Expression pattern of zygote arrest 1 (ZAR1), maternal antigen that embryo requires (MATER), growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15) genes in ovine oocytes and in vitro-produced preimplantation embryos
Daniela Bebbere A E , Luisa Bogliolo B , Federica Ariu B , Stefano Fois B , Giovanni Giuseppe Leoni C , Silvia Tore D , Sara Succu C , Fiammetta Berlinguer A , Salvatore Naitana A and Sergio Ledda B
+ Author Affiliations
- Author Affiliations
A Department of Animal Biology, University of Sassari, via Vienna 2, 07100 Sassari, Italy.
B Department of Veterinary Clinics and Pathology, University of Sassari, via Vienna 2, 07100 Sassari, Italy.
C Department of Physiological, Biochemical and Cellular Science, University of Sassari, via Muroni 25, 07100 Sassari, Italy.
D Institute of Population Genetics, Research National Council, 07041 Alghero (SS), Italy.
E Corresponding author. Email: dbebbere@uniss.it
Reproduction, Fertility and Development 20(8) 908-915 https://doi.org/10.1071/RD08095
Submitted: 6 May 2008 Accepted: 25 July 2008 Published: 10 October 2008
Abstract
The expression patterns of four maternal effect genes (MEG), namely zygote arrest 1 (ZAR1), maternal antigen that embryo requires (MATER), growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15), were determined in ovine oocytes and in vitro-produced preimplantation embryos. The existence of ZAR1 and MATER in ovine species has not been reported previously. Reverse transcription–polymerase chain reaction was performed on germinal vesicle and IVM MII oocytes, as well as in in vitro fertilised and cultured two-, four-, eight- and 12/16-cell embryos, morulae and blastocysts. Quantification of gene expression by real-time polymerase chain reaction showed the highest abundance of all transcripts analysed in the immature oocyte. During the following stages of preimplantation development, the mRNAs examined exhibited different patterns of expression, but often significant decreases were observed during maturation and maternal–embryonic transition. The transcription of the four genes did not resume with activation of the genome.
Acknowledgements
The authors thank Dr Gianbattista Maestrale and Stefania Casula for technical assistance and Dr Francesca Mossa for helpful revision and English language editing of the manuscript. The authors declare that there is no conflict of interest that would prejudice the impartiality of this scientific work. This study was supported by RAS (Special Project Biodiversity), Fondazione Banco di Sardegna and MIUR Prin 2006.
References
Akam, M. (1987). The molecular basis for metameric pattern in the Drosophila embryo. Development 101, 1–22.
| PubMed | CAS |
Alizadeh, Z. , Kageyama, S. , and Aoki, F. (2005). Degradation of maternal mRNA in mouse embryos selective degradation of specific mRNAs after fertilization. Mol. Reprod. Dev. 72, 281–290.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Bowerman, B. (1998). Maternal control of pattern formation in early Caenorhabditis elegans embryos. Curr. Top. Dev. Biol. 39, 73–117.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Brevini, T. A. , Cillo, F. , Colleoni, S. , Lazzari, G. , Galli, C. , and Gandolfi, F. (2004). Expression pattern of the maternal factor zygote arrest 1 (Zar1) in bovine tissues, oocytes, and embryos. Mol. Reprod. Dev. 69, 375–380.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Burns, K. H. , Viveiros, M. M. , Ren, Y. , Wang, P. , DeMayo, F. J. , Frail, D. E. , Eppig, J. J. , and Matzuk, M. M. (2003). Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science 300, 633–636.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Chang, H. , Brown, C. W. , and Matzuk, M. M. (2002). Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr. Rev. 23, 787–823.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Dade, S. , Callebaut, I. , Paillisson, A. , Bontoux, M. , Dalbies-Tran, R. , and Monget, P. (2004). In silico identification and structural features of six new genes similar to MATER specifically expressed in the oocyte. Biochem. Biophys. Res. Commun. 324, 547–553.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Dean, J. (2002). Oocyte-specific genes regulate follicle formation, fertility and early mouse development. J. Reprod. Immunol. 53, 171–180.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
DiNitto, J. P. , Cronin, T. C. , and Lambright, D. G. (2003). Membrane recognition and targeting by lipid-binding domains. Sci. STKE 213, re16.
Di Pasquale, E. , Beck-Peccoz, P. , and Persani, L. (2004). Hypergonadotropic Ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am. J. Hum. Genet. 75, 106–111.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Donnison, M. , and Pfeffer, P. L. (2004). Isolation of genes associated with developmentally competent bovine oocytes and quantitation of their levels during development. Biol. Reprod. 71, 1813–1821.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Droin, A. (1992). The developmental mutants of Xenopus. Int. J. Dev. Biol. 36, 455–464.
| PubMed | CAS |
Elvin, J. A. , Yan, C. , and Matzuk, M. M. (2000). Oocyte-expressed TGF-beta superfamily members in female fertility. Mol. Cell. Endocrinol. 159, 1–5.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Galloway, S. M. , McNatty, K. P. , Cambridge, L. M. , Laitinen, M. P. , and Juengel, J. L. , et al. (2000). Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 25, 279–283.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Hamatani, T. , Carter, M. G. , Sharov, A. A. , and Ko, M. S. (2004). Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 6, 117–131.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Hanrahan, J. P. , Gregan, S. M. , Mulsant, P. , Mullen, M. , Davis, G. H. , Powell, R. , and Galloway, S. M. (2004). Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol. Reprod. 70, 900–909.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Kopecny, V. (1989). High-resolution autoradiographic studies of comparative nucleologenesis and genome reactivation during early embryogenesis in pig, man and cattle. Reprod. Nutr. Dev. 29, 589–600.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Latham, K. E. (1999). Mechanisms and control of embryonic genome activation in mammalian embryos. Int. Rev. Cytol. 193, 71–124.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Latham, K. E. , and Schultz, R. M. (2001). Embryonic genome activation. Front. Biosci. 6, D748–D759.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Lee, G. S. , Kim, H. S. , Hwang, W. S. , and Hyun, S. H. (2008). Characterization of porcine growth differentiation factor-9 and its expression in oocyte maturation. Mol. Reprod. Dev. 75, 707–714.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Livak, K. J. , and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(–Delta Delta C(T)) method. Methods 25, 402–408.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
McNatty, K. P. , Juengel, J. L. , Wilson, T. , Galloway, S. M. , and Davis, G. H. , et al. (2003). Oocyte-derived growth factors and ovulation rate in sheep. Reprod. Suppl. 61, 339–351.
| PubMed | CAS |
McNatty, K. P. , Smith, P. , Moore, L. G. , Reader, K. , Lun, S. , Hanrahan, J. P. , Groome, N. P. , Laitinen, M. , Ritvos, O. , and Juengel, J. L. (2005). Oocyte-expressed genes affecting ovulation rate. Mol. Cell. Endocrinol. 234, 57–66.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
McNatty, K. P. , Lawrence, S. , Groome, N. P. , Meerasahib, M. F. , Hudson, N. L. , Whiting, L. , Heath, D. A. , and Juengel, J. L. (2006). Meat and Livestock Association Plenary Lecture 2005. Oocyte signalling molecules and their effects on reproduction in ruminants. Reprod. Fertil. Dev. 18, 403–412.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Memili, E. , and First, N. L. (1998). Developmental changes in RNA polymerase II in bovine oocytes, early embryos, and effect of alpha-amanitin on embryo development. Mol. Reprod. Dev. 51, 381–389.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Memili, E. , and First, N. L. (1999). Control of gene expression at the onset of bovine embryonic development. Biol. Reprod. 61, 1198–1207.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Memili, E. , and First, N. L. (2000). Zygotic and embryonic gene expression in cow a review of timing and mechanisms of early gene expression as compared with other species. Zygote 8, 87–96.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Payer, B. , Saitou, M. , Barton, S. C. , Thresher, R. , Dixon, J. P. C. , Zahn, D. , Colledge, W. H. , Carlton, M. B. L. , Nakano, T. , and Surani, M. A. (2003). Stella is a maternal effect gene required for normal early development in mice. Curr. Biol. 13, 2110–2117.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Pennetier, S. , Uzbekova, S. , Perreau, C. , Papillier, P. , Mermillod, P. , and Dalbiès-Tran, R. (2004). Spatio-temporal expression of the germ cell marker genes MATER, ZAR1, GDF9, BMP15, andVASA in adult bovine tissues, oocytes, and preimplantation embryos. Biol. Reprod. 71, 1359–1366.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Pennetier, S. , Perreau, C. , Uzbekova, S. , Thélie, A. , Delaleu, B. , Mermillod, P. , and Dalbiès-Tran, R. (2006). MATER protein expression and intracellular localization throughout folliculogenesis and preimplantation embryo development in the bovine. BMC Dev. Biol. 6, 26.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rajkovic, A. , and Matzuk, M. M. (2002). Functional analysis of oocyte-expressed genes using transgenic models. Mol. Cell. Endocrinol. 187, 5–9.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Schultz, R. M. (1993). Regulation of zygotic gene activation in the mouse. Bioessays 15, 531–538.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sendai, Y. , Itoh, T. , Yamashita, S. , and Hoshi, H. (2001). Molecular cloning of a cDNA encoding a bovine growth differentiation factor-9 (GDF-9) and expression of GDF-9 in bovine ovarian oocytes and in vitro-produced embryos. Cloning 3, 3–10.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Shimasaki, S. , Moore, R. K. , Otsuka, F. , and Erickson, G. F. (2004). The bone morphogenetic protein system in mammalian reproduction. Endocr. Rev. 25, 72–101.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Shimizu, T. , Miyahayashi, Y. , Yokoo, M. , Hoshino, Y. , Sasada, H. , and Sato, E. (2004). Molecular cloning of porcine growth differentiation factor 9 (GDF-9) cDNA and its role in early folliculogenesis. Direct ovarian injection of GDF-9 gene fragments promotes early folliculogenesis. Reproduction 128, 537–543.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Telford, N. A. , Watson, A. J. , and Schultz, G. A. (1990). Transition from maternal to embryonic control in early mammalian development a comparison of several species. Mol. Reprod. Dev. 26, 90–100.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Thelie, A. , Papillier, P. , Pennetier, S. , Perreau, C. , Traverso, J. M. , Uzbekova, S. , Mermillod, P. , Joly, C. , Humblot, P. , and Dalbies-Tran, R. (2007). Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Dev. Biol. 7, 125.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tong, Z. B. , and Nelson, L. M. (1999). A mouse gene encoding an oocyte antigen associated with autoimmune premature ovarian failure. Endocrinology 140, 3720–3726.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Tong, Z. B. , Gold, L. , Pfeifer, K. E. , Dorward, H. , Lee, E. , Bondy, C. A. , Dean, J. , and Nelson, L. M. (2000). Mater, a maternal effect gene required for early embryonic development in mice. Nat. Genet. 26, 267–268.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Tong, Z. B. , Bondy, C. A. , Zhou, J. , and Nelson, L. M. (2002). A human homologue of mouse Mater, a maternal effect gene essential for early embryonic development. Hum. Reprod. 17, 903–911.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Tong, Z. B. , Gold, L. , De Pol, A. , Vanevski, K. , Dorward, H. , Sena, P. , Palumbo, C. , Bondy, C. A. , and Nelson, L. M. (2004). Developmental expression and subcellular localization of mouse MATER, an oocyte-specific protein essential for early development. Endocrinology 145, 1427–1434.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Uzbekova, S. , Roy-Sabau, M. , Dalbiès-Tran, R. , Perreau, C. , and Papillier, P. , et al. (2006). Zygote arrest 1 gene in pig, cattle and human evidence of different transcript variants in male and female germ cells. Reprod. Biol. Endocrinol. 4, 12.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Walker, S. K. , Hill, J. L. , Kleemann, D. O. , and Nancarrow, C. D. (1996). Development of ovine embryos in synthetic oviductal fluid containing amino acids at oviductal fluid concentrations. Biol. Reprod. 55, 703–708.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Wu, X. , Viveiros, M. M. , Eppig, J. J. , Bai, Y. , Fitzpatrick, S. L. , and Matzuk, M. M. (2003a). Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat. Genet. 33, 187–191.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wu, X. , Wang, P. , Brown, C. A. , Zilinski, C. A. , and Matzuk, M. M. (2003b). Zygote arrest 1 (Zar1) is an evolutionarily conserved gene expressed in vertebrate ovaries. Biol. Reprod. 69, 861–867.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Zeng, F. , and Schultz, R. M. (2003). Gene expression in mouse oocytes and preimplantation embryos use of suppression subtractive hybridization to identify oocyte- and embryo-specific genes. Biol. Reprod. 68, 31–39.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
