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RESEARCH |
1 Departments of Obstetrics and Gynecology, 2 Molecular and Integrative Physiology, 3 Urology and 4 Reproductive Sciences Program, University of Michigan, Ann Arbor, Michigan 48109-0617, USA
Correspondence should be addressed to G D Smith, 6428 Medical Sciences Building I, 1301 E. Catherine St, Ann Arbor, Michigan 48109-0617, USA; Email: smithgd{at}umich.edu
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Abstract |
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Introduction |
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Phosphorylation/dephosphorylation events are critical for resumption of meiosis (Bornslaeger et al. 1986). Specific phosphorylation events during meiosis are regulated, in part, by M-phase promoting factor (MPF) and/or mitogen activated protein kinase (MAP kinase) (Hashimoto & Kishimoto 1988, Naito & Toyoda 1991, Chesnel & Eppig 1995). Serine/threonine protein phosphatases (PPs) have also been implicated in regulating meiosis (Rime & Ozon 1990, Gavin et al. 1991, Schwartz & Schultz 1991, Hampl & Eppig 1995, Smith et al. 1998b). Okadaic acid stimulates GVB in starfish (Pondaven & Cohen 1987), Xenopus (Goris et al. 1989), mouse (Alexandre et al. 1991, Gavin et al. 1991, Schwartz & Schultz 1991), bovine (Levesque & Sirard 1995) and macaque (Smith et al. 1998b) oocytes. These reports using OA, either through microinjection or in culture, suggest that PP1 and/or PP2A are involved in the G2/M cell-cycle transition. Recently, it has been demonstrated that both PP1 and PP2A are present within mouse (Smith et al. 1998a) and monkey (Smith et al. 1998b) oocytes. In meiotically-competent germinal vesicle (GV)-intact oocytes PP1 is predominantly nuclear and appears to be the PP that regulates GVB, whereas PP2A is predominantly cytoplasmic (Smith et al. 1998a,b, Swain et al. 2003).
Protein phosphatase-1, but not PP2A, is sensitive to the heat- and acid-stable cytoplasmic inhibitors 1 and 2 (I1 and I2) (Cohen 1989). Inactivation of PP1 by I1 is dependent on I1 phosphorylation by protein kinase-A (PKA) (Nimmo & Cohen 1978), whereas I2 does not require phosphorylation for PP1 inhibition (Nimmo & Cohen 1978). Protein phosphatase-1 is activated by a reaction controlled by glycogen synthase kinase-3 (GSK-3) phosphorylation of I2 (Hemmings et al. 1982, Resink et al. 1983). Because PP1 has been detected in the nuclei of numerous cell types (Jessus et al. 1989, Ohkura et al. 1989), experiments have focused on identification of a nuclear PP1 inhibitor. Nuclear inhibitor of PP1 (NIPP-1) has been isolated, characterized and cloned from thymus and liver (Beullens et al. 1992, Jagiello et al. 1995, Van Eynde et al. 1995). In addition, PP1 activity in somatic cells can be inhibited by phosphorylation at Thr320 (Van Eynde et al. 1995). This phosphorylation and inactivation of PP1 is regulated by cyclin dependent kinase-1 (CDK1) (Dohadwala et al. 1994), which oscillates during mitotic cell cycle progression (Kwon et al. 1997). M-phase promoting factor (Mitra & Schultz 1996) and PP1 (Smith et al. 1998a,b) translocate into oocyte nuclei in accordance with acquisition of meiotic competence, and remain predominantly nuclear until GVB. Because MPF is composed of CDK1 and cyclin-B, it is possible that oocyte nuclear MPF regulates nuclear PP1 phosphorylation and activity, and that this mechanism may be important in regulating phosphorylation of nuclear proteins in association with GVB. Such an event has yet to be reported.
The objectives of the present study were to elucidate intra-oocyte mechanisms of PP1 regulation in relation to cellular events influenced by the PP1/PP2A inhibitor, OA. Experiments were conducted to determine differential intracellular localization of PP1 and to investigate the role of endogenous cytoplasmic and nuclear inhibitors of PP1 and MPF-regulated PP1 phosphorylation and inactivation during acquisition of OA-sensitive meiotic competence and resumption of meiosis.
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Materials and Methods |
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Immunohistochemistry (IHC)
Fixed, paraffin-embedded ovaries were sectioned at 5-micron intervals, placed on superfrost-plus slides (Fisher Scientific, Itasca, IL, USA), deparaffinized, placed in 100 mM glycine buffer (pH 3.65) and microwaved for 10 min for antigen retrieval (Shi et al. 1995). To reduce background signal, samples were placed in Tris-buffered saline (TBS; 50 mM Tris pH 7.6, 150 mM NaCl) containing 5.0% dimethyl sulfoxide and 0.2% Tween-20 for 10 min, rinsed in TBS and incubated for 10 min in TBS containing 0.3% BSA, 1 mg/ml sodium azide and 1.6% normal goat serum (Vector Laboratories, Burlingame, CA, USA). In addition, endogenous avidin and biotin were neutralized with an avidin/biotin blocking kit (Vector Laboratories). Slides were rinsed and incubated overnight with anti-PP1
antibody diluted 1:250 at room temperature in a humidified chamber. Slides were then rinsed, washed (TBS + 0.05% Tween-20) and incubated with the biotinylated secondary antibody for 30 min at room temperature. Following secondary antibody exposure, slides were quenched in 3.0% H2O2 in 90% methanol for 30 min, then rinsed and incubated for 30 min in avidinbiotin conjugated to peroxidase (Vector Laboratories). After several rinses, sections were exposed to 0.025% 3,3'-diaminobenzidine (Dojindo Labs-Wako Chemical, Richmond, VA, USA), rinsed, counterstained with Mayer’s hematoxylin (Sigma Chemical Co.), dehydrated by three changes of ethanol, then three changes of xylene, and mounted. Negative controls included (1) elimination of the primary antibody (not shown) and (2) non-immune rabbit serum in place of the primary antibody.
The ratios of PP1 nuclear-to-cytoplasmic staining intensity in GVB-incompetent and -competent oocytes were determined with a Leica DMR microscope (x 1000; Leica Microsystems Inc., Bannockburn, IL, USA), using image acquisition with a SPOT-RT digital camera (Diagnostic Instruments Inc., Sterling Heights, MI, USA) and subjected to computerized densitometry (Scion Image, Scion Corp., Frederick, MD, USA). Briefly, oocyte micrographs had hematoxylin staining digitally removed prior to conversion to gray-scale (Adobe Photograph, Adobe System Inc., Mountain View, CA, USA). Regions of interest containing 80–90% of either cytoplasm or nucleus were used to calculate mean pixel intensity of PP1 staining within the cytoplasm and nucleus. Differences in nuclear-to-cytoplasmic staining intensity ratios of PP1 in oocytes within ovaries isolated from 11-, 15- and 17-day-old mice were evaluated for statistical significance using Student’s unpaired t-test. Differences were considered statistically significant at P < 0.05.
Oocyte collection and meiosis
Fully grown GVB-competent oocytes were collected from eCG-treated (10 IU) 19- to 23-day-old CF-1 mice utilizing a protocol approved by the University of Michigan Committee on the Use and Care of Animals. Oocytes were collected by puncturing antral follicles in HEPES-buffered human tubal fluid medium (H-HTF; Irvine Scientific, Santa Ana, CA, USA) with 0.3% polyvinylpyrrolidone (PVP; Sigma Chemical Co.). Oocytes used for Western blot analysis or RT-PCR were completely freed of attached cumulus cells via repeated mouth pipetting before freezing in liquid nitrogen and storage at –80 °C. Cumulus-enclosed meiotic-competent oocytes were cultured in HTF + 0.3% BSA (control) or HTF containing 150 µM of the CDK1 inhibitor, roscovitine (ROSC; Tocris, Ballwin, MO, USA) without oil overlay for 2 h at 37 °C with 5% CO2. This dose of ROSC was chosen based on dose-titration experiments and it completely inhibits oocyte GVB in our studies. A subset of ROSC-treated oocytes was removed from culture after 2 h, washed extensively in H-HTF + 0.3% PVP and placed into HTF + 0.3% BSA for an additional 2 h. At the end of culture cumulus cells were removed, GVB was assessed with an inverted microscope with Hoffman optics at x 400, and oocytes were frozen in liquid nitrogen and stored at –80 °C until used for Western blot analysis.
Oocyte RNA isolation and RT-PCR
Eighty to one hundred oocytes were thawed in 20 IU RNa-sin (Promega, Madison, WI, USA), pooled and lysed with 5 freeze/thaw cycles in liquid nitrogen. Total RNA was isolated as previously described (Heikinheimo et al. 1995, Smith et al. 1998a). Complementary DNA was synthesized using the Superscript Preamplification System for First Strand cDNA Synthesis reagents and methodology (Gibco BRL, Gaithersburg, MD, USA). Oligo-dT was used to prime reverse transcription reactions. For I1, I2, and NIPP-1 PCR, sense and antisense primers were designed from areas with least homology between related cDNAs (i.e. I1 and I2) to amplify size-discernible products with distinct restriction endonuclease digestion sites (Table 1
). Each PCR was performed with five oocyte equivalents of cDNA, 20 pmoles of each primer, and a PCR cocktail (0.4 mM of each dNTP, 2.0 mM MgCl2, 10.0 mM Tris–HCl (pH 8.3), 50.0 mM KCl and 2 IU Taq DNA polymerase (Perkin-Elmer, Foster City, CA, USA)). In addition, control reactions were conducted consisting of (1) no template with primers and cocktail; (2) no primers with cDNA template and cocktail; (3) no template or primer with cocktail and (4) total RNA as template (equivalent to 5 oocytes) with primers and cocktail. Total RNA controls were only performed if amplification signals were previously identified in oocytes. Polymerase chain reactions entailed 1 cycle for 2 min at 94 °C; 35 cycles at 94 °C for 1 min, 55 °C (NIPP-1), 57 °C (I1) and 58 °C (I2) for 1 min, 72 °C for 1 min and 1 cycle at 72 °C for 2 min.
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PP1 cytoplasmic inhibitor assay
In order to determine the presence of I1 and/or I2 at the protein level, human sperm, mouse brain and approximately 200 meiotic-incompetent and -competent oocytes were used to prepare heat-stable extracts as previously described (Smith et al. 1996). Pooled human sperm sonicates were prepared and used as the PP1 source in this assay (Smith et al. 1996, Vijayaraghavan et al. 1996). Boiled extracts (inhibitor source) and a PP1 source were incubated in duplicate for 10 min at 30 °C before a standard PP assay was performed using 32P-phosphorylase-a as the PP substrate (Gibco BRL) (Smith et al. 1996). After incubation with 32P-phosphorylase-a, reactions were terminated with the addition of ice-cold 20% trichloroacetic acid (TCA) on ice for 10 min; samples were centrifuged and supernatants were evaluated for 32P release in response to the PP source with or without previous inhibitor source exposure. To identify the PP inhibitor (I1 or I2) present in mouse oocytes, heat stable sonicates were incubated in duplicate with 10 µm ATP (Sigma Chemical Co.) with or without 1–2 mU PKA (Sigma Chemical Co.) for 10 min at 30 °C. Reactions were terminated in a 100 °C water bath for 10 min and cooled at 30 °C. The protein phosphatase source was added before the PP assay was conducted. Positive control reactions for the assay of specific inhibitors utilized boiled extracts prepared from mouse brain (I1 and I2) (Endo et al. 1996, Kawai et al. 2001) and human sperm (I2) (Smith et al. 1996). Experiments were performed in duplicate.
Electrophoresis and Western blot analysis
Two hundred frozen cumulus cell-free fully grown GV-intact and GVB oocytes were thawed in pre-warmed 2 x SDS PAGE sample loading buffer (80 mM Tris–HCl (pH = 6.8), 20% glycerol, 4% SDS, 4% ß-mercaptoethanol, 0.04% bromophenol blue), vortexed and placed on ice for 15 min. Following sonication on ice, samples were denatured at 90 °C for 10 min and cooled on ice for 5 min. Total protein from two hundred mouse oocytes was added per lane and separated by one-dimensional SDS-PAGE (Laemmli 1970). Approximately 5 µg of rat and mouse liver protein were loaded per lane as positive controls for detecting NIPP-1. HeLa cell lysate was used as a positive control for recognizing PP1 and phospho-Thr320-PP1. Gels were equilibrated and transferred to Hybond-P PVDF transfer membrane (Amersham Life Sciences, UK) by Semi-Dry Electrophoretic Transfer (Bio-Rad Laboratories, Hercules, CA, USA) according to the manufacturer’s instructions. After blocking, blots were incubated with either anti-NIPP-1 antibody (diluted 1:5000; kindly provided by Dr Bollen), or anti-phospho-Thr320-PP1 (diluted 1:1000; Cell Signaling Technology Inc., Beverly, MA, USA) antibody in TBST (25 mM Tris pH 7.6, 125 mM NaCl, 0.1% Tween-20) plus 5% nonfat milk overnight at 4 °C with agitation. Blots were washed in TBST, incubated with anti-rabbit horseradish peroxidase-conjugated IgG (diluted 1:10 000) at room temperature for 1 h, washed again in TBST and developed with ECL Plus reagents (Amersham Life Sciences) according to the manufacturer’s instructions. After phospho-Thr320-PP1 assessment, blots were stripped for 30 min at 50 °C in a water bath with agitation using a stripping buffer (62.5 mM Tris–HCl (pH 6.7), 100 mM ß-mercaptoethanol and 2% SDS). Completely stripped blots were blocked in 5% nonfat milk in TBST for 1 h at room temperature, then incubated with anti-PP1 antibody (diluted 1:1000; kindly provided by Dr Angus Nairn, Rockefeller University) overnight at 4 °C with agitation, and processed further as described above.
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). On day 11, oocytes contained in secondary/preantral follicles had a nuclear-to-cytoplasmic staining intensity ratio of 1.1±0.1 (arbitrary units, mean±S.E.; Fig. 1B). At 15 and 17 days of age oocytes began to display intense nuclear PP1 staining in accordance with approximately 10% and 60% acquisition of meiotic competence, respectively (Fig. 1A). On day 15, oocytes within follicles had a nuclear-to-cytoplasmic staining intensity ratio of 2.2±0.1 (arbitrary units, mean±S.E.; Fig. 1B). On day 17, oocytes within follicles had a nuclear-to-cytoplasmic staining intensity ratio of 1.85±0.1 (arbitrary units, mean±S.E.; Fig. 1B). Oocyte PP1 nuclear-to-cytoplasmic staining intensities on days 15 and 17 of age were significantly greater than on day 11 of age (P < 0.01).
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, lane F and G). Using the same primers, with fully grown GV-intact mouse oocyte mRNA as a template, RT-PCR experiments revealed that oocytes do not contain the I1 transcript (Fig. 2A, lane E). A similar approach was employed to assess oocytes for the presence of I2 mRNA. The fully grown mouse oocyte cDNA produced by RT-PCR with primers specific for I2 yielded a 330 bp product (Fig. 2B, lane F) that contained an anticipated HindIII digestion site (Fig. 2B, lane G). Control PCR showed no reaction contamination. The sequenced mouse oocyte PCR product was identical to mouse liver I2.
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). Co-incubation with PKA did not influence the inhibitor potential of boiled human sperm extracts. This is in agreement with our previous identification and characterization of I2 in human, monkey and bovine sperm (Smith et al. 1996, Vijayaraghavan et al. 1996). Incubation of boiled mouse brain extract with the PP source resulted in a PP activity that was 85% of the control activity. When PKA was co-incubated with boiled mouse brain extract a fourfold increase in the inhibitory potential of this extract was observed. These controls, human sperm containing I2 and mouse brain containing I1 and I2, performed as expected in validation of the assay’s ability to identify heat-stable PP1 inhibitors and to differentiate between I1 and I2 activity. Both meiotic-incompetent and -competent mouse oocytes contain PP1 cytoplasmic inhibitor activity (Fig. 3). In the absence of PKA, boiled meiotic-incompetent and -competent oocyte extracts resulted in PP activity that was 81% and 74% of control activity respectively. Co-incubation of either meiotic-incompetent or -competent extracts with PKA did not alter their inhibitory activity. Thus, the biological properties of the meiotic-incompetent and -competent mouse oocyte PP cytoplasmic inhibitor resemble those of I2.
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, lane F). This RT-PCR product also contained the anticipated single BamHI site, that when cut yielded 331 and 71 bp products (Fig. 4A, lane G). As assessed by RT-PCR, mouse meiotic-competent oocytes did not contain mRNA for NIPP-1 (Fig. 4A, lane E). No amplification signals were detected in control reactions (Fig. 4A, lanes A-D). Western blots were performed with an antibody that previously had been described to recognize calf thymus NIPP-1a and NIPP-1b at 18 and 16 kDa, respectively (Beullens et al. 1992). In rat liver extracts, the major band recognized by the anti-NIPP-1 antibody corresponded to approximately 19 kDa. This immunogenically identified protein from rat liver matched the reported molecular mass of the purified 19 kDa PP1 inhibitory protein, which is believed to represent the rat liver homolog of calf thymus NIPP-1 (Zhao et al. 1996). In addition, this antibody also identified a similar protein band from mouse liver. However, protein extracts from fully grown GV-intact oocytes were devoid of NIPP-1 (Fig. 4B). Thus, fully grown mouse oocytes do not contain NIPP-1 transcript or protein.
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). This inhibitory effect of ROSC was reversible since 86.7% (n = 230) of ROSC-treated oocytes underwent GVB within 2 h following ROSC removal (Fig. 5A).
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. Protein phosphatase-1 was expressed at comparable levels in mouse oocytes at different developmental stages and under different treatments (Fig. 5B, top panel). Germinal vesicle-intact oocytes did not contain Thr320-phospho-PP1, while GVB oocytes did contain the phosphorylated protein. Blocking GVB with ROSC eliminated phosphorylation of PP1. If GV-intact oocytes were treated with ROSC for 2 h, washed extensively, and cultured for an additional 2 h, 87% of oocytes underwent GVB, and GVB oocytes contained phospho-Thr320-PP1 (Fig. 5B, bottom panel). |
Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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The presence of both PP1 and PP2A within mammalian oocyte cytoplasm raises questions about the functional importance of this intraoocyte location and the methods of PP1/PP2A activity regulation. Of particular importance are differential methods of regulating oocyte cytoplasmic PP1 or PP2A. One such pathway involves the heat- and acid-stable inhibitors, I1 and I2. Currently no reports suggest the presence or absence of I1 in mammalian oocytes. Lack of I1 mRNA within fully grown oocytes, in conjunction with the inability to identify I1-like activity in germinal vesicle breakdown-incompetent and –competent oocytes indicate the absence of I1 in mouse oocytes. Presently, the only methods of assessing presence or absence of I1 protein are by chromatography purification and/or differential heat-stable PP1 inhibitor assays. Lack of an I1 specific antibody prevents immunodetection. The heat-stable PP1 inhibitor assay we have employed is commonly used to differentiate between I1 and I2 within cell and tissue extracts (Cohen 1978, Pondaven & Cohen 1987, Vijayaraghavan et al. 1996, Smith et al. 1996). Absence of I1 in mouse oocytes is in agreement with the report that starfish oocytes do not contain I1 (Pondaven & Cohen 1987).
Starfish oocytes contain a heat-stable PP1 inhibitor with characteristics similar to I2 (Pondaven & Cohen 1987). Here, we demonstrate that mouse oocytes also contain I2 as indicated by RT-PCR, cycle sequencing and inhibitor activity assay. As in starfish oocytes, the heat-stable inhibitor in mouse oocytes did not respond to preincubation with MgATP and PKA with respect to PP1 inhibitory activity, indicating that the heat-stable inhibitor is I2. Characteristics of the mouse oocyte heat-stable PP1 inhibitor are the same for both meiotic-incompetent and -competent oocytes. A recent report indicates that I2 translocates from cytoplasm to nuclei of HeLa and PC3 cells (Leach et al. 2002). This raises the possibility that I2 not only controls cytoplasmic PP1 activity, possibly in association with condensing chromatin, but also controls nuclear PP1 activity in the regulation of nuclear lamin phosphorylation and GVB. Additionally, because I2 requires no activation to inhibit PP1 these data would suggest that oocyte PP1 is susceptible to I2 inhibition and that levels of I2, or the state of I2 phosphorylation, may be important determinants of overall oocyte PP1 activity. It is useful to remember that when I2 is phosphorylated by GSK-3, PP1 activity is restored. We have recently demonstrated that mouse oocytes also contain GSK-3 (Wang et al. 2003). Whether GSK-3 and/or I2 activity change with respect to meiotic progression remains to be investigated. In addition, the possible role of this oocyte-derived PP1/I2 system in fertilization and early embryo development warrants future attention.
During mitosis, PP1 phosphorylation at Thr320 is associated with inhibition of PP1 activity (Dohadwala et al. 1994). In somatic cells PP1 becomes phosphorylated by CDK1 at the M2/G transition (Dohadwala et al. 1994, Kwon et al. 1997). Because inhibition of PP1 with exogenous means (such as OA administration) stimulates GVB, we surmised that an endogenous mechanism of inhibiting PP1 may be linked to GVB. At or around the time of GVB, PP1 becomes phosphorylated at Thr320. This PP1 phosphorylation is regulated by the CDK1 activity of MPF. Whether CDK1 directly phosphorylates the Thr320 residue and what proportion of oocyte PP1 becomes phosphorylated is not known at this time. This PP1 phosphorylation is not a time-dependent event in relation to removal of the oocyte from the follicle, but is dependent on MPF activity. These data also open up a new avenue of investigation involving MPF, PP1 and other nuclear proteins in the regulation of nuclear envelope integrity, breakdown, and reformation during oocyte meiosis.
In conclusion, differential intra-oocyte localization of PP1 to the nucleus when oocytes begin to gain meiotic competence suggests its importance in the regulation of meiotic competence acquisition, nuclear events during meiotic arrest, and GVB. In conjunction with GVB, PP1 becomes phosphorylated at Thr320, which is known to inhibit PP1 activity. This phosphorylation of oocyte PP1 is regulated by CDK1 activity of MPF. These studies have provided a link between MPF and PP1 at a developmental time-point when both these enzymes appear to be important in regulating oocyte GVB.
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Footnotes |
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X-T Liu is now at Department of Pediatrics/Division of Neonatal-Perinatal Medicine, UT Southwestern Med CTT, 5323 Harry Hine Blvd, Dallas, Texas 75235-7216, USA
Received 14 January 2004
First decision 1 April 2004
Revised manuscript received 23 June 2004
Accepted 5 July 2004
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References |
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  J. E. Swain, J. Ding, D. L. Brautigan, E. Villa-Moruzzi, and G. D. Smith Proper Chromatin Condensation and Maintenance of Histone H3 Phosphorylation During Mouse Oocyte Meiosis Requires Protein Phosphatase Activity Biol Reprod, April 1, 2007; 76(4): 628 - 638. [Abstract] [Full Text] [PDF]
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 A. Mishra and K. P. Joy 2-hydroxyestradiol-17{beta}-induced oocyte maturation: involvement of cAMP-protein kinase A and okadaic acid-sensitive protein phosphatases, and their interplay in oocyte maturation in the catfish Heteropneustes fossilis J. Exp. Biol., July 1, 2006; 209(13): 2567 - 2575. [Abstract] [Full Text] [PDF]
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