Proteomic-based identification of maternal proteins in mature mouse oocytes
© Zhang et al; licensee BioMed Central Ltd. 2009
Received: 24 February 2009
Accepted: 3 August 2009
Published: 3 August 2009
The mature mouse oocyte contains the full complement of maternal proteins required for fertilization, reprogramming, zygotic gene activation (ZGA), and the early stages of embryogenesis. However, due to limitations of traditional proteomics strategies, only a few abundantly expressed proteins have yet been identified. Our laboratory applied a more effective strategy: one-dimensional sodium dodecyl sulfate polyacrylamide gel electrophoresis (1D SDS-PAGE) and reverse-phase liquid chromatography tandem mass spectrometry (RP-LC-MS/MS) were employed to analyze the mature oocyte proteome in depth.
Using this high-performance proteomic approach, we successfully identified 625 different proteins from 2700 mature mouse oocytes lacking zona pellucidae. This is the largest catalog of mature mouse oocyte proteins compiled to date. According to their pattern of expression, we screened 76 maternal proteins with high levels of mRNA expression both in oocytes and fertilized eggs. Many well-known maternal effect proteins were included in this subset, including MATER and NPM2. In addition, our mouse oocyte proteome was compared with a recently published mouse embryonic stem cell (ESC) proteome and 371 overlapping proteins were identified.
This proteomics analysis will be a valuable resource to aid in the characterization of important maternal proteins involved in oogenesis, fertilization, early embryonic development and in revealing their mechanisms of action.
Mammalian reproduction is a complicated physiological process involving many important events, such as generation of mature gametes, fertilization, zygotic gene activation (ZGA), and embryonic development. Thus far, the key molecules and mechanisms involved in these events remain poorly characterized. Mammalian oocytes, a highly specialized cell type, play unique roles in reproduction because only in these cells are maternal proteins and transcripts crucial for the above-mentioned processes.
During oogenesis, oocytes synthesize and accumulate a number of maternal proteins. Some of them function in the formation of follicles and/or the growth of the oocytes, including, Figα, GDF9, and BMP15 [1–3]. However, many maternal proteins stored in oocytes play significant roles in later stages, namely fertilization and early embryogenesis. The corresponding genes are called maternal effect genes , and we call the proteins they code for maternal effect proteins. Maternal effect genes/proteins have been shown to be important in early embryonic development of Drosophila melanogaster and Xenoupus laevis [5, 6]. Several maternal-effect genes/proteins have recently been identified in mammals, and their importance in embryonic development has also been demonstrated. MATER (Maternal antigen that embryos require; official name Nlrp5) is one of the first characterized maternal effect proteins in mice, the absence of which precludes embryonic progression beyond the 2-cell stage . Npm2 is another well characterized maternal effect protein, which is required for nuclear and nucleolar organization during embryonic development . Much research has been done to identify maternal effect genes or proteins essential for preimplantation or postimplantation mouse embryo development. Dppa3, Padi6, Tle6 and Floped were successfully identified in individual studies [9–11], but there remain many unknown players. Therefore, the identification and molecular characterization of novel maternal proteins will be of great significance and novel proteomic technologies can potentially deduce most of the maternal proteins in mature oocytes.
There are several recent reports utilizing proteomics approaches to the study of ooctyes, including the exploration of the bovine, pig and mouse oocyte proteomes [12–16]. For example, Calvert et al. identified 8 highly abundant heat shock proteins (HSPs) and related chaperones in the mature mouse egg by two-dimensional electrophoresis (2DE) . Vitale et al. used 2DE and mass spectrometry (MS) to identify 12 proteins that appeared to be differentially expressed between germinal vesicle (GV) and metaphase II (MII) murine oocytes . In our previous work that demonstrated post-translational modifications of maternal proteins, we used a similar approach to perform large-scale protein identification in mature mouse oocytes, and we successfully identified a total of 380 different proteins corresponding to 869 proteins spots . The 2DE platform is valuable to analyze heterogeneity of proteins in the forms of alternative splicing, post-translation modifications, etc [18, 19]. Although 2DE continues to be a very popular tool for studying the proteome, it has some limitations in identifying proteins that have either high or low molecular masses, those with extreme isoelectric points (pIs), those are highly hydrophobic, and those of low abundance . 1D SDS-PAGE liquid chromatography tandem mass spectrometry (LC-MS/MS)-a combination of 1DE protein separation and LC-MS/MS analysis-has been used widely and is generally accepted as a more effective method of studying the proteome [21, 22]. It is technically simple and combines improved protein separation capability that also captures those proteins typically not accessible via 2D PAGE (notably large proteins and those with transmembrane domains) with the well-established sensitivity of gel-based protein identification using MS for less complex samples . For the purpose of identifying novel maternal proteins, we employed this high-performance proteomic approach to analyze proteins extracted from 2700 mature mouse oocytes lacking zona pellucidae and we successfully identified 625 different proteins. The maternal protein compilation provided here is intended to serve as an important tool for expanding our knowledge of the regulation of multiple processes in mammalian reproduction.
Identification of Mature Oocyte Proteins
GO and Pathway Analysis of the Identified Proteins
Analysis of High Abundance Proteins
The number of unique peptides identified is generally accepted as a semiquantitative measure of protein abundance [30, 31]. We sorted the 625 proteins in our dataset according to the number of unique peptides identified. The highest ranked 23 proteins represented by more than 10 unique peptides are listed [see Additional file 5]. Among the high abundance proteins, some members have already been well characterized in oocytes. For example, DNA methyltransferase 1 (Dnmt1), is the predominant form of DNA (cytosine-5-)-methyltransferase in mammals and is essential for embryo development . This protein was represented by 25 unique peptides and was the second-most abundant protein in our dataset.
Screening for Proteins with Special mRNA Expression Patterns
Unique or atypical mRNA expression patterns of maternal proteins suggest their key roles in oogenesis or early embryo development and this notion has been validated by other functional research on maternal effect proteins [7–11]. We adopted an in silico approach to investigate the expression patterns of proteins in our dataset by examining their expression in the mouse transcriptome database SymAtlas http://symatlas.gnf.org/SymAtlas/, which describes gene expression patterns in 45 mouse tissues . Surprisingly, many of the proteins in our dataset exhibited patterns worthy of note. We were particularly interested in genes highly expressed in oocytes and fertilized eggs (where expression was 10-fold higher than the corresponding median values). In total, 76 proteins, representing approximately 12% of the entire dataset, were included in this subset [see Additional file 5]. As expected, many well known maternal effect proteins in mice were found in this subset. Included in this subset were the earliest identified maternal protein MATER, as well as the recently identified TLE6 . In addition to these well-known maternal effect proteins, many of the proteins we identified as highly expressed in oocytes and fertilized eggs have not been characterized.
To explore the functions of the 76 proteins with abundant mRNA expression levels, we analyzed their domain composition with Babelomics. Statistical analysis indicated that the most significantly overrepresented domain was the F-box domain (Pfam: 6 proteins, p = 3.9E-05) and the 6 maternal proteins containing F-box domains are listed [see Additional file 5]. Different F-box proteins, as components of the Skp1-Cullin1-F-box (SCF) complex, can recruit particular substrates for ubiquitination and play central roles in cell-cycle regulation .
Intersection Between the Oocyte and ESC Proteome
Somatic cells can be reprogrammed by transferring their nuclear contents into oocytes  or by fusion with embryonic stem (ES) cells [36, 37]. This fact indicates that unfertilized eggs and ES cells probably contain similar factors that can confer totipotency or pluripotency to somatic cells. In order to identify a common set proteins shared between oocytes and ES cells, mouse MII oocyte proteins were compared with recently published data for proteins expressed in mouse ES cells . This analysis resulted in an overlap of 371 proteins [see Additional file 5]. As expected, developmental pluripotency associated 5 (DPPA5), which has been implicated in cell pluripotency, was included in this set. Of the 371 proteins, 108 (29%) were either exclusively found in mouse ES cells or highly enriched in ES cells compared to differentiated ES cells [see Additional file 5] . It is likely that novel factors associated with reprogramming are included in this subset.
Activation of the embryonic genome in mice begins late in one-cell zygote and is fully underway by the two-cell cleavage stage . The silencing of nuclear transcription occurring between meiotic maturation in oocytes and activation of the embryonic genome implies critical roles for preexisting stores of proteins and transcripts . Through knockout and knockdown strategies, individual maternal proteins have been demonstrated as essential for cleavage stage development in mice. In the present study, we identified many new and unknown maternal proteins in mice by constructing an MII oocyte proteome. In-depth analysis of these maternal proteins will assist us in screening for a proportion of great interest.
Interestingly, many maternal transcripts deposited in mammalian oocytes are not polyadenylated and therefore not translated into proteins . Independent confirmation of the protein expression of maternal genes is therefore necessary. This was also an important reason for us to construct the oocyte proteome. As a case in point, NALP14, NALP5 (MATER), and NALP4f were included in our subset of abundantly expressed maternal proteins. These three proteins belong to the multifunctional NACHT nucleoside triphosphatase (NTPase) family. NALP14 and NALP5 were previously reported as maternal effect proteins and play significant roles in mouse preimplantation embryo development [7, 41, 42]. NALP4f was represented by 14 unique peptides in our present study and a previous analysis demonstrated that NALP4f was an oocyte-specific gene . Our research has independently confirmed the high protein expression level of NALP4f in mature oocytes. Assuming that NALP4f has similar roles to NALP14 and NALP5, it is highly likely that NALP4f is an important factor necessary for normal embryogenesis and is a good candidate to be a maternal effect protein. In addition, we identified NALP2, NALP4b, and NALP9b in our oocyte proteome. Although the precise functions of NACHT NTPase family members remain to be determined, we speculate that these members play significant roles in early embryo development based on their homology to NALP14 and NALP5.A distinguishing characteristic of maternal effect proteins identified to date is that the majority of them have an abundant mRNA expression in oocytes and many are expressed only in oocytes [7–11]. This fact led us to filter maternal products in our protein list by analyzing their corresponding mRNA expression patterns. As a result, 76 maternal proteins with high mRNA expression levels in oocytes and fertilized eggs were selected out. Of these proteins, we discovered that 9 previously described maternal effect proteins (MATER, STELLA, DNMT1, ZAR1, NPM2, PADI6, TLE6, TCL1, FILIA) were enriched in this subset. These maternal effect proteins have been reported to be absolutely necessary for oogenesis, fertilization or early embryo development. Indeed, apart from these well-known examples, the majority of proteins in this subset have not been previously studied or reported in oocytes. We suggest that these proteins are excellent candidates as maternal effect proteins.
Domain composition analysis is an effective way to predict the functions of proteins identified in a proteomics analysis. Among 76 proteins singled out because their corresponding genes are highly expressed in oocytes, 6 proteins (FBXL10, FBXW14, FBXW16, FBXW19, EG382106, E330009P21Rik) contained an F-box domain, which was first described as a sequence motif in cyclin-F that interacts with the SKP1 protein. Different F-box proteins, as substrate-specific adaptor subunits of the Skp1-Cullin1-F-box (SCF) complexes, recruit particular substrates for ubiquitination via specific protein-protein interaction domains. Coincidentally, three core protein subunits (SKP1, RBX1, CUL1) of the SCF complex were all definitively identified in our proteome. As one of the major classes of ubiquitin ligases, the SCF complex plays a central role in cell-cycle regulation . In early stages of embryo development, degradation of maternal proteins is crucial for the oocyte-to-embryo transition . Our results suggest that the maternal SCF complex probably exists in oocytes and may be important for the oocyte-to-embryo transition by recruiting specific substrates for degradation.
Pluripotent stem cells are of considerable current interest as they can proliferate indefinitely in vitro and give rise to many adult cell types, serving as a potentially unlimited source for tissue replacement in regenerative medicine. Recently, Takahashi et al. demonstrated that pluripotent stem cells can be induced from mouse fibroblasts by retroviral introduction of Oct3/4, Sox2, c-Myc and Klf4 , indicating that the combination of these four factors can induce reprogramming of somatic cells to a pluripotent state. However, the use of retrovirus-transduced oncogenes represents a serious barrier to the eventual use of reprogrammed cells for therapeutic application because of tumor formation by c-myc reactivation . Therefore it is necessary to discover factors responsible for reprogramming that would be safer for therapeutic use. We compared the maternal proteins in our oocyte proteome with a recently published mouse ES cell proteome and identified an overlap of 371 proteins. In addition to some pluripotency markers, this group included many uncharacterized proteins, some of which may be good candidates for studying the mechanism of reprogramming. A good example is translationally-controlled tumor protein (Tpt1), which facilitates the first step of somatic cell reprogramming . Recent studies on Tpt1 demonstrate that this protein activates transcription of oct4 and nanog in transplanted somatic nuclei . We believe that further analysis of these candidate proteins at the functional level will uncover novel proteins that are essential for reprogramming and indirectly promote the application of therapeutic cloning.
In this study, we used 1D SDS-PAGE and RP-LC-MS/MS to investigate the maternal proteins stored in mature mouse oocytes. This high-performance strategy allowed us to define a set of 625 different mouse MII oocyte proteins. This is the largest catalog of mature mouse oocyte proteins compiled to date. We believe that this study will help us to understand the diverse biological processes occurring in mouse oocytes and during early embryo development. However, compared with proteomic analyses of other cells and tissues, such as embryonic stem cells and liver, the proteins identified in mature mouse oocytes were limited. This was mainly because of the fact that mature oocytes obtained from each mouse were very limited. We believe that the catalog of maternal proteins present in this article is a starting point and we anticipate that more research on the oocyte proteome will deduce most of the maternal proteins.
All experiments requiring the use of animals received prior approval from Nanjng Medical University and were performed according to USDA-approved protocols.
Urea (Cat. No. 17-1319-01), 3-[(3-Cholamidopropyl) dimethylammonio]-1-propanesulfonate (CHAPS) (Cat. No. 17-1314-01), iodoacetamide (Cat. No. RPN6302), and Dithiothreitol (DTT) (Cat. No.17-1318-02) were from GE Healthcare (Uppsala, Sweden); Thiourea (Cat. No. T7875), acetonitrile (ACN) (Cat. No. 34851), ammonium bicarbonate (NH4HCO3) (Cat. No. A6141), and trifluoracetic acid (TFA) (Cat. No. T0274) were from Sigma Chemical (St. Louis, MO); Protease inhibitor cocktail (Cat. No.78437) was purchased from Pierce Biotechnology (Rockford, IL).
Oocyte collection and protein extraction
Mature oocytes were obtained from ICR female mice weighing 25-30 g. The mice were superovulated by intraperitoneal injection of 10 IU pregnant mare serum gonadotropin followed by 10 IU human chorionic gonadotropin after 48 h. After 14-16 h, oocyte-cumulus cell complexes were collected from the ampulla of the oviduct, and the cumulus cells were removed by brief exposure to 1 mg/ml hyaluronidase (Sigma Chemical, St. Louis, MO, USA). Zona pellucidae (ZP) were removed by treating oocytes for a few seconds with acid Tyrode solution (pH 2.5) followed by mechanical shearing. During this process, oocyte morphology was monitored rigorously and the oocytes with shape abnormalities or with cytoplasmic abnormalities (dark cytoplasm, granular cytoplasm, and refractile body) were discarded. Only the denuded oocytes with normal morphology were selected for further investigation. ZP-free oocytes were washed 3 times in 0.01 M PBS, and stored in lysis buffer at -80°C until needed. The lysis buffer consisted of 7 M urea, 2 M thiourea, 4% (w/v) 3-[(3-cholamidopropyl)dimethylammonio]-1-propanesulfonate (CHAPS), 65 mM dithiothreitol (DTT), and 1% (v/v) protease inhibitor cocktail.
One-dimensional SDS-PAGE and in-gel digestion
In brief, proteins extracted from the 2700 MII oocytes were dissolved in SDS-PAGE loading buffer, boiled for 5 min, and loaded in a single lane on a 1-mm-thick 10% polyacrylamide gel. After separation, the gel was visualized by silver staining according to a published procedure , except that glutaraldehyde was omitted in the sensitizing solution. Thereafter, the gel was cut into 29 slices, and each slice was cut into 1-mm3 gel particles for in-gel digestion. In-gel digestion was performed as follows: gel particles were washed 3 times in deionized water and subsequently dehydrated with 100% acetonitrile (ACN) for 10 min. The particles were incubated with 10 mM DTT in 25 mM ammonium bicarbonate for 1 h at 56°C for protein reduction. The resulting free thiol (-SH) groups were subsequently alkylated by incubating the samples with 55 mM iodoacetamide in 25 mM ammonium bicarbonate for 45 min in the dark. Gels were washed with 25 mM ammonium bicarbonate and 50% ACN solution and dehydrated with 100% ACN sequentially. The gel pieces were rehydrated with 10 ng/μl trypsin (Promega, Madison, WI, USA) in 25 mM ammonium bicarbonate and incubated for 12 h at 37°C for protein digestion. Supernatants were transferred to fresh tubes, and the remaining peptides were extracted by incubating the gel pieces twice with 30% ACN in 3% trifluoroacetic acid (TFA), followed by dehydration with 100% ACN. The extracts were combined and lyophilized to dryness, and the resulting peptides were used for mass spectrometric analysis.
Online reverse-phase LC-MS/MS
For capillary reverse-phase LC (cLC) and mass spectrometric analysis, 29 fractions were sequentially loaded onto a Michrom peptide CapTrap (MW 0.5-50 kD, 0.5 × 2 mm; Michrom BioResources, Inc., Auburn, CA) at a flow rate of 50 μl/min with buffer A (see below). The trap column effluent was then transferred to a reverse-phase microcapillary column (0.1 × 150 mm, packed with Magic C18, 5 μm, 100 Å; Michrom Bioresources, Auburn, CA). The reverse-phase separation of peptides was performed using the following buffers: 5% ACN, 0.1% formic acid (buffer A) and 95% ACN, 0.1% formic acid (buffer B); a 56-min gradient (5-45% buffer B for 41 min, 90% buffer B for 5 min, and 5% buffer B for 10 min) was used. Peptide analysis was performed using Finnigan LTQ ORBitrap (ThermoFinnigan, San Jose, CA) coupled directly to an LC column. An MS survey scan was obtained for the m/z range 400-1800, and MS/MS spectra were acquired from the survey scan for the 10 most intense ions (as determined by Xcaliber mass spectrometer software in real time). Dynamic mass exclusion windows of 60 s were used, and siloxane (m/z 445.120025) was used as an internal standard.
Database search and bioinformatics
DTA files (Bioworks version 3.3) in ASCII format for each MS/MS spectrum with a minimum ion count of 8 were generated from the raw data for the peptide mass range of 400-8,000. The resulting spectra were independently searched against the International Protein Index Mouse database (ipi.MOUSE.v3.30, downloaded from http://ftp.ebi.ac.uk/pub/databases/IPI) containing 56450 entries by using SEQUEST analysis software (Bioworks version 3.3, ThermoFinnigan). Carbamidomethylation of cysteine was set as a fixed modification, and oxidized methionine was sought as a variable modification. The initial mass tolerances for protein identification on MS and MS/MS peaks were 10 ppm and 0.6 Da, respectively. Two missed cleavages were permitted. The criteria used for filtering peptides with low confidence scores were the following: cross-correlation values (Xcorr) greater than 2.0 and 2.5 were used for doubly charged ions and triply or higher charged ions, respectively; ΔCn values (difference in Xcorr with the next highest value) less than 0.1 were removed from the matched sequences. Singly charged ions were discarded because they were small in number. All output files were searched against the forward and reversed IPI mouse database separately, and FDR for all peptide-to-spectrum matches was calculated as FDR = # of False peptides/(# of True peptides + # of False peptides).
For bioinformatics analysis, each IPI accession number was converted to an Entrez Gene ID according to the IPI protein cross-references file downloaded from http://ftp.ebi.ac.uk/pub/databases/IPI. We used Babelomics to find statistically over- and underrepresented GO categories in our oocyte proteome dataset. To compare the mouse oocyte proteome with other mouse tissue proteomes, we generated a combined database for the mouse based on the following mouse tissues and cell cultures characterized by LC-MS/MS: mouse heart , liver [51–53], brain [51, 54], lung [51, 55], kidney , spleen , placenta, cortical neurons cell culture, sperm , islet alpha-cell culture . For enrichment analysis, our identified oocyte proteome was set as a test dataset and the combined mouse proteome was set as a reference. The enrichment analysis was done using 'fisher exact test', and all GO terms that were significant with adjusted P < 0.05 (after correcting for multiple term testing by using the FDR procedure of Bonferroni-Hochberg) were selected as overrepresented. An analysis of cellular processes influenced by the protein profile obtained was performed using PathwayStudio (v5.00) software (Ariadne Genomics, Inc., Rockville, MD). PathwayStudio includes an automated text-mining tool which enables the software to generate pathways from the PubMed database and other public sources. Each identified cellular process was confirmed through the PubMed/Medline hyperlink embedded in each node. The domain annotations were assigned using the Pfam database.
This study was supported by grants from 973 Program (No. 2006CB701503), NSFC (No. 90919014) and Program for Changjiang Scholars and Innovative Research Team in University (No. IRT0631).
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