Hostname: page-component-7dd5485656-tbj44 Total loading time: 0 Render date: 2025-10-31T14:32:40.535Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  01 December 2008

K. L. Yi ,
X. Zhou ,
D. S. Shi ,
H. H. Chen ,
Q. L. Qin ,
Y. Chen ,
C. J. Li ,
Z. H. Zhao  and
S. Y. Xing
K. L. Yi
Affiliation:
College of Animal Science and Veterinary Medicine, and Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University, 5333 Xi’an Road, Changchun 130062, PR China
X. Zhou*
Affiliation:
College of Animal Science and Veterinary Medicine, and Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University, 5333 Xi’an Road, Changchun 130062, PR China
D. S. Shi
Affiliation:
Animal Reproduction Institute, Guangxi University, Nanning, Guangxi, 530005, PR China
H. H. Chen
Affiliation:
Animal Reproduction Institute, Guangxi University, Nanning, Guangxi, 530005, PR China
Q. L. Qin
Affiliation:
Animal Reproduction Institute, Guangxi University, Nanning, Guangxi, 530005, PR China
Y. Chen
Affiliation:
Animal Reproduction Institute, Guangxi University, Nanning, Guangxi, 530005, PR China
C. J. Li
Affiliation:
College of Animal Science and Veterinary Medicine, and Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University, 5333 Xi’an Road, Changchun 130062, PR China
Z. H. Zhao
Affiliation:
College of Animal Science and Veterinary Medicine, and Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University, 5333 Xi’an Road, Changchun 130062, PR China
S. Y. Xing
Affiliation:
College of Animal Science and Veterinary Medicine, and Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University, 5333 Xi’an Road, Changchun 130062, PR China
*
E-mail: xzhou65@vip.sina.com
Get access

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.

Keywords

BDNFIVFparthenogenetic activationnuclear transfercattle

Information

Type
Full Paper
Information
animal , Volume 2 , Issue 12 , December 2008 , pp. 1786 - 1794
Copyright
Copyright © The Animal Consortium 2008

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.)

Article purchase

Temporarily unavailable

References

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.CrossRefGoogle ScholarPubMed
Barbacid, M 1994. The Trk family of neurotrophin receptors. Journal of Neurobiology 25, 1386–1403.CrossRefGoogle ScholarPubMed
Choi, Y, Rajkovic, A 2006. Genetics of early mammalian folliculogenesis. Cellular and Molecular Life Sciences 63, 579–590.CrossRefGoogle ScholarPubMed
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, 575–583.CrossRefGoogle ScholarPubMed
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, 281–288.CrossRefGoogle ScholarPubMed
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, 4066–4069.CrossRefGoogle ScholarPubMed
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, 4681–4692.CrossRefGoogle Scholar
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, 752–755.CrossRefGoogle ScholarPubMed
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, 89–96.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 532–540.CrossRefGoogle ScholarPubMed
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, 745–756.CrossRefGoogle ScholarPubMed
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, 12889–12894.CrossRefGoogle ScholarPubMed
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, 93–99.CrossRefGoogle ScholarPubMed
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, 2087–2095.CrossRefGoogle ScholarPubMed
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, 193–199.CrossRefGoogle ScholarPubMed
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, 231–237.Google ScholarPubMed
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, 9206–9211.CrossRefGoogle ScholarPubMed
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, 147–158.CrossRefGoogle ScholarPubMed
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, 4939–4947.CrossRefGoogle ScholarPubMed
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, 1309–1319.CrossRefGoogle ScholarPubMed
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, 423–434.CrossRefGoogle ScholarPubMed
McGrath, SA, Esquela, AF, Lee, SJ 1995. Oocyte-specific expression of growth/differentiation factor-9. Molecular Endocrinology 9, 131–136.Google ScholarPubMed
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, 65–73.CrossRefGoogle ScholarPubMed
Pangas, SA, Rajkovic, A 2006. Transcriptional regulation of early oogenesis: in search of masters. Human Reproduction Update 12, 65–76.CrossRefGoogle ScholarPubMed
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, 430–449.CrossRefGoogle ScholarPubMed
Rajkovic, A, Pangas, SA, Ballow, D, Suzumori, N, Matzuk, MM 2004. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305, 1157–1159.CrossRefGoogle ScholarPubMed
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, 377–386.CrossRefGoogle ScholarPubMed
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, 589–595.CrossRefGoogle ScholarPubMed
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, 1131–1135.CrossRefGoogle ScholarPubMed
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, 655–659.CrossRefGoogle ScholarPubMed
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, 451–452.CrossRefGoogle ScholarPubMed
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, 152–160.Google ScholarPubMed
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, 1704–1715.CrossRefGoogle ScholarPubMed
Tessarollo, L 1998. Pleiotropic functions of neurotrophins in development. Cytokine and Growth Factor Reviews 9, 125–137.CrossRefGoogle ScholarPubMed
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, 281–287.CrossRefGoogle ScholarPubMed
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, 133–140.CrossRefGoogle ScholarPubMed
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, 309–317.CrossRefGoogle ScholarPubMed
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, 187–191.CrossRefGoogle ScholarPubMed
Young, LE, Butterwith, SC, Wilmut, I 1998. A novel method for quantifying mRNA levels in single embryos. Theriogenology 49, 192–192.CrossRefGoogle Scholar