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Current Molecular Pharmacology

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ISSN (Print): 1874-4672
ISSN (Online): 1874-4702

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Research Article

Evaluation of the Effects of 1,25 Vitamin D3 on Regulatory T Cells and T Helper 17 Cells in Vitamin D-deficient Women with Unexplained Recurrent Pregnancy Loss

Author(s): Elham Abdollahi, Seyed Abdolrahim Rezaee, Nafiseh Saghafi, Maryam Rastin, Vicki Clifton, Amirhossein Sahebkar and Houshang Rafatpanah*

Volume 13, Issue 4, 2020

Page: [306 - 317] Pages: 12

DOI: 10.2174/1874467213666200303130153

Price: $65

Abstract

Background: Vitamin D insufficiency and deficiency can be associated with adverse effects on pregnancy outcomes, which may include recurrent pregnancy loss through the mechanisms that are yet unknown. The aim of this study was to evaluate the effect of 1,25VitD3 on regulatory T cells (Tregs) and T helper17 (Th17) cell populations In vitro in unexplained recurrent pregnancy loss (URPL) patients and healthy women.

Methods: Samples from 20 non-pregnant women with a history of URPL were compared to 20 normal non-pregnant women. Peripheral blood mononuclear cells (PBMC) were divided into 3 wells for each subject: in the presence of 1, 25 VitD3 (50 nM, for 16 hours), PHA (positive control) (10μM), and without any treatment (as a baseline or negative control). The percentage of regulatory T cells and Th17 cells was measured by flow cytometry at baseline and then after cell culture experiments.

Results: Our study indicated that the percentage of Tregs in patients with URPL was significantly lower than the control group (2.42 ± 0.27 vs. 3.41 ± 0.29, P= 0.01). The percentage of Th17 cells was significantly greater in URPL patients compared to the control group (2.91 ± 0.33 vs. 1.18± 0.15, P=0.001). 1, 25VitD3 treatment significantly increased the percentage of Tregs from the baseline in the URPL group compared to that in the control group (1.23 ± 0.03 vs. 1.00 ± 0.03, P= 0.01).

Conclusion: Vitamin D deficiency may be a contributor to recurrent pregnancy loss and suggests supplementation of women with Vit D pre-pregnancy may be protective against URPL.

Keywords: Recurrent Pregnancy Loss, tregs, Th17 cells, 1, 25vitD3, cell culture, cytometry analysis.

Graphical Abstract

[1]
Rai, R.; Regan, L. Recurrent miscarriage. Lancet, 2006, 368(9535), 601-611.
[http://dx.doi.org/10.1016/S0140-6736(06)69204-0] [PMID: 16905025]
[2]
Heuser, C; Dalton, J; Macpherson, C; Branch, DW; Porter, TF; Silver, R.M. Idiopathic recurrent pregnancy loss recurs at similar gestational ages. Am. J. Obstetrics and Gynecology, 2010, 203(4), 343-e1-5.
[3]
Aluvihare, V.R.; Kallikourdis, M.; Betz, A.G. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol., 2004, 5(3), 266-271.
[http://dx.doi.org/10.1038/ni1037] [PMID: 14758358]
[4]
Guerin, L.R.; Prins, J.R.; Robertson, S.A. Regulatory T-cells and immune tolerance in pregnancy: a new target for infertility treatment? Hum. Reprod. Update, 2009, 15(5), 517-535.
[http://dx.doi.org/10.1093/humupd/dmp004] [PMID: 19279047]
[5]
Pei, C-Z.; Kim, Y.J.; Baek, K-H. Pathogenetic factors involved in recurrent pregnancy loss from multiple aspects. Obstet. Gynecol. Sci., 2019, 62(4), 212-223.
[http://dx.doi.org/10.5468/ogs.2019.62.4.212] [PMID: 31338338]
[6]
Kanannejad, Z.; Jahromi, B.N.; Gharesi-Fard, B. T Cell Subsets Profiling in Unexplained Infertile Women with Successful and Unsuccessful in Vitro Fertilization Outcome: Focus on the Effect of Seminal Plasma. Iran. J. Allergy Asthma Immunol., 2019, 18(2), 163-172.
[7]
Tsuda, S.; Nakashima, A.; Shima, T.; Saito, S. New Paradigm in the Role of Regulatory T Cells During Pregnancy. Front. Immunol., 2019, 10, 573.
[http://dx.doi.org/10.3389/fimmu.2019.00573] [PMID: 30972068]
[8]
Lastovicka, J. The phenotypic markers of CD4+ CD25+ T regulatory lymphocytes. Res. Immunol., 2013, 2013, 1-14.
[9]
Tang, Q.; Bluestone, J.A. The Foxp3+ regulatory T cell: a jack of all trades, master of regulation. Nat. Immunol., 2008, 9(3), 239-244.
[http://dx.doi.org/10.1038/ni1572] [PMID: 18285775]
[10]
Deshmukh, H.; Way, S.S. Immunological basis for recurrent fetal loss and pregnancy complications. Annu. Rev. Pathol., 2019, 14, 185-210.
[http://dx.doi.org/10.1146/annurev-pathmechdis-012418-012743] [PMID: 30183507]
[11]
Corthay, A. How do regulatory T cells work? Scand. J. Immunol., 2009, 70(4), 326-336.
[http://dx.doi.org/10.1111/j.1365-3083.2009.02308.x] [PMID: 19751267]
[12]
Vignali, D.A.; Collison, L.W.; Workman, C.J. How regulatory T cells work. Nat. Rev. Immunol., 2008, 8(7), 523-532.
[http://dx.doi.org/10.1038/nri2343] [PMID: 18566595]
[13]
Aluvihare, V.R.; Betz, A.G. The role of regulatory T cells in materno-fetal tolerance.Immunol. Pregnancy; , 2006, pp. pp. 171-178.
[14]
Saito, S.; Nakashima, A.; Shima, T.; Ito, M. Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am. J. Reprod. Immunol., 2010, 63(6), 601-610.
[http://dx.doi.org/10.1111/j.1600-0897.2010.00852.x] [PMID: 20455873]
[15]
Korn, T.; Bettelli, E.; Oukka, M.; Kuchroo, V.K. IL-17 and Th17 Cells. Annu. Rev. Immunol., 2009, 27, 485-517.
[http://dx.doi.org/10.1146/annurev.immunol.021908.132710] [PMID: 19132915]
[16]
Noack, M.; Miossec, P. Th17 and regulatory T cell balance in autoimmune and inflammatory diseases. Autoimmun. Rev., 2014, 13(6), 668-677.
[http://dx.doi.org/10.1016/j.autrev.2013.12.004] [PMID: 24418308]
[17]
Lee, S.K.; Kim, J.Y.; Lee, M.; Gilman-Sachs, A.; Kwak-Kim, J. Th17 and regulatory T cells in women with recurrent pregnancy loss. Am. J. Reprod. Immunol., 2012, 67(4), 311-318.
[http://dx.doi.org/10.1111/j.1600-0897.2012.01116.x] [PMID: 22380579]
[18]
Wang, W-J.; Hao, C-F. Yi-Lin.; Yin, G.J.; Bao, S.H.; Qiu, L.H.; Lin, Q.D. Increased prevalence of T helper 17 (Th17) cells in peripheral blood and decidua in unexplained recurrent spontaneous abortion patients. J. Reprod. Immunol., 2010, 84(2), 164-170.
[http://dx.doi.org/10.1016/j.jri.2009.12.003] [PMID: 20106535]
[19]
Abdollahi, E.; Tavasolian, F.; Ghasemi, N.; Mirghanizadeh, S.A.; Azizi, M.; Ghoryani, M.; Samadi, M. Association between lower frequency of R381Q variant (rs11209026) in IL-23 receptor gene and increased risk of recurrent spontaneous abortion (RSA). J. Immunotoxicol., 2015, 12(4), 317-321.
[http://dx.doi.org/10.3109/1547691X.2014.978056] [PMID: 26269135]
[20]
Abdollahi, E.; Tavasolian, F.; Momtazi-Borojeni, A.A.; Samadi, M.; Rafatpanah, H. Protective role of R381Q (rs11209026) polymorphism in IL-23R gene in immune-mediated diseases: A comprehensive review. J. Immunotoxicol., 2016, 13(3), 286-300.
[http://dx.doi.org/10.3109/1547691X.2015.1115448] [PMID: 27043356]
[21]
Liu, Y.S.; Wu, L.; Tong, X.H.; Wu, L.M.; He, G.P.; Zhou, G.X.; Luo, L.H.; Luan, H.B. Study on the relationship between Th17 cells and unexplained recurrent spontaneous abortion. Am. J. Reprod. Immunol., 2011, 65(5), 503-511.
[http://dx.doi.org/10.1111/j.1600-0897.2010.00921.x] [PMID: 21029245]
[22]
Hosseini, S.; Shokri, F.; Ansari Pour, S.; Jeddi-Tehrani, M.; Nikoo, S.; Yousefi, M.; Zarnani, A.H. A shift in the balance of T17 and Treg cells in menstrual blood of women with unexplained recurrent spontaneous abortion. J. Reprod. Immunol., 2016, 116, 13-22.
[http://dx.doi.org/10.1016/j.jri.2016.03.001] [PMID: 27128988]
[23]
Bettelli, E.; Carrier, Y.; Gao, W.; Korn, T.; Strom, T.B.; Oukka, M.; Weiner, H.L.; Kuchroo, V.K. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature, 2006, 441(7090), 235-238.
[http://dx.doi.org/10.1038/nature04753] [PMID: 16648838]
[24]
Yang, H.; Qiu, L.; Chen, G.; Ye, Z.; Lü, C.; Lin, Q. Proportional change of CD4+CD25+ regulatory T cells in decidua and peripheral blood in unexplained recurrent spontaneous abortion patients. Fertil. Steril., 2008, 89(3), 656-661.
[http://dx.doi.org/10.1016/j.fertnstert.2007.03.037] [PMID: 17543960]
[25]
Somerset, D.A.; Zheng, Y.; Kilby, M.D.; Sansom, D.M.; Drayson, M.T. Normal human pregnancy is associated with an elevation in the immune suppressive CD25+ CD4+ regulatory T-cell subset. Immunology, 2004, 112(1), 38-43.
[http://dx.doi.org/10.1111/j.1365-2567.2004.01869.x] [PMID: 15096182]
[26]
Lee, S.K.; Kim, J.Y.; Hur, S.E.; Kim, C.J.; Na, B.J.; Lee, M.; Gilman-Sachs, A.; Kwak-Kim, J. An imbalance in interleukin-17-producing T and Foxp3+ regulatory T cells in women with idiopathic recurrent pregnancy loss. Hum. Reprod., 2011, 26(11), 2964-2971.
[http://dx.doi.org/10.1093/humrep/der301] [PMID: 21926059]
[27]
Wang, W-J.; Hao, C-F.; Qu, Q-L.; Wang, X.; Qiu, L-H.; Lin, Q-D. The deregulation of regulatory T cells on interleukin-17-producing T helper cells in patients with unexplained early recurrent miscarriage. Hum. Reprod., 2010, 25(10), 2591-2596.
[http://dx.doi.org/10.1093/humrep/deq198] [PMID: 20685755]
[28]
Sasaki, Y.; Sakai, M.; Miyazaki, S.; Higuma, S.; Shiozaki, A.; Saito, S. Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol. Hum. Reprod., 2004, 10(5), 347-353.
[http://dx.doi.org/10.1093/molehr/gah044] [PMID: 14997000]
[29]
Mei, S.; Tan, J.; Chen, H.; Chen, Y.; Zhang, J. Changes of CD4+CD25high regulatory T cells and FOXP3 expression in unexplained recurrent spontaneous abortion patients. Fertil. Steril., 2010, 94(6), 2244-2247.
[http://dx.doi.org/10.1016/j.fertnstert.2009.11.020] [PMID: 20056219]
[30]
Wu, L.; Luo, L-H.; Zhang, Y-X.; Li, Q.; Xu, B.; Zhou, G-X.; Luan, H.B.; Liu, Y.S. Alteration of Th17 and Treg cells in patients with unexplained recurrent spontaneous abortion before and after lymphocyte immunization therapy. Reprod. Biol. Endocrinol., 2014, 12(1), 74.
[http://dx.doi.org/10.1186/1477-7827-12-74] [PMID: 25086467]
[31]
Nakashima, A.; Ito, M.; Shima, T.; Bac, N.D.; Hidaka, T.; Saito, S. Accumulation of IL-17-positive cells in decidua of inevitable abortion cases. Am. J. Reprod. Immunol., 2010, 64(1), 4-11.
[http://dx.doi.org/10.1111/j.1600-0897.2010.00812.x] [PMID: 20219063]
[32]
Heyden, E.L.; Wimalawansa, S.J.; Vitamin, D.; Vitamin, D. Effects on human reproduction, pregnancy, and fetal well-being. J. Steroid Biochem. Mol. Biol., 2018, 180, 41-50.
[http://dx.doi.org/10.1016/j.jsbmb.2017.12.011] [PMID: 29262380]
[33]
Prosser, D.E.; Jones, G. Enzymes involved in the activation and inactivation of vitamin D. Trends Biochem. Sci., 2004, 29(12), 664-673.
[http://dx.doi.org/10.1016/j.tibs.2004.10.005] [PMID: 15544953]
[34]
Dabrowski, F.A.; Grzechocinska, B.; Wielgos, M. The role of vitamin D in reproductive health--a Trojan Horse or the Golden Fleece? Nutrients, 2015, 7(6), 4139-4153.
[http://dx.doi.org/10.3390/nu7064139] [PMID: 26035242]
[35]
Luk, J.; Torrealday, S.; Neal Perry, G.; Pal, L. Relevance of vitamin D in reproduction. Hum. Reprod., 2012, 27(10), 3015-3027.
[http://dx.doi.org/10.1093/humrep/des248] [PMID: 22824625]
[36]
Gonçalves, D.R.; Braga, A.; Braga, J.; Marinho, A. Recurrent pregnancy loss and vitamin D: A review of the literature. Am. J. Reprod. Immunol., 2018, 80(5), e13022.
[http://dx.doi.org/10.1111/aji.13022] [PMID: 30051540]
[37]
Vijayendra Chary, A.; Hemalatha, R.; Seshacharyulu, M.; Vasudeva Murali, M.; Jayaprakash, D.; Dinesh Kumar, B. Vitamin D deficiency in pregnant women impairs regulatory T cell function. J. Steroid Biochem. Mol. Biol., 2015, 147, 48-55.
[http://dx.doi.org/10.1016/j.jsbmb.2014.11.020] [PMID: 25448751]
[38]
Blomberg Jensen, M.; Gerner Lawaetz, J.; Andersson, A-M.; Petersen, J.H.; Nordkap, L.; Bang, A.K.; Ekbom, P.; Joensen, U.N.; Prætorius, L.; Lundstrøm, P.; Boujida, V.H.; Lanske, B.; Juul, A.; Jørgensen, N. Vitamin D deficiency and low ionized calcium are linked with semen quality and sex steroid levels in infertile men. Hum. Reprod., 2016, 31(8), 1875-1885.
[http://dx.doi.org/10.1093/humrep/dew152] [PMID: 27496946]
[39]
Young, B.E.; Cooper, E.M.; McIntyre, A.W.; Kent, T.; Witter, F.; Harris, Z.L.; O’Brien, K.O. Placental vitamin D receptor (VDR) expression is related to neonatal vitamin D status, placental calcium transfer, and fetal bone length in pregnant adolescents. FASEB J., 2014, 28(5), 2029-2037.
[http://dx.doi.org/10.1096/fj.13-246736] [PMID: 24558197]
[40]
Knabl, J.; Vattai, A.; Ye, Y.; Jueckstock, J.; Hutter, S.; Kainer, F.; Mahner, S.; Jeschke, U. Role of placental VDR expression and function in common late pregnancy disorders. Int. J. Mol. Sci., 2017, 18(11), 2340.
[http://dx.doi.org/10.3390/ijms18112340] [PMID: 29113124]
[41]
Shahbazi, M.; Jeddi-Tehrani, M.; Zareie, M.; Salek-Moghaddam, A.; Akhondi, M.M.; Bahmanpoor, M.; Sadeghi, M.R.; Zarnani, A.H. Expression profiling of vitamin D receptor in placenta, decidua and ovary of pregnant mice. Placenta, 2011, 32(9), 657-664.
[http://dx.doi.org/10.1016/j.placenta.2011.06.013] [PMID: 21764449]
[42]
Chang, S.H.; Chung, Y.; Dong, C. Vitamin D suppresses Th17 cytokine production by inducing C/EBP homologous protein (CHOP) expression. J. Biol. Chem., 2010, 285(50), 38751-38755.
[43]
Barad, D.H.; Kushnir, V.A.; Gleicher, N. Focus on recurrent miscarriage phenotypes. Fertil. Steril., 2017, 107(1), 64-65.
[http://dx.doi.org/10.1016/j.fertnstert.2016.10.034] [PMID: 27887715]
[44]
Lee, S.K.; Na, B.J.; Kim, J.Y.; Hur, S.E.; Lee, M.; Gilman-Sachs, A.; Kwak-Kim, J. Determination of clinical cellular immune markers in women with recurrent pregnancy loss. Am. J. Reprod. Immunol., 2013, 70(5), 398-411.
[http://dx.doi.org/10.1111/aji.12137] [PMID: 23656517]
[45]
Tavasolian, F.; Abdollahi, E.; Samadi, M. Association of the IL4R single-nucleotide polymorphism I50V with recurrent spontaneous abortion (RSA). J. Assist. Reprod. Genet., 2014, 31(7), 851-856.
[http://dx.doi.org/10.1007/s10815-014-0234-z] [PMID: 24803421]
[46]
Jørgensen, N.; Persson, G.; Hviid, T.V.F. The Tolerogenic Function of Regulatory T Cells in Pregnancy and Cancer. Front. Immunol., 2019, 10, 911.
[http://dx.doi.org/10.3389/fimmu.2019.00911] [PMID: 31134056]
[47]
Yang, F.; Zheng, Q.; Jin, L. Dynamic function and composition changes of immune cells during normal and pathological pregnancy at the maternal-fetal interface. Front. Immunol., 2019, 10, 2317.
[http://dx.doi.org/10.3389/fimmu.2019.02317] [PMID: 31681264]
[48]
Care, A.S.; Bourque, S.L.; Morton, J.S.; Hjartarson, E.P.; Robertson, S.A.; Davidge, S.T. Reduction in regulatory T cells in early pregnancy causes uterine artery dysfunction in mice. Hypertension, 2018, 72(1), 177-187.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.118.10858] [PMID: 29785960]
[49]
Pandey, M.K.; Thakur, S.; Agrawal, S. Lymphocyte immunotherapy and its probable mechanism in the maintenance of pregnancy in women with recurrent spontaneous abortion. Arch. Gynecol. Obstet., 2004, 269(3), 161-172.
[http://dx.doi.org/10.1007/s00404-003-0560-3] [PMID: 14652774]
[50]
Omwandho, C.A.; Tinneberg, H.R.; Tumbo-Oeri, A.G.; Roberts, T.K.; Falconer, J. Recurrent pregnancy losses and the role of immunotherapy. Arch. Gynecol. Obstet., 2000, 264(1), 3-12.
[http://dx.doi.org/10.1007/PL00007480] [PMID: 10985611]
[51]
La Rocca, C.; Carbone, F.; Longobardi, S.; Matarese, G. The immunology of pregnancy: regulatory T cells control maternal immune tolerance toward the fetus. Immunol. Lett., 2014, 162(1 Pt A), 41-48.
[http://dx.doi.org/10.1016/j.imlet.2014.06.013] [PMID: 24996040]
[52]
Pandey, M.K.; Rani, R.; Agrawal, S. An update in recurrent spontaneous abortion. Arch. Gynecol. Obstet., 2005, 272(2), 95-108.
[http://dx.doi.org/10.1007/s00404-004-0706-y] [PMID: 15906053]
[53]
Krieg, S.A.; Fan, X.; Hong, Y.; Sang, Q-X.; Giaccia, A.; Westphal, L.M.; Lathi, R.B.; Krieg, A.J.; Nayak, N.R. Global alteration in gene expression profiles of deciduas from women with idiopathic recurrent pregnancy loss. Mol. Hum. Reprod., 2012, 18(9), 442-450.
[http://dx.doi.org/10.1093/molehr/gas017] [PMID: 22505054]
[54]
Teles, A.; Thuere, C.; Wafula, P.O.; El-Mousleh, T.; Zenclussen, M.L.; Zenclussen, A.C. Origin of Foxp3(+) cells during pregnancy. Am. J. Clin. Exp. Immunol., 2013, 2(3), 222-233.
[55]
Jin, L-P.; Chen, Q-Y.; Zhang, T.; Guo, P-F.; Li, D-J. The CD4+CD25 bright regulatory T cells and CTLA-4 expression in peripheral and decidual lymphocytes are down-regulated in human miscarriage. Clin. Immunol., 2009, 133(3), 402-410.
[http://dx.doi.org/10.1016/j.clim.2009.08.009] [PMID: 19766059]
[56]
Saito, S.; Sasaki, Y.; Sakai, M. CD4(+)CD25high regulatory T cells in human pregnancy. J. Reprod. Immunol., 2005, 65(2), 111-120.
[http://dx.doi.org/10.1016/j.jri.2005.01.004] [PMID: 15811516]
[57]
Tilburgs, T.; Roelen, D.L.; van der Mast, B.J.; de Groot-Swings, G.M.; Kleijburg, C.; Scherjon, S.A.; Claas, F.H. Evidence for a selective migration of fetus-specific CD4+CD25bright regulatory T cells from the peripheral blood to the decidua in human pregnancy. J. Immunol., 2008, 180(8), 5737-5745.
[http://dx.doi.org/10.4049/jimmunol.180.8.5737] [PMID: 18390759]
[58]
Darmochwal-Kolarz, D.; Leszczynska-Gorzelak, B.; Rolinski, J.; Oleszczuk, J. The immunophenotype of patients with recurrent pregnancy loss. Eur. J. Obstet. Gynecol. Reprod. Biol., 2002, 103(1), 53-57.
[http://dx.doi.org/10.1016/S0301-2115(02)00025-8] [PMID: 12039464]
[59]
Vassiliadou, N.; Searle, R.F.; Bulmer, J.N. Immunoregulatory activity of decidua in spontaneous early pregnancy loss. Hum. Reprod., 1999, 14(9), 2252-2256.
[http://dx.doi.org/10.1093/humrep/14.9.2252] [PMID: 10469690]
[60]
Saito, S.; Sasaki, Y.; Sakai, M. CD4(+)CD25high regulatory T cells in human pregnancy. J. Reprod. Immunol., 2005, 65(2), 111-120.
[http://dx.doi.org/10.1016/j.jri.2005.01.004] [PMID: 15811516]
[61]
Jeffery, L.E.; Burke, F.; Mura, M.; Zheng, Y.; Qureshi, O.S.; Hewison, M.; Walker, L.S.; Lammas, D.A.; Raza, K.; Sansom, D.M. 1,25-Dihydroxyvitamin D3 and IL-2 combine to inhibit T cell production of inflammatory cytokines and promote development of regulatory T cells expressing CTLA-4 and FoxP3. J. Immunol., 2009, 183(9), 5458-5467.
[http://dx.doi.org/10.4049/jimmunol.0803217] [PMID: 19843932]
[62]
Bubanovic, I. 1α,25-dihydroxy-vitamin-D3 as new immunotherapy in treatment of recurrent spontaneous abortion. Med. Hypotheses, 2004, 63(2), 250-253.
[http://dx.doi.org/10.1016/j.mehy.2003.11.037] [PMID: 15236784]
[63]
Deluca, H.F.; Cantorna, M.T. Vitamin D: its role and uses in immunology. FASEB J., 2001, 15(14), 2579-2585.
[http://dx.doi.org/10.1096/fj.01-0433rev] [PMID: 11726533]
[64]
Tavakoli, M.; Jeddi-Tehrani, M.; Salek-Moghaddam, A.; Rajaei, S.; Mohammadzadeh, A.; Sheikhhasani, S.; Kazemi-Sefat, G.E.; Zarnani, A.H. Effects of 1,25(OH)2 vitamin D3 on cytokine production by endometrial cells of women with recurrent spontaneous abortion. Fertil. Steril., 2011, 96(3), 751-757.
[http://dx.doi.org/10.1016/j.fertnstert.2011.06.075] [PMID: 21880282]
[65]
Prots, I.; Skapenko, A.; Wendler, J.; Mattyasovszky, S.; Yoné, C.L.; Spriewald, B.; Burkhardt, H.; Rau, R.; Kalden, J.R.; Lipsky, P.E.; Schulze-Koops, H. Association of the IL4R single-nucleotide polymorphism I50V with rapidly erosive rheumatoid arthritis. Arthritis Rheum., 2006, 54(5), 1491-1500.
[http://dx.doi.org/10.1002/art.21832] [PMID: 16646030]
[66]
Zhao, A.; Liu, K.; Qi, Y. Natural killer T cells from peripheral blood of patients with pregnancy-induced hypertension inhibit the proliferation and migration of vascular endothelial cells by secreting interleukin-17. Biotechnol. Biotechnol. Equip., 2019, 1-12.
[http://dx.doi.org/10.1080/13102818.2019.1577698]
[67]
Rajaei, S.; Mirahmadian, M.; Jeddi-Tehrani, M.; Tavakoli, M.; Zonoobi, M.; Dabbagh, A.; Zarnani, A.H. Effect of 1,25(OH)2 vitamin D3 on cytokine production by endometrial cells of women with repeated implantation failure. Gynecol. Endocrinol., 2012, 28(11), 906-911.
[http://dx.doi.org/10.3109/09513590.2012.683062] [PMID: 22616713]
[68]
Nakashima, A.; Shima, T.; Inada, K.; Ito, M.; Saito, S. The balance of the immune system between T cells and NK cells in miscarriage. Am. J. Reprod. Immunol., 2012, 67(4), 304-310.
[http://dx.doi.org/10.1111/j.1600-0897.2012.01115.x] [PMID: 22364212]
[69]
Mandal, M.; Marzouk, A.C.; Donnelly, R.; Ponzio, N.M. Maternal immune stimulation during pregnancy affects adaptive immunity in offspring to promote development of TH17 cells. Brain Behav. Immun., 2011, 25(5), 863-871.
[http://dx.doi.org/10.1016/j.bbi.2010.09.011] [PMID: 20854892]
[70]
Peelen, E.; Knippenberg, S.; Muris, A-H.; Thewissen, M.; Smolders, J.; Tervaert, J.W.C.; Hupperts, R.; Damoiseaux, J. Effects of vitamin D on the peripheral adaptive immune system: a review. Autoimmun. Rev., 2011, 10(12), 733-743.
[http://dx.doi.org/10.1016/j.autrev.2011.05.002] [PMID: 21621002]
[71]
Rafiee, M.; Gharagozloo, M.; Ghahiri, A.; Mehrabian, F.; Maracy, M.R.; Kouhpayeh, S.; Pieper, I.L.; Rezaei, A. Altered Th17/Treg ratio in recurrent miscarriage after treatment with paternal lymphocytes and vitamin D3: a Double-Blind Placebo-Controlled study. Iran. J. Immunol., 2015, 12(4), 252-262.
[PMID: 26714417]

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