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Placental Folate Transport During Pregnancy

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Placental Folate Transport During Pregnancy Biosci. Biotechnol. Biochem., 72 (9), 2277–2284, 2008 Placental Folate Transport during Pregnancy Satoru YASUDA, Satoko HASUI, Chiaki YAMAMOTO, Chihiro YOSHIOKA, y Masaki KOBAYASHI, Shirou ITAGAKI, Takeshi HIRANO, and Ken ISEKI Laboratory of Clinical Pharmaceutics and Therapeutics, Division of Pharmascience, Faculty of Pharmaceutical Sciences, Hokkaido University, Kita 12-jo, Nishi 6-chome, Kita-ku, Sapporo 060-0812, Japan Received February 22, 2008; Accepted May 22, 2008; Online Publication, September 7, 2008 [doi:10.1271/bbb.80112] The aim of this study was to elucidate the mechanism growth,5) and that deficiencies in folates impair fetal of folate transport in the placenta over the course of development.6) It has been reported that folate defi- pregnancy. We found that folate receptor (FR ) and ciency during pregnancy increases the risk of the reduced folate carrier (RFC) localized on the apical side development of neural-tube defects in the infant.7,8) of human placental villi. Since folate binding to Although folates are important vitamins, mammals placental brush-border membrane vesicles (BBMVs) cannot synthesize them by themselves. Hence, intake of was strongly inhibited by phosphatidylinositol-specific folates from dietary sources is essential, and systems phospholipase C (PI-PLC) treatment, it is possible that for the absorption of folates from the intestine play an FR , a glycosyl phosphatidylinositol linked glycopro- important role in this process. These systems have been tein, is a candidate for folate uptake from maternal described, and the mechanisms of carrier-mediated blood to the placenta. Moreover, additional inhibitory absorption of folates have been identified.9,10) Folate effects of thiamine pyrophosphate (TPP) and hemin on receptor (FR ), a glycosylphosphatidylinositol linked folate uptake after PI-PLC treatment suggested that not glycoprotein, utilizes high-affinity binding of folates at only FR but also RFC and heme carrier protein 1 the membrane surface and mediates unidirectional flux (HCP1) are involved in the folate transport mechanism following internalization of the receptor-folate com- in the human placenta. It was also found that accumu- plex, in the same manner as that of many other ligand- lation of folate after intravenous injection increased receptor processes.11,12) Reduced folate carrier (RFC/ with the progress of gestation in the rat placenta and the SLC19A1) utilizes binding to a transporter at the fetus. Furthermore, increases in the expression levels of membrane surface to mediate internalization through mRNA of rFR , rRFC, and rHCP1 in the rat placenta membranes, and this process is capable of mediating during pregnancy were observed. These findings suggest bidirectional flux.13,14) It has been found that these that FR , RFC, and HCP1 are important carriers of carriers are pH-sensitive and are expressed not only in folate in the placenta during pregnancy. The results of the intestine but also in other organs, including the this study suggest that increases in the expression levels placenta.15–17) Furthermore, it is possible that intra- of FR , RFC, and HCP1 in the placenta play an cellular accumulation of folates reflects the operation important role in the response to increased need for of outward transport mediated by members of the folate for the placenta and fetus during development family of ATP-binding cassette transporters, such as with the progress of gestation. MRPs and breast cancer resistance protein (BCRP/ ABCG2).18) Key words: folate; placenta; folate receptor ; reduced It is known that the placenta is an organ that folate carrier; heme carrier protein 1 develops in a short period of time, and that its functions change with the progress of gestation. It has been The placenta is viewed as a protective barrier and a reported that expression levels of transporters that con- site for nutrient and waste exchange between mother and tribute to the transfer of nutrients and waste between fetus. It has been found that transporters play an the mother and the fetus change during pregnancy,19–21) important role in this nutrient and waste exchange in but the expression levels of carriers of folates in the the placenta.1–3) placenta over the course of pregnancy have not been Folates are essential nutrients required for the provi- investigated. sion of one-carbon moieties in biosynthetic processes.4) It is possible that heme carrier protein 1 (HCP1) is a It is known that they are essential for cell division and proton-coupled folate carrier in the intestine.22) Since y To whom correspondence should be addressed. Tel/Fax: +81-11-706-3770; E-mail: [email protected] 2278 S. YASUDA et al. folate uptake in placental cell lines has been found to be Preparation of BBMVs. BBMVs were prepared from pH-sensitive, it is conceivable that HCP1 also contrib- the human term placentas by the magnesium precipita- utes to folate transfer from mother to fetus. We have also tion method, with modifications.24) All steps were reported that HCP1 is a candidate folate carrier in the performed on ice or at 4 C. The placenta was washed placental cell line BeWo,23) but the function of HCP1 in with ice-cold saline. Then placental villi were cut as the human placenta has not determined. Thus, the tissue samples. The tissue samples (about 100 g wet mechanism by which folate is transported from mother weight) were stirred in 300 ml of ice-cold experimental to fetus, i.e., intake from the apical side of the placenta buffer (100 mMD-mannitol, 100 mM KCl, 20 mM villi, has not been clarified and investigation of this is HEPES/Tris, pH 7.4). After filtration with gauze, the necessary to identify the physiological system that samples were homogenized with a Waring blender at responds to folate demand in fetal development during 9,000 rpm for 4 min. MgCl2 solution (0.5 M) was added pregnancy. to a final concentration of 10 mM, and the homogenate The aim of this study was to determine the mecha- was allowed to stand for 20 min. The homogenate was nism of folate transport in the placenta over the course centrifuged at 4;300 Â g for 15 min, and then the super- of pregnancy. We investigated the folate transport natant was recentrifuged at 34;700 Â g for 30 min. The mechanism using human term placental brush-border resulting pellet was resuspended in 20 ml of experi- membrane vesicles (BBMVs). We also investigated mental buffer and homogenized in a glass/Teflon changes in folate accumulation in the placenta and fetus Dounce-type homogenizer at 10 strokes. After a final using pregnant rats at various days of gestation. centrifugation at 34;700 Â g for 30 min, the brush- border membranes were suspended in a buffer contain- Materials and Methods ing 100 mMD-mannitol, 100 mM KCl, and 20 mM MES/ Tris (pH 6.0), and homogenized with a Dounce-type Chemicals. [30,50,7,9-3H]Folic acid (23.0 Ci/mmol) homogenizer at 10 strokes. Then the samples were was purchased from Amersham Biosciences (Piscat- homogenized with a 25G syringe 10 times. When away, NJ). Folic acid (Folate) (pteroylglutamic acid, phosphatidylinositol-specific phospholipase C (PI-PLC) C19H19N7O6, Mw: 441.4) and folinic acid calcium salt treatment was needed, vesicles were incubated with (C20H21CaN7O7, Mw: 511.5) was purchased from Wako PI-PLC at 37 C for 30 min before the uptake experi- (Osaka, Japan) and Sigma-Aldrich (St. Louis, MO). All ment. The level of alkaline phosphatase (a marker other reagents were of the highest grade available and enzyme of the brush-border membrane) activity of the were used without further purification. brush-border membrane was more than 16-fold higher than that of the initial homogenate. Animals. Pregnant Wistar rats were obtained from Slc (Hamamatsu, Japan). The experimental protocols were Study of uptake by BBMVs. The uptake of [3H]-folic reviewed and approved by the Hokkaido University acid (0.5 mCi/ml) into brush-border membrane vesicles Animal Care Committee, in accordance with the ‘‘Guide was determined by the rapid filtration technique de- for the Care and Use of Laboratory Animals.’’ scribed previously.25) Twenty ml of membrane vesicle (8 mg protein/ml) suspension was added to 100 mlof Tissue collection. Human placental tissue (39–40 substrate mixture kept at 37 C. At the end of the incuba- weeks) was obtained, with informed consent and ethical tion period, uptake was stopped by diluting the incuba- committee approval, from patients admitted to Sapporo tion medium with 5 ml of ice-cold stop buffer (150 mM Maternity Women’s Hospital, Sapporo. Placentas were KCl, 20 mM HEPES/Tris, pH 7.5). The mixture was collected at term, following caesarean section, from immediately filtered through a Millipore filter (Millipore, women who had uncomplicated pregnancies. Billerica, MA; 0.45 mm in pore size, 2.5 cm in diameter; HAWP). The filter was rinsed with 5 ml of the same Immunohistochemistry. Tissue samples were obtained buffer. The radioactivity of the substrate trapped on from human placentas. They were snap-frozen in the filter was determined by scintillation spectrometry Optimal Cutting Temperature (OCT) compound and (1600TR, Packard Instruments, Meriden, CT). used for cryosections. Immunohistochemical staining was performed on paraformaldehyde-fixed and paraffin- Administration of folic acid and collection of placenta embedded sections. Tissue samples were incubated with and fetus. [3H]-Folic acid was administered in saline a monoclonal antibody of FR (Alexis, Lausen, Switzer- at a concentration of 282.5 ng/kg of body weight (13.5 land) or RFC (Alpha Diagnostic International, San Ci/ml) by intravenous injection from the jugular vein Antonio, TX) (dilution, 1:100). After washing with PBS, under ether anesthesia. The experimental rats were the samples were incubated with an FITC- or PE- beheaded 3 h after administration of folate, and samples conjugated secondary antibody at a dilution of 1:100.
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