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Effect of lanosterol on the in vitro maturation in semi-defined culture system of prepubertal ewe oocytes

Published online by Cambridge University Press:  15 August 2011

F. Marco-Jiménez*
Affiliation:
Laboratory of Biotechnology of Reproduction, Institute of Science and Animal Technology (ICTA) at the Polytechnic University of Valencia, C/Camino de Vera s/n, 46022 Valencia, Spain. Institute of Science and Animal Technology, Laboratorio de Biotecnología de la Reproducción, Universidad Politécnica de Valencia, Valencia, 46022, Spain.
J.S. Vicente
Affiliation:
Institute of Science and Animal Technology, Laboratorio de Biotecnología de la Reproducción, Universidad Politécnica de Valencia, Valencia, 46022, Spain.
M.P. Viudes-de-Castro
Affiliation:
Centro de Investigación y Tecnología Animal, Instituto Valenciano de Investigaciones Agrarias, Segorbe, 12400, Spain.
*
All correspondence to: Francisco Marco-Jiménez, Laboratory of Biotechnology of Reproduction, Institute of Science and Animal Technology (ICTA) at the Polytechnic University of Valencia, C/Camino de Vera s/n, 46022 Valencia, Spain. Tel.: +34 96 3879435. Fax: +34 96 3877439. e-mail address: fmarco@dca.upv.es

Summary

The choice of medium and supplements can affect meiotic regulation and may have an impact on the regulation of mammalian oocyte growth and embryonic cell function. The aim of the present study was to assess the effects of oxygen concentration and endogenous lanosterol on the in vitro maturation (IVM) media without serum and based on recombinant human chorionic gonadotrophin in prepubertal ewe oocytes. Firstly, the effect of varying oxygen concentrations (5% and 20%) during IVM in TCM-199 supplemented (4 mg/ml bovine serum albumin (BSA), 100 μM cysteamine, 0.3 mM sodium pyruvate, 0.1 UI/ml recombinant follicle-stimulating hormone (r-FSH; Gonal-F® 75 UI, Serono, Italy), 0.1 UI/ml recombinant leuteinizing hormone (r-LH; Lhadi® 75 UI, Serono, Italy) and 1 μg/ml estradiol-17β) on subsequent nuclear maturation of oocytes examined under ultraviolet light following staining with bisbenzimide (Hoechst 33342) was investigated. Secondly, two concentrations of lanosterol (0, 10 and 50 μM) were added to the IVM medium. Nuclear maturation of oocytes was examined as previously. Lipid content in oocytes, an important indicator of cytoplasmic maturity, was also measured using Nile red fluorescent stain. The results showed that low oxygen concentration affected the nuclear maturation. Similarly, a significantly higher rate of meiosis resumption was observed with 10 μM (72.3%) of lanosterol compared with the control (51.8%) or 50 μM of lanosterol (59.4%). A significantly higher content of lipids was also observed with 10 and 50 μM of lanosterol (7.3 ± 0.2 × 106 and 7.4 ± 0.2 × 106 arbitrary units of fluorescence) compared with the control (6.7 ± 0.2 × 106 arbitrary units of fluorescence). The results indicate that 10 μM lanosterol during IVM in medium without serum and based on recombinant human chorionic gonadotrophin has a positive effect on maturation of prepubertal ewe oocytes.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011 

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References

Accardo, C., Dattena, M., Pilichi, S., Mara, L., Chessa, B. & Cappai, P. (2004). Effect of recombinant human FSH and LH on in vitro maturation of sheep oocytes; embryo development and viability. Anim Reprod Sci 81, 7786.CrossRefGoogle ScholarPubMed
Ali, A. & Sirard, M.A. (2002a). The effects of 17β-estradiol and protein supplement on the response to purified and recombinant follicle stimulating hormone in bovine oocytes. Zygote. 10, 6571.CrossRefGoogle ScholarPubMed
Ali, A. & Sirard, M.A. (2002b). Effect of the absence or presence of various protein supplements on further development of bovine oocytes during in vitro maturation. Biol. Reprod. 66, 901–5.CrossRefGoogle ScholarPubMed
Anderiesz, C., Ferraretti, A., Magli, C., Fiorentino, A., Fortini, D., Gianaroli, L., Jones, G.M. & Trounson, A.O. (2000). Effect of recombinant human gonadotrophins on human, bovine and murine oocyte meiosis, fertilisation and embryonic development in vitro Hum. Reprod. 15, 1140–8.CrossRefGoogle ScholarPubMed
Bavister, B.D. (1995). Culture of preimplantation embryos: facts and artefacts. Hum. Reprod. Update 1, 91148.CrossRefGoogle Scholar
Bavister, B.D., Rose-Hellekant, T.A. & Pinyopummintr, T. (1992). Development of in vitro matured/in vitro fertilised bovine embryos into morulae and blastocysts in defıned culture media. Theriogenology 37, 127–46.CrossRefGoogle Scholar
Berthelot, F. & Terqui, M. (1996). Effects of oxygen, CO2/pH and medium on the in vitro development of individually cultured porcine one- and two-cell embryos. Reprod. Nutr. Dev. 36, 241–51.CrossRefGoogle ScholarPubMed
Boelhauve, M., Sinowatz, F., Wolf, E., Paula-Lopes, F.F., Cao, X., Zhou, P., Luo, H., Zhao, Y. & Shi, G. (2005). Maturation of bovine oocytes in the presence of leptin improves development and reduces apoptosis of in vitro-produced blastocysts. Biol. Reprod. 73, 737–44.CrossRefGoogle ScholarPubMed
Bokal, E.V., Tacer, K.F., Vrbnjak, M., Leposa, S., Virant-Klun, I., Verdenik, I. & Rozman, D. (2006). Follicular sterol composition in gonadotrophin-stimulated women with polycystic ovarian syndrome. Mol. Cell. Endocrinol. 249, 92–8.CrossRefGoogle ScholarPubMed
Buccione, R., Schroeder, A.C. & Eppig, J.J. (1990). Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol. Reprod. 43, 543–7.CrossRefGoogle ScholarPubMed
Byskov, A.G., Yding Andersen, C., Hossaini, A. & Guoliang, X. (1977) Cumulus cells of oocyte–cumulus complexes secrete a meiosis-activating substance when stimulated with FSH. Mol. Reprod. Dev. 46, 296305.3.0.CO;2-K>CrossRefGoogle Scholar
Byskov, A.G., Andersen, C.Y., Leonardsen, L. (2002). Role of meiosis activating sterols, MAS, in induced oocyte maturation. Mol. Cell. Endocrinol. 187, 189–96.CrossRefGoogle ScholarPubMed
Byskov, A.G., Andersen, C.Y., Nordholm, L., Thogersen, H., Xia, G., Wassmann, O., Andersen, J.V., Guddal, E. & Roed, T. (1995). Chemical structure of sterols that activate oocyte meiosis. Nature 374, 559–62.CrossRefGoogle ScholarPubMed
Cao, X., Zhou, P., Luo, H., Zhao, Y. & Shi, G. (2009). The effect of VEGF on the temporal-spatial change of alpha-tubulin and cortical granules of ovine oocytes matured in vitro. Anim. Reprod. Sci. 113, 236–50.CrossRefGoogle ScholarPubMed
Cetica, P., Pintos, L., Dalvit, G. & Beconi, M. (2002). Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction 124, 675–81.CrossRefGoogle ScholarPubMed
Choi, Y.H., Carnevale, E.M., Seidel, G.E. Jr. & Squire, E.L. (2001). Effects of gonadotropins on bovine oocytes matured in TCM-199. Theriogenology 56, 661–70.CrossRefGoogle ScholarPubMed
Cortvrindt, R.G., Hu, Y., Liu, J. & Smitz, J.E. (1998). Timed analysis of the nuclear maturation of oocytes in early preantral mouse follicle culture supplemented with recombinant gonadotropin. Fertil. Steril. 70, 1114–25.CrossRefGoogle ScholarPubMed
deMatos, D.G., Gasparrini, B., Pasqualini, S.T. & Thompson, J.G. (2002). Effect of glutathione synthesis stimulation during in vitro maturation of ovine oocytes in embryo development and intracellular peroxide content. Theriogenology 57, 1443–51.CrossRefGoogle Scholar
Downs, S.M. & Mastropolo, A.M. (1997). Culture conditions affect meiotic regulation in cumulus cell-enclosed mouse oocytes. Mol. Reprod. Dev. 46, 551–66.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Eppig, J.J. & Wigglesworth, K. (1995). Factors affecting the developmental competence of mouse oocytes grown in vitro: oxygen concentration. Mol. Reprod. Dev. 42, 447–56.CrossRefGoogle ScholarPubMed
Farin, P.W., Crosier, A.E. & Farin, C.E. (2001). Influence of in vitro systems on embryo survival and fetal development in cattle. Theriogenology 55, 151–70.CrossRefGoogle ScholarPubMed
Ferguson, E.M. & Leese, H.J. (1999). Triglyceride content of bovine oocytes and early embryos. J. Reprod. Fert. 116, 373–8.CrossRefGoogle ScholarPubMed
Fujihira, T., Kishida, R. & Fukui, Y. (2004). Developmental capacity of vitrified immature porcine oocytes following ICSI: effects of cytochalasin B and cryoprotectants. Cryobiology 49, 286–90.CrossRefGoogle ScholarPubMed
Gandolfi, F., Vassena, R. & Lauria, A. (2000). The developmental competence of the oocyte before puberty: is something missing? Reprod. Domest. Anim. 35, 6671.Google Scholar
Genicot, G., Leroy, J.L., Soom, A.V. & Donnay, I. (2005). The use of a fluorescent dye, Nile red, to evaluate the lipid content of single mammalian oocytes. Theriogenology 63, 1181–94.CrossRefGoogle ScholarPubMed
Grøndahl, C. (2008). Oocyte maturation. Basic and clinical aspects of in vitro maturation (IVM) with special emphasis of the role of FF-MAS. Dan. Med. Bull. 55, 116.Google ScholarPubMed
Grøndahl, C., Ottesen, J.L., Lessl, M., Faarup, P., Murray, A., Gronvald, F.C., Hegele- Hartung, C. & Ahnfelt-Ronne, I. (1998). Meiosis-activating sterol promotes resumption of meiosis in mouse oocytes cultured in vitro in contrast to related oxysterols. Biol. Reprod. 58, 1297–302.CrossRefGoogle ScholarPubMed
Grøndahl, C., Lessl, M., Faerge, I., Hegele-Hartung, C., Wassermann, K. & Ottesen, J.L. (2000). Meiosis-activating sterol-mediated resumption of meiosis in mouse oocytes in vitro is influenced by protein synthesis inhibition and cholera toxin. Biol. Reprod. 62, 775–80.CrossRefGoogle ScholarPubMed
Hashimoto, S., Minami, N., Takakura, R., Yamada, M., Imai, H. & Kashima, N. (2000). Low oxygen tension during in vitro maturation is beneficial for supporting the subsequent development of bovine cumulus–oocyte complexes. Mol. Reprod. Dev. 57, 353–60.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Izquierdo, D., Villamediana, P. & Paramio, M.T. (1999). Effect of culture media on embryo development from prepubertal goat IVM–IVF oocytes. Theriogenology 52, 847861.CrossRefGoogle ScholarPubMed
Jamnongjit, M. & Hammes, S.R. (2005). Oocyte maturation: the coming of age of a germ cell. Semin. Reprod. Med. 23, 234–41.CrossRefGoogle ScholarPubMed
Khatir, H., Lonergan, P. & Mermillod, P. (1998). Kinetics of nuclear maturation and protein profiles of oocytes from prepubertal and adult cattle during in vitro maturation. Theriogenology 50, 917–29.CrossRefGoogle ScholarPubMed
Kikuchi, K., Onishi, A., Kashiwazaki, N., Iwamoto, M., Noguchi, J., Kaneko, H., Akita, T. & Nagai, T. (2002). Successful piglet production after transfer of blastocysts produced by a modified in vitro system. Biol. Reprod. 66, 1033–41.CrossRefGoogle ScholarPubMed
Kim, J.Y., Kinoshita, M., Ohnishi, M. & Fukui, Y. (2001). Lipid and fatty acid analysis of fresh and frozen-thawed immature and in vitro matured bovine oocytes. Reproduction 122, 131–8.CrossRefGoogle ScholarPubMed
Kim, H.S., Jeong, Y.I., Lee, J.Y., Jeong, Y.W., Hossein, M.S., Hyun, H.S. & Hwang, W.S. (2010). Effects of recombinant relaxin on in vitro maturation of porcine oocytes. J. Vet. Med. Sci. 3, 333–7.CrossRefGoogle Scholar
Kito, S. & Bavister, B.D. (1997). Male pronuclear formation and early embryonic development of hamster oocytes matured in vitro with gonadotrophins, amino acids and cysteamine. J. Reprod. Fertil. 110, 3546.CrossRefGoogle ScholarPubMed
Laurincík, J., Kroslak, P., Hyttel, P., Pivko, J. & Sirotkin, A.V. (1992). Bovine cumulus expansion and corona–oocyte disconnection during culture in vitro. Reprod. Nutr. Dev. 32, 151–61.CrossRefGoogle ScholarPubMed
Lawrence, T.H., Beers, W.H. & Guila, N.B. (1978). Transmission of hormonal stimulation by cell-to-cell communication. Nature 272, 501–6.CrossRefGoogle ScholarPubMed
Ledda, S., Bogliolo, L., Calvia, P., Leoni, G. & Naitana, S. (1997). Meiotic progression and developmental competence of oocytes collected from juvenile and adult ewes. J. Reprod. Fertil. 109, 73–8.CrossRefGoogle ScholarPubMed
Leemuis, J.A.J., Van der Louw, J. & Groen, M.B. (1998). 17-allyloxy(thio)alkylandrostane derivatives for the modulation of meiosis. The Patent Cooperation Treaty, WO 98/55498.Google Scholar
Leoni, G.G., Bebbere, D., Succu, S., Berlinguer, F., Mossa, F., Galioto, M., Bogliolo, L., Ledda, S. & Naitana, S. (2007). Relations between relative mRNA abundance and developmental competence of ovine oocytes. Mol. Reprod. Dev. 74, 249–57.CrossRefGoogle ScholarPubMed
Marco-Jiménez, F., Llobat, L. & Vicente, J.S. (2010). Effects of lanosterol on in vitro maturation of porcine oocytes. Anim. Reprod. Sci. 117, 288–94.CrossRefGoogle ScholarPubMed
Marín-Bivens, C.L., Lindenthal, B., O'Brien, M.J., Wigglesworth, K., Blume, T., Grøndahl, C. & Eppig, J.J. (2004). A synthetic analogue of meiosis-activating sterol (FF-MAS) is a potent agonist promoting meiotic maturation and preimplantation development of mouse oocytes maturing in vitro. Hum. Reprod. 19, 2340–4.CrossRefGoogle ScholarPubMed
Marquant-Le Guienne, B. & Humblot, P. (1998). Practical measures to improve in vitro blastocyst production in the bovine. Theriogenology 449, 311.CrossRefGoogle Scholar
Mather, J.P. (1998). Making informed choices: medium, serum, and serum-free medium. How to choose the appropiate medium and culture systems for the model you wish to create. Meth. Cell. Biol. 57, 1930.CrossRefGoogle Scholar
Mattioli, M. (1994). Transduction mechanisms for gonadotrophin-induced oocyte maturation in mammals. Zygote 2, 347–9.CrossRefGoogle ScholarPubMed
McEvoy, T.G., Coull, G.D., Broadbent, P.J., Hutchinson, J.S. & Speake, B.K. (2000). Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J. Reprod. Fertil. 118, 163–70.CrossRefGoogle ScholarPubMed
Mermillod, P., Le Bourhis, D., Lonergan, P., Khatir, H. & Heyman, Y. (1998). Assessment of cytoplasmic competence of prepubertal calf oocytes by use of nuclear transfer. Theriogenology 49, 187.CrossRefGoogle Scholar
Modina, S., Luciano, A.M., Scesi, L., Perazzoli, F., Lauria, A. & Gandolfi, F. (2000). Recombinant FSH stimulates developmental competence of bovine oocytes and B-catenin can be used as en early marker of normal embryonic development. In: Proceedings of the 14th International Congress on Animal Reproduction, Stockholm, 2–6 July, (Abstract Book), p. 148.Google Scholar
Moreira, F., Paula-Lopes, F.F., Hansen, P.J., Badinga, L. & Thatcher, W.W. (2002). Effects of growth hormone and insulin-like growth factor-I on development of in vitro derived bovine embryos. Theriogenology 57, 895907.CrossRefGoogle ScholarPubMed
Niimura, S., Takano, H., Onishi, A. & Hosoe, M. (2002). Changes in the amount of proteins, glycogen and lipids in porcine oocytes during in vitro meiotic maturation. Anim. Sci. J. 73, 327–32.CrossRefGoogle Scholar
O'Brien, J.K., Dwarte, D., Ryan, J.P., Maxwell, W.M.C. & Evans, G. (1996). Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep. Reprod. Fertil. Dev. 8, 1029–37.CrossRefGoogle ScholarPubMed
Park, J.I., Hong, J.Y., Yong, H.Y., Hwang, W.S., Lim, J.M. & Lee, E.S. (2005). High oxygen tension during in vitro oocyte maturation improves in vitro development of porcine oocytes after fertilization. Anim. Reprod. Sci. 87, 133–41.CrossRefGoogle ScholarPubMed
Pinyopummintr, T. & Bavister, B.D. (1995). Optimum gas atmosphere for in vitro maturation and in vitro fertilization of bovine oocytes. Theriogenology 44, 471–7.CrossRefGoogle ScholarPubMed
Ptak, G., Loi, P., Dattena, M., Tischner, M. & Cappai, P. (1999). Offspring from one-month-old lambs: studies on the developmental capability of prepubertal oocytes. Biol. Reprod. 61, 1568–74.CrossRefGoogle ScholarPubMed
Rao, B.S., Naidu, K.S., Amarnath, D., Vagdevi, R., Rao, A.S., Brahmaiah, K.V. & Rao, V.H. (2002). In vitro maturation of sheep oocytes in different media during breeding and non breeding season. Small. Rumin. Res. 43, 31–6.CrossRefGoogle Scholar
Rozman, D., Cotman, M. & Frangez, R. (2002). Lanosterol 14alpha-demethylase and MAS sterols in mammalian gametogenesis. Mol. Cell. Endocrinol. 187, 179–87.CrossRefGoogle ScholarPubMed
Ruan, B., Gerst, N., Emmons, G.T., Shey, J. & Schroepfer, G.J.J. (1997). Sterol synthesis. A timely look at the capabilities of conventional and silver ion high performance liquid chromatography for the separation of C27 sterols related to cholesterol biosynthesis. J. Lipid. Res. 38, 2615–26.CrossRefGoogle Scholar
Salamone, D.F., Damiani, P., Fissore, R.A., Robl, J.M. & Duby, R.T. (2001). Biochemical and developmental evidence that ooplasmic maturation of prepubertal bovine oocytes is compromised. Biol. Reprod. 64, 1761–8.CrossRefGoogle ScholarPubMed
Shirazi, A., Shams-Esfandabadi, N., Ahmadi, E. & Heidari, B. (2010). Effects of growth hormone on nuclear maturation of ovine oocytes and subsequent embryo development. Reprod. Domest. Anim. 45, 530–6.CrossRefGoogle ScholarPubMed
Sturmey, R.G. & Leese, H.J. (2003). Energy metabolism in pig oocytes and early embryos. Reproduction 126, 197204.CrossRefGoogle ScholarPubMed
Succu, S., Leoni, G.G., Berlinguer, F., Madeddu, M., Bebbere, D., Mossa, F., Bogliolo, L., Ledda, S. & Naitana, S. (2007). Effect of vitrification solutions and cooling upon in vitro matured prepubertal ovine oocytes. Theriogenology 68, 107–14.CrossRefGoogle ScholarPubMed
Sun, Q.Y. & Nagai, T. (2003). Molecular mechanisms underlying pig oocyte maturation and fertilization. J. Reprod. Dev. 49, 347–59CrossRefGoogle ScholarPubMed
Thompson, J.G. (2000). In vitro culture and embryo metabolism of cattle and sheep embryos – a decade of achievement. Anim. Reprod. Sci. 30, 273–80.Google Scholar
Törnell, J., Bergh, C., Selleskog, U. & Hillensjö, T. (1995). Effect of recombinant human gonadotrophins on oocyte meiosis and steroidogenesis in isolated pre-ovulatory rat follicles. Hum. Reprod. 10, 1619–22.Google ScholarPubMed
Vanroose, G., Van Soom, A. & de Kruif, A. (2001). From co-culture to defined medium: state of the art and practical considerations. Reprod. Dom. Anim. 36, 25–8.CrossRefGoogle ScholarPubMed
Xia, G., Byskov, A.G. & Andersen, C.Y. (1994). Cumulus cells secrete a meiosis-inducing substance by stimulation with forskolin and dibutyric cyclic adenosine monophosphate. Mol. Reprod. Dev. 39, 1724.Google ScholarPubMed
Xia, G.L., Kikuchi, K., Noguchi, J. & Izaike, Y. (2000). Short time priming of pig cumulus-oocyte complexes with FSH and forskolin in the presence of hypoxanthine stimulates cumulus cells to secrete a meiosis-activating substance. Theriogenology 53, 1807–15.CrossRefGoogle ScholarPubMed
Yamashita, Y., Shimada, M., Okazaki, T., Maeda, T. & Terada, T. (2003). Production of progesterone from de novo-synthesized cholesterol in cumulus cells and its physiological role during meiotic resumption of porcine oocytes. Biol. Reprod. 68, 1193–8.CrossRefGoogle ScholarPubMed
Young, L.E., Sinclair, K.D. & Wilmut, I. (1998). Large offspring syndrome in cattle and sheep. Rev. Reprod. 3, 155163. Review.CrossRefGoogle ScholarPubMed
Younis, A.I., Brackett, B.G. & Fayer-Hosken, R.A. (1989). Influence of serum and hormones on bovine oocyte maturation and fertilization in vitro. Gamete. Res. 23, 189201.CrossRefGoogle ScholarPubMed
Zuelke, K.A. & Brackett, B.G. (1990). Luteinizing hormone enhanced in vitro maturation of bovine oocytes with and without protein supplementation. Biol. Reprod. 48, 815–20.CrossRefGoogle Scholar