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RESEARCH |
Monash Institute of Medical Research, Centre for Reproduction and Development, 27-31 Wright Street, Clayton, Victoria 3168, Australia
Correspondence should be addressed to N Borg; Email: neil.borg.2007{at}gmail.com
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Abstract |
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Introduction |
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HA is abundant in the uterine, oviductal and follicular fluids of murine (Sato et al. 1987), porcine (Archibong et al. 1989), bovine (Lee & Ax 1984) and human (Suchanek et al. 1994, Hamamah et al. 1996, Ohta et al. 2001) species. Furthermore, HA has been proposed to be an essential player of macaque spermatozoa capacitation and fertilisation (Cherr et al. 1999). CS has been identified in human (Hamamah et al. 1996) and porcine (Ax & Ryan 1979, Yanagishita et al. 1979) follicular fluid. Hydrolysation of rat granulosa cells with chondroitinase ABC revealed that CS is the major GAG of rat granulosa cells (Yanagishita & Hascall 1979).
The synthesis of HA occurs at the cell membrane by HA synthases (HAS; Watanabe & Yamaguchi 1996, Spicer et al. 1997b, Weigel et al. 1997). There are three isoenzymes that facilitate this process: HAS1 (Watanabe & Yamaguchi 1996), HAS2 (Salustri et al. 1989, 1992) and HAS3 (Spicer et al. 1997a). HAS1 protein has been identified in equine cumulus cells (Marchal et al. 2003). HAS2 mRNA transcripts have been detected in bovine oocyte–cumulus complexes (OCC; Schoenfelder & Einspanier 2003) and murine (Salustri et al. 1989, Fulop et al. 1997) and porcine cumulus cells (Kimura et al. 2002). mRNA transcripts for HAS3 are expressed in bovine OCC (Schoenfelder & Einspanier 2003) and porcine metaphase II (MII) oocytes (Kimura et al. 2002). Additionally, HAS3 protein has been identified in equine cumulus cells (Marchal et al. 2003).
There have been six glycosyltransferases identified that regulate the synthesis of CS (Sakai et al. 2007) within the Golgi apparatus (Silbert & Freilich 1980). These are CS synthase-1 (CSS-1; Kitagawa et al. 2001), CSS-2 (Yada et al. 2003a), CSS-3 (Yada et al. 2003b), CS N-acetylgalactosaminetransferase-1 (CSGalNAcT-1; Gotoh et al. 2002b, Uyama et al. 2002) and CSGalNAcT-2 (Sato et al. 2003) and CS glucuronyltransferase (CSGlcAT; Gotoh et al. 2002a). CSS have been reported to stimulate cumulus expansion and HAS activity in mice (Eppig 1981).
The primary receptor for HA is the cell surface glycoprotein CD44, which also functions as a receptor for CS (Culty et al. 1990). CD44 is thought to interact with HA via a highly conserved transmembrane region (Isacke 1994, Entwistle et al. 1996, Liu et al. 1998, Shi et al. 2001). This receptor has been identified on a wide range of cells that include epithelial cells (Alho & Underhill 1989), macrophages (Green et al. 1988a, 1988b) and lymphocytes (Lesley et al. 1993). The CD44 receptor has also been identified in bovine OCC (Schoenfelder & Einspanier 2003) and pre-implantation embryos (Furnus et al. 2003), porcine cumulus cells (Kimura et al. 2002, Yokoo et al. 2002a, 2002b, 2007), germinal vesicle-intact and MII oocytes and cleaved parthenotes (Toyokawa et al. 2005).
The use of extracellular HA and CS for in vitro maturation (IVM), in vitro culture (IVC) and in vitro fertilisation (IVF) media is documented in mammalian species, including canine (Kawakami et al. 2000), porcine (Kano et al. 1998), bovine (Lenz et al. 1983, Lee et al. 1986, Jang et al. 2003, Therien et al. 2005) and human (Eriksen et al. 1994, Hamamah et al. 1996) but not the rat. These studies reported significant influences on spermatozoa (increased motility and incidence of acrosome exocytosis), oocytes (elevated IVF rates) and pre-implantation embryos (improved rates of development in IVC) in GAG-supplemented media.
Here, we report on the ability of GAGs, HA and CS in a rat IVF system to improve overall fertilisation outcomes and potentially suppress spontaneous activation. Furthermore, we report on the expression of CD44 in Sprague–Dawley gametes and MII cumulus cells.
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Results |
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By 72 h, there were significantly fewer fragmented oocytes for mR1ECM+BSA supplemented with HA (Fig. 1D and E, 36–39%, P<0.0001) compared with the control (Fig. 1). Any positive effect of CS by this time had ended (Fig. 1B and C). Numbers of two-cell parthenotes were significantly higher in CS-500 (Fig. 1C, 20%; P<0.05) and higher for all GAG-supplemented media (Fig. 1B–E, 8–16%) compared with the control (Fig. 1A, 6%).
Spermatozoa motility
At the onset of co-incubation, all dishes were inspected to ensure that spermatozoa appeared healthy to the naked eye. CS-supplemented media contained greater numbers of visually motile caudal epididymal spermatozoa. While not as active, spermatozoa in all other media still presented a very healthy motility prior to insemination (Table 1).
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IVF of MII oocytes in GAG-supplemented medium
A control IVF experiment was run alongside IVF-GAG experiments to confirm normal oocyte and spermatozoa function (Table 2). All experiments were conducted with cumulus-intact oocytes as in previous IVF experiments. Thus, unlike the incubation experiments, MII oocytes were not denuded. The control outcomes observed were reasonably consistent with past laboratory experiments. EKRB (65.8%) and M16 (54.8%) had substantially higher numbers of fertilised embryos than mR1ECM+BSA (36.7%; Table 2).
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mRNA expression of the HA receptor CD44 in Sprague–Dawley gametes and cumulus cells
RT-PCR revealed a CD44 mRNA transcript present in cumulus cells collected from MII oocytes obtained from superovulated immature female rats (Fig. 2). The band obtained corresponded to the predicted amplicon size (1090 bp). Both MII oocytes and caudal epididymal spermatozoa showed no presence of the CD44 transcript. All samples were also probed with primers for adenyl cyclase III (ACIII) as a control gene to confirm that mRNA was obtained from the extraction procedure. The ACIII PCR product was present for all samples and the liver positive control (Fig. 2).
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50 kDa) present in both caudal epididymal spermatozoa and cumulus cells obtained from ovulated MII oocytes (Fig. 3). The presence of a CD44 protein in the sperm sample was contradictory to the RT-PCR result (Fig. 2) that did not detect an mRNA transcript. Faint signals were present in the liver controls.
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Discussion |
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After granulosa cell (GC) differentiation into mural GCs and oocyte-bound cumulus cells and the subsequent LH surge, expansion of cumulus cells is essential to the final stages of maturation (Dekel & Phillips 1979, Kimura et al. 2002, Yokoo et al. 2007). During this process of expansion, HA is actively synthesised and accumulates in the cumulus matrix (Dekel & Phillips 1979, Eppig 1979, Salustri et al. 1990). The ability of HA to suppress oocyte fragmentation has been observed in murine (Sato et al. 1987), bovine (Sato et al. 1988) and porcine (Sato et al. 1994) species. The incubation experiments in this study implicate a role for the CD44-HA signal pathway in oocyte maturation and/or maintenance prior to fertilisation. The ability of HA and CS to suppress oocyte fragmentation in vitro supports a role for HA within the extracellular matrix of cumulus cells.
IVF experiments in media supplemented with HA or CS did not improve fertilisation rates above those of controls, suggesting that there is a limit to their usefulness in vitro. Indeed, it seemed that the two GAGs promoted spontaneous activation of MII oocytes. Resumption of meiosis in MII oocytes is controlled by maturation promoting factor protein that acts to regulate MAP kinase (MAPK) via activation of an oocyte exclusive kinase. The active c-mos kinase promotes MAP kinase (MEK) phosphorylation of MAPK and its activation (Lu et al. 2002, Josefsberg et al. 2003).
CD44 has been observed to induce proliferation in colon cancer cells (Singh et al. 2006) and mouse thymoma EL4 cells via activation of MAPK (Marhaba et al. 2005). Furthermore, there is a large body of evidence to show that HA and CD44 are active in many signal pathways (Kobayashi et al. 2002, Roscic-Mrkic et al. 2003, Bourguignon et al. 2005, 2006, Lugli et al. 2006, Shi et al. 2006). The primer sequence (Kon et al. 2006) for CD44 in RT-PCR targeted the transcript for the whole protein. There are over 30 exons present in the entire CD44 sequence that through alternative mRNA splicing generates numerous isoforms (Screaton et al. 1992, Tolg et al. 1993, Bajorath 2000). There is a reasonable likelihood that one of these may be present in rat oocytes that could function to induce parthenogenesis in vitro due to extracellular HA or CS stimulation. This hypothesis would support the effect of HA and CS on rat MII oocytes and requires further investigation.
The CD44 protein detected in spermatozoa and cumulus cells was 50 kDa in mass. The apparent standard for CD44 is a protein in the range of 85–90 kDa (Lesley & Hyman 1998, Yokoo et al. 2002b). The amino acid sequence for CD44 predicts a band of 40 kDa, yet bands ranging from 73 to 88 kDa were detected in porcine cumulus cells (Yokoo et al. 2002b). The level of CD44 glycosylation is thought to be responsible for the apparent differences in mass (Borland et al. 1998).
The CD44 mRNA transcript was also absent in caudal epididymal spermatozoa yet immunoblotting detected the protein. It is probable that the CD44 protein is bound to spermatozoa during maturation as are other proteins (Cuasnicu et al. 1990, Cohen et al. 2000). Furthermore, in the presence of extracellular CS, sperm motility was greatly enhanced in human (Eriksen et al. 1994, Hamamah et al. 1996) and canine (Kawakami et al. 2000) spermatozoa motility. CD44 is a receptor for CS (Culty et al. 1990) which has been identified in human follicular fluid (Hamamah et al. 1996) and canine oviductal and uterine fluids (Kawakami et al. 2000). Additionally, CS is reported to be the primary GAG within rat granulosa cells (Yanagishita & Hascall 1979). The presence of CS within uterine or oviductal fluids or the OCC matrix may act to stimulate spermatozoa so that they can reach the zona pellucida.
In conclusion, CD44 is present in rat cumulus cells and caudal epididymal spermatozoa, suggesting roles in cumulus expansion, oocyte maturation and motility stimulation. The protein detected suggests a low level of glycosylation or a specific isoform. Further investigation is required to assess the mRNA transcripts for CD44 isoforms in MII oocytes and pre-implantation embryos. The identification of HAS is also required.
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Materials and Methods |
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Animals
Rats were obtained from the Monash University Central Animal Services (MUCAS, Clayton, Victoria, Australia) outbred Sprague–Dawley (OBSD) – specific pathogen-free (spf) colony. Rats were housed at the Block B animal house facility, Monash Medical Centre in standard rat sized boxes (one male per box, five females per box) with high top cage lids. Rats were kept under a standard 12 h light:12 h darkness cycle (0800:2000 h) and provided water and food ad libitum. The holding room temperature was maintained at 22 °C with an average humidity of 50%. This study was approved by the Monash Medical Centre Animal Ethics Committee.
Media
All media used in these experiments were made from a specific salt solutions with additional compounds added at different concentrations (Table 1). The rat-specific medium, modified rat 1-cell embryo culture medium, mR1ECM+BSA (Oh et al. 1998), was used for all MII oocyte incubations and as an IVF medium. In addition the media, namely enriched Krebs–Ringer bicarbonate (EKRB; Bendahmane et al. 2002) and M16 (Whittingham 1971) were used in IVF experiments. The osmolarity of all IVF media was set at 310 mOsm for all experiments.
Caudal epididymal spermatozoa collection and in vitro capacitation
Spermatozoa were obtained from the caudal epididymides of sexually mature (3–4 months old) OBSD males. Rat MII oocytes were fertilised following standard IVF methodology (Toyoda & Chang 1974) with some minor modification. The caudae were washed in pre-warmed calcium (Ca2+)/magnesium (Mg2+)-free Dulbecco's PBS (DPBS) and were immediately placed into standard mR1ECM+BSA, EKRB or M16 for 5 min to facilitate sperm dispersal. A sperm count was conducted to produce a working concentration of 7.5 x 105 spermatozoa per ml. Dishes were subsequently returned to the incubator for a 6-h incubation period to facilitate capacitation (37 °C, 5% CO2).
MII oocyte collection
MII-stage oocytes were obtained from sexually immature (24-days old) females superovulated with pregnant mare's serum gonadotrophin (10–15 i.u. i.p.) at 0 h and human chorionic gonadotrophin (hCG; 10–15 i.u.) at 48 h by i.p. injection. OCC were immediately transferred to dishes for specific experiments.
Denuding of MII oocytes
To prepare MII oocytes for incubation in GAG-supplemented mR1ECM+BSA, the surrounding cumulus matrix was removed. OCC were placed into HEPES-buffered mR1ECM+BSA supplemented with hyaluronidase (100 i.u./ml) for 5 min, after which the oocytes were washed in clean HEPES-buffered mR1ECM+BSA. Oocytes were subsequently transferred to mR1ECM+BSA with/without GAGs.
Incubation of MII oocytes in GAG-supplemented mR1ECM+BSA
Oocytes were placed into a 400 µl drop of pre-equilibrated mR1ECM-BSA (37 °C, 5% CO2). Standard mR1ECM+BSA was the control medium for incubation experiments. The mR1ECM+BSA was supplemented with HA or CS at 250 or 500 µg/ml. All dishes were placed into an incubator (37 °C, 5% CO2) for 72 h and their status checked every 24 h.
IVF of MII oocytes in GAG-supplemented media
OCC designated for IVF were immediately transferred to their respective insemination medium after collection. The insemination dish with spermatozoa (3.0x105 in 400 µl) and OCC present was returned to the incubator (37 °C, 5% CO2 in air) for an 11.5-h co-incubation period.
Primer sequence
To probe samples for CD44 mRNA transcripts, the forward (F) and reverse (R) sequences described by Kon et al. (2006) were used. These sequences would yield an amplicon 1095 bp in size:
To confirm the presence of mRNA during RT, adenyl cyclase III was selected to act as a control gene as its presence had previously been identified in rat caudal epididymal spermatozoa (Wade et al. 2003). Additionally, it was probable that this particular splice variant would be present in rat MII oocytes and liver. These sequences would yield an amplicon 290 bp in size:
mRNA isolation
The isolation of mRNA from caudal epididymal spermatozoa and MII oocytes was achieved with the Dynal Dynabead mRNA purification kit (Invitrogen). Oocytes were collected in 5 µl mRNA lysis buffer (485.5 µl DEPC water, 25 µl dithiothreitol (DTT), 4 µl IGEPAL (MP Biomedicals Inc., Melbourne, Australia) and 12.5 µl RNAseout (Invitrogen) and immediately snap frozen in liquid nitrogen (N2(l)) and stored at –80 °C until required. Spermatozoa was collected as described above on the day of RT-PCR and kept in DPBS for use.
The mRNA extracted from rat liver to act as a positive control was done by the Trizol (Invitrogen) method to the specifications of the manufacturer.
RT-PCR
RT of mRNA samples to produce cDNA was done in a RT solution; 19 µl Ultrapure DNase/RNase-free distilled water, 8 µl 5x buffer (Superscript III kit, Invitrogen), 2 µl random primers (1:10 dilution; Invitrogen), 2 µl of 10 mM dNTP (Fisher Biotech, Perth, Western Australia), 2 µl of 0.1 mM DTT (Superscript III kit, Invitrogen) and 2 µl RNAseout. Immediately prior to RT, 2 µl Superscript III was added to the sample. The rat liver control RT to act as a positive control was obtained by the Superscript II method to the specifications of the manufacturer.
PCR of samples was performed in a PCR solution; 33.8 µl DNase/RNase-free distilled water, 5 µl of 2 mM dNTP, 5 µl of 10x PCR buffer, 3 µl of 1.5 mM MgCl2, 1 µl forward primer (1:32.3 dilution), 1 µl reverse primer (1:32.3 dilution), 0.2 µl Taq polymerase (#TAQ-3,Fisher Biotech) and 1 µl sample cDNA.
Protein extraction
Spermatozoa were collected as described above in DPBS and the solution transferred to a Centricon YM-100 centrifugal filter device (Millipore, Melbourne, Australia) and the manufacturer's instructions were followed to remove salts and isolate spermatozoa. The spermatozoa pellet was transferred into 400 µl mammalian protein extraction reagent (M-PER; Pierce, Sydney, Australia) with 5 µl Calbiochem Protease Inhibitor Cocktail set III. The spermatozoa sample was constantly shaken for 4 h at RT.
MII oocytes were collected and denuded as described in Leibovitz L-15 tissue culture medium (Gibco, Invitrogen) supplemented with 1 mg/ml PVA. Rat liver was homogenised and protein extracted in the same manner as spermatozoa with M-PER, snap frozen in N2(l) and kept at –80 °C until required for electrophoresis.
Electrophoresis and electrotransfer
Protein samples were separated on a 12% bis-acrylamide gel in a Bio-Rad Mini-Protean 3 cell as specified by the manufacturer. To prepare samples for probing with a CD44 MAB (mAb), the 12% gel was prepared according to instructions for the Immobilon transfer polyvinylidene difluoride membrane (Millipore).
Western blot
Following electrotransfer of proteins, the membrane was blocked and blotted with mouse anti-ratCD44 mAb (PharMingen, BD Biosciences, Sydney, Australia) following the methods for the LI-COR Odyssey infrared imaging system. The primary antibody was used at a ratio of 1:500 in a Tris-buffered saline solution with 0.2% Tween-20.
Hoechst 33258 staining
To evaluate sperm penetration and pronuclei formation post-insemination, oocytes were fixed in 4%-paraformaldehyde for a minimum period of 12 h at 4 °C. Oocytes were subsequently transferred to 15 µg/ml bisbenzimide (Hoechst 33258) in DPBS for 15 min to permit labelling.
Statistical analysis
2 analysis was performed by comparing experimental groups with the control group for the numbers of fertilised and polyspermic embryos and unfertilised oocytes. A value of P
0.05 was considered to be statistically significant.
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Acknowledgements |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsAcknowledgementsReferences |
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Received 13 June 2007
First decision 6 September 2007
Revised manuscript received 16 October 2007
Accepted 31 October 2007
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References |
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