Inflammation, NK cells and implantation: Friend and foe (the good, the bad and the ugly?): Replacing placental viviparity in an evolutionary perspective

Journal of Reproductive Immunology

Volumn 97, Issue 1, 2013, Pages 2-13

  Chaouat, Gérard ^a  

^a SAINT LOUIS HOSPITAL   (France)

Author keywords

Evolution; Implantation; Inflammation; Paradigms; Placental; Viviparity

Indexed keywords

ADAPTIVE IMMUNITY; ARTICLE; BLOOD PLACENTA BARRIER; ENDOMETRIOSIS; HUMAN; IMMUNE DEFICIENCY; IMMUNE SYSTEM; INFERTILITY; INFLAMMATION; NATURAL KILLER CELL; NIDATION; PREGNANCY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REPRODUCTION; TH1 CELL; TH2 CELL; UTERUS; VIVIPARITY;

ANIMALS; BIOLOGICAL EVOLUTION; EMBRYO IMPLANTATION; ENDOMETRIOSIS; FEMALE; HUMANS; IMMUNE TOLERANCE; INFLAMMATION; KILLER CELLS, NATURAL; PLACENTA; PREGNANCY; T-LYMPHOCYTES, REGULATORY; TH1-TH2 BALANCE; VIVIPARITY, NONMAMMALIAN;

EID: 84874528204     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2012.10.009     Document Type: Article

References (112)

1. Abbondanzo S.J., Cullinan E.B., McIntyre K., Labow M.A., Stewart C.L. Reproduction in mice lacking a functional type 1 IL-1 receptor. Endocrinology 1996, 137:3598-3601.
2. Adelman M.K., Schluter S.F., Marchalonis J.J. The natural antibody repertoire of sharks and humans recognizes the potential universe of antigens. Protein J. 2004, 23(2):103-118.
3. Adelstein S., Pritchard-Briscoe H., Loblay R.H., Basten A. Suppressor T-cell memory. Curr. Top. Microbiol. Immunol. 1990, 159:123-138.
4. Ahmed A., Singh J., Khan Y., Seshan S.V., Girardi G. A new mouse model to explore therapies for preeclampsia. PLoS ONE 2010, 5(10):e13663.
5. Allen W.R., Short R. Interspecific and extraspecific pregnancies in equids: anything goes. J. Hered. 1997, 88(5):384-392.
6. Allen W.R., Kydd J.H., Antczak D.F. Successful application of immunotherapy to a model of pregnancy failure in equids. Reproductive Immunology 1986, 253-261. Elsevier, Amsterdam. D.A. Clark, B.A. Croy (Eds.).
7. Allison J.L., Schust D.J. Recurrent first trimester pregnancy loss: revised definitions and novel causes. Curr. Opin. Endocrinol. Diab. Obes. 2009, 16(6):446-450.
8. Altincicek B., Vilcinskas A. Identification of immune inducible genes from the velvet worm Epiperipatus biolleyi (Onychophora). Dev. Comp. Immunol. 2009, 32(12):1416-1421.
9. Arceci B., Shanahan F., Stanley E.R., Pollard J.W. The temporal expression and localisation of colony stimulating factor (CSF-1) and its receptor in the female reproductive tract are consistent with CSF-1 regulated placental development. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:8818-8822.
10. Basak S., Dubanchet S., Zourbas S., Chaouat G., Das C. Expression of pro-inflammatory cytokines in mouse blastocysts during implantation: modulation by steroid hormones. Am. J. Reprod. Immunol. 2002, 47(1):2-11.
11. Bazer F.W., Spencer T.E., Johnson G.A., Burghardt R.C., Wu G. Comparative aspects of implantation. Reproduction 2009, 138(2):195-209.
12. Blackburn D.G., Flemming A.F. Invasive implantation and intimate placental associations in a placentotrophic African lizard, Trachylepis ivensi (scincidae). J. Morphol. 2012, 273(2):137-159.
13. Bobé P., Kiger N. Immunogenetic studies of spontaneous abortion in mice. III. Non-H-2 antigens and gestation. J. Immunogenet. 1989, 16(3):223-231.
14. Bobé P., Stanislawski M., Kiger N. Immunogenetic studies of spontaneous abortions in mice. Immunoregulation and Fetal Survival. 2nd Banff Conference 1987, 252-263. Oxford University Press, New York. T.G. Wegmann, T.J. Gill, E. Nisbet Brown (Eds.).
15. Chaouat G. Innately moving away from the Th1/Th2 paradigm in pregnancy. Clin. Exp. Immunol. 2003, 131(3):393-395.
16. Chaouat G., Kiger N., Chaouat G., Kolb J.P., Wegmann T.G., Guenet J.L. Immunogenetic studies of spontaneous abortion in mice. Preimmunisation of the mother with allogeneic spleen cells. J. Immunol. 1985, 134:2966-2972.
17. Chaouat G., Assal Meliani A., Martal J., et al. Il-10 prevents inflammatory cytokine-mediated foetal death and is inducible by tau interferon. J. Immunol. 1995, 152:2411-2420.
18. Chaouat G., Tranchot Diallo J., Volumenie J.L., et al. Immune suppression and Th1/Th2 balance in pregnancy revisited: a (very) personal tribute to Tom Wegmann. Am. J. Reprod. Immunol. 1997, 37(6):427-434.
19. Chaouat G., Zourbas S., Ostojic S., et al. A brief review of recent data on some cytokine expressions at the materno-foetal interface which might challenge the classical Th1/Th2 dichotomy. J. Reprod. Immunol. 2002, 53(1-2):241-256.
20. Chaouat G., Ledée-Bataille N., Dubanchet S., Zourbas S., Sandra O., Martal J. Th1/Th2 paradigm in pregnancy: paradigm lost? Cytokines in pregnancy/early abortion: reexamining the TH1/TH2 paradigm. Int. Arch. Allergy Immunol. 2004, 134(2):93-119.
21. Chaouat G., Robillard P.Y., Dekker G. Fourth international workshop on immunology of pre-eclampsia, December 2004, Reunion, France. J. Reprod. Immunol. 2005, 67(1-2):103-111.
22. Chaouat G., Robillard P.Y., Dekker G. Fourth International Workshop on immunology of pre-eclampsia, December 2004, Reunion, France. J. Reprod. Immunol. 2005, 67(1-2):103-111.
23. Chaouat G., Petitbarat M., Bulla R., et al. Early regulators in abortion and implications for a preeclampsia model. J. Reprod. Immunol. 2009, 82(2):131-140.
24. Chaouat G., Rodde N., Petitbarat M., et al. An insight into normal and pathological pregnancies using large-scale microarrays: lessons from microarrays. J. Reprod. Immunol. 2011, 89(2):163-172.
25. Chaouat, G., Rahmati, M., Bensussan, A., Clark, D.A. Seminal plasma peptides determine maternal immune response that alters success or failure of pregnancy in the abortion-prone CBAxDBA/2 model. J. Reprod. Immunol., in this issue.
26. Chatterjee-Hasrouni S., Lala P.K. Localization of H-2 antigens on mouse trophoblast cells. J. Exp. Med. 1979, 149(5):1238-1253.
27. Chen, T., Darrasse-Jèze, G., Bergot, A.S., Valdivia, K., Strominger, J.L., Chaouat, G., Klatzmann, D. Self-specific memory regulatory T cells protect embryos at implantation in a manner resembling protection of nascent tumors, submitted for publication.
28. Clark D.A., Flanders K.C., Hirte H., et al. Characterization of murine pregnancy decidua transforming growth factor beta. I. Transforming growth factor beta 2-like molecules of unusual molecular size released in bioactive form. Biol. Reprod. 1995, 52(6):1380-1388.
29. Clark D.A., Chaouat G., Banwatt D., Friebe A., Arck P.C. Ecology of danger-dependent cytokine-boosted spontaneous abortion in the CBA×DBA/2 mouse model. II. Fecal LPS levels in colonies with different basal abortion rates. Am. J. Reprod. Immunol. 2008, 60(6):529-533.
30. Criscitiello M.F., Ohta Y., Saltis M., McKinney E.C., Flajnik M.F. Evolutionarily conserved TCR binding sites, identification of T cells in primary lymphoid tissues, and surprising trans-rearrangements in nurse shark. J. Immunol. 2010, 184(12):6950-6960.
31. D'Hooghe T.M., Nugent N.P., Cuneo S., et al. Recombinant human TNFRSF1A (r-hTBP1) inhibits the development of endometriosis in baboons: a prospective, randomized, placebo- and drug-controlled study. Biol. Reprod. 2006, 74(1):131-136.
32. Dimitriadis E., Menkhorst E. New generation contraceptives: interleukin 11 family cytokines as non-steroidal contraceptive targets. J. Reprod. Immunol. 2011, 88(2):233-239.
33. Ding G.L., Chen X.J., Luo Q., Dong M.Y., Wang N., Huang H.F. Attenuated oocyte fertilization and embryo development associated with altered growth factor/signal transduction induced by endometriotic peritoneal fluid. Fertil. Steril. 2010, 93(8):2538-2544.
34. Early embryo development, uterine preparation and role of cytokines in implantation and labour. Colloque Université Paris sud. Inserm Fondation Mérieux 1995, Fondation Mérieux Ed.
35. Engleman E.G., McMichael A.J., Batey M.E., McDevitt H.O. A suppressor T cell of the mixed lymphocyte reaction in man specific for the stimulating alloantigen. Evidence that identity at HLA-D between suppressor and responder is required for suppression. J. Exp. Med. 1978, 147(1):137-146.
36. Engleman E.G., McMichael A.J., McDevitt H.O. Suppression of the mixed lymphocyte reaction in man by a soluble T-cell factor. Specificity of the factor for both responder and stimulator. J. Exp. Med. 1978, 147(4):1037-1043.
37. Giannubilo S.R., Landi B., Pozzi V., et al. The involvement of inflammatory cytokines in the pathogenesis of recurrent miscarriage. Cytokine 2012, 58(1):50-56.
38. Girardi G., Bulla R., Salmon J.E., Tedesco F. The complement system in the pathophysiology of pregnancy. Mol. Immunol. 2006, 43(1-2):68-77.
39. Girardi G., Prohászka Z., Bulla R., Tedesco F., Scherjon S. Complement activation in animal and human pregnancies as a model for immunological recognition. Mol. Immunol. 2011, 48(14):1621-1630.
40. Gnainsky Y., Granot I., Aldo P.B., et al. Local injury of the endometrium induces an inflammatory response that promotes successful implantation. Fertil. Steril. 2010, 94(6):2030-2036.
41. Hamilton M.S., Hamilton B.L. Environmental influences on immunologically associated recurrent spontaneous abortion in CBA/J mice. J. Reprod. Immunol. 1987, 11:237-241.
42. Hamlett W.C. Ultrastructure of the maternal-fetal interface of the yolk sac placenta in sharks. Ital. J. Anat. Embryol. 2005, 10(2 Suppl. 1):175-181.
43. Hedley M.L., Drake B.L., Head J.R., Tucker P.W., Forman J. Differential expression of the class I MHC genes in the embryo and placenta during midgestational development in the mouse. J. Immunol. 1989, 142(11):46-53.
44. Hill J.A. T helper 1 immunity to trophoblast: evidence for a new immunological mechanism for recurrent abortion in women. Hum. Reprod. 1995, 10:114-120.
45. Holder B.S., Tower C.L., Forbes K., Mulla M.J., Aplin J.D., Abrahams V.M. Immune cell activation by trophoblast-derived microvesicles is mediated by syncytin 1. Immunology 2012, 136(2):184-191.
46. Horgan C., Terrero G., Wessel G. In the extremes - traumatic insemination. Mol. Reprod. Dev. 2011, 78(5). Fmi.
47. Kachkache M., Acker G.M., Chaouat G., Noun A., Garabedian M. Hormonal and local factors control the immuno histochemical distribution of immunocytes in the rat uterus before conceptus implantation: effects of ovariectomy. Fallopian tube section and RU 486 injection. Biol. Reprod. 1991, 45:860-865.
48. Kaye M.D., Jones W.R., Anderson D.T. Immunology and placentation in viviparous invertebrates. J. Reprod. Fertil. 1972, 31(2):335-336.
49. Kolomiets O.L., Kurilo L.F., Malashenko A.M., Sakharova NIu, Chebotareva T.A. The effect of mutation dominant spotting-Yurlovo (KitW-Y) on spermatogenesis, early embryogenesis, and fertility of C57BL/6JY mice. Genetika 2005, 41(10):1377-1386.
50. Komine-Aizawa S., Izumi Y., Imai S., Fujita K., Hayakawa S. The therapeutic potential of the recombinant antigen from Dirofilaria immitis (rDiAg) for immune-mediated pregnancy loss. J. Reprod. Immunol. 2011, 92(1-2):21-26.
51. Kumasawa K., Ikawa M., Kidoya H., et al. Pravastatin induces placental growth factor (PGF) and ameliorates preeclampsia in a mouse model. Proc. Natl. Acad. Sci. U.S.A. 2011, 108(4):1451-1455.
52. Laissue P., Burgio G., l'Hôte D., et al. Identification of quantitative trait loci responsible for embryonic lethality in mice assessed by ultrasonography. Int. J. Dev. Biol. 2009, 53b(4):623-629.
53. Lebovic D.I., Mwenda J.M., Chai D.C., Santi A., Xu X., D'Hooghe T. Peroxisome proliferator-activated receptor-(gamma) receptor ligand partially prevents the development of endometrial explants in baboons: a prospective, randomized, placebo-controlled study. Endocrinology 2010, 151(4):1846-1852.
54. Lédée-Bataille N., Bonnet-Chea K., Hosny G., Dubanchet S., Frydman R., Chaouat G. Role of the endometrial tripod interleukin-18-15, and -12 in inadequate uterine receptivity in patients with a history of repeated in vitro fertilization-embryo transfer failure. Fertil. Steril. 2005, 83(3):598-605.
55. Lédée-Bataille N., Olivennes F., Kadoch J., et al. Detectable levels of interleukin-18 in uterine luminal secretions at oocyte retrieval predict failure of the embryo transfer. Hum. Reprod. 2006, 19(9):1968-1973.
56. Legac E., Vaugier G.L., Bousquet F., Bajelan M., Leclerc M. Primitive cytokines and cytokine receptors in invertebrates: the sea star Asterias rubens as a model of study. Scand. J. Immunol. 1996, 44(4):375-380.
57. Lightner A., Schust D.J., Chen Y.B., Barrier B.F. The fetal allograft revisited: does the study of an ancient invertebrate species shed light on the role of natural killer cells at the maternal-fetal interface?. Clin. Dev. Immunol. 2008, 2008:631920.
58. Litjens N.H., Boer K., Betjes M.G. Identification of circulating human antigen-reactive CD4+ FOXP3+ natural regulatory T cells. J. Immunol. 2012, 188(3):1083-1090.
59. Loblay R.H., Pritchand-Briscoe H., Basten A. Suppressor T-cell memory. Suppressor T-cell memory. Nature 1978, 272(5654):620-622.
60. Loke Y.W., King A. Recent developments in the human maternal-fetal immune interaction. Curr. Opin. Immunol. 1991, 5:762-766.
61. Loke Y.W., King A. Human Implantation: Cell Biology and Immunology 1995, Cambridge University Press.
62. Loke Y.W., King A. Immunology of human implantation: an evolutionary perspective. Hum. Reprod. 1996, 11(2):283-286.
63. Long J.A., Trinajstic K., Young G.C., Senden T. Live birth in the Devonian period. Nature 2008, 453(7195):650-652.
64. Luo Z.X., Yuan C.X., Meng Q.J., Ji Q. A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 2011, 476(7361):442-445.
65. MacMaster M.T., Newton R.C., Dey S.K., Andrews G.K. Activation and distribution of inflammatory cells in the mouse uterus during the pre-implantation period. J. Immunol. 1992, 148:1699-1705.
66. Madeja Z., Yadi H., Apps R., Boulenouar S., Roper S.J., Gardner L., et al. Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:4012-4017.
67. Mangeney M., Renard M., Schlecht-Louf G., Bouallaga I., Heidmann O., Letzelter C., Richaud A., Ducos B., Heidmann T. Placental syncytins: genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins. Proc. Natl. Acad. Sci. U.S.A. 2007, 104(51):20534-20539.
68. Martal J.L., Chene N.M., Huynh L.P., L'Haridon R.M., Reinaud P.B., Guillomot M.W., Charlier M.A., Charpigny S.Y. IFN-tau: a novel subtype I IFN1. Structural characteristics, non-ubiquitous expression, structure-function relationships, a pregnancy hormonal embryonic signal and cross-species therapeutic potentialities. Biochimie 1998, 80(8-9):755-777.
69. Mas A.E., Petitbarat M., Dubanchet S., Fay S., Ledée N., Chaouat G. Immune regulation at the interface during early steps of murine implantation: involvement of two new cytokines of the IL-12 family (IL-23 and IL-27) and of TWEAK. Am. J. Reprod. Immunol. 2008, 59(4):323-338.
70. Matzinger P. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 1994, 12:991-1045.
71. Medawar P. Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Symp. Soc. Exp. Biol. 1953, 7:320-338.
72. Meisser A., Chardonnens D., Campana A., Bischof P. Effects of tumour necrosis factor-alpha, interleukin-1 alpha, macrophage colony stimulating factor and transforming growth factor beta on trophoblastic matrix metalloproteinases. Mol. Hum. Reprod. 1999, 5(3):252-260.
73. Mellor A.L., Munn D.H. Immunology at the maternal-fetal interface: lessons for T cell tolerance and suppression. Annu. Rev. Immunol. 2000, 18:367-391.
74. Mellor A.L., Munn D.H. Tryptophan catabolism prevents maternal T cells from activating lethal anti-fetal immune responses. J. Reprod. Immunol. 2001, 52(1-2):5-13.
75. Menzies F.M., Higgins C.A., Shepherd M.C., Nibbs R.J., Nelson S.M. Mast cells reside in myometrium and cervix, but are dispensable in mice for successful pregnancy and labor. Immunol. Cell Biol. 2012, 90(3):321-329.
76. Mitra S., Alnabulsi A., Secombes C.J., Bird S. Identification and characterization of the transcription factors involved in T-cell development, t-bet, stat6 and foxp3, within the zebrafish, Danio rerio. FEBS J. 2010, 277(1):128-147.
77. Moffett A., Loke C. Immunology of placentation in eutherian mammals. Nat. Rev. Immunol. 2006, 6(8):584-594.
78. Mohamed O.A., Jonnaert M., Labelle-Dumais C., Kuroda K., Clarke H.J., Dufort D. Uterine Wnt/beta-catenin signaling is required for implantation. Proc. Natl. Acad. Sci. U.S.A. 2005, 102(24):8579-8584.
79. 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.
80. Oftedal O.T. The evolution of milk secretion and its ancient origins. Animal 2012, 6(3):355-368.
81. Paldi A. Genomic imprinting and feto maternal relationship. Biologie cellulaire et moléculaire de la relation materno fetale. Colloque INSERM 254 1991, 61-66.
82. Parham P., Norman P.J., Abi-Rached L., Hilton H.G., Guethlein L.A. Review: Immunogenetics of human placentation. Placenta 2012, 33(Suppl.):S71-S80.
83. Parham P., Norman P.J., Abi-Rached L., Guethlein L.A. Human-specific evolution of killer cell immunoglobulin-like receptor recognition of major histocompatibility complex class I molecules. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2012, 367(1590):800-811.
84. Park C.B., DeMayo F.J., Lydon J.P., Dufort D. NODAL in the uterus is necessary for proper placental development and maintenance of pregnancy. Biol. Reprod. 2012, 86(6):194.
85. Petitbarat M., Rahmati M., Sérazin V., et al. TWEAK appears as a modulator of endometrial IL-18 related cytotoxic activity of uterine natural killers. PLoS ONE 2011, 6(1):e14497.
86. Petrányi G.G. The complexity of immune and alloimmune response. Transpl. Immunol. 2002, 10(2-3):91-100.
87. Pires M.N., Arendt J., Reznick D.N. The evolution of placentas and superfetation in the fish genus Poecilia (Cyprinodontiformes: Poeciliidae: subgenera Micropoecilia and Acanthocephalus). Biol. J. Linnean Soc. 2010, 99:784-796.
88. Quintana F.J., Iglesias A.H., Farez M.F., et al. Adaptive autoimmunity and Foxp3-based immunoregulation in zebrafish. PLoS ONE 2010, 5(3):e9478.
89. Reznick D.N., Mateos M., Springer M.S. Independent origins and rapid evolution of the placenta in the fish genus Poeciliopsis. Science 2002, 298:1018-1020.
90. Ryland J.S., Bishop J.D.D. Prevalence of cross-fertilization in the hermaphroditic compound ascidian Diplosoma listerianum. Mar. Ecol. Prog. Ser. 1990, 61:125-132.
91. Sabri A., Hance T., Leroy P.D., et al. Placenta-like structure of the aphid endoparasitic wasp Aphidius ervi: a strategy of optimal resources acquisition. PLoS ONE 2011, 6(4):e18847.
92. Sacks G.P., Redman C.W., Sargent I.L. Monocytes are primed to produce the Th1 type cytokine IL-12 in normal human pregnancy: an intracellular flow cytometric analysis of peripheral blood mononuclear cells. Clin. Exp. Immunol. 2003, 131(3):490-497.
93. Sakaguchi S., Miyara M., Costantino C.M., Hafler D.A. FOXP3+ regulatory T cells in the human immune system. Nat. Rev. Immunol. 2010, 10(7):490-500.
94. Samstein R.M., Josefowicz S.Z., Arvey A., Treuting P.M., Rudensky A.Y. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell 2012, 150(1):29-38.
95. Sanford T.R., De M., Wood G. Expression of colony stimulating factors and inflammatory cytokines in the uterus if CD1 mice during days 1 to days 3 of pregnancy. J. Reprod. Fertil. 1992, 94(1):213-220.
96. Sargent I.L., Borzychowski A.M., Redman C.W. NK cells and human pregnancy - an inflammatory view. Trends Immunol. 2006, 27(9):399-404.
97. Shi L., Takahashi K., Dundee J., Shahroor-Karni S., Thiel S., Jensenius J.C., Gad F., Hamblin M.R., Sastry K.N., Ezekowitz R.A. Mannose-binding lectin-deficient mice are susceptible to infection with Staphylococcus aureus. J. Exp. Med. 2004, 199(10):1379-1390.
98. Simon C., Frances A., Piquette G.N., et al. Embryonic implantation in mice is blocked by interleukin-1 receptor antagonist. Endocrinology 1994, 134:521-528.
99. Simpson E., Chandler P., Pole D. A model of T-cell unresponsiveness using the male-specific antigen, H-Y. Cell Immunol. 1981, 2:251-257.
100. Smith R.N., Powell A.E. The adoptive transfer of pregnancy-induced unresponsiveness to male skin grafts with thymus-dependent cells. J. Exp. Med. 1977, 146:899-904.
101. Stewart C., Kaspar P., Brunet L.J., et al. Blastocyst implantation depends on maternal expression of leukemia inhibitory factor. Nature 1992, 359:76-79.
102. Stilley J.A., Birt J.A., Nagel S.C., et al. Neutralizing TIMP1 restores fecundity in a rat model of endometriosis and treating control rats with TIMP1 causes anomalies in ovarian function and embryo development. Biol. Reprod. 2010, 83(2):185-194.
103. Stilley J.A., Birt J.A., Sharpe-Timms K.L. Cellular and molecular basis for endometriosis-associated infertility. Cell Tissue Res. 2012, 349(3):849-862.
104. Vatin M., Burgio G., Renault G.L., et al. Refined mapping of a quantitative trait locus on chromosome 1 responsible for mouse embryonic death. PLoS ONE 2012, 7(8):e43356.
105. Wegmann T.G. Fetal protection against abortion: is it immuno suppression or immuno stimulation?. Ann. Immunol. (Inst. Pasteur.) 1984, 135D:309-311.
106. Wegmann T.G., Lin H., Guilbert L., Mossman T.H. Bidirectional cytokines interactions in the materno fetal relationship: is successful allopregnancy a Th2 phenomenon?. Immunol. Today 1993, 14(7):353-356.
107. Wen Y., Fang W., Xiang L.X., Pan R.L., Shao J.Z. Identification of Treg-like cells in Tetraodon: insight into the origin of regulatory T subsets during early vertebrate evolution. Cell. Mol. Life Sci. 2011, 68(15):2615-2626.
108. Wible J.R., Rougier G.W., Novacek M.J., Asher R.J. Cretaceous eutherians and Laurasian origin for placental mammals near the K/T boundary. Nature 2007, 447(7147):1003-1006.
109. Wordinger R.J., Jackson F.L., Morrill A. Implantation, deciduoma formation and live births in mast cell-deficient mice (W/Wv). J. Reprod. Fertil. 1986, 77(2):471-476.
110. Zhang Z., Chi H., Niu C., Bøgwald J., Dalmo R.A. Molecular cloning and characterization of Foxp3 in Atlantic salmon (Salmo salar). Fish Shellfish Immunol. 2011, 30(3):902-909.
111. Zhu C., Lee V., Finn A., et al. Origin of immunoglobulin isotype switching. Curr. Biol. 2012, 22(10):872-880.
112. Zourbas S., Dubanchet S., Martal J., Chaouat G. Localization of pro-inflammatory (IL-12, IL-15) and anti-inflammatory (IL-11, IL-13) cytokines at the foetomaternal interface during murine pregnancy. Clin. Exp. Immunol. 2001, 126(3):519-528.