Skip to main content Accessibility help
×
Home

The mRNA expression of brain-derived neurotrophic factor in oocytes and embryos and its effects on the development of early embryos in cattle

  • K. L. Yi (a1), X. Zhou (a1), D. S. Shi (a2), H. H. Chen (a2), Q. L. Qin (a2), Y. Chen (a2), C. J. Li (a1), Z. H. Zhao (a1) and S. Y. Xing (a1)...

Abstract

The aims of the study were to measure the mRNA expression of brain-derived neurotrophic factor (BDNF) in bovine oocytes and early embryos derived from in vitro fertilization (IVF), parthenogenetic activation (PA) and nuclear transfer (NT), and to investigate the effects of BDNF on the development of IVF and parthenogenetic embryos. Bovine oocytes matured in vitro for 22 h were in vitro fertilized or parthenogenetic activated. By reverse transcription-PCR and quantitative real-time PCR, we found that germinal vesicle (GV) oocytes, metaphase II (MII) oocytes, 4-cell and 8-cell embryos, morulae, and blastocysts were all shown to express mRNA for BDNF. The mRNA levels for BDNF gene were different in bovine oocytes and IVF embryos at different stages (P < 0.01), with the highest expression in MII oocytes and the lowest expression in 8-cell embryos. The mRNA for BDNF was highly expressed in the PA and IVF blastocysts compared to the NT blastocysts (P < 0.01). Supplementation of culture media with BDNF at the concentration of 40 μg/l caused a significant increase in the rates of in vitro-fertilized blastocyst formation (P < 0.05) and parthenogenetic blastocyst formation (P < 0.05). However, the rate of oocyte cleavage in BDNF groups was not significantly different from that in the BDNF-free control (P > 0.05) after IVF or PA. We have also investigated the effects of BDNF on the growth of granulosa cells, which were used for co-culture of bovine early embryos. The results revealed that supplementation of culture media with 20 μg/l BDNF promoted the growth of granulosa cells (P < 0.01). Taken together, these results provided evidence for the role of neurotrophins in promoting early embryonic development as well as in the growth of granulosa cells by the co-culture system, indicating that BDNF can directly or indirectly promote bovine early embryo development.

Copyright

Corresponding author

References

Hide All
Ayers, D, Clements, DN, Salway, F, Day, PJ 2007. Expression stability of commonly used reference genes in canine articular connective tissues. BMC Veterinary Research 3, 7.
Barbacid, M 1994. The Trk family of neurotrophin receptors. Journal of Neurobiology 25, 13861403.
Choi, Y, Rajkovic, A 2006. Genetics of early mammalian folliculogenesis. Cellular and Molecular Life Sciences 63, 579590.
Currie, RA, Walker, KS, Gray, A, Deak, M, Casamayor, A, Downes, CP, Cohen, P, Alessi, DR, Lucocq, J 1999. Role of phosphatidylinositol 3,4,5-trisphosphate in regulating the activity and localization of 3-phosphoinositide-dependent protein kinase-1. Biochemical Journal 337, 575583.
Daniels, R, Hall, VJ, French, AJ, Korfiatis, NA, Trounson, AO 2001. Comparison of gene transcription in cloned bovine embryos produced by different nuclear transfer techniques. Molecular Reproduction and Development 60, 281288.
De Ketelaere, A, Goossens, K, Peelman, L, Burvenich, C 2006. Technical note: validation of internal control genes for gene expression analysis in bovine polymorphonuclear leukocytes. Journal of Dairy Science 89, 40664069.
Dissen, GA, Hirshfield, AN, Malamed, S, Ojeda, SR 1995. Expression of neurotrophins and their receptors in themammalian ovary is developmentally regulated: changes at the time of folliculogenesis. Endocrinology 136, 46814692.
Finch, PW, Rubin, JS, Miki, T, Ron, D, Aaronson, SA 1989. Human KGF is FGF-related with properties of a paracrine effector of epithelial cell growth. Science 245, 752755.
Fischer, M, Skowron, M, Berthold, F 2005. Reliable transcript quantification by real-time reverse transcriptase-polymerase chain reaction in primary neuroblastoma using normalization to averaged expression levels of the control genes HPRT1 and SDHA. Journal of Molecular Diagnostics 7, 8996.
Goossens, K, Van Poucke, M, Van Soom, A, Vandesompele, J, Van Zeveren, A, Peelman, LJ 2005. Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos. BMC Developmental Biology 5, 27.
Harvey, MB, Arcellana-Panlilio, MY, Zhang, X, Schultz, GA, Watson, AJ 1995. Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture. Biology of Reproduction 53, 532540.
Heikinheimo, O, Gibbons, WE 1998. The molecular mechanisms of oocyte maturation and early embryonic development are unveiling new insights into reproductive medicine. Molecular Human Reproduction 4, 745756.
Humpherys, D, Eggan, K, Akutsu, H, Friedman, A, Hochedlinger, K, Yanagimachi, R, Lander, ES, Golub, TR, Jaenisch, R 2002. Abnormal gene expression in cloned mice derived from embryonic stem cell and cumulus cell nuclei. Proceedings of the National Academy of Sciences of the United States of America 99, 1288912894.
Ichikawa, H, Terayama, R, Yamaai, T, Yan, Z, Sugimoto, T 2007. Brain-derived neurotrophic factor-immunoreactive neurons in the rat vagal and glossopharyngeal sensory ganglia; co-expression with other neurochemical substances. Brain Research 1155, 9399.
Jensen, T, Johnson, AL 2001. Expression and function of brain-derived neurotrophin factor and its receptor, TrkB, in ovarian follicles from the domestic hen (Gallus gallus domesticus). Journal of Experimental Biology 204, 20872095.
Joo, BS, Kim, MK, Na, YJ, Moon, HS, Lee, KS, Kim, HD 2001. The mechanism of action of coculture on embryo development in the mouse model: direct embryo-to-cell contact and the removal of deleterious components. Fertility and Sterility 75, 193199.
Kato, Y, Tani, T, Tsunoda, Y 2000. Cloning of calves from various somatic cell types of male and female adult, newborn and fetal cows. Journal of Reproduction and Fertility 120, 231237.
Kawamura, K, Kawamura, N, Mulders, SM, Sollewijn Gelpke, MD, Hsueh, AJ 2005. Ovarian brain-derived neurotrophic factor (BDNF) promotes the development of oocytes into preimplantation embryos. Proceedings of the National Academy of Sciences of the United States of America 102, 92069211.
Kawamura, K, Kawamura, N, Fukuda, J, Kumagai, J, Hsueh, AJ, Tanaka, T 2007. Regulation of preimplantation embryo development by brain-derived neurotrophic factor. Developmental Biology 311, 147158.
Liang, L, Soyal, SM, Dean, J 1997. FIGα, a germ cell specific transcription factor involved in the coordinate expression of the zona pellucida genes. Development 124, 49394947.
Lu, F, Shi, D, Wei, J, Yang, S, Wei, Y 2005. Development of embryos reconstructed by interspecies nuclear transfer of adult fibroblasts between buffalo (Bubalus bubalis) and cattle (Bos indicus). Theriogenology 64, 13091319.
Martins da Silva, SJ, Gardner, JO, Taylor, LE, Springbett, A, Sousa, PA, Anderson, RA 2005. Brain-derived neurotrophic factor promotes bovine oocyte cytoplasmic competence for embryo development. Reproduction 129, 423434.
McGrath, SA, Esquela, AF, Lee, SJ 1995. Oocyte-specific expression of growth/differentiation factor-9. Molecular Endocrinology 9, 131136.
Nilsson, EE, Kezele, P, Skinner, MK 2002. Leukemia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Molecular and Cellular Endocrinology 188, 6573.
Pangas, SA, Rajkovic, A 2006. Transcriptional regulation of early oogenesis: in search of masters. Human Reproduction Update 12, 6576.
Paredes, A, Romero, C, Dissen, GA, DeChiara, TM, Reichardt, L, Cornea, A, Ojeda, SR, Xu, B 2004. TrkB receptors are required for follicular growth and oocyte survival in the mammalian ovary. Developmental Biology 267, 430449.
Rajkovic, A, Pangas, SA, Ballow, D, Suzumori, N, Matzuk, MM 2004. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305, 11571159.
Riley, JK, Carayannopoulos, MO, Wyman, AH, Chi, M, Ratajczak, CK, Moley, KH 2005. The PI3K/Akt pathway is present and functional in the preimplantation mouse embryo. Developmental Biology 284, 377386.
Rizos, D, Lonergan, P, Boland, MP, Arroyo-García, R, Pintado, B, de la Fuente, J, Gutiérrez-Adán, A 2002. Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implication for blastocyst quality. Biology of Reproduction 66, 589595.
Ruddock, NT, Wilson, KJ, Cooney, MA, Korfiatis, NA, Tecirlioglu, RT, French, AJ 2004. Analysis of imprinted messenger RNA expression during bovine preimplantation development. Biology of Reproduction 70, 11311135.
Seifer, DB, Feng, B, Shelden, RM, Chen, S, Dreyfus, CF 2002. Brainderived neurotrophic factor: a novel human ovarian follicular protein. Journal of Clinical Endocrinology and Metabolism 87, 655659.
Seifer, DB, Lambert-Messerlian, G, Schneyer, AL 2003. Ovarian brain-derived neurotrophic factor is present in follicular fluid from normally cycling women. Fertility and Sterility 79, 451452.
Sugimoto, T, Kuroda, H, Horii, Y, Moritake, H, Tanaka, T, Hattori, S 2001. Signal transduction pathways through TRK-A and TRK-B receptors in human neuroblastoma cells. Japanese Journal of Cancer Research 92, 152160.
Suteevun, T, Smith, S, Muenthaisong, S, Yang, X, Parnpai, R, Tian, X 2006. Anomalous mRNA levels of chromatin remodeling genes in swamp buffalo (Bubalus bubalis) cloned embryos. Theriogenology 65, 17041715.
Tessarollo, L 1998. Pleiotropic functions of neurotrophins in development. Cytokine and Growth Factor Reviews 9, 125137.
Tong, ZB, Nelson, LM, Dean, J 2000. Mater encodes a maternal protein in mice with a leucine-rich repeat domain homologous to porcine ribonuclease inhibitor. Mammalian Genome 11, 281287.
Van Wezel, IL, Umapathysivam, K, Tilley, WD, Rodgers, RJ 1995. Immunohistochemical localization of basic fibroblast growth factor in bovine ovarian follicles. Molecular and Cellular Endocrinology 115, 133140.
Wrenzycki, C, Wells, D, Herrmann, D, Miller, A, Oliver, J, Tervit, R, Niemann, H 2001. Nuclear transfer protocol affects messenger RNA expression patterns in cloned bovine blastocysts. Biology of Reproduction 65, 309317.
Wu, X, Viveiros, MM, Eppig, JJ, Bai, Y, Fitzpatrick, SL, Matzuk, MM 2003. Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nature Genetics 33, 187191.
Young, LE, Butterwith, SC, Wilmut, I 1998. A novel method for quantifying mRNA levels in single embryos. Theriogenology 49, 192192.

Keywords

The mRNA expression of brain-derived neurotrophic factor in oocytes and embryos and its effects on the development of early embryos in cattle

  • K. L. Yi (a1), X. Zhou (a1), D. S. Shi (a2), H. H. Chen (a2), Q. L. Qin (a2), Y. Chen (a2), C. J. Li (a1), Z. H. Zhao (a1) and S. Y. Xing (a1)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed