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Novel transcripts and alternatively spliced genes are associated with early development in bovine embryos

Published online by Cambridge University Press:  03 February 2012

B. Zhang ,
F. Peñagaricano ,
H. Chen  and
H. Khatib
B. Zhang
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, China Department of Dairy Science, University of Wisconsin – Madison, Madison, WI 53706, USA
F. Peñagaricano
Affiliation:
Department of Animal Sciences, University of Wisconsin – Madison, Madison, WI 53706, USA
H. Chen
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, China
H. Khatib*
Affiliation:
Department of Animal Sciences, University of Wisconsin – Madison, Madison, WI 53706, USA
*
†E-mail: [email protected]
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Abstract

Infertility in cattle is a major concern of farmers worldwide and despite the enormous improvements in assisted reproduction technologies, the success rates of pregnancies are still low. Embryonic loss is considered one of the main factors of infertility in cattle. As such, the identification of genetic markers for embryo quality and development can help elucidate the molecular mechanisms involved in the formation of embryos with the highest developmental potential. In a previous study, using next-generation RNA sequencing, we identified novel transcripts and alternatively spliced genes that were associated with embryo quality. The objectives of this study were to characterize these transcripts and validate their expression in new biological replications of embryos using quantitative real-time PCR. Two types of embryos differing in morphological and developmental statuses (blastocysts and degenerate embryos) were produced using in vitro fertilization. Quantitative expression of eight novel transcripts revealed a range of 2.5- to 90-fold difference in expression between degenerate embryos and blastocysts. Some of these novel transcripts showed sequence similarity to human and cattle genes known to affect differentiation, growth and development. In addition, expression analysis of alternative splicing isoforms of five genes (MYL6, NOP10, RNF187, RPS24 and RPS28) revealed significant differential expression of these isoforms in the different embryo types. Thus, results of this study suggest that novel transcripts and alternatively spliced genes, found to be differentially expressed between blastocysts and degenerate embryos, can be used as markers for blastocyst formation and development.

Keywords

embryofertilitygene expressionnovel transcriptsalternative splicing
Type
Full Paper
Information
animal , Volume 6 , Issue 8 , August 2012 , pp. 1199 - 1205
Copyright
Copyright © The Animal Consortium 2012

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References

Blencowe, BJ 2006. Alternative splicing: new insights from global analyses. Cell 126, 37–47.CrossRefGoogle ScholarPubMed
Bressan, FF, De Bem, TH, Perecin, F, Lopes, FL, Ambrosio, CE, Meirelles, FV, Miglino, MA 2009. Unearthing the roles of imprinted genes in the placenta. Placenta 30, 823–834.CrossRefGoogle ScholarPubMed
Bromer, J, Seli, E 2008. Assessment of embryo viability in assisted reproductive technology: shortcomings of current approaches and the emerging role of metabolomics. Current Opinion in Obstetrics and Gynecology 20, 234–241.CrossRefGoogle ScholarPubMed
Craig, KL, Tyers, M 1999. The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Progress in Biophysics and Molecular Biology 72, 299–328.CrossRefGoogle ScholarPubMed
Dinger, ME, Amaral, PP, Mercer, TR, Mattick, JS 2009. Pervasive transcription of the eukaryotic genome: functional indices and conceptual implications. Briefings in Functional Genomics and Proteomics 8, 407–423.CrossRefGoogle ScholarPubMed
Dobson, H, Smith, R, Royal, M, Knight, CH, Sheldon, I 2007. The high-producing dairy cow and its reproductive performance. Reproduction in Domestic Animals 42 (suppl. 2), 17–23.CrossRefGoogle ScholarPubMed
Flisikowski, K, Venhoranta, H, Nowacka-Woszuk, J, McKay, SD, Flyckt, A, Taponen, J, Schnabel, R, Schwarzenbacher, H, Szczerbal, I, Lohi, H, Fries, R, Taylor, JF, Switonski, M, Andersson, M 2010. A novel mutation in the maternally imprinted PEG3 domain results in a loss of MIMT1 expression and causes abortions and stillbirths in cattle (Bos taurus). PLoS One 5, e15116.CrossRefGoogle Scholar
Gazda, HT, Grabowska, A, Merida-Long, LB, Latawiec, E, Schneider, HE, Lipton, JM, Vlachos, A, Atsidaftos, E, Ball, SE, Orfali, KA, Niewiadomska, E, Da Costa, L, Tchernia, G, Niemeyer, C, Meerpohl, JJ, Stahl, J, Schratt, G, Glader, B, Backer, K, Wong, C, Nathan, DG, Beggs, AH, Sieff, CA 2006. Ribosomal protein S24 gene is mutated in Diamond–Blackfan anemia. American Journal of Human Genetics 79, 1110–1118.CrossRefGoogle ScholarPubMed
Goossens, K, Van Soom, A, Van Poucke, M, Vandaele, L, Vandesompele, J, Van Zeveren, A, Peelman, LJ 2007. Identification and expression analysis of genes associated with bovine blastocyst formation. BMC Developmental Biology 7, 64.CrossRefGoogle ScholarPubMed
Grandjean, V, Gounon, P, Wagner, N, Martin, L, Wagner, KD, Bernex, F, Cuzin, F, Rassoulzadegan, M 2009. The miR-124-Sox9 paramutation: RNA-mediated epigenetic control of embryonic and adult growth. Development 136, 3647–3655.CrossRefGoogle ScholarPubMed
Huang, W, Khatib, H 2010. Comparison of transcriptomic landscapes of bovine embryos using RNA-Seq. BMC Genomics 11, 711.CrossRefGoogle ScholarPubMed
Huang, W, Kirkpatrick, BW, Rosa, GJ, Khatib, H 2010a. A genome-wide association study using selective DNA pooling identifies candidate markers for fertility in Holstein cattle. Animal Genetics 41, 570–578.CrossRefGoogle ScholarPubMed
Huang, W, Yandell, BS, Khatib, H 2010b. Transcriptomic profiling of bovine IVF embryos revealed candidate genes and pathways involved in early embryonic development. BMC Genomics 11, 23.CrossRefGoogle ScholarPubMed
Khatib, H, Monson, RL, Schutzkus, V, Kohl, DM, Rosa, GJ, Rutledge, JJ 2008. Mutations in the STAT5A gene are associated with embryonic survival and milk composition in cattle. Journal of Dairy Science 91, 784–793.CrossRefGoogle ScholarPubMed
Khatib, H, Huang, W, Wang, X, Tran, AH, Bindrim, AB, Schutzkus, V, Monson, RL, Yandell, BS 2009. Single gene and gene interaction effects on fertilization and embryonic survival rates in cattle. Journal of Dairy Science 92, 2238–2247.CrossRefGoogle ScholarPubMed
Kim, J, Bergmann, A, Choo, JH, Stubbs, L 2007. Genomic organization and imprinting of the Peg3 domain in bovine. Genomics 90, 85–92.CrossRefGoogle ScholarPubMed
Kim, J, Bergmann, A, Wehri, E, Lu, X, Stubbs, L 2001. Imprinting and evolution of two Kruppel-type zinc-finger genes, ZIM3 and ZNF264, located in the PEG3/USP29 imprinted domain. Genomics 77, 91–98.CrossRefGoogle ScholarPubMed
Kipreos, ET, Pagano, M 2000. The F-box protein family. Genome Biology 1, REVIEWS3002.CrossRefGoogle ScholarPubMed
Kuroiwa, Y, Kaneko-Ishino, T, Kagitani, F, Kohda, T, Li, LL, Tada, M, Suzuki, R, Yokoyama, M, Shiroishi, T, Wakana, S, Barton, SC, Ishino, F, Surani, MA 1996. Peg3 imprinted gene on proximal chromosome 7 encodes for a zinc finger protein. Nature Genetics 12, 186–190.CrossRefGoogle ScholarPubMed
Lefebvre, V, Behringer, RR, de Crombrugghe, B 2001. L-Sox5, Sox6 and Sox9 control essential steps of the chondrocyte differentiation pathway. Osteoarthritis Cartilage 9 (suppl. A), S69–S75.CrossRefGoogle ScholarPubMed
Leroy, JL, Opsomer, G, Van Soom, A, Goovaerts, IG, Bols, PE 2008. Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part I. The importance of negative energy balance and altered corpus luteum function to the reduction of oocyte and embryo quality in high-yielding dairy cows. Reproduction in Domestic Animals 43, 612–622.CrossRefGoogle Scholar
Livak, KJ, Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408.CrossRefGoogle ScholarPubMed
Meola, J, Rosa e Silva, JC, Dentillo, DB, da Silva, WA Jr, Veiga-Castelli, LC, Bernardes, LA, Ferriani, RA, de Paz, CC, Giuliatti, S, Martelli, L 2010. Differentially expressed genes in eutopic and ectopic endometrium of women with endometriosis. Fertility and Sterility 93, 1750–1773.CrossRefGoogle ScholarPubMed
Morris, D, Diskin, M 2008. Effect of progesterone on embryo survival. Animal 2, 1112–1119.CrossRefGoogle ScholarPubMed
Paidas, MJ, Krikun, G, Huang, SJ, Jones, R, Romano, M, Annunziato, J, Barnea, ER 2010. A genomic and proteomic investigation of the impact of preimplantation factor on human decidual cells. American Journal of Obstetrics and Gynecology 202, 459.e1–8.CrossRefGoogle ScholarPubMed
Santos, JE, Thatcher, WW, Chebel, RC, Cerri, RL, Galvão, KN 2004. The effect of embryonic death rates in cattle on the efficacy of estrus synchronization programs. Animal Reproduction Science 82–83, 513–535.CrossRefGoogle ScholarPubMed
Tunster, SJ, Tycko, B, John, RM 2010. The imprinted Phlda2 gene regulates extraembryonic energy stores. Molecular and Cellular Biology 30, 295–306.CrossRefGoogle ScholarPubMed
The ENCODE Project Consortium 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447, 799–816.CrossRefGoogle Scholar
Vandesompele, J, De Preter, K, Pattyn, F, Poppe, B, Van Roy, N, De Paepe, A, Speleman, F 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, RESEARCH0034.CrossRefGoogle ScholarPubMed
Veiga-Castelli, LC, Silva, JC, Meola, J, Ferriani, RA, Yoshimoto, M, Santos, SA, Squire, JA, Martelli, L 2010. Genomic alterations detected by comparative genomic hybridization in ovarian endometriomas. Brazilian Journal of Medical and Biological Research 43, 799–805.CrossRefGoogle ScholarPubMed
Walne, AJ, Vulliamy, T, Marrone, A, Beswick, R, Kirwan, M, Masunari, Y, Al-Qurashi, FH, Aljurf, M, Dokal, I 2007. Genetic heterogeneity in autosomal recessive dyskeratosis congenita with one subtype due to mutations in the telomerase-associated protein NOP10. Human Molecular Genetics 16, 1619–1629.CrossRefGoogle ScholarPubMed
Wang, ET, Sandberg, R, Luo, S, Khrebtukova, I, Zhang, L, Mayr, C, Kingsmore, SF, Schroth, GP, Burge, CB 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456, 470–476.CrossRefGoogle ScholarPubMed
Xu, J, Yang, X 2000. Telomerase activity in bovine embryos during early development. Biology of Reproduction 63, 1124–1128.CrossRefGoogle ScholarPubMed
Supplementary material: File

Zhang Supplementary Table

Supplementary Table 1 Results of the BLAST analysis of novel transcripts

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