Immunological Response during Pregnancy in Humans and Mares
Abstract
:1. Introduction
2. Cell-Mediated Immune Response during a Healthy Pregnancy
2.1. NK Cells
2.2. Lymphocytes T
2.3. Macrophages
2.4. Other Antigen-Presenting Cells
3. Cytokine Response during Pregnancy
3.1. Systemic Cytokine Response
3.2. Local Cytokine and Hormonal Response
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Stokes, D.M.; Male, P.V. Immunolog; Elsevier Health Sciences: Amsterdam, The Netherlands, 2020. [Google Scholar]
- Dymarska, E. The factors modulating the human immune system. Zesz. Nauk. Państwowej Wyższej Szkoły Zawodowej Witelona W Legn. 2016, 19, 21–27. [Google Scholar]
- Trzeciak-Ryczek, A.; Tokarz-Deptuła, B.; Niedźwiedzka-Rystwej, P.; Deptuła, W. Adipose tissue—Component of the immune system. Cent.-Eur. J. Immunol. 2011, 36, 95–99. [Google Scholar]
- Trowsdale, J.; Betz, A.G. Mother’s little helpers: Mechanisms of maternal-fetal tolerance. Nat. Immunol. 2006, 7, 241–246. [Google Scholar] [CrossRef]
- Aluvihare, V.R.; Kallikourdis, M.; Betz, A.G. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 2004, 5, 266–271. [Google Scholar] [CrossRef] [PubMed]
- Weetman, A.P. The Immunology of Pregnancy. Thyroid 1999, 9, 643–646. [Google Scholar] [CrossRef]
- Noronha, L.E.; Antczak, D.F. Maternal Immune Responses to Trophoblast: The Contribution of the Horse to Pregnancy Immunology. Am. J. Reprod. Immunol. 2010, 64, 231–244. [Google Scholar] [CrossRef]
- Olmos-Ortiz, A.; Flores-Espinosa, P.; Mancilla-Herrera, I.; Vega-Sánchez, R.; Díaz, L.; Zaga-Clavellina, V. Innate Immune Cells and Toll-like Receptor–Dependent Responses at the Maternal–Fetal Interface. Int. J. Mol. Sci. 2019, 20, 3654. [Google Scholar] [CrossRef] [Green Version]
- Ehsu, P.; Nanan, R.K.H. Innate and Adaptive Immune Interactions at the Fetal–Maternal Interface in Healthy Human Pregnancy and Pre-Eclampsia. Front. Immunol. 2014, 5, 125. [Google Scholar] [CrossRef]
- Bilate, A.M.; Lafaille, J.J. Induced CD4+Foxp3+ Regulatory T Cells in Immune Tolerance. Annu. Rev. Immunol. 2012, 30, 733–758. [Google Scholar] [CrossRef] [Green Version]
- Fan, D.-X.; Duan, J.; Li, M.-Q.; Xu, B.; Li, D.-J.; Jin, L.-P. The decidual gamma-delta T cells up-regulate the biological functions of trophoblasts via IL-10 secretion in early human pregnancy. Clin. Immunol. 2011, 141, 284–292. [Google Scholar] [CrossRef]
- Tilburgs, T.; Schonkeren, D.; Eikmans, M.; Nagtzaam, N.M.; Datema, G.; Swings, G.M.; Prins, F.; Van Lith, J.M.; Van Der Mast, B.J.; Roelen, D.L.; et al. Human Decidual Tissue Contains Differentiated CD8+Effector-Memory T Cells with Unique Properties. J. Immunol. 2010, 185, 4470–4477. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mincheva-Nilsson, L.; Baranov, V.; Yeung, M.; Hammarstrom, S.; Hammarstrom, M.L. Immunomorphologica studies in human decidua-associated lymphoid cells in normal early pregnancy. J. Immuno. 1994, 152, 2020–2032. [Google Scholar]
- Mor, G.; Abrahams, V.M. Potential role of macrophages as immunoregulators of pregnancy. Reprod. Biol. Endocrinol. 2003, 1, 119. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, L.; Liu, X. Contributions of Drug Transporters to Blood-Placental Barrier. Drug Transp. Drug Dispos. Eff. Toxic. 2019, 1141, 505–548. [Google Scholar] [CrossRef]
- Pozor, M. Equine placenta—A clinician’s perspective. Part 1: Normal placenta—Physiology and evaluation. Equine Veter.-Educ. 2015, 28, 327–334. [Google Scholar] [CrossRef]
- Wood, K.J.; Sakaguchi, S. Regulatory T cells in transplantation tolerance. Nat. Rev. Immunol. 2003, 3, 199–210. [Google Scholar] [CrossRef]
- Cristiani, C.M.; Palella, E.; Sottile, R.; Tallerico, R.; Garofalo, C.; Carbone, E. Human NK Cell Subsets in Pregnancy and Disease: Toward a New Biological Complexity. Front. Immunol. 2016, 7, 656. [Google Scholar] [CrossRef]
- Gaynor, L.M.; Colucci, F. Uterine Natural Killer Cells: Functional Distinctions and Influence on Pregnancy in Humans and Mice. Front. Immunol. 2017, 8, 467. [Google Scholar] [CrossRef] [Green Version]
- Moffett-King, A. Natural killer cells and pregnancy. Nat. Rev. Immunol. 2002, 2, 656–663. [Google Scholar] [CrossRef]
- Fernekorn, U.; Kruse, A. Regulation of Leukocyte Recruitment to the Murine Maternal/Fetal Interface. Immunol. Pregnancy 2005, 89, 105–117. [Google Scholar] [CrossRef]
- Williams, P.; Searle, R.; Robson, S.; Innes, B.; Bulmer, J. Decidual leucocyte populations in early to late gestation normal human pregnancy. J. Reprod. Immunol. 2009, 82, 24–31. [Google Scholar] [CrossRef] [PubMed]
- Viveiros, M.; Antczak, D. Characterization of equine natural killer and IL-2 stimulated lymphokine activated killer cell populations. Dev. Comp. Immunol. 1999, 23, 521–532. [Google Scholar] [CrossRef]
- Croy, B.; Waterfield, A.; Wood, W.; King, G.J. Normal murine and porcine embryos recruit NK cells to the uterus. Cell. Immunol. 1988, 115, 471–480. [Google Scholar] [CrossRef]
- Carter, A.M.; Enders, A.C. The Evolution of Epitheliochorial Placentation. Annu. Rev. Anim. Biosci. 2013, 1, 443–467. [Google Scholar] [CrossRef] [PubMed]
- Noronha, L.; Huggler, K.; de Mestre, A.; Miller, D.; Antczak, D. Molecular evidence for natural killer-like cells in equine endometrial cups. Placenta 2012, 33, 379–386. [Google Scholar] [CrossRef] [Green Version]
- Allen, W.R. The physiology of early pregnancy in the mare. AAEP Proc. 2000, 46, 338–354. [Google Scholar]
- Grünig, G.; Triplett, L.; Canady, L.; Allen, W.; Antczak, D. The maternal leucocyte response to the endometrial cups in horses is correlated with the developmental stages of the invasive trophoblast cells. Placenta 1995, 16, 539–559. [Google Scholar] [CrossRef]
- Fujiwara, H.; Ono, M.; Sato, Y.; Imakawa, K.; Iizuka, T.; Kagami, K.; Fujiwara, T.; Horie, A.; Tani, H.; Hattori, A.; et al. Promoting Roles of Embryonic Signals in Embryo Implantation and Placentation in Cooperation with Endocrine and Immune Systems. Int. J. Mol. Sci. 2020, 21, 1885. [Google Scholar] [CrossRef] [Green Version]
- Herrler, A.; von Rango, U.; Beier, H.M. Embryo-maternal signalling: How the embryo starts talking to its mother to accomplish implantation. Reprod. Biomed. Online 2003, 6, 244–256. [Google Scholar] [CrossRef]
- Rao, C.; Lei, Z. The past, present and future of nongonadal LH/hCG actions in reproductive biology and medicine. Mol. Cell. Endocrinol. 2007, 269, 2–8. [Google Scholar] [CrossRef]
- Fazleabas, A.; Kim, J.; Strakova, Z. Implantation: Embryonic Signals and the Modulation of the Uterine Environment—A Review. Placenta 2004, 25, S26–S31. [Google Scholar] [CrossRef] [PubMed]
- Goff, A.K. Embryonic Signals and Survival. Reprod. Domest. Anim. 2002, 37, 133–139. [Google Scholar] [CrossRef]
- Klohonatz, K.M.; Cameron, A.D.; Hergenreder, J.R.; Da Silveira, J.C.; Belk, A.D.; Veeramachaneni, D.N.R.; Bouma, G.J.; Bruemmer, J.E. Circulating miRNAs as Potential Alternative Cell Signaling Associated with Maternal Recognition of Pregnancy in the Mare. Biol. Reprod. 2016, 95, 124. [Google Scholar] [CrossRef] [PubMed]
- Parham, P. NK Cells and Trophoblasts. J. Exp. Med. 2004, 200, 951–955. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Manaster, I.; Mandelboim, O. The Unique Properties of Uterine NK Cells. Am. J. Reprod. Immunol. 2010, 63, 434–444. [Google Scholar] [CrossRef] [PubMed]
- Di Santo, J.P. Natural killer cells: Diversity in search of a niche. Nat. Immunol. 2008, 9, 473–475. [Google Scholar] [CrossRef] [PubMed]
- Lash, G.E.; Bulmer, J.N. Do uterine natural killer (uNK) cells contribute to female reproductive disorders? J. Reprod. Immunol. 2011, 88, 156–164. [Google Scholar] [CrossRef] [PubMed]
- Madeja, Z.; Yadi, H.; Apps, R.; Boulenouar, S.; Roper, S.J.; Gardner, L.; Moffett, A.; Colucci, F.; Hemberger, M. Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth. Proc. Natl. Acad. Sci. USA 2011, 108, 4012–4017. [Google Scholar] [CrossRef] [Green Version]
- Hiby, S.E.; Apps, R.; Sharkey, A.; Farrell, L.E.; Gardner, L.; Mulder, A.; Claas, F.H.; Walker, J.; Redman, C.C.; Morgan, L.; et al. Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J. Clin. Investig. 2010, 120, 4102–4110. [Google Scholar] [CrossRef]
- King, A. Uterine leukocytes and decidualization. Hum. Reprod. Updat. 2000, 6, 28–36. [Google Scholar] [CrossRef]
- Engelhardt, H.; King, G.J. Uterine natural killer cells in species with epitheliochorial placentation. Nat. Immun. 1996, 15, 53–69. [Google Scholar] [PubMed]
- Svensson-Arvelund, J.; Mehta, R.B.; Lindau, R.; Mirrasekhian, E.; Rodriguez-Martinez, H.; Berg, G.; Lash, G.E.; Jenmalm, M.C.; Ernerudh, J. The Human Fetal Placenta Promotes Tolerance against the Semiallogeneic Fetus by Inducing Regulatory T Cells and Homeostatic M2 Macrophages. J. Immunol. 2015, 194, 1534–1544. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zenclussen, A.C. Regulatory T cells in pregnancy. Springer Semin. Immunopathol. 2006, 28, 31–39. [Google Scholar] [CrossRef] [PubMed]
- Piccinni, M.-P. T cells in normal pregnancy and recurrent pregnancy loss. Reprod. Biomed. Online 2006, 13, 840–844. [Google Scholar] [CrossRef]
- Mjösberg, J.; Svensson-Arvelund, J.; Johansson, E.; Hellström, L.; Casas, R.; Jenmalm, M.; Boij, R.; Matthiesen, L.; Jönsson, J.-I.; Berg, G.; et al. Systemic Reduction of Functionally Suppressive CD4dimCD25highFoxp3+Tregs in Human Second Trimester Pregnancy Is Induced by Progesterone and 17β-Estradiol. J. Immunol. 2009, 183, 759–769. [Google Scholar] [CrossRef] [Green Version]
- Leber, A.; Teles, A.; Zenclussen, A.C. Regulatory T Cells and Their Role in Pregnancy. Am. J. Reprod. Immunol. 2010, 63, 445–459. [Google Scholar] [CrossRef]
- Christoffersen, M.; Troedsson, M. Inflammation and fertility in the mare. Reprod. Domest. Anim. 2017, 52 (Suppl S3), 14–20. [Google Scholar] [CrossRef]
- Agrícola, R.; Carvalho, H.; Barbosa, M.; Pereira, M.; Medeiros, J.; Ferreira-Dias, G. Blood Lymphocyte Subpopulations, Neutrophil Phagocytosis and Proteinogram During Late Pregnancy and Postpartum in Mares. Reprod. Domest. Anim. 2008, 43, 212–217. [Google Scholar] [CrossRef]
- Noronha, L.E.; Antczak, D.F. Modulation of T-cell Reactivity During Equine Pregnancy is Antigen Independent. Am. J. Reprod. Immunol. 2012, 68, 107–115. [Google Scholar] [CrossRef]
- Yamada, K. Analysis on the CTL-p frequency before and after immunotherapy for patients with unexplained habitual abortion. Nihon Sanka Fujinka Gakkai Zasshi 1993, 45, 527–532. [Google Scholar]
- Kotlan, B.; Fülöp, V.; Padányi, Á.; Szigetvári, I.; Réti, M.; Gyódi, É.; Fehér, É.; Petrányi, G. High anti-paternal cytotoxic T-lymphocyte precursor frequencies in women with unexplained recurrent spontaneous abortions. Hum. Reprod. 2001, 16, 1278–1285. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Uckan, D.; Steele, A.; Cherry; Wang, B.Y.; Chamizo, W.; Koutsonikolis, A.; Gilbert-Barness, E.; Good, R.A. Trophoblasts express Fas ligand: A proposed mechanism for immune privilege in placenta and maternal invasion. Mol. Hum. Reprod. 1997, 3, 655–662. [Google Scholar] [CrossRef] [Green Version]
- Care, A.S.; Diener, K.; Jasper, M.J.; Brown, H.M.; Ingman, W.V.; Robertson, S.A. Macrophages regulate corpus luteum development during embryo implantation in mice. J. Clin. Investig. 2013, 123, 3472–3487. [Google Scholar] [CrossRef] [PubMed]
- Schonkeren, D.; van der Hoorn, M.-L.; Khedoe, P.; Swings, G.; van Beelen, E.; Claas, F.; van Kooten, C.; de Heer, E.; Scherjon, S. Differential Distribution and Phenotype of Decidual Macrophages in Preeclamptic versus Control Pregnancies. Am. J. Pathol. 2011, 178, 709–717. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mizuno, M.; Aoki, K.; Kimbara, T. Functions of Macrophages in Human Decidual Tissue in Early Pregnancy. Am. J. Reprod. Immunol. 1994, 31, 180–188. [Google Scholar] [CrossRef]
- Gordon, S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3, 23–35. [Google Scholar] [CrossRef]
- Ning, F.; Liu, H.; Lash, G.E. The Role of Decidual Macrophages During Normal and Pathological Pregnancy. Am. J. Reprod. Immunol. 2016, 75, 298–309. [Google Scholar] [CrossRef]
- Böckle, B.; Sölder, E.; Kind, S.; Romani, N.; Sepp, N. DC-SIGN+ CD163+ Macrophages Expressing Hyaluronan Receptor LYVE-1 Are Located within Chorion Villi of the Placenta. Placenta 2008, 29, 187–192. [Google Scholar] [CrossRef]
- Gustafsson, C.; Mjösberg, J.; Matussek, A.; Geffers, R.; Matthiesen, L.; Berg, G.; Sharma, S.; Buer, J.; Ernerudh, J. Gene Expression Profiling of Human Decidual Macrophages: Evidence for Immunosuppressive Phenotype. PLoS ONE 2008, 3, e2078. [Google Scholar] [CrossRef]
- De, M.; Wood, G.W. Influence of Oestrogen and Progesterone on Macrophage Distribution in the Mouse Uterus. J. Endocrinol. 1990, 126, 417–424. [Google Scholar] [CrossRef]
- Piacentini, M.; Autuori, F. Immunohistochemical localization of tissue transglutaminase and Bcl-2 in rat uterine tissues during embryo implantation and post-partum involution. Differentiation 1994, 57, 51–61. [Google Scholar] [CrossRef] [PubMed]
- Miller, L.; Hunt, J.S. Sex steroid hormones and macrophage function. Life Sci. 1996, 59, 1–14. [Google Scholar] [CrossRef]
- Tachi, C.; Tachi, S. Macrophages and Implantation. Ann. N. Y. Acad. Sci. 1986, 476, 158–182. [Google Scholar] [CrossRef] [PubMed]
- Skarzynski, D.J.; Szóstek-Mioduchowska, A.Z.; Rebordão, M.R.; Jalali, B.M.; Piotrowska-Tomala, K.K.; Leciejewska, N.; Ferreira-Dias, G.M. Neutrophils, monocytes and other immune components in the equine endometrium: Friends or foes? Theriogenology 2020, 150, 150–157. [Google Scholar] [CrossRef]
- Watson, E.D.; Dixon, C.E. An immunohistological study of MHC Class II expression and T lymphocytes in the endometrium of the mare. Equine Veter-J. 1993, 25, 120–124. [Google Scholar] [CrossRef]
- Frayne, J.; Stokes, C. MHC Class II positive cells and T cells in the equine endometrium throughout the oestrous cycle. Veter-Immunol. Immunopathol. 1994, 41, 55–72. [Google Scholar] [CrossRef]
- Summerfield, N.J.; Watson, E.D. Endometrial macrophage populations in genitally normal mares at oestrus and dioestrus and in mares susceptible to endometritis. Equine Veter-J. 1998, 30, 79–81. [Google Scholar] [CrossRef]
- Rieger, L.; Honig, A.; Sütterlin, M.; Kapp, M.; Dietl, J.; Ruck, P.; Kämmerer, U. Antigen-Presenting Cells in Human Endometrium During the Menstrual Cycle Compared to Early Pregnancy. J. Soc. Gynecol. Investig. 2004, 11, 488–493. [Google Scholar] [CrossRef]
- Clark, D.A.; Chaouat, G.; Wong, K.; Gorczynski, R.M.; Kinsky, R. REVIEW ARTICLE: Tolerance Mechanisms in Pregnancy: A Reappraisal of the Role of Class I Paternal MHC Antigens*. Am. J. Reprod. Immunol. 2009, 63, 93–103. [Google Scholar] [CrossRef]
- Hart, D.N. Dendritic Cells: Unique Leukocyte Populations Which Control the Primary Immune Response. Blood 1997, 90, 3245–3287. [Google Scholar] [CrossRef]
- Bachy, V.; Williams, D.J.; Ibrahim, M.A.A. Altered dendritic cell function in normal pregnancy. J. Reprod. Immunol. 2008, 78, 11–21. [Google Scholar] [CrossRef] [PubMed]
- Blois, S.; Tometten, M.; Kandil, J.; Hagen, E.; Klapp, B.F.; Margni, R.A.; Arck, P.C. Intercellular Adhesion Molecule-1/LFA-1 Cross Talk Is a Proximate Mediator Capable of Disrupting Immune Integration and Tolerance Mechanism at the Feto-Maternal Interface in Murine Pregnancies. J. Immunol. 2005, 174, 1820–1829. [Google Scholar] [CrossRef] [Green Version]
- Askelund, K.; Liddell, H.; Zanderigo, A.; Fernando, N.; Khong, T.; Stone, P.; Chamley, L. CD83+Dendritic Cells in the Decidua of Women with Recurrent Miscarriage and Normal Pregnancy. Placenta 2004, 25, 140–145. [Google Scholar] [CrossRef]
- Blois, S.M.; Kammerer, U.; Soto, C.A.; Tometten, M.C.; Shaikly, V.; Barrientos, G.; Jurd, R.; Rukavina, D.; Thomson, A.W.; Klapp, B.F.; et al. Dendritic Cells: Key to Fetal Tolerance? Biol. Reprod. 2007, 77, 590–598. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jaworska, J.; Tobolski, D.; Janowski, T. Is similarity in Major Histocompatibility Complex (MHC) associated with the incidence of retained fetal membranes in draft mares? A cross-sectional study. PLoS ONE 2020, 15, e0237765. [Google Scholar] [CrossRef]
- Dinarello, C.A. Historical insights into cytokines. Eur. J. Immunol. 2007, 37 (Suppl S1), S34–S45. [Google Scholar] [CrossRef] [Green Version]
- Saini, V.; Arora, S.; Yadav, A.; Bhattacharjee, J. Cytokines in recurrent pregnancy loss. Clin. Chim. Acta 2011, 412, 702–708. [Google Scholar] [CrossRef]
- Robertson, S.A.; Care, A.S.; Moldenhauer, L.M. Regulatory T cells in embryo implantation and the immune response to pregnancy. J. Clin. Investig. 2018, 128, 4224–4235. [Google Scholar] [CrossRef] [Green Version]
- Chaouat, G.; Menu, E.; Delage, G.; Moreau, J.F.; Khrishnan, L.; Hui, L.; Meliani, A.A.; Martal, J.; Raghupathy, R.; Lelaidier, C.; et al. Immuno-endocrine interactions in early pregnancy. Hum. Reprod. 1995, 10 (Suppl S2), 55–58. [Google Scholar] [CrossRef]
- Spence, T.; Allsopp, P.J.; Yeates, A.J.; Mulhern, M.S.; Strain, J.J.; McSorley, E.M. Maternal Serum Cytokine Concentrations in Healthy Pregnancy and Preeclampsia. J. Pregnancy 2021, 2021, 6649608. [Google Scholar] [CrossRef]
- Reinhard, G.; Noll, A.; Schlebusch, H.; Mallmann, P.; Ruecker, A.V. Shifts in the TH1/TH2 Balance during Human Pregnancy Correlate with Apoptotic Changes. Biochem. Biophys. Res. Commun. 1998, 245, 933–938. [Google Scholar] [CrossRef] [PubMed]
- Mor, G.; Cardenas, I. The Immune System in Pregnancy: A Unique Complexity. Am. J. Reprod. Immunol. 2010, 63, 425–433. [Google Scholar] [CrossRef] [Green Version]
- Mor, G.; Cardenas, I.; Abrahams, V.; Guller, S. Inflammation and pregnancy: The role of the immune system at the implantation site. Ann. N. Y. Acad. Sci. 2011, 1221, 80–87. [Google Scholar] [CrossRef] [Green Version]
- Doria, A.; Cutolo, M.; Ghirardello, A.; Zen, M.; Villalta, D.; Tincani, A.; Punzi, L.; Iaccarino, L.; Petri, M. Effect of pregnancy on serum cytokines in SLE patients. Arthritis Res. Ther. 2012, 14, R66. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Subha, M.; Pal, P.; Pal, G.K.; Habeebullah, S.; Adithan, C.; Sridhar, M.G. Decreased baroreflex sensitivity is linked to sympathovagal imbalance, low-grade inflammation, and oxidative stress in pregnancy-induced hypertension. Clin. Exp. Hypertens. 2016, 38, 666–672. [Google Scholar] [CrossRef] [PubMed]
- Straszewski-Chavez, S.L.; Abrahams, V.M.; Mor, G. The Role of Apoptosis in the Regulation of Trophoblast Survival and Differentiation during Pregnancy. Endocr. Rev. 2005, 26, 877–897. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lindsay, K.L.; Buss, C.; Wadhwa, P.D.; Entringer, S. Maternal Stress Potentiates the Effect of an Inflammatory Diet in Pregnancy on Maternal Concentrations of Tumor Necrosis Factor Alpha. Nutrients 2018, 10, 1252. [Google Scholar] [CrossRef] [Green Version]
- Murphy, S.P.; Tayade, C.; Ashkar, A.A.; Hatta, K.; Zhang, J.; Croy, B.A. Interferon Gamma in Successful Pregnancies1. Biol. Reprod. 2009, 80, 848–859. [Google Scholar] [CrossRef] [Green Version]
- Nayak, M.; Eekhoff, E.; Peinhaupt, M.; Heinemann, A.; Desoye, G.; van Poppel, M.N. Cytokines and their association with insulin resistance in obese pregnant women with different levels of physical activity. Cytokine 2016, 77, 72–78. [Google Scholar] [CrossRef]
- Chatterjee, P.; Chiasson, V.L.; Bounds, K.R.; Mitchell, B.M. Regulation of the Anti-Inflammatory Cytokines Interleukin-4 and Interleukin-10 during Pregnancy. Front. Immunol. 2014, 5, 253. [Google Scholar] [CrossRef] [Green Version]
- Witkowska-Piłaszewicz, O.; Pingwara, R.; Winnicka, A. The Effect of Physical Training on Peripheral Blood Mononuclear Cell Ex Vivo Proliferation, Differentiation, Activity, and Reactive Oxygen Species Production in Racehorses. Antioxidants 2020, 9, 1155. [Google Scholar] [CrossRef] [PubMed]
- Sipak-Szmigiel, O.; Podolska, M.; Płonka, T.; Włodarski, P.; Ronin-Walknowska, E. Changes in the concentration of sHLA-I and selected cytokines in pregnancy complicated by antiphospholipid syndrome. Ginekol. Pol. 2011, 82, 354–358. [Google Scholar]
- Schäfer-Somi, S. Cytokines during early pregnancy of mammals: A review. Anim. Reprod. Sci. 2002, 75, 73–94. [Google Scholar] [CrossRef]
- Fedorka, C.; Ball, B.; Walker, O.; McCormick, M.; Scoggin, K.; Kennedy, L.; Squires, E.; Troedsson, M. Alterations of Circulating Biomarkers During Late Term Pregnancy Complications in the Horse Part I: Cytokines. J. Equine Veter-Sci. 2021, 99, 103425. [Google Scholar] [CrossRef]
- Fedorka, C.E.; Scoggin, K.E.; Ali, H.E.; Loux, S.C.; Dini, P.; Troedsson, M.H.T.; Ball, B.A. Interleukin-6 pathobiology in equine placental infection. Am. J. Reprod. Immunol. 2020, 85, e13363. [Google Scholar] [CrossRef]
- Arikan, D.C.; Aral, M.; Coskun, A.; Ozer, A. Plasma IL-4, IL-8, IL-12, interferon-γ and CRP levels in pregnant women with preeclampsia, and their relation with severity of disease and fetal birth weight. J. Matern. Neonatal Med. 2012, 25, 1569–1573. [Google Scholar] [CrossRef]
- Pinheiro, M.B.; Martins-Filho, O.A.; Mota, A.P.L.; Alpoim, P.N.; Godoi, L.C.; Silveira, A.C.; Teixeira-Carvalho, A.; Gomes, K.B.; Dusse, L.M. Severe preeclampsia goes along with a cytokine network disturbance towards a systemic inflammatory state. Cytokine 2013, 62, 165–173. [Google Scholar] [CrossRef] [Green Version]
- Ferreira, L.M.; Meissner, T.B.; Tilburgs, T.; Strominger, J.L. HLA-G: At the Interface of Maternal–Fetal Tolerance. Trends Immunol. 2017, 38, 272–286. [Google Scholar] [CrossRef]
- Yockey, L.J.; Iwasaki, A. Interferons and Proinflammatory Cytokines in Pregnancy and Fetal Development. Immunity 2018, 49, 397–412. [Google Scholar] [CrossRef] [Green Version]
- Sentman, C.L.; Meadows, S.K.; Wira, C.R.; Eriksson, M. Recruitment of Uterine NK Cells: Induction of CXC Chemokine Ligands 10 and 11 in Human Endometrium by Estradiol and Progesterone. J. Immunol. 2004, 173, 6760–6766. [Google Scholar] [CrossRef] [Green Version]
- Saito, S.; Nakashima, A.; Shima, T.; Ito, M. Th1/Th2/Th17 and Regulatory T-Cell Paradigm in Pregnancy. Am. J. Reprod. Immunol. 2010, 63, 601–610. [Google Scholar] [CrossRef] [PubMed]
- Peck, A.; Mellins, E.D. Plasticity of T-cell phenotype and function: The T helper type 17 example. Immunology 2010, 129, 147–153. [Google Scholar] [CrossRef]
- Crome, S.Q.; Wang, A.Y.; Levings, M.K. Translational Mini-Review Series on Th17 Cells: Function and regulation of human T helper 17 cells in health and disease. Clin. Exp. Immunol. 2009, 159, 109–119. [Google Scholar] [CrossRef] [PubMed]
- Yang, D.; Dai, F.; Yuan, M.; Zheng, Y.; Liu, S.; Deng, Z.; Tan, W.; Chen, L.; Zhang, Q.; Zhao, X.; et al. Role of Transforming Growth Factor-β1 in Regulating Fetal-Maternal Immune Tolerance in Normal and Pathological Pregnancy. Front. Immunol. 2021, 12, 689181. [Google Scholar] [CrossRef] [PubMed]
- Keskin, D.B.; Allan, D.S.J.; Rybalov, B.; Andzelm, M.M.; Stern, J.N.H.; Kopcow, H.D.; Koopman, L.A.; Strominger, J.L. TGFβ promotes conversion of CD16 + peripheral blood NK cells into CD16 NK cells with similarities to decidual NK cells. Proc. Natl. Acad. Sci. USA 2007, 104, 3378–3383. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lash, G.E.; Schiessl, B.; Kirkley, M.; Innes, B.A.; Cooper, A.; Searle, R.F.; Robson, S.C.; Bulmer, J.N. Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy. J. Leukoc. Biol. 2006, 80, 572–580. [Google Scholar] [CrossRef]
- Zhang, X.; Wei, H. Role of Decidual Natural Killer Cells in Human Pregnancy and Related Pregnancy Complications. Front. Immunol. 2021, 12, 728291. [Google Scholar] [CrossRef]
- Gomez-Lopez, N.; Estrada-Gutierrez, G.; Jimenez-Zamudio, L.A.; Vega-Sanchez, R.; Vadillo-Ortega, F. Fetal membranes exhibit selective leukocyte chemotaxic activity during human labor. J. Reprod. Immunol. 2009, 80, 122–131. [Google Scholar] [CrossRef]
- Gomez-Lopez, N.; Tanaka, S.; Zaeem, Z.; Metz, G.A.; Olson, D.M. Maternal circulating leukocytes display early chemotactic responsiveness during late gestation. BMC Pregnancy Childbirth 2013, 13, S8. [Google Scholar] [CrossRef] [Green Version]
- King, A.; Allan, D.S.; Bowen, M.; Powis, S.J.; Joseph, S.; Verma, S.; Braud, V.M. HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur. J. Immunol. 2000, 30, 1623–1631. [Google Scholar] [CrossRef]
- Lennard, S.N.; Stewart, F.; Allen, W.R. Transforming growth factor ?1 expression in the endometrium of the mare during placentation. Mol. Reprod. Dev. 1995, 42, 131–140. [Google Scholar] [CrossRef] [PubMed]
- Lennard, S.; Stewart, F.; Allen, W.; Heap, R. Growth Factor Production in the Pregnant Equine Uterus1. Biol. Reprod. 1995, 52, 161–170. [Google Scholar] [CrossRef]
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Figarska, A.; Witkowska-Piłaszewicz, O. Immunological Response during Pregnancy in Humans and Mares. Agriculture 2022, 12, 431. https://doi.org/10.3390/agriculture12030431
Figarska A, Witkowska-Piłaszewicz O. Immunological Response during Pregnancy in Humans and Mares. Agriculture. 2022; 12(3):431. https://doi.org/10.3390/agriculture12030431
Chicago/Turabian StyleFigarska, Aleksandra, and Olga Witkowska-Piłaszewicz. 2022. "Immunological Response during Pregnancy in Humans and Mares" Agriculture 12, no. 3: 431. https://doi.org/10.3390/agriculture12030431