Immunosuppressive macromolecules of endometrial and conceptus origins in livestock species

Journal of Reproductive Immunology

Volumn 48, Issue 1, 2000, Pages 27-46

  Segerson, E C ^a   Beetham, P K ^a  

^a North Carolina AT State Uni6ersity ^*  (United States)

Author keywords

Immune cells; Immunosuppression; Livestock

Indexed keywords

IMMUNOSUPPRESSIVE AGENT;

AGRICULTURE; CELL MEDIATED CYTOTOXICITY; CYTOLYSIS; EFFECTOR CELL; EMBRYO; ENDOMETRIUM; ESTRUS CYCLE; FETUS; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; IMMUNOSURVEILLANCE; MACROMOLECULE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN SECRETION; REPRODUCTION; REVIEW; SPECIES DIFFERENCE; T LYMPHOCYTE SUBPOPULATION; TROPHOBLAST;

ANIMAL; CYTOTOXICITY, IMMUNOLOGIC; ENDOMETRIUM; FEMALE; HUMAN; IMMUNE TOLERANCE; PREGNANCY; TROPHOBLASTS;

EID: 0033830429     PISSN: 01650378     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-0378(00)00059-0     Document Type: Article

References (120)

1. Allen R.L., Murray F.A., Wietsma H.T. Immunosuppression in the mouse by porcine uterine secretory protein. Am. J. Reprod. Immunol. 1:1981;193-198.
2. Arck P.C., Ferrick D.A., Steele-Norwood D., Croitoru K., Clark D.A. Murine T cell determination of pregnancy outcome: I. Effects of strain, alpha beta T cell receptor, gamma delta T cell receptor, and gamma delta T cell subsets. Am. J. Reprod. Immunol. 37:1997;492-502.
3. Arck P.C., Ferrick D.A., Steele-Norwood D., Croitoru K., Clark D.A. Regulation of abortion by gamma delta T cells. Am. J. Reprod. Immunol. 37:1997;87-93.
4. Avril T., Jarousseau A.C., Watier H., Boucraut J., Le Bouteiller P., Bardos P., Thibault G. Trophoblast cell line resistance to NK lysis mainly involves an HLA class I-independent mechanism. J. Immunol. 162:1999;5902-5909.
5. Ayalon N. A review of embryonic mortality in cattle. J. Reprod. Fertil. 54:1978;483-493.
6. Bazer F.W. Establishment of pregnancy in sheep and pigs. Reprod. Fertil. Dev. 1:1989;237-242.
7. Beer A.E., Sio J.O. Placenta as an immunological barrier. Biol. Reprod. 26:1982;15-27.
8. Bischof R.J., Brandon M.R., Lee C.S. Cellular immune responses in the pig uterus during pregnancy. J. Reprod. Immunol. 29:1995;161-178.
9. Bolhuis R.L.H. T-cells responses to cancer. Feldmann M., Lamb J., Owen M.J. T-Cells. Cell Biology: A Series of Monographs. 7:1989;347-364 Wiley, New York.
10. Brinsfield T.H., Hawk H.W., Leffel E.C. Control by ovarian hormones of the inflammatory response in the sheep uterus. J. Reprod. Fertil. 6:1963;79-86.
11. Chao K.H., Yang Y.S., Ho H.N., Chen S.U., Dai H.J., Huang S.C., Gill T.J. Decidual natural killer cytotoxicity decreased in normal pregnancy but not in anembryonic pregnancy and recurrent spontaneous abortion. Am. J. Reprod. Immunol. 34:1995;274-280.
12. Charpigny G., Reinaud P., Huet J.C., Guillomot M., Charlier M., Ernallet J.C., Martal J. High homology between trophoblastic protein (trophoblastin) isolated from ovine embryo and α-interferons. Fed. Eur. Biochem. Soc. 228:1988;12-16.
13. Clark D.A., Slapsys R., Croy B.A., Krcek J., Rossant J. Local active suppression by suppressor cells in the decidua: a review. Am. J. Reprod. Immunol. 5:1984;78-83.
14. Clark D.A., Falbo M., Rowley R.B., Banwatt D., Stedronska-Clark J. Active suppression of host-vs-graft reaction in pregnant mice. IX. Soluble suppressor activity obtained from allopregnant mouse decidua that blocks cytolytic effector response to IL-2 is related to transforming growth factor-β J. Immunol. 141:1988;3833-3840.
15. 2. J. Immunol. 144:1990;3008-3014.
16. 2-like molecules of unusual molecular size released in bioactive form. Biol. Reprod. 52:1995;1380-1388.
17. 2-related immunosuppressive molecules express a bone marrow-derived natural suppressor cell marker and γδT-cell receptor. Biol. Reprod. 56:1997;1351-1360.
18. Cobb S.P., Watson E.D. Immunohistochemical study of immune cells in the bovine endometrium at different stages of the estrous cycle. Res. Vet. Sci. 59:1995;229-237.
19. Croy B.A., Wood W., King G.J. Evaluation of intrauterine immune suppression during pregnancy in a species with epitheliochorial placentation. J. Immunol. 139:1987;1088-1095.
20. Croy B.A., Waterfield A., Wood W., King G.J. Normal murine and porcine embryos recruit NK cells to the uterus. Cell. Immunol. 115:1988;471-480.
21. Daya S., Clark D.A., Devlin C., Jarrell J. Suppressor cells in human decidua. Am. J. Obstet. Gynecol. 151:1985;267-270.
22. Daya S., Clark D.A., Devlin C., Jarrell J. Preliminary characterization of two types of suppressor cells in the human uterus. Fertil. Steril. 44:1985;778-785.
23. Diskin M.G., Sreenan J.M. Fertilization and embryonic mortality rates in beef heifers after artificial insemination. J. Reprod. Fertil. 59:1980;463-468.
24. Drake B.L., Head J.R. Murine trophoblast can be killed by lymphokine-activated killer cells. J. Immunol. 143:1989;9-14.
25. Edey T.N. Embryo mortality. Tomes G.J., et al. Sheep Breeding. 1979;315-325 Butterworths, London.
26. Engelhardt H., King G.J. Uterine natural killer cells in species with epitheliochorial placentation. Nat. Immunol. 15:1996;53-69.
27. Etzel B.J., Murray F.A., Grifo A.P., Kinder J.E. Partial purification of uterine secretory protein capable of suppressing lymphocyte reactivity in vitro. Theriogenology. 10:1978;469-480.
28. Fisher S.J., Gimenez T., Henricks D.M. Immunosuppressive activity associated with early pregnancy in the bovine. Biol. Reprod. 32:1985;894-906.
29. Fox A., Lee C.S., Brandon M.R., Meeusen E.N. Effects of pregnancy on lymphocytes within sheep uterine interplacentomal epithelium. Am. J. Reprod. Immunol. 40:1998;295-302.
30. Gitlin D., Boesman M. Fetus-specific serum proteins in several mammals and their relation to human α-fetoprotein. Comp. Biochem. Physiol. 21:1967;327-336.
31. Godkin J.D., Bazer F.W., Roberts R.M. Ovine trophoblast protein-1, an early secreted blastocyst protein, binds specifically to uterine endometrium and affects protein synthesis. Endocrinology. 114:1984;120-130.
32. Gogolin-Ewens K.J., Lee C.S., Mercer W.R., Brandon M.R. Site-directed differences in the immune response to the fetus. Immunology. 66:1989;312-317.
33. Gottshall S.L., Hansen P.J. Regulation of leucocyte subpopulations in the sheep endometrium by progesterone. Immunology. 76:1992;636-641.
34. Gumperz J.E., Parham P. The enigma of the natural killer cell. Nature. 378:1995;245-248.
35. Gupta A., Bazer F.W., Jaeger L.A. Differential expression of beta transforming growth factors (TGFβ1, TGFβ2, and TGFβ3) and their receptors (type I and type II) in peri-implantation porcine conceptuses. Biol. Reprod. 55:1996;796-802.
36. Gupta A., Dekaney C.M., Bazer F.W., Madrigal M.M., Jaeger L.A. Beta transforming growth factors (TGFβ) at the porcine conceptus-maternal interface. Part II: Uterine TGFβ bioactivity and expression of immunoreactive TGFβs (TGFβ1, TGFβ2, and TGFβ3) and their receptors. Biol. Reprod. 59:1998;911-917.
37. Hanley S. Prenatal mortality in farm animals. J. Reprod. Fertil. 2:1961;182-194.
38. Hansen P.J., Segerson E.C., Bazer F.W. Skin graft survival in the uterine lumen of ewes treated with progesterone. Am. J. Reprod. Immunol. Microbiol. 12:1986;48-54.
39. Hansen P.J., Segerson E.C., Bazer F.W. Characterization of immunosuppressive substances in the basic protein fraction of uterine secretions from pregnant ewes. Biol. Reprod. 36:1987;393-403.
40. 2α content of uterine fluid in pregnant sheep. J. Reprod. Fertil. 48:1976;61-66.
41. Hayakawa S., Shiraishi H., Saitoh S., Satoh K. Decidua as a site of extrathymic V gamma I T-cell differentiation. Am. J. Reprod. Immunol. 35:1996;233-238.
42. Head J.R., Billingham R.E. Mechanisms of non-rejection of the feto-placental allograft. Crighton D.B. Immunological Aspects of Reproduction in Mammals. 1984;133-152 Butterworths, London.
43. Heap R.B., Robinson D.W., Lamming G.E. The relationship between ovarian hormones and uterine infection in the rabbit. A possible mode of action. J. Endocrinol. 23:1986;351-356.
44. Hein W.R., Dudler L. TCR gamma delta+ cells are prominent in normal bovine skin and express a diverse repertoire of antigen receptors. Immunology. 91:1997;58-64.
45. Honda M., Chan C., Shevach E.M. Characterization and partial purification of a specific interleukin-2 inhibitor. J. Immunol. 135:1985;1834-1839.
46. Imakawa K., Anthony R.V., Kazemi M., Maroti K.R., Polites H.G., Roberts R.M. Interferon-like sequence of ovine trophoblast protein secreted by embryonic trophectoderm. Nature. 330:1987;377-379.
47. Imakawa K., Hansen T.R., Malathy P.V., Anthony R.V., Polites H.G., Marotti K.R., Roberts R.M. Molecular cloning and characterization of cDNA corresponding to bovine trophoblast protein-1. A comparison with ovine trophoblast protein-1 and bovine interferon-αII. Mol. Cell. Endocrinol. 3:1989;127-129.
48. Ireland A.C., Segerson E.C. Ovine endometrial cells fail to lyse K-562 target cells: a preliminary investigation. Theriogenology. 51:1999;1431-1440.
49. Kazemi M., Malathy P.V., Keisler D.H., Roberts R.M. Ovine trophoblast protein-1 and bovine trophoblast protein-1 are present as specific components of uterine flushings of pregnant ewes and cows. Biol. Reprod. 39:1988;457-463.
50. Kimura M., Hanawa H., Watanabe H., Ogawa M., Abo T. Synchronous expansion of intermediate TCR cells in the liver and uterus during pregnancy. Cell. Immunol. 162:1995;15-25.
51. Kimura M., Goff J.P., Kehrli M.E. Jr, Harp J.A. Phenotype analysis of peripheral blood mononuclear cells in periparturient dairy cows. J. Dairy Sci. 82:1999;315-319.
52. King A., Loke Y.W. Human trophoblast and JEG choriocarcinoma cells are sensitive to lysis by IL-2-stimulated decidual NK cells. Cell. Immunol. 127:1990;230-237.
53. King A., Birby A., Loke Y.W. Early human decidual cells exhibit NK activity against the K562 cell line but not first trimester trophoblast. Cell. Immunol. 118:1989;337-344.
54. King A., Hiby S.E., Verma S., Burrows T., Gardner L., Loke Y.W. Uterine NK cells and trophoblast HLA class I molecules. Am. J. Reprod. Immunol. 37:1997;459-462.
55. Knickerbocker J.J., Niswender G.D. Characterization of endometrial receptors for ovine trophoblast protein-1 during the estrous cycle and early pregnancy in sheep. Biol. Reprod. 40:1989;361-369.
56. Knight J.W., Bazer F.W., Wallace H.D. Hormonal regulation of porcine uterine protein secretions. J. Anim. Sci. 36:1973;546-553.
57. Krcek J., Clark D.A. Selective localization of a bone marrow cell subpopulation at the implantation site in murine decidua. Am. J. Reprod. Immunol. 7:1985;95-98.
58. Kydd J.H., Butcher G.W., Antczak D.F., Allen W.R. Expression of major histocompatibility complex (MHC) class 1 molecules on early trophoblast. J. Reprod. Fertil. 44:((Suppl.)):1991;463-477.
59. Lambert E., Williams D.H., Lynch P.B., Hanrahan T.J., McGeady T.A., Austin F.H., Boland M.P., Roche J.F. The extent and timing of prenatal loss in gilts. Theriogenology. 36:1991;655-665.
60. Lanier L.L. Unusual lymphocytes-γδ T cells and NK cells. Janeway C.A. Jr, Marrak P., Jacintia N., Natvig J.B. The Immunologist. Proceedings Reports from the IXth International Congress of Immunology, July 23-29, San Francisco. 1995;182-184 Hogrefe Huber Publishers, Germany.
61. Lee C.S., Gogolin-Ewens K., Brandon M.R. Identification of a unique lymphocyte subpopulation in the sheep uterus. Immunology. 63:1988;157-164.
62. Lee C.S., Meeusen E., Gogolin-Ewens K., Brandon M.R. Quantitative and qualitative changes in the intraepithelial lymphocyte population in the uterus of non-pregnant and pregnant sheep. Am. J. Reprod. Immunol. 28:1992;90-96.
63. LeFevre F., Martinat-Botte F., Guillomot M., Zouari K., Charley B., LaBonnardiere C. Interferon-gamma gene and protein are spontaneously expressed by the porcine trophectoderm early in gestation. Eur. J. Immunol. 20:1990;2485-2490.
64. Liu W.J., Gottshall S.L., Hansen P.J. Increased expression of cell surface markers on endometrial gamma delta T-cell receptor+ intraepithelial lymphocytes induced by the local presence of the sheep conceptus. Am. J. Reprod. Immunol. 37:1997;199-205.
65. Low B.G., Hansen P.J., Drost M., Gogolin-Ewens K.J. Expression of major histocompatibility complex antigens on the bovine placenta. J. Reprod. Fertil. 90:1990;235-243.
66. Maddox J.F., Mackay C.R., Brandon M.R. The sheep analogue of leucocyte common antigen (LCA). Immunology. 55:1985;347-353.
67. Male D., Lelchuk R., Curry S., Pryce G., Playfair J.H.L. Serum IL-2 inhibitor in mice. II. Molecular characteristics. Immunology. 56:1985;119-125.
68. Martal J., Chene N., Camous S., Huynh L., Lantier F., Hermier P., L'Haridon R., Charpigny G., Charlier M., Chaouat G. Recent developments and potentialities for reducing embryo mortality in ruminants: the role of IFN-τ and other cytokines in early pregnancy. Reprod. Fertil. Dev. 9:1997;355-380.
69. Martal J.L., Chene N.M., Huynh L.P., L'Haridon R.M.L., Reinaud P.B., Guillomot M.W., Charlier M.A., Charpigny S.Y. IFN-tau: a novel subtype I IFN. 1. Structural characteristics, non-ubiquitous expression, structure-function relationships, a pregnancy hormonal embryonic signal and cross-species therapeutic potentialities. Biochimie. 80:1998;755-777.
70. Maurer R.R., Chenault J.R. Fertilization failure and embryonic mortality in parous and non-parous beef cattle. J. Anim. Sci. 56:1983;1186-1189.
71. Meeusen E., Fox A., Brandon M., Lee C.S. Activation of uterine intraepithelial γδ T cell receptor-positive lymphocytes during pregnancy. Eur. J. Immunol. 23:1993;1112-1117.
72. Murgita R.A., Tomasi T.B. Suppression of the immune response by α-fetoprotein. II. The effect of mouse α-fetoprotein on mixed lymphocyte reactivity and mitogen-induced lymphocyte transformation. J. Exp. Med. 141:1975;440-451.
73. Murray F.A., Segerson E.C., Brown F.T. Suppression of lymphocytes in vitro by porcine uterine secretory protein. Biol. Reprod. 19:1978;15-25.
74. Murray M.K., Segerson E.C., Hansen P.J., Bazer F.W., Roberts R.M. Suppression of lymphocyte activation by a high-molecular-weight glycoprotein released from preimplantation ovine and porcine conceptuses. Am. J. Reprod. Immunol. Microbiol. 14:1987;38-44.
75. Newton G.R., Vallet J.L., Hansen P.J., Bazer F.W. Inhibition of lymphocyte proliferation by ovine trophoblast protein-1 and a high molecular weight glycoprotein produced by the peri-implantation sheep conceptus. Am. J. Reprod. Immunol. 19:1989;99-107.
76. Niwano Y., Hansen T.R., Kazemi M., Malathy P.-V., Johnson H.D., Roberts R.M., Imakawa K. Suppression of T-lymphocyte blastogenesis by ovine trophoblast protein-1 and human interferon-α may be independent of interleukin-2 production. Am. J. Reprod. Immunol. 20:1989;21-26.
77. Pope W.F. Uterine asynchrony: a cause of embryonic loss. Biol. Reprod. 39:1988;999-1003.
78. Pope W.F., First N.L. Factors affecting the survival of pig embryos. Theriogenology. 23:1985;91-105.
79. Ramsoondar J.J., Christopherson R.J., Guilbert L.J., Dixon W.T., Ghahary A., Ellis S., Wegmann T.G., Piedrahita J.A. Lack of class I major histocompatibility antigens of trophoblast of periimplantation blastocysts and term placenta in the pig. Biol. Reprod. 60:1999;387-397.
80. Reimers T.J., Dziuk P.J. The survival of intrauterine skin autografts and allografts in sheep. J. Reprod. Fertil. 38:1974;465-467.
81. Roberts G.P. Inhibition of lymphocyte stimulation by bovine uterine proteins. J. Reprod. Fertil. 50:1977;337-339.
82. Roberts G.P., Parker J.M. Macromolecular components of the luminal fluid from the bovine uterus. J. Reprod. Fertil. 40:1974;291-303.
83. Roberts A.B., Anzano M.A., Wakefield L.M., Roche N.S., Stern D.F., Sporn M.B. Type beta transforming growth factor, a bifunctional regulator of cellular growth. Proc. Natl. Acad. Sci. USA. 82:1985;119-123.
84. Roberts R.M., Imakawa K., Niwano Y., Kazemi M., Malathy P.V., Hansen T.R., Glass A.A., Kronenberg L.H. Interferon production by the preimplantation sheep embryo. J. Interferon Res. 9:1989;175-187.
85. Roth T.L., White K.L., Thompson D.L. Jr, Barry B.E., Capehart J.S., Colborn D.R., Rabb M.H. Suppression of lymphocyte proliferation by a >30 000 molecular weight factor in horse conceptus-conditioned medium. Biol. Reprod. 43:1990;298-304.
86. Roth T.L., White K.L., Thompson D.L. Jr, Rahmanian S., Horohov D.W. Involvement of interleukin 2 receptors in conceptus-derived suppression of T and B cell proliferation in horses. J. Reprod. Fertil. 96:1992;309-322.
87. Segerson E.C. Immunosuppressive effect of ovine uterine secretory protein upon lymphocytes in vitro. Biol. Reprod. 25:1981;77-84.
88. Segerson E.C. Suppression of interleukin-2 mediated T-lymphocyte blastogenesis by ovine uterine luminal protein. Biol. Reprod. 38:1988;256-263.
89. Segerson E.C. Immunosuppressive activity of a porcine high molecular weight uterine macromolecule is associated with transforming growth factor-β J. Reprod. Immunol. 29:1995;47-60.
90. Segerson E.C., Bazer F.W. High molecular weight basic and acidic immunosuppressive protein components in uterine secretion of pregnant cows. Biol. Reprod. 41:1989;1014-1023.
91. 2 activity suppresses natural killer cell responses. J. Anim. Sci. 78, 1697-2020.
92. Segerson, E.C., Beetham, P.K., 2000b. Suppressor activity of bone marrow cells and localization of fluorescent-labeled bone marrow cells within ovine endometrial tissue. J. Anim. Sci. 78, 709-717.
93. Segerson E.C., Gunsett F.C. Suppression of interleukin-2 mediated T-lymphocyte blastogenesis by bovine uterine secretions. Am. J. Reprod. Immunol. 22:1990;117-123.
94. Segerson E.C., Gunsett F.C. Secretion of ovine lymphocyte suppressor factor from curetted uterine luminal cells. J. Anim. Sci. 70:1992;1895-1903.
95. Segerson E.C., Gunsett F.C. Temporal patterns of secretion of porcine uterine suppressor and stimulatory macromolecules. Theriogenology. 40:1993;669-678.
96. Segerson E.C., Gunsett F.C. In vitro and in vivo effects of lymphokine-activated killer cells upon preattachment ovine conceptuses. J. Immunol. 152:1994;2938-2951.
97. Segerson E.C., Libby D.W. Interaction of bovine uterine luminal protein with interleukin-2 and the interleukin-2 receptor of T lymphocytes. Biol. Reprod. 43:1990;619-628.
98. 2 activity is temporally associated with a porcine high-molecular-weight uterine component recovered during early pregnancy. J. Anim. Sci. 75:1997;462-468.
99. Segerson E.C., Libby D.W., Getz W.R., Randel R.D. Immunosuppressive effect of uterine secretory protein from Angus and Brahman cows upon lymphocytes in vitro. J. Anim. Sci. 59:1984;1047-1059.
100. Segerson E.C., Hansen T.R., Libby D.W., Randel R.D., Getz W.R. Ovarian and uterine morphology and function in Angus and Brahman cows. J. Anim. Sci. 59:1984;1026-1046.
101. Segerson E.C., Moffatt R.J., Bazer F.W., Roberts R.M. Suppression of phytohemagglutinin-stimulated lymphocyte blastogenesis by ovine uterine milk protein. Biol. Reprod. 30:1984;1175-1186.
102. Segerson E.C., Williams T.D., Gunsett F.C. Lymphocyte suppressor and stimulatory factors within uterine luminal protein secretions of pregnant gilts. Theriogenology. 35:1991;1095-1110.
103. Segerson E.C., Matterson P.M., Gunsett F.C. Endometrial T-lymphocyte subset infiltration during the ovine estrous cycle and early pregnancy. J. Reprod. Immunol. 20:1991;221-236.
104. Segerson E.C., Li H., Talbott C.W. Estradiol-17β and progesterone increase ovine uterine suppressor cell activity. J. Anim. Sci. 75:1997;2778-2787.
105. Segerson E.C., Li H., Talbott C.W., Allen J.W., Gunsett F.C. Partial characterization of ovine intrauterine suppressor cells. Biol. Reprod. 58:1998;397-406.
106. Shipp S.A., Segerson E.C. Endometrial suppressor cells in beef cattle. Theriogenology. 50:1998;779-791.
107. Slapsys R.M., Clark D.A. Active suppression of host-vs-graft reaction in pregnant mice. IV. Local suppressor cells in decidua and uterine blood. J. Reprod. Immunol. 4:1982;355-364.
108. Squire G.D., Bazer F.W., Murray F.A. Electrophoretic patterns of porcine uterine protein secretions during the estrous cycle. Biol. Reprod. 7:1972;321-325.
109. Stephenson D.C., Hansen P.J., Newton G.R., Bazer F.W., Low B.G. Inhibition of lymphocyte proliferation by uterine fluid from the pregnant ewe. Biol. Reprod. 41:1989;1063-1075.
110. Stewart H.J., McCann S.H.E., Berker P.J., Lee K.E., Lamming G.E., Flint A.P.F. Interferon sequence homology and receptor binding activity of ovine trophoblast antiluteolytic protein. J. Endocrinol. 115:1987;R13-R15.
111. Suzuki T., Hiromatsu K., Ando Y., Okamoto T., Tomoda Y., Yoshikai Y. Regulatory role of gamma delta T cells in uterine intraepithelial lymphocytes in maternal antifetal immune response. J. Immunol. 154:1995;4476-4484.
112. Szekeres-Bartho J., Barakonyi A., Polgar B., Par G., Faust Z., Palkovics T., Szereday L. The role of gamma/delta T cells in progesterone-mediated immunomodulation during pregnancy: a review. Am. J. Reprod. Immunol. 42:1999;44-48.
113. Templeton J.W., Tipton R.C., Garber T., Bondioli K., Kraemer D.C. Expression and genetic segregation of parental BoLA serotypes in bovine embryos. Anim. Genet. 18:1987;317-322.
114. Trebichavsky I., Sinkora J., Rehakova Z., Splichal I., Whyte A., Binns R., Pospisil R., Tuckova L. Distribution of gamma delta T cells in the pig foetus. Folia Biol. (Czech Republic). 41:1995;227-237.
115. Watson E.D. Suppression of lymphocyte reactivity by culture supernatant from horse embryos and endometrium. Biol. Reprod. 42:1990;294-300.
116. Wilmut I., Sales D.I., Ashworth C.J. Maternal and embryonic factors associated with prenatal loss in mammals. J. Reprod. Fertil. 76:1986;851-864.
117. Yachnin S. Fetuin, an inhibitor of lymphocyte transformation. J. Exp. Med. 141:1975;242-256.
118. Yu Z., Croy B.A., Chapeaus C., King G.J. Elevated endometrial natural killer cell activity during early porcine pregnancy is conceptus-mediated. J. Reprod. Immunol. 24:1993;153-165.
119. Yu Z., Croy B.A., King G.J. Lysis of porcine trophoblast cells by endometrial NK-like effector cells in vitro does not require IL-2. Biol. Reprod. 51:1994;1279-1284.
120. Zuckerman F.A., Head J.R. Murine trophoblast resists cell-mediated lysis. II. Resistance to natural cell-mediated cytotoxicity. Cell. Immunol. 116:1988;274-286.