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1 Department of Obstetrics and Gynecology,
2 Division of Blood Purification, School of Medicine, Kanazawa University, 13-1 Takara-machi, Kanazawa, Ishikawa, 920-0934 Japan,
3 Department of Physiological Chemistry and Metabolism,
4 Molecular Preventive Medicine, Graduate School of Medicine, University of Tokyo, 7-3–1 Hongo, Bunkyo-ku, Tokyo, 113-0033 Japan and
5 Center for the Development of Molecular Target Drugs, Cancer Research Institute, Kanazawa University, 13-1 Takara-machi, Kanazawa, Ishikawa, 920-0934 Japan
(Requests for offprints should be addressed to K Kuno; Email: kkuno{at}kenroku.kanazawa-u.ac.jp)
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Abstract |
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 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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As a metalloproteinase associated with the extracellular matrix (ECM) (Kuno & Matsushima 1998, Kuno et al. 1999), ADAMTS-1 cleaves aggrecan and versican (Kuno et al. 2000, Sandy et al. 2001, Rodriguez-Manzaneque et al. 2002). ADAMTS-1 also possesses anti-angiogenic activity (Vazquez et al. 1999, Luque et al. 2003) and ADAMTS-1 or its C-terminal half region suppresses tumor growth and experimental metastatic potential (Iruela-Arispe et al. 2003, Kuno et al. 2004).
The physiological functions of ADAMTS-1 have been investigated using gene knockout mice produced in our laboratories (Shindo et al. 2000). ADAMTS-1 null mice display renal anomalies involving enlarged calices and atrophic renal papillae, which resemble ureteropelvic junction (UPJ) obstruction in humans (Shindo et al. 2000). This finding indicates that ADAMTS-1 plays an important role in tissue architecture and function in ureteropelvic junction tissue.
We demonstrated that the second major phenotype of ADAMTS-1 null mice is female infertility featuring a markedly low delivery rate and number of pups, indicating that ADAMTS-1 is important in the function of female reproductive organs (Shindo et al. 2000). Decreased number of implantation sites was also reported in ADAMTS-1 null mice (Shindo et al. 2000, Mittaz et al. 2004). ADAMTS-1 mRNA expression is induced in the granulosa cells of the preovulatory follicles after administration of luteinizing hormone (LH) (Espey et al. 2000, Robker et al. 2000, Boerboom et al. 2003), and is sustained in a progesterone-dependent manner (Robker et al. 2000). The ADAMTS-1 protein increases after an LH surge and is localized in the cumulus-oocyte complex (COC) of the preovulatory follicles (Russell et al. 2003). Recently, Mittaz et al.(2004) reported that ADAMTS-1 null mice trap mature oocytes in ovarian follicles, suggesting that ADAMTS-1 is required for normal ovulation.
In the present study, we conducted a detailed examination of the ovarian morphology of ADAMTS-1 null female mice and showed that impairment of ovulation function in ADAMTS-1 null mice can be attributed not only to the to the ovulatory process of mature follicles but also to changes in the growth process of immature follicles.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Pregnant mare serum gonadotropin (PMSG) and human chorionic gonadotropin (hCG) were purchased from Teikokuzouki Pharmaceutical Co., (Tokyo, Japan)
Animals and hormone treatment
ADAMTS-1 null mice were generated as described previously (Shindo et al. 2000). Littermates obtained by mating heterozygous females (+/–) with homozygous males (–/–) with the genetic background of the 129/Sv x C57BL/6 hybrid were used for phenotypic analysis. Animal experiments complied with the standards stipulated by the Takara-machi Campus of Kanazawa University and adhered to the principles of the UFAW Handbook on the Care and Management of Laboratory Animals, 7th edition.
Measurement of ovulated oocytes
Female mice at 24–26 days old were injected i.p. with 7.5 IU of PMSG followed by 7.5 IU of hCG i.p. 48 h later. Oviducts and ovaries were excised from mice 15 h after hCG administration and were placed into dishes containing PBS. COC was recovered by dissection of both the ampulla and the oviduct, and under a dissecting microscope, the number of ovulated oocytes was determined after treatment with 500 units/ml hyaluronidase (Sigma).
Histological studies and statistical analyses
Excised ovarian tissues were fixed in 10% neutral buffered formalin (Wako Pure Chemical, Osaka, Japan) as described previously (Lydon et al. 1995). After the requisite fixation time, ovaries were trimmed, dehydrated with ethanol, cleared in xylene, and infiltrated with paraffin wax.
For analysis of the number of ovarian follicles, each paraffin-embedded ovary was placed with the ovarian hilum at the side and serially sectioned parallel to its longitudinal plane at 2.5 µm using a microtome. Every sixth section was mounted and stained with hematoxylin and eosin. Serial sections of ovaries were photographed and printed at x100 magnification, which enabled clear discrimination of each growing follicle. Each follicle was then numbered on the serial photographs and counted only once when the oocyte was seen. Classification and nomination of ovarian follicles were based on Pederson & Peters (1968). Follicles at the preantral stage were deemed atretic if the oocyte was degenerating (convoluted and condensed or fragmented) (Morita et al. 1999).
Area of medullar zone of each ovary was determined on digital microscopic images of the serial sections using MacSCOPE software (Mitani Co., Fukui, Japan). The medullar zone was defined expediently as the internal area of the ovarian cortex which consists of follicles and surrounding ovarian stroma. The section with the largest medullary area among the serial sections (defined as the central plane) was used as the representative section for comparison. The blood vessel area in the medullary zone was also measured on the central plane using MacSCOPE.
The Mann–Whitney test was used for statistical evaluation and P < 0.05 was considered to be statistically significant. Fisher’s direct probability test was used for statistical evaluations of frequency of unruptured follicles showing COC expansion and frequency of large follicles having two vascular plexus layers.
Immunohistochemical analyses
Cryostat sections of ovary tissue were stained with anti-mouse CD31 monoclonal antibody (Becton-Dickinson, Sunnyvale, CA, USA) with the aid of a HISTOFINE system (Nichirei Co., Tokyo, Japan) as described previously (Kuno et al. 2004).
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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In order to evaluate the total ovarian function of ADAMTS-1 null mice, we first examined the ovulation of oocytes in response to exogenous gonadotropins. Immature mice were used for the study because they ovulate solely in response to exogenous gonadotropins, by which the super-ovulation scheme was applied. We confirmed that ADAMTS-1 +/– females were as fertile as +/+ mice (data not shown), and thus ADAMTS-1 +/– female mice were used as controls for assessment of ovarian function. After treatment with PMSG followed by hCG, ovulated oocytes in the oviduct were collected and counted. As shown in Fig. 1
, ovaries of the ADAMTS-1 null females ovulated one ninth the number of oocytes as control mice. These data suggest that the total ovarian function of ADAMTS-1 null female mice is impaired.
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To examine whether ADAMTS-1 is involved in the maturation process of follicles, we first compared the number of total mature follicles in immature mice after PMSG/hCG treatment. The numbers of corpus luteum (CL), unruptured follicles (UF, mature follicles that have not undergone ovulation), and luteinized unruputred follicles (LUF, luteinized follicles that trap oocyte inside) per ovary were separately counted for each ovary and the sum of these was defined as the number of total mature follicles (Table 1). As shown in Fig. 2A, the number of total mature follicles in the ovaries of ADAMTS-1 null mice was one-third lower than that of control mice, suggesting that follicular maturation is significantly impaired in ADAMTS-1 knockout mice.
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), during (PMSG alone, Fig. 2C) and after PMSG/hCG treatment (Fig. 2D). The results were similar at these time points. The number of type 5b follicles (late preantral follicles with more than four layer of granulosa cells) and higher stage follicles were decreased in ADAMTS-1 null mice, whereas the number of the earlier type 4 follicles (small preantral follicles with only two layers of granulosa cells) were increased in ADAMTS null mice, although the difference was not sufficient to reach significance in mice treated with PMSG alone. For type 5a follicles (small preantral follicles with three layers of granulosa cells), the difference was barely significant in mice treated with PMSG alone (Fig. 2C). These results demonstrate that follicular development is significantly impaired at type 5b and thereafter in pre-pubertal ADAMTS-1 null mice, independent of the exogenous gonadotropin environment. The increases in early-stage follicles (type 4) may be attributable to impairment of follicular growth from the type 4 stage to advanced stages. PMSG-induced follicular growth may explain the relative decrease in the number of type 4 follicles observed in mice treated with PMSG alone (Fig. 2C). Reduction in general atretic pathways in ADAMTS-1 null mice
To examine whether follicular atresia explains the decreased number of growing follicles, we analyzed changes in atretic follicles in ADAMTS-1 null ovaries. As shown in Fig. 3B and C, the number of atretic follicles from preantral follicles (types 4, 5a, and 5b) was markedly lower in ADAMTS-1 null mice treated with PMSG or PMSG/hCG than in control mice. Similarly, under the unstimulated condition, a significant reduction in the number of atretic follicles derived from preantral follicles was observed in ADAMTS-1 null ovaries (Fig. 3A). These data do not support the notion that enhanced atresia causes the reduction in healthy follicles in ADAMTS-1 null ovaries.
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Further detailed analysis of ovarian histology revealed that a number of unusual follicles without cytoplasmic fragmentation and not surrounded by layers of normal-looking granulosa cells appeared in unstimulated ADAMTS-1 null ovaries, while such unusual follicles were rarely seen in the controls (Fig. 4A and C). These were not classified as atretic follicles based on the criteria that we used in this study because there were no apparent fragmentation of oocytes, a sign of authentic follicular atresia. These unusual follicles were clearly delineated from usual atresia observed in control ovaries (Fig.4A and B). The number of these unusual follicles in ADAMTS-1 null mice was not dependent on exogenous gonadotropin stimulation (Fig. 4C). These unusual oocytes were larger than oocytes of healthy type 3 follicles, and approximately equivalent in size to oocytes of type 4 follicles (Fig. 4A). Therefore, such unusual follicles might be formed from follicles at type 4 or later preantral stages by losing their granulosa cell layers in ADAMTS-1 null ovaries. ADAMTS-1 may be required for maintenance of follicle structure at the preantral stages.
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The role of ADAMTS-1 in the ovulatory process was evaluated by determining the proportion of total anovulatory follicles (UF+LUF) as a percentage of the total mature follicles (UF+LUF+CL). As seen in Fig. 5A, the percentage of anovulatory follicles significantly increased in ADAMTS-1 null mice treated with PMSG /hCG when compared with control mice, indicating that ovulatory ability is significantly compromised in ADAMTS-1 null females. The increase in the anovulatory follicle rate in ADAMTS-1 null mice was attributable to an increase in UF but in LUF (Fig. 5B and C). In 20 of 22 UFs found in ADAMTS-1 null ovaries, the cumulus cells had already expanded around the oocytes (Fig. 6B, D and E), thus suggesting that COC expansion is not affected. In this respect, UF in ADAMTS-1 null mice resemble preovulatory follicles, except for degeneration of the oocyte and the zona pellucida (Fig. 6B and D). In addition, partial luteinizing changes were sporadically observed in the granulosa layer in UF in ADAMTS-1 null ovaries (Fig. 6F) and UF in ADAMTS-1 null mice often retained the thick theca layer despite hCG treatment (Fig. 6E). These findings indicate that thinning and rupture of the follicle wall are compromised in ADAMTS-1 null mice and that luteinization, albeit incomplete, proceeded in the resultant follicles.
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Alteration of ovarian blood vessels in ADAMTS-1 null mice was examined by immunohistochemical staining with anti-CD31 antibody. In preantral (type 5b) and small antral follicles (type 6), a single-layer capillary network was observed in the theca layer in ADAMTS-1 null ovaries (Fig. 7B and D), as in control mice (Fig. 7A and C). In contrast, the vasculature of large follicles in ADAMTS-1 null mice was somewhat different from that in control mice. Large follicles in ADAMTS-1 null ovaries often had additional layers of capillary network outside the capillary plexus in the theca layer (Fig. 7G and H), while most large follicles in control mice had only a single capillary layer (Fig. 7E). In ADAMTS-1 null ovaries, 10 of 18 large follicles had two layers of vascular plexus, while in control ovaries, this number was 3 of 28, P < 0.01.
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). Under super-ovulatory conditions, various sizes of blood vessels, including a number of large blood vessels (50–150 µm in diameter), were formed in the medullar zone of control ovaries (Fig. 8A and C). Large blood vessels (more than 50 µm in diameter) were very few in ovaries of unstimulated control mice, and formation of large blood vessels was induced by administration of gonadotropins in control ovaries (Fig. 8F). In contrast, ADAMTS-1 null ovaries had a small medullar zone (Fig. 8B and E). Formation of large blood vessels of the medullary zone in the presence of gonadotropins (PMSG or PMSG/hCG) was significantly impaired in ADAMTS-1 null mice although smaller vessels were present (Fig. 8B, D, and F). These observations demonstrate that the vascular network of the ovarian medulla is dysplastic or disorganized in ADAMTS-1 null mice.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Ovarian folliculogenesis starts with the recruitment of nongrowing primordial follicles in the perinatal stage, and proceeds through the primary follicle, preantral, and antral stages (Matzuk et al. 2002), under the influence of various factors including FSH, estrogen and growth factors such as c-kit and GDF-9 (Dong et al. 1996, Dierich et al. 1998, Couse et al. 1999, Donovan & de Miguel 2001, Matzuk et al. 2002). This study demonstrated that ADAMTS-1 is also required for complete folliculogenesis. In ADAMTS-1 null mice, the number of type 4 follicles was increased when compared with controls, whereas the number of type 5 b follicles and later stages were decreased. Instead of healthy preantral follicles at type 5b or later, unusual follicles containing enlarged oocytes without fragmentation and losing normal granulosa cells, probably originating from an unusual atretic process in type 4 or 5 follicles, were elevated in the ADAMTS-1 ovaries. Atresia was not accelerated in preantral follicles. These findings are compatible with the notion that ADAMTS-1 is important for follicles to autonomously develop beyond the type 4 or 5a into the next stage and that abrogation of ADAMTS-1 leads to formation of unusual atretic follicles without granulosa cell layers. Granulosa cells rapidly proliferate from the preantral follicle stage (type 4 and 5a), and the ECM in the granulosa cell layer must be reconstituted during follicular development. Thus, ADAMTS-1 may be involved in folliculogenesis as well as the maintenance of follicular structure by participating in the remodeling of the ECM surrounding the granulosa cells of growing follicles.
Ovulation initiated by the LH surge consists of several sequential events involving enlargement of the antrum, expansion of the COC, degradation of the follicle and ovarian wall at the apex of the mature follicles, and release of the COC (Tsafriri et al. 1996, Murdoch 2000, Richards et al. 2002). We found that the proportion of anovulatory follicles, specifically of UF to total mature follicles, was significantly higher in the ovaries of ADAMTS-1 null mice treated with PMSG/hCG. Significant induction of ADAMTS-1 mRNA expression in rats and in mice has been shown to occur in the granulosa layer of the large follicles after hCG administration (Espey et al. 2000, Robker et al. 2000). A more recent study demonstrated that ADAMTS-1 protein predominantly accumulates in the ECM of the COC during cumulus cell expansion after hCG administration (Russell et al. 2003). Russell et al.(2003) also reported that processing of versican is reduced in COC of Progesterone receptor knockout mice in which ADAMTS-1 expression is downregulated (Russell et al. 2003). It has therefore been hypothesized that ADAMTS-1 is involved in the re-organization of the COC matrix by modulating versican prior to hCG-induced ovulation. We observed that cumulus cell expansion occurred in most of the unruptured large follicles of PMSG/hCG-treated ADAMTS-1 null ovaries, thus indicating that ADAMTS-1 is not essential for cumulus cell expansion. However, other ADAMTS family members, such as ADAMTS-4 which has similar substrate specificity to ADAMTS-1, may compensate for the loss of the function of ADAMTS-1 in cumulus expansion; it has been shown that ADAMTS family members including ADAMTS-4 and -5 are expressed in preovulatory follicles in the ovary (Madan et al. 2003, Russell et al. 2003). Similarly, the incomplete blockage of the ovulatory process observed in ADAMTS-1 knockout mice might be due to the compensatory functions of other ADAMTS family members, such as ADAMTS-4 and -5.
Degradation of ECM within the theca layer and tunica albuginea is necessary for follicle rupture. Matrix metalloproteinases (MMPs), such as MMP13, have been suggested to contribute to the breakdown of the follicle wall (Curry et al. 2001). We found that ADAMTS-1 null mice exhibited impairment of theca layer thinning and the ovulatory response to PMSG/hCG treatment (Fig. 6). Although ADAMTS-1 is not capable of degrading fibrillar collagens, such as collagens I and III (Rodriguez-Manzaneque et al. 2002), it is possible that ADAMTS-1 indirectly promotes degradation of the collagenous layers of the follicle wall by triggering signals that activate MMPs. Our previous study showed that ADAMTS-1 null mice exhibit renal phenotypes that resemble human UPJ stenosis, accumulating excessive collagen fibers in UPJ tissue (Shindo et al. 2000). It is likely that ADAMTS-1 plays a similar role in regulation of ECM remodeling in both UPJ tissue and ovaries.
Vascular endothelial growth factor (VEGF)-mediated follicular angiogenesis is involved in gonadotropin-dependent follicle development (Zimmermann et al. 2003). As ADAMTS-1 generally functions as an anti-angiogenic factor through inhibition of VEGF action, it can be expected that loss of ADAMTS-1 may affect vasculature in the ovary. In the present study, we found that the follicular angiogenesis of large follicles was somehow upregulated in ADAMTS-1 null ovaries. This might be due to loss of anti-angiogenic activity of ADAMTS-1. In contrast, more significant changes in the vasculature network in ADAMTS-1 null ovaries were observed in the medullary zone. We found that gonadotropin-induced formation of large blood vessels in the medullary zone was significantly impaired in ADAMTS-1 null mice. This shows that ADAMTS-1 does not function merely as an anti-angiogenic factor in the ovary, but positively regulates the formation of the blood vessel network, although the mechanisms remain to be investigated. ADAMTS-1 might participate in branching and dilation processes of blood vessel formation, although we cannot exclude the possibility that vascular changes in the medullary zone are the result of a decreased number of mature follicles.
As we found that types 5b and 6 follicles in ADAMTS-1 null mice had normal vascular plexus, it is unlikely that the decreased follicular development of ADAMTS-1 null mice can be attributed to alteration in follicular angiogenesis. However, dysplasia of large blood vessels in the medullary zone may affect blood supply to growing follicles and, therefore retard gonadotropin-dependent follicular development in ADAMTS-1 null mice.
In summary, our results provide evidence that ADAMTS-1 is involved in the ovulatory response of mature follicles, follicular development, and the organization of the medullary vascular network. An interesting question regarding the human ovary that arises based on the present results is whether defective ADAMTS-1 expression is a model for any ovarian dysfunction observed in human patients. Further studies on the functions of ADAMTS family members, including ADAMTS-1, in the ovary can be expected to advance the understanding of the molecular mechanisms of infertility.
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Acknowledgements |
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Funding |
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This work was supported by a Grant-in-Aid from the Ministry of Education, Science, and Culture of Japan. The authors declare that there is no conflict of interest that would prejudice the impartiality of this work.
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References |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Received in final form 16 June 2005
Accepted 22 June 2005
Made available online as an Accepted Preprint 14 July 2005
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