Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-10T20:29:15.639Z Has data issue: false hasContentIssue false
  • English
  • Français

Expression and cellular distribution of estrogen and progesterone receptors and the real-time proliferation of porcine cumulus cells

Published online by Cambridge University Press:  16 October 2014

Bartosz Kempisty ,
Agnieszka Ziółkowska ,
Sylwia Ciesiółka ,
Hanna Piotrowska ,
Paweł Antosik ,
Dorota Bukowska ,
Klaus P. Brüssow ,
Michał Nowicki  and
Maciej Zabel
Bartosz Kempisty*
Affiliation:
Department of Histology and Embryology, Department of Anatomy, Poznan University of Medical Sciences, 6 Swiecickiego St., 60–781 Poznan, Poland. Department of Anatomy, Poznan University of Medical Sciences, 6 Swiecickiego St. 60–781 Poznan, Poland.
Agnieszka Ziółkowska
Affiliation:
Department of Histology and Embryology, Poznan University of Medical Sciences, 6 Swiecickiego St. 60–781 Poznan, Poland.
Sylwia Ciesiółka
Affiliation:
Department of Histology and Embryology, Poznan University of Medical Sciences, 6 Swiecickiego St. 60–781 Poznan, Poland.
Hanna Piotrowska
Affiliation:
Department of Toxicology, Poznan University of Medical Sciences, 30 Dojazd St. 60–631 Poznan, Poland.
Paweł Antosik
Affiliation:
Institute of Veterinary Sciences, Poznan University of Life Sciences, 52 Wojska Polskiego St. 60–628, Poznan, Poland.
Dorota Bukowska
Affiliation:
Institute of Veterinary Sciences, Poznan University of Life Sciences, 52 Wojska Polskiego St. 60–628, Poznan, Poland.
Klaus P. Brüssow
Affiliation:
Institute of Reproductive Biology, Department of Experimental Reproductive Biology, Leibniz Institute for Farm Animal Biology, Dummerstorf, Germany.
Michał Nowicki
Affiliation:
Department of Histology and Embryology, Poznan University of Medical Sciences, 6 Swiecickiego St. 60–781 Poznan, Poland.
Maciej Zabel
Affiliation:
Department of Histology and Embryology, Wroclaw Medical University, 6a Chalubinskiego St., 50–368 Wroclaw, Poland.
*
All correspondence to: Bartosz Kempisty. Department of Histology and Embryology, Department of Anatomy, Poznan University of Medical Sciences, 6 Swiecickiego St., 60–781 Poznan, Poland. Tel: +48 61 8546419. Fax: +48 61 8546455. E-mail: etok@op.pl
Get access Rights & Permissions [Opens in a new window]

Summary

Although the expression of estrogen and progesterone receptors within porcine ovary and cumulus–oocyte complexes (COCs) is well recognized, still little information is known regarding expression of the progesterone receptor (PGR), PGR membrane component 1 (PGRMC1) and of estrogen-related receptors (ERRγ and ERRβ/γ) in separated cumulus cells in relation to real-time proliferation. In this study, a model of oocytes-separated cumulus cells was used to analyze the cell proliferation index and the expression PGR, PGRMC1 and of ERRγ and ERRβ/γ during 96-h cultivation in vitro using real-time quantitative PCR (qRT-PCR) and confocal microscopic observation. We found that PGR protein expression was increased at 0 h, compared with PGR protein expression after 96 h of culture (P < 0.001). The expression of PGRMC1, ERRγ and ERRβ/γ was unchanged. After using qRT-PCR we did not found statistical differences in expression of PGR, PGRMC1, ERRγ and ERRβ/γ during 96 h of cumulus cells in vitro culture (IVC). We supposed that the differential expression of the PGR protein at 0 h and after 96 h is related to a time-dependent down-regulation, which may activate a negative feedback. The distribution of PGR, PGRMC1 proteins may be linked with the translocation of receptors to the cytoplasm after the membrane binding of respective agonists and intra-cytoplasmic signal transduction. Furthermore, cumulus cells analyzed at 0 h were characterized by decreased proliferation index, whereas those after 96 h of culture revealed a significant increase of proliferation index, which may be associated with differentiation/luteinization of these cells during real-time proliferation.

Keywords

Cumulus cellsEstrogen receptorsPorcine oocyte–cumulus complexesProgesterone receptorsProliferation index
Type
Research Article
Information
Zygote , Volume 23 , Issue 6 , December 2015 , pp. 836 - 845
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Al-Aghbari, A.M. & Menino, A.R. (2002). Survival of oocytes recovered from vitrified sheep ovarian tissues. Anim. Reprod. Sci. 71, 101–11.Google Scholar
Aparicio, I.M., Garcia-Herreros, M., O’Shea, L.C., Hensey, C., Lonergan, P. & Fair, T. (2011). Expression, regulation, and function of progesterone receptors in bovine cumulus oocyte complexes during in vitro maturation. Biol. Reprod. 84, 910–21.Google Scholar
Bagg, M.A., Nottle, M.B., Armstrong, D.T. & Grupen, C.G.(2009). Effect of follicle size and dibutyryl cAMP on the cAMP content and gap junctional communication of porcine prepubertal cumulus–oocyte complexes during IVM. Reprod. Fertil. Dev. 21, 796–804.CrossRefGoogle ScholarPubMed
Cardenas, H. & Pope, W.F. (2005). Estrogen receptors in the uterus and ovarian follicles of gilts treated with dihydrotestosterone. Domest. Anim. Endocrinol. 29, 523–33.CrossRefGoogle ScholarPubMed
Dode, M.A. & Graves, C.N. (2003). Role of estradiol-17beta on nuclear and cytoplasmic maturation of pig oocytes. Anim. Reprod. Sci. 78, 99–110.Google Scholar
Doege, C.A., Inoue, K., Yamashita, T., Rhee, D.B., Travis, S., Fujita, R., Guarnieri, P., Bhagat, G., Vanti, W.B., Shih, A., Levine, R.L., Nik, S., Chen, E.I. & Abeliovich, A. (2012). Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature 488, 652–5.CrossRefGoogle ScholarPubMed
Elassar, A., Liu, X., Scranton, V., Wu, C.A. & Peluso, J.J. (2012). The relationship between follicle development and progesterone receptor membrane component-1 expression in women undergoing in vitro fertilization. Fertil. Steril. 97, 572–8.CrossRefGoogle ScholarPubMed
Fair, T. & Lonergan, P. (2012). The role of progesterone in oocyte acquisition of developmental competence. Reprod. Domest. Anim. 47, 142–7.Google Scholar
Feng, G., Shi, D., Yang, S. & Wang, X. (2013). Co-culture embedded in cumulus clumps promotes maturation of denuded oocytes and reconstructs gap junctions between oocytes and cumulus cells. Zygote 21, 231–7.Google Scholar
Gomez, M.N., Kang, J.T., Koo, O.J., Kim, S.J., Kwon, D.K., Park, S.J., Atikuzzaman, M., Hong, S.G., Jang, G. & Lee, B.C. (2012). Effect of oocyte-secreted factors on porcine in vitro maturation, cumulus expansion and developmental competence of parthenotes. Zygote 20, 135–45.Google Scholar
Hirao, Y. (2011). Conditions affecting growth and developmental competence of mammalian oocytes in vitro. Anim. Sci. J. 82, 187–97.Google Scholar
Jackowska, M., Kempisty, B., Antosik, P., Bukowska, D., Budna, J., Lianeri, M., Rosińska, E., Woźna, M., Jagodziński, P.P. & Jaśkowski, J.M. (2009). The morphology of porcine oocytes is associated with zona pellucida glycoprotein transcript contents. Reprod. Biol. 9, 79–85.Google Scholar
Ju, S. & Rui, R. (2012). Effects of cumulus cells on in vitro maturation of oocytes and development of cloned embryos in the pig. Reprod. Domest. Anim. 47, 521–9.Google Scholar
Kawashima, I., Okazaki, T., Noma, N., Nishibori, M., Yamashita, Y. & Shimada, M. (2008). Sequential exposure of porcine cumulus cells to FSH and/or LH is critical for appropriate expression of steroidogenic and ovulation-related genes that impact oocyte maturation in vivo and in vitro. Reproduction 136, 9–21.Google Scholar
Kempisty, B., Ziółkowska, A., Piotrowska, H., Zawierucha, P., Antosik, P., Bukowska, D., Ciesiółka, S., Jaśkowski, J.M., Brüssow, K.P., Nowicki, M. & Zabel, M. (2013). Real-time proliferation of porcine cumulus cells is related to the protein levels and cellular distribution of Cdk4 and Cx43. Theriogenology 80, 411–20Google Scholar
Knapczyk, K., Duda, M., Durlej, M., Galas, J., Koziorowski, M. & Slomczynska, M. (2008). Expression of estrogen receptor alpha (ERalpha) and estrogen receptor beta (ERbeta) in the ovarian follicles and corpora lutea of pregnant swine. Domest. Anim. Endocrinol. 35, 170–9.Google Scholar
Li, J., Mao, G. & Xia, G. (2012). FSH modulates PKAI and GPR3 activities in mouse oocyte of COC in a gap junctional communication (GJC)-dependent manner to initiate meiotic resumption. PLoS One 7, e37835.Google Scholar
Luo, J., Sladek, R., Bader, J.A., Matthyssen, A., Rossant, J. & Giguère, V. (1997). Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-beta. Nature 388, 778–82.Google Scholar
Mao, G.K., Li, J.X., Bian, F.H., Han, Y.Y., Guo, M., Xu, B.S., Zhang, M.J. & Xia, G.L. (2013). Gap junction-mediated cAMP movement between oocytes and somatic cells. Front. Biosci. 5, 755–67.Google Scholar
Motola, S., Popliker, M. & Tsafriri, A. (2008). Response of follicle cells to ovulatory stimuli within the follicle and in primary culture. Mol. Cell. Endocrinol. 282, 26–31.Google Scholar
Nagyová, E. (2012). Regulation of cumulus expansion and hyaluronan synthesis in porcine oocyte-cumulus complexes during in vitro maturation. Endocr. Regul. 46, 225–35.Google Scholar
Nascimento, A.B., Albornoz, M.S., Che, L., Visintin, J.A. & Bordignon, V. (2010). Synergistic effect of porcine follicular fluid and dibutyryl cyclic adenosine monophosphate on development of parthenogenetically activated oocytes from pre-pubertal gilts. Reprod. Domest. Anim. 45, 851–9.Google Scholar
Pant, D., Reynolds, L.P., Luther, J.S., Borowicz, P.P., Stenbak, T.M., Bilski, J.J., Weigl, R.M., Lopes, F., Petry, K., Johnson, M.L., Redmer, D.A. & Grazul-Bilska, A.T. (2005). Expression of connexin 43 and gap junctional intercellular communication in the cumulus–oocyte complex in sheep. Reproduction 129, 191–200.Google Scholar
Procházka, R., Petlach, M., Nagyová, E. & Nemcová, L. (2011). Effect of epidermal growth factor-like peptides on pig cumulus cell expansion, oocyte maturation, and acquisition of developmental competence in vitro: comparison with gonadotropins. Reproduction 141, 425–35.CrossRefGoogle ScholarPubMed
Qiu, H.B., Lu, S.S., Ji, K.L., Song, X.M., Lu, Y.Q., Zhang, M. & Lu, K.H. (2008). Membrane progestin receptor beta (mPR-beta): a protein related to cumulus expansion that is involved in vitro maturation of pig cumulus-oocyte complexes. Steroids 73, 1416–23.Google Scholar
Saint-Dizier, M., Sandra, O., Ployart, S., Chebrout, M. & Constant, F. (2012). Expression of nuclear progesterone receptor and progesterone receptor membrane components 1 and 2 in the oviduct of cyclic and pregnant cows during the post-ovulation period. Reprod. Biol. Endocrinol. 10, 76.Google Scholar
Schams, D. & Berisha, B. (2002). Steroids as local regulators of ovarian activity in domestic animals. Domest. Anim. Endocrinol. 23, 53–65.Google Scholar
Shimada, M., Yamashita, Y., Ito, J., Okazaki, T., Kawahata, K. & Nishibori, M. (2004). Expression of two progesterone receptor isoforms in cumulus cells and their roles during meiotic resumption of porcine oocytes. J. Mol. Endocrinol. 33, 209–25.Google Scholar
Slonina, D., Kowalik, M.K. & Kotwica, J. (2012). Expression of progesterone receptor membrane component 1, serpine mRNA binding protein 1 and nuclear progesterone receptor isoforms A and B in the bovine myometrium during the estrous cycle and early pregnancy. J. Reprod. Dev. 58, 288–94.Google Scholar
Soboleva, T.K., Pleasants, A.B., van Rens, B.T., van der Lende, T. & Peterson, A.J. (2004). A dynamic model for ovulation rate reveals an effect of the estrogen receptor genotype on ovarian follicular development in the pig. J. Anim. Sci. 82, 2329–32.Google Scholar
Zhao, X.M., Ren, J.J., Du, W.H., Hao, H.S., Liu, Y., Qin, T., Wang, D. & Zhu, H.B. (2014). Effect of mouse cumulus cells on the in vitro maturation and developmental potential of bovine denuded germinal vesicle oocytes. Zygote 22, 348–55.Google Scholar