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RESEARCH |
1 Department of Gynecology and Obstetrics, Faculty of Medicine2 Institute for Virus Research, Kyoto University, Sakyo-Ku, Kyoto 606, Japan
Correspondence should be addressed to M Ueda; Email: mueda{at}virus.kyoto-u.ac.jp
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Abstract |
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 Top Abstract IntroductionResultsDiscussionMaterials and MethodsDeclaration of interestFundingAcknowledgementsReferences |
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Introduction |
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We previously reported that the expression profiles of several cell surface molecules on luteal cells became changed from CL of menstrual cycle to CL of pregnancy. For example, membrane-bound aminopeptidase-N and dipeptidyl peptidase-IV were highly expressed on small luteal cells in the CL of menstrual cycle, but it was hardly detected on small luteal cells in the CL of pregnancy (Fujiwara et al. 1992a, 1992b). Other membrane-bound peptidases, carboxypeptidase-M and endothelin-converting enzyme-1, expressed their isotypes only in CL of pregnancy (Yoshioka et al. 1998a, 1998b), suggesting that these peptidases are involved in the function of CL of pregnancy (Fujiwara 2004). On the other hand, integrin 
6 was expressed on large luteal cells in the CL of menstrual cycle, but it was not expressed on those in the CL of pregnancy (Honda et al. 1995). In addition to these cell surface molecules, relaxin gene expression was reported to increase in the CL of pregnancy (Bogic et al. 1995). Furthermore, we observed that the responses to immune cells in the luteal cell cultures were different between women in mid-luteal phase and early pregnancy. In the luteal cell culture derived from CL of pregnancy, interleukin 4 (IL4) and IL10 productions by the immune cell stimulation were significantly higher than those in the culture derived from CL collected during the mid-luteal phase. In addition, IL4 and IL10 promoted progesterone production by luteal cells as much as human chorionic gonadotropin (HCG) in vitro (Hashii et al. 1998). These results supported that human CL of pregnancy is functionally different from CL in mid-luteal phase and proposed that the CL function is regulated not only by HCG (Takao et al. 1997) but also by immune cells (Fujiwara 2006).
From these findings, it is speculated that CL of pregnancy is in a further differentiated stage compared as CL of menstrual cycle. However, there has been no definite evidence to conform this concept. Therefore, in this study, to identify the key substances that are specifically involved in the physiology of CL of pregnancy, we raised mAbs against human CL of pregnancy and obtained a mAb, named human corpus luteum (HCL)-4, which highly reacted with cytoplasmic molecules in luteal cells in the CL of pregnancy. The subsequent analysis of purified antigen demonstrated that HCL-4 mAb detects monoamine oxidase A (MAOA, EC1.4.3.4). Since MAOA catabolizes biogenic amines such as dopamine, norepinephrine, and epinephrine that are well known to regulate vasoconstriction, this enzyme can be one of the crucial molecules to regulate the function of CL of pregnancy. Therefore, we further examined the precise expression profiles of MAOA in human follicles, CL of menstrual cycle, and CL of pregnancy in relation to their differentiation stages.
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Results |
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In growing follicles, 4–5 mm in diameter, HCL-4 antigen was rarely detected on granulosa or theca interna cells (Fig. 1A–C). In two of three preovulatory follicles, 18–20 mm in diameter, HCL-4 antigen was weakly detected on theca interna cells but not on the granulosa cells. In the remaining one preovulatory follicle, HCL-4 antigen was not detected on the granulosa cells or theca interna cells (data not shown).
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In CL of pregnancy at 6–15 weeks of gestation, HCL-4 antigen was highly expressed on large luteal cells and weakly or moderately expressed on small luteal cells (Fig. 1G–I). It was not expressed in ovarian stromal cells or blood vessels.
The intensity score of HCL-4 antigen expression on large luteal cells in CL of pregnancy was significantly higher than that of CL of menstrual cycle (P<0.01). HCL-4 antigen expression on small luteal cells in CL of pregnancy was also significantly higher than that of CL of menstrual cycle (P<0.01; Table 1).
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Discussion |
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In the present study, we raised mAb that highly reacted with cytoplasmic molecules in the luteal cells in CL of pregnancy. This mAb also reacted with syncytiotrophoblasts of placenta. The purified molecule from CL and placenta showed a molecular mass of 61 kDa, which corresponded to the calculated value for MAO (Bach et al. 1988) and accorded with that of MAOA (61 kDa) in adipose tissue (Pizzinat et al. 1999). The partial amino acid sequence of purified antigenic molecule from human placenta was completely identical to the sequence from the 31st to the 50th amino acid of MAOA. Although it also showed 70% homology with the sequence of MAOB, from the fact that HCL-4 mAb was not reactive to peripheral blood mononuclear cells or ovarian blood vessels that were reported to strongly express MAOB (Yoshimoto et al. 1986, Berry et al. 1994), it has been concluded that the HCL-4 mAb is specifically reactive to human MAOA.
Immunohistochemical study showed that immunoreactive MAOA protein was abundantly expressed in the CL of pregnancy. The expression of MAOA on the large luteal cells in CL of menstrual cycle remained constantly low throughout the luteal phase. MAOA expression on the small luteal cells during menstrual cycle was not detected although weak expression was observed in the theca interna cells in the preovulatory follicles. The apparent difference in MAOA protein expression between CL of menstrual cycle and pregnancy was also shown by immunoaffinity chromatography (Fig. 2). In addition, western and northern blot analyses showed high expression of MAOA protein at 61 kDa and mRNA at 4.4 and 2.1 kbp in CL of pregnancy (Figs 5 and 7). These profiles of MAOA mRNA accord with the reported ones that were derived from the adipose tissue (Pizzinat et al. 1999). Taken together with the profiles obtained by immunohistochemistry and SDS-PAGE, we conclude that MAOA expression increases in CL of pregnancy, supporting the concept that CL of pregnancy is in the further differentiated state from CL of menstrual cycle. However, it should be noted that because these CL samples were obtained from patients having uterine myoma and benign ovarian cysts, these diseases may anatomically influence vascular circulation and ovarian function affecting MAOA expressions. In northern blot analysis, MAOA mRNA expression in the CL derived from 12 weeks of gestation, when luteo-placental shift has already occurred (Schindler 2005), was relatively high. Although the precise reasons are unclear, there is discrepancy between the expression intensity among western (Fig. 5) and northern blot analyses. This may be caused by unknown regulatory mechanisms for inherent expression of MAOA.
In the rat ovary, MAOA-like enzyme activity was detected in the CL of estrous cycle (Yoshimoto et al. 1986). The total MAO activity in the rat ovary was reported to gradually increase during pregnancy until delivery (Kono et al. 1994). It is widely known that MAO plays a protective role in various tissues by oxidizing amines in circulation. MAOA expressed in the syncytiotrophoblast layer in human placenta was suggested to protect against hypertension caused by catecholamines and serotonin in circulating blood, which arise in toxemia of pregnancy (Yoshimoto et al. 1986). Consequently, high expression of MAOA on the luteal cells of CL of pregnancy suggests that MAOA is involved in metabolizing biogenic amines within CL of pregnancy. By transvaginal color velocity imaging and pulsed Doppler ultrasonography, human CL blood flow was reported to remain constant during normal early pregnancy from 6 to 12 weeks of gestation (Salim et al. 1994, Alcazar et al. 1996). The vascular network in CL is established in the mid-luteal phase and further matured during early pregnancy. Innervation of peripheral nerve system, which contains a catecholamine system, may develop around newly constructed vessels. In perfused human ovaries, -adrenergic agonists were shown to cause vasoconstriction, while β-adrenergic agonists cause vasodilation (Varga et al. 1979). Thus, MAOA expressed in the human CL of pregnancy is speculated to regulate luteal blood flow in early pregnancy by decreasing the biological activity of catecholamines.
Accumulating evidence has shown that catecholamines directly affect luteal cell function. Norepinephrine stimulation was reported to enhance progesterone secretion from bovine CL (Bogacki & Kotwica 1999). The presence of norepinephrine and dopamine was also demonstrated in bovine CL (Battista et al. 1989, Kotwica et al. 1996). Epinephrine was shown to promote progesterone and oxytocin concentration in goat CL as well (Cooke & Payne 1998). However, in the rabbit, catecholamines reduced the responsiveness of LH in the luteal cells (Jena & Abramowitz 1989). It was also reported that the administration of β-adrenergic receptor antagonist to pseudo-pregnant rabbit did not affect progesterone secretion (Gadsby et al. 1985). The direct effects of catecholamines on primate luteal cell function are controversial. It is assumed that the local concentrations and effects of catecholamines on CL must be taken into considerations. It was reported that epinephrine and norepinephrine stimulated progesterone production by cultured luteinizing human granulosa cells, which correspond to luteal cells in the early luteal phase (Webley et al. 1988). Although the precise mechanisms for direct effects of catecholamines on luteal cells are unknown, the high expression of MAOA in human CL of pregnancy suggests the physiological roles of catecholamines and MAOA in the function of CL of pregnancy.
In conclusion, this study indicated that MAOA was prominently expressed on large and small luteal cells in CL of pregnancy. The apparent increase in MAOA expression in CL from menstrual cycle to early pregnancy suggests that catecholamines play important roles in the function of CL of pregnancy.
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Materials and Methods |
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mAb production
Luteal cells were isolated from CL tissue at 15 weeks of gestation as described previously (Fujiwara et al. 1996). Briefly, the CL was separated from the connective tissue, minced with scissors, and then incubated in RPMI 1640 medium (Flow Laboratories, Irvine, Scotland) containing 0.2% collagenase type I (Sigma Chemical Co.) and 0.01% DNase I (Sigma Chemical Co.) at 37 °C for 15 min. The cell suspension was incubated with 1000 IU/ml dispase (Godo Shusei Co. Ltd, Tokyo, Japan) in RPMI 1640 containing 10% fetal calf serum (Flow Laboratories, McLean, VA, USA) at 37 °C for 30 min. Eight-week-old BALB/c mice were injected intraperitoneally with 3x106 human luteal cells three times with about 1-month interval. Under ethanol anesthesia, blood was taken from the immunized mice and then the spleen was removed after killing by cervical vertebrae dislocation. Spleen cells were isolated and fused with X63Ag8.653 myeloma cells using polyethylene glycol 1500 3 days after the last immunization (Köhler & Milstein 1975). Supernatants from the growing hybridomas were screened by indirect immunofluorescence staining of CL cryosections, which were prepared as described (Fujiwara et al. 1996). Briefly, fresh CL of menstrual cycle (CL on day 7) or CL of pregnancy (15 weeks of gestation) was embedded in OCT compound (Tissue-Tec; Miles Scientific, Naperville, IL, USA), snap-frozen in liquid nitrogen, and stored at –80 °C. Frozen tissues were cut into 7 µm thick sections using a cryostatic microtome (Histostat, Reichert-Jung, Heidelberg, Germany). The sections were immediately and thoroughly air-dried on Neoplene (Nisshin EM Co. Ltd, Tokyo, Japan)-coated glass slides and then fixed with acetone at –20 °C. For screening, cryosections prepared from CL of pregnancy were incubated with supernatants of the growing hybridomas for 60 min at room temperature. After washing in PBS, specimens were incubated with FITC-conjugated rabbit anti-mouse pAb (diluted 1:50; DAKO Japan Co. Ltd, Kyoto, Japan) for 30 min at room temperature in the dark. The slides were washed, mounted with an anti-fade mounting agent (Perma Fluor Aqueous Mounting Medium; Immunon, Pittsburgh, PA, USA) to reduce fluorescence fading, and examined under a fluorescence microscope (Nikon, Tokyo, Japan).
The hybrid cells of interest were cloned twice by limiting the dilution method. The immunoglobulin isotype was determined using an isotyping kit for mouse mAbs (Serotec Ltd, Oxford, UK). The positive hybrid cells were injected intraperitoneally into mice previously treated with pristane (2,6,10,14-tetramethylpentadecane; Aldrich Chemical Co., Milwaukee, WI, USA). The IgG3 fraction was purified from ascitic fluid using Affi-Gel protein A (Bio-Rad Labs).
Immunohistochemical examination of HCL-4 antigen expression on CL and placenta
Purified HCL-4 mAb (5 µg/ml, diluted in culture medium) was used for indirect immunofluorescence staining as described above. Anti-trinitrophenyl (TNP) mouse mAb (IgG3 class, 5 µg/ml), which was an unrelated mAb raised against TNP, was used as the negative control (Tsujimura et al. 1990). The slides were washed, mounted with an anti-fade agent (Perma Fluor Aqueous Mounting Medium), and were examined within 6 h under a fluorescent microscope by two individuals. The intensity of antigen expression was graded from – to +++ based on its fluorescence intensity and scored for statistical analysis (–, absence of staining, score 0; +, weak staining, score 1; ++, medium staining, score 2; and +++, intense staining, score 3). If judgments differed, the lower value was selected. Two samples, a CL on day 8 (Fig. 1D–F) and a CL of pregnancy at 10 weeks of gestation (Fig. 1G–I), the fluorescence intensities of which were scores 1 and 3 respectively were used as the standard visual assessment throughout this study as described previously (Fujiwara et al. 1994).
For double staining, the slides were incubated with HCL-1 mAb (5 µg/ml), which specifically reacted with cell surface of large luteal cells in human CL (Fujiwara et al. 1996), HCL-4 mAb (5 µg/ml), or negative control mAb (5 µg/ml) for 60 min at room temperature. After washing in PBS, the slides were incubated with rhodamine-conjugated goat anti-mouse pAb (diluted 1:40; Santa Cruz Biotechnology, Inc., Santa Cruz, CA, USA) for 30 min at room temperature in the dark. After washing, FITC-conjugated sheep anti-human von Willebrand factor pAb (100 µg/ml; Binding Site, Birmingham, UK) or FITC-conjugated sheep anti-rat IgG (negative control, 100 µg/ml; Binding Site) was incubated for 30 min to detect the endothelial cells. After reacting with rhodamine-conjugated goat anti-mouse pAb, the other slides were incubated with rabbit anti-human HSD pAb (Oxygene, Dallas, TX, USA) or rabbit immunoglobulin (negative control) and then reacted with FITC-conjugated swine anti-rabbit pAb (DAKO, Glostrup, Denmark). After washing, the slides were mounted and examined under a confocal laser scanning microscope (Carl Zeiss, Inc., Jena, Germany).
Purification of the HCL-4 antigen from CL of pregnancy
Purification of the antigenic proteins was performed as previously reported (Honda et al. 1995). Tissue specimens (CL on day 9 or CL of pregnancy at 10 weeks of gestation, 0.5 g wet weight each) were homogenized in 5 ml of 40 mM phosphate buffer (pH 7.3) containing 150 mM NaCl, 5 mM EDTA, 1% Nonidet P-40 (Sigma Chemical Co.), 2 mM p-amidinophenylmethane sulfonylfluoride hydrochloride (Wako Pure Chemicals, Osaka, Japan), 10 µg/ml leupeptin (Peptide Institute, Inc., Osaka, Japan), and 10 µg/ml pepstatin (Peptide Institute, Inc.). After centrifugation (10 000 g, 30 min), the concentration of Nonidet P-40 was diluted to 0.3%. The supernatant was passed through a column containing 5 ml anti-TNP-conjugated Affi-gel 10 (Bio-Rad Labs; 2 mg IgG/ml gel) at 4 °C to remove nonspecifically bound components. The through-pass fraction was incubated with 0.1 ml HCL-4-conjugated Affi-gel 10 (2 mg IgG/ml gel) at 4 °C for 2 h. After washing the gel extensively, the antigen was eluted with 0.5 M NH4OH containing 0.1% Nonidet P-40. The eluate was dried in vacuo at room temperature. The sample was dissolved in lysis buffer with 0.1 M dithiothreitol, and separated by 10% SDS-PAGE. Proteins in the gel were stained with a silver stain kit (Wako Pure Chemicals). The same procedure was repeated three times with distinct samples.
Purification of the HCL-4 antigen from placenta and partial amino acid sequence analysis
Human placenta (40 g wet weight) were homogenized in 400 ml of 40 mM phosphate buffer (pH 7.3) containing 150 mM NaCl, 5 mM EDTA, 1% Nonidet P-40, and 2 mM p-amidinophenylmethane sulfonylfluoride hydrochloride. After centrifugation (10 000 g, 30 min), the concentration of Nonidet P-40 was reduced by dilution to 0.3%. The supernatant was mixed with 25 ml anti-TNP-conjugated Affi-gel 10. The unbound fraction was incubated with 1 ml HCL-4-conjugated Affi-gel 10 (2 mg IgG/ml gel) at 4 °C overnight. After washing the gel, the antigen was eluted with 0.5 M NH4OH containing 0.1% Nonidet P-40. The eluate was dried in vacuo at room temperature. The sample was separated by 10% SDS-PAGE, and proteins in the gel were transblotted onto the PVDF membrane (Millipore Corp., Bedford, MA, USA) in Tris/boric acid buffer with 0.05% SDS and 20% methanol. The protein on the PVDF membrane was stained with 0.1% Coomassie Blue R-250 (Nacalai Tesque, Kyoto, Japan) in 50% methanol and the protein band was used for N-terminal amino acid sequence analysis. Sequencing was performed by TAKARA, Japan. In some experiments, the dried eluate was treated with lysyl endopeptidase (1 mg/ml, Nacalai Tesque) at 37 °C in 0.1 M citrate buffer (pH 5.0) overnight, and the protein fragments obtained were separated by 15% SDS-PAGE. They were transblotted onto PVDF membrane as described above, and N-terminal amino acid sequences of main band were analyzed. The SWISS-PROT database was used in the analysis of amino acid sequence homology.
Western blotting analysis of CL
CL of menstrual cycle (CL days 7, 8, and 9) and CL of pregnancy of 7 (n=2) and 12 weeks of gestation was homogenized by sonication with lysis buffer including 2 mM p-amidinophenylmethane sulfonylfluoride hydrochloride, and they were centrifuged at 15 000 g for 20 min. Chorion from the term placenta was also dissolved. Each supernatant including 40 µg protein was electrophoresed in 10% SDS-polyacrylamide gel, and transblotted on the PVDF membrane as above in Tris/glycine buffer with 0.03% SDS and 20% methanol. The PVDF membrane was treated with Block Ace (Dainihon Pharmaceutics, Osaka, Japan), rabbit pAb against human MAOA (H-70, Santa Cruz Biotechnology, Inc.) and human β-actin (ab8227; Abcam Co. Tokyo, Japan), and then horseradish peroxidase (HRP)-conjugated goat antibody to rabbit Igs (DAKO Japan; Honda et al. 1995). HRP was visualized with 3,3'-diaminobenzidine tetrahydrochrolide (Dojin, Kumamoto, Japan). The intensity of the bands was quantified and analyzed by an NIH image software program (Image/J, http://rsb.info.nih.gov/ij/). The data were expressed as a ratio of MAOA densitometric intensity divided by the corresponding intensity of β-actin.
RNA isolation and northern blotting
Total RNAs from human menstrual CL on CL days 7, 8 (n=2), and 9, and pregnant CL at 7 (n=2), 9, and 12 weeks of gestation were isolated using a commercial kit (TRIzol, Invitrogen). Five micrograms of total RNA from the CL were reverse transcribed with random primers using a commercial kit (First-Strand cDNA Synthesis Kit; Pharmacia, Inc). The resulting cDNA mixtures were subjected to 30 cycles of PCR amplification with oligonucleotide primers designed based on the sequence of human MAOA cDNA (sense primer 5'-AGGAAATAAGGAAGAAGA-3': positions 1170–1189; antisense primer 5'-ACACTGACAAATAAGATGGA-3': positions 1848–1867, GenBank M68840; Bach et al. 1988), or with human RPS26 primers (sense primer 5'-GGTCCGTGCCTCCAAGATGA-3': positions 8–27; antisense primer 5'-TAAATCGGGGTGGGGGTGTT-3': positions 308–327; Vincent et al. 1993). After PCR amplification, 10 µl of each PCR product was electrophoresed on a 1.5% agarose gel, and amplified bands were detected by ethidium bromide staining. After cloning, the PCR product and verifying its sequence, the enzymatically digested cDNA insert was purified and used as a probe for subsequent northern blot analysis that was performed as previously reported (Higuchi et al. 1995). In brief, 10 µg total RNAs were electrophoresed on a 1.0% agarose–formaldehyde gel and then transferred to nylon membranes. The membranes were incubated with a prehybridization solution (Rapid Hyb, Amersham-Pharmacia) for 30 min at 65 °C and then hybridized with [32P] dCTP-labeled MAOA cDNA probes in the same solution for 2 h at 65 °C. After hybridization, the filters were washed according to the manufacturer's protocol and then subjected to autoradiography. The membranes were stripped and then reprobed with RPS26 cDNA. The intensity of the bands was quantified and analyzed by an NIH image software program (Image/J). The data were expressed as a ratio of MAOA densitometric intensity divided by the corresponding intensity of RPS26.
Statistical analysis
Data are shown as means±S.E.M. The data of bands of MAOA protein (western blot) and mRNA (northern blot) in corpora lutea of mid-luteal phase and pregnancy were analyzed by an unpaired t-test. The expression scores of HCL-4 antigen on large and small luteal cells in CL of menstrual cycle and CL of pregnancy were analyzed by Mann–Whitney analysis. The above statistical analyses were performed by the personal computer soft StatView J 5.0.
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Declaration of interest |
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Funding |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestFundingAcknowledgementsReferences |
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Acknowledgements |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestFundingAcknowledgementsReferences |
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Received 3 January 2008
First decision 26 February 2008
Revised manuscript received 30 April 2008
Accepted 21 May 2008
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References |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestFundingAcknowledgementsReferences |
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