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(IFN-Γ/IL-4) Cytokine Mrna Ratio of Rat Embryos in the Pregnant Mouse Uterus

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(IFN-Γ/IL-4) Cytokine Mrna Ratio of Rat Embryos in the Pregnant Mouse Uterus Journal of Reproduction and Development, Vol. 53, No. 2, 2007 —Full Paper— Increased Th1/Th2 (IFN-γ/IL-4) Cytokine mRNA Ratio of Rat Embryos in the Pregnant Mouse Uterus Chang-Long NAN1,2), Zi-Li LEI1,2), Zhen-Jun ZHAO1,2), Li-Hong SHI1,2), Ying-Chun OUYANG1), Xiang-Fen SONG1), Qing-Yuan SUN1) and Da-Yuan CHEN1) 1)State Key Laboratory of Reproductive Biology, Institute of Zoology and 2)Graduate School, Chinese Academy of Sciences, #25 Bei-Si-Huan-Xi Lu, Hai Dian, Beijing 100080, P. R. China Abstract. Somatic cell nuclei can be dedifferentiated in ooplasm from another species, and interspecies cloned embryos can be implanted into the uteri of surrogates. However, no full pregnancies have been achieved through interspecific mammalian cloning. Rat blastocysts transferred into mouse uteri provide a unique model for studying the causes of interspecific pregnancy failure. In this study, intraspecific pregnancy (mouse-mouse) and interspecific pregnancy (rat-mouse) models were established. On Day 9 of pregnancy, the fetoplacental units were separated from the uterine implantation sites and the expression of messenger (m)RNA was quantitated by real- time PCR. We compared the mRNA expression levels of type-1 T helper (Th1) and type-2 T helper (Th2) cytokines, interferon-gamma (IFN-γ), and interleukin-4 (IL-4) in fetoplacental units between intraspecific and interspecific pregnancy groups. The mRNA expression of IFN-γ in the fetoplacental units of the interspecific pregnancy group was significantly higher than that of the intraspecific pregnancy group (P<0.05). The mRNA expression of IL-4 in the interspecific pregnancy group was significantly lower than that in the intraspecific pregnancy group (P<0.05). We also analyzed the ratio of IFN-γ/IL-4 mRNA, and an increased IFN-γ/IL-4 mRNA ratio was observed in the interspecific pregnancy compared with that in the intraspecific pregnancy group. The IFN-γ and IL-4 mRNA expressions indicate that there is a Th1/Th2 imbalance in the feto-maternal interface of interspecific pregnancies. Bias of Th1 cytokine dominance may be a barrier to reproductive success between species. Key words: Interferon (IFN)-γ, Interleukin (IL)-4, Interspecific pregnancy, Mouse, Rat (J. Reprod. Dev. 53: 219–228, 2007) o far, somatic cell nuclear transfer (SCNT) has explored to produce cloned offspring, and usually succeeded in generating live animals in many includes interspecific somatic cell nuclear transfer species, including sheep, cattle, mice, goats, pigs, and interspecific pregnancy. In previous research, rabbits, cats, rats, mules, horses, dogs, and ferrets the oocytes of bovine, sheep, and rabbits have been [1–4]. However, it is impractical to clone used for iSCNT, and interspecific reconstructed endangered species by intraspecific SCNT because embryos have been obtained [5–13]. Interspecific of insufficient numbers of oocytes and surrogate reconstructed embryos can implant into females. So, interspecific SCNT (iSCNT) has been interspecific uteri, but only three speices have been successfully cloned by iSCNT [14–16]. Bovine Accepted for publication: October 14, 2006 Published online: November 29, 2006 ooplasm was capable of reprogramming the Correspondence: D-Y Chen (e-mail: [email protected]) banteng [Bos javanicus, listed as a threatened 220 NAN et al. species by the IUCN Red List (2002)] nucleus to recurrent spontaneous abortion [30, 31], achieve blastocyst stage embryos, and two preeclampsia [32–34], intrauterine growth pregnancies were established with heartbeats retardation [35], preterm delivery, and premature detectable at day 30, but both pregnancies were rupture of membranes [36, 37]. Shift of the Th1/ subsequently lost [17]. In another study, two Th2 balance to Th1 dominance contributes to the pregnancies were established after iSCNT using failure of pregnancy. domestic sheep (Ovis aries) for recipient ooplasts In order to investigate the importance of the and an exotic argali (Ovis ammon) as a karyoplast Th1/Th2 balance in the failure of interspecific donor, but these two pregnancies were lost by day pregnancy, we transferred rat or mouse blastocysts 59 of gestation [8]. In our laboratory, we have into mouse uteri in this study to produce models of reconstructed approximately 2300 panda intraspecific and interspecific pregnancy. The (Ailuropoda melanoleuca, a highly endangered mRNA expressions of IFN-γ and IL-4 at the feto- species) -rabbit interspecific cloned embryos and maternal interface of intraspecific and interspecific transferred them into the oviducts of 100 recipient pregnancies were quantitated by real-time PCR. cats. We found that panda-rabbit cloned embryos Thus, for the purposes of this study, the ratio of could be implanted into the uteri of a third species, IFN-γ mRNA to IL-4 mRNA was accepted as the but pregnancies were lost after 45 days [10]. The Th1/Th2 ratio [38] in order to determine whether high failure rate of interspecific pregnancies has incorrect modulation of the Th1/Th2 balance become a major obstacle to successful interspecific occurs in interspecific pregnancy. cloning. Therefore, it is necessary to understand the reason for interspecific pregnancy failure. Studies of embryo transfer between rats and mice Materials and Methods have shown that rat embryos can adhere closely to the epithelium of mouse uteri [18], and rat embryos Collection of blastocysts can survive up to the ninth day of pregnancy [19]. Adult females of outbred Kunming mice (5–6 This provides us with a good model for weeks old) and outbred SD rats (10–14 weeks old) investigating the mechanisms of interspecific were superovulated with 10 IU and 40 IU pregnant pregnancy failure. mare serum gonadotropin (PMSG, Tianjin T lymphocytes can be classified as type-1 T Experimental Animal Center, Tianjin, P.R. China), helper (Th1) cells and type-2 T helper (Th2) cells. followed by 10 IU and 40 IU human chorionic Th1 cells produce mainly interleukin (IL)-2, gonadotropin (hCG; Institute of Zoology, CAS, interferon (IFN)-γ, and tumor necrosis factor (TNF)- Beijing, P.R. China) 48 h later, respectively. Then, β, i.e. Th1-type cytokines, and induce cellular the superovulated females were mated with male immunity. Th2 cells synthesize IL-4, IL-5, IL-6, IL- animals of the same species. The females were 10, and IL-13, i.e. Th2-type cytokine, and induce checked the next morning for the presence of a antibody production [20]. During pregnancy, the vaginal plug to confirm successful mating. The first cytokines produced by Th2 cells predominate and morning that a vaginal plug was observed was suppress Th1-type immune reaction. Reversal of designated Day 1 of pregnancy. Day 4 female mice the Th2 cytokines bias, which was referred to as “a and Day 5 female rats were euthanized post-coitus Th2 phenomenon” by Wegmann et al. [21], plays an by cervical dislocation, and embryos were flushed important role in normal pregnancy. Many clinical from the uteri with M2 medium [39]. Mouse and laboratory findings support Wegmann’s blastocysts were transferred into droplets of CZB hypothesis [22–28]. Excessive amounts of Th1 medium [40] and rat blastocysts were transferred cytokines could hamper the immunological into mR1ECM medium [41]. Both were then tolerance of the female to the foreign antigens of the incubated at 37 C in 5% CO2 in a humidified fetus. Increased expression of Th1 cytokines or an chamber before embryo transfer. increased ratio of Th1/Th2 cytokines has been observed at the feto-maternal interface in abortion- Embryo transfer and sample collection prone mice [29], and this occurs not only at the feto- The foster mothers for embryo transfer were maternal interface but also in the peripheral blood Kunming females mated with vasectomized males. in many human pregnancy failures, such as Five or six rat blastocysts in 1–3 µl mR1ECM were TH1/TH2 RATIO IN RAT-MOUSE PREGNANCY 221 surgically transferred into a single uterine horn of ATT-TTC-ATG-3’ (3’ primer); 5’-ACA-GGA-GAA- Day 3 pseudopregnant mice. The same number of GGG-ACG-CCA-T-3’ (5’ primer) and 5’-GAA- mouse blastocysts was transferred into a single GCC-CTA-CAG-ACG-AGC-TCA-3’ (3’ primer); 5’- uterine horn of Day 3 pseudopregnant mice to be CCC-TAA-GGC-CAA-CCG-TGA-A-3’ (5’ primer) used as a control group. The pregnant animals and 5’-CAG-CCT-GGA-TGG-CTA-CGT-ACA-3’ (3’ were enthanized by cervical dislocation on Day 9, primer), respectively. The cycling conditions were and the uterine horns with conceptuses were 94 C for 30 sec, 55 C for 30 sec, and 72 C for 30 sec dissected and isolated. They were opened for 40 cycles with Pyrobest DNA polymerase longitudinally, and the fetoplacental units were (TaKaRa, Ohtsu, Japan). Each of these amplicons separated from the uterine implantation sites, was purified on silica columns (Qiagen, Valencia, immediately frozen in liquid nitrogen, and stored CA, USA). Plasmid standards for each target gene at –80 C for later use. of interest were constructed by cloning a partial cytokine cDNA fragment into a pGEM-T easy RNA extraction and cDNA synthesis plasmid vector (TaKaRa). The exact sequences of Frozen tissues from fetoplacental units were the cloned amplicons were analysed by cycle pulverized in liquid nitrogen. Total RNA sequencing. Concentrations of standard plasmids extractions were performed using TRIzol reagent were measured by UV-spectrophotometry, and (Invitrogen, Carlsbad, CA, USA) according to the copy numbers were calculated as described by Manufacturer’s instructions, and were diluted in Overbergh [42]. RNase-free water. Residual genomic DNA was removed by treatment with 2 units of DNase I Real-time PCR (Promega, Madison, WI, USA) at 37 C for 30 min Total tissue RNA of fetoplacental units was followed by inactivation at 65 C for 10 min. The extracted from 22 mouse-mouse and 22 rat-mouse samples were re-extracted with an equal volume of pregnancies.
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