Superovulation alters embryonic poly(A)-binding protein (Epab) and poly(A)-binding protein, cytoplasmic 1 (Pabpc1) gene expression in mouse oocytes and early embryos
Saffet Ozturk A , Aylin Yaba-Ucar B , Berna Sozen A , Derya Mutlu C and Necdet Demir A D
+ Author Affiliations
- Author Affiliations
A Department of Histology and Embryology, Akdeniz University, School of Medicine, Campus, 07070, Antalya, Turkey.
B Department of Histology and Embryology, Istanbul Bilim University, School of Medicine, 34394, Sisli, Istanbul, Turkey.
C Department of Medical Microbiology, Akdeniz University, School of Medicine, Campus, 07070, Antalya, Turkey.
D Corresponding author. Email: necdet08@yahoo.com
Reproduction, Fertility and Development 28(3) 375-383 https://doi.org/10.1071/RD14106
Submitted: 20 March 2014 Accepted: 12 June 2014 Published: 18 July 2014
Abstract
Embryonic poly(A)-binding protein (EPAB) and poly(A)-binding protein, cytoplasmic 1 (PABPC1) play critical roles in translational regulation of stored maternal mRNAs required for proper oocyte maturation and early embryo development in mammals. Superovulation is a commonly used technique to obtain a great number of oocytes in the same developmental stages in assisted reproductive technology (ART) and in clinical or experimental animal studies. Previous studies have convincingly indicated that superovulation alone can cause impaired oocyte maturation, delayed embryo development, decreased implantation rate and increased postimplantation loss. Although how superovulation results in these disturbances has not been clearly addressed yet, putative changes in genes related to oocyte and early embryo development seem to be potential risk factors. Thus, the aim of the present study was to determine the effect of superovulation on Epab and Pabpc1 gene expression. To this end, low- (5 IU) and high-dose (10 IU) pregnant mare’s serum gonadotropin (PMSG) and human chorionic gonadotrophin (hCG) were administered to female mice to induce superovulation, with naturally cycling female mice serving as controls. Epab and Pabpc1 gene expression in germinal vesicle (GV) stage oocytes, MII oocytes and 1- and 2-cell embryos collected from each group were quantified using quantitative reverse transcription–polymerase chain reaction. Superovulation with low or high doses of gonadotropins significantly altered Epab and Pabpc1 mRNA levels in GV oocytes, MII oocytes and 1- and 2-cell embryos compared with their respective controls (P < 0.05). These changes most likely lead to variations in expression of EPAB- and PABPC1-regulated genes, which may adversely influence the quality of oocytes and early embryos retrieved using superovulation.
Additional keyword: preimplantation embryo.
References
Allen, W. R., and Moor, R. M. (1972). The origin of the equine endometrial cups. I. Production of PMSG by fetal trophoblast cells. J. Reprod. Fertil. 29, 313–316.| The origin of the equine endometrial cups. I. Production of PMSG by fetal trophoblast cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE387nslKitQ%3D%3D&md5=63c204316b9727aa6c2e7a5226b44cb7CAS | 5023705PubMed |
Beaumont, H. M., and Smith, A. F. (1975). Embryonic mortality during the pre- and post-implantation periods of pregnancy in mature mice after superovulation. J. Reprod. Fertil. 45, 437–448.
| Embryonic mortality during the pre- and post-implantation periods of pregnancy in mature mice after superovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XlsVGnsg%3D%3D&md5=9834b193efc78d8d210c343215c78368CAS | 1206643PubMed |
Bettegowda, A., and Smith, G. W. (2007). Mechanisms of maternal mRNA regulation: implications for mammalian early embryonic development. Front. Biosci. 12, 3713–3726.
| Mechanisms of maternal mRNA regulation: implications for mammalian early embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXms1Kmur0%3D&md5=d64a651f9345fd6d687179e94dde0fb0CAS | 17485333PubMed |
Braude, P., Bolton, V., and Moore, S. (1988). Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 332, 459–461.
| Human gene expression first occurs between the four- and eight-cell stages of preimplantation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhvVCiurk%3D&md5=d5b23fc5fdcef27bba3834605377b26fCAS | 3352746PubMed |
De Geyter, C., De Geyter, M., Steimann, S., Zhang, H., and Holzgreve, W. (2006). Comparative birth weights of singletons born after assisted reproduction and natural conception in previously infertile women. Hum. Reprod. 21, 705–712.
| Comparative birth weights of singletons born after assisted reproduction and natural conception in previously infertile women.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD287ksVWiuw%3D%3D&md5=1afc87e201cfd1ba4b1eb580a0e3c898CAS | 16284064PubMed |
Ertzeid, G., and Storeng, R. (1992). Adverse effects of gonadotrophin treatment on pre- and postimplantation development in mice. J. Reprod. Fertil. 96, 649–655.
| Adverse effects of gonadotrophin treatment on pre- and postimplantation development in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpsVGhtw%3D%3D&md5=25646861cbdec63fb78435f41ec10eefCAS | 1339844PubMed |
Ertzeid, G., and Storeng, R. (2001). The impact of ovarian stimulation on implantation and fetal development in mice. Hum. Reprod. 16, 221–225.
| The impact of ovarian stimulation on implantation and fetal development in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFGrs70%3D&md5=2fcf94966ec5819b5027be9139240981CAS | 11157810PubMed |
Fauque, P., Jouannet, P., Lesaffre, C., Ripoche, M. A., Dandolo, L., Vaiman, D., and Jammes, H. (2007). Assisted reproductive technology affects developmental kinetics, H19 imprinting control region methylation and H19 gene expression in individual mouse embryos. BMC Dev. Biol. 7, 116.
| Assisted reproductive technology affects developmental kinetics, H19 imprinting control region methylation and H19 gene expression in individual mouse embryos.Crossref | GoogleScholarGoogle Scholar | 17949482PubMed |
Flach, G., Johnson, M. H., Braude, P. R., Taylor, R. A., and Bolton, V. N. (1982). The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J. 1, 681–686.
| 1:CAS:528:DyaL38XltVOrsL0%3D&md5=79fe7b91ab21eff1b688ef7d0dffceaaCAS | 7188357PubMed |
Fortier, A. L., Lopes, F. L., Darricarrere, N., Martel, J., and Trasler, J. M. (2008). Superovulation alters the expression of imprinted genes in the midgestation mouse placenta. Hum. Mol. Genet. 17, 1653–1665.
| Superovulation alters the expression of imprinted genes in the midgestation mouse placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvFSrtL8%3D&md5=f3031d9c249a63884e77dbd96904330fCAS | 18287259PubMed |
Gates, A. H. (1956). Viability and developmental capacity of eggs from immature mice treated with gonadotrophins. Nature 177, 754–755.
| Viability and developmental capacity of eggs from immature mice treated with gonadotrophins.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG28%2FnsVCgtQ%3D%3D&md5=a8f2447f91cae3a3a05d13bd0f4932ebCAS | 13321955PubMed |
Guzeloglu-Kayisli, O., Pauli, S., Demir, H., Lalioti, M. D., Sakkas, D., and Seli, E. (2008). Identification and characterization of human embryonic poly(A) binding protein (EPAB). Mol. Hum. Reprod. 14, 581–588.
| Identification and characterization of human embryonic poly(A) binding protein (EPAB).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltV2jtQ%3D%3D&md5=10fa19462007e811dea4420fedb22398CAS | 18716053PubMed |
Guzeloglu-Kayisli, O., Lalioti, M. D., Aydiner, F., Sasson, I., Ilbay, O., Sakkas, D., Lowther, K. M., Mehlmann, L. M., and Seli, E. (2012). Embryonic poly(A)-binding protein (EPAB) is required for oocyte maturation and female fertility in mice. Biochem. J. 446, 47–58.
| Embryonic poly(A)-binding protein (EPAB) is required for oocyte maturation and female fertility in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFShsL%2FI&md5=6bfe0635d6f43197b28ebdced10e2927CAS | 22621333PubMed |
Guzeloglu-Kayisli, O., Lalioti, M. D., Babayev, E., Torrealday, S., Karakaya, C., and Seli, E. (2014). Human embryonic poly(A)-binding protein (EPAB) alternative splicing is differentially regulated in human oocytes and embryos. Mol. Hum. Reprod. 20, 59–65.
| Human embryonic poly(A)-binding protein (EPAB) alternative splicing is differentially regulated in human oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1Gqtg%3D%3D&md5=38beb9fb00c60fd83ae0dd371f9fc30aCAS | 24002949PubMed |
Kozlov, G., Trempe, J. F., Khaleghpour, K., Kahvejian, A., Ekiel, I., and Gehring, K. (2001). Structure and function of the C-terminal PABC domain of human poly(A)-binding protein. Proc. Natl Acad. Sci. USA 98, 4409–4413.
| Structure and function of the C-terminal PABC domain of human poly(A)-binding protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtVagtrw%3D&md5=f6bcd9c9ecea7a6e2ee3c02a30e0490cCAS | 11287632PubMed |
Kumar, T. R., Wang, Y., Lu, N., and Matzuk, M. M. (1997). Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat. Genet. 15, 201–204.
| Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtVOks7c%3D&md5=2386b34fc17798aca3c4aabbd7f6c656CAS | 9020850PubMed |
Laprise, S. L. (2009). Implications of epigenetics and genomic imprinting in assisted reproductive technologies. Mol. Reprod. Dev. 76, 1006–1018.
| Implications of epigenetics and genomic imprinting in assisted reproductive technologies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFent7rF&md5=421c575df5b3020e321f659c81bb35dbCAS | 19484754PubMed |
Liang, X. W., Cui, X. S., Sun, S. C., Jin, Y. X., Heo, Y. T., Namgoong, S., and Kim, N. H. (2013). Superovulation induces defective methylation in line-1 retrotransposon elements in blastocyst. Reprod. Biol. Endocrinol. 11, 69.
| Superovulation induces defective methylation in line-1 retrotransposon elements in blastocyst.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Gksb7I&md5=e2aca1e040de0e94dda53b60b079764bCAS | 23866265PubMed |
Luckett, D. C., and Mukherjee, A. B. (1986). Embryonic characteristics in superovulated mouse strains. Comparative analyses of the incidence of chromosomal aberrations, morphological malformations, and mortality of embryos from two strains of superovulated mice. J. Hered. 77, 39–42.
| 1:STN:280:DyaL287mvFGnug%3D%3D&md5=7c5238ffb7f106962aaa9fcacac86ad6CAS | 3958480PubMed |
Mangus, D. A., Evans, M. C., and Jacobson, A. (2003). Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol. 4, 223.
| Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression.Crossref | GoogleScholarGoogle Scholar | 12844354PubMed |
Market-Velker, B. A., Zhang, L., Magri, L. S., Bonvissuto, A. C., and Mann, M. R. (2010). Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Hum. Mol. Genet. 19, 36–51.
| Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGhu7jL&md5=b8cca1dce26e18349a044f37588dd87fCAS | 19805400PubMed |
Méduri, G., Charnaux, N., Driancourt, M. A., Combettes, L., Granet, P., Vannier, B., Loosfelt, H., and Milgrom, E. (2002). Follicle-stimulating hormone receptors in oocytes? J. Clin. Endocrinol. Metab. 87, 2266–2276.
| Follicle-stimulating hormone receptors in oocytes?Crossref | GoogleScholarGoogle Scholar | 11994374PubMed |
Mundim, T. C., Ramos, A. F., Sartori, R., Dode, M. A., Melo, E. O., Gomes, L. F., Rumpf, R., and Franco, M. M. (2009). Changes in gene expression profiles of bovine embryos produced in vitro, by natural ovulation, or hormonal superstimulation. Genet. Mol. Res. 8, 1398–1407.
| Changes in gene expression profiles of bovine embryos produced in vitro, by natural ovulation, or hormonal superstimulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFWiu73J&md5=3778d68784161b82811e0878e44f041dCAS | 19937584PubMed |
Oh, B., Hwang, S., McLaughlin, J., Solter, D., and Knowles, B. B. (2000). Timely translation during the mouse oocyte-to-embryo transition. Development 127, 3795–3803.
| 1:CAS:528:DC%2BD3cXmvFSmtLw%3D&md5=c4acad185bf50bc14e2805a5b063c8deCAS | 10934024PubMed |
Ozturk, S., Guzeloglu-Kayisli, O., Demir, N., Sozen, B., Ilbay, O., Lalioti, M. D., and Seli, E. (2012). Epab and Pabpc1 are differentially expressed during male germ cell development. Reprod. Sci. 19, 911–922.
| Epab and Pabpc1 are differentially expressed during male germ cell development.Crossref | GoogleScholarGoogle Scholar | 22814100PubMed |
Patsoula, E., Loutradis, D., Drakakis, P., Kallianidis, K., Bletsa, R., and Michalas, S. (2001). Expression of mRNA for the LH and FSH receptors in mouse oocytes and preimplantation embryos. Reproduction 121, 455–461.
| Expression of mRNA for the LH and FSH receptors in mouse oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisFWjsrY%3D&md5=95dae5e89962a8fd53643a89d0cbd3fbCAS | 11226072PubMed |
Patsoula, E., Loutradis, D., Drakakis, P., Michalas, L., Bletsa, R., and Michalas, S. (2003). Messenger RNA expression for the follicle-stimulating hormone receptor and luteinizing hormone receptor in human oocytes and preimplantation-stage embryos. Fertil. Steril. 79, 1187–1193.
| Messenger RNA expression for the follicle-stimulating hormone receptor and luteinizing hormone receptor in human oocytes and preimplantation-stage embryos.Crossref | GoogleScholarGoogle Scholar | 12738515PubMed |
Russell, D. L., and Robker, R. L. (2007). Molecular mechanisms of ovulation: co-ordination through the cumulus complex. Hum. Reprod. Update 13, 289–312.
| Molecular mechanisms of ovulation: co-ordination through the cumulus complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtlCisbc%3D&md5=9facc09dc8d1837b624de765bc168eb6CAS | 17242016PubMed |
Sato, A., Otsu, E., Negishi, H., Utsunomiya, T., and Arima, T. (2007). Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum. Reprod. 22, 26–35.
| Aberrant DNA methylation of imprinted loci in superovulated oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlChtb%2FI&md5=03b71f9ed0e92bc71e7fb1ed070c3ac9CAS | 16923747PubMed |
Seli, E., Lalioti, M. D., Flaherty, S. M., Sakkas, D., Terzi, N., and Steitz, J. A. (2005). An embryonic poly(A)-binding protein (ePAB) is expressed in mouse oocytes and early preimplantation embryos. Proc. Natl Acad. Sci. USA 102, 367–372.
| An embryonic poly(A)-binding protein (ePAB) is expressed in mouse oocytes and early preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXptFSksw%3D%3D&md5=b6899f8fef661f12e06548692e32de61CAS | 15630085PubMed |
Shi, W., and Haaf, T. (2002). Aberrant methylation patterns at the two-cell stage as an indicator of early developmental failure. Mol. Reprod. Dev. 63, 329–334.
| Aberrant methylation patterns at the two-cell stage as an indicator of early developmental failure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnslSnsbg%3D&md5=58d24e2910dc1a4bfed53a7a58a88786CAS | 12237948PubMed |
Tisdall, D. J., Watanabe, K., Hudson, N. L., Smith, P., and McNatty, K. P. (1995). FSH receptor gene expression during ovarian follicle development in sheep. J. Mol. Endocrinol. 15, 273–281.
| FSH receptor gene expression during ovarian follicle development in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpvVGjtb4%3D&md5=aef0ab251167bcb6b38afa6f0a9d18dcCAS | 8748134PubMed |
Van der Auwera, I., and D’Hooghe, T. (2001). Superovulation of female mice delays embryonic and fetal development. Hum. Reprod. 16, 1237–1243.
| Superovulation of female mice delays embryonic and fetal development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzhsVWgsA%3D%3D&md5=2df96480be090e113bb21255dd02e01cCAS | 11387298PubMed |
Voeltz, G. K., Ongkasuwan, J., Standart, N., and Steitz, J. A. (2001). A novel embryonic poly(A) binding protein, ePAB, regulates mRNA deadenylation in Xenopus egg extracts. Genes Dev. 15, 774–788.
| A novel embryonic poly(A) binding protein, ePAB, regulates mRNA deadenylation in Xenopus egg extracts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisFSku7s%3D&md5=50ec2d7d685ae5edd46ab1be6f710940CAS | 11274061PubMed |
Zudova, D., Wyrobek, A. J., Bishop, J., and Marchetti, F. (2004). Impaired fertility in T-stock female mice after superovulation. Reproduction 128, 573–581.
| Impaired fertility in T-stock female mice after superovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVSis7nM&md5=7f6d07a9a67018649036758f061a63edCAS | 15509703PubMed |
