Whole-genome approaches for large-scale gene identification and expression analysis in mammalian preimplantation embryos
James Adjaye
+ Author Affiliations
- Author Affiliations
Max Planck Institute for Molecular Genetics, Department of Vertebrate Genomics, Ihnestrasse 73, D-14195 Berlin, Germany. Email: adjaye@molgen.mpg.de
Reproduction, Fertility and Development 17(2) 37-45 https://doi.org/10.1071/RD04075
Submitted: 1 August 2004 Accepted: 1 October 2004 Published: 1 January 2005
Abstract
The elucidation, unravelling and understanding of the molecular basis of transcriptional control during preimplantion development is of utmost importance if we are to intervene and eliminate or reduce abnormalities associated with growth, disease and infertility by applying assisted reproduction. Importantly, these studies should enhance our knowledge of basic reproductive biology and its application to regenerative medicine and livestock production. A major obstacle impeding progress in these areas is the ability to successfully generate molecular portraits of preimplantation embryos from their minute amounts of RNA. The present review describes the various approaches whereby classical embryology fuses with molecular biology, high-throughput genomics and systems biology to address and solve questions related to early development in mammals.
Extra keywords: bioinformatics, cDNA libraries, embryonic cells, gene expression, microarrays, preimplantation development, RNA amplification, signalling pathways, systems biology.
References
Adjaye, J. , and Monk, M. (2000). Transcription of homeobox-containing genes in cDNA libraries derived from human oocytes and preimplantation embryos. Mol. Hum. Reprod. 6, 707–711.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dahlquist, K. D. , Salomonis, N. , Vranizan, K. , Lawlor, S. C. , and Conklin, B. R. (2002). GenMAPP, a new tool for viewing and analysing microarray data on biological pathways. Nat. Genet. 31, 19–20.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Daniels, R. , Adjaye, J. , Bolton, V. , and Monk, M. (1998). Detection of a novel splice variant of the HPRT gene in human oocytes and preimplantation embryos. Implications for an RT-PCR based preimplantation diagnosis of Lesch Nyhan syndrome. Mol. Hum. Reprod. 4, 785–789.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dieterich, C. , Herwig, R. , and Vingron, M. (2003). Exploring potential targets of signaling pathways by predicting conserved transcription factor binding sites. Bioinformatics 19, 50–56.
| Crossref | GoogleScholarGoogle Scholar |
Dobson, A. T. , Raja, R. , Abeyta, M. J. , Taylor, T. , Shen, S. , Haqq, C. , and Pera, R. (2004). The unique transcriptome through day 3 of human preimplantation development. Hum. Mol. Genet. 13, 1461–1470.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Eberwine, J. (1996). Amplification of mRNA populations using aRNA generated from immobilized oligo(dT)-T7 primed cDNA. Biotechniques 20, 584–589.
| PubMed |
Eisen, M. B. , Spellman, P. T. , Brown, P. O. , and Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc. Natl Acad. Sci. USA 95, 14 863–14 868.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Evertsz, E. M. , Au-Young, J. , Ruvolo, M. V. , Lim, A. C. , and Reynolds, M. A. (2001). Hybridization cross-reactivity within homologous gene families on glass microarrays. Biotechniques 31, 1182–1192.
| PubMed |
Evsikov, A. V. , De Vries, W. N. , Peaston, A. E. , Radford, E. E. , Fancher, K. S. , Chen, F. H. , Blake, J. A. , Bult, C. J. , Latham, K. E. , Solter, D. , and Knowles, B. B. (2004). Systems biology of the 2-cell mouse embryo. Cytogenet. Genom. Res. 105, 2–4.
Ge, H. , Walhout, A. J. M. , and Vidal, M. (2003). Integrating ‘omic’ information: a bridge between genomics and systems biology. Trends Genet. 19, 551–560.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Goto, T. , Adjaye, J. , Rodeck, C. , and Monk, M. (1999). Identification of human primordial germ cell specific transcribed genes by differential display. Mol. Hum. Reprod. 5, 851–860.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hamatani, T. , Carter, M. G. , Sharov, A. A. , and Ko, M. S. H. (2004a). Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 6, 117–131.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hamatani, T. , Daikoku, T. , Wang, H. , Matsumoto, H. , Carter, M. G. , Ko, M. S. , and Dey, S. K. (2004b). Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation. Proc. Natl Acad. Sci. USA 101, 10 326–10 331.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Harris, M. A. , Clark, J. , Ireland, A. , Lomax, J. , and Ashburner, M. , et al. (2004). Gene Ontology Consortium. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res. 32, D258–D261.
| Crossref | GoogleScholarGoogle Scholar |
Hastie, T. , Tibshirani, R. , Eisen, M. B. , Alizadeh, A. , Levy, R. , Staudt, L. , Chan, W. C. , Botstein, D. , and Brown, P. (2000). ‘Gene shaving’ as a method for identifying distinct sets of genes with similar expression patterns. Genome Biol. 1, 3.1–3.21.
| Crossref | GoogleScholarGoogle Scholar |
Herwig, R. , Poustka, A. J. , Müller, C. , Bull, C. , Lehrach, H. , and O’Brien, J. (1999). Large-scale clustering of cDNA fingerprinting data. Genome Res. 9, 1093–1105.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Herwig, R. , Aanstad, P. , Clark, M. , and Lehrach, H. (2001). Statistical evaluation of differential expression on cDNA nylon arrays with replicated experiments. Nucleic Acids Res. 29, 117E.
| Crossref | GoogleScholarGoogle Scholar |
Huntriss, J. , Daniels, R. , Bolton, V. N. , and Monk, M. (1998). Imprinted expression of SNRPN in human preimplantation embryos. Am. J. Hum. Genet. 63, 1009–1014.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Huntriss, J. , Hinkins, M. , Oliver, B. , Harris, S. E. , Beazley, J. C. , Rutherford, A. J. , Gosden, R. G. , Lanzendorf, S. E. , and Picton, H. M. (2004). Expression of mRNAs for DNA methyltransferases and methyl-CpG-binding proteins in the human female germ line, preimplantation embryos, and embryonic stem cells. Mol. Reprod. Dev. 67, 323–336.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hurley, J. , Huntriss, J. , and Adjaye, J. (2000). Molecular approaches to the study of gene expression during human preimplantation development. Hum. Fertil. (Camb.) 3, 48–51.
| PubMed |
Ji, W. , Zhou, W. , Gregg, K. , Yu, N. , and Davis, S. (2004). A method for cross-species gene expression analysis with high-density oligonucleotide arrays. Nucleic Acids Res. 32, e93.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kanehisa, M. , Goto, S. , Kawashima, S. , and Nakaya, A. (2002). The KEGG databases at GenomeNet. Nucleic Acids Res. 30, 42–46.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Khatri, P. , Bhavsar, P. , Bawa, G. , and Draghici, S. (2004). Onto-Tools: an ensemble of web-accessible, ontology-based tools for the functional design and interpretation of high-throughput gene expression experiments. Nucleic Acids Res. 32, D449–D456.
| Crossref | GoogleScholarGoogle Scholar |
Ko, M. S. H. (2001). Embryogenomics: developmental biology meets genomics. Trends Biotechnol. 19, 511–518.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ko, M. S. H. (2004). Embryogenomics of pre-implantation mammalian development: current status. Reprod. Fertil. Dev. 16, 79–85.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ko, M. S. H. , Kitchen, J. R. , Wang, X. , Threat, T. A. , Hasegawa, A. , Sun, T. , Grahovac, M. J. , Kargul, G. J. , Lim, M. K. , Cui, Y. , Sano, Y. , Tanaka, T. , Liang, Y. , Mason, S. , Paonessa, P. D. , Sauls, A. D. , DePalma, G. E. , Sharara, R. , Rowe, L. B. , Eppig, J. , Morrell, C. , and Doi, H. (2000). Large scale cDNA analysis reveals phased gene expression patterns during preimplantation mouse development. Development 127, 1737–1749.
| PubMed |
Latham, K. E. , and Schultz, R. M. (2001). Embryonic genome activation. Front. Biosci. 6, D748–D759.
| PubMed |
Lazzari, L. , Wrenzycki, C. , Herrmann, D. , Duchi, R. , Kruip, T. , Niemann, H. , and Galli, C. (2002). Cellular and molecular deviations in bovine in vitro produced embryos are related to the Large Offspring syndrome. Biol. Reprod. 67, 767–775.
| PubMed |
Lockhart, D. J. , Dong, H. , Bryne, M. C. , Folletie, M. T. , Gallo, M. V. , Chee, M. S. , Mittmann, M. , Want, C. , Kobayashi, M. , Horton, H. , and Brown, E. L. (1996). DNA expression monitoring by hybridisation to high-density oligonucleotide arrays. Nat. Biotechnol. 14, 1675–1680.
| PubMed |
Ma, J. , Svoboba, P. , Schultz, R. M. , and Stein, P. (2001). Regulation of zygotic gene activation in the preimplantation mouse embryo: global activation and repression of gene expression. Biol. Reprod. 64, 1713–1721.
| PubMed |
Miller, N. A. , Gong, Q. , Bryan, R. , Ruvolo, M. , Turner, L. A. , and LaBrie, S. T. (2002). Cross-hybridization of closely related genes on high-density macroarrays. Biotechniques 32, 620–625.
| PubMed |
Neilson, L. , Andalibi, A. , Kang, D. , Coutifaris, C. , Strauss, F. J. , Stanton, J. A. , and Green, D. P. (2000). Molecular phenotype of the human oocyte by PCR-SAGE. Genomics 63, 13–24.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Niemann, H. , and Wrenzycki, C. (2000). Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development. Theriogenology 53, 21–34.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Piko, L. , and Clegg, K. B. (1982). Quantitative changes in total RNA, total poly(A), and ribosomes in early mouse embryos. Dev. Biol. 89, 362–378.
| PubMed |
Pitera, J. , Milla, P. , Scambler, P. , and Adjaye, J. (2001). Cloning of HOXD1 from unfertilised human oocytes and expression analyses during murine oogenesis and embryogenesis. Mech. Dev. 109, 377–381.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ponsuksili, S. , Wimmers, K. , Adjaye, J. , and Schellander, K. (2001). Expression of homeobox-containing genes in cDNA libraries derived from bovine unfertilised oocytes and preimplantation embryos. Mol. Reprod. Dev. 60, 297–301.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ponsuksili, S. , Tesfaye, D. , El-Halawany, N. , Schellander, K. , and Wimmers, K. (2002a). Stage-specific expressed sequence tags obtained during preimplantation bovine development by differential display RT-PCR and suppression subtractive hybridization. Prenat. Diagn. 12, 1135–1142.
| Crossref | GoogleScholarGoogle Scholar |
Ponsuksili, S. , Wimmers, K. , Adjaye, J. , and Schellander, K. (2002b). A source for expression profiling in single preimplantation bovine embryos. Theriogenology 57, 1611–1624.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ponsuksili, S. , Tesfaye, D. , El-Halawany, N. , Schellander, K. , and Wimmers, K. (2002c). Stage-specific expression sequence tags obtained during preimplantation bovine development by differential display RT-PCR and suppression subtractive hybridisation. Prenat. Diagn. 22, 1135–1142.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Quackenbush, J. (2001). Computational analysis of microarray data. Nat. Rev. Genet. 2, 418–427.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rajkovic, A. , Yan, M. S. C. , Klysik, M. , and Matuk, M. (2001). Discovery of germ cell-specific transcripts by expressed sequence tag database analysis. Fertil. Steril. 76, 550–554.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roberts, C. , Barnes, F. L. , Hue, I. , and Sirard, M. A. (2000). Subtractive hybridisation used to identify mRNA associated with the maturation of bovine oocytes. Mol. Reprod. Dev. 57, 167–175.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roozemond, R. C. (1976). Ultramicrochemical determination of nucleic acids in individual cells using the Zeiss UMSP-I microspectrophotometer. Application to isolated rat hepatocytes of different ploidy classes. Histochem. J. 8, 625–638.
| PubMed |
Rothstein, J. L. , Johnson, D. , Jessee, J. , Skowronski, J. , DeLoia, J. A. , Solter, D. , and Knowles, B. B. (1993). Construction of primary and subtracted cDNA libraries from early embryos. Methods Enzymol. 225, 587–610.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sasaki, N. , Nagaoka, S. , Itoh, M. , Izawa, M. , Konno, H. , Carninci, P. , Yoshiki, A. , Kusakabe, M. , Moriuchi, T. , Muramatsu, M. , Okazaki, Y. , and Hayashizaki, Y. (1998). Characterization of gene expression in mouse blastocyst using single-pass sequencing of 3995 clones. Genomics 49, 167–179.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schena, M. , Shalon, D. , Davis, R. W. , and Brown, P. O. (1995). Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270, 467–470.
| PubMed |
Sharov, A. A. , Piao, Y. , Matoba, R. , Dudekula, D. B. , and Qian, Y. , et al. (2003). Transcriptome analysis of mouse stem cells and early embryos. PLoS Biol. 1, E74.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Smelt, V. A. , Upton, A. , Adjaye, J. , Payton, M. , Boukouvala, S. , Johnson, N. , Mardon, H. J. , and Sim, E. (2000). Expression of arylamine N-acetyltransferases in pre-term placentals and in human pre-implantation embryos. Hum. Mol. Genet. 9, 1101–1107.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stanton, J. L. , and Green, D. P. (2002). A set of 1542 mouse blastocyst and pre-blastocyst genes with well-matched human homologues. Mol. Hum. Reprod. 8, 149–166.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stanton, J. L. , Bascand, M. , Fisher, L. , Quinn, M. , Macgregor, A. , and Green, D. P. (2002). Gene expression profiling of human GV oocytes: an analysis of a profile obtained by Serial Analysis of Gene Expression (SAGE). J. Reprod. Immunol. 53, 193–201.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stanton, J. L. , Macgregor, A. B. , and Green, D. P. (2003). Gene expression in the mouse preimplantation embryo. Reproduction 125, 457–468.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Steuerwald, N. , Cohen, J. , Herrera, R. J. , and Brenner, C. A. (1999). Analysis of gene expression in single oocytes and embryos by real-time rapid cycle fluorescence monitored RT-PCR. Mol. Hum. Reprod. 5, 1034–1039.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tamayo, P. , Slonim, D. , Mesirov, J. , Zhu, Q. , Kitareewan, S. , Dmitrovsky, E. , Lander, E. S. , and Golub, T. R. (1999). Interpreting patterns of gene expression with self-organizing maps: methods and applications to hematopoietic differentiation. Proc. Natl Acad. Sci. USA 96, 2907–2912.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tanaka, T. S. , and Ko, M. S. H. (2004). A global view of gene expression in the preimplantation mouse embryo: morula versus blastocyst. Eur. J. Obstet. Gynecol. Reprod. Biol. 115, S85–S91.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tesfaye, D. , Ponsuksili, S. , Wimmers, K. , Gilles, M. , and Schellander, K. (2003). Identification and quantification of differentially expressed transcripts in in vitro-produced bovine preimplantation stage embryos. Mol. Reprod. Dev. 66, 105–114.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Uenishi, H. , Eguchi, T. , Suzuki, K. , Sawazaki, T. , Toki, D. , Shinkai, H. , Okumura, N. , Hamasima, N. , and Awata, T. (2004). PEDE (Pig EST Data Explorer): construction of a database for ESTs derived from porcine full-length cDNA libraries. Nucleic Acids Res. 32, D484–D488.
| Crossref | GoogleScholarGoogle Scholar |
Volinia, S. , Evangelisti, R. , Francioso, F. , Arcelli, D. , Carella, M. , and Gasparini, P. (2004). GOAL: automated Gene Ontology analysis of expression profiles. Nucleic Acids Res. 32, D492–D499.
Wang, Q. T. , Piotrowska, K. , Ciemerych, M. A. , Milenkovic, L. , Scott, M. P. , Davis, R. W. , and Zernicka-Goetz, M. (2004). A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev. Cell 6, 133–144.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wolfinger, R. D. , Gibson, G. , Wolfinger, E. D. , Bennett, L. , Hamadeh, H. , Bushel, P. , Afshari, C. , and Paules, R. S. (2001). Assessing gene significance from cDNA microarray expression data via mixed models. J. Comput. Biol 8, 625–637.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wrenzycki, C. , Herrmann, D. , Keskintepe, L. , Martins, A. , Sirisathien, S. , Brackett, B. , and Niemann, H. (2001). Effects of basic culture medium and protein supplementation on mRNA expression in preimplantation bovine embryos. Hum. Reprod. 16, 893–901.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wrenzycki, C. , Herrmann, D. , and Niemann, H. (2003). Timing of blastocyst expansion affects spatial mRNA expression patterns of genes in bovine blastocysts produced in vitro. Biol. Reprod. 68, 2073–2080.
| PubMed |
Yang, Y. H. , Dudoit, S. , Luu, P. , Lin, D. M. , Peng, V. , Ngai, J. , and Speed, T. P. (2002). Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30, 15E.
| Crossref | GoogleScholarGoogle Scholar |
Yao, Y.-Q. , Xu, J.-S. , Lee, W. M. , Yeung, W. S. B. , and Lee, K.-F. (2003). Identification of mRNAs that are up-regulated after fertilization in the murine zygote by suppression subtractive hybridization. Biochem. Biophys. Res. Commun. 304, 60–66.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zimmermann, I. W. , and Schultz, R. M. (1994). Analysis of gene expression in the preimplantation embryo: use of mRNA differential display. Proc. Natl Acad. Sci. USA 91, 5456–5460.
| PubMed |
