosome long-arm deletion
Katarzyna Kotarska A C , Małgorzata Lenartowicz A , Małgorzata Przybyło B , Aniela Gołas A and Józefa Styrna AA Department of Genetics and Evolution, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Krakow, Poland.
B Department of Glycoconjugate Biochemistry, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Krakow, Poland.
C Corresponding author. Email: katarzyna.kotarska@uj.edu.pl
Reproduction, Fertility and Development 25(6) 900-906 https://doi.org/10.1071/RD12086
Submitted: 19 March 2012 Accepted: 26 July 2012 Published: 31 August 2012
Abstract
Cumuli oophori surrounding ovulated oocytes of B10.BR(Ydel) females (sired by males with the Y-chromosome long-arm deletion) are more resistant to hyaluronidase digestion than cumuli oophori around eggs of genetically identical females but sired by males with the intact Y chromosome (B10.BR). This has been interpreted as a result of differences in paternal genome imprinting, which females of both groups inherit from their fathers. The following study shows that it is not hyaluronan, but rather excessive protein concentration, that makes the cumulus extracellular matrix of B10.BR(Ydel) oocytes more resistant to enzymatic treatment. It was revealed, additionally, that cumulus cells around ovulating oocytes of B10.BR(Ydel) females display higher surface accumulation of prostaglandin EP2 subtype receptors and higher expression of the Ptgs2 gene (encoding a rate-limiting enzyme of prostaglandin E2 synthesis) in relation to the cells of control B10.BR females. The expression levels of the prostaglandin-dependent Tnfaip6 and Ccl2 genes were also altered in B10.BR(Ydel) cumulus cells in a manner indicating increased prostaglandin signalling. The study provides further evidence for the divergence in reproductive phenotypes between B10.BR and B10.BR(Ydel) female mice. It supports the hypothesis that genes of the Y-chromosome long arm may be involved in establishment of epigenetic marks in X-bearing spermatozoa.
Additional keywords: cumulus oophorus, epigenetics, extracellular matrix, ovulation.
References
Burgoyne, P. S. (1998). The role of Y-encoded genes in mammalian spermatogenesis. Semin. Cell Dev. Biol. 9, 423–432.| The role of Y-encoded genes in mammalian spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvFyr&md5=9c161166bcd52aa4ccb0c325388c74b3CAS | 9813189PubMed |
Chen, L., Zhang, H., Powers, R. W., Russell, P. T., and Larsen, W. J. (1996). Covalent linkage between proteins of the inter-α-inhibitor family and hyaluronic acid is mediated by a factor produced by granulosa cells. J. Biol. Chem. 271, 19 409–19 414.
| Covalent linkage between proteins of the inter-α-inhibitor family and hyaluronic acid is mediated by a factor produced by granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvFymsLg%3D&md5=60adeede21140480e202879f425366e5CAS |
Cocquet, J., Ellis, P. J. I., Yamauchi, Y., Mahadevaiah, S. K., Affara, N. A., Ward, M. A., and Burgoyne, P. S. (2009). The multicopy gene Sly represses the sex chromosomes in the male mouse germline after meiosis. PLoS Biol. 7, e1000244.
| The multicopy gene Sly represses the sex chromosomes in the male mouse germline after meiosis.Crossref | GoogleScholarGoogle Scholar | 19918361PubMed |
Davis, B. J., Lennard, D. E., Lee, C. A., Tiano, H. F., Morham, S. G., Wetsel, W. C., and Langenbach, R. (1999). Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1β. Endocrinology 140, 2685–2695.
| Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1β.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtlKhtb4%3D&md5=62390e42d52eb0a2b7985113bbad0f90CAS | 10342859PubMed |
Duffy, D. M., McGinnis, L. K., VandeVoort, C. A., and Christenson, L. K. (2010). Mammalian oocytes are targets for prostaglandin E2 (PGE2) action. Reprod. Biol. Endocrinol. 8, 131.
| Mammalian oocytes are targets for prostaglandin E2 (PGE2) action.Crossref | GoogleScholarGoogle Scholar | 21040553PubMed |
Durcova-Hills, G., Hajkova, P., Sullivan, S., Barton, S., Surani, M. A., and McLaren, A. (2006). Influence of sex chromosome constitution on the genomic imprinting of germ cells. Proc. Natl. Acad. Sci. USA 103, 11 184–11 188.
| Influence of sex chromosome constitution on the genomic imprinting of germ cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvVCmtr8%3D&md5=ca73d62c5c4042c783abc802c655d734CAS |
Ellis, P. J. I., Clemente, E. J., Ball, P., Toure, A., Ferguson, L., Turner, J. M. A., Loveland, K. L., Affara, N. A., and Burgoyne, P. S. (2005). Deletions on mouse Yq lead to upregulation of multiple X- and Y-linked transcripts in spermatids. Hum. Mol. Genet. 14, 2705–2715.
| Deletions on mouse Yq lead to upregulation of multiple X- and Y-linked transcripts in spermatids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvFeqsr8%3D&md5=699098ccf662ee1c90f01f7e402a62d3CAS |
Ellis, P. J. I., Ferguson, L., Clemente, E. J., and Affara, N. A. (2007). Bidirectional transcription of a novel chimeric gene mapping to mouse chromosome Yq. BMC Evol. Biol. 7, 171.
| Bidirectional transcription of a novel chimeric gene mapping to mouse chromosome Yq.Crossref | GoogleScholarGoogle Scholar |
Grzmil, P., Gołas, A., Müller, C., and Styrna, J. (2007). The influence of the deletion on the long arm of the Y chromosome on sperm motility in mice. Theriogenology 67, 760–766.
| The influence of the deletion on the long arm of the Y chromosome on sperm motility in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlCksLk%3D&md5=acf89345d7891a2e9e9afdc56a8502b0CAS | 17126391PubMed |
Hizaki, H., Segi, E., Sugimoto, Y., Hirose, M., Saji, T., Ushikubi, F., Matsuoka, T., Noda, Y., Tanaka, T., Yoshida, N., and Narumiya, S. (1999). Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP2. Proc. Natl. Acad. Sci. USA 96, 10 501–10 506.
| Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvFemsrg%3D&md5=0a67420b68153b5cdad7531ec073ea44CAS |
Koh, E., Sin, H.-S., Fukushima, M., and Namiki, M. (2010). Azoospermia factor and male infertility. Reprod. Med. Biol. 9, 129–137.
| Azoospermia factor and male infertility.Crossref | GoogleScholarGoogle Scholar |
Kotarska, K., and Lenartowicz, M. (2011). Sperm migration and selection in the reproductive tract of female mice is mostly affected by male genotype. Folia Biol. 59, 71–75.
| Sperm migration and selection in the reproductive tract of female mice is mostly affected by male genotype.Crossref | GoogleScholarGoogle Scholar |
Kotarska, K., and Styrna, J. (2012). Can the partial deletion in the Y chromosome of male mice affect the reproductive efficiency of their daughters? Syst. Biol. Reprod. Med. 58, 81–87.
| Can the partial deletion in the Y chromosome of male mice affect the reproductive efficiency of their daughters?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktV2ntLo%3D&md5=d81cc9640ce7d0aced3e5beb056ac1d0CAS | 22149694PubMed |
Kotula-Balak, M., Grzmil, P., Styrna, J., and Bilińska, B. (2004). Immunodetection of aromatase in mice with a partial deletion in the long arm of the Y chromosome. Acta Histochem. 106, 55–64.
| Immunodetection of aromatase in mice with a partial deletion in the long arm of the Y chromosome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsVGhtb0%3D&md5=36bea67a29aa27f9595d319fc2013349CAS | 15032329PubMed |
Krzanowska, H., Lorenc, E., Koncewicz, A., and Lipina, B. (1984). The rate of maturation and fertilizability of oocytes in KE and CBA/Kw female mice with induced superovulation. Zwierz. Lab. 21, 3–13.
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=c02316d2aa02af4c464251269a77c9c9CAS | 11846609PubMed |
Ochsner, S. A., Russell, D. L., Day, A. J., Breyer, R. M., and Richards, J. S. (2003). Decreased expression of tumour necrosis factor-α-stimulated gene 6 in cumulus cells of the cyclooxygenase-2 and EP2 null mice. Endocrinology 144, 1008–1019.
| Decreased expression of tumour necrosis factor-α-stimulated gene 6 in cumulus cells of the cyclooxygenase-2 and EP2 null mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslCqtrw%3D&md5=9e9dddce5e40ba91d782f6c42cae1deaCAS | 12586778PubMed |
Richards, J. S. (2005). Ovulation: new factors that prepare the oocyte for fertilization. Mol. Cell. Endocrinol. 234, 75–79.
| Ovulation: new factors that prepare the oocyte for fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1SqtLk%3D&md5=c99e6f6f764656e055d194d54a13806aCAS | 15836955PubMed |
Roberts, K. P. (1998). Y chromosome deletions and male infertility: state of the art and clinical implications. J. Androl. 19, 255–259.
| 1:CAS:528:DyaK1cXkt1Sls78%3D&md5=c537a69113a3d4c15c484c4446b3f6f2CAS | 9639042PubMed |
Russell, D. L., Ochsner, S. A., Hsieh, M., Mulders, S., and Richards, J. S. (2003). Hormone-regulated expression and localization of versican in the rodent ovary. Endocrinology 144, 1020–1031.
| Hormone-regulated expression and localization of versican in the rodent ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslCqtr0%3D&md5=c38477480de72a279300244e0f3883d5CAS | 12586779PubMed |
Scarchilli, L., Camaioni, A., Bottazzi, B., Negri, V., Doni, A., Deban, L., Bastone, A., Salvatori, G., Mantovani, A., Siracusa, G., and Salustri, A. (2007). PTX3 interacts with inter-α-trypsin inhibitor: implications for hyaluronan organization and cumulus oophorus expansion. J. Biol. Chem. 282, 30 161–30 170.
| PTX3 interacts with inter-α-trypsin inhibitor: implications for hyaluronan organization and cumulus oophorus expansion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFagtbbL&md5=c8934f0ca5379a9a9077a933fd10640cCAS |
Segi, E., Haraguchi, K., Sugimoto, Y., Tsuji, M., Tsunekawa, H., Tamba, S., Tsuboi, K., Tanaka, S., and Ichikawa, A. (2003). Expression of messenger RNA for prostaglandin E receptor subtypes EP4/EP2 and cyclooxygenase isozymes in mouse periovulatory follicles and oviducts during superovulation. Biol. Reprod. 68, 804–811.
| Expression of messenger RNA for prostaglandin E receptor subtypes EP4/EP2 and cyclooxygenase isozymes in mouse periovulatory follicles and oviducts during superovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFGlu70%3D&md5=fb69b1d5f0c7aae5fcad8ec857ae8e64CAS | 12604629PubMed |
Sirois, J., Sayasith, K., Brown, K. A., Stock, A. E., Bouchard, N., and Dore, M. (2004). Cyclooxygenase-2 and its role in ovulation: a 2004 account. Hum. Reprod. Update 10, 373–385.
| Cyclooxygenase-2 and its role in ovulation: a 2004 account.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsVyiuro%3D&md5=b0293f349224daa2c4df3d868f18fdadCAS | 15205395PubMed |
Styrna, J. (1995). Partial deletion of the Y chromosome removes the effect of paternal genome imprinting on periovum sensitivity to hyaluronidase in mice. Genet. Res. 65, 229–231.
| Partial deletion of the Y chromosome removes the effect of paternal genome imprinting on periovum sensitivity to hyaluronidase in mice.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2MzktVWksg%3D%3D&md5=6df24faac25da883c84a40580a699ccaCAS | 7615260PubMed |
Styrna, J., Imai, H. T., and Moriwaki, K. (1991a). An increased level of sperm abnormalities in mice with a partial deletion of the Y chromosome. Genet. Res. 57, 195–199.
| An increased level of sperm abnormalities in mice with a partial deletion of the Y chromosome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3ns1ahuw%3D%3D&md5=45317a5a6ea2095ac97d6d9fadb291aeCAS | 2055460PubMed |
Styrna, J., Klag, J., and Moriwaki, K. (1991b). Influence of partial deletion of the Y chromosome on mouse sperm phenotype. J. Reprod. Fertil. 92, 187–195.
| Influence of partial deletion of the Y chromosome on mouse sperm phenotype.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3nvVShug%3D%3D&md5=567833685e675dd2e30fab2d3dd7ec61CAS | 2056490PubMed |
Styrna, J., Bilińska, B., and Krzanowska, H. (2002). The effect of a partial Y chromosome deletion in B10.BR-Ydel mice on testis morphology, sperm quality and efficiency of fertilization. Reprod. Fertil. Dev. 14, 101–108.
| The effect of a partial Y chromosome deletion in B10.BR-Ydel mice on testis morphology, sperm quality and efficiency of fertilization.Crossref | GoogleScholarGoogle Scholar | 12051515PubMed |
Sugimoto, Y., and Narumiya, S. (2007). Prostaglandin E receptors. J. Biol. Chem. 282, 11 613–11 617.
| Prostaglandin E receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktFemtbs%3D&md5=49e480e5421dd30b21e362aa5aea9c90CAS |
Takahashi, T., Morrow, J. D., Wang, H., and Dey, S. K. (2006). Cyclooxygenase-2-derived prostaglandin E2 directs oocyte maturation by differentially influencing multiple signalling pathways. J. Biol. Chem. 281, 37 117–37 129.
| Cyclooxygenase-2-derived prostaglandin E2 directs oocyte maturation by differentially influencing multiple signalling pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1elt7%2FP&md5=a67d48024bc398919deb5b1967dde99bCAS |
Tamba, S., Yodoi, R., Segi-Nishida, E., Ichikawa, A., Narumiya, S., and Sugimoto, Y. (2008). Timely interaction between prostaglandin and chemokine signalling is a prerequisite for successful fertilization. Proc. Natl. Acad. Sci. USA 105, 14 539–14 544.
| Timely interaction between prostaglandin and chemokine signalling is a prerequisite for successful fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Sgt77P&md5=0d7ef69ea49eb2f7e8ea2613643078a1CAS |
Tamba, S., Yodoi, R., Morimoto, K., Inazumi, T., Sukeno, M., Segi-Nishida, E., Okuno, Y., Tsujimoto, G., Narumiya, S., and Sugimoto, Y. (2010). Expression profiling of cumulus cells reveals functional changes during ovulation and central role of prostaglandin EP2 receptor in cAMP signalling. Biochimie 92, 665–675.
| Expression profiling of cumulus cells reveals functional changes during ovulation and central role of prostaglandin EP2 receptor in cAMP signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmslGhtbw%3D&md5=58e4e439b48865e18fb492e31e440925CAS | 20399827PubMed |
Touré, A., Szot, M., Mahadevaiah, S. K., Rattigan, A., Ojarikre, O. A., and Burgoyne, P. S. (2004). A new deletion of the mouse Y chromosome long arm associated with the loss of Ssty expression, abnormal sperm development and sterility. Genetics 166, 901–912.
| A new deletion of the mouse Y chromosome long arm associated with the loss of Ssty expression, abnormal sperm development and sterility.Crossref | GoogleScholarGoogle Scholar | 15020475PubMed |
Touré, A., Clemente, E. J., Ellis, P., Mahadevaiah, S. K., Ojarikre, O. A., Ball, P. A. F., Reynard, L., Loveland, K. L., Burgoyne, P. S., and Affara, A. (2005). Identification of novel Y chromosome-encoded transcripts by testis transcriptome analysis of mice with deletions of the Y chromosome long arm. Genome Biol. 6, R102.
| Identification of novel Y chromosome-encoded transcripts by testis transcriptome analysis of mice with deletions of the Y chromosome long arm.Crossref | GoogleScholarGoogle Scholar | 16356265PubMed |
Ward, M. A., and Burgoyne, P. S. (2006). The effect of deletions of the mouse Y chromosome long arm on sperm function – intracytoplasmic sperm injection (ICSI)-based analysis. Biol. Reprod. 74, 652–658.
| The effect of deletions of the mouse Y chromosome long arm on sperm function – intracytoplasmic sperm injection (ICSI)-based analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XislKqsbs%3D&md5=8a92e955dae6d9dcdfcbc109c3d6cf8cCAS | 16354792PubMed |
Wijchers, P. J., and Festenstein, R. J. (2011). Epigenetic regulation of autosomal gene expression by sex chromosomes. Trends Genet. 27, 132–140.
| Epigenetic regulation of autosomal gene expression by sex chromosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvV2murg%3D&md5=94e30da3f4ffafe1a71f7af16df4d7d3CAS | 21334089PubMed |
Xian, M., Azuma, S., Naito, K., Kunieda, T., Moriwaki, K., and Toyoda, Y. (1992). Effect of a partial deletion of Y chromosome on in vitro-fertilizing ability of mouse spermatozoa. Biol. Reprod. 47, 549–553.
| Effect of a partial deletion of Y chromosome on in vitro-fertilizing ability of mouse spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s%2Fgtl2isQ%3D%3D&md5=4714035faa94172fe0c533197c29c432CAS | 1327209PubMed |
Zhuo, L., and Kimata, K. (2001). Cumulus oophorus extracellular matrix: its construction and regulation. Cell Struct. Funct. 26, 189–196.
| Cumulus oophorus extracellular matrix: its construction and regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosVWqs7g%3D&md5=793d1f1e2e73b5fd1b08f7b7c04452c3CAS | 11699635PubMed |