Molecular Human Reproduction, Vol. 7, No. 6, 521-543,
June 2001
© 2001 European Society of Human Reproduction and Embryology
Embryology |
A set of 840 mouse oocyte genes with well-matched human homologues
Department of Anatomy and Structural Biology, University of Otago, Medical School, P.O.Box 913, Dunedin, New Zealand
Abstract
GenBank contains 14 477 expressed sequence tags (EST) derived from mouse oocyte cDNA libraries: 3499 of these are from two unfertilized oocyte libraries and 10 978 are from two fertilized oocyte libraries. Gene expression profiles were obtained for these libraries by matching library EST to UniGene clusters. The 14 477 EST identified 4226 UniGenes. These were screened using HomoloGene to identify 1386 homologous UniGene clusters in two other species with one of the matches being human. Within these human matches, 840 encoded named proteins, 223 encoded hypothetical proteins, and 323 encoded clustered EST. The set of named genes provides the first step in establishing a database of genes expressed in mouse oocytes and, by extension, human oocytes.
gene expression/HomoloGene/human homologues/oocytes/UniGene
Introduction
The ovulated mammalian oocyte is a large spherical cell arrested in second meiotic metaphase. Fertilization releases the oocyte from cell cycle arrest and initiates a succession of events that include incorporation of the male nucleus and the activation of embryonic development. Little is known of the molecular bases of these events. A major impediment is the dearth of information about the molecular composition of mammalian oocytes.
One approach to eliminating this shortage of information is to use DNA sequence data deposited in GenBank. Among these data are 71 346 EST derived from 15 mouse preimplantation cDNA libraries. Two of these libraries, derived from unfertilized mouse oocytes, contain an aggregate of 3499 EST; a further two libraries, derived from fertilized oocytes, contained 10 978 EST. Collectively, these amounted to 14 477 EST. A majority of the EST (~80%) could be mapped to UniGene clusters. This mapping produced a set of 4226 mouse oocyte UniGenes. UniGenes can be screened using the HomoloGene database to identify those with homology to UniGenes in two other species. In the case of the mouse oocyte, this screen produced 1386 genes with human homologues of which 840 are for named genes. This set of named genes provides the first step in establishing a database of genes expressed in mouse oocytes and, by extension, human oocytes.
This paper describes the procedures used to obtain these results and a discussion of the impact of data sets of this size on our understanding of mouse preimplantation development.
Materials and methods
The 14 477 EST used in this analysis were downloaded as UniGene libraries from www.ncbi.nlm.nih.gov/CGAP/. The catalogue numbers of the UniGene libraries in this analysis were 89 (403 EST) and 151 (3096 EST) for the unfertilized oocyte, and 106 (3314 EST) and 319 (7664 EST) for the fertilized oocyte. Detailed descriptions of cDNA library construction are available from the UniGene website. The cDNA libraries were non-normalized.
The UniGene libraries were imported into FileMaker Pro (Claris Corporation, Santa Clara, California, USA) for construction of three EST databases: one for unfertilized oocytes (3499 EST), one for fertilized oocytes (10 978 EST), and one for the combined set of EST (14 477 EST). UniGene Cluster Numbers were identified for each EST GenBank Accession Number. Digital gene expression profiles were generated by summing UniGene cluster abundances. Gene expression profiles for unfertilized and fertilized mouse oocytes were compared using Fisher's exact test. The HomoloGene database (ftp://ftp.ncbi.nlm.nih.gov/pub/HomoloGene) was also imported into FileMaker Pro. We used the non-redundant homology sets in the hmlg.trip.ftp file. These sets are reciprocal best matches that are mutually consistent between at least three organisms. We identified the subset of mouse oocyte UniGenes in this file with human UniGenes as one of the matches. The version of the HomoloGene database that we used was constructed from UniGene build #8 for Danio rero (zebrafish), #79 for Mus musculus (mouse), #77 for Rattus norvegicus (rat), and #118 for Homo sapiens (human). Additional information on mouse UniGenes was obtained using the Locus Link database and the Online Mendelian Inheritance in Man (OMIM) database, both found at the NIH website listed above.
Results
The starting point for the work described in this paper is a collection of 14 477 EST that are deposited in GenBank. These EST were derived from random sequencing of four mouse oocyte cDNA libraries. The EST from each cDNA library were imported into FileMaker Pro as UniGene libraries and converted to an in-house database. Each of the EST had a GenBank entry number. In about 80% of cases, the GenBank entry could be matched to a UniGene cluster. Sub-routines could be written in FileMaker Pro to allow sorting of UniGene numbers. This generated a profile of UniGene cluster abundances. Digital gene expression profiles were generated for single cDNA libraries or combinations of libraries.
All four cDNA libraries whose EST were used in this study were non-normalized. Two libraries were derived from unfertilized oocytes and two from fertilized oocytes. We first asked whether the gene expression profile of the unfertilized mouse oocyte differed significantly from that of the fertilized oocyte using Fisher's exact test. Using this test, there were no genes whose transcript levels differed significantly between unfertilized and fertilized mouse oocytes. All EST were therefore amalgamated into a single set and treated as representative of the mouse oocyte at the time of fertilization.
The EST obtained by this method generated 4226 UniGenes. These genes all merit further investigation. However, to make the analysis tractable, we began with a subset of mouse UniGenes with homologues in two other species, one of which was human. This restricted the analysis to 1386 UniGenes. Each UniGene was classified into one of three categories: (i) a matched gene with an official symbol and name (840 Unigenes), (ii) a gene encoding a hypothetical protein (223 UniGenes), or (iii) a set of overlapping EST (323 UniGenes).
The advantage of knowing the human homologue of a particular mouse gene cannot be overestimated. It provides access to Online Mendelian Inheritance in Man (OMIM) and Locus Link. Using this approach, each of the 840 UniGenes with well-matched human homologues was assigned to one of 17 Tables. Tables I–XVI
are based on function, and Table XVII represents the balance of unassigned genes (see appendix or http://anatomy.otago.ac.nz/green_egg_database). The structure of each entry is as follows: mouse Unigene number, corresponding human UniGene number, the official gene symbol currently employed by the NIH, and the number of EST assigned by us to that UniGene from the catalogue of 14 477 EST. The next line contains the official description of the gene as assigned by the NIH. Genes were assigned to a Table after investigation of their database entry. This investigation included, where possible, an evaluation of their OMIM entry and their domain structure in Locus Link, as well as BLAST searches. In most cases, the gene had a single, dominant function and was assigned to one of the Tables on that basis. In some cases, a gene could be assigned functionally to more than one Table. In these cases, it was entered in each Table as appropriate.
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Discussion
Preliminary comparison of unfertilized and fertilized oocyte gene expression showed no significant differences in expression between the two stages. This is consistent with the maternal origin of most, if not all, transcripts in the fertilized oocyte. An analysis of the aggregate of 14 477 mouse oocyte EST identified 840 genes that match genes of human and one other species. The rigour of this three-way matching makes it unlikely that the mouse-human matches will be reassigned at a future date. These genes therefore currently represent the most secure gene assignments available for mammalian oocytes. Because the EST in GenBank are invariably longer than those obtained by Serial Analysis of Gene Expression (SAGE), the assignments in this set are inherently more reliable than those obtained by SAGE analysis of the human oocyte (Neilson et al., 2000).
The UniGene clusters identified in this paper (Tables I–XVII
)
all have gene symbols and names. These are assigned by the NIH. In some cases, these are official gene symbols and names, in other cases they are interim assignments. The gene symbols are of various kinds: some are abbreviations of the name; others represent the catalogue number assigned by one of a number of sequencing projects (typically a KIAA number or a DKFZ number). Care is needed in identifying the function of a gene product because its name, as an annotation of function, can often be misleading. An example is the UniGene cluster (mouse no. 2411, human no. 6727) whose description is `Ras GTP-ase activating protein SH3 domain-binding protein 2'. This is a highly expressed transcript with 63 EST. The Reference Sequence (RefSeq) in Locus Link identifies three domains: an RNA recognition motif, a domain found in RNA transport proteins, and a nuclear transport factor 2 [NTF2] domain. It lacks a GTPase-activating domain and a binding site for SH3 motifs. The gene is therefore catalogued in Table XVI (RNA, Transcription). A second example of early misidentification is the `regulator of G protein signalling 2' that is now recognized to regulate G protein signalling (Ross and Wilkie, 2000). When first discovered, it was regarded as a transcription factor because of an apparent helix–loop–helix motif. Rigorously identifiable domains are not currently available for many genes in the set published here. As a consequence, definitive assignments of function are not always possible.
The availability of large sets of candidate genes makes it possible to focus on complex pathways and systems operating in cells. Particular clarity can be brought to bear on the analysis when the focus is restricted to a single cell type, because of the absence of potentially confounding signals that groups of differentiated cells are likely to introduce. Preimplantation embryogenesis provides a useful test for this approach because it follows a single cell type through a succession of defined developmental stages.
Two of the most important experimental challenges in mammalian fertilization are the mechanism of sperm fusion with the oocyte and the mechanism of oocyte activation. A significant body of evidence over the past decade has suggested a role for the interaction of disintegrins in spermatozoa with integrins in the oocyte, with a particular focus on 
6ß1 integrin. Expression of 6 integrin has been demonstrated in mouse oocytes by RT-PCR (Tarone et al., 1993). Transcripts for 6 integrin exist in the current catalogue (Table VII). Despite evidence that 6ß1 integrin plays a role in mouse fertilization, recent experiments indicate that 6 -/- knockout mice are fertile (Miller et al., 2000). The mouse oocyte catalogue also contains transcripts for 9 integrin. Recent data on 9 suggest that it has a widespread and highly conserved function in recognition of disintegrins and it has been suggested that this function may play a role in sperm binding to oocytes (Eto et al., 2000). The mouse oocyte 9 integrin EST in GenBank are the first evidence that these oocytes express 9. Mouse oocytes also contain transcripts for fibulin 5 (Nakamura et al., 1999), a newly-identified secreted protein that contains an RGD sequence motif that may be a novel ligand for integrin receptors. Fibulin 5 could play an autocrine function in the developing embryo if secreted into the perivitelline space.
Mouse oocytes also contain transcripts for a number of receptors in addition to the integrins. These are of interest because of their possible role in oocyte activation. When viewed in conjunction with proteins involved in signalling pathways, the most striking transcript is that for `regulator of G protein signallling 2' (RGS2), for which there are 29 EST in the mouse oocyte catalogue. Levels of RGS2 collapse following the first cell division (J.L.Stanton and D.P.L.Green, unpublished data) suggesting a role for RGS2 protein that ceases after fertilization. Mouse oocytes also contain transcripts for `regulator of G protein signalling 17', although these do not change their level significantly following fertilization. RGS proteins are a recently identified family that attenuate G protein signalling (Ross and Wilkie, 2000). It has been suggested that RGS proteins suppress basal signal output without sacrificing maximum signalling capacity. Following this line of thought, high transcript levels of RGS proteins would suggest that unfertilized oocytes need to suppress the risk of premature activation from excessive basal activity of G proteins. Since oocyte activation produces the zona pellucida block to polyspermy, suppression of premature activation ensures that an oocyte remains fertilizable. Moreover, the presence of at least two, newly discovered, regulators of G protein signalling as major transcripts in mouse oocytes suggests that the role of G protein signalling in mammalian oocytes is still poorly understood, notwithstanding the considerable body of experimental data that has accumulated in the past decade. There are several G protein-coupled receptors (GPCR) in the catalogue (GPCR 56, GPCR 85, an orphan GPCR, and BAI3) but the significance of these receptors is unclear at the present time.
One of the consequences of the first and subsequent cell divisions following fertilization is that blastomeres bring their surfaces to bear on each other and generate the capacity for contact-mediated intercellular signalling. Transcripts for these proteins have to be present prior to translation and presentation. Membrane proteins that already have known or putative functions following blastomere contact include E-, N- and P-cadherins, mcl1 (Rinkenberger et al., 2000), angio-associated migratory cell protein (AAMP) (Beckner et al., 1995), ninjurin (NINJ1) (Araki et al., 1997), FAT (Mahoney et al., 1991), and the G protein-coupled receptor `brain-specific angiogenesis inhibitor 1' (BAI3). E-cadherin is concentrated at contacts between blastomeres (Vestweber et al., 1987) and plays a major role in their adhesion (Larue et al., 1994; Riethmacher et al., 1995; Torres et al., 1997), as both E-cadherin- and -catenin-null mutant embryos are unable to form a trophectoderm epithelium at the blastocyst stage (Larue et al., 1994; Riethmacher et al., 1995; Torres et al., 1997). Mcl1 is a membrane protein associated with early differentiation of stem cells (Kozopas et al., 1993). Its function is currently unknown, although homozygous mcl1 -/- knockouts result in peri-implantation lethality due to a failure to implant (Rinkenberger et al., 2000). The defect lies with the trophectoderm cells, not with the inner cell mass. Affected embryos also show delayed compaction. BAI3 is closely related to BAI1 which has an extended extracellular domain containing an RGD motif and five thrombospondin I repeats (Nishimori et al., 1997; Shiratsuchi et al., 1997). It may be capable of interacting with integrins on adjacent blastomeres through its RGD motif and with CD36 through its thrombospondin repeats.
The previous paragraph dealt with surface interactions. In this paragraph, we draw attention to gene transcripts that may underpin signalling downstream from these interactions, particularly from cadherin/catenin complexes. The catalogue includes transcripts for - and ß-catenins, presenilins 1 and 2, DLG1 (Drosophila `discs large'), and LLGL1 (Drosophila `lethal giant larvae'). Transcripts also exist in mouse preimplantation embryos for APC (adenomatous polyposis coli), glycogen synthase kinase 3ß (Gsk3ß), axin, T-cell factor 1 (Tcf1), and EST highly similar to exportin 1 (XPO1, also = Crm1) (J.L.Stanton and D.P.L.Green, unpublished data). ß-catenin plays a central role in Wnt/wingless signalling and, in the absence of activity in this pathway, ß-catenin is degraded by a complex containing axin, Gsk3ß, and the tumour suppressor gene product, APC. When Frizzled receptors are stimulated by Wnt ligands, the constitutive activity of GSK3ß in the degradation complex is inhibited and ß-catenin translocates into the nucleus, where it stimulates transcription of target genes (including T-cell transcription factors). APC shuttles ß-catenin using the CRM1 pathway (Henderson, 2000; Rosin-Arbesveld et al., 2000) and inactivating mutations of APC result in constitutive nuclear signalling and gene activation.
APC-ß-catenin complexes also bind to DLG1, the prototype of the MAGUK family (membrane-associated guanylate kinase homologues). DLG1 regulates cortical localization of the gene product of lethal giant larvae (Lgl) in Drosophila (Ohshiro et al., 2000; Peng et al., 2000) in a process that is essential for asymmetric cortical localization in mitotic neuroblasts. This creates intrinsic differences between daughter cells that would otherwise be identical. Given that transcripts for these proteins are present in mouse oocytes at fertilization, similar processes might operate in establishing polarity and cell fate in mouse embryos as they move to compaction.
E-cadherin, -catenin and ß-catenin also form complexes with the membrane proteins, presenilin 1 and 2 at intercellular contacts (Georgakopoulos et al., 1999). Presenilins are essential for Notch signalling through endoproteolysis of Notch and release of Notch intracellular domain (NICD) (De Strooper et al., 1999). They are also responsible for cleavage of members of the APP family and Ire1. Their potential recruitment at cell–cell junctions between blastomeres may activate Notch signalling in early embryogenesis. Although mice lacking both presenilin genes do not show embryonic lethality until embryonic day 9.5 (Donoviel, 1999), numerous developmental defects emerge before death. Finally, cadherin-catenin complexes also interact with other proteins such as p120ctn, 
-catenin, actin, vinculin, ZO-1, IQGAP1, receptor tyrosine phosphatases, and tyrosine kinase receptors (Gumbiner, 2000). Transcripts for -catenin, actin, vinculin, receptor tyrosine phosphatases and tyrosine kinase receptors exist in mouse oocytes or mouse preimplantaion embryos (J.L.Stanton and D.P.L.Green, unpublished data).
The discussion of the cadherin-catenin system, although speculative, is underpinned by the existence of transcripts for most of the proteins in mouse oocytes or preimplantation embryos and the proven importance of E-cadherin and -catenin in early mouse embryogenesis. It illustrates the capacity of large gene sets to identify complex pathways and systems in single cell types where the molecular phenotype is not confused by transcripts from other cells. Other pathways and systems that could equally have been discussed include histone acetylation and deacetylation, the cell cycle, circadian genes, ubiquitination and proteasome degradation. Relevant gene transcripts exist in mouse oocytes for all these pathways.
One of the questions raised by the genes identified here is the function of the remaining 546 UniGenes in the set of 1386 that are not currently named but for which no indication of function is currently available. These hypothetical proteins and EST represent a rich source of potentially novel proteins. Because of the way that UniGene clusters are established, they may be germ-line variants of genes encoding somatic cell proteins or they may be members of entirely novel and unsuspected gene families. Particular interest attaches to proteins associated with chromatin assembly and transcription because of the recently identified ability of enucleated oocytes to reprogramme somatic cell nuclei to totipotency (Wilmut et al., 1997; Wakayama et al., 1998). The efficiency of this process is low but could conceivably be improved by a greater understanding of: (i) the perturbations produced by the enucleation/renucleation step, and (ii) the differences in chromatin structure and transcription factors that distinguish oocytes from somatic cells.
In addition to gene discovery, the set of genes described in this paper provides the basis for building DNA microarrays targeted at the ovulated oocyte and early embryonic development in mouse. Given the relative inaccessibility of human embryonic material, the use of HomoloGene to identify genes likely to be found in human oocytes and human preimplantation embryos provides a route to a DNA microarray targeted at human embryos. Many UniGenes, whether mouse or human, have corresponding IMAGE clones (I.M.A.G.E. consortium http://image.llnl.gov/) that provide the source material for building these microarrays. Targeted DNA microarrays promise high throughput monitoring of mouse embryogenesis for experimental purposes and the possibility of diagnostics for assessing human embryo quality in assisted human reproduction.
Appendix
Acknowledgements
We wish to thank Andrew MacGregor for his invaluable assistance in helping construct databases in FileMaker Pro. This work was supported by grants from the Marsden Fund and the New Economy Research Fund.
Notes
1 To whom correspondence should be addressed. E-mail: david.green{at}stonebow.otago.ac.nz 
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