Impact of mouse pregnancy on thymic T lymphocyte subsets
María E. Cortina A , Silvana Litwin A , María E. Roux A and Silvia Miranda A BA Laboratorio de GlicoInmunoBiología, Instituto de Investigaciones Cardiológicas Prof. Dr Alberto C. Taquini (CONICET-UBA), Marcelo T. de Alvear 2270, C1122AAJ Ciudad de Buenos Aires, Argentina.
B Corresponding author. Email: smiranda@ffyb.uba.ar
Reproduction, Fertility and Development 24(8) 1123-1133 https://doi.org/10.1071/RD11252
Submitted: 30 September 2011 Accepted: 28 February 2012 Published: 24 April 2012
Abstract
It has been reported that fetal lymphoid progenitor cells are acquired during gestation and are able to develop in the maternal mouse thymus into functional T cells. Moreover, previous pregnancies increase the number of fetal cells in the mother. In the present study, we investigated whether mouse pregnancy induces changes in T lymphocyte subsets in the maternal thymus. We determined the T lymphocyte subsets in two allogeneic cross-breedings, namely CBA/J × BALB/c (normal) and CBA/J × DBA/2 (abortion prone), and investigated the effects of the age and parity of the female, as well as pregnancy outcome, on thymocyte populations. In addition, hormonal effects were evaluated in a syngeneic combination (CBA/J × CBA/J). We found that during pregnancy both hormonal and allogeneic stimuli induced a reduction in the CD4+CD8+ subset with an increase in the CD4+CD8– population. Only young females of the normal combination exhibited an increase in the CD4–CD8+ population. All young mice showed an increase in CD4+CD25+FoxP3+ T cells. Interestingly, the γδT thymus pool was increased in all females of the normal allogeneic pregnancy only, suggesting the participation of this pool in the observed beneficial effect of multiparity in this cross-breeding. Our results demonstrate that allogeneic pregnancies induce important variations in maternal thymocyte subpopulations depending on the age of the female and the male component of the cross-breeding.
Additional keywords: age, thymocytes.
References
Aït-Azzouzene, D., Gendron, M. C., Houdayer, M., Langkopf, A., Burki, K., Nemazee, D., and Kanellopoulos-Langevin, C. (1998). Maternal B lymphocytes specific for paternal histocompatibility antigens are partially deleted during pregnancy. J. Immunol. 161, 2677–2683.| 9743323PubMed |
Aït-Azzouzene, D., Caucheteux, S., Tchang, F., Wantyghem, J., Moutier, R., Langkopf, A., Gendron, M. C., and Kanellopoulos-Langevin, C. (2001). Transgenic major histocompatibility complex class I antigen expressed in mouse trophoblast affects maternal immature B cells. Biol. Reprod. 65, 337–344.
| Transgenic major histocompatibility complex class I antigen expressed in mouse trophoblast affects maternal immature B cells.Crossref | GoogleScholarGoogle Scholar | 11466198PubMed |
Aluvihare, V. R., Kallikourdis, M., and Betz, A. G. (2004). Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 5, 266–271.
| Regulatory T cells mediate maternal tolerance to the fetus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsFeitL8%3D&md5=ae88567084d3cc619d4dd96f26514289CAS | 14758358PubMed |
Arck, P. C., Ferrick, D. A., Steele-Norwood, D., Croitoru, K., and Clark, D. A. (1997). Regulation of abortion by γδT cells. Am. J. Reprod. Immunol. 37, 87–93.
| Regulation of abortion by γδT cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3gsFKrsQ%3D%3D&md5=bff24baeb5a2320aa09cff68ba5c3f0aCAS | 9138458PubMed |
Arck, P., Dietl, J., and Clark, D. (1999). From the decidual cell internet: trophoblast-recognizing T cells. Biol. Reprod. 60, 227–233.
| From the decidual cell internet: trophoblast-recognizing T cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotlyisA%3D%3D&md5=5f6931df9f651fd8509a6ad13b186150CAS | 9915985PubMed |
Aspinall, R. (1997). Age-associated thymic atrophy in the mouse is due to a deficiency affecting rearrangement of the TCR during intrathymic T cell development. J. Immunol. 158, 3037–3045.
| 1:CAS:528:DyaK2sXit1Cgurc%3D&md5=111cb5368c18c5037218659a075c621cCAS | 9120255PubMed |
Bianchi, D. W., Zickwolf, G. K., Weil, G. J., Sylvester, S., and DeMaria, M. A. (1996). Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum. Proc. Natl. Acad. Sci. USA 93, 705–708.
| Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnslOlsQ%3D%3D&md5=30d947d7693f522e06f3d8dd91ee5feeCAS | 8570620PubMed |
Billingham, R. E., Silvers, W. K., and Wilson, D. B. A. (1965). Second study on the H-Y transplantation antigen in mice. Proc. R. Soc. Lond. B Biol. Sci. 163, 61–89.
| Second study on the H-Y transplantation antigen in mice.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF2M7ktleqsQ%3D%3D&md5=f36c0378a5aa94bff905c327105313b8CAS | 14338494PubMed |
Blois, S., Alba Soto, C., Olmos, S., Chuluyán, E., Gentile, T., Arck, P., and Margni, R. (2004). Therapy with dendritic cells influences the spontaneous resoprtion rate in the CBA/J × DBA/2J mouse model. Am. J. Reprod. Immunol. 51, 40–48.
| Therapy with dendritic cells influences the spontaneous resoprtion rate in the CBA/J × DBA/2J mouse model.Crossref | GoogleScholarGoogle Scholar | 14725565PubMed |
Brunelli, R., Frasca, D., Baschieri, S., Spano, M., Fattorossi, A., Mosiello, L. F., Dámelio, R., Zichella, L., and Doria, G. (1992). Changes in thymocyte subsets induced by estradiol administration or pregnancy. Ann. N. Y. Acad. Sci. 650, 109–114.
| Changes in thymocyte subsets induced by estradiol administration or pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XltVCmsbs%3D&md5=39a2384b71dad47df7e1e405370e52a4CAS | 1351374PubMed |
Chafetz, I., Kuhnreich, I., Sammar, M., Tal, Y., Gibor, Y., Meiri, H., Cuckle, H., and Wolf, M. (2007). First-trimester placental protein 13 screening for preeclampsia and intrauterine growth restriction. Am. J. Obstet. Gynecol. 35, 1–7.
| First-trimester placental protein 13 screening for preeclampsia and intrauterine growth restriction.Crossref | GoogleScholarGoogle Scholar |
Chambers, S. P., and Clarke, A. G. (1979). Measurement of thymus weight, lumbar node weight and progesterone levels in syngeneically pregnant, allogeneically pregnant, and pseudopregnant mice. J. Reprod. Fertil. 55, 309–315.
| Measurement of thymus weight, lumbar node weight and progesterone levels in syngeneically pregnant, allogeneically pregnant, and pseudopregnant mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXitVWnurw%3D&md5=40d9712f4660f5c0615a9f20d6458e4dCAS | 439064PubMed |
Chaouat, G., Fowlkes, B. J., Leiserson, W. L., and Asofsky, R. (1982). Modification of thymocytes subsets during pregnancy analysed by flow microfluorometry: role of the alloantigenic status of the conceptus. Thymus 4, 299–308.
| 1:STN:280:DyaL3s%2FpsVemsw%3D%3D&md5=8c11fb8e3c7be1525a4b7dec12db0756CAS | 6983746PubMed |
Chaouat, G., Petitbarat, M., Dubanchet, S., Rahmati, M., and Ledé, N. (2010). Tolerance to the foetal allograft? Am. J. Reprod. Immunol. 63, 624–636.
| Tolerance to the foetal allograft?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXot1Kjtbw%3D&md5=d370459fcd39e71a15ca1bddc03b4239CAS | 20367624PubMed |
Chaplin, D. D. (2003). Overview of the immune response. J. Allergy Clin. Immunol. 111, 442–459.
| Overview of the immune response.Crossref | GoogleScholarGoogle Scholar |
Chavez, D. J., McIntyre, J. A., Colliver, J. A., and Faulk, W. P. (1987). Allogeneic matings and immunization have different effects on nulliparous and multiparous mice. J. Immunol. 139, 85–88.
| 1:STN:280:DyaL2s3isVWrsQ%3D%3D&md5=4634a8f7eb3996a03215761434b21f27CAS | 3584989PubMed |
Clark, D. A., Dermatt, M. R., and Szewezuk, M. R. (1980). Impairment of host-vs-graft reaction in pregnant mice. II. Selective suppression of cytotoxic T-cell generation correlates with soluble suppressor activity and with successful allogeneic pregnancy. Cell. Immunol. 52, 106–118.
| Impairment of host-vs-graft reaction in pregnant mice. II. Selective suppression of cytotoxic T-cell generation correlates with soluble suppressor activity and with successful allogeneic pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c3it12jug%3D%3D&md5=6d91046839d13c786329f48e6511f8faCAS | 6446406PubMed |
Clark, D. A., Chaput, A., and Tutton, D. (1986). Active suppression of host-vs-graft reaction in pregnant mice. VII. Spontaneous abortion of allogeneic CBA/J × DBA/2 fetuses in the uterus of CBA/J mice correlates with deficient non-T suppressor cell activity. J. Immunol. 136, 1668–1675.
| 1:STN:280:DyaL287ktFOhuw%3D%3D&md5=ab34d1a626fade136bbbc9c78f8daad1CAS | 2936806PubMed |
Clarke, A. G., and Miller, N. G. A. (1991). Major thymocyte subpopulations of the thymus in pregnant mice using flow cytometry. In ‘Lymphatic Tissues and In Vivo Immune Responses’. (Eds B. A. Imhof, S. Berrih-Aknin and S. Ezine.) pp. 189–198. (Marcel Dekker: New York.)
Dixon, M. E., Chien, E. K., Osol, G., Callas, W., and Bonney, E. A. (2006). Failure of decidual arteriolar remodeling in the CBA/J × DBA/2 murine model of recurrent pregnancy loss is linked to increased expression of tissue inhibitor of metalloproteinase 2 (TIMP-2). Am. J. Obstet. Gynecol. 194, 113–119.
| Failure of decidual arteriolar remodeling in the CBA/J × DBA/2 murine model of recurrent pregnancy loss is linked to increased expression of tissue inhibitor of metalloproteinase 2 (TIMP-2).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFehuw%3D%3D&md5=70ae787e4042bd494a1b6fa948e7853eCAS | 16389019PubMed |
Fontenot, J. D., Gavin, M. A., and Rudensky, A. Y. (2003). FoxP3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4, 330–336.
| FoxP3 programs the development and function of CD4+CD25+ regulatory T cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitlyqs74%3D&md5=e75f0450126d1c93b2822c8ac1a7911eCAS | 12612578PubMed |
Gendron, R. L., Farookhi, R., and Baines, M. G. (1990). Resoprtion of CBA/J × DBA/2 mouse conceptuses in CBA/J uteri correlates with failure of the feto-placental unit to suppress natural killer cell activity. J. Reprod. Fertil. 89, 277–284.
| Resoprtion of CBA/J × DBA/2 mouse conceptuses in CBA/J uteri correlates with failure of the feto-placental unit to suppress natural killer cell activity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3czisFWlug%3D%3D&md5=d32b0d9b018f5723c6e2bc596dc5f50eCAS | 2374121PubMed |
Gilpin, B. J., Loechel, F., Mattei, M. G., Engvall, E., Albrechtsen, R., and Wewer, U. M. (1998). A novel, secreted form of human ADAM 12 (meltrin α) provokes myogenesis in vivo. J. Biol. Chem. 273, 157–166.
| 1:CAS:528:DyaK1cXjvFShtw%3D%3D&md5=a47f58c575b7d702a139fe972d4111b7CAS | 9417060PubMed |
Herzenberg, L. A., Bianchi, D. W., Schröder, J., Cann, H. M., and Iverson, G. M. (1979). Fetal cells in the blood of pregnant women: detection and enrichment by fluorescence-activated cell sorting. Proc. Natl Acad. Sci. USA 76, 1453–1455.
| Fetal cells in the blood of pregnant women: detection and enrichment by fluorescence-activated cell sorting.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1M7otVajuw%3D%3D&md5=a89d95414114ff361c24efb713dc737bCAS | 286330PubMed |
Hirokawa, K., Sato, K., and Makinodan, T. (1982). Influence of age of thymic graft on the differentiation of T cells in nude mice. Clin. Immunol. Immunopathol. 24, 251–262.
| Influence of age of thymic graft on the differentiation of T cells in nude mice.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3s%2Fgt1ClsQ%3D%3D&md5=24e9cb6c108a2b00781ff5929f6a2b1cCAS | 6981482PubMed |
Hirokawa, K., Utsuyama, M., Kasai, M., Kurashima, C., Ishijima, S., and Zeng, Y. X. (1994). Understanding the mechanism of the age change of thymic involution to promote T cell differentiation. Immunol. Lett. 40, 269–277.
| Understanding the mechanism of the age change of thymic involution to promote T cell differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmt1yjsbg%3D&md5=0d2ebe8f6c1d3da5307c70f72ae0d1caCAS | 7959895PubMed |
Hori, S., Nomura, T., and Sakaguchi, S. (2003). Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057–1061.
| Control of regulatory T cell development by the transcription factor Foxp3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFarsbw%3D&md5=c2688090f39da951ae076d3a0817983cCAS | 12522256PubMed |
James, E., Chai, J. G., Dewchand, H., Macchiarulo, E., Dazzi, F., and Simpson, E. (2003). Multiparity induces priming to male-specific minor histocompatibility antigen, HY, in mice and humans. Blood 102, 388–393.
| Multiparity induces priming to male-specific minor histocompatibility antigen, HY, in mice and humans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltFels70%3D&md5=87d62d800365394d83813e9861fb9704CAS | 12649154PubMed |
Kallikourdis, M., Andersen, K. G., Welch, K. A., and Betz, A. G. (2007). Alloantigen-enhanced accumulation of CCR5+ ‘effector’ regulatory T cells in the gravid uterus. Proc. Natl Acad. Sci. USA 104, 594–599.
| Alloantigen-enhanced accumulation of CCR5+ ‘effector’ regulatory T cells in the gravid uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXovFaqtg%3D%3D&md5=615167cba23e1d6262988d02f8277927CAS | 17197426PubMed |
Kendall, M. D., and Clarke, A. G. (2000). The thymus in the mouse changes its activity during pregnancy: a study of the microenvironment. J. Anat. 197, 393–411.
| The thymus in the mouse changes its activity during pregnancy: a study of the microenvironment.Crossref | GoogleScholarGoogle Scholar | 11117626PubMed |
Khattri, R., Cox, T., Yasayko, S. A., and Ramsdell, F. (2003). An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat. Immunol. 4, 337–342.
| An essential role for Scurfin in CD4+CD25+ T regulatory cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitlyqs7s%3D&md5=e551444fbbd2942a3cb70fe2e511c4a7CAS | 12612581PubMed |
Khosrotehrani, K., Leduc, M., Bachy, V., Nguyen Huu, S., Oster, M., Abbas, A., Uzan, S., and Aractingi, S. (2008). Pregnancy allows the transfer and differentiation of fetal lymphoid progenitors into functional T and B cells in mothers. J. Immunol. 180, 889–897.
| 1:CAS:528:DC%2BD1cXhsVyhtA%3D%3D&md5=9eac5684c659a53f953f0846d6533d9cCAS | 18178828PubMed |
Kiger, N., Chaouat, G., Kolb, J. P., Wegmann, T. G., and Guenet, J. L. (1985). Immunogenetic studies of spontaneous abortion in mice. Preimmunization of females with allogeneic cells. J. Immunol. 134, 2966–2970.
| 1:STN:280:DyaL2M7lvFSjsg%3D%3D&md5=1dd5e0bb6f5b6e7fe824e27e85502983CAS | 3980987PubMed |
Liégois, A., Gaillard, M. C., Ouvre, E., and Lewin, D. (1981). Microchimerism in pregnant mice. Transplant. Proc. 13, 1250–1252.
Litwin, S., Lagadari, M., Barrientos, G., Roux, M. E., Margni, R., and Miranda, S. (2005). Comparative immunohistochemical study of M-CSF and G-CSF in feto–maternal interface in a multiparity mouse model. Am. J. Reprod. Immunol. 54, 311–320.
| Comparative immunohistochemical study of M-CSF and G-CSF in feto–maternal interface in a multiparity mouse model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1Sgsg%3D%3D&md5=f0cad478460cc9df7ac68c60280f6d8cCAS | 16212652PubMed |
Litwin, S., Cortina, M. E., Barrientos, G. L., Prados, M. B., Roux, M. E., and Miranda, S. E. (2010). Multiparity increases trophoblast invasion and vascular endothelial growth factor expression at the maternal–fetal interface in mice. J. Reprod. Immunol. 85, 161–167.
| Multiparity increases trophoblast invasion and vascular endothelial growth factor expression at the maternal–fetal interface in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntlGhtL8%3D&md5=f2e7def16dd09109cb1ee1b945d4c507CAS | 20462640PubMed |
Meeusen, E., Fox, A., Brandon, M., and Lee, C. S. (1993). Activation of uterine intraepithelial γδT cell receptor-positive lymphocytes during pregnancy. Eur. J. Immunol. 23, 1112–1117.
| Activation of uterine intraepithelial γδT cell receptor-positive lymphocytes during pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s3jvVylug%3D%3D&md5=6b5b6fd15f609885f54e2e0ac7c405faCAS | 8477805PubMed |
Miranda, S., Malán Borel, I., and Margni, R. (1998). Altered modulation of the in vitro antibody synthesis by placental factors from the CBA/J × DBA/2 abortion-prone mating combination. Am. J. Reprod. Immunol. 39, 341–349.
| Altered modulation of the in vitro antibody synthesis by placental factors from the CBA/J × DBA/2 abortion-prone mating combination.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3msV2lsQ%3D%3D&md5=09aa06fee35a0e08b9dad440a62524c4CAS | 9602253PubMed |
Pepper, F. J. (1961). The effect of age, pregnancy and lactation on the thymus gland and lymph nodes of the mouse. J. Endocrinol. 22, 335–348.
| The effect of age, pregnancy and lactation on the thymus gland and lymph nodes of the mouse.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF3c%2FltlyhsA%3D%3D&md5=6c9b2b1c7f4f1b8b9b506cd83a3a0604CAS | 13734178PubMed |
Persike, E. C. (1940). Involution of thymus during pregnancy in young mice. Proc. Soc. Exp. Biol. Med. 45, 315–317.
Phuc, L. H., Papiernik, M., Berrih, S., and Duval, D. (1981). Thymic involution in pregnant mice. I. Characterization of the remaining thymocyte subpopulations. Clin. Exp. Immunol. 44, 247–252.
| 1:STN:280:DyaL38%2FntVyrtQ%3D%3D&md5=d8c3b7a6f485646c898f0b7684ecf526CAS | 6975672PubMed |
Prados, M. B., Solano, M. E., Friebe, A., Blois, A., Arck, P., and Miranda, S. (2011). Stress increases VCAM-1 expression at the fetomaternal interface in an abortion-prone mouse model. J. Reprod. Immunol. 89, 207–211.
| Stress increases VCAM-1 expression at the fetomaternal interface in an abortion-prone mouse model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVWkur4%3D&md5=ef7dc21372328d599051ed8619ad739dCAS | 21529964PubMed |
Sahraravand, M., Järvelä, I. Y., Laitinen, P., Tekay, A. H., and Ryynänen, M. (2011). The secretion of PAPP-A, ADAM12, and PP13 correlates with the size of the placenta for the first month of pregnancy. Placenta 32, 999–1003.
| The secretion of PAPP-A, ADAM12, and PP13 correlates with the size of the placenta for the first month of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFGjt7bN&md5=6fff5acec4b1dc17373790d223e786d3CAS | 22015022PubMed |
Sasaki, Y., Sakai, M., Miyazaki, S., Higuma, S., Shiozaki, A., and Saito, S. (2004). Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol. Hum. Reprod. 10, 347–353.
| Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c7pslOkug%3D%3D&md5=104e3201776499fe21e4bb00b3b3be9fCAS | 14997000PubMed |
Savion, S., and Toder, V. (1995). Pregnancy associated effects on mouse thymocytes in vitro. Cell. Immunol. 162, 282–287.
| Pregnancy associated effects on mouse thymocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXls1Kqur8%3D&md5=288dd8da38f1842209d1c5d39fd4c0d8CAS | 7743556PubMed |
Shi, Z., Xu, W., Loechel, F., Wewer, U. M., and Murphy, L. J. (2000). ADAM 12, a disintegrin metalloprotease, interacts with insulin-like growth factor-binding protein-3. J. Biol. Chem. 275, 18 574–18 580.
| 1:CAS:528:DC%2BD3cXktlyls7c%3D&md5=5ccbb76039b636dd2583160697a74bf2CAS |
Simpson, E., Benjamin, D., and Chandler, P. (1981). Nonresponsiveness to H-Y: tolerance in H-2b mice. Transplant. Proc. 13, 1880–1883.
| 1:STN:280:DyaL387jtVamtQ%3D%3D&md5=18c132ba806145dbe9f9ad58e69d8114CAS | 7036481PubMed |
Smith, R. N., and Powell, A. E. (1977). The adoptive transfer of pregnancy-induced unresponsiveness to male skin grafts with thymus-dependent cells. J. Exp. Med. 146, 899–904.
| The adoptive transfer of pregnancy-induced unresponsiveness to male skin grafts with thymus-dependent cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s3ltFejuw%3D%3D&md5=952915c1ccf5085affe77d2ae698ef67CAS | 330791PubMed |
Stutman, O., and Good, R. A. (1974). Duration of thymic function. Ser. Haematol. 7, 505–523.
| 1:STN:280:DyaE2M7itFyqug%3D%3D&md5=8534f73c29fdfabb4d0f8ce5f611ea27CAS | 4616336PubMed |
Szekeres-Bartho, J., Barakonyi, A., Polgar, B., Par, G., Faust, Z. S., Palkovics, T., and Szereday, L. (1999). The role of γ/δT cells in progesterone-mediated immunomodulation during pregnancy. Am. J. Reprod. Immunol. 42, 44–48.
| The role of γ/δT cells in progesterone-mediated immunomodulation during pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MzlvVeqtQ%3D%3D&md5=c4a011445f9112aecf6eb33ba2350dfbCAS | 10429766PubMed |
Szekeres-Bartho, J., Barakonyi, A., Miko, E., Polgar, B., and Palkovics, T. (2001). The role of γδT cells in the feto–maternal relationship. Semin. Immunol. 13, 229–233.
| The role of γδT cells in the feto–maternal relationship.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvVOkuro%3D&md5=81f263fda1c907c6e2d76d05e6ecce2aCAS | 11437630PubMed |
Tafuri, A., Alferink, J., Möller, P., Hämmerling, G. J., and Arnold, B. (1995). T cell awareness of paternal alloantigens during pregnancy. Science 270, 630–633.
| T cell awareness of paternal alloantigens during pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovFGrsrY%3D&md5=02a97edc127373485b30c501eafe6d97CAS | 7570020PubMed |
Tibbetts, T. A., DeMayo, F., Rich, S., Conneely, O. M., and O’Malley, B. W. (1999). Progesterone receptors in the thymus are required for thymic involution during pregnancy and for normal fertility. Proc. Natl. Acad. Sci. USA 96, 12 021–12 026.
| Progesterone receptors in the thymus are required for thymic involution during pregnancy and for normal fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvVGjsbw%3D&md5=10b301c777ac40844cb842c5aaf0eb24CAS |
Vallejo, A. N., Michel, J. J., Bale, L. K., Lemster, B. H., Borghesi, L., and Conover, C. A. (2009). Resistance to age-dependent thymic atrophy in long-lived mice that are deficient in pregnancy-associated plasma protein A. Proc. Natl Acad. Sci. USA 106, 11 252–11 257.
| Resistance to age-dependent thymic atrophy in long-lived mice that are deficient in pregnancy-associated plasma protein A.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptVWlsLg%3D&md5=d65091ce7c811c5915fa03f3c68263d1CAS |
Vernochet, C., Caucheteux, S. M., and Kanellopoulos-Langevin, C. (2007). Bi-directional cell trafficking between mother and fetus in mouse placenta. Placenta 28, 639–649.
| Bi-directional cell trafficking between mother and fetus in mouse placenta.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2szktlOhsw%3D%3D&md5=232c43deccac58d6ed9dc93fee9a9fd5CAS | 17116327PubMed |
Zenclussen, A. C., Gerlof, K., Zenclussen, M. L., Sollwedel, A., Bertoja, A. Z., Ritter, T., Kotsch, K., Leber, J., and Volk, H. D. (2005). Abnormal T-cell reactivity against paternal antigens in spontaneous abortion: adoptive transfer of pregnancy-induced CD4+CD25+ T regulatory cells prevents fetal rejection in a murine abortion model. Am. J. Pathol. 166, 811–822.
| Abnormal T-cell reactivity against paternal antigens in spontaneous abortion: adoptive transfer of pregnancy-induced CD4+CD25+ T regulatory cells prevents fetal rejection in a murine abortion model.Crossref | GoogleScholarGoogle Scholar | 15743793PubMed |
Zoller, A. L., and Kersh, G. J. (2006). Estrogen induces thymic atrophy by eliminating early thymic progenitors and inhibiting proliferation of beta-selected thymocytes. J. Immunol. 176, 7371–7378.
| 1:CAS:528:DC%2BD28Xlt1Clu78%3D&md5=1cd1f7132f4089403b48e48bc84ca705CAS | 16751381PubMed |
Zoller, A. L., Schnell, F. J., and Kersh, G. (2007). Murine pregnancy leads to reduced proliferation of maternal thymocytes and decreased thymic emigration. J. Immunol. 121, 207–215.
| Murine pregnancy leads to reduced proliferation of maternal thymocytes and decreased thymic emigration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1eqs7w%3D&md5=b0ffeb27925a69907c0211cb11e7499aCAS |