Abstract
Transcriptional profiling by microarray hybridization has become a standard method to analyze global gene expression and has resulted in the availability of enormous amounts of experimental data. Given the number of different microarray platforms currently in use, it is critical to determine how reproducible results are from one platform to another. Additional variability may also arise from tissue collection and protocol differences among laboratories. In an effort to identify genes whose maternal mRNA pools are critical during preimplantation development, we compared published results of three independent studies of the mouse preimplantation embryo transcriptome, each performed in a different laboratory using different microarray platforms. We searched the combined data set for genes whose expression patterns were consistent among the three experiments. Querying for presence or absence at single developmental windows indicates that between 52% and 60% of genes are in agreement among the three experiments. Searching for expression patterns across three developmental windows (oocyte + 1-cell, 2- through 8-cell, and blastocyst stage) revealed approximately 33% agreement among the three experiments, although the majority of these genes were either always present or always absent. Using this approach, we identified 51 genes with a predicted expression pattern of maternal RNA only (not present during 2-cell through 8-cell or at the blastocyst stage). RT-PCR validation indicates 37 (72%) of these candidates have the microarray-predicted expression pattern and represent candidate maternal-effect genes. Based on our analysis, we conclude that data mining microarray experiments in this way greatly enhances candidate gene expression pattern accuracy.
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Calabi F, Pannell R, Pavloska G (2001) Gene targeting reveals a crucial role for MTG8 in the gut. Mol Cell Biol 21, 5658–5666
Carabatsos MJ, Sellitto C, Goodenough DA, Albertini DF (2000) Oocyte-granulosa cell heterologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence. Dev Biol 226, 167–179
Christians E, Davis AA, Thomas SD, Benjamin IJ (2000) Maternal effect of Hsf1 on reproductive success. Nature 407, 693–694
Colledge WH, Carlton MB, Udy GB, Evans MJ (1994) Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature 370, 65–68
Dai M, Wang P, Boyd AD, Kostov G, Athey B, et al. (2005) Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res 33, e175
Draghici S, Khatri P, Martins RP, Ostermeier GC, Krawetz SA (2003) Global functional profiling of gene expression. Genomics 81, 98–104
Fisher CR, Graves KH, Parlow AF, Simpson ER (1998) Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc Natl Acad Sci USA 95, 6965–6970
Gunther T, Chen ZF, Kim J, Priemel M, Rueger JM, et al. (2000) Genetic ablation of parathyroid glands reveals another source of parathyroid hormone. Nature 406, 199–203
Hamatani T, Carter MG, Sharov AA, Ko MS (2004) Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 6, 117–131
Howell CY, Bestor TH, Ding F, Latham KE, Mertineit C, et al. (2001) Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 104, 829–838
Ibrahim AF, Hedley PE, Cardle L, Kruger W, Marshall DF, et al. (2005) A comparative analysis of transcript abundance using SAGE and Affymetrix arrays. Funct Integr Genomics 5, 163–174
Khatri P, Draghici S, Ostermeier GC, Krawetz SA (2002) Profiling gene expression using onto-express. Genomics 79, 266–270
Kim SK, Lund J, Kiraly M, Duke K, Jiang M, et al. (2001) A gene expression map for Caenorhabditis elegans. Science 293, 2087–2092
Kissel H, Timokhina I, Hardy MP, Rothschild G, Tajima Y, et al. (2000) Point mutation in kit receptor tyrosine kinase reveals essential roles for kit signaling in spermatogenesis and oogenesis without affecting other kit responses. EMBO J 19, 1312–1326
Kitsukawa T, Shimizu M, Sanbo M, Hirata T, Taniguchi M, et al. (1997) Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19, 995–1005
Ko MS, Kitchen JR, Wang X, Threat TA, Wang X, et al. (2000) Large-scale cDNA analysis reveals phased gene expression patterns during preimplantation mouse development. Development 127, 1737–1749
Kuo WP, Jenssen TK, Butte AJ, Ohno-Machado L, Kohane IS (2002) Analysis of matched mRNA measurements from two different microarray technologies. Bioinformatics 18, 405–412
Mecham BH, Klus GT, Strovel J, Augustus M, Byrne D, et al. (2004) Sequence-matched probes produce increased cross-platform consistency and more reproducible biological results in microarray-based gene expression measurements. Nucleic Acids Res 32, e74
Ny A, Leonardsson G, Hagglund AC, Hagglof P, Ploplis VA, et al. (1999) Ovulation in plasminogen-deficient mice. Endocrinology 140, 5030–5035
Park PJ, Cao YA, Lee SY, Kim JW, Chang MS, et al. (2004) Current issues for DNA microarrays: platform comparison, double linear amplification, and universal RNA reference. J Biotechnol 112, 225–245
Rankin T, Talbot P, Lee E, Dean J (1999) Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss. Development 126, 3847–3855
Ratnam S, Mertineit C, Ding F, Howell CY, Clarke HJ, et al. (2002) Dynamics of Dnmt1 methyltransferase expression and intracellular localization during oogenesis and preimplantation development. Dev Biol 245, 304–314
Segi E, Sugimoto Y, Yamasaki A, Aze Y, Oida H, et al. (1998) Patent ductus arteriosus and neonatal death in prostaglandin receptor EP4-deficient mice. Biochem Biophys Res Commun 246, 7–12
Sun X, Meyers EN, Lewandoski M, Martin GR (1999) Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev 13, 1834–1846
Tan PK, Downey TJ, Spitznagel EL Jr, Xu P, Fu D, et al. (2003) Evaluation of gene expression measurements from commercial microarray platforms. Nucleic Acids Res 31, 5676–5684
Tetzlaff MT, Yu W, Li M, Zhang P, Finegold M, et al. (2004) Defective cardiovascular development and elevated cyclin E and Notch proteins in mice lacking the Fbw7 F-box protein. Proc Natl Acad Sci U S A 101, 3338–3345
Tong ZB, Gold L, Pfeifer KE, Dorward H, Lee E, et al. (2000) Mater, a maternal effect gene required for early embryonic development in mice. Nat Genet 26, 267–268
Varfolomeev EE, Schuchmann M, Luria V, Chiannilkulchai N, Beckmann JS, et al. (1998) Targeted disruption of the mouse Caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9, 267–276
Wang QT, Piotrowska K, Ciemerych MA, Milenkovic L, Scott MP, et al. (2004) A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev Cell 6, 133–144
White KP, Rifkin SA, Hurban P, Hogness DS (1999) Microarray analysis of Drosophila development during metamorphosis. Science 286, 2179–2184
Wu X, Viveiros MM, Eppig JJ, Bai Y, Fitzpatrick SL, et al. (2003) Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat Genet 33, 187–191
Yuen T, Wurmbach E, Pfeffer RL, Ebersole BJ, Sealfon SC (2002) Accuracy and calibration of commercial oligonucleotide and custom cDNA microarrays. Nucleic Acids Res 30, e48
Zeng F, Schultz RM (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
Zeng F, Schultz RM (2005) RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. Dev Biol 283, 40–57
Zeng F, Baldwin DA, Schultz RM (2004) Transcript profiling during preimplantation mouse development. Dev Biol 272, 483–496
Acknowledgments
The authors thank Rocio M. Rivera for setting up timed matings for embryo collection. JM is supported by a postdoctoral fellowship from the Damon Runyon Cancer Research Foundation, and this work was supported in part by NIH grant HD-42026 (MSB and RMS) and the Howard Hughes Medical Institute (MSB).
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Mager, J., Schultz, R.M., Brunk, B.P. et al. Identification of candidate maternal-effect genes through comparison of multiple microarray data sets. Mamm Genome 17, 941–949 (2006). https://doi.org/10.1007/s00335-006-0034-6
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DOI: https://doi.org/10.1007/s00335-006-0034-6