Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-23T00:29:34.632Z Has data issue: false hasContentIssue false

Effects of embryonic stem cell-conditioned medium on the preimplantation development of mouse embryos

Published online by Cambridge University Press:  17 February 2022

Saber Miraki
Affiliation:
Department of Anatomy, Faculty of Medicine, Kurdistan University of Medical Sciences, Sanandaj, Iran
Asrin Rashidi
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Omid Banafshi
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Masoud Alasvand
Affiliation:
Cancer and Immunology Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Fardin Fathi*
Affiliation:
Department of Anatomy, Faculty of Medicine, Kurdistan University of Medical Sciences, Sanandaj, Iran
Mohammad Ghasem Golmohammadi
Affiliation:
Research Laboratory for Embryology and Stem Cells, Department of Anatomical Sciences, School of Medicine, Ardabil University of Medical Sciences, Ardabil, Iran
*
Author for correspondence: Fardin Fathi, Department of Anatomy, Faculty of Medicine, Kurdistan University of Medical Sciences, Pasdaran St, Sanandaj, Iran. Tel: +98 87 33664673. E-mail: farfath@gmail.com

Summary

The production of high-quality embryos in the laboratory and a successful pregnancy are closely related to the condition and contents of oocyte and embryo culture media. In this study, we investigated the effects of embryonic stem cell-conditioned medium (ESCCM) and embryonic stem cells growth medium (ESCGM) compared with potassium-enriched simplex optimized medium (KSOM) on preimplantation embryo development stages during natural or in vitro fertilization (IVF). Birth rate of pups was measured. To obtain mature oocytes, and 2-cell and 8-cell embryos, human chorionic gonadotropin (HCG) was injected 48 h after i.p. injection of 5 units of pregnant mare serum gonadotropin. Mature oocytes were obtained from non-mated female mice 14 h after HCG injection. To obtain 2-cell and 8-cell embryos, mated female mice, 1 day and 3 days, respectively, after HCG injection, were used. Mature oocytes were fertilized in HTF medium. Embryos obtained from natural or in vitro fertilization were cultured in experimental media, ESCCM and ESCGM, or KSOM as the control culture medium. Embryos that developed to the blastocyst stage were transferred to the uteri of pseudopregnant mice and effects of the experimental media on embryo viability were determined. ESCCM and ESCGM could not pass the embryo after the 2-cell stage, but they were suitable for the development of the embryo from the 8-cell stage to the blastocyst. It can be concluded that the embryo has various requirements at different stages of development.

Type
Research Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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

Abramczuk, J, Solter, D and Koprowski, H (1977). The beneficial effect of EDTA on development of mouse one-cell embryos in chemically defined medium. Dev Biol 61, 378–83.CrossRefGoogle ScholarPubMed
Adib, M, Seifati, SM, Dehghani Ashkezari, M, Akyash, F, Khoradmehr, A and Aflatoonian, B (2020). Effect of human testicular cells conditioned medium on in vitro maturation and morphology of mouse oocytes. Int J Fertil Steril 14, 175–84.Google ScholarPubMed
Agarwal, A, Durairajanayagam, D and Du Plessis, SS (2014). Utility of antioxidants during assisted reproductive techniques: an evidence based review. Reprod Biol Endocrinol 12, 112.CrossRefGoogle Scholar
Alak, BM, Coskun, S, Friedman, CI, Kennard, EA, Kim, MH and Seifer, DB (1998). Activin A stimulates meiotic maturation of human oocytes and modulates granulosa cell steroidogenesis in vitro . Fertil Steril 70, 1126–30.CrossRefGoogle ScholarPubMed
Amit, M, Carpenter, MK, Inokuma, MS, Chiu, CP, Harris, CP, Waknitz, MA, Itskovitz-Eldor, J and Thomson, JA (2000). Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 227, 271–8.CrossRefGoogle ScholarPubMed
Arat, S, Caputcu, AT, Cevik, M, Akkoc, T, Cetinkaya, G and Bagis, H (2016). Effect of growth factors on oocyte maturation and allocations of inner cell mass and trophectoderm cells of cloned bovine embryos. Zygote 24, 554–62.CrossRefGoogle ScholarPubMed
Bavister, B (2000). Interactions between embryos and the culture milieu. Theriogenology 53, 619–26.CrossRefGoogle ScholarPubMed
Beebe, LF and Kaye, PL (1991). Maternal diabetes and retarded preimplantation development of mice. Diabetes 40, 457–61.CrossRefGoogle ScholarPubMed
Ben-Rafael, Z, Benadiva, CA, Ausmanas, M, Barber, B, Blasco, L, Flickinger, GL and Mastroianni, L (1987). Dose of human menopausal gonadotropin influences the outcome of an in vitro fertilization program. Fertil Steril 48, 964–68.CrossRefGoogle ScholarPubMed
Bendall, SC, Hughes, C, Campbell, JL, Stewart, MH, Pittock, P, Liu, S, Bonneil, E, Thibault, P, Bhatia, M and Lajoie, GA (2009). An enhanced mass spectrometry approach reveals human embryonic stem cell growth factors in culture. Mol Cell Proteomics 8, 421–32.CrossRefGoogle ScholarPubMed
Biggers, J, Whittingham, D and Donahue, R (1967). The pattern of energy metabolism in the mouse oocyte and zygote. Proc Natl Acad Sci USA 58, 560–67.CrossRefGoogle ScholarPubMed
Brinster, RL (1965). Studies on the development of mouse embryos in vitro. IV Interaction of energy sources. J Reprod Fertil 10, 227–40.CrossRefGoogle ScholarPubMed
Brinster, R and Thomson, JL (1966). Development of eight-cell mouse embryos in vitro . Exp Cell Res 42, 308–15.CrossRefGoogle ScholarPubMed
Brower, PT and Schultz, RM (1982). Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth. Dev Biol 90, 144–53.CrossRefGoogle ScholarPubMed
Chronopoulou, E and Harper, JC (2015). IVF culture media: past, present and future. Hum Reprod Update 21, 3955.CrossRefGoogle ScholarPubMed
Conaghan, J, Handyside, A, Winston, R and Leese, H (1993). Effects of pyruvate and glucose on the development of human preimplantation embryos in vitro . J Reprod Fertil 99, 8795.CrossRefGoogle ScholarPubMed
Das, K, Stout, LE, Hensleigh, HC, Tagatz, GE, Phipps, WR and Leung, BS (1991). Direct positive effect of epidermal growth factor on the cytoplasmic maturation of mouse and human oocytes. Fertil Steril 55, 1000–4.CrossRefGoogle ScholarPubMed
De La Fuente, R, O’Brien, MJ and Eppig, JJ (1999). Epidermal growth factor enhances preimplantation developmental competence of maturing mouse oocytes. Human Reproduction 14, 3060–68.CrossRefGoogle ScholarPubMed
De Matos, DG, Miller, K, Scott, R, Tran, CA, Kagan, D, Nataraja, SG, Clark, A and Palmer, S (2008). Leukemia inhibitory factor induces cumulus expansion in immature human and mouse oocytes and improves mouse two-cell rate and delivery rates when it is present during mouse in vitro oocyte maturation. Fertil Steril 90, 2367–75.CrossRefGoogle ScholarPubMed
Desai, N, Abdelhafez, F, Bedaiwy, MA and Goldfarb, J (2008). Live births in poor prognosis IVF patients using a novel non-contact human endometrial co-culture system. Reprod Biomed Online 16, 869–74.CrossRefGoogle ScholarPubMed
Desai, N, Alex, A, Abdelhafez, F, Calabro, A, Goldfarb, J, Fleischman, A and Falcone, T (2010). Three-dimensional in vitro follicle growth: overview of culture models, biomaterials, design parameters and future directions. Reprod Biol Endocrinol 8, 119.CrossRefGoogle ScholarPubMed
Desai, N, Lawson, J and Goldfarb, J (2000) Assessment of growth factor effects on post-thaw development of cryopreserved mouse morulae to the blastocyst stage. Hum Reprod 15, 410–18.CrossRefGoogle Scholar
Dimitriadis, E, Stoikos, C, Stafford-Bell, M, Clark, I, Paiva, P, Kovacs, G and Salamonsen, LA (2006). Interleukin-11, IL-11 receptora and leukemia inhibitory factor are dysregulated in endometrium of infertile women with endometriosis during the implantation window. J Reprod Immunol 69, 5364.CrossRefGoogle Scholar
Eppig, JJ (2018). Reproduction: oocytes call, granulosa cells connect. Curr Biol 28, R3546.CrossRefGoogle ScholarPubMed
Fathi, F, Altiraihi, T, Mowla, SJ and Movahedin, M (2010). Transplantation of retinoic acid treated murine embryonic stem cells & behavioural deficit in Parkinsonian rats. Indian J Med Res 131, 536–44.Google ScholarPubMed
Fatma, S, Selby, DE, Singla, RD and Singla, DK (2010). Factors released from embryonic stem cells stimulate c-kit-FLK-1(+ve) progenitor cells and enhance neovascularization. Antioxid Redox Signal 13, 1857–65.CrossRefGoogle ScholarPubMed
Feng, P, Catt, KJ and Knecht, M (1988). Transforming growth factor-β stimulates meiotic maturation of the rat oocyte. Endocrinology 122, 181–86.CrossRefGoogle ScholarPubMed
Fuchs, E, Tumbar, T and Guasch, G (2004). Socializing with the neighbors: stem cells and their niche. Cell 116, 769–78.CrossRefGoogle ScholarPubMed
Gardner, DK and Lane, M (1996). Alleviation of the ‘2-cell block’ and development to the blastocyst of CF1 mouse embryos: role of amino acids, EDTA and physical parameters. Hum Reprod 11, 2703–12.CrossRefGoogle Scholar
Gelber, K, Tamura, AN, Alarcon, VB and Marikawa, Y (2011). A potential use of embryonic stem cell medium for the in vitro culture of preimplantation embryos. J Assist Reprod Genet 28, 659–68.CrossRefGoogle ScholarPubMed
Giuffrida, D, Rogers, IM, Nagy, A, Calogero, AE, Brown, TJ and Casper, RF (2009). Human embryonic stem cells secrete soluble factors that inhibit cancer cell growth. Cell Prolif 42, 788–98.CrossRefGoogle ScholarPubMed
Głabowski, W, Kurzawa, R, Wiszniewska, B, Baczkowski, T, Marchlewicz, M and Brelik, P (2005). Growth factors effects on preimplantation development of mouse embryos exposed to tumor necrosis factor alpha. Reprod Biol 5, 8399.Google ScholarPubMed
Gómez, E, Tarin, JJ and Pellicer, A (1993). Oocyte maturation in humans: the role of gonadotropins and growth factors. Fertil Steril 60, 40–6.CrossRefGoogle ScholarPubMed
Guo, Y, Graham-Evans, B and Broxmeyer, HE (2006). Murine embryonic stem cells secrete cytokines/growth modulators that enhance cell survival/anti-apoptosis and stimulate colony formation of murine hematopoietic progenitor cells. Stem Cells 24, 850–56.CrossRefGoogle ScholarPubMed
Harvey, MB and Kaye, PL (1991). Mouse blastocysts respond metabolically to short-term stimulation by insulin and IGF-1 through the insulin receptor. Mol Reprod Dev 29, 253–58.CrossRefGoogle ScholarPubMed
Heyner, S, Smith, RM and Schultz, GA (1989). Temporally regulated expression of insulin and insulin-like growth factors and their receptors in early mammalian development. Bioessays 11, 171–76.CrossRefGoogle ScholarPubMed
Jafarzadeh, H, Nazarian, H, Ghaffari Novin, M, Shams Mofarahe, Z, Eini, F and Piryaei, A (2018). Improvement of oocyte in vitro maturation from mice with polycystic ovary syndrome by human mesenchymal stromal cell-conditioned media. J Cell Biochem 119, 10365–75.CrossRefGoogle ScholarPubMed
Kim, J, Funahashi, H, Niwa, K and Okuda, K (1993). Glucose requirement at different developmental stages of in vitro fertilized bovine embryos cultured in semi-defined medium. Theriogenology 39, 875–86.CrossRefGoogle ScholarPubMed
LaFramboise, WA, Petrosko, P, Krill-Burger, JM, Morris, DR, McCoy, AR, Scalise, D, Malehorn, DE, Guthrie, RD, Becich, MJ and Dhir, R (2010). Proteins secreted by embryonic stem cells activate cardiomyocytes through ligand binding pathways. J Proteomics 73, 9921003.CrossRefGoogle ScholarPubMed
Lighten, AD, Hardy, K, Winston, RM and Moore, GE (1997). Expression of mRNA for the insulin-like growth factors and their receptors in human preimplantation embryos. Mol Reprod Dev 47, 134–39.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
Ling, B, Feng, D, Zhou, Y, Gao, T, Wei, H and Tian, Z (2008). Effect of conditioned medium of mesenchymal stem cells on the in vitro maturation and subsequent development of mouse oocyte. Braz J Med Biol Res 41, 978–85.CrossRefGoogle ScholarPubMed
Lorenzo, P, Illera, J, Silvan, G, Munro, C, Illera, M and Illera, M (1997). Steroid-level response to insulin-like growth factor-1 in oocytes matured in vitro . J Reprod Immunol 35, 1129.CrossRefGoogle ScholarPubMed
Makarevich, AV and Markkula, M (2002). Apoptosis and cell proliferation potential of bovine embryos stimulated with insulin-like growth factor I during in vitro maturation and culture. Biol Reprod 66, 386–92.CrossRefGoogle ScholarPubMed
Malekshah, AK, Moghaddam, AE and Daraka, SM (2006) Comparison of conditioned medium and direct co-culture of human granulosa cells on mouse embryo development. Indian J Exp Biol 44, 189–92.Google ScholarPubMed
Meiyu, Q, Liu, D and Roth, Z (2015). IGF-I slightly improves nuclear maturation and cleavage rate of bovine oocytes exposed to acute heat shock in vitro . Zygote 23, 514–24.CrossRefGoogle ScholarPubMed
Miraki, S, Mokarizadeh, A, Banafshi, O, Assadollahi, V, Abdi, M, Roshani, D and Fathi, F (2017). Embryonic stem cell conditioned medium supports in vitro maturation of mouse oocytes. Avicenna J Med Biotechnol 9, 114–9.Google ScholarPubMed
Möller, B, Rasmussen, C, Lindblom, B and Olovsson, M (2001). Expression of the angiogenic growth factors VEGF, FGF-2, EGF and their receptors in normal human endometrium during the menstrual cycle. Mol Hum Reprod 7, 6572.CrossRefGoogle ScholarPubMed
Nagy, A, Gertsenstein, M, Vintersten, K and Behringer, R (2003). Manipulating the Mouse Embryo: A Laboratory Manual. Firefly Books.Google Scholar
Naveiras, O and Daley, GQ (2006). Stem cells and their niche: a matter of fate. Cell Mol Life Sci 63, 760–6.CrossRefGoogle ScholarPubMed
Nottola, SA, Cecconi, S, Bianchi, S, Motta, C, Rossi, G, Continenza, MA and Macchiarelli, G (2011). Ultrastructure of isolated mouse ovarian follicles cultured in vitro . Reprod Biol Endocrinol 9, 3.CrossRefGoogle ScholarPubMed
Odorico, JS, Kaufman, DS and Thomson, JA (2001). Multilineage differentiation from human embryonic stem cell lines. Stem Cells 19, 193204.CrossRefGoogle ScholarPubMed
Österlund, C, Wramsby, H and Pousette, Å (1996). Preimplantation embryology: temporal expression of platelet-derived growth factor (PDGF)-A and its receptor in human preimplantation embryos. Mol Hum Reprod 2, 507–12.CrossRefGoogle Scholar
Paria, B, Lim, H, Das, SK, Reese, J and Dey, S (2000). Molecular signaling in uterine receptivity for implantation. Semin Cell Dev Biol 11, 6776.CrossRefGoogle ScholarPubMed
Pawshe, CH, Rao, KB and Totey, SM (1998). Effect of insulin-like growth factor I and its interaction with gonadotropins on in vitro maturation and embryonic development, cell proliferation, and biosynthetic activity of cumulus-oocyte complexes and granulosa cells in buffalo. Mol Reprod Dev 49, 277–85.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Picton, HM, Harris, SE, Muruvi, W and Chambers, EL (2008). The in vitro growth and maturation of follicles. Reproduction 136, 703–15.CrossRefGoogle ScholarPubMed
Richani, D and Gilchrist, RB (2018). The epidermal growth factor network: role in oocyte growth, maturation and developmental competence. Hum Reprod Update 24, 114.CrossRefGoogle ScholarPubMed
Richter, KS (2008). The importance of growth factors for preimplantation embryo development and in-vitro culture. Curr Opin Obstet Gynecol 20, 292304.CrossRefGoogle ScholarPubMed
Sakkas, D and Trounson, A (1991). Formulation of a complex serum-free medium (CSM) for use in the co-culture of mouse embryos with cells of the female reproductive tract. Reprod Fertil Dev 3, 99108.CrossRefGoogle ScholarPubMed
Schultz, RM and Williams, CJ (2002). The science of ART. Science 296, 2188–90.CrossRefGoogle Scholar
Smith, AG, Heath, JK, Donaldson, DD, Wong, GG, Moreau, J, Stahl, M and Rogers, D (1988) Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 336, 688.CrossRefGoogle ScholarPubMed
Smotrich, DB, Stillman, RJ, Widra, EA, Gindoff, PR, Kaplan, P, Graubert, M and Johnson, KE (1996). Immunocytochemical localization of growth factors and their receptors in human pre-embryos and Fallopian tubes. Hum Reprod 11, 184–90.CrossRefGoogle ScholarPubMed
Stewart, CL, Kaspar, P, Brunet, LJ, Bhatt, H, Gadi, I, Köntgen, F and Abbondanzo, SJ (1992). Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359, 76–9.CrossRefGoogle ScholarPubMed
Swain, JE (2010) Optimizing the culture environment in the IVF laboratory: impact of pH and buffer capacity on gamete and embryo quality. Reprod Biomed Online 21, 616.CrossRefGoogle ScholarPubMed
Taketsuru, H and Kaneko, T (2016). In vitro maturation of immature rat oocytes under simple culture conditions and subsequent developmental ability. J Reprod Dev 62, 521–26.CrossRefGoogle ScholarPubMed
Thomson, JA, Itskovitz-Eldor, J, Shapiro, SS, Waknitz, MA, Swiergiel, JJ, Marshall, VS and Jones, JM (1998). Embryonic stem cell lines derived from human blastocysts. Science 282, 1145–7.CrossRefGoogle ScholarPubMed
Thongkittidilok, C, Tharasanit, T, Sananmuang, T, Buarpung, S and Techakumphu, M (2014). Insulin-like growth factor-1 (IGF-1) enhances developmental competence of cat embryos cultured singly by modulating the expression of its receptor (IGF-1R) and reducing developmental block. Growth Horm IGF Res 24, 7682.CrossRefGoogle ScholarPubMed
Wånggren, K, Lalitkumar, PG, Hambiliki, F, Ståbi, B, Gemzell-Danielsson, K and Stavreus-Evers, A (2007). Leukaemia inhibitory factor receptor and gp130 in the human fallopian tube and endometrium before and after mifepristone treatment and in the human preimplantation embryo. Mol Hum Reprod 13, 391–97.CrossRefGoogle ScholarPubMed
Williams, RL, Hilton, DJ, Pease, S, Willson, TA, Stewart, CL, Gearing, DP, Wagner, EF, Metcalf, D, Nicola, NA and Gough, NM (1988). Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 336, 684–7.CrossRefGoogle ScholarPubMed
Ying, QL, Nichols, J, Chambers, I and Smith, A (2003). BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115, 281–92.CrossRefGoogle ScholarPubMed