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http://dx.doi.org/10.14348/molcells.2017.0058

Adverse Effect of Superovulation Treatment on Maturation, Function and Ultrastructural Integrity of Murine Oocytes  

Lee, Myungook (Department of Agricultural Biotechnology, Seoul National University)
Ahn, Jong Il (Research Institutes of Agriculture and Life Sciences, Seoul National University)
Lee, Ah Ran (Department of Agricultural Biotechnology, Seoul National University)
Ko, Dong Woo (Department of Agricultural Biotechnology, Seoul National University)
Yang, Woo Sub (Department of Agricultural Biotechnology, Seoul National University)
Lee, Gene (Laboratory of Molecular Genetics, Dental Research Institute, School of Dentistry, Seoul National University)
Ahn, Ji Yeon (Department of Agricultural Biotechnology, Seoul National University)
Lim, Jeong Mook (Department of Agricultural Biotechnology, Seoul National University)
Publication Information
Molecules and Cells / v.40, no.8, 2017 , pp. 558-566 More about this Journal
Abstract
Regular monitoring on experimental animal management found the fluctuation of ART outcome, which showed a necessity to explore whether superovulation treatment is responsible for such unexpected outcome. This study was subsequently conducted to examine whether superovulation treatment can preserve ultrastructural integrity and developmental competence of oocytes following oocyte activation and embryo culture. A randomized study using mouse model was designed and in vitro development (experiment 1), ultrastructural morphology (experiment 2) and functional integrity of the oocytes (experiment 3) retrieved after PMSG/hCG injection (superovulation group) or not (natural ovulation; control group) were evaluated. In experiment 1, more oocytes were retrieved following superovulation than following natural ovulation, but natural ovulation yielded higher (p < 0.0563) maturation rate than superovulation. The capacity of mature oocytes to form pronucleus and to develop into blastocysts in vitro was similar. In experiment 2, a notable (p < 0.0186) increase in mitochondrial deformity, characterized by the formation of vacuolated mitochondria, was detected in the superovulation group. Multivesicular body formation was also increased, whereas early endosome formation was significantly decreased. No obvious changes in other microorganelles, however, were detected, which included the formation and distribution of mitochondria, cortical granules, microvilli, and smooth and rough endoplasmic reticulum. In experiment 3, significant decreases in mitochondrial activity, ATP production and dextran uptake were detected in the superovulation group. In conclusion, superovulation treatment may change both maturational status and functional and ultrastuctural integrity of oocytes. Superovulation effect on preimplantation development can be discussed.
Keywords
artificial reproductive Technology (ART); development; gonadotrophins; microorganelle function; oocyte maturation;
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1 Assey, R.J., Hyttel, P., Roche, J.F., and Boland, M. (1994). Oocyte structure and follicular steroid concentrations in superovulated versus unstimulated heifers. Mol. Reprod. Dev. 39, 8-16.   DOI
2 Baart, E.B., Martini, E., Eijkemans, M.J., Van Opstal, D., Beckers, N.G., Verhoeff, A., Macklon, N.S., and Fauser, B.C. (2007). Milder ovarian stimulation for in-vitro fertilization reduces aneuploidy in the human preimplantation embryo: a randomized controlled trial. Hum. Reprod. 22, 980-988.   DOI
3 Balaban, R.S., Nemoto, S., and Finkel, T. (2005). Mitochondria, oxidants, and aging. Cell 120, 483-495.   DOI
4 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.   DOI
5 Burdette, J.E., Kurley, S.J., Kilen, S.M., Mayo, K.E., and Woodruff, T.K. (2006). Gonadotropin-induced superovulation drives ovarian surface epithelia proliferation in CD1 mice. Endocrinology 147, 2338-2345.   DOI
6 Byers, S.L., Payson, S.J., and Taft, R.A. (2006). Performance of ten inbred mouse strains following assisted reproductive technologies (ARTs). Theriogenology 65, 1716-1726.   DOI
7 Calarco, P.G. (1995). Polarization of mitochondria in the unfertilized mouse oocyte. Dev. Genet. 16, 36-43.   DOI
8 Chi, S., Cao, H., Wang, Y., and McNiven, M.A. (2011). Recycling of the epidermal growth factor receptor is mediated by a novel form of the clathrin adaptor protein Eps15. J. Biol. Chem. 286, 35196-35208.   DOI
9 Combelles, C.M., and Albertini, D.F. (2003). Assessment of oocyte quality following repeated gonadotropin stimulation in the mouse. Biol. Reprod. 68, 812-821.   DOI
10 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.   DOI
11 Miller, B.G., and Armstrong, D.T. (1981). Effects of a superovulatory dose of pregnant mare serum gonadotropin on ovarian function, serum estradiol, and progesterone levels and early embryo development in immature rats. Biol. Reprod. 25, 261-271.   DOI
12 Moor, R.M., Osborn, J.C., and Crosby, I.M. (1985). Gonadotrophininduced abnormalities in sheep oocytes after superovulation. J. Reprod. Fertil. 74, 167-172.   DOI
13 Moore, A., Weissleder, R., and Bogdanov, A., Jr. (1997). Uptake of dextran-coated monocrystalline iron oxides in tumor cells and macrophages. J. Magn. Reson. Imaging 7, 1140-1145.   DOI
14 Munoz, I., Rodriguez de Sadia, C., Gutierrez, A., Blanquez, M.J., and Pintado, B. (1994). Comparison of superovulatory response of mature outbred mice treated with FSH or PMSG and developmental potential of embryos produced. Theriogenology 41, 907-914.   DOI
15 Nagy A, G.M., Vintersten K & Behringer T (2003). Manipulating the Mouse Embryo: A Laboratory Manual (Cold Spring Harbor).
16 Ozturk, S., Yaba-Ucar, A., Sozen, B., Mutlu, D., and Demir, N. (2016). Superovulation alters embryonic poly(A)-binding protein (Epab) and poly(A)-binding protein, cytoplasmic 1 (Pabpc1) gene expression in mouse oocytes and early embryos. Reprod. Fertil. Dev. 28, 375-383.   DOI
17 Plachot, M. (2003). Genetic analysis of the oocyte--a review. Placenta 24 Suppl B, S66-69.   DOI
18 Edwards, R.G., and Gates, A.H. (1959). Timing of the stages of the maturation divisions, ovulation, fertilization and the first cleavage of eggs of adult mice treated with gonadotrophins. J. Endocrinol. 18, 292-304.   DOI
19 Qin, J.Z., Pang, L.H., Li, M.Q., Xu, J., and Zhou, X. (2013). Risk of chromosomal abnormalities in early spontaneous abortion after assisted reproductive technology: a meta-analysis. PLoS One 8, e75953.   DOI
20 Eden, E.R., White, I.J., and Futter, C.E. (2009). Down-regulation of epidermal growth factor receptor signalling within multivesicular bodies. Biochem. Soc. Trans. 37, 173-177.   DOI
21 Field, C., Li, R., and Oegema, K. (1999). Cytokinesis in eukaryotes: a mechanistic comparison. Curr. Opin. Cell Biol. 11, 68-80.   DOI
22 Eichenlaub-Ritter, U., Vogt, E., Yin, H., and Gosden, R. (2004). Spindles, mitochondria and redox potential in ageing oocytes. Reprod. Biomed. Online 8, 45-58.   DOI
23 Elbling, L., and Colot, M. (1985). Abnormal development and transport and increased sister-chromatid exchange in preimplantation embryos following superovulation in mice. Mutat Res 147, 189-195.   DOI
24 Ertzeid, G., and Storeng, R. (1992). Adverse effects of gonadotrophin treatment on pre- and postimplantation development in mice. J. Reprod. Fertil. 96, 649-655.   DOI
25 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.   DOI
26 Fowler, R.E., and Edwards, R.G. (1957). Induction of superovulation and pregnancy in mature mice by gonadotrophins. J. Endocrinol. 15, 374-384.   DOI
27 Fowler, R.E., and Edwards, R.G. (1960). Effect of progesterone and oestrogen on pregnancy and embryonic mortality in adult mice following superovulation treatment. J. Endocrinol. 20, 1-8.   DOI
28 Dobrowolski, R., and De Robertis, E.M. (2011). Endocytic control of growth factor signalling: multivesicular bodies as signalling organelles. Nat. Rev. Mol. Cell Biol. 13, 53-60.
29 Steward, R.G., Lan, L., Shah, A.A., Yeh, J.S., Price, T.M., Goldfarb, J.M., and Muasher, S.J. (2014). Oocyte number as a predictor for ovarian hyperstimulation syndrome and live birth: an analysis of 256,381 in vitro fertilization cycles. Fertil. Steril. 101, 967-973.   DOI
30 Salminen, A., Kaarniranta, K., Hiltunen, M., and Kauppinen, A. (2014). Krebs cycle dysfunction shapes epigenetic landscape of chromatin: novel insights into mitochondrial regulation of aging process. Cell Signal. 26, 1598-1603.   DOI
31 Takeuchi, T., Neri, Q.V., Katagiri, Y., Rosenwaks, Z., and Palermo, G.D. (2005). Effect of treating induced mitochondrial damage on embryonic development and epigenesis. Biol. Reprod. 72, 584-592.   DOI
32 Templeton, A., and Morris, J.K. (1998). Reducing the risk of multiple births by transfer of two embryos after in vitro fertilization. N Engl. J. Med. 339, 573-577.   DOI
33 West, M.A., Wallin, R.P., Matthews, S.P., Svensson, H.G., Zaru, R., Ljunggren, H.G., Prescott, A.R., and Watts, C. (2004). Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 305, 1153-1157.   DOI
34 Van Blerkom, J. (1991). Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured mouse oocytes. Proc. Natl. Acad. Sci. USA 88, 5031-5035.   DOI
35 Van Blerkom, J., and Runner, M.N. (1984). Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte. Am. J. Anat. 171, 335-355.   DOI
36 Van der Auwera, I., and D'Hooghe, T. (2001). Superovulation of female mice delays embryonic and fetal development. Hum. Reprod. 16, 1237-1243.   DOI
37 Yun, Y.W., Yu, F.H., Yuen, B.H., and Moon, Y.S. (1989). Effects of a superovulatory dose of pregnant mare serum gonadotropin on follicular steroid contents and oocyte maturation in rats. Gamete Res. 23, 289-298.   DOI
38 Guerin, P., El Mouatassim, S., and Menezo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the preimplantation embryo and its surroundings. Hum. Reprod. Update 7, 175-189.   DOI
39 Ghavami, M., Mohammadnejad, D., Beheshti, R., Solmani-Rad, J., and Abedelahi, A. (2015). Ultrastructural and Morphalogical Changes of Mouse Ovarian Tissues Following Direct Cover Vitrification with Different Cryoprotectants. J. Reprod. Infertil. 16, 138-147.
40 Gras, L., McBain, J., Trounson, A., and Kola, I. (1992). The incidence of chromosomal aneuploidy in stimulated and unstimulated (natural) uninseminated human oocytes. Hum. Reprod. 7, 1396-1401.   DOI
41 Hamberger, L., and Wikland, M. (1993). Regulations and results concerning assisted reproduction in Sweden. J. Assist. Reprod. Genet. 10, 243-245.   DOI
42 Hasegawa, A., Takahashi, T., Igarashi, H., Amita, M., Matsukawa, J., and Nagase, S. (2015). Predictive factors for oocyte retrieval failure in controlled ovarian hyperstimulation protocols: a retrospective observational cohort study. Reprod. Biol. Endocrinol. 13, 53.   DOI
43 Hohmann, F.P., Macklon, N.S., and Fauser, B.C. (2003). A randomized comparison of two ovarian stimulation protocols with gonadotropin-releasing hormone (GnRH) antagonist cotreatment for in vitro fertilization commencing recombinant follicle-stimulating hormone on cycle day 2 or 5 with the standard long GnRH agonist protocol. J. Clin. Endocrinol. Metab. 88, 166-173.   DOI
44 Kulkarni, G.V., Lee, W., Seth, A., and McCulloch, C.A. (1998). Role of mitochondrial membrane potential in concanavalin A-induced apoptosis in human fibroblasts. Exp. Cell Res. 245, 170-178.   DOI
45 Huffman, S.R., Pak, Y., and Rivera, R.M. (2015). Superovulation induces alterations in the epigenome of zygotes, and results in differences in gene expression at the blastocyst stage in mice. Mol. Reprod. Dev. 82, 207-217.   DOI
46 Jang, M., Lee, E.J., Lee, S.T., Cho, M., and Lim, J.M. (2007). Preimplantation and fetal development of mouse embryos cultured in a protein-free, chemically defined medium. Fertil. Steril. 87, 445-447.   DOI
47 Ziebe, S., Bangsboll, S., Schmidt, K.L., Loft, A., Lindhard, A., and Nyboe Andersen, A. (2004). Embryo quality in natural versus stimulated IVF cycles. Hum. Reprod. 19, 1457-1460.   DOI
48 Kalthur, G., Salian, S.R., Nair, R., Mathew, J., Adiga, S.K., Kalthur, S.G., Zeegers, D., and Hande, M.P. (2015). Distribution pattern of cytoplasmic organelles, spindle integrity, oxidative stress, octamerbinding transcription factor 4 (Oct4) expression and developmental potential of oocytes following multiple superovulation. Reprod. Fertil. Dev. doi: 10.1071/RD15184. [Epub ahead of print]   DOI
49 Katzmann, D.J., Odorizzi, G., and Emr, S.D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3, 893-905.   DOI
50 Kim, K.W. (2008). Visualization of micromorphology of leaf epicuticular waxes of the rubber tree Ficus elastica by electron microscopy. Micron 39, 976-984.   DOI
51 Labarta, E., Bosch, E., Alama, P., Rubio, C., Rodrigo, L., and Pellicer, A. (2012). Moderate ovarian stimulation does not increase the incidence of human embryo chromosomal abnormalities in in vitro fertilization cycles. J. Clin. Endocrinol. Metab. 97, E1987-1994.   DOI
52 Legge, M., and Sellens, M.H. (1994). Optimization of superovulation in the reproductively mature mouse. J. Assist. Reprod. Genet. 11, 312-318.   DOI
53 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.   DOI
54 Mancini, M., Anderson, B.O., Caldwell, E., Sedghinasab, M., Paty, P.B., and Hockenbery, D.M. (1997). Mitochondrial proliferation and paradoxical membrane depolarization during terminal differentiation and apoptosis in a human colon carcinoma cell line. J. Cell Biol. 138, 449-469.   DOI